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Emotional state affects gait initiation in individuals with Parkinson disease

Permanent Link: http://ufdc.ufl.edu/UFE0042013/00001

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Title: Emotional state affects gait initiation in individuals with Parkinson disease
Physical Description: 1 online resource (223 p.)
Language: english
Creator: Gamble, Kelly
Publisher: University of Florida
Place of Publication: Gainesville, Fla.
Publication Date: 2010

Subjects

Subjects / Keywords: emotion, gait, parkinson
Applied Physiology and Kinesiology -- Dissertations, Academic -- UF
Genre: Health and Human Performance thesis, Ph.D.
bibliography   ( marcgt )
theses   ( marcgt )
government publication (state, provincial, terriorial, dependent)   ( marcgt )
born-digital   ( sobekcm )
Electronic Thesis or Dissertation

Notes

Abstract: Individuals with Parkinson disease (PD) experience postural instability and difficulty initiating gait, which are often highly disabling and not effectively treated by current pharmacological or surgical options. A pressing need exists to develop novel complimentary therapeutic strategies to treat these disabling gait disturbances. The purpose of the present study was to determine the impact of emotional state on gait initiation in persons with PD and healthy older adults. Following the presentation of pictures that are known to elicit specific emotional responses, participants initiated gait and continued to walk for several steps at their normal pace. Reaction time, the displacement and velocity of the COP trajectory during the preparatory postural adjustments, and length and velocity of the first two steps were measured. Analysis of the gait initiation measures revealed that exposure to (1) threatening pictures speeded the initiation of gait for PD patients and healthy older adults, (2) pleasant emotional pictures (erotic and happy people) facilitated the anticipatory postural adjustments of gait initiation for PD patients and healthy older adults as evidenced by greater displacement and velocity of the COP movement, and (3) emotional pictures modulated gait initiation parameters in PD patients to the same degree as healthy older adults. Collectively, these findings hold significant implications for the development of emotion-based interventions designed to maximize improvements in gait initiation for individuals with PD.
General Note: In the series University of Florida Digital Collections.
General Note: Includes vita.
Bibliography: Includes bibliographical references.
Source of Description: Description based on online resource; title from PDF title page.
Source of Description: This bibliographic record is available under the Creative Commons CC0 public domain dedication. The University of Florida Libraries, as creator of this bibliographic record, has waived all rights to it worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law.
Statement of Responsibility: by Kelly Gamble.
Thesis: Thesis (Ph.D.)--University of Florida, 2010.
Local: Adviser: Janelle, Christophe M.

Record Information

Source Institution: UFRGP
Rights Management: Applicable rights reserved.
Classification: lcc - LD1780 2010
System ID: UFE0042013:00001

Permanent Link: http://ufdc.ufl.edu/UFE0042013/00001

Material Information

Title: Emotional state affects gait initiation in individuals with Parkinson disease
Physical Description: 1 online resource (223 p.)
Language: english
Creator: Gamble, Kelly
Publisher: University of Florida
Place of Publication: Gainesville, Fla.
Publication Date: 2010

Subjects

Subjects / Keywords: emotion, gait, parkinson
Applied Physiology and Kinesiology -- Dissertations, Academic -- UF
Genre: Health and Human Performance thesis, Ph.D.
bibliography   ( marcgt )
theses   ( marcgt )
government publication (state, provincial, terriorial, dependent)   ( marcgt )
born-digital   ( sobekcm )
Electronic Thesis or Dissertation

Notes

Abstract: Individuals with Parkinson disease (PD) experience postural instability and difficulty initiating gait, which are often highly disabling and not effectively treated by current pharmacological or surgical options. A pressing need exists to develop novel complimentary therapeutic strategies to treat these disabling gait disturbances. The purpose of the present study was to determine the impact of emotional state on gait initiation in persons with PD and healthy older adults. Following the presentation of pictures that are known to elicit specific emotional responses, participants initiated gait and continued to walk for several steps at their normal pace. Reaction time, the displacement and velocity of the COP trajectory during the preparatory postural adjustments, and length and velocity of the first two steps were measured. Analysis of the gait initiation measures revealed that exposure to (1) threatening pictures speeded the initiation of gait for PD patients and healthy older adults, (2) pleasant emotional pictures (erotic and happy people) facilitated the anticipatory postural adjustments of gait initiation for PD patients and healthy older adults as evidenced by greater displacement and velocity of the COP movement, and (3) emotional pictures modulated gait initiation parameters in PD patients to the same degree as healthy older adults. Collectively, these findings hold significant implications for the development of emotion-based interventions designed to maximize improvements in gait initiation for individuals with PD.
General Note: In the series University of Florida Digital Collections.
General Note: Includes vita.
Bibliography: Includes bibliographical references.
Source of Description: Description based on online resource; title from PDF title page.
Source of Description: This bibliographic record is available under the Creative Commons CC0 public domain dedication. The University of Florida Libraries, as creator of this bibliographic record, has waived all rights to it worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law.
Statement of Responsibility: by Kelly Gamble.
Thesis: Thesis (Ph.D.)--University of Florida, 2010.
Local: Adviser: Janelle, Christophe M.

Record Information

Source Institution: UFRGP
Rights Management: Applicable rights reserved.
Classification: lcc - LD1780 2010
System ID: UFE0042013:00001


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1 EMOTIONAL STATE AFFECTS GAIT INITIATION IN INDIVIDUALS WITH PARKINSON DISEASE By KELLY MARIE GAMBLE A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2010

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2 2010 Kelly Gamble

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3 To my family, for all their prayers and support

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4 ACKNOWLEDGMENTS I would first like to thank God for the abilities that I have been granted and for the p eople he has placed in my life which has helped me to complete this journey. I would like to thank my mom and dad for their continued support and unconditional love throughout my life, their belief in me has enabled me to be the person I am today. My siste r and brother, Lori and Brian, for their friendship and love, and my grandma, Marcella for her constant support and faith in me. I would like to thank my mentor, Dr. Christopher Janelle for his continual confidence in me, as well as his wisdom and willingn ess to guide me not only through this dissertation process, but also in my academic and professional development. I would like to acknowledge the committee for their hard work and assistance in the development and completion of this project. I would lik e to thank Dr. Chris Hass for his excellent guidance and support in my doctoral career and this project. I thank Dr. James Cauraugh for his continued guidance, insight, and support in helping me to create this project I thank Dr. Dawn Bowers for her hel ping me fine tune this topic and for her consistently positive attitude in this journey. I would like to thank Steve Coombes for all of his help and guidance, especially in the early stages of doctoral years. I would like to acknowledge Jessica Joyner, Ad am Field, Candice Langdon, and Anastasia Jdanova for helping run subjects through the experiment and for the abundant amount of time spent processing data. Finally, I would like to thank my new husband, Keith Naugle. You bring a smile to my face every day Thank you for your patience, understanding, and love throughout my doctoral career. You are a wonderful reminder of what life is all about!

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5 TABLE OF CONTENTS page ACKNOWLEDGMENTS ................................ ................................ ................................ .. 4 LIST OF TABLES ................................ ................................ ................................ ............ 8 LIST OF FIGURES ................................ ................................ ................................ .......... 9 ABSTRACT ................................ ................................ ................................ ................... 12 CHAPTER 1 I NTRODUCTION ................................ ................................ ................................ .... 14 Posture and Gait Performance in PD ................................ ................................ ...... 15 Emotion Deficits in PD ................................ ................................ ............................ 17 Emotion and Motor Function: An Integrated Approach ................................ ........... 19 Emotion Modulated Movement ................................ ................................ ......... 20 The I ntegration of Emotion and Motor Processes ................................ ............ 21 Hypotheses ................................ ................................ ................................ ............. 24 Reaction Time: ................................ ................................ ................................ 24 COP Trajectory and Step Execution Measures: ................................ ............... 24 2 REVIEW OF LITERATURE ................................ ................................ .................... 27 Introduction ................................ ................................ ................................ ............. 27 Parkinson Disease ................................ ................................ ................................ .. 28 Pathophysiology of Parkinson Disease ................................ ............................ 28 Treatment for PD ................................ ................................ .............................. 30 Pharmacological treatments ................................ ................................ ....... 31 Surgical treatments deep brain stimulation ................................ .............. 32 Physical therapy ................................ ................................ ......................... 34 Overview of Movement ................................ ................................ ........................... 35 Theories of Motor Control ................................ ................................ ................. 36 Cognitive theories of movement control and coordination ......................... 36 Ecological theories of movement control and coordination ........................ 44 Summary ................................ ................................ ................................ .... 49 Gait Initiation ................................ ................................ ................................ .... 51 The neural control of gait initiation and execution ................................ ...... 53 Gait initiation deficits in Parkinson disease ................................ ................ 58 Summary ................................ ................................ ................................ .... 61 Overview of Emotion ................................ ................................ ............................... 62 Theories of Emotion ................................ ................................ ......................... 62 Behavioral theories of emotion ................................ ................................ ... 62 Cognitive theories of emot ion ................................ ................................ ..... 63 Biological theories of emotion ................................ ................................ .... 66

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6 Integrative theories of emotion ................................ ................................ ... 66 Circuitry of Emotion ................................ ................................ .......................... 69 Neuroscientific models of emotion ................................ ............................. 70 The role of specific brain regions for emotional operat ions ........................ 74 Limbic circuits involving the basal ganglia ................................ ................. 79 Emotion deficits in Parkinson disease ................................ ........................ 81 Summary ................................ ................................ ................................ .......... 85 Emotion and Movement ................................ ................................ .......................... 86 Emotion Modulated Movement Approach and Avoidance Movements .......... 87 Emotion Modulated Movement Nondirection Specific Movements ................ 99 The Integration of Emotion and Motor Processes ................................ .......... 103 The thalamo cortico thalamic pathway ................................ .................... 103 The striato nigro striatal (SNS) pathway ................................ .................. 105 Emotion, Movement, and PD ................................ ................................ ................ 109 Future Research ................................ ................................ ................................ ... 110 3 M ETHODS ................................ ................................ ................................ ............ 129 Participants ................................ ................................ ................................ ........... 129 Inclusion/Exclusion Criteria for Parkinson Group. ................................ .......... 129 Exclusion Criteria for All Participants ................................ .............................. 130 Instrumentation ................................ ................................ ................................ ..... 131 Emotion Manipulation ................................ ................................ ..................... 131 Task ................................ ................................ ................................ ............... 132 Procedure ................................ ................................ ................................ ............. 133 Data Reduction ................................ ................................ ................................ ..... 134 Statistical Analyses ................................ ................................ ............................... 137 Primary Statistical Analyses ................................ ................................ ........... 137 Secondary Statistical Analyses ................................ ................................ ...... 139 4 RESULTS ................................ ................................ ................................ ............. 142 Participants ................................ ................................ ................................ ........... 142 Primary Statistical Results ................................ ................................ .................... 143 Reaction Time ................................ ................................ ................................ 143 S1 Region of the COP Trace ................................ ................................ .......... 144 S2 Region of the COP Trace ................................ ................................ .......... 147 S3 Region of the COP Trace ................................ ................................ .......... 148 Average Step Length and Step Velocity of the 1 st and 2 nd Steps ................... 149 Instantaneous Velocity of t he 1 st and 2 nd Steps ................................ .............. 150 SAM Ratings ................................ ................................ ................................ .. 151 Secondary Statistical Results ................................ ................................ ............... 152 Reaction Time ................................ ................................ ................................ 152 S1 Region of the COP Trace ................................ ................................ .......... 152 S2 Region of the COP Trace ................................ ................................ .......... 153 S3 Region of the COP Trace ................................ ................................ .......... 154 Average Step Length and Step Velocity of the 1 st and 2 nd Steps ................... 154

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7 5 D ISCUSSION ................................ ................................ ................................ ....... 164 Reaction Time ................................ ................................ ................................ ....... 165 Preparatory Postural Adjustments ................................ ................................ ........ 167 Step Execution ................................ ................................ ................................ ...... 173 Summary ................................ ................................ ................................ .............. 175 Limitations ................................ ................................ ................................ ............. 176 Practical Im plications and Future Directions ................................ ......................... 179 Conclusion ................................ ................................ ................................ ............ 183 APPENDIX: P ERMISSION TO USE FIGURES ................................ .......................... 184 LIST OF REFERENCES ................................ ................................ ............................. 192 BIOGRAPHICAL SKETCH ................................ ................................ .......................... 223

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8 LIST OF TABLES Table page 4 1 Demographic, affective, and clinical characteristics of sample ........................ 143

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9 LIST OF FIGURES Figure page 2 1 A schematic diagram illus trating the changes occurring in the basal ganglia circuitry in Parkinson disease ................................ ................................ ........... 113 2 2 The response chaining hypothesis ................................ ................................ ... 114 2 3 Planning of human action production. ................................ .............................. 114 2 4 The control of human action production. ................................ .......................... 115 2 5 teracting constraints ................................ ....... 115 2 6 Overhead view of the COP trajectory during forward GI when stepping with the right foot ................................ ................................ ................................ ...... 116 2 7 Th e volitional and automatic control of locomotor movements ......................... 116 2 8 Basal Ganglia thalamocortical control of gait ................................ ................. 117 2 9 Basal Ganglia Brain stem control of gait ................................ ....................... 118 2 10 COP displacements in the anterior/ posterior and medial/ lateral directions du ring forward gait initiation ................................ ................................ .............. 118 2 11 Hypothetical model for the control of gait by the basal ganglia ......................... 119 2 12 Schematic illustration of the embodiment of emotion ................................ ....... 120 2 13 A schematic illustration of the defensive cascade model for the electrodermal, startle, and cardiac response systems ................................ ...... 120 2 14 Inputs and outputs to amy gdala nuclei ................................ ............................. 121 2 15 Basal ganglia thalamocortical limbic circuit. ................................ ..................... 121 2 16 New organization of limbic circuit ................................ ................................ ..... 122 2 17 Summary of thalamic terminal or ganization in cortical layers ........................... 123 2 18 Proposed schema of information flow between thalamic relay nuclei and frontal cortical areas ................................ ................................ ......................... 124 2 19 Diagram of the 3 SNS components for each striatal region illustrating an overlapping system in the midbrain ................................ ................................ .. 125

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10 2 20 Diagram of the organization of SNS projections ................................ ............... 126 2 21 A schematic diagram illustrating the integration of limbic information into the basal ganglia systems regulat ing locomotion in healthy individuals and potentially PD patients while on stand ard antiparkinsonian medication ............ 127 2 22 A schematic diagram illustrating 1) the changes associated with PD in t he basal ganglia circuitry regulating locomotion and 2) the reduced integration of limbic input into mot or basal ganglia circuits in PD ................................ .......... 128 3 1 Overhead view of the path of the COP during for ward GI when stepping with the right foot ................................ ................................ ................................ ...... 135 4 1 Mean reaction time (Figure 4 1a) and mean percent change scores for reaction time (Figure 4 1b) across category conditions for the PD and Cont rol groups. ................................ ................................ ................................ ............. 156 4 2 COP movement in the S1 region across category conditions for the PD and Control groups for the mean displacement in the posterior direction (Figure 4 2a), mean velocity in the posterior direction (Figure 4 2b), mean displacement in the lateral direction (Figure 4 2c), and mean velocity in the lateral direction (Figure 4 2d) ................................ ................................ ............ 157 4 3 COP movement percent change sc ores in the S1 region across category conditions for the PD and Control groups for the mean percent change displacement in the posterior direction (Figure 4 3a), mean percent change velocity in the posterior direction (Figure 4 3b), mean percent change dis placement in the lateral direction (Figure 4 3c), and mean percent change velocity in the lateral direction (Figure 4 3d) ................................ ..................... 158 4 4 COP movement in the S2 region across category conditions for t he PD and Control groups for the mean displacement in the posterior direction (Figure 4 4a), mean velocity in the posterior direction (Figure 4 4b), mean displacement in the medial (Figure 4 4c), and mean velocity in the medial direction (Figure 4 4d) ................................ ................................ ...................... 159 4 5 COP movement percent change scores in the S2 region across category conditions for the PD and Control groups for the mean percent change displacement in the posterior direction (Figure 4 5 a), mean percent change velocity in the posterior direction (Figure 4 5b), mean percent change displacement in the medial direction (Figure 4 5c), and mean percent change velocity in the medial direction (Figure 4 5d) ................................ .................... 160 4 6 Mean length of step 1 (Figure 4 6a), mean velocity of step 1 (Figure 4 b), mean stride length (Figure 4 6c), mean length of step 2 (Figure 4 6d) and mean velocity of step 2 (Figure 4 6e) across category conditions for the PD and Control groups ................................ ................................ ........................... 161

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11 4 7 Mean percent change scores across category conditions for the PD and Control groups for length of step 1 (Figure 4 7a), velocity of step 1 (Figure 4 7b), length o f step 2 (Figure 4 7c), and velocity of step 2 (Figure 4 7d) ........... 162 4 8 Mean SAM valence ratings (Figure 4 8a) and arousal ratings (Figure 4 8b) across category conditions for the PD and Control groups. The higher a pleasant or arousing, respectively. ................................ ................................ ... 163

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12 Abstract of Dissertation Presented to the Graduate School of t he University of Florida in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy EMOTIONAL STATE AFFECTS GAIT INITIATION IN INDIVIDUALS WITH PARKINSON DISEASE By Kelly Marie Gamble August, 2010 Chair: Christoph er Janelle Major: Health and Human Performance Individuals with Parkinson disease (PD) experience postural instability and difficulty initiating gait, which are often highly disabling and not effectively treated by current pharma cological or surgical opti ons. A pressing need exists to develop novel complimentary therapeutic strategies to treat thes e disabling gait disturbances. The purpose of the present study was to determine the impact of emotional state on gait initiation in persons wit h PD and healthy older adults. Following the presentation of pictures that are known to elicit specific emotional responses participants initiated gait and continued to walk for sever al steps at their normal pace. Reaction time, the displacement and velocity of the COP tr ajectory during the preparatory postural adjustments, and length and velocity of the first two steps were measured. Analysis of the gait initiation measures revealed that exposure to (1) threatening pictures speeded the initiation of gait for PD patients a nd healthy older adults, (2) pleasant emotional pictures (erotic and happy people) facilitated the anticipatory postural adjustments of gait initiation for PD patients and healthy older adults as evidenced by greater displacement and velocity of the COP mo vement, and (3) emotional pictures modulated gait initiation parameters in PD patients to the same d egree as healthy older adults.

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13 Collectively, these findings hold significant implications for the development of emotion based interventions designed to max imize improvements in gait initiation for individuals with PD.

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14 CHAPTER 1 INTRODUCTION Parkinson disease (PD) is a progressive neurodegenerative disease of the basal ganglia characterized by debilitating motor sympt oms and emotional dysfunction. PD is the affects approximately 1.5 million individuals in the U.S. with 70,000 new cases diagnosed each year (Orr, Rowe, & Hallida y, 2002; Hampton, JAMA, 2005). The cardinal motor symptoms of PD include bradykinesia, tremor, rigidity, postural instability and gait dysfuncti on. Most motor symptoms of PD are driven by nigrostriatal dopamine depletion which causes a cascade of alterations in all components of the basal ganglia functional ci rcu itry (Pahwa & Lyons, 2007). Suffers of PD incur additional countless and measureless costs in terms of functional impairments that permeate and interfere with virtually every facet of daily living. Despite their benefits, current pharmacological and surg ical therapies for patients with PD are limited in their ability to adequately treat postural instability and gait difficulties (Sethi, 2008; Rodriguez Oroz, Obeso, Lang, Houeto Po llack, Rehcrona, et al., 2005). Furthermore, gait problems are arguably one of the largest unmet needs in the symptomatic treatment of PD (Pahwa & Lyons, 2007). The high and rising prevalence of PD coupled with the lack of adequate treatment for gait deficits in PD, necessitate the development of novel and cost effective intervent i ons for locomotor dysfunction. Given that recent evidence has demonstrated that pleasant emotional states facilitate the initiation of gait in healthy individuals (Gamble, Joyner, Coombes, Hass, & Janelle, in review), manipulating emotional state may be a n efficacious strategy to enhance gait initiation parameters in persons with PD. Thus, the primary goal of this

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15 project was to delineate whether and how emotional manipulations would alter gait initiation in persons with PD. Posture and Gait Performance in PD Gait initiation, the phase between motionless standing and rhythmic walking, requires effective balance control as one moves from stable balance to continuously unstable gait (Halliday, G ai, Blessing, & Geffen, 1990). Prior to the initiation of the ste pping movement, anticipatory postural adjustments (APAs) decouple the center of mass (COM) and the net center of pressure (COP). These postural adjustments include a series of muscle activations and changes in ground reaction forces that move the net cente r of pressure backward and laterally over the swing limb to move the net COM forward over the stance limb ( APA phase ) (Crenna, Frigo, Giovannini, & Piccolo, 1990; Massion, 1992). This backward shift produces the forward momentum needed to initiate gait. Th e lateral shift of the COP towards the swing limb propels the COM toward the stance limb producing the stance side momentum needed to initiate gait (Polcyn, Lipsit z, Kerrigan, & Collins, 1998). A subsequent and quick medial (from swing limb to stance limb ) shift of the COP continues to accelerate the COM forward and away from the stance limb ( weight shift phase ) allowing the swing limb to be unloaded before stepping (Jian, Einter, Ishac, & Gilchrist, 1993). Finally, the COP moves anteriorly until toe off o f the initial stance limb ( locomotor phase ). Execution of the first step begins when weight has been transferred to the stance limb (Crenna et al., 1990). The initiation of gait is regulated in parallel by two circuits involving the basal ganglia: 1) bas al ganglia thalamocortical loop, and 2) bas al ganglia brainstem system. The basal ganglia thalamocortical loop controls the initiation of gait via GABAergic basal ganglia output to the motor cortices through the thalamus. Basal

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16 ganglia output to the su pplementary motor area (SMA) likely contribute s to the ou, Kraakevik, & Horak, 2009). Basal ganglia output to the primary motor cortex play s a greater role in the execution of the first and second steps (Massion, 1992). Studies on rats have demonstrated that GABAergic projections from the substantia nigra pars reticulate (SNr) to the brainstem, and in particular the pedunculopontine nucleus (PPN), are also important in the initiati on of gait (Takakusaki, Habaguchi, Ohtinata Sugimoto, Saitoh & Sakamoto, 2003; Takakusaki, Saitoh, Harada, & Kashiwayanagi, 2004; Nandi, Jenkinson, Stein, & Aziz, 2009). Difficulty initiating gait typically emerges in PD when patients begin to suffer from postural instability, which progressively appears at the later stages of the disease. The dopaminergic denervation of the striatum causes over activity of the GABAergic output to the thalamus and brainstem, resulting in increased inhibitory control over t he basal ganglia thalamocortical loop and the basal ganglia brainstem system (Taka kusaki, Tomita, & Yano, 2008). Excessive inhibition of thalamocortical projections thereby leads to defective activation of the motor cortical areas controlling gait initiati on (i.e ., SMA, primary motor cortex). Additionally, excessive inhibition of the PPN and other structures in the brainstem critical for gait initiation (i.e., midbrain locomotor region) contribute to gait failure. Abnormalities in the circuitry of gait in PD result in inefficient anticipatory postural adjustments as evidenced by increased movement preparation time, and decreased velocity and magnitude of the COP displacements (Burleigh Jacobs, Horak, Nutt, Obeso, 1997; Crenna et al., 1990; Halliday et al., 1998). In particular, the initial posterior

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17 and lateral COP movement toward the swing foot during the APAs is reduced and slower in persons with PD. Additionally, the initial steps of persons with PD are characterized by reduced step length and velocity compared to age matched c ontrols (Crenna et al., 1990). Collectively, research has shown that gait initiation parameters in persons with PD (relative to healthy controls) are smaller, slower, and less forcefu l. As the disease progresses, these gait abnorma lities become more pronounced, limiting quality of life (Morris, Iansek, Smithson, & Huxham, 2000). Pharmacological interventions typically involve the administration of levodopa or dopamine agonists which alleviate motor symptoms by normalizing dopamine l evels (Sethi, 2008). While some symptoms of gait disturbance in PD respond to standard anti parkinsonian medication, postural symptoms and akinesia are often minimally improved or even exacerbated by levodopa therapy (Pullman, Watts, Juncos, Chase, & Sanes 1998; Starkstein, Esteguy, Berthi er, Garci, & Leiguarda, 1989). The high and rising prevalence of PD coupled with the lack of adequate treatment for gait deficits in PD necessitates the development of novel and cost effective interventions designed to op timize motor therapy for locomotor dysfunction in PD. Emotion Deficits in PD The nigrostriatal neuronal degeneration in PD causes dysfunction not only in motor circuits, but also in limbic pathways (e.g., mesocortic olimbic dopaminergic pathway). Additiona lly, individuals with PD exhibit pathological changes in structures of limbic circuits including the amygdala and ventral tegmental area (Harding, Stimson, Henderson, & Halliday, 2002; German, Manaye, & Smith, 1989; Uhl, Hedreen, & Price, 1985). Not surpri singly then, PD is increasingly link ed with emotional dysfunction. For example, individuals with PD exhibit impairments in affective recognition as indexed by

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18 both facial expressions and prosodic production (Smith, Smith, & Ellgring, 1996; Caekebeke, Jenne kens Schinkel, van den Linde, Buruma, & Ross, 1991). Deficits in perception of emotional expression and greater symptoms of depression, anxiety, and apathy also characterize PD (McDonald, Richard, & DeLong, 2003; Slaughter, Slaughter, Nich ols, Holmes, & Ma rtens, 2001). I mportantly, these emotional symptoms in PD represent a distinct deficit in PD and are not just a product of motor dysfunction. Research has also revealed that individuals with PD exhibit reduced psychophysiological reactivity to aversive sti muli. Bowers and colleagues demonstrated to aversive pictures compared to healthy controls, while startle reactivity to pleasant pictures was similar to that of heal thy controls (Bowers, Miller, Mikos, et al., 2006) Miller et al., (2009) later qualified these findings by revealing a lack of startle potentiation to only a specific subcategory of aversive pictures; namely, mutilations. Similar startle reactivity in response to attack, contamination, pleasant, and neutral pictures was observed among control and PD patients. However, further statistical analysis indicated t hat the mutilation pictures may have been the only category of aversive pictures that were sufficiently arousing to detect a deficit in emotio nal reactivity in PD patients. The basis of this reactivity is unknown, but may be linked to disease related dopam ine depletion and the subsequent inhibition of the amygdala in respon se to stress inducing stimuli. While empirical investigations have examined how emotion alters involuntary movement (i.e., startle eye blink) in PD, researchers have yet to explore whethe r emotion modulates voluntary movements of persons with PD and whether such modulation is similar to that observed in h ealthy individuals. The current

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19 project will be the first investigation of how emotion impacts voluntary movement in persons with Parkin son disease. Emotion and Motor Function: An Integrated Approach A growing body of literature supports the long held notion that human emotions have evolved as fundamental action dispositions, facilitating behaviors essential for survival (Frijda, 2009; F rijda, Kuipers, & ter Schure, 1989; Lang, 1995). As such, emotions motivate behavioral responses to approach pleasant and avoid unpleasant stimuli and situatio ns. In general, unpleasant emotions activate defensive circuitry and prime avoidance behaviors, w hereas pleasant emotions activate appetitive circuits that prime approach behaviors. Importantly, however, accumulating evidence has revealed that not all aversive stimuli facilita te avoidance related behavior. For example, fearful facial expressions, rate d as appearing highly submissive and as equally affiliative as happy expressions (Hess, Blairy, & Kleck, 2000), have been shown to facilitate approach related upper extremity pulling movements (M arsh, Ambady, & Kleck, 2005). Additionally, although fear is generally associated with a withdrawal response (i.e., approach to safe places or an approach to threatening stimuli (Blanchard & Blanchard, 1994). Finally, several lines of research have shown that a nger, although negative in valence, elicits approach motivational tendencies (See Carver & Harmon Jones, 2009 for a review). As such, grouping of affective stimuli into specific categories (i.e., attack, mutilation), rather than broad valence categories (i .e., unpleasant, pleasant), is essential to a comprehensive understanding of ho w emotion influences movement. Based on the aforementioned evidence, particularly the Miller et al. (2009) study indicating a possible emotion specific

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20 reactivity deficit in PD, we utilize d the emotion specific approach in the current project by exploring how the elicitation of discrete emotions influences the initiation of gait. Emotion Modulated M ovement Collectively, behavioral and transcranial magnetic stimulation (TMS) dat a suggest that emotional stimu li prime or facilitate action. TMS evidence indicates that increases in emotional arousal (intensity) lead to greater primary motor cortex excitability when passively viewing emotional images (Hajcak, Molnar, George, et al., 2 007). This finding has been recently expanded and specified by Coombes, Tandonnet et al. (2009) who found increased corticospinal motor tract excitability during the preparation of a voluntary motor action when participants viewed emotional arousing images compared to neutral images. Behavioral evidence demonstrates that emotional state significantly influences parameters underlying single joint and whole body movements. Intense emotional states increase force production on non directional submaximal sustai ned movements (i.e., pinch grip: Coombes, Gamble, Cauraugh, & Janelle, 2008), while unpleasant emotional states increase force production on sustained extension movements at maximal exertion (Coombes, Cauraugh, & Janelle, 2006). Additionally, exposure to a ttack images compared to mutilation, pleasant, and neutral images, has been shown to speed reaction times on ballistic pinch grip and wrist extension movements (Coombes, Higgins, Gamble, Cauraugh, & Janelle, 2009; Coombes, Cauraugh, & Janelle, 2007). Coomb es et al. (2007) provided evidence that speeded reaction times in response to threatening images are driven by expedited central processing ti mes that precede the movement. These studies also further support the categorization of affective stimuli into emo tion specific, rather than broad valenced categories when evaluating emotion modulated movement.

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21 Critical to the current proposal, we recently evaluated the influence of emotional state on forward gait initiation in healthy young adul ts (Gamble et al., in review ). Participants initiated gait following the offset of affective stimuli (low and high arousing unpleasant, low and high arousing pleasant, and neutral) and continued to walk toward the location of the prese nted stimuli for several steps. Viewing hi ghly arousing unpleasant stimuli (i.e., attack images) speeded the initial motor response compared to all other affective stimuli, supporting the notion that threatening cues prime the motor system for action regardless of movement direction. However, the presentation of the pleasant stimuli facilitated the initiation of forward gait as indexed by greater posterior and lateral COP movement toward the swing limb during the anticipatory postural adjustments, as well as grea ter velocity of the COP shift. Furth ermore, the first step was executed with increased velocity following the presentation of pleasant images compared to unpleasant images. These data provided evidence that emotional state systemat ically alters gait initiation. Moreover, given that forward g ait represents a clear approach oriented behavior in this context, the finding that pleasantly valenced emotional pictures facilitated gait is consistent with the notion that affective valence uniquely contributes to movement modulation beyond the initial reaction time. As such, activating emotional circuits may an effective method to optimize the quality of intended movement, particularly for PD patients suffering gait initiation impairment. The Integration of Emotion and M o tor P rocesses Behavioral and T MS evidence collectively suggests that motor circuits are not segregated from affective processes; indeed such proc esses are largely desegregated. Based on research involving primates and rodents, Haber and colleagues proposed that emotion can be integrate d into the motor circuits via two potential mechanisms involving

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22 the basal ganglia (Haber, 2003; Haber & Calzavara, 2009). First, affective information can be channeled across functional basal ganglia cortical circuits via thalamic relay nuclei linking fun ctionally adjacent frontal cortical areas (limbic cognitive motor). Thus, information is channeled in a feedforward manner from the limbic basal ganglia thalamocortical loop to the cognitive and then motor loop, allowing affective information to shape the final motor output. Secondly, the limbic pathway can influence motor output via the striato nigro striatal pathway, in which the affective region of the striatum (i.e., ventral) modulates the motor and more dorsal region of the striatum thro ugh midbra in dopamine neurons. Critically, individuals with PD exhibit atypical activation within motor and limbic basal ganglia circuits via loss of dopaminergic neurons in the SN, causing mo tor and emotional dysfunction. DBS and DA therapy) emotion information may not be integrated into the motor system as in healthy individua ls. Parkinsonian pharmacological treatments normalize DA levels, we predict that emotion information will be successfully integrated into the motor system allowing emotional input to impact the quality of intended movements. In sum, persons with PD exhibit postural instability and difficulty initiating gait, which have highly disabling consequences that are not effectively treated by current pharma cological or surgical options. Research indicates that activating emotional circuits accelerates the initiation and execution of voluntary motor actions, and most importantly, facilitates anticipatory postural a djustments and step execution d uring forward gait initiation. A high degree of integration is known to exist among circuits involved with the production and regulation of emotion and motor systems, including the

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23 circuits involved with the regulation of gai t. However, important questions remain concerning how emotion modulate s movement in persons with PD. Given the integration of the emotion and motor circuits, and considering consistent behavioral evidence that emotional state modulates simple and complex m ovements, we postulate that manipulating emotional conditions may be an efficacious method to improving gait initiation parameters in persons with PD. The p urpose of the proposed project wa s to determine the impact of emotional state on the quality of ga it initiation in persons with PD. Individuals with PD and healthy aged matched controls were exposed to attack, mutilation, contamination, erotica, happy people neutral, and blank pictures. Participants initiate d gait at picture offset and continue d to wa lk for sever al steps at their normal pace. Of specific interest was to determine the extent to which specific emotion categories alter the speed of movement initiation (reaction time), the quality of the postural adjustments during gait initiation (as inde xed by COP displacements and velocities), and step execution (as evidenced by the length and velocity of the first and second steps). Comparisons of these dependent measures were made between the PD and control groups after viewing exemplars from the seven picture categories. Additionally, and replicating previous work (Gamble et al., in review ), we evaluate d the degree of change in gait initiation performance due to each affective category relative to the neutral pictures (i.e., percent change scores). The degree of change under such conditions was also compared across groups. The fo llowing hypotheses we re offered:

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24 Hypotheses Reaction T ime: 1) Across stimulus conditions, control participants would exhibit faster reaction times on the gait initiation task c ompared to participants with PD. 2) Exposure to attack pictures would lead to significantly faster reaction times on the gait initiation task compared to all other picture categories for all participants. 3a) If emotion modulates the speed of the initia tion of gait in PD patients to the same degree as healthy controls, then no significant differences would exist between control and PD participants for the attack percent change scores. 3b) However, if emotion does not modulate the speed of the initiatio n of gait in PD patients in the same way as healthy controls, then the attack percent change scores would be significantly smaller (smaller change relative to neutral category) for the PD participants compared to control participants. COP Trajectory and S tep Execution M easures: 4) Compared to PD participants and across all conditions, control participants would exhibit a) greater displacement and velocity of the posterior and lateral COP movement during the APA phase, b) greater displacement and velocity of the medial COP movement during the weight shift phase, c) greater displacement and velocity of the anterior COP movement during the locomotor phase and d) greater length and velocity of the first and second steps. 5) For all participants, exposure to the approach related categories of erotica and happy people would facilitate forward gait initiation compared to all other categories as evidenced by: a) greater displacement and velocity of the posterior and lateral

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25 movement during the APA phase, b) great er velocity of the medial movement during the weight shift phase, and c) greater length and velocity of the first and second steps. 6a) If approach related emotions modulate COP movements and step execution in PD patients the same way as healthy controls then no significant differences would exist between control and PD participants for the erotica and happy people percent change scores. 6b) However, if approach related emotions do not modulate COP movements and step execution in PD patients in the sam e way as healthy controls, then the erotica and happy p eople percent change scores would be significantly smaller for the PD participants compared to control participants. 7) For all participants, exposure to the pure withdrawal related categories of m ut ilation and contamination would debilitate forward gait initiation compared to all other categories as evidenced by: a) decreased displacement and velocity of the posterior and lateral movement during the APA phase and b) decreased velocity of the medial m ovement during the weight shift phase, and c) decreased length and velocity of the first and second steps. 8a) If withdrawal related emotions modulate COP movements and step execution in PD patients the same way as healthy controls, then no significant d ifferences would exist between control and PD participants for the contamination and mutilation percent change scores. 8b) However, if withdrawal related emotions do not modulate COP movements and step execution in PD patients in the same way as healthy controls, then the

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26 absolute value of the mutilation and contamina tion percent change scores would be significantly smaller for the PD participants compared to control participants.

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27 CHAPTER 2 REVIEW OF LITERATURE Introduction The purpose of this review is to synthesize relevant literature concerning the integration of emotion and motor function, with a specific focus on gait initiation. An additional objective is to gain a greater understanding of how the brain circuits involved with emotion and movement integration are altered among individuals who have Parkinson disease (PD), a disease with co morbi d emotional and motor deficits. Implications for understanding the disease as well as potential avenues toward developing novel treatments for PD (and other movement and affective disorders) are offered based on careful consideration of the current knowledge base and promising future research directions. The current chapter represents a focused review of the extant behavioral, neuroanatomical, and physiologica l basis for understanding the interplay of emotions and motor actions. Comprehensive treatment of this topic required assimilation of diverse and unique bodies of literature, as reflected in the organizat ion of the paper. First, an introduction to Parkinso n disease is provided with discussion of the underlying pathophysiological mechanisms of the disease and a review of the most common treatment options. Second, a section on motor function with specific emphasis on gait initiation is presented, including de scription of the neural circuitry involved and relevant theories of movement planning and control. The section concludes with a discussion of gait deficits in PD and its underlying pathophysiology. Third, information related to the study of emotion is prov ided, including a review of theoretical perspectives, the circuitry of emotio n, and emotion deficits in PD. Fourth, evidence for how emotions modulate

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28 movement, with emphasis on approach and avoidanc e movements, is elucidated. Current knowledge concerning the neural circuitry integrating emotion and mot or function is also addressed. Finally, the implications of how emotion may impact movement for individuals with PD are discussed. Parkinson Disease Parkinson Disease (PD) is a progressive neurodegenerative d isease of the basal ganglia that affects over one million individuals in the United States each year (Van Den Eeden, Tanner, Bernstein et al., 2003) Driven by dopamine depletion within the complex basal ganglia circuitry, persons with PD exhibit debilitating motor symptoms as well a s emotional dysfunction. The cardinal motor symptoms of PD in clude bradykinesia, tremor, rigidity, postural instability, and gait dysfunction. PD is the second most common degenerative disorder after Alzheimers, with an overall incidence of 13.4 per 100,000 (Van Den Eeden et al., 2003; Orr, Rowe, & Halliday, 2002) The incidence of PD dramatically in creases for people over 60 years old and with the aging US population, this number is projected to rise significantly in the coming years (Van Den Eeden et al., 2003) Sufferers of PD incur countless and measureless additional costs in terms of functional impairments that permeate and interfere with virtually every facet of daily living. Path ophysiology of Parkinson Disease PD is characterized by a loss of nigrostriatal neurons in the substantia nigra pars compacta (SNpc) of the basal ganglia (Pahwa & Lyons, 2007) The degeneration of dopaminergic containing neurons results in severe dopaminergic denervation of the striatum and a cascade of subsequent functional changes involving all components of basal ganglia circuitry (Blandini, Nappi, Tassorelli, & Martignoni, 2000) These

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29 path ological changes underlie most motor symptoms of PD, particularly akinesia (i.e., failure or slowness of willed movement) (Rosin et al., 2007) The onset of clini cal symptoms is associated with a 50 60% loss of nigrostriatal neurons and a 70% decrease in striatal dopamine concentrations (Bernheimer, Birkmayer, Hornykiewicz, Jellinger, & Seitelberger, 1973) Initially, the surviving neurons increase dopamine synthesis to compensate for the cell loss. However, as the disease progresses and neuronal loss increases the compensatory mechanisms fail and th e nigrostriatal neurons lose the ability to appropriately store and release DA (Mouradian, Juncos, Fabbrini, & Chase, 1987) Figure 2 1 demonstrates a schematic view of the internuclear connectivity of the basal ganglia neuronal networks, as well as the changes associated with PD. The striatum of the basal ganglia relays information from the cerebral cortex to the basal ganglia output nuclei (i.e., GPi and SNr) via direct and indirect pathways (Sohn & Hallet, 2005; Blandini, Nappi, Tassorelli, & Martignoni, 2000) In the direct pathway the striatum projects a subset of GABAergic neurons, expressing D1 dopaminergic receptors, to the GPi and SNr. Thus, the direct pathway inhibits the GABAergic inhibitory output of the GPi/SNr, resulting in the subsequent disinhibition of thalamic and brain stem nuclei. In the indirect pathway the striatum projects a subset of GABAergic neurons, expressing D2 dopaminergic receptors, to th e GPe. GABAergic inhibitory neurons of the GPe project to the STN, which sends excitatory glutamine rgic input to the GPi an d SNr. Thus, the indirect pathway increases the inhibitory output of the GPi/SNr to the thalamus and brainstem via the inhibition of GPe and subseq uent disinhibition of the STN. Collectively, the net output of the basal ganglia is regulated by

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30 the indirect (i.e., increases the inhibitory output of GPi/SNr) and direct pathways (i.e., inhibits the inhibitory output of GPi/SNr). Balanced activity between these the two pathways is essential for the control of voluntary movement. As shown in Figure 1, PD is char acterized by an imbalance of activity resulting from dopamine depletion of the SNc, which decreases the activity of the direct pathway while increasing the act ivity of the indirect pathway. This imbalance produces excessive inhibition of the thalamocortica l and brainstem motor systems, ultimately causing movement dysfunction. Researchers and clinicians now accept that the pathology associated with PD extends beyond nig rostriatal dopamine depletion. PD has been associated with the neurodegeneration of sero tonin and norepinephrine pathways in limbic circuits, and nerve cells in the dorsal motor nucleus of the vagus, the pedunculopontine nucleus (PPN), olfactory region, ventral tegmental area (VTA) and hippocampus (German, Manaye, & Smith, 1989; Pahapill & Lozano, 2000; Remy, Doder, & Lees, 2005; Sethi, 2008) Neurodegeneration in these nondopaminergic regions likely acc ounts for the non motor features of PD, including neuropsychiatric symptoms (i.e., affective disorders, dementia, hallucinations), sleep disorders, autonomic symptoms (i.e., urinary disturbances, sexual dysfunction), and sensory symptoms (i.e., pain, olfac tory symptoms) (Sethi, 2008) Treatment for PD Multiple treatment options cur rently exist for the management of PD, however, there is no cure for the disease and no trea tment alleviates all symptoms. A brief overview of the most common pharmacological and surgical approaches to the treatment of PD is presented next.

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31 Pharmacological treatments Levodopa For the past 40 years Levodopa (L 3,4 dihydroxyphenylalanine) has been the mainstay of symptomatic therapy for PD (Sethi, 2008) Levodopa, a metabolic precursor of the neurotransmitter dopamine, traverses the blood brain barrier normalizing dopamine levels. Research has shown that levodopa alleviates symptoms at all stages of the disease and does not result in tolerance over time (Markham & Diamond, 1981, 1986) The symptoms of bradykinesia (i.e., slowne ss of movement) and rigidity show the best response to this pharmacological treatment. Although providing benefits to virtually all patients, levodopa does not stop the progression of the disease and prese nts with several shortcomings. First, the duration of the medication action becomes progressively shorter with chronic usage (Muenter & Tyce, 1971) Additionally, chronic usage is associated with adverse effects, such as motor fluctuations and dyskinesia (i.e., the impairment of voluntary movements resulting from jerky motions) (Pahwa & Lyons, 2007) Furthermore, levodopa has little or no effect on certain motor (i.e., freezing of gait and postural instability) and non motor symptoms (i.e., sleep disturbances, cognition, and mood), which likely arise from the degeneration of n ondopaminergic systems (Sethi, 2008) Levodopa is typically prescribed with adjunctive therapies, such as dopamine agonists. Dopamine Agonists. Dopamine agonists were first used to treat PD in the late (Birkmayer & Hornykiewicz, 1961) In the last 30 years, DA agonists have been used to improve motor symptoms at all stages of PD, both as an adjunct therapy and as monotherapy. I n contrast to levodopa, this medication provides therapeutic benefits while delaying the development of dyskinesia and motor fluctuations (Brannan, Prikhojan, Yahr, 1997; Cedarbaum, Leger, Reches, &

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32 Guttman, 1990) DA agonists work by activating striatal D2 dopamine receptors, thereby normalizing the activity of the indirect pathway of the ba sal ganglia. Similar to levodopa, DA agonists fail to alleviate symptoms resulting from nondopaminergic pathology. Several side effects include nausea, sleepiness, confusion, orthostatic hypotension, and hallucinations (Poewe, 2005) Sur gical treatments deep brain s timulation Deep brain stimulation did not become a popular treatmen t for PD until the late 1980s. This neurosurgical treatment involves the surgical implantation of a battery operated neurostimulator, which is used to deliver a steady pulse of mild elect rical signals to targeted areas in the brain (Pahwa & Lyons, 2007) The electrical pulses are thought to block any abnormal firing of neurons. DBS in PD patients typically targets either the ventral intermediate nucleus of the thalamus, GPi, or STN (Benabid, LeBas, Grand, Krack, Cha bardes, Fraix et al., 2005) DBS of the ventral intermediate nucleus is the preferred target to treat th e medication resistant tremor. Studies have reported that DBS of this target significantly reduces Parkinsonism tremor in 60 95% of PD patients receivi ng the surgery (Benabid, Pollack, Gervason,1991; Koller, Pahwa, Busenbark, Hubble, Wilkinson, Lang et al., 1997) While tremor improves, other symptoms continue to progress (Hubble et al., 1997; Pah wa et al., 2006) Thus, DBS of the thalamus is only used for PD patients whose primary d isability is caused by tremor. DBS targeting the GPi and STN have been shown to improve all the cardinal symptoms of PD, as well as levodopa induced dyskinesia. Additi onally, research has documented the long term benefits of STN DBS (Pahwa, Wilkinson, Overman, & Lyons, 2003; Rodriguez Oroz, Obeso, Lang, Houeto, Pollak, Rehcrona, et a l., 2005) For example Rodriguez Oroz et al., conducting the first worldwide multicenter trial of DBS in PD, assessed 69 PD

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33 patients 3 4 years following bilateral DBS surgery (STN = 49, GPi = 20). At the 3 4 year follow up, patients who received STN DBS s III), while GPi DBS induced a 39% improvement. Stimulation of both targets also improved the cardinal features of PD (except postural i nstability), activities of daily living However, comparison of the improvement induced by STN stimulation at 1 year compared to the 3 4 year follow up demonstrated a significan t worsening in both the III, ADLs, speech, postural stability, and gait. Similarly, comparison between improvement induced by GPi stimulation at 1 year and 3 4 years revealed a significant worsening in th medication states on t he UPDRS III, gait, and ADLs. Thus, while STN and GPi DBS surgery appear promising for improving motor symptoms in PD, the beneficial effects on gait and postural stability do not appear to persist long term. Although DBS is c onsidered a relatively safe procedure, adverse effects usually arise from one of three complications: surgical, hardware related, or stimulation (Pahwa & Lyons, 2007) Surgical complications may include hemorrhage, seizures, infections, and mispla ced leads (electrodes). Such complications usually occur within 30 days post surgery and occur in less than 5% of all patients. Hardware related complications include electrode and extension wire (i.e., connects electrode to neurostimulator) failure and of t en require repeated surgeries. Stimulation complications depend on the exact location of the lead and intensity of stimulation and may include double vision, dystonic

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34 posturing (i.e., sustained unnatural positioning of a body part with a rotational compon ent), depression, mood changes, pain, and limb and facial muscle spasms. Physical therapy A variety of physical therapy approaches have b een used to treat PD patients. The focus of therapy is largely directe d by the stage of the disease. Patients with mil d to moderate PD are usually taught exercises designed to delay or prevent the aggravation of motor impairment (Lugassy & Gracies, 2005) Additionally, a major goal of physical therapy is to improve postural control and reduce the fre quency of falls (Pelissier & Perennou, 2000) These exercise techniques may include resistance training, attentional strategies and sensory cueing, active mobilization and stretching, a s well as treadmill training. Research has shown that lower limb resistance trainin g in PD patients improves balance and gait by increasing lower limb muscle strength (Hirsch, Toole, Maitland, & Rider, 2003; Scandalis, Bosak, Berliner, Helman, & Wells, 2001) Additionally, an increa singly prevalent technique in physical therapy is the use of external visual or auditor y cues to enhance performance. For example, a number of studies have shown that horizontal floor markers used as visual cues normalize PD patients stride length, velocit y, and cadence (Morris, Iansek, Matyas, & Summers, 1996) In adv anced PD, patients who experience freezing episodes can be taught to replace the deficient internal motor cues normally provided by the basal ganglia with external auditory, visual, or proprioceptive cues to initiate movement (Morris, Iansek, & Kirkwood, 1995) Research is needed to investigate the long term benefits of physical therapy and the most eff ective regimens for improving motor symptoms. In sum, current pharmacological and surgical therapies for patients with PD have shown clear but limited benefits as treatments for postural ins tability and gait difficulties.

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35 Gait symptoms are disabling and co ntribute to the progression towards loss of independence and ultimate confinement to a wheel chair. A pressing need therefore exists to develop novel complimentary therapeutic strategies to treat disabling gait disturbances. Additionally, the high prevalen ce of non motor symptoms, such as depression and apathy, often complicate therapy and reduce overall quality of life A high degree of integration is known to exist among neural circuits involved with the production and regulation of human emotion and moto r systems, including those involved with the regulation of gait (Haber, 2003; Haber & Calzavara, 2009; McFarland & Haber, 2002) Given the integration of emotion and motor circuits along with recent behavioral ev idence demonstrating the impact of emotion on movement (e.g., Coombes, Cauraugh, & Janelle, 2007; Coombes, Gamble, Cauraugh, & Jane lle, 2008; Gamble, Joyner, Coombes, Hass, & Janelle, 2009) manipulation of emotion may be a viable strategy for improving mo vement in individuals with PD. This review will attempt to provide a foundation from which to advance these efforts and establish clear links between emotion and motor function by presenting a comprehensive account of the processes involved with human movement and emotion. As a basis for discussion of how emotions influence motor function, traditional and contemporary theoretical app roaches to explaining the mechanisms that underlie motor execution are reviewed next. Overview of Movement The purpose of this section is to first provide an introduction to the theoretical perspectives that have guided the field of motor behavior. Follow ing the review of general motor theory, the focus will narrow to discussion of a specific movement, gait

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36 initiation. The neural mechanisms underlying gait initiation will be detailed followed by a review of gait dysfunction in PD. Theories of Motor Contr ol Two schools of thought have dominated the motor learning and control literature (Newell, 2003) The cognitive (indirect) school of thought interprets human motor behavior based on the ideas of schema theory and motor programs. An ecological (direct) school of thought arose as a competing theor y to the cognitive approaches and views motor behavior through a dynamical systems framework. The dominant theories of both perspectives will be discussed next. Cognitive theories of movement control and coordination The cognitive approach to understandin g motor behavior views the mind largely as a computer analogue, able to form symbolic representations in the c entral n ervous s ystem (CNS) during goal directed behavior. The early cognitive phenomenological approaches to understanding motor behavior (e.g., Closed Loop Theory, Schema Theory) were concerned with the development of laws and principles of motor behavior, without regard for the underlying brain circuitry that regulates emergent behaviors. These theories will be reviewed first, followed by discuss ion of a more recent structural model of motor action which distinguishes the neural substrates underlying motor planning and motor control. One of the earliest theories of motor control was proposed b y psychologist William James (James, 1890) requi re much conscious involvement. James hypothesized that while attention is needed to in itiation an action, the remainder of the movement is controlled

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37 Response chaining Hypothesis movement is initiated by internal or external signals th at cause a muscle contraction. The movement produced b y the muscle contraction generates sensory information, or response produced feedback. As demonstrated in Figure 2 2 feedback triggers the 2nd muscle contraction, which again produces response produced feedback which t riggers the third contraction. This pattern continues until the performer produces all the muscle contractions ne eded to complete the movement. Response Chaining Hypothesis was disproved by the many studies on deafferented animals (Polit & Bizzi, 1978; Taub & Berman, 1968) and humans (Kelso, 1977; Kelso, Holt, & Flatt, 1980; Smith, Roberts, & Atkins, 1972), demonstrating that movements can occur in the absence of a ny movement produced feedback. Additionally, research on locomotion and gait revealed how movement can occur without sensor y feedback (i.e., central pattern generators). Adams Closed Loop Theory (1970). existence of two structures (i.e., a memory trace and a perceptual trace) which produce and regulate movements through open and closed lo op processes (Adams, 1971) Initiated by the volition of the individual, a memory trace acts in an open loop fashion by selecting and in itiating the desired movement. The memory trace is a central representation of the sensory feedback from a previously successfully execu ted movement of the same type. In essence, the memory trace acts as a motor program to i nitiate moveme nt in the absence of feedback. After the response is executed, a perceptual trace evaluates the correctness of the motor response as executed by the memory trace. As such, the perceptual trace provides a reference as how to adjust the

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38 next mo vement based on the knowledge of re sults that have been received. However, response produced feedback is often too slow to guide the control of rapid movement. movements. Moto r Program Concept (1975) Originally dating back to the thinking of James (1890) Lashley (1917) Keele (1968) and Keele and Summers (1975) the motor program concept applied a computer metaphor to the control and lea rning of human motor behavior. According to this open loop view, central structures or programs represent the desir ed characteristics of a movement and when activated, these abstract representations produce the movement with minimal regard for sensory information. Only after sufficient time has passed can central information processing mechanisms modify the movement. E arly studies of the motor program concept primarily investigated rapid discrete motor responses (< 250 ms) in an effort to reduce any feedback corrections that would taint the results. Two major challenges for motor control and learning theorists arose fro (Schmidt, 2003) : 1) the storage problem for memory of movement and 2) the novelty problem. memory trace, assumed that a program or trace was ne eded for every separate movement that could be performed. The storage problem held that the limited memory capacity of the human central nervous system was not capable of storing the vast amount of movement representational details for all the actions of a n individual over a lifetime. The novelty problem highlighted the inability of current theoretical approaches

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39 to account for how humans produce a movement that has not been previously performed. Schmidt developed Schema Theory to address these limitations Schema Theory (1975). Loop theory and the motor program concept, Schmidt (1975) developed a theory designed to account for how humans produce and store the numerous movement variatio ns capable of being performed. In contrast to the previous theories, Schema theory could also explain the control and learning of rapid and slow movements, discrete movements, movements with and without visual feedback, and tracking movements. A central tenet of schema theory is that two independent memory representations control programmed movements. First, an abs tract memory structure, called the general motor program (GMP), is capable of transforming stored codes into patterns of movement. The GMP is the basis for producing motor responses within a movement class that share invariant characteristics (i.e., sequen ce of submovements, relativ e timing, and relative force). The second memory representation, the parameters specifies the variant characteristics of the movement before execution (i.e., absolute time, absolute force, and muscle selection). The major suppor t for the GMP and parameters as separate memory states originated from studies showing that the structure of the movement remains invariant while the temporal, spatial, and force dimensions of the movement vary (Gentner, 1987; Schmidt, 1985; Wright & Shea, 2001; Wulf & Schmidt, 1989; Wulf, Schmidt, & Deubel, 1993) The GMP was an upgra de of the motor program concept and the most important idea distinguishing Schema theory from the Closed loop theory. A key feature of the GMP concept is that the programs are generalized so that humans can execute many different movements with the same

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40 program and generate novel movements through the selection of parameters that have not been previously used. and novelty problems of motor control and learning. However, Schema theory is limited by i ts failure to address how GMPs are acquired or modified; the existence of GMPs is merely assumed with no neurological basis for the assumption. Schmidt also proposed that humans develop schema rules through practice and experience across a lifetime. A sche ma rule is the relationship between the movement outcomes of past attempts and the parameters selected on those at tempts. Schema rules can be categorized into recall and recognition schemas. A recall schema describes the relationship between the parameters selected for a motor program on each movement trial and the achieved movement outcome. Essentially, recall schema is used to scale movements governed by the GMP across one or more superficial dimensions (e.g., speed, size, muscles used) and by the allocat ion of movement parameters ( e.g., absolute time or force). Recognition schema is a rule that describes how past sensory consequences caused by running the motor program are related t o the outcomes of the program. Schema theory predicts that variable practi ce within a class of movements (i.e., practice in parameter selection for the GMP) facilitates the development of schema rules, and thereby enhances the ability to select novel parameters in future situations. Although still one of the primary cognitive a ccounts of human motor control and learning, schema theory is deficient in a number of ways. One major problem of schema theory is the lack of explanation for how GMPs are acquired or modified. Rather, the theory focuses primarily on how individuals learn to scale GMPs. Additional problems

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41 have arisen from the GMP concept including 1) evidence disproving the idea that relative force is invariant in the GMP and 2) studies showing that the GMP cannot account for movements involving gravity (e.g., Schmidt & McGown, 1980) Finally, as notions of schema theory were based primarily on studies of discrete actions, environment are beyond the scope of the theory (Schmidt, 2003) Thus, while schema theory has provided important insights into certain aspects of motor control and learning, modification of some of the basic tenets is needed to account for a greater database of empirical findings. Planning Control Model Glover (2004) proposed a model of human action production which dichotomized human motor behavior into motor plannin g and motor control processes. Evidence from brain damaged samples (Grea et al., 2002; Jakobson, Archibald, Carey, & Goodale, 1991; Jeannerod, 1986) and brain imaging studies (Desmurget et al., 2001; Graf ton, Mazziotta, Woods, & Phelps, 1992; Krams, Rushworth, Deiber, Frackowiak, & Passingham, 1998) link the planning and control stages of action with distinct visual representations in the inferior parietal lobe (IPL) and the superior pari etal lobe (SPL), respectively. The planning stage generally takes place before movement initiation with the aim of selecting and initiating an adaptive motor program, while the control stage guides the execution of the action with the focus of on line correction of the spa tial parameters of the movement. Glover contends that the planning of a movement corresponds to brain activity in the inferior parietal lobe (IPL). Figure 2 3 gives a schematic illustration of the motor planning process. The initialization of motor plann ing begins with the descention of

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42 visual, cognitive, and sensory information from three separate regions of the brain to the IPL for integratio n. Visual information utilized for planning (i.e., spatial and non spatial characteristics of the actor and targe t, and the visual context surrounding the target) travels to the IPL via the temporal l obe and a third visual stream. The frontal lobes provide information on the overarching goals of the action and make decisions of executive control (cognitive input), wh ile the somatosensory association areas of the brain supply pr oprioceptive input to the IPL. The integration of these three sources of basal ganglia, and subcortical s tru ctures for the ensuing action. The selected motor program descends from the frontal lobes and subcortex to the peripheral nervous system initiating the movement. Ultimately, the planning system is responsible for selecting the target and the macroscopi c aspects of the movement and determining all movement parameters relating to the non spatial target characteristics, the initial movement parameters relating to spatial characteristics and the timing of movements. As the movement progresses, an efference copy of the plan is transmitted from the IPL to the superior parietal lobe (SPL) and cerebellum where the control system gradually takes over the movement. other sources of information (i.e. visual feedback and proprioceptive input) are removed or missing, the action will be executed according to the efference copy provided by the IPL and thus entirely as planned without the benefit of online adjustments. The gradual crossover of the planning stage to the control stage allows for smooth corrections of the movement. Through feedback (visual and proprioceptive input) and feedforward (efference copy) mechanisms, the control system monitors and

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43 adjusts the motor programs in flight (See Figure 2 4). A tr ansient visual representation (via the dorsal stream) integrates with proprioception and the efference copy in the superior parietal lobe (SPL) to p roduce the online corrections. theory, the control system, in contrast to the planning system, operates outside of conscious awareness and is confined to utilizing the spatial parameters of the target to guide online adj ustments. However, several studies (e.g., Brenner & Smeets, 1997) provide evidence indicating that control processes may not be completely immune to the interference of th e surrounding visual context of the target and cognitive processes. movement was planned, during the execution of the plan (i.e., noise in the neuromuscular system), or from unanti cipated changes in spatial characteristics. Because the control system often corrects for errors in planning, control processes routinely contribute t o errors in action production. Furthermore, the accuracy of longer duration movements, which provide visu al and proprioceptive feedback loops more time to operate, primarily rely upon the control system. Indeed, removal or alteration of any success/outcome of the intended movement. The control model appears to be its over simplistic nature in the distinction between motor p lanning and control processes. inferior pari etal lobe (IPL) and motor control is mediated by the superior parietal lobe (SPL) is too strong and schematic (Battaglini, Naranjo, & Brov elli, 2002) Similarly, not all movements can be neatly partitioned into p lanning and control processes. For

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44 example, as will be discussed later in the Movement section of this review, the initiation of gait involves a preparatory and execution component, both of which likely involve a combination of planning and control processes. In addition, the mechanisms underlying planning may be much more div erse than suggested by Glover. Based on evidence from models of deficits in apraxia (i.e., the inability to e xecute complex coordinated movements without muscular or sensory impairments), Longo & Bertenthal (2004) suggested that in complex, ecological situations planning will have goals of both selecting adaptive motor programs (as stated by Glover) and inhibiting non adaptive motor pr ograms. motor planning and motor control currently provides an attractive conceptual framework for understanding and analyzing human action production. Ecological theories of movement cont rol and coordination The ecological approach emerged from efforts to alleviate the limitations within the cogniti ve approach to motor control. These limitations include: 1) the arbitrary nature of the description of the abstract representations, 2) the ass umption of performer environment independence and the resulting focus on the elements of movement outcome rather than on the intrinsic dynamics of the constraints that guide dynamical organization to movement outcome, and 3) the disregard for the level of control inherent in the musculo skeletal system (Davids, Button, & Bennett, 2003) The following section reviews the ecological perspective of motor behavior with a primary focus on Dynamical Dynamical systems theory. Dynamical systems theory (DST) rejects the concept of a symbolic representation guiding mot or control and focuses on the natural control within the nonlinear dynamics of the musculo skeletal system (Kelso, 1995;

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45 Newell, 1986) DST incorporates biology, psychology, mathematics, and chemistry to de scribe biological movement systems as complex dynamical systems (Williams, D avids, & Williams, 1999) The human neuromuscular system is perceived as an integrated network of co dependent subsystems compo sed of many interacting parts. These subsystems function over multiple scales of space and time. Rather than viewing the organis m and environment as independent, DST views the organism environment as the unit of analysis for studying moveme nt in the natural environment. Ultimately, patterns of coordination and control emerge through physical processes of self organization and the c onstraints imposed on the neuromusculoskeletal system by the vast arrays of energy surrou nding the biological organism. Over the past several decades, ecological oriented scientists have effectively applied DST to movement coordination and control (Beek & O., 1988; Davids, Button et al., 2003; Kelso, 1995) Support for DST has been primarily based on st udies of two limb interactions. Research shows that two stable coordination patterns naturally emerge during the timing of continuous, oscillatory, and bimanual movements (Oscillation tasks: Ke lso, 1984; wrist rotation task: Lee, Blandin, & Proteau, 1996) The most stable pattern of coordination, termed in phase, occurs when timing of landmarks within one cycle is similar (0 degrees). The less stable, anti phase mode of coordination is a 1 80 de gree shift from in phase. A phase transition occurs when one coordinat ion pattern changes to another. Increased speed of the anti phase pattern results in an unintended phase transition to the in phase mode of coordination. Importantly, this unintended pha se transition illustrates the self organization principle of DST, which asserts that organisms exhibit a natural tendency to perform more stable patterns and switch into more efficient

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46 patterns under certain parameter condi tions (e.g., increased speed). Ad ditionally, these phase transitions to more stable patterns occur often without conscious control and can be accelerated or delayed with mental effort, as well as by emotional input (i.e., anxiety; Court, Benn et, Davids, & Williams, 1998). More specificall y, self organization is the principle of spontaneous pattern formation in movement that results from a large num ber of interacting components. Critically, self organization alleviates much of the decision making responsibilities about movement from the exe cutive system, and therefore allows the biological system to operate automatically, yet sub ject to conscious intervention. DST proposes that scientists will gain a greater understanding of human motor behavior in organizational principles rather than psych ological constructs such as symbolic representations in the CNS (Kelso & Schoner, 1988) According to DST, different organizational states surface due to the internal and external constraints placed on a biological system (Newell, 1986) By limiting the number of possible configurations that a complex system can assum e, these constraints impose the boundaries in which the human neuromuscular system must function and thus, channel and guide patterns of movement coordination and control. The biological system, at any time, will always produce optimal states of organizati on for the specific con straints acting on the system. Newell (1986) classified constraints into three categories, discussed next. One of the most organizing individual neuromuscular system to produce optimal patterns of coordination and

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47 movement. Newell also proposed that the constraints imposed on the dynamical movement system fluctuate over time, with the optimal pattern of movement coordination and control changing accordingly. According to Newell (1986) three categories of constraints converge to shape the patterns of coordination and control produced by th e neuromusculoskeletal system. These constraints include organismic, environmental, and task (See Figure 2 5). Organismic constraints are endogenous to the individual neuromusculoskeletal s ystem and can be further divided into structur al and functional constraints. Structural constraints are the physical constraints that are generally constant over time and include characteristics such as height, body mass, genetic make up, and anthropometri c and inertial chara cteristics of torso and limbs. Functional constraints vary over time, exhibit relatively faster rates of change, and can be physical or psycholo gical. These constraints may include intentions, perception, emotion memory, and decision m aking. The current study will examine how different emotional states constrain the specific movement of gait initiation. Environmental constraints are exogenous to the individual neuromusculoskeletal system and relate to the spatial and temporal la yout of the surrounding world. These constraints include ambient light, temperature, altit ude, and acoustic information. Newell and Jordan (Newell & Jordan, 2007) recently expanded the definition of the environmental constraints to include any physical constraint beyond the boundaries of the individual, such as tools and apparatus (i.e., originally considered task constraints). Task constraints are specific to the task being performed by the individual and pertain to the goals a nd rules guiding performance and the boundaries and instructi ons

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48 imposed on the performers. These constraints act as an umbrella over all the other constraints in determining what patterns of movement coordination the individual produces. led approach has important implications for scientists and clinicians. The traditional medical model considers variation in movement patterns as deviations from accepted norms and abnormal health as problems (Davids, Glazier, Araujo, & Bartlett, 2003) Alternatively, and taking a more adaptive approach, DST views disease as well as physical, cognitive, and perceptual disability as a constraint on the structure or function of the neuromusculoskeletal sy stem. Furthermore, DST considers movement variability as a functional means of allowing the individual to adapt to these numerous and ever changing constraints. Based on this approach, movement rehabilitation should focus on the achievement of an ideal mot or pattern during therapy and aim to help the individual satisfy the unique constraints imposed on him/her, improving functionality and performance (Glazier & Davids, 2009) Empirically, efforts should seek to determine the interacting constraints most influential in shaping and guiding patterns of m otor control and coordination. An increasing number of studies have used a constraint led approach to the study of movement, whereby different environment and task constraints have been experimentally manipulated to examine their influence on different movements in indivi duals with and without movement disorders (Davids, Kingsbury, & George, 1999; Van Emmerik & Van Wegen, 2000) The goal of the c urrent study is to explore which emotional states lead to the ideal performance on a gait initiation task in individuals with and without Parkinson disease.

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49 Such knowledge could be used to optimize movement rehabilitation for those suffering from gait impa irment. While DST has provided both concepts and tools that have been successfully applied to the study of human movement, the theory is not without limitations. First, DST has been criticized for poorly defining important theoretical concepts, such as se lf organization and constraints. For example, Beek et al. (1995) commented that some scientist s incorrectly view self organization as a magical ability which causes movement Secondly, few predictions of DST have been tested beyond the behavioral level, leading to a subsequent disconnect between the concepts of pattern formation and the neurophysiology of movement (Davids, Button et al., 2003) Summary Two significant perspectives of motor control currently exist. Cognitive based theories are based on the idea that information about movements is symbolically represented and stored as abstr act representation in the CNS. An alternative ecological approach views motor behavior as emerging from physical processes of self organization and the constraints imposed on th e neuromusculoskeletal system. The cognitive and ecological perspectives have exerted a widespread impact on the field of motor learning and control, providing the basis for a flurry of experimental work. However, both theories are limited by their abstractness in major theoretical concepts (e.g., GMP, self organization) and lack of reference to the mechanisms and structures of the human nervous system. A recently developed cognitivel y based structural model of human action production (Glover, 2004) proposed the existence of separate neural structures underlying motor planning and motor control processes. The planning control

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50 model, while providing a nice conceptual and basic framework for understanding the production of movement, was empirically founded on studies of hand and arm movements (i.e., reaching and grasping movements) and therefore best applied to such movements. In sum, one model has yet to describe all the major features o f human motor behavior yet theoretical advancements continue through disproof of existing conceptual notions As previously described, postural instability and gait difficulties are cardinal symptoms of Parkinson disease. Moreover, current pharmacologic al and surgical therapies are limited in their ability to treat gait dysfunction, and in particular the initiation of gait. Therefore, my objective is to substantiate the potential of a largely untapped strategy to optimize the quality of gait initiation p arameters through manipulation of emotion. Focus now shifts from discussion of motor theories to the specific movement of interest; gait initiation. Our theoretical approach to understanding the production of gait is influenced by concepts from the plannin g control model and involves a preparatory phase (postural adjustments prior to first step) and a locomotive phase (execution of first and second step), each of which is re gulated by slightly regulate the initiation of the pre paratory postural adjustments. Additionally, the automatic aspects of gait (i.e., rhythmic limb movements during gait ) are likely controlled by processes, which that operate outside of conscious awareness. However, as the transition is made from the preparatory phase to the locomotive phase of gait initiation to the automatic phase of gait, distinguishing between motor p lanning and

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51 motor contro l processes becomes difficult. As such, gait initiation will be viewed as emerging from the interaction of a preparatory phase and an execution or locomotive phase, rather than strictly planning and control processes. We will also how gait initiation is restricted by task, environmenta l, and organismic constraints. Humans adapt their gait in response to numerous situational constraints, and in the context of this revie w, the emotional state of the individual is the primary situational constraint of interest. Additionally and as will be discussed later, emotional state interacts with task constraints (e.g., the goal of the movement such as to approach or avoid an object) to determine the impact of emotion on movement. Organismic constraints include unique characteristics of the ind ividual, including disability. As such, Parkinson disease is considered a physical constraint on the function of the neuromuscular system. Anot dispositional susceptibility to emotional reactivity which is particularly important when studying PD, a disease characterized by high rates of apathy, depr ession, and anxiety disorders. Before explo ring the potential impact of the aforementioned constraints on gait initiation, it is critical to achieve an understanding of the processes and neural substrates regulating this specific movement, which is discussed below. Gait I nitiation Gait, or biped al locomotion, is a functional task involving the complex interaction and coordination of the major lower extremity joints of the body. This fundamental task is critical to performing ma ny activities of daily living. Consequently, scientists have sought to understand the typical body movements involved in normal gait, pathological conditions of gait, as well as therapeutic interventions to improve gait dysfunction. The

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52 follow discussion centers specifically on the initiation of gait, providing a description of initiation dysfunction in PD. Gait initiation (GI) is the phase between motionless standing and rhythmic walking (Hallet, 1990) Successful GI requires effective balance control as one moves from stable balance to continuously unstable gait (Halliday, Gai, Blessing, & Geffen, 1990) Prior to the initiation of the stepping movement, anticipatory postural adjustments (APAs) decouple the center of mass (COM) and the net center of pressure (COP). These postural adjustments include a series of muscle activations and changes in ground reaction forces that move the net center of p ressure (COP) backward and toward the initial swing limb to move the COM forward over the stance limb (Crenna, Frigo, Giovannini, & Piccolo, 1990; Massion, 1992) Execution of the first step beg ins when weight has been transferred to the stance limb (Crenna et al., 1990) Recent investigations of g ait initiation indicate that the COP trajectory during the preparatory postural adjustments can be divided into three separate periods (S1, S2, S3) based on two important landmark events (See Figure 2 6: Halliday, Winter, Frank, Patla, & Prince, 1998; Hass et al., 2004; Martin et al., 2002) S1 begins with the signal to initiate gait and e posterior and lateral position toward the initial swing limb. This backward displacement, caused by deactivation of the gastrocnemii and soleus muscles (Winter, 1995) produces the momentum needed to initiate forward gait (Polcyn, Lipsitz, Kerrigan, & Collins, 1998) Another important aspect of the S1 phase is the generation of stance side momentum caused by the lateral shift toward the swing limb to propel the COM

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53 towards the stance limb (Polcyn et al., 1998) A momentary loading of the swing leg by the hip abductors produces this later al displacement (Winter, 1995) S2 is the actual transfer of the COP from landmark 1 towards the stance limb, ending at the position under the stance limb on which the COP begins to move forwar d under the foot (landmark 2). This rapid transfer of the COP toward the stance limb propels the COM forward accelerating it away from the stance limb (Jian, Winter, Ishac, & Gilc hrist, 1993) The final region of the COP trajectory, S3, begins at landmark 2 and ends at toe off of the initial stance limb as the COP moves anteriorly. The neural control of gait initiation and execution As addressed earlier, the basal ganglia consist of the gray matter located at the base of the cerebral hemispheres, consisting of a group of interconnected subcortical nuclei including the striatum (caudate and putamen), globus pallidus, subthalamic nucleus (STN), and the substantia nigra (SN). Disorde rs of the basal ganglia, such as Parkinson Disease, are often characterized by an inability to initiate voluntary movements, slowness of movement, and an abnormal postural tone. Disturbances in gait initiation and postural instability are particularly prom inent in patients with PD. The presence of gait difficulties in disorders of the basal ganglia combined with research implicating the basal ganglia in the planning and execution of voluntary movements (Alexander & Crutcher, 1990; DeLong, 1990; Middleton & Strick, 2000) led researchers to propose that the basal ganglia play a prominent role in controlling locomot ion. Although knowledge is still limited, research on primates and rats suggests that gait is continuously regulated by inhibitory projections from the basal ganglia. Takakusaki et al. (Takakusaki, Habaguchi, Ohtinata Sugimoto, Saitoh, & Sakamoto, 2003) postulated that multiple channels from the basal ganglia brainstem system and the basal ganglia

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54 thalamocortical system control postural muscle tone and regulate the central pattern genera tors (CPG) in the spinal cord. The CPGs are circuits in the spinal cord responsible for producing the bas ic locomotor rhythm and alternating muscle activity during locomotion (Ivanenko, Poppele, & Lacquaniti, 2009) While details of this circuitry in humans are primarily unknown, Cazaletes & Bertrand (2000) suggest that upper lumbar segments in the spinal cord are th e major site for CPG activity. Central commands combined with proprioceptive feedback control CPGs (Drew, Prentice, & Schepens, 2004). As demonstrated in Figure 2 7, GABAergic basal ganglia output to the motor cortices via the tha lamus is thought to regulate the volitional aspects of gait, while GABAergic output to the brainstem regulates the automatic control processes of locomotion. The role of these two systems in controlling gait is outlined next. Basal ganglia thalamocortical loop The basal ganglia are involved in up to five known parallel and segregated circuits linking the cerebral cortex, basal ganglia, and thalamus (Alexander, DeLong, & Strick, 1986) The basal ganglia thalamocortical loops with the motor cortices are thought to control the volitio nal aspects of locomotion, such as initiation and termination of gait and modulation of gait pattern s based on environmental cues. GABAergic neurons from the internal segment of the globus pallidus (GPi) influence cortical areas v ia the thalamic relay neur ons. This basal ganglia output reaches both the premotor cortices and primary motor cortex, each of which serves a different function in the control of gait (See Figure 2 8). The secondary motor areas likely control the postural adjustments preceding gai t initiation (Massion, 1992) Research on bipedal walking in monkeys has shown that the supplementary motor area (SMA) has dense connections with the pontomedullary

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55 reticular formation ( PMRF : Keizer & Kuypers, 1989) the brain area responsible for regulating po stural control during walking. Furthermore, research on quadrupeds ind icates that the PMRF is involved in the control of posture via brainstem spinal pathways that are activated by motor corticofugal projections (Drew, Prentice, & Schepens, 2004; Kably & Drew, 1998; Prentice & Drew, 2001; Schepens & Drew, 2003) As such, the cortico reticular projections fr om the SMA are assumed to control the timing and planning of the anticipatory postural adjustments that precede gait initiation. This notion is supported by multiple studies showing the activation of t he SMA during gait initiation. For example, Yazawa et a l. (1997) found greater bilateral activation of the SMA during initiation of externally cued gait re lative to simple foot dorsiflexion, suggesting that the SMA plays a more important role in gait initiation than in simple foot movements. Additionally, several studies have shown activation of the SMA, lateral premotor areas (PM), and the cingulated motor areas (CMA) during gait related activity (Fukuyama et al., 1997; Hanakawa et al., 1999; Miyai et al., 2001) Finally, individuals with damaged premotor cortices, including the SMA, frequently display freezing of gait or gait initiation difficulties. While the preparatory phase of gait initiation is likely controlled by the SMA, the primary motor cortex controls the stepping phase of gait initiation (Massion, 1992) Research indicates that basal ganglia output to the motor cortex controls the generation and velocity of voluntary movement (DeLong et al., 1984; Turner & Anderson, 1997) The primary motor cortex projects directly to the spinal cord, allowing for direct influence on the CPGs. Additionally, research on macaque monkeys and cats has provided evidence that the primary motor cortex has excitatory glutamatergic projections to the

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56 structures in the brain stem regulating p ostural muscle tone (i.e., PPN: Matsumura et al., 2000) and locomotion (i.e., PMRF: Matsuyama & Drew, 1997) Studies on cats indicate that the fine control of stepping movements, as well as adaptive walking movements, are largely d ependent on the primary motor cortex (Armstrong, 1988; Drew, Jiang, Kably, & Lavoie, 1996) Less is known about the cerebral control of human gait. However, using a near infrared spectroscopic topography technique, Miyai et al. (2001) found increased levels of oxygenated and total hemoglobin in the primary motor cortex and SMA when part icipants walked on a treadmill. Activation of the primary and secondary mo tor cortices during the volitional control of walking in healthy human subjects has also been demonstrated in studies using fMRI with mental imagery paradigms (Jahn et al., 2 008) and in studies applying single photon emission computed tomography (SPECT: Fukuyama et al., 1997; Hanakawa et al., 1999) Basal ganglia Brai n stem system The basal ganglia brain stem system controls the automatic regulation of postural muscle tone and rhythmic limb movements during gait through medial and lateral projections to the mesopontine tegmentum of the brain stem (See Figure 2 9). I n the mesopontine tegmentum, the midbrain locomotor region (MLR) and the muscle tone inhibitory region in the ventrolateral part of the pedunculopontine nucleus (PPN) are the two areas important for control of locomotion and postural muscle tone, respectiv ely (Takakusaki, Habaguchi et al., 2003) Research on decerebate cats with the striatum, thalamus, and cerebral cortex removed but SNr intact indicates that GABAergic efferents 1) to the PPN suppresses activity of the mu scle tone inhibitory system and 2) to the MLR suppresses activity of a locomotor executing system (Takakusaki, Habaguchi et al., 2003) Specifically, GABAergic

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57 efferents from the SNr activate cholinergic neurons in the P PN (Grofova & Zhou, 1998; Saitoh, Hattori, Song, Isa, & Takakusaki, 2003) which in turn activate the muscle tone inhibitory system via cholinoceptive pontine reti cular formation (PRF) neurons. T he inhibitory system controls the level of muscle tone by regulating the excitability of the motor neurons of the extensor and flexor muscles via postsynaptic inhibitory effects on (Takakusaki, Kohyama, & Matsuyama, 2003; Takakusaki, Kohyama, Matsuyama, & Mori, 2001) Additionally and as shown in Figure 9, the basal ganglia efferent to the MLR contr ols the locomotor pattern through two major pathways (i.e., pontomedullary locomotor strip, PMLS; medial medullary reticulospinal tract) descending from the MLR to the spinal cord (Grillner, 1981; Takakusaki, Habaguchi et al., 2003) ontrolling rhythmic limb movements. Several studies indicate that the basal ganglia brainstem system plays an important role in the initiation of gait (Garcia Rill, 1991; Skinner, Kinjo, Henderson, & Garcia Rill, 1990) Takakusaki et al. (2003) found that stimulating the SNr in rats with progressively increasing strength disturbed rhythmic limb movements, increased cycle ti me, and delayed onset of gait. Thus, Takakusaki suggested that the SNr GABAergic projections to the brainstem are involved in both the steady (e.g., postural control, rhythmic limb movements) and dynamic aspects (e .g., gai t initiation) of gait. Several studies have also demonstrated that lesioning the PPN in primates produces akinetic symptoms (Aziz, Davies, Stein, & France, 1998; Kojima et al., 1997) Furthermore, research on individuals with Parkinson Disease has revealed that damage to the PPN or pathological in put to the PPN from the basal ganglia causes movement initiation

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58 problems (Nandi, Jenkinson, Stein, & Aziz, 2008) The cholinergic PPN neurons likely regulate the initiation of gait through the modulation of postural muscle tone (Takakusaki, Habaguchi et al., 2003) Takakusaki et al. (2004) suggested that when an individual is preparing to initiate gait, tonic activity of the SNr neurons would continu ously inhibit the PPN and MLR until the arrival of a signal triggering gait onset. Upon the arrival of a trigger, decreased inhibitory input from the SNr to the brainstem structures would release the activity of the locomotor system (MLR CPGs) and the mus cle tone control system (PPN muscle tone inhibitory system) leading to the initiation of locomotion accompanied by the reductio n of the level of muscle tone. Importantly, the PPN and pontemedullary reticular formation receive excitatory input from the mo tor cortices and direct inhibitory input from the basal ganglia. Thus, the control of postural muscle tone and locomotion is likely regulated in parallel by a combination of basal ganglia inhibition and motor cortex excitation of the brainstem. Gait initia tion deficits in Parkinson disease A typical sign of akinesia (i.e., failure or slowness of willed movement) in persons with PD is difficulty initiating gait (Hallet, 1990) These gait initiation difficulties emerge when PD patients begin to suffer from postural instability and progressively appear at the later stages of the disease. Additionally, gait initiation dysfun ction is considered one of the most debilitating motor symptoms of PD and often remains even after the relief of all other symptoms. A major pathophysiological mechanism underlying hindered gait initiation in PD patients is start hesitation (Burleigh Jacobs, Horak, Nutt, & Obeso, 1997; Crenna et al., 1990) and inefficient anticipatory postural adjustments (Burleigh Jacobs et al., 1997; Crenna et al., 1990; Gantchev, Viallet, Aurenty, & Massion, 1996; Halliday et al., 1998; Hass, Waddell, Fleming, Juncos, & Gregor, 2005; Rosin, Topka, &

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59 Dichgans, 1997) Crenna et al (1990) showed that PD patients exhibit an increased duration of the postural phase of gait initiation, decreased propulsive forces during both the postural phase and the stepping phas e, and reduced length and v elocity of the first two steps. Similarly, Halliday and colleagues (1998) demonstrated that while gait initiation in PD is characterized by similar temporal and spatial patterns to that of healthy older and younger individuals, t are smaller and the step lengths and velocities during the stepping phase are shorter and slower, respectively (See Figure 2 10). Several studies have since supported (Rocchi et al., 2006; Vaugoyeau, Viallet, Mesure, & Massion, 2003) confirming that gait initiation parameters in individuals with PD are slower, smaller, and less forceful. As the disease progresses, these gait abnormalities become more pronounced, limiting the quality of life. The moto r deficits of PD are caused by progressive degeneration of the dopaminergic neurons of the substantia nigra pars compacta and the subsequent DA depletion of the striatum (Forno, 1996) As mentioned earlier, striatal DA depletion is estimated to have reached 70% at the time of diagnosis of PD, and even up to 90% in the posterior putamen ( the region of the striatum that is part of motor circuit) (Whone, Moore, Piccini, & Brooks, 2003) Ultimately, the dopaminergic denervation of the striatum increases the activity of the basal ganglia output nuclei resulting in increased inhibitory control over the basal ganglia thalamocortical loop and the basal ganglia brainstem system (Blandini et al., 2000; Takakusaki, Tomita, & Yano, 2008) Gait dysfunction is likely a spe cific disturbance of the GABAergic basal ganglia output to both the motor cortices and the brainstem (See Figure 2 11).

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60 In the basal ganglia thalamocortical loop, the motor cortical areas receiving basal ganglia output use the corticospinal tract to cont rol the volitional aspects of locomotion, in cluding the initiation of gait. In PD, a loss of dopaminergic neurons of the SNc and the subsequent abnormalities in the basal ganglia thalamocortical circuit leads to defective activation of the motor related c ortical areas during gait initiation (DeLong, 199 0; Playford et al., 1992) Specifically, the dopaminergic denervation of the striatum leads to decreased inhibitory control over the GPi and SNr, which causes excessive inhibition of the thalamocortical projectio ns to the motor related areas. Such thalamo cortical projections fail to facilitate activation of the motor cortical areas controlling gait initiation (i.e., SMA and primary motor cortex). Impaired anticipatory postural adjustments required for successful gait initiation may reflec t reduced activity of the SMA. Additionally, decreased cortical excitation to the PPN could increase the level of muscle tone, while decreased cortical excitation to the reticular formation and spinal cord may decrease the amount (hypokinesia) and velocity (bradykinesia) of movement (Takakusaki et al., 2008) In the basal ganglia brainstem system, the basal ganglia output to the MLR controls the automatic aspects of locomotion while output to the PPN regulates muscle tone. In PD, excessive GABAergic output from the SNr to the PPN, in combination with decreased cortical excitation of the PPN, may increase the level of muscle tone (Takakusaki, Habaguchi et al., 2003; Takak usaki et al., 2004) Additionally, several neuropathological studies on humans have shown that individuals with PD have up to a 50% loss of the cholinergic neurons of the lateral part of the PPN (Gai, Halliday, Blumbergs, Geffen, & Blessing 1991; Hirsch, Graybiel, Duyckaerts, & Javoy Agid,

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61 1987; Jellinger, 1988) Thus, the suppression of PPN activity as well as the loss of PPN neurons could result in gait an d posture abnormalities in PD. Furthermore, excessive GABAergic inhibition of the M LR combined with decreased cortical excitation of the MLR likely contributes to gait failure (Takakusaki, Habaguchi et al., 2003; Takakusaki et al., 2004) Dysfunction of the basal ganglia brainstem system along wi th that of the basal ganglia thalamocortical loop therefore, appears to be the most likely underlying locus for the pathogenesis of gait difficulties in Parkinson Disease (Takakusaki et al., 20 08) Summary In sum, gait initiation is likely regulated in parallel by the basal ganglia thalamocortical system and the basal ganglia brainstem system. Individuals with Parkinson disease exhibit disturbance in both systems caused by a loss of dopaminerg ic neurons of the SNc and a loss of PPN neurons. This dysfunction likely causes the slower, smaller and less forceful gait initiation pa rameters characteristic of PD. Identification of the constraints that impact gait is essential to the optimization of ga it parameters in indi viduals with Parkinson disease. Despite the growing body of literature supporting the long held notion that emotions prepare the body for action, little research has investigated how this situational constraint infl uences the initiatio n of gait. overview of emotion is provided. Knowledge of emotion theory, the circuitry of emotion, as well as the emotional deficits that typically characterize PD is essent ial to understanding 1) how emotion and motor systems are integrated in the human brain

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62 Overview of Emotion The purpose of this section is to describe the prominent theoretical perspectives in the study of emotion, as well as the neural mechanisms involve d in emotional processes. The section will conclude with a review of emotional dysfunction in Parkinson disease. Theories of Emotion Beginning with Darwin in the late 1800s, behavioral, biological and cognitive views of emotion have developed and progres sed almost independently. However, most theorists would now agree that emotion consists of several components including the subjective experience of affect, expressive behaviors, an integrated neurob iological response, and cognitive perception (Barlow, 2002) A brief overview of the behavioral, cognitive, and biological approaches to emotion is provide d, followed by a widely accepted integrative model of emotion that provides a foundation for understanding and analyzing the influence of affective states on human movement. Behavioral theories of emotion In 1872, Charles Darwin published The Expressio n of Emotions in Man and Animals and initiated the study of emotional behavior. Darwin investigated expressive behavior, emphasizing facial expressions and posture as f undamental aspects of emotion. He argued that the behavioral expressions of emotion are innate and have evolved because of functional significance; the preparation for action and communication. Importantly, his expressive behavioral approach assumes that the basic patterns of emotio n are fundamentally different. Studies by Ekman in the 1970s (Ekman & F riesen, 1971) distinct patterns of facial expression for primary emotions, such as fear, anger,

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63 happiness, and disgust across numerous and varied cultures. Additional behavioral and psychopatholog ical evidence also supported this notion (Ekman, Levenson, & Friesen, 1983; Izard, 1990) In The Principles of Psychology (1890) and Emotions (1922, written with physiologist C. Carl Lang), William James proposed a highly influential approach to emotions. The James Lang Theory proposed that certain behavioral and bodily reactions (e.g., changes in heart rate and blood pressure) are associated with specific emotions, and humans feel emotions because they perceive these bodily and behavioral changes. James proposed that three steps are ne cessary to produce an emotion. First, particular visceral, vascular or somatic changes are init iated in response to some antecedent event. Secondly, peripheral sensory receptors, detecting these changes, transmit signals to the brain. Finally, the brain produces activity necessary for La ng theory views basic emotions as differing from one another and having adaptive functional value. However, visceral reactions, rather than facial expressions, were viewed as the primary component of emotion. Research eventually refuted James ideas by sho wing that emotions can be experienced without visceral or somatic changes (Cannon, 1929; Lang, 1994) Cognitive theorie s of emotion Several cognitive approaches to emo tion have been proposed. Schachter & Singer (1962) first asserted that when humans experience generalized arousal, arousal is labeled based on the appraisal of the context. For example, if an individual were aroused by the presence of an intruder in the home then arousal would be labeled as fear However, if an individual experienced the same level of arousal during sexual

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64 relations, then arousal would be labeled as love Thus, emotion results from perception of a generalized arousal state, which is based on appraisal of the environmental context. Appraisal Theory was empirically tested in the following decades and received little support (Marshall & Zimbardo, 1979; Reisenzein, 1983) Several studies showed that emotional behavior can occur in the absence of arousal (Lang, 1968) The second cognitive approach, also based on cognitive appraisal, was proposed by Richard Lazarus (Lazarus, 1991; Lazarus, Averill, & Opton, 1970) Lazarus asserted that cognitive appraisals are the primary determi na nts of the emotional response. For example, if an individual appraises an approaching dog as dangerous, th en he/she will experience fear. et al. (1 964) showed that the stress response (i.e., skin conductance response) of subjects watching an anxiety provoking film was greater when the film was accompanied by a soundtrack which heightened the threatening aspects of the film compared to an intellectua lization soundtrack and no soundtrack. cognitive appraisal of the traumatic events in the film played an important role in determin ing their emotional responses. However, several problems have emerged with First, humans of ten experience irrational emotions, in which the emotional response is not preceded by any conscious rational appraisal (Barlow, 2002) Secondly, Zajonc (1984) showed that neural activity associated with affective processes can occur faster than the neural activity req uired for cognitiv e processes. According to Zajonc, emotions can be generated without prior cognitive processes, such as appraisals.

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65 Recently, psychologists have developed a more complete model of processing emotional information based on theories of embodied cognition (Niedenthal, 2007; Niedenthal, Mondillon, Winkielman, & Vermeulen, 2009) These theories view ly states and processes in modality specific systems that occurred when the information was initially acquired (Niedenthal, Barsalou, Winkielman, Krauth Gruber, & Ric, 2005; Smith & Semin, 2007) Interaction with a particular entity or situation during the initial acquisit ion of information (i.e., encoding) engages the sensory, mot or, and introspective systems. Future activation of any one of these response modalities, when the original entity or situation is not present, results in partial reactivation of the other encodin g modalities. As applied to emotion, emotional information processing involves reactivating at least potions of neural states across the relevant modalities that occurred during the original encoding of that emotion. Niedenthal (2007) gave a schematic illu stration of embodied emotion using the perception of an emotional stimulus : a snarling bear (See Figure 2 12). Encountering a snarling bear is a multimodal experience involving seeing the bear, hearing the bear growl, feeling afraid, and withdrawing or run ning away from the bear. Thus, neurons in the visual, auditory, affective, and motor systems are activated and highly interco nnected during this encounter. When thinking about or seeing a picture of a snarling bear in the future, the visual impression of t he bear reactivates the visual original experience, with a selective focus on aspects of the experience m ost salient to the individual. As the emotion of fear is likely t o be a particularly salient aspect of the experience, this affective state is likely to be reinstantiated followed by reactivation of

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66 parts of the motor system (e.g., withdrawal/avoidance behavior). Further discussion of the emodied emotion view as it expl ains the relationship between emotion and approach/avoidant movements is presented in the Emotion and Movement section. Biological theories of emotion Walter Cannon (1929) first proposed that emotions are a function of brain howed that the surgical removal of various brain regions in animals influenc ed the experience of emotions. For example, emotions appeared to be released when th e cerebral cortex was removed. Therefore, Cannon hypothesized that the cerebral cortex exerted c ontrol over emotions, rather than having direct involvement in the generation of emotions. Researchers continued to investigate the brain processes underlying emotion using methods of brain ablation and stimulation to determine specific anatomical regions associated with different emotions (Barlow, 2002) The limbic system was the focus of much of the early investigations (e.g., MacLean, 1963) To date, researchers have discovered multiple cortical and subcortical pathways underlying emotional processes (LeDoux, 1996; Lang, Bradley, & Cuthbert, 1998) and recently, scientists have begun to focus on the relationship of emotions to specific neurotransmitte rs and neuromodulator systems. Several neuroscientific models of emotion are presented in the Circuitry of Emotion section later. Integrative theories of emotion Modern affective theorists now apply a more integrative study to emotion, and realize emotional processing involves a complex interaction of neurobiological, beha vioral, and cognitive systems. One the most prominent integrative theories of (Lang, 1995; Lang, Bradley, & Cuthbert, 1998) conceptualizes emotions as fundamental action dispositions which have evolved to

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67 activate beh aviors essential for survival. Produ cts of Darwinian evolution, emotions are organized by two motivational systems in the brain that adaptively respond to appetitive and aversive stimuli (Dickinson & Dearing, 1979; Konorski, 1967; Lang et al., 1998) The appetitive s ystem, associated with pleasant emotions, directs behavioral responses to approach appetitive stimuli. The aversive system, associated with unpleasant emotions, directs behavioral responses to wit hdrawal from aversive stimuli. Based primarily on animal res earch, Lang hypothesized that each system consists of distinct neurophysiological circuits in the brain, which are primarily subcortical. Furthermore, each system can vary in intensity of act ivation (metabolic or neural). Thus, according to Lang, all human emotions can be organized according to two dimensions: valence (pleasant v. unpleasant) and arousal (i ntensity of activation). Furthermore, a large database has shown that emotional expression can be measured in three reactive response systems including 1 ) evaluative and expressive language, 2) physiological events, and 2) behaviors. Before discussing the neurocircuitry of emotion, a brief overview of the defensive and appetitive motivational systems, as indexed by the physiological and behavior systems, i s provided. Defensive system Animal studies show that threatening cues activate the defensive system, preparing the organism for overt defensive behavior including freezing and active flight (Fanselow, 1994) fear bradycardia (Kapp, 1979) and potentiation of the startle response (Davis, 2000) Several animal behavioral th eorists propose that defensive reflex reactivity to threatening stimuli is sequentially organized to reflect the imminence of threat (e.g. Blanchard & Blanchard, 1977 ; Fanselow, 1994 ) Accordingly, passive responses (e.g., freezing) initially increase with the proximity of a

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68 threatening stimulus, however as the predato r reaches striking distance the organism shifts to overt defensive beh avior (e.g., fight or flight). Based on physiological reactions measured during affective picture perception, Lang and colleagues (Codispoti, Bradley, & Lang, 20 01; Lang, Bradley, & Cuthbert, 1997) proposed a similar defensive response in humans, which they terme d the defensive cascade model. According to the model, increases in defensive motivation correspond to patterns of change in specific response systems (S ee Figure 2 13). Importantly, the level of arousal indicates the level of defensive activation. In the early stages of defense, characterized by low activation, orienting and attention to the threat ening stimulus is heightened. In this stage physiological changes include cardiac deceleration, inhibition of the probe startle reflex, and moderate increa ses in electrodermal activity. As arousal increases and threat becomes more imminent, metabolic mobilization for active defense replaces orienting behavior, si gnaled by increased electrodermal activity and potentiated startle reflex (Bradley, Cuthbert, & Lang, 1999) Additionally, at higher levels of defens ive activation when the organism is preparing for action, the cardiac response shifts from deceleration to acceleration. Finally, these physiological changes support the selected overt defensive reactions (e.g. fight or flight) when danger is most proximal Lang et al. (1997) suggested that in picture viewing contexts, unpleasant pictures most often elicit reactions analogous to the freezing animal and the post encounter stage. Furthermore, pictures of attack and mutilation, representing more imminent threa t than most other unpleasant picture categories (e.g., pollution, loss, illness, and contamination), likely activate the defensive system most strongly.

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69 Appetitive system The appetitive system is activated in contexts that promote survival (i.e., procr eation, nurturance, ingestion) and organizes behavior involved in approaching desired rewards or goals. Similar to defensive motivation, increased activation involves an initial orien ting followed by overt action. This orienting period is characterized by an initial cardiac deceleration and increased electrodermal activity. Furthermore, engagement of the appetitive system is associated with startle reflex inhibition (Bradley et al., 1999) possibly reflecting an increased inhibition of defensive reflexes during appetitive activation or sustained motivated attention (Bradley, Cuthbert, & Lang, 1993) Stimuli eliciting greater activation of the appetitive system (erotic couples v. hap py families) produce greater changes in the different resp onse systems. The current study will examine whether such affective pictures activate the defensive and appetitive systems similarly in individuals with PD compared to healthy controls, as evidenced in the fundamental parameters involved in movement execution In summary, the past century has seen the development of several independent views of emotion which have uniquely contributed to our understanding of the experience of emotion. Today, affectiv e theorists generally accept the idea that emotional experience involves the integration of each of these fundamental components. In addition to the aforementioned theories of emotion, several purely structural models of emotion have been proposed. The fol lowing section reviews these models, as well as the specific neural structures and circuits underlying emotional processes. Circuitry of Emotion The focus of this section is threefold: 1) to describe the key neuroscientific models of emotion which have gu ided contemporary research, including single system

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70 models of emotion, dual system models of emotion, and categorical accounts of emotion, 2) to elucidate the role of subcortical and cortical structures in the expression of emotions, and 3) to describe lim bic circuits specifically involving the basal ganglia. These concepts are reviewed with an eye towards identification of common structures and circuits that integrate emotion and motor system s Neuroscientific models of emotion Several models emanating fro m the neuroscience of human emotion have been developed based on fMRI and PET studies, as well as studies using lesion methods and pharmacological manipu lations on animals and humans. MacLean (1949; MacLean, 1952) proposed one of the earliest and most popular models, suggesting that the broad array of emotions humans exp erience are regulated by a single neural system comprised of a special group of integrated brain structu res, called the limbic system. The primate forebrain was thought to have evolved in hierarchical fashion into three basic patterns referred to as reptil ian, paleomammalian, and neomammalian. The neocortical tissue, which is only well developed in mammals, was predicted to be in volved in cognitive processes. primitive circuits that had been conserved t hroug hout mammalian evolution. MacLean which he proposed med iated all emotional processes. The primary structure of the limbic system included the hippocampal formation, alo ng with the hypothalamus, amygdala, septal area, and orbito frontal cortex. While the limbic system later expanded to include areas of the midbrain (Nauta, 1979) the inclusion criteria for limbic brain sc ientists until it was challenged on both theoretical and anatomical grounds particularl y

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71 during the last two decades. PET and fMRI studies have shown that emotional processes likely involve a more widespread pattern of activity than proposed by the Limbic regarded as an inadequate structural theory of emotion (LeDoux, 2000) Another early neural model of emotion hypothesized that all emotions, regardless of valence, are preferentially processed in the right hemisphere (Sackeim & Gur, 1978) Support for this hypothesis has primarily been acquired through lesions studies and patients with right hemisphere damage (Bowers, Bauer, & Coslett, 1985; DeKosky, Heilman, Bowers, & Valenstein, 1980; Heller, 1993; Mand al, Mohanty, Pandey, & Mohanty, 1996) However, behavioral studies with neurologically intact humans have provided conflicting evidence for th e right hemisphere hypothesis. For example, Smith and Bulman Fleming (2005) found a right hemisphere advantage f or processing negative stimuli, but failed to detect any hemispheric differences i n processing positive stimuli. Additionally, the right hemisphere model has been refuted by several neuroimaging studies showing the involvement of both the right and left he mispheres during the perception of emotion (Murphy, Nimmo Smith, & Lawrence, 2003) Collectively, the extant research indicates that the right hemisphere likely plays a critical role in only certain aspects of emotional processing, su ch as the recognition of emotion, as expressed by speech prosody and facial expressions (Bowers et al., 1985; Bowers, Blonder, Feinberg, & Heilman, 19 91; Davidson, Shackman, & Maxwell, 2004; Harciarek, Heilman, & Jodzio, 2006; Heilman, Blonder, Bowers, & Valenstein, 2003) The prosodic elements of speech include the melodic and rhythmic components of spoken language, such as tone of voice, which play a significant role in communicating the emotional state

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72 of an individual (e.g., happy, sad, angry). While this refinement to the right hemisphere model has received considerable support, affective theorists have begun to conceptualize the neural basis of em otion based on dimensional and multisystem neuroscientific models. Affective theorists have proposed two primary dimensional models of emotion. The valence asymmetry model (Davidson, 1984) hypothesizes that the left cortical areas are involved in the processing of positive emotions, while the right cortical areas are involved with pr ocessing of negative emotions. The action tendency model of emotion, representing a variation of the valence asymmetry model, organizes emotions based o n approach and withdrawal action tendencies (Carver, Sutton, & Scheier, 2000; Davidson, 1998; Lang et al., 1997) This model predicts differential involvement of the left and right anterior brain regions in approach and withdrawal related emotions, respectively. For example, ac cording to the action tendency/ motivational direction model, the emotion of anger, although negative in valence, is considered an approach related emotion and therefore should be preferentially processed by the left hemisphere (Harmon Jones & Allen, 1998) EEG research and brain based behavioral studies have provided greater support for the approach/ avoidance classification of emotions, compared to the valence classification (Carver & Harmon Jones, 2009; Harmon Jones & Allen, 1998; Lane, Reiman, Axelrod, Yun, Holmes, & Schwartz, 1997) A meta analysis examining the functional neuroimaging data on the study of human emotion (106 PET and fMRI studies) found greater left compared to right sided activity for approach related emotion, but symmetrical activity for withdrawal related emotions (Murphy et al., 2003) Several explanations have been proposed for why the asymmetry

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73 model of approach/withd rawal emotion has only been partially supported. First, the classification of emotions based on their associated action tendencies may only apply for particular emotions (e.g., anger, happ iness). Additionally, confusion exists regarding the categorization of c ertain emotions, such as fear. Although fear is generally associated with a withdrawal response, it can also elicit approach to safe places or an approach (Blanchard & Bla nchard, 1994) Finally, Davidson suggested that resting brain asymmetries, called affective style, predict reactivity to experimental elicitors of emotion (Davidson, 1998) Specifically, individuals with greater right frontal activation demonstrate greater reactivity to unpleasant stimuli, while individuals with gre ater left frontal activation demonstrate increased r eactivity to pleasant stimuli. Thus, individual differences in affective style could influence the degree of left and right brain activation in response to emotional stimuli and many neuroimaging studies have not accounted for such differences. Categorical accounts of emotion are becoming increasingly popular, which propose that unique patterns of neural activity mediate a small set of discrete emotions (Ekman, 1999) In contrast to the dimensional models of emotion which link neural activity to specific hem ispheres, the categorical account suggests regional specialization for the discrete emotions of fear, disgust, and anger (Murphy et al., 2003) In particular, research shows the amygdala to be selectively associated with fear (Laber, LeDoux, Spencer, & Phelps, 1995; Calder, Lawrence, & Young, 2001; Adolphs, Russell, & Tranel 1994) However, many investigators now view the amygdala as a detector of salience, rather than specifically fear (this issue is revisited later in the review). The globus pallidus of the basal ganglia and the insula appear to be particular

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74 active in m ediating the emotion of disgust (Sprengelmeyer et al., 1997 ; Calder, Keane, Manes, Antoun, & Young, 2000; Gray, Young, Barker, Curtis, & Gibson, 1997) while anger has been linked with activity of the lateral orbital frontal cortex (OFC: Adolphs et al., 1999) While both the action tendency an d categorical neuroscientific models of emotion have received considerable support, no available model can comprehensively account for the neuro logical basis of all emotions. The specific brain regions hypothesized to have specialized functions for emotion al processing are outlined next The role of specific brain regions for emotional operations The potential functional roles for several brain structures implicated in emotional o perations are summarized next. In particular, this section will focus on the brain regions with the greatest implications for PD, considering their functions in emo tion and movement integration. To begin, the roles of the medial prefrontal cortex (MPFC) and anterior cingulated cortex (ACC) are briefly addressed. Medial Prefrontal Cortex and ACC The medial prefrontal cortex is thought to be involved in emotional processing. Research has demonstrated that the MPFC is activated in response to emotional films, pictures, and recall, as well as positive and negative emotions (Lane et al., 1997; R eiman, Lane, Ahern, et al., 1997) Additional research suggests that the MPFC may be specifically involved in the cognitive aspects of emotional processing (Drevets & Raichle, 1998; Lane et al., 1998) such as attention to emo tion and appraisal of emotion. The cognitive appraisal of aversive stimuli (versus pass ive viewing) and regulating emotion while viewing emotionally evocative stimuli have been associated with greater activation of the MPFC and attenuation of amygdala activity (Hariri, Bookheimer, & Mazziota, 2000; Taylor Phan, Decker, & Liberzon, 2003)

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75 Furthermore, activity of the amygdala is inversely associated with MPFC activity (Abercrombie et al., 1996; Liberzon et al., 2002) reciprocal connections with the subcortical limbic structures, including the amygdala, researchers have postulated that the MPFC could act as a top down regulator of intense emotional responses generated by the amygdala (Phan, Wager, Taylor, & Liberzon, 2004) The ACC is also hypothesized to be involved with the cognitive components of emotional processing and may interact with the MPFC to regulate interconnected cognitive and em otional tasks (e.g., recognition or rating of emotional stimuli) (Phan et al., 2004). The ACC also appears to be preferentially important for the cognitive generation of affect (e.g., emotions induced by memories or imagery of affective events) (Teasdale et al., 1999) Finally, several studies suggest that the ACC mediates physiological arousal indexed by the galvanic skin conductance response and may be involved in regulating conflicting internal states (Critchley, Mathias, & Dolan, 2001) Amygdala The amygdala, located within the medial portion of the temporal lobe, is the primary brain region implicated in emotion. This subcortical limbic region consists of several nuclei, each of which can be partitioned into subnuclei. Additionally, each nucleus has unique inputs and outputs (LeDoux, 2007) A comprehensive discussion of the nuclei along with all their connections is beyond the scope of this review, therefore only a brief description of the primary nuclei and related functions is provided As shown in Figure 2 14, the amygdala consists of the late ral, central and basal nuclei. The lateral nucleus is considered the gatekeeper, as it receives inputs from the sensory systems (i.e., visual, auditory, somatosensory, o lfactory, and taste).

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76 connections to the central and bas al nuclei, which have strong output connec tions to other brain regions. The central nucleus, an important output region, controls physiological responses and emotional reactions ( such as freezing ) via connections to the brainstem. Finally, the basal nucle us is involved with the control of instrumental actions through connections with the ventral striatum. The amygdala was originally hypothesized to be involved specifical ly in fear related responding. Consistent with this notion, animal, lesion, and imagi ng studies have demonstrated that the amygdala is involved in detecting signals of threat (Isenberg, Silbersweig, & Engelien, 1999; Phillips, Young, & Scott, 1998; Scott et al., 1997) and coordinating the appropriate responses (King & Conway, 1992; Kulver & Bucy, 193 9; Weiskrantz, 1956) generating fearful emotional responses (Halgren, Walter, Cherlow, & Crandall, 1978; Ketter, Andreason, & George, 1996) and maintaining fear related emotions (Buchel & Dolan, 2000; LeDoux, 2000) M ore recent neuroimaging data indicates that the amygdala is also activated in response to appetitive stimuli (Garavan, Pendergrass, Ross, Stein, & Risinger, 2001; Hammann, Ely, Hoffman, & Kilts, 2002) Additionally, Phan et al. (2003) found that the perceived intensity of the emotional response positively correl ates with amygdala activation. Therefore, the amygdala is now hypothesized to have a more general role for responding to salient stimuli, regardless of valence (Davis & Whalen, 2001) Periaqueductal Gray (PAG) The PAG is considered the final common path for all defensive responses (Vianna & Brandao, 2003) Lesions of the PAG can permanently abolish defensive reactions (Graeff, 1994) or cause significant reductions

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77 of innate (Blanchard, Williams, & Lee, 1981) and learned defensive behaviors (LeDoux, Iwata, Cichetti, & Reis, 1988) Furthermore, lesions of the PAG can abolish defensive responses induced by amygdala and hypothalamic stimulation, whereas lesions of the amygdala or hypothalamus do not block defensive reactions elicited by PAG stimulation (Graeff, 1994). The PAG consists of four main longitudinal columns: dorsal medial PAG (dmPAG), dorsal lateral PAG (dlPAG), lateral PAG (lPAG), an d ventral lateral PAG (vlPAG). While the specific functio ns of these PAG subdivisions remain debatable, general hypoth eses have been forwarded. The dlPAG is thought to be involved in regulating unconditioned fear responses (i.e., freezing and escape behavior) induced by immediate danger (Canteras, 2002) Furthermore, the dlPAG has dense reciprocal connections to the hypothalamic nuclei mediating defensive responses (Cameron, Khan, Westlund, Cliffer, & Willis, 1995; Vianna & Brandao, 2003) The vlPAG likely mediates responses of conditioned freezing and quiescence via direct and reciprocal connections with the central nucleus of the amygdala (Rizvi, Ennis, Behbehani, & Shipley, 1991; Vianna & Brandao, 2003) Lesions of the amygdala reduce conditioned fear responses, such as freezing and the potentiated startle response, but do not affect the freezing response to i mmediate danger (Antoniadis & McDonald, 2001) Less appears i s known about the dm and lPAG. However, similar to the dlPAG, the dmPAG is likely invol ved in th e unconditioned fear response. The lPAG has been linked to attack defensive behavior. In addition to the dense reciprocal projections with the amygdala and hypothalamus, the PAG connects to the lower brain stem regions and the basal gan glia (Via nna & Brandao, 2003). The dlPAG has descending project ions to the cuneiform

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78 nucleus. Stimulation of the cuneiform nucleus produces freezing and escape behavior. The dmPAG, lPAG, and vlPAG project to the caudal raphe nuclei located in the medial porti on of the reticular formation. Stimulation of the caudal raphe nuclei elicits immobility (Morgan & Whitney, 2000) The vlPAG also sends direct projections to the motoneurons of the ventral horn of the spinal cord (Mouton & Holstege, 1994) The dPAG receives inhibitory GABAergic projections from the substantia nigra pars reticulat e (SNpr) of the basal ganglia. Lesions of the SNpr have been shown to increase defensive responses elicited by stimulation of the d PAG (Coimbra & Brandao, 1993) As such, the SNpr likely exerts inhibitory control of the defensive behavior organized at the level of the midbrain tectum. Basal Ganglia The basal ganglia nuclei implicated in affective processes include the ventral striatum (nucleus accumbens), ventral pallidum, medial tip of the S Nr, and medial tip of the STN. Neuroimaging studies hav e linked emotional processing, particularly related to reward and happiness, to increased neuronal activation in the ventral striatum and ventral pallidum. For example, several studies have found activation of the ventral striatum in response to happy face s (Morris, Frith, Perret, et al., 1996; Phillips, Bullmore, Howard, & Woodruff, 1998) and pleasant pictures (Lane, Chua, & Dolan, 1999) Additionally, increased cerebral blood flow in the striatum (head of caudate nucleus and putamen) has be en positively associated with viewing highly arousing sexual stimuli in males (Redoute, Stoleru, Gregoire, et al., 2000) Similarly, Rauch et al. (1999) found increased activation of the ventral globus pallidus during sexual and competitive arousal, as indexed by physiological resp onses and subjective ratings. Furthermore, Kampe and colleagues (2001) demonstrated that the

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79 perceived attractiveness of an unfamiliar face increased activation of the ventral striatum of the viewer when meetin Given the basal ventral striatum is ideally located to respond to incentive reward motivation and to the attainment of positive affect, such as happiness, that results from the progression t oward a desired goal (Davidson & Irwin, 1999) The basal ganglia may also have a functional role in processing the withdraw al related emotion o f disgust. Neuroimaging studies show increased basal ganglia activity in response to facial expressions of disgust compared to other emotions (Phillips et al., 1998; Phillips, Young, et al., 1997) Obsessive compulsive disorder who have basal ganglia dysfunction, exhibit impaired recognition of facial expressions of disgust (Sprengelmeyer et al., 1997) Given the n motor behavior, the basal ganglia may coordinate appropriate action responses toward a desired goal, such as approaching pleasant stimuli and withdr awing from unpleasant stimuli. Several limbic circuits involving the basal ganglia have been proposed base d on animal and human research. Given that a primary focus of this review is on a disorder of the basal ganglia (namely, Parkinson D isease), the limbic circuitry involving the basal ganglia will be reviewed in further detail. Knowledge of these circuits is crucial to understanding the emotional symptoms of PD resulting from basal ganglia dysfunction, as well as the potential integration of emotion into the motor circuit. Limbic circuits involving the basal ganglia Haegelen and colleagues (2009) proposed two limbic circuits involving the basal ganglia, along with the medial pref rontal cortex (anterior cingulated cortex (ACC), orbital

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80 frontal cortex (OFC), septal area), amygdala, hippocampus, the centromedian parafascicular nuclei of the thalamus, and the ventral tegmentum area (VTA). The limbic regions of the basal ganglia includ e ventral striatum [Nucleus accumbens (NAcc)], ventral pallidum, medial tip of the SNr, and medial tip of STN. In both circuits, the anatomically centrally located STN is considered a regulator of the limbic pathways. The first circuit consists of one of t he five parallel and segregated basal ganglia thalamacortical loops (Alexander & Crutcher, 1990; Alexander et al., 1986 ; Middleton & Strick, 2000), in which the higher and lower regions of the brain communicate with the basal ganglia (See Figure 2 15). The medial prefrontal cortex, including th e ACC, OFC, septal area, and medial surface of frontal lobe, send excitatory dopaminergic projections to the NAcc of the ventral striatum. The ventral striatum sends GABAergic inhibitory projections to the ventral pallidum, a major output region of the lim bic system, and the centromedial nucleus of the thalamus through the SNr. The thalamus sends excitatory projections back to the medial prefrontal cortex. In an indirect pathway, the STN receives inhibitory input from the ventral pallidum and excitatory glu tamatergic input from the media l prefrontal cortex. The STN then sends excitatory glutamatergic projections to the SNr, which sends inhibitor y projections to the thalamus. According to this model, a balance of the direct cortico subthalamic and indirect co rtico striato pallidal subthalamic pathways controls emotional processes (Alexander et al., 1986) Haegelen et al. (2009) proposed that a second circuit, involving the basal ganglia, amygdala, hippocampus, and the ventral tegmental area, plays a larger role in regulating emotional processes. In this circuit, the STN of the basal ganglia receives affective information from the limbic cortex (medial prefrontal cortex, amygdala,

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81 hippocampus) through an indirect and direct pathway (See Figure 2 16). First, the medial prefrontal cortex (i.e., ACC, OFC, septal area) directly sends affective and motivational information to the STN, which has reciprocal connections to the ventral pallidum. The STN sends excitatory glutamatergic projections to the ventral pallidum, which in turn sends inhibi tory projections back to the STN. n the indirect pathway, the medial prefrontal cortex excites the NAcc, which inhibits the ventral pallidum, possibly reducing the inhibition of th e STN from the direct pathway. The STN relays affective information from th e cortex to the VTA, via excitatory glutamatergic projections. The VTA sends excitatory dopam inergic input back to the STN. The VTA, a group of neurons located in the mes en cephalon, is considered the origin of the mesolimbic dopaminergic pathway and highly implicated in natural reward circuitry and motivation (Haber, 2005) Thus, according to Haegelen et al. limb ic information from the medial prefrontal cortex, indirect striatonigral pathway and the mesolimbic pathway (VTA) can be integrated and processed in the STN. As will be discussed in the Emotion and Movement section, emotion information from both limbic cir cuits may be integrated into motor basal ganglia circuitry. Emotion deficits in Parkinson d isease The nigrostriatal neuronal degeneration in PD influences all pathway connections involving the SN and striatum, including the mesocorticolimbic dopaminergi c pathways (Braak & Braak, 2000) Not surprisingly then, Parkinson Disease has been increasingly linked with emotional dysfunction. Indeed, impairments in emotional processing represent a distinct de ficit in PD. PD patients often display monotonous, flat, and poorly inflated speech, and are recognized as exhibiting masked faces (i.e., blunted facial

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82 expressivity) with the inability to make spontaneous emotional expressions (Ariatti, Benuzzi, & Nichelli, 2008) Greater symptoms of apathy, depression, anxiety, and anhedonia (i.e., the inability to experience pleasure in normally pleasurable act ivities) also characterize PD. For example, Leentjens, Marinus et al. (2003) reported the prevalence rate of Major Depression in PD to be 20 25%. A clinic based study of PD patients reported clinically significant depressive symptomatology in 5 7% of patients (Rojo, Aguilar, & Garolera, 2003) Furthermore, individuals with an affective disorder are at a greater risk of being diagnosed with PD compared to patients with osteoarthritis or diabetes ( Nilsson, Kessing, & Bolwig, 2001) Apathy, often masked as depression, can occur with or without depression. Thus, although apathy is a characteristic feature of PD, the exact prevalence of apathy is difficult to determine. Similar to the rates of depress ion, 20 52% of PD patients exhibit clinically significant anxiety symptoms (Shulman, Taback, & Rabinstein, 2002) Anxiety may present as generalized anxiety disorder, phobias, or panic attacks. The presence of anxiety m ay exace rbate existing motor symptoms. For example, Adkin et al. (2003) found that fear of falling was associated with impaired postural instability in PD patients. While the mechanisms underlying the increased rates of depression, apathy, and anxiety in PD are not completely understood, researchers acknowledge that they are likely independent from the functional disability and motor deficits characteristic of PD (Leentjens et al., 2003) Neurodegeneration of subcortical nuclei and ascending DA, serotonin, and norepinephrine pathways within the basal ganglia frontal circuits may play a critical role in producing depression and anxiety symptoms in PD (Remy et al., 2005) Remy et al., found that depressed PD patients

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83 compared to non depressed patients have a greater loss of dopami nergic and noradrenergic innervations in several regions of the limbic system, including the amygdala, thalamus, l eft ventral striatum, and ACC. Additionally, patients with greater anxiety symptoms had greater loss of dopaminergic and noradrenergic innerva tions in the amygdala and thalamus. Dopamine deficiency in the limbic areas may also be a cause of apathy (Czernecki, Schupback, & Regis, 2008) A consistent feature of idiopathic PD is significant patholo gical changes in the amygdala. Harding et al. (2002) found a 20% reduction in total amygdala volume and high concentratio ns of lewy body formation, particularly in the basolate ral amygdala. Furthermore, Ouchi et al. (1999) discovered that individuals with PD show up to a 45% decrease of dopamine agonist binding in the amygdala. Using fMRI, Tessitore et al. demonstrated that an emotional task was associated with bilateral amygdala activation in healthy subjects, but not in non medicated PD patients. I mportantly, dopaminergic repletion partially restored amygdala activation. The amygdala is not the only damaged structure of the limbic system found in PD, however. Mesolimbic dopaminergic networks are also damaged (Braak & Braak, 2000). Pos tmortem studies show that individuals with PD exhibit a 40% reduction in the number of ventral tegmental neurons (German et al., 1989) a 40 60% loss of cells in the VTA (Uhl, Hedreen, & Price, 1985) and a significant decrease in dopamine in the frontal cortex and hippo campus (Scatton, Rouqui er, Javoy Agid, & Agid, 1982) The amygdalar hypoactivity, resulting from reduced mesolimbic dopaminergic input from VTA, may cause the deficits in emotional expression and recognition found in PD.

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84 The extant research suggests that PD patients exhibit im paired recognition of emotion from prosodic cues and facial expressions, with a selective and disproportionate deficit for the discrete emotions of anger (Lawrence, Goerendt, & Brooks, 2007) disgust (Dujardin, Blairy, Defebvre, et al., 2004; Suzuki, Hoshino, Shigemasu, & Kawamura, 2006) and fear (Ariatti et al., 2008; Dara, Monetta, & Pell, 2008) These deficits may be caused by dopamine loss in the basal ganglia limbic circuits. Suppo rting this notion, Sprengelmeyer et al. (2003) showed that impaired recognition of disgust and anger from facial expressions can be partially attenuated by dopaminergic repletion. Furthermore, neuroimaging evidence has implicated a role of the basal gangli a in the processing of disgust and anger, as well as emotional prosody processes (Kotz, Meyer, Alter, et al., 2003; Wildgruber, Riecker, Hertrich, et al., 2005) Thus, a functional basal ganglia may be necessary for recognizing certain emotional meanings from the prosodic element of speech. Several studies have indicated that individuals with PD show reduced ps ychophysiological reactivity to emotional stimuli For example, Bowers and colleagues blink magnitude to aversive pictures, while startle reactivity to pleasant pictures was similar to that of healthy controls (Bowers et al., 2006) Miller et al., (2009) later qualified these findings by revealing a lack of startle potentiat ion to only a specific subcategory of aversive pictures ( mutilations ) Similar startle reactivity in response to fear, pleasant, and neutral pictures was observed among control and PD patients. However, the authors suggested that mutilation pictures may h ave been the only category of aversive pictures sufficiently arousing to detect a deficit in emotional reactivity in PD patients.

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85 Indeed, further analysis indicated that control subjects displayed greater eye blink magnitude for highly arousing negative pi ctures relative to the low arousing negative pictures, whereas the PD patients did not exhibit changes in startle eye blink magnitude a s a function of arousal level. The authors concluded that blunted physiological response to highly arousing aversive stim uli is likely caused by the inability of individuals with PD to translate an aversive motivational state into a physiological response. Startle circuitry involves projections of the amygdala to structures in the brain stem. The prefrontal cortex typically exerts inhibitory control over the amygdala (Rosenkranz & Grace, 2002) until stress induced DA release in the basolateral amygdala suppresses this inhibition (Marowsky, Yanagawa, Obata, & Vogt, 2005) These findings prompted Bowers, Miller, and colleagues (2006, 2009) to postulate that dopamine depletion, evidenced in PD, would reduce the disinhibition of the amygdala in response to stres sful stimuli, thereby inhibiting startle reactivity. While research has examined the impact of emotion on involuntary movement in PD, whether emotion impacts voluntary movement in PD patients the same way as health y controls remains unexplored. The curre voluntary motor reactivity to affective stimuli, as indexed by the initiation of gait. Summary Two limbic circuits involving the basal ganglia regulate emotional processes. PD is characterized by dopaminergic and noradr energic denervation of limbic basal ganglia pathways, as well as patholo gical changes in the amygdala. Dysfunction in these circuits likely underlies emotional symptoms in PD, such as high rates of apathy and depression, impaired recognition of emotion fro m prosodic cues and facial expressions, and reduced physiological re activity to emotional stimuli. Despite the recognition that

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86 motor behavior an important component of the affective experience, it is surprising that researchers have largely ignored the im plications of impaired emotional functi oning on motor behavior in PD. The impact of emotion on movement will now be discussed in detail. Emotion and Movement A growing body of literature supports the long held notion that human emotion and motor actions ar e largely intertwined and reciprocally interrelated (Niedenthal, 2007) Affective theorists traditionally agree that emotions prime or facilitate action (Frijda, 2009; Frijda, Kuipers, & ter Schure, 1989; Lang, 1995) moti vating behavioral responses to approach pleasant and avoid unpl easant stimuli and situations. The motivational direction hypothesis is founded on the principle that unpleasant emotions activate defensive circuitry and prime avoidance behaviors (although anger is one exception: Harmon Jones & Allen, 1998; Harmon Jones, Harmon Jones, Abramson, & Peterson, 2009) whereas pleasant emotions activate appetitive circuits that prime a pproach behaviors (Cacioppo, Priester, & Berntson, 1993; Centerbar & Clore, 2006; Chen & Bargh, 1999; Duckworth, Bargh, Garcia, & Chaiken, 2002) In the early 1990s, researchers began to explore the in fluence of emotion on approach an d avoidance related movements. Such evidence has typically been acquired using protocols that manipulate emotional states prior to or during the execution of arm movements which are made toward or away from the body. Infer ences have been drawn from these data regarding the interdependence of emotion and approach/ avoidant behavior based on several different theoretical approaches, including muscle activation, distance regulation, evaluative co ding, and embodiment accounts. These theories will first be reviewed in detail, as they potentially have important implications concerning the impact

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87 of emotional state on any directional movement, including gait initiation toward or a way from an affective stimulus. A n overview of the e vidence for emotional modulated movement which is not focused on direction specific movements will follow. S uch movements include i nvoluntary postural adjustments, pinch grip tasks, and motor cortex excitability. Finally, the possible neural circuitry resp onsible for integrating emotional and motor systems will be discussed. Emotion Modulated Movement Approach and Avoidance M ovements Muscle activation accounts assume that specific motor responses manifest as approach and avoidant behaviors. U npleasant em otional cues have routinely been found to facilitate arm extension movements, while pleasant emotional cues facilitate arm flexion. This link is typically explained by a form of higher order Pavlovian conditioning, in which long term associations are forme d between arm flexion and approaching an object (i.e., the consumption of desired goods) Additionally, an association is formed between arm extension and avoiding an aversive object (Cacioppo, Priester, & Berntson, 1993; Neumann & Strack, 2000) Several studies have provided a direct link between evaluation of an affective object and approach and avoidance behavior, as defined by flexion and extension arm movements respect ively (Cacioppo et al., 1993; Chen & J.A. Bargh, 1999; Duckworth et al., 2002; Forster & Strack, 1996; Neumann & Strack, 2000) For example, Chen and Bargh (1999) examined whe ther automatic affective evaluation primed activation of approach and avoidance muscular tendencies. One group of participants was instructed to push a lever away from them (extension movement) in response to negatively evaluated stimulus words and to pull the lever towards them (flexion movement) in response to positi vely evaluated stimulus words. Another group of participants was gi ven the

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88 opposite instructions. As hypothesized, the intentional evaluation of a stimulus as positive facilitated flexion (pul l) relative to extension (push) movements, and the negative evaluation of a stimulus speeded extension relative to flexion arm movements. A second experiment removed the task instructions of evaluating the stimulus words. Thus, participants were required t o push or pull the lever in response to stimulus presentation, irrespective of affective meaning. The results replicated experiment 1, suggesting that affective processing automatically and unconsciously motivates approach and avoidance response tendencies Duckworth et al., (Experiment 3; 2002) behavioral tendency is non conscious. Similar to experiment 2 of Chen and Bargh, pushing or pulling a lever in response to the mere presence of novel, affectively valenced stimuli generated muscular predispositions to approach positive stimuli (flexion) and avoid negative stimuli (extension). Evidence suggests that the relationship b etween muscular tendencies and affect is bidirectional. Cacioppo, Priester, & Berntson (1993) showed that bodily positions influence ev aluation of affective stimuli. Specifica lly, participants gave a more positive evaluation of presented stimuli when their arm was simultaneously flexed rather than extended. Additionally, Forster and Strack (1996) demonstrated that p erforming arm flexion enhanced the recall of positively compared to negatively evaluated information, whereas performing arm extension tended to enhance the recall of negatively evaluated information relative to positive and neutral. Rotteveel and Phaf (2004) further inve stigated whether affective stimuli automatically and unconsciously prime corresponding action tendencies. In contrast to

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89 previous studies, button presses rather than lever movements were used to ind uce arm flexion and extension. Participants were instructe d to push a lower (extension) or upper (flexion) button on a vertical stand in response to the emotional valence of angry or joyful facial expressions. Similar to Chen and Bargh, the affect congruent conditions (joy faces arm flexion and angry faces ar m extension) generated shorter latencies than the affect incongruent conditions (joy faces arm extension and angry faces arm affective features (e.g. gender) of valenced faces failed to reveal an influence of affect on the corresponding action tendencie s. Thus, the authors concluded that the link between affect and arm flexion and extension may depend on the intentional goal of evaluating the affective properties of a stim ulus. Importantly, later studies have yielded inconsistent results regarding the classification of arm flexion and extension as representing approach and avoidance movements, respectively (Lavender & Hommel, 2007; Markman & Brendl, 2005; Neumann & Strack, 2000; Wentura, Rothermund, & Bak, 2000) Neumann and Strack (Experiment 2; 2000) sought to determine whether approach and avoidance behavior could be conceptualized as behavior that regulates the distance toward important objects. Thus, the reduction of spa tial distance toward an object would be considered approach, while increasing spatial distance from an object woul d be interpreted as avoidance. To test this distance regulation hypothesis, the authors induced the visual illusion that participants were eit her moving toward or away from the computer screen while they were evaluating the valence of positive and negative adjectives. As predicted, participants were faster to categorize positive adjectives when they had the

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90 impression of moving toward the screen and faster to categorize negative adjectives when they had the impression of moving away from the screen. Replicating these results in the absence of the goal of affective evaluation (Experiment 3), the authors concluded that 1) affective information is p erceived automatically from a stimulus without conscious evaluation, and 2) approach and avoidance behavior can have many manifestations. Similarly, Markman and Brendl (2005) demonstrated distance regulating effects in approach and avoidance behavior while also revealing that body movements are ma de relative to representation of the self in space rather than physical location. The authors constructed a variant of the Chen and Bargh task in fro m the representation of their body in space. Positive and negative words were presented either further away or nearer to the name of the participant that was placed in the center of a corridor receding in depth on a computer screen. In half of the trials, participants were instructed to move the words ( with a joystick ) toward their name if the word was positive and away from their name if the word was negative. In the other half of the trials, participants were instructed to do the opposite. Participants we re faster to move positive words toward their name on the screen than away from their name, with the opposite pattern of results found for movements in response to negative words. Importantly, this pattern of results was found regardless of whether the res ponse required an extension (e.g., pushing a positive word toward representation of self on screen) or flexion (e.g., pulling a negative word away from the representation of self) arm movement.

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91 Research has also shown that the manifestation of approach a nd avoidance behavior is mediated by the intentions and goals of the acting indi vidual. Lavender and Hommel (2007) systematically pitted the influence of arm flexion/extension response tendencies against cognitively based, goal dependent response tendencies. Similar to Markman and Brendl (2005) the authors argued that the goals of the action, rather than the specific muscle activations, modulate the compatibility between affective stimuli and behavioral tendencies. In this study, participants were instructed to move a doll toward (approa ch) or away (avoidance) from a computer screen as quickly as possible in response to the presentation of affective pictures. Pictures were either unpleasantly or pleasantly valenced and slightly rotated either to the left or right. Half of the participants were instructed to evaluate the affective valence of the picture, while the other half evaluated the spatial orientation of the picture. Additionally, half of the affective instruction group was instructed to make avoidance movements in response to negati ve pictures and approach movements in response to pleasant pictures. The other half received reversed instructions. Participants receiving spatial instructions were asked to make an avoidance movement in response to left oriented pictures, and an approach movement in response to right oriented pictures. Again, the other half of participants received reversed instructions. Thus, based on the goals of the action, the authors hypothesized that pleasant stimuli should facilitate movement toward the screen (requ iring arm extension), whereas unpleasant stimuli should facilitate movement away from the s creen (requiring arm flexion). Alternatively, if muscle activation patterns play a stronger role than cognitive interpretations of movements, then the opposite patte rn of results should be found. The results confirmed the former hypothesis: pleasant stimuli

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92 facilitated arm extension (approach goal ) and unpleasant stimuli facilitated arm flexion ( avoidance goal ). Thus, the arm movements provided ambiguous behavioral me asures, rather than default measures of approach and avoidance as postulated by muscle activation accounts. Furthermore, supporting Rotteveel and Phaf (2004), participants receiving the spatial focused instructions failed to demonstrate any affective stimu lus response relation. Lavender and Hommel concluded that the cognitive representation of actions, as well as the presence of an affective evaluation goal, determines whether a given muscle movement is coded as approach or avoidance. Eder and Rothermund (2008) proposed an evaluative response coding view of approach and avoidance reactions in an attempt to resolve the inconsistencies concerning which specific motor responses manifest a s ap proach and avoidance behavior. This approach is based on three primary assumptions, which explain how identical motor reactions can be positively coded in one context and negatively coded in another. First valuative coding approach assumes that the evaluative implications of action instructions and goals assign affective codes to motor response s on a representational level. Thus, the representation of approach behavior should be linked to a positive response code, while the representation of avoidance behavior should be linked to a negative response code. Secondly motor action codes consist of a network of distributed feature codes, specifying properties of the action on several dimensions (e.g., evaluative dimension). Therefore, the affective value of motor representations is flexibly set based on current goals and relev ant situational constraints. Third response labels (e.g., toward v. away) used in task instructions and relevant semantic action knowledge may directly

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93 determine the codes controlling instrumental behavior. For example, labeling the pull of a lever as an away or downwards movement should assign a negative code to the movement, where as labeling the identical movement as towards oneself or up wards would assign a positive code to the lever pull. Eder and Rothermund conducted a series of experiments testing the evaluative response coding approach against the muscle activation and distance regulation approaches. In the first experiment, response labels of towards away and up down were given to lever push and pull movements. A preliminary study indicated that the word up was judged more positively than down and toward more positively than away Participants used the push/pull movements of the leve r to classify the valence o f positive and negative words. One group of participants was instructed to pull the lever toward them or downward in response to positive words and to push the lever away from them or upward in response to negative words. The oth er group of participants rece ived the reverse instructions. The toward away labels replicated the standard positive pull/negative push effect found in studies supporting the muscle activation account. However, the upward/downward labels produced the revers ed effect. The downward label elicited a slower pull movement (flexion) in evaluation of positive stimuli, while the upward label elicited a slower push movement (extension) in e valuation of negative stimuli. The results supported the notion that flexion a nd extension arm movements are not sufficient to explain valence modulations of lever movements (Lavender & Hommell, 2007; Markman & Brendl, 200 5) Experiment 2 tested the predictions of the distance regulation hypothesis against the evaluative coding explanation. Using an experimental set up similar to Lavender and Hommel,

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94 participants were instructed to move the lever towards or away from the e valuated st imulus on the computer screen. As in experiment 1, another group of participants was instructed to move the lever downwards (push) and upwards (pull) in respo nse to the evaluated stimulus. Supporting distance regulation accounts (e.g., Neuman & Strack, 2000), instructions to move toward the evaluated stimulus (extension) speeded evaluations of positive words, while instructions to move away (flexion) from the evaluated stimulus speeded evaluation of negative words. The reverse effect was once aga in found for the upward/downward instructions. Taken together, experiments 1 and 2 indicated that the positive and negative evaluative connotations of the response labels (toward/up positive, away/down negative) modulated the facilitation of arm push and p ull lever movements. Experiment 3 extended the findings to left and right lever movements; movements that by themselves were unrelated to approach/avo idance or distance regulation. For example, labeling of left and right lever movements with positive conno tations ( upwards or towards) facilitated movements in positive evaluations. Overall, these experiments support the evaluative response coding view of approach and avoidant reactions, suggesting that the valence of movements toward and away from a reference point is reliant upon the evaluative connotation of the response labels used to guide these behaviors. The evaluative coding view can thereby accommodate a diverse set of empirical findings that were originally interpreted through more specialized theoret ical accounts of approach and avoidance behavior (e.g., muscle ac tivation, distance regulation). Importantly, Eder and Rothermund suggested, however, that specialized accounts should not be completely dismissed because they

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95 likely shed light on the reasons why behaviors are coded in a certain way in a specific situation. Recently embodiment views of emotion have provided another promising explanation for the relationship between bodily states of emotion (e.g., arm flexion/extension, facial expressions, pos ture) and the processing of emotional information (Niedenthal, 2007; Niedenthal et al., 2005; Niede nthal, Mondillon, Winkielman, & Vermeulen 2009) As previously discussed, embodiment accounts postulate that the processing of emotional information involves the ability of the sensory motor systems to partially reenact aspects of the original states that occurred when the emotion was experienced. According to this view point, conceptual representations (i.e., emotional meaning) of approach and avoidance behavior are originally encoded from concr ete sensory motor experiences. As such, emotion concepts can be represented by simulations of approach and av oidance behavior. Several studies supporting the embodiment view have shown that performing actions with a particular valence (e.g., smiling v. frowning) results in compatibility effects in subsequent evaluat ions (Niedenthal et al., 2009; Oberman, Winkielman, & Ramachandran, 2007; Strack, Martin, & Stepper, 1988) For example, Strack, Martin & Stepper (1988) required participants to ho ld a pencil with their front teeth or between their lips while evaluating the funniness of different cartoons. Holding the pencil with their teeth facilitated a smile, while holding the pencil between their lips inhibited a smiles were inhibited. In a similar study, participants who were prevented from engaging expression relevant facial muscles (i.e., biting a pen) exhibited impaired recognition of

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96 happy facial expressions (Oberman et al., 2007) Thus, recognition performance was maximized when the perceived emotion was congruent with t state. This same concept has been used to explain how approach (i.e., moving the lever toward a reference point) and avoidant lever movements (moving the lever away from a reference point) are facilitated by positive and negative vale nced conditions, respectively. For example, the embodiment view postulates that the processing of positively valenced emotional information is at least partially grounded in the motor states involved in approach responses, such as pulling a lever toward the body or pushing a lever toward pleasant stimuli. Similar to the evaluative coding explanation of affective mapping effects, e mbodiment theories of emotion stress the importance of contextualized, situated representations of approach and avoidant behavior allowing for some flexibility in the link between valence and specific body movements. As briefly alluded to in the Emotion se ction, another controversial issue in the emotion and movement literature involves the congruence of unpleasant stimuli with withdrawal motivation. Research has revealed that not all aversive stimuli facilitate avoidance related behavior. For example, fear expressions, rated as appearing highly submissive and as equally affiliative as happy expressions (Hess, Blairy, & Kleck, 2000) have been shown to predominantly elicit approach related responding (Marsh, Ambady, & Kleck, 2005) Specifically, Marsh et al. instructed participants to push or pull a lever in response to anger and fearful facial expressions. As expected, participants exhibited faster pushing (avoidance) relative to pulling lever (approach) movements in response to ang ry faces. However, fearful faces, although also unpleasant in valence, elicited faster approach related pulling movements. Fearful faces may elicit caregiving or

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97 empathy from observers and consequently represent an affiliative stimulus. Collectively, the a uthors interpreted the behavioral responses as emotion specific rather than reflecting broad valence dimensions. In contrast to the Marsh study, several lines of research have shown that anger, although negative in valence, elicits approach motivational te ndencies (See Carver & Harmon Jones, 2009 for a review) For example, research has shown that anger is associated 1) with att ack, an approach behavior (Berkowitz, 1993) a nd 2) with relative left prefrontal activation (associated with approach motivation) (Harmon Jones & Allen, 1998) Furthermore, trait anger has been linked to greater assertiveness and competitiveness, traits associated with approach related motivation (Buss & Perry, 1992) Thus, extant research suggests that fearful facial expressions and anger appear to defy this relationship of valence and motivational direction. Also seeking to understand the relation between affective valence, motivational direction, and behavior, Coombes and colleagues (2007) examined the peripheral and central components of a wrist extension m ovement during exposure to affective stimuli representing specific unpleasant affective categori es (i.e., attack, mutilation). Participants demonstrated speeded premotor reaction times (reflecting central processes) for extension movements initiated during exposure to attack pictures relative to all other categories (mutilation, erotic couples, opposite sex nudes, neutral huma ns, household objects, blank). While the authors concluded that unpleasant states do not unitarily prime withdrawal movements, this i nterpretation of the results n eeds to be taken with caution. As discussed above, recent conceptual efforts have shown that movements should not be classified into approach/withdrawal related behavior based

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98 solely on muscle activation patterns, such as exte nsion and flexion. Importantly, the authors also noted that an accelerated motor response to threatening stimuli offers organisms an advantage in dangerous environments supporting the notion that the emotion system has evolved to prime organisms to react to stimuli in a way that promotes survival (hman, Hamm, & Hugdahl, 2000; hman, & Soares, 1998) Thus, as an alternative interpretation of the results, exposure to extremely threatening stimuli compared to other valenced stimuli may speed the initiation of movement (regardless of movement direction), motivated by one of the most primitive and fundamental goals of survival. This notion is f urther supported by research showing that exposure to attack pictures compared to erotic, mutilation, and neutral pictures speeds reaction times on a non directional goal directed ballistic pinch grip task (Coombes et al., 2009) Taken together, t he Coombes et al. studies and others demonstrate that the categorization of affective stimuli into broad valenced, rather than emotion specific categories is likely not sufficient for a comprehensive understanding of emotion modulated movement. While con temporary affective scientists have admirably attempted to understand the interaction of motivational priming and the direction of intended movement, these conceptual efforts have been limited by their focus on such a small range of movements (e.g., facial expressions and arm move ments). Until recently, the influence of emotional state on voluntary whole body movements remained unexplored. Addressing this limitation, Gamble et al. ( in review ) investigated the influence of emotional sta te on forward gait initiation. Requiring participants to walk toward or away from the presentation of an affective stimulus clearly indexes an approach or avoidant behavior, thereby removing the directional ambiguity found in previous work. Participants initiated

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99 gait in response to the offset of emotional stimuli and continued to walk toward the loca tion of the presented stimuli. The authors we re therefore able to explore the impact of unpleasant and pleasant stimuli on a purely approach related behavior. As expected, exposure to high and low arousing pleasant stimuli facilitated the COP movements a nd execution of the first step. Interestingly, however, the high arousing unpleasant pictures (attack) compared to all other conditions, speeded reaction times on the gait initiation task, despite the movement cl early being approach oriented. This result supports the notion that faster movements, regar dless of direction, are primed in threatening situations. Collectively, the authors concluded that highly arousing unpleasant conditions accelerated the initiation of a motor response, but as the direction of the movement emerged, the pleasant conditions r elative to the unpleasant ones, clearly facilitated the initiation of gait. While this study was a first step in exploring the impact of emotion on voluntary whole body movements, much work remains. For example, future research needs to investigate 1) the influence of more specific emotion categories on gait initiation, 2) how emotion impacts gait initiation, conceptualized as an avoidance behavior, and 3) how dispositional differences in emotional reactivity interact with emotional state to influence spec ific gait initiation parameters. Emotion Modulated Movement Nondirection Specific M ovements T he emotion movement database has grown considerably in the last decade with researchers beginning to investigate the influence of emotion on aspects of human mov ement not just related to approach or avoidant behavior. Collectively, this evidence also supports the notion that emotions prime or facilitate action. Hajcak et al. (2007) used transcranial magnetic stimulation to directly investigate the i nfluence of passively viewing emotional stimuli on motor cortex excitabilit y. The

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100 magnitude of muscle evoked potentials (MEPs) elicited in the abductor pollicus brevis muscle was measured while participants viewed pleasant, unpleasant, and neutral pictures The TMS induced MEP was greater while participants viewed the highly arousing pleasant and unpleasant pic tures relative to the neutral. Thus, the intensity of emotional states, regardless of valence, increa sed motor cortex excitability. B ehavioral eviden ce also supports the notion that emotional arousal, rather than valence, modulates non directional movements. For example, Coombes et al. (2008) recently studied the impact of picture induced affect o n a precision pinch grip task. Pa rticipants sustained a pinch grip force at 10% of maximum voluntary contraction wh ile receiving online feedback. After a short interval f eedback was replaced with either a pleasant, unplea sant, or neutral IAPS picture. Following removal of feedback, force product ion decayed in all conditions. However, exposure to the more arousing pleasant and unpleasant images similarly reduced the magnitude of decay relative to the less arousing neutral images. Gamble et al. ( in review ) later replicated and extended thes e results at the 2% and 35% target force levels, while additionally finding that self report judgments of valence and arousal predicted force output on the pinch grip task. Interestingly, at the 35% target force level the relationship between affective st ate and force control varied according to individual differences in depression. This effect of depression on force control was only evident shortly following picture presentation and disappeared as time progressed. Coombes et al. (2009) also demonstrated the importance of considering the influence of the trait component of th e affective experience on motor behavior Specifically, participants high and low in trait anxiety executed a ballistic goal directed

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101 pinch grip task at 10% or 35% of MVC at the offset of e motional and neutral pictures. The high trait anxiety group compare d to low trait anxiety group exhibited slower reaction times on the pinch grip task at 10% of MVC, regardle ss of the affective condition. No differences were found for the pinch grip at 35% of MVC. Taken together, the our prior work has demonstrated that t he characteristics of the task (e.g., target force level), the nature of the emotion eliciting stimuli, as well as individual differences in affective reactivity all appear to modulate force and speed related parameters of a subsequent movement. While th e upper extremity remains a favored target area for research examining emotion modulated movement, emotion evoked postural adjustments during quiet st anding have also been studied. For example, Hillman, Rosengren, & Smith (2004) required participants to view pleasant, unpleasant, and neutral pictures while quietly standing on a force plate. The results revealed that females exhibited increased center of pressure (COP) movement in the posterior direction (i.e., away from pictures ) when viewing unpleasant pictures, whereas males demonstrated modest posterior postur al sway under such conditions. The authors suggested that the increased posterior movement was motivated by behavioral withdrawal from the unpleasant stimuli, and may ref lect early preparation for the initiation of Contrary to expectations, neither males nor females demonstrated a COP shift toward pleasant pictures. Conflicting findings were reported by Azevedo and colleagues (2005) however, who revealed that passive viewing of mutilation pictures reduced overall body sway in the medial lateral direction (i.e., standard d eviation of COP trajectory) in male

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102 however, Azevedo et al. postulated that reduced sway also reflected the activation of a Methodological differences regarding the gender of participants, size of pictures, and outcome measures may have accounted for the contrasting withdrawal responses to unpleasant pictures in these two studies (i.e., increased freezing vs. incre ased posterior movement). of the COP in the anterior posterior direction, while Azevedo focused on the standard deviation of the COP displ acement and the mean position. Hillman also presented pictures much greater in size than Azevedo, which cou ld have led to larger effects. Finally, Hillman found the greatest modulation of postural responses to unpleasant stimuli in females, while Azevedo on ly assessed male participants. Nonetheless, these two studies demonstrated that unpleasant emotions are associated with specific postural adjustments. In sum, variation in emotional state has been putatively associated wi th modulation of motor action. TMS evidence indicates that increases in emotional arous al (intensity) lead to greater primary motor cortex excitability when actively and passi vely viewing emotional images. Behavioral evidence demonstrates that emotion significantly influences basic central and peripheral parameters underlying single joint pa rame ters and whole body movements. Collectively, the data suggest that motor system is not segregated from affective processes; indeed such processes are largel y desegregated and integrated. The potential mechanisms underlying the integration of emotion in to motor processes are discussed next.

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103 The Integration of Emotion and Motor P rocesses Based on animal research, Haber and colleagues (2003, 2009) have proposed three mechanisms through which information can be channeled from limbic to motor circuits. First, the axons and dendrites within each structure of the basal ganglia often cross functional domains, allowing distal de ndrites from one functional region to invade adjacent functional regions. Thus, activation of basal ganglia regions of the emotion circuit (i.e.,ventral GP, ventral striatum) may also activate basal ganglia regions associated with the motor circuit ( i.e., GPi, dorsal striatum). Secondly, the basal ganglia pathways consist of two neural networks, composed of complex non reciprocal connections, which allow a continuous feedforward mechanism of information flow from limbic circuits to motor circuits (Haber, Fudge, & McFarland, 2000; Joel & Weiner, 1997; M cFarland & Haber, 2000) These two pathways, thalamo cortico thalamic and striato nigro strial, are reviewed in further detail. The thalamo cortico thalamic pathway As previously mentioned, the basal ganglia form several segregated, functionally orga nized pathways with the frontal cortex, in which functionally defined regions of the frontal cortex terminate topographically in the basal ganglia structures, which in turn project back to the cortex via the thalamus (Middleton & Strick, 2000) The functional regions of the frontal cortex are orga nized in a hierarchical manner and include the orbital and medial prefrontal cortex (OMPFC emotion and motivation), dorsolateral prefrontal cortex (DLPFC higher cognitive processes), and premotor and motor areas ( motor planning and execution). Addition ally, regions within each basal ganglia nuclei are associated with specific basal ganglia cortical pathways (ventral emotion; central cognition; dorsolateral motor), with the pathway involving the motor cortex

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104 considered the final step to action (Fuster, 2001) Studies on primates and rodents now provide evidence that information from these parallel segregated basal gan glia cortical circuits indeed influence each other (Haber & Calzavara, 2009) Specifically, thalamo cortico thalamic projections are in an ideal position to integrate information across functional basal ganglia cortical loops. I n theses loops, the thalamus relays information from the basal ganglia to the cortex. McFarland & Haber (2002) revealed that the thalamic pathway back to the cortex has one component reinforcing each basal ganglia cortical circuit, and another component which relays information between circuits via nonreciprocal corticothalamic pathways and through the organization of thalamic projections to different cortical layers. As demonstrated in Figure 2 17, the thalamus projects to the superficial (layers I/II), middle (layers III/IV), and deep (layers V) cortical layers (McFarland & Haber, 2002) The thalamic projections to layer V continue the processing of informati on in each specific basal ganglia cortico system via corticothala mic and corticostriatal loops. Furthermore, terminals in layer V interface with other circuit systems through a nonreciprocal projection to a thalamic region part of another cortical circuit system. Thalamic projections to layer I/II interface with corticocortical connections from layer III, also influencing adjacent basal ganglia cortico circuits. Haber proposed a schema illustrating how cognitive and affective information can be integrate d across functional basal ganglia cortical circuits via thalamic relay nuclei linking functionally adjacent frontal cortical areas (Figure 2 18). A feedforward pathway, beginning with the nonreciprocal projection from the sensory/limbic frontal regions to the MD thalamus likely channels affective information from limbic cortices to higher

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105 association cortical areas (Jones, 1998) The central MD thalamic nuclei have reciprocal connections with the DLPFC, forming part of the associati ve basal ganglia cortico loop. The VA receives input from the DLPFC, while also having reciprocal connections with the caudal motor and rostral motor areas involved in the cognitive aspects of motor action (e.g., planning). Thus, the VA thalamic nuclei relay information from the DLPFC t o the caudal and rostral motor areas. Finally, the rostral motor cortices feedforward information to the VLo thalamic nuclei, which reciprocally connect to the primary and secondary motor cortices. In sum, information can be relayed from the limbic system to the motor system through these nonreciprocal corticothalamic feedforward pathways, shaping final motor output. The striato nigro striatal (SNS) pathway Research on rodents provided the first evidence that the limbic pathway could influence motor outp ut via the SNS pathway, in which the ventral striatum modulates the dorsal striatum through midbrain dopamine neurons (Nauta, Smith, Faull, & Domesick, 1978; Somogyi, Bolam, Totterdell, & Smith, 1981) As demonstrated in Figure 18, a functional gradient from limbic (red) to associative (green) to motor (blue) domains is imposed on both the cortical projections to the striatum and on the three components of each striatal region (VMS ventral medial striatum; CS central striatum; DLS dorsolateral striat um). The VMS consists of shell and core subdivisions (Kunishio & Haber, 1994; Lynd Balta & Haber, 1994) The m edial prefrontal cortex, receiving dense innervations from the orbital prefrontal cortex, amygdala, and hypothalamus, terminates on the shell of the VMS (Freedman, Insel, & Smith, 2000; Fudge et al., 2002; Kunishio & Haber, 1 994) Additionally, the VMS receives direct projections from the amygdala and hippocampus (Fudge et al., 2002) The DLPFC projects to the rostral striatum,

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106 mediating working memory and planning processes (Goldman Rakic, 1996; Haber, 2003) whereas projections from the motor cortex t erminate in the DLS (McFa rland & Haber, 2000) Interactions between the functional regions of the striatum occur through spiraling a scending midbrain connections. Midbrain DA cells terminate on the striatum while also receiving projections from the striatum. These DA midbrain c ells are divided into a dorsal tier and a ventral tier (Francois, Yelnik, Percheron, & Fenelon, 1994; Haber et al., 1995) The dorsal tier includes cells from the VTA and SNc, while the ventral t ier includes cells of the SNr. Forming an inverse dorsal ventral topographic organization, cells of the dorsal tier project to the VS and CS, while cells of the ventral tier project to the DLS (Francois, Yelnik, Tande et al., 1999; Haber, Fudge, & McFarland, 2000; Haber et al., 1994) Additionally, the ventral med ial striatum projects to the VTA and the medial SNc, as well as the medial pars reticulata. The CS projects more ventrally and in the pars reticulata region, while the DLS projects to the ventral regio ns of the midbrain in the SNr. Importantly, the ascendi ng and descending striatum midbrain dopamine connections in each functional area differs in their proportional projections. For instance, the ventral striatum projects to a large midbrain region, influenci ng a wide range of DA neurons. However, the VS rec eives input from o nly a limited midbrain region. Conversely, the DLS receives a large DA midbrain input, while projecting to only a limited midbrain region. Each striatal region consists of three components as illustrated in Figure 2 19: 1) midbrain cell s dorsal to its reciprocal terminal field (first oval non reciprocal component), 2) midbrain cells lying within its reciprocal terminal field (second oval

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107 reciprocal component), and 3) ventral region of midbrain cells composed of nonreciprocal terminal s (third oval nonreciprocal component). Importantly, this third component overlaps with cells of the subsequent dorsal SNS system. Taken together, each striatal region consists of one reciprocal connection and two non reciprocal connections with the mid brain. The nonreciprocal connections create on overlapping system in the midbrain, resulting in feedforward spiraling projections from ventral to dorsal striatal regions. Through a series of spiraling connections, as demonstrated in Figure 2 20, informati on from the limbic system can reach the motor system. The shell of the VS sends information primarily from the amygdala and hippocampus to the midbrain, terminating in the VTA and SNc of the dorsal tier (red arr ows). The VTA projects back to the shell, for min g a closed SNS reciprocal loop. However, the shell region also projects to an area of the medial SN (i.e., lateral and dorsal to the dorsal tier) which feeds forward information to the core (orange and yell ow arrows). Thus, this spiraling connection wit h the midbrain allows information from the shell to influence the core The core, also receiving input from the OMPFC, has a reciprocal connection with the medial SN and projects ventral of its reciprocal component to the densocellular region of the dorsal tier. The CS interfaces with the core, via a reciprocal loop with the densocellular region (green arrows). Thus, information is transferred from the core to the CS The CS also has a non reciprocal projection to the ventral SNr and the cell columns, which are reciprocally connected to the DLS (blue). Thus, the transfer of information continues from the CS to the DLS and final motor outcome Taken together, a series of ascending

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108 spiraling connections through the different functional regions of the striatum and midbrain allow the ventral striatum to influence the dorsal striatum of the motor system. 2007 for a review) indicates that circuitry involving the striatum, and more spec ifically the NAcc, as well as the VTA, amygdala, and frontal cortex may be particularly important in regulating behavioral activation (i.e., the energizing effects of behavior produced by motivational conditions). A primary method for studying behavioral a ctivation is to measure locomotor activity in rats following psychomotor stimulants. NAcc depletions (Kelly, Seviour, & Iversen, 1975) and intra NAcc injections of haloperidol have been shown to suppress rat locomotion, while injections of stimulants into the NAcc have been shown to increase locomotor activity (Delfs, Schreiber, & Kelley, 1990) Additionally, Baldo et al. (2002) found that D1 and D2 antagonists injected into either the shell or core of the NAcc suppressed locomotor activity. These studies are consistent with the notion that the NAcc may act as an interface between limbic areas involved in emotion and the components of the motor system controlling behavioral output (Mogensen, Jones, & Yim, 1980; Salamone et al., 2007) In sum, research on primates has provided substantial evidence that parallel emotion and motor circuits interact vi a striato nigral striatal and thalamo cortico thalamic networks, channeling information from limbic t o cognitive to motor circuits. Hypotheses derived from these integrated models have yet to be tested in humans. Thus, how emotion and motor systems intera ct in the human brain remains largely unspecified.

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109 Emotion, Movement, and PD Parallel emotion and motor circuits ensure that execution of specific behavio rs are maintained and focused. Importantly, integration of these parallel circuits is necessary to ad apt and modify motor behavior based on the affective state of the individual. Thus, parallel and integrative emotion and motor circuits must work together to coordinate behavior. As applied to bipedal locomotive behavior, emotional information from limbic basal ganglia circuits could potentially influence the initiation of gait through both the basal ganglia thalamocortical system and the basal ganglia brainstem system. As demonstrated in Figure 2 21 thalamic cortico thalamic pathways integrate limbic and motor basal ganglia thalamocortical circuits, allowing emotional input to impact the volitional aspects of locomotion, including gait initiation. Additionally, limbic input could be integrated into the motor region of the striatum via midbrain dopaminerg ic neurons of the SNS pathway. Through this mechanism, limbic input could influence the basal ganglia thalamocortical system and the basal ganglia br ainstem system. As such, emotional signals from limbic structures may be involved in the control of voluntary gait. Indeed, emotional signals may motivate locomotor behavior to approach appetitive stimuli or wit hdrawal from aversive stimuli. Furthermore, aversive individu al must ap proach a threatening stimulus. Alternatively, aversive states activating ward a threatening stimulus. Critically, individuals with Parkinson disease exhibit atypical activation within m otor and limbic basal ganglia circuits, causing mo tor and emotional dysfunction. Thus, by an impaired link between emotion and motor circuits. As demonstrated in Figure 2

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110 22 a loss of dopaminergic neurons in the SN should decrease the transfer of information from affective striatal regions to the more dorsal motor striatal regions. Additionally, inhibition of thalamic cortical projections via increased GABAergic output f rom the basal ganglia will likely impair the integration of parallel cortico basal ganglia circuits. Importantly and as discussed in the introduction, standard pharmacological treatments (e.g. levodopa, DA agonists) normalize dopamine levels in individuals with Parkinson disease, alleviating symptoms at all stages of the disease. Thus, the integration of limbic and motor systems via midbrain dopaminergic neurons may be l imited by their failure to adequately treat postural instability and gait dysfunction, manipulating emotional circuits may be a promising strategy to improve gait initiation and execution in persons with PD. Future Research Future research should be direct ed to delineating the degree to which the emotional and motor systems of individuals with PD interact to influence the quality of gait initiation and execution, as well as determine the genetic, biological, neurological, and psychological mechanisms underl ying such findings. Furthermore, future work should determine whether pharmacological or surgical interventions influence gait parameters executed under different a ffective states. These findings would not only lead to a greater understanding of the mechan isms that underpin emotion modulated movement, but may also have important practical implications. Indeed, we ( Gamble et al., in review ) recently demonstrated that pleasant emotional states facilitate forward gait init iation in healthy individuals. Specifi cally, exposure to pleasant stimuli improved the quality of the anticipatory postural adjustments during gait initiation and increased

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111 the velocity of the first step. Given that persons with PD exhibit inefficient preparatory postural adjustments and reduce d step velocities, manipulation of emotion circuitry standard anti Parkinsonian medi cation. Similar research efforts are necessary to establish whether manipulating em otional state is an efficacious strategy to improve gait initiation in persons with Parkinson disease. If research documents that the presentation of standardized and empirically established pleasant emotional stimuli facilitate gait initiation in PD, fut ure trials could investigate emotion manipulations of different modalities (i.e., emotionally evocative sounds, imagery based techniques, virtual reality applications). For example, research has recently revealed that common neural representations exist fo r perceiving emotion in another, feeling an emotion, and imaging an emotion (Jabbi, Bastiaansen, & Keysers, 2008). As such, mental imagery may be a particularly effective route to modify em otion in the clinical setting. Futhermore, future research could in vestigate how physical therapy sessions/ clinical setting can be tailored to induce positive emotional states during gait training to maximize improvements in gait. Additionally, future investigations could examine the clinical utility of long term gait t raining in a consistently positive environment or with an approach oriented strategy. S ignificant implications also arise if voluntary movement in PD is not modulated by emotion in the same way as healthy individuals. This finding would suggest an impaired link between emotion and motor circuits in individuals with PD. Affect theorists traditionally agree that the evolutionary purpose of emotion is to facilitate action, motivating behavioral responses to approach pleasant and avoidant unpl easant stimuli

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112 and situations. Consequently, if emotion information is not being integrated into the motor system in patients with PD, then it is possible that dysfunctional movement in PD is being exacerbated by the failure of emotion to drive or shape final motor behavi or as in healthy individuals. In this case, researchers would need to examine the neural mechanisms underlying the defective emotion and movement link evidenced in PD. In conclusion, manipulating emotional state to alter motor function may be a promising in novative technique to help those suffering from mot or deficits, such as Parkinson disease. Wi th continued empirical effort to understand how emotion modulates movement, researchers may be able to prov ide valuable recommendations to enhance motor therapy f or locomotor dysfunction.

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113 Figure 2 1 A schematic diagram illustrating the changes occurring in the basal ganglia circuitry in Parkinson disease. In the figure on the right, thinner lines from the SNc to the striatum indicate reduced nigrostriatal dopaminergic activity in PD, which ultimately leads to increased inhibitory output of the GPi/SNr (thicker dotted lines) to the thalamus and brainstem, via direct and indirect pathways. Black lines indicate output is excitatory. Dotted lines indicate ou tput is inhibitory. Relative thickness of lines indicates the degrees of activation of the transmitter pathways. D1, D2: Dopamine receptors; GPe: external segment of globus pallidus; GPi: internal segment of globus pallidus; STN: Subthalamic nuclei; SNc substantia nigra pars compacta; SNr: substantia nigra pars reticulate; Glu: glutamate; DA: dopamine. Adapted from Sohn, Y.H. & Hallet, M. (2005). Basal ganglia, motor control and Parkinsonism. In N. Galvez Jimenez (Ed), Scientific basis for the treatment of Parkinson Disease (2 nd ed.). New York: Taylor & Francis.

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114 Figure 2 2. The response chaining hypothesis The response produced feedback from prior portions of the movement acts as a trigger for later portions. Adapted from Schmidt, R.A. & Lee, T.D. ( 1999). Motor control and learning: A behavioral emphasis Human Kinetics, Champaign, IL. Figure 2 3. Planning of human action production. Adapted from Glover, S. (2004). Separate visual representations in the planning and control of action. Behavioral and Brain Sciences, 27, 3 78.

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115 Figure 2 4. The control of human action production. Adapted from Glover, S. (2004). Separate visual representations in the planning and control of action. Behavioral and Brain Sciences, 27, 3 78. Figure 2 5. eoretical model of interacting constraints (1986). Adapted from Newell, K.M. (1986). Constraints on the development of coordination. In M. Wade & H.T. A. Whiting (Eds.), Motor development in children: Aspects of coordination and control (pp. 341 360). Do recht: Martinus Nijhoff.

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116 Figure 2 6. Overhead view of the COP trajectory during forward GI when stepping with the right foot. The COP trace can be divided into 3 sections (S1, S2, and S3) base on the identification of two landmarks. Adapted from Hass et al. (2004). The influence of Tai Chi training on the center of pressure trajectory during gait initiation in older adults. Arch Phys Med Rehabil, 85 2172 2176 Figure 2 7. The volitional and automatic control of locomotor movements. Dotted lines ind icate output is inhibitory. Black lines indicate output is excitatory. Adapted from Takakusaki, Saitoh, Harada, & Kashiwayanagi. (2004). Role of the Basal ganglia brainstem pathways in the control of motor behaviors. Neuroscience Research 50, 137 151.

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117 Figure 2 8. Basal Ganglia thalamocortical control of gait. Dotted lines indicate that output is inhibitory. Black and grey lines indicate output is excitatory. Motor cortical neurons receiving BG output via the thalamus control the volitional aspect s of gait. SMA projections to the PMRF regulate the APAs during GI, while M1 projections to the brain stem and spinal cord regulate step execution and postural muscle tone. Adapted from Takakusaki, Saitoh, Harada, & Kashiwayanagi. (2004). Role of the Basa l ganglia brainstem pathways in the control of motor behaviors. Neuroscience Research 50, 137 151.

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118 Figure 2 9 Basal Ganglia Brain stem control of gait. Dotted lines indicate that output is inhibitory. Black lines indicate output is excitato ry. A GABAergic projection from the SNr to the MLR controls locomotion through connections with the CPGs in the spinal cord. A GABAergic projection from the SNr to the PPN controls postural muscle tone via the muscle tone inhibitory system. Adapted from Takakusaki et al. (2003). Basal ganglia efferents to the brainstem centers controlling postural muscle tone and locomotion: A new concept for understanding motor disorders in basal ganglia dysfunction. Neuroscience, 119 (2003). 293 308. Figure 2 10. C OP displacements in the anterior/ posterior and medial/ lateral directions during forward gait initiation. PD participants exhibit reduced COP displacements relative to the young, elderly. Reprinted from Halliday, Winter, Frank, Patla, & Prince. (1998). The initiation of gait in young, elderly, and Parkinson Disease subjects Gait and Posture, 8 8 14.

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119 Figure 2 11. Hypothetical model for the control of gait by the basal ganglia. A. Normal basal ganglia control of voluntary movements, locomotion, an d muscle tone. GABAergic basal ganglia projections (in black) to the thalamocortical neurons are involved in volitional control of locomotion, while those to the MLR and PPN are responsible for the automatic control processes of locomotor movements and pos tural muscle tone. B. Disturbances in the basal ganglia thalamocortical loop and basal ganglia brainstem system in PD. Reduced dopaminergic influence on the basal ganglia increases the GABAergic inhibitory outputs of the basal ganglia to the 1) thalamus reducing activation of the motor cortices and 2) the PPN and MLR in the brain stem. Reprinted from Takakusaki, K., Tomita, N., and Yano, M. (2008). Substrates for normal gait and pathophysiology of gait disturbances with respect to the basal ganglia dysfun ction. Journal of Neurology, 255 19 29.

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1 20 Figure 2 12. Schematic illustration of the embodiment of emotion. Adapted from Niedenthal, P.M. (2007). Embodying Emotion. Science, 316 1002 1005. Figure 2 13. A schematic illustration of the defensive cascade model for the electrodermal, startle, and cardiac response systems. The intensity of defensive activation corresponds to the stages of pre encounter, post encounter, and overt action, as defined by theories of animal behavior. Adapted from Bradely et al (2001). Emotion and Motivation I: Defensive and appetitive reactions in picture processing. Emotion, 1 276 298.

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121 Figure 2 14. Inputs and outputs to amygdala nuclei. Itc = intercalated cells; NE = norepinephrine; DA = dopamine; Ach = acetylcholine; 5H T=serotonin; NS = nervous system. Adapted from LeDoux, J. (2007). The amygdala. Current Biology, 17 R868 874. Figure 2 15. Basal ganglia thalamocortical limbic circuit. Dotted arrows indicate output is inhibitory. Black arrows indicate output is excitat ory. Adapted from Haegelen, Rouaud, Darnault, & Morandi. (2009). The subthalamic nucleus is a key structure of limbic basal ganglia function. Medical Hypothesis, 72, 421 426.

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122 Figure 2 16. New organization of limbic circuit. Glutamatergic excitatory proj ections are + thin black arrows; Dopaminergic excitatory projections are + thick black arrows; GABAergic inhibitory projections are dotted arrows. Adapted from Haegelen, Rouaud, Darnault, & Morandi. (2009). The subthalamic nucleus is a key structure of limbic basal ganglia function. Medical Hypothesis, 72 421 426.

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123 Figure 2 17. Summary of thalamic terminal organization in cortical layers. Projections to layer V (A) reinforce corticothalamic and corticostriatal inputs to specific cortico BG circui ts and (B) interface with other cortico BG circuits via a non reciprocal projection to a thalamic region part of another circuit system. Projections to layer I interact with dendrites of layer V, further reinforcing each parallel circuit and influence ad jacent circuits via corticocortical projections from layer III. Adapte d from McFarland & Haber, (2002). Thalamic relay nuclei of the basal ganglia form both reciprocal and nonreciprocal cortical connections, linking multiple frontal cortical areas. Journa l of Neuroscience, 22 8117 8132.

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124 Figure 2 18. Proposed schema of information flow between thalamic relay nuclei and frontal cortical areas. Thalamic areas central MD, VA, and VLo are depicted on the left and the corresponding prefrontal, premotor and motor cortical areas on the right. Black lines between cortical regions demonstrate the diverse corticocortical interconnections between adjacent frontal cortical areas. Colored gradients in boxes indicate the functional association between particular thalamic and frontal cortical areas (from most limbic, red, to motor, blue). Arrows illustrate the major thalamocortical and corticothalamic connections between areas. Information is transmitted in a feedfoward manner through strong reciprocal thalamocortical thalamic connections and prominent nonreciprocal corticothalamic inputs from more rostral, cognitive, or limbic association areas. Adapted from McFarland & Haber, (2002). Thalamic relay nuclei of the basal ganglia form both reciprocal and n onreciprocal cortical connections, linking multiple frontal cortical areas. Journal of Neuroscience, 22 8117 8132.

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125 Figure 2 19. Diagram of the 3 SNS components for each striatal region illustrating an overlapping system in the midbrain. Each str iatal region (i.e., shell, core, central, & dorsolateral) has three midbrain components, represented by three ovals. See the text for more explanation. Adapted from Haber, Fudge, & McFarland, (2000). Striatonigostriatal pathways in primates form ascendin g spiral from the shell to the dorsolateral striatum. Journal of Neuroscience, 20 2369 2382.

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126 Figure 2 20. Diagram of the organization of SNS projections. The colored gradient in rostral and caudal schematics of the striatum illustrates the organization of functional corticostriatal inputs (red = limbic, green = associative, blue = motor). See text for explanation of the spiraling projections, allowing the ventral striatum regions to influence the more dorsal striatal regions. The magnified oval region shows a hypothetical model of the synaptic interactions of SNS projections in reciprocal versus feedforward loops. The reciprocal component (red arrows) of each limb of the SNS projection terminated directly ( a ) on a DA cell, resulting in inh ibition. The nonreciprocal component (orange arrow) terminated indirectly ( b ) on a DA cell via GABAergic interneuron (brown cell), resulting in disinhibition and facilitation of DA cell burst firing. S = shell. Adapt ed from Haber, Fudge, & McFarland, (20 00). Striato nigostriatal pathways in primates form ascending spiral from the shell to the dorsolateral striatum. Journal of Neuroscience, 20 2369 2382.

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127 Figure. 2 21 A schematic diagram illustrating the integration of limbic information into the basal ganglia systems regulating locomotion in healthy individuals and potentially PD patients while on standard antiparkinsonian medication. Limbic input is integrated into 1) the basal ganglia thalamacortical loop via the thalamic coritco thalamic pathw ay & SNS pathway and 2) the basal ganglia brainstem system via the SNS pathway.

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128 Figure. 2 22 A schematic diagram illustrating 1) the changes associated with PD in the basal ganglia circuitry regulating locomotion and 2) the reduced integration of limbic input into motor basal ganglia circuits in PD. Black lines indicate output is excitatory. Dotted lines indicate output is inhibitory. Relative thickness of lines indicates the degree of activation of transmitter pathways. Red boxes and lines indic ate limbic circuitry.

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129 CHAPTER 3 METHODS Participants Participants included 26 patients with idiopathic P D and 26 age matched controls. A power analysis was conducted using data from a previous emotion and gait study in healthy individua ls (Gambl e et al., in review). This prior research has demonstrated moderate to large effect sizes for the measures of interest [lowest effect sizes (r) for comparisons of pleasant and unpleasant conditions for: reaction time = .436; COP movements = .283; velocity of first step = .350]. Thus, a total sample of 50 (25 per group) permitted identification of significant differences with power = .80 at a critical alpha level of p < .05. Patients with PD were recruited through the University of r Center and local neurology offices, and from physical and occupational therapy practices in the Gainesville, FL, community The control participants were recruited from the same community and were age and gender matched to the PD patients. All participan ts reported no lower extremity injuries that would affect movement, neurological disorders (other than PD for the Parkinson group), major psychiatric disturbances, or medications affecting balance or alertness/attention. All participants were fully informe d of the nature of the study and their right to decline participation or withdraw from parti cipation at any point of time. Written informed consent for participation was obtained according to University and Federal guidelines. Inclusion/Exclusion Criteria for Parkinson G roup. Participants had to have a clinical diagnosis of idiopathic PD (Hughes, Ben Shlomo, Daniel, & Lees, 1992; Hughes, Daniel, Kilford, & Lees, 1992). The diagnosis was based on the presence of at least two of three cardinal motor signs o f PD (i.e.,

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130 akinesia, bradykinesia, resting tremor, and rigidity), with at least one of these signs being rest ing tremor or bradykinesia. Further inclusion criteria included: 1) complaints of persistent gait disturbance despite optimal medical therapy (sco motor portion of the UPDRS), 2) a modified Hoehn and Yahr stage between 2.0 and 4.0 of 55 80 years; and 4) a stable regimen of anti Parkinsoni an and psychotropic drug therapy for 30 days prior to participation in the study. Exclusion criteria included atypical Parkinsonian features, peripheral neuropathy, vestibular dysfunction, medications affecting balance or alertness/attention, and patients on item 14 on th e motor portion of the UPDRS). The presence and severity of freezing of gait was also assessed with the New Freezing of Gait Questionnaire (NFOG Q; Nieuwboer, Rochester, Herman, Vandenberghe, Emil, Thomaes, & Giladi, 2009). A indicates the presence of FOG. The total score ranges from 0 to 24, with higher scores corresponding to more severe FOG. Exclusion Criteria for All P articipants Exclusion criteria for all participants include d 1) neurological disturbance (other than Parkinson disease for the PD group) or chronic medical illness (i.e., renal, HW, metastatic cancer, etc.); 2) history of major psychiatric disorder (i.e., schizophrenia, bipolar disorder, substance abuse); 3) perip heral neuropathy, orthopedic, vestibular, assisted devices; 4) history of head injury, epilepsy, stroke, or learning disability; 5) dementia. Dementia was screened using the Montreal Cognitive Assessment (MOCA: Nasreddine, Phil lips, Bedirian, et al., 2005) Participants with a MOCA score < 26/30 were excluded from the study. Depression symptom severity was screened with the Beck Depression Inventory II (BDI 2: Beck, Ste er, & Brown, 1996). Participants scoring

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131 above 19 on the BDI II (i.e., the cut off for mo derate/severe depre ssive symptoms) were excluded. Additionally, participants exhibiting high levels of trait anxiety as evidence by a score greater than 45 on the Trait scale of the State Trait Anxiety Inventory (STAI: Speilberger, 1983) were excluded from the study. Instrumentation Emotion Manipulation Picture viewing was used to induce emotional states during experimental trials. Presented stimuli included 30 digitized photographs selected from the International Affective Picture System (IAPS: Lang, Bradl e y, & Cuthbert, 2001) representing six affective categories: 1) erotica, 2) happy people, 3) mutilation, 4) contamination, 5) attack, and 6) neutral 1 All pictures were chosen according to affective norms (NIMH, CSEA, 2005). Threat (i.e., pointed guns, kni fe attacks), mutilation (i.e., mutilated bodies and faces), and erotica (i.e., erotic couples) stimuli are rated high in arousal and strongly activate defensive and appetitive systems (Bradley, Codispoti, Sabatinelli, & Lang, 2001; Bradley, Codispoti, Cuth bert, & Lang, 2001) respectively Erotic and threat pictures were included because they have been previously shown to alter gait parameters in healthy individuals (Gamble et al., in review). While the effect of mutilations on gait in healthy individuals h as not been evaluated, this category was included because of research showing a mutilation specific hyporeactiviy in PD (Miller et al., 2009). The happy people category (i.e., babies, children, happy couples) was 1 1. IAPS Pictures: Attack: 6210, 6250, 6260, 6370, 6510; Mutilation: 3060, 3071, 3100, 3150, 3130; Contamination: 9300, 7359, 9301, 7380, 9320; Erotica: 4607, 4670, 4694, 4608, 4676; Pleasants: 4598, 2071, 4623, 2345, 2058; Neutral: 2190, 2200, 2210, 2104, 2305.

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132 included because, similar to the more arous ing erotic category, it has been shown to facilitate gait initiation in healthy individua ls (Gamble et al., in review). The contamination category (i.e., dirty toilets, bugs on food) provides an unpleasant category which matches the arousal level of the pl easant category and induces clear avoidance motivation. The neutral pictures (i.e., neutral faces) are less arousing than all affective categories. Five blank trials were also included, in which no image (a blank black screen) was presented. Pictures wer e projected onto a 3.3 m x 2 m screen using NEC VT 670 digital projector. The screen was located 6 m in front of participants. Pictures were 127 cm x 91 cm and 1024 x 768 pixels. Stimulus presentation and order was randomized and counte rbalanced across pa rticipants. A custom LabVIEW program (LabVIEW 8.1; National Instruments, Austin, TX) was used to control trial onset, trial offset, and visu al stimulus presentation. A computerized 9 point version of the self assessment manikin (SAM: Lang, 1980) was used t o obtain subjective ratings of valence and arousal at the conclusion of gait testing. Task Participants were fitted with retro reflective markers which were placed bilaterally on the lower body at the following locations: anterior superior iliac, posterio r superior iliac, lateral epicondyle of the knee, lower lateral 1/3 surface of the thigh, lateral malleolus, tibia, second metatarsal head, and calcane us. Once the reflective markers were in place, each participant was given the opportunity to walk around the testing environment to become accustomed to the instrumentation. During the gait initiation trials participants stood with their feet in a self selected stance width, with both feet on one force platform (Bertec, Columbus, Ohio model

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133 4060). The posit ioning of the feet was recorded to allow for standard ization for all future trials. In response to picture offset, participants began walking and continued for seve ral steps (approximately 4 m). Participants walked at picture offset rather than onset to av oid possible attentional effects on performance resulting from viewing the picture and s imultaneously initiating gait. Additionally, this approach replicates previous work examining the influence of emotional state on gait initiation in healthy individuals (Gamble et al., in review). The kinematic characteristics of the locomotor tasks were sampled at a rate of 120 Hz using a ten camera Optical Motion Capture system (Vicon Peak, Oxford, UK ). The motion capture system collected three dimensional coordinate data from retro reflective markers. Ground reaction forces (GRF) and COP measurements were collected at 1200 Hz using three Bertec force platforms (Bertec, Newton, MA; size 60 x 40 cm) mounted flush with the laboratory floor. Procedure Participants with dosa ge of dopaminergic medication. Participants were also instructed to wear any eye glasses or contacts that they typically wear so that poor visual acuity would not interfere with picture viewing d uring the experimental tasks. Upon arrival to the laboratory, Review Board and all questions were answered. Participants also completed a battery of self report quest ionnaires including: demographics, the state and trait forms of the STAI (Spielberger, 1983), the state version of the Positive and Negative Affect Schedule (PANAS: Watson, Clarke, & Tellegen, 1988), the BDI 2 (Beck et al. 1996), t he Apathy

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134 Scale (Starkst ein, Mig liorelli, Manes, Teson, Petracca, Chemerinski et al., 1995), and the NFOG Q (Nieub oer et al., 2009). The experimenter then administered the MOCA. Following completion of questionnaires, the following measurements were obtained: height, weight, leg length knee width, and ankle width. Participants were fitted with retro reflective markers and familiarized with the protocol, completing three practice trials using unique neutral pictures and one blank picture. The practice trials were immediately fol lowed by 35 data collection trials. Participants were informed that each trial begins with the presentation of a fixation cross on the video screen (2 s), which would be replaced by a picture for 2 4 s. Participants were instructed to look at the picture t he entire time it was on the screen. At picture offset, th e screen became blank (white). Participants were instructed to initiate walking with their preferred limb immediately as possible following picture offset and to continue walking for several step s at their self selected pace. Each participant performed 5 trials for each affective category and 5 trials using the blank black screen for a total of 35 trials. To determine if participants became physically fatigued during the experimental session, parti cipants also completed five self initiated trials with no picture presentation before (pre trials) and after (post trials) the experimental trials. Following completion of the gait initiation trials, participants completed the computerized SAM scale to pro vide an arousal and valence rating (scale: 1 9) for each picture previously viewed. Data Reduction Reaction time, displacement and velocity of COP in a given direction, step length, average step velocity, and instantaneous velocity of the first and second steps were calculated.

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135 Reaction time (RT). Reaction time was operationalized as the latency from the movement trigger (picture offset) to the ini tiation of the motor response. Initiation of motor response was defined as the time at which the vertical dif ferentiation between the swing limb and stance limb reaches a 5% threshold of force production (Diermayr, Gynsin, Hass, & Gordon, 2008). COP Displacement and Velocity Movement of the COP trajectory was quantified by the displacements and velocities of the COP trace observed over time in both the medio lateral (MP) and anterior posterior (AP) direction. The COP trace during the gait initiation trials was divided into three periods (S1: anticipatory postural adjustment; S2: weight transfer; S3: locomotor ) by identifying two landmark events (Hass et al., 2004) (See Figure 3 1). Figure 3 1. Overhead view of the path of the COP during forward GI when stepping with the right foot. Adapted from Hass, C.J. Gregor, R.J., Waddell, D.E., Oliver, A., Smith, D .W., Fleming, R.P. et al. (2004). The influence of Tai Chi training on the center of pressure trajectory during gait initiation in older adults. Arch Phys Med Rehabil, 85 (10), 1593 1598. S1 begins with picture offset and ends with COP located in its mos t posterior and lateral position toward the in itial swing limb (Landmark 1). S2 is defined as the translation of

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136 the COP toward the stance limb ending at landmark 2, which is the position under the stance limb on which the COP begins to move forward under the foot. S3 begins at landmark 2 until toe off of the initial stance limb as the COP is translated anteriorly. During these three periods, the following dependent variables were evaluated: 1) displacement of the COP in the x (AP) and y (ML) direction, and 2) the average velocity of the COP in the x and y direction. Step length and velocity The gait cycle was time normalized from the instance of heel strike to the nex t heel strike of the same leg. Step length of the first step was calculated as the disp lacement in centimeters (cm) of the initial swing limb heel marker from its initial resting position until heel strike. Step length of the second step was calculated as the displacement in centimeters from the heel position of the swing leg at first heel s trike to the heel position of the stance leg at heel strike. An average velocity of the swing leg was calculated for each step as the step length divided by the corresponding change in time in centimeters per second (cm/s). The instantaneous velocity of th e first and second steps was also calculated using the central difference method: v( t i ) = [v( t i+1 ) v( t i 1 Percent change scores. Replicating previous research, we created a single index for each movement variable that represented the change in m ovement due to each affective category rel ative to the neutral category. Because PD patients exhibited smaller and slower COP adjustments and steps compared to the control participants, percent change scores rather than raw bias scores were used to remove the influence of baseline differences. Percent change scores were calculated with the following formula: [(emotional category /neutral category)*100] 100. A positive score therefore

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137 indicates greater values for the dependent variable during the emotional category relative to the neutral category, while a negative score indicates reduced values for the dependent variable during the emotional category relative to the neutral category. The actual values for each gait measure as well as the percent change scor es were the basis for statistical analyses. Statistical Analyses Descriptive characteristics were calculated for each group for age, height, weight, and all affective state and trait measures. Independent samples t tests were used to determine whether th e PD and control groups differed on any of th e descriptive characteristics. Additionally, to determine whether fatigue may have influenced the gait initiation trials as the experimental session progressed, the COP variables and the step variables for the p re and post trials were each analyzed with a 2 (GROUP: PD, control) 2 (Time: pre, post) MANOVA with repeated measures on the second factor. Primary Statistical Analyses To determine whether affective category and the presence of PD altered the speed at which gait was initiated, RT was analyzed in a 2 (GROUP: PD, control) 7 (CATEGORY: erotica, happy people, mutilation, contamination, attack, neutral, blank) analysis of variance (ANOVA) with repeated measures on the second factor. To establish whether the degree of change in RT due to each affective category compared to the neutral category differed between the PD and control groups, RT percent change scores were analyzed with a 2 (GROUP: PD, control) 5 (CATEGORY: erotica, happy people, mutilation, c ontamination, attack) ANOVA with repeated measures on the second factor. The CATEGORY factor for all analyses involving the percent change scores had only five levels because these analyses were only concerned with

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138 evaluating the change in movement followi ng the five affective categories relative to the neutral category. COP displacement and velocity values and percent change scores were evaluated during the 3 periods of the COP trace (S1, S2, S3). Thus, 3 separate 2 (GROUP: PD, control) 7 (CATEGORY: er otica, happy people, mutilation, contamination, attack, neutral, blank) multivariate analyses of variance (MANOVA) with repeated measures on the second factor was conducted to determine whether affective category and the presence of PD alters the COP traje ctory, while controlling for type I error. The percent change scores for the COP dependent variables were also analyzed in 3 separate 2 (GROUP: PD, control) 5 (CATEGORY: erotica, happy people, mutilation, contamination, attack) MANOVAs with repeate d mea sures on the last factor. The dependent variables for each MANOVA included AP and ML displacement and AP and ML velocity. Step length and velocity of the first and second steps and stride length were analyzed in a 2 (GROUP: PD, control) 7 (CATEGORY: ero tica, happy people, mutilation, contamination, attack, neutral, blank) MANOVA with repeated measures on the second factor. To determine whether differences existed between the PD and control groups in the degree of change observed in the step execution par ameters due to each affective category relative to the neutral, percent change scores for step length and velocity of the first and second steps and stride length were analyzed in a 2 (GROUP: PD, control) 5 (CATEGORY: erotica, happy people, mutilation, contamination, attack) MANOVA with repeated measures on the second factor.

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139 For each MANOVA, separate two way ANOVAs were performed for follo w up testing when appropriate. We also conducted two way ANOVAs (Group Category) on the SA M valence and arousal ra tings. For the ANOVAs for RT and SAM data, if the sphericity assumption was violated, then Greenhouse Geisser degrees of freedom corrections were applied to obtain the critical p value. Follow up analyses were conducted using Tukey HSD procedure and simple effects test s for significant main effects a nd interactions, respectively. For all analyses, the critical probability value was set at p < .05. Secondary Statistical Analyses Even though the PD and control group were selected to be as homogenous as possi ble on dispositional variables (i.e., mood variables and disease severity), we acknowledge that some degree of heterogeneity characterized our sample Additionally, analyses showed that the PD group differed from the control group on the dispositional vari ables of d epression, apathy, and height. Our study design produced a multilevel data set in which gait initiation outcomes varied both between tr ials and between participants. Thus we used hierarchical linear modeling (HLM) and HLM 6.6 (Raudenbush & Byrk, 2002) to examine 1) the effect of self reported valence and self reported arousal on gait initiation parameters, 2) the effect of depression, apathy, and PD on gait initiation parameters, while controlling for height, and 3) the moderating effect of depres sion, apathy, and PD on level 1 effects (i.e., the effect of valence/arousal on movement parameters), while controlling for height. 1 gait initiation outcome variables i n the level 2 person vari able. The focus of the analyses was on how the emotion induction, measured by the valence and arousal ratings, influenced the gait

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140 initiation parameters. Thus, we included only the data from the trials in which an IAPS image was presented (i.e., 30 trials per person). Level 1 predictors included two continuous variables: 1) SAM valence ratings (Valence), and 2) SAM arousal ratings (Arousal). Level 2 predictors included three continuous variables and one dichotomous variable, respectively: 1) level of depres sion (BDI score), 2) level of apathy (Apathy Scale score), 3), height (HT), and 4) PD (Control = 0; PD = 1). The level 1 independent variables were group mean centered and the level 2 variables were grand mean centered. An initial analyses was conducted on the PD group with disease severity (UPDRS score) as a level 2 variable. These analyses showed that disease severity was not a significant predictor of any of the gait initiation parameters, therefore the PD and control groups were combined for the all of the HLM analyses and PD was included as a level 2 variable. Per recommendations of Raudenbush and Bryk (2002) four distinct hierarchical linear models for each dependent variable assessin g gait initiation were tested. First, a Random ANOVA model tested whether significant variation existed in the dependent v ariables between participants. Second, a Means as Outcomes (MAO) model determined whether between person variation in the dependent variables was predicted by depression, apathy, or PD, after controll ing for height. Third, a random regression coefficient model was conducted to test whether self reported measures of arousal and valence predicted between trial variati on in the dependent variables. Fourth, an intercepts and slopes as outcomes (IASO) model tested whether depression, apathy, or PD predicted between trial (i.e., arousal, valence) effects. The level 1 and level 2 models for the IASO analyses were:

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141 Level 1 : GI ij 0j 1j (Valence) 2j (Arousal) + e ij Level 2 : 0j 00 01 02 03 04 (HT) + r 0j 1j 10 11 12 13 14 (HT) + r 1j 2j 20 21 22 23 24 (HT) + r 2j

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142 CHAPTER 4 RESULTS Participants Twenty six individuals with idiopathic PD (female = 3) and twenty five aged matched controls (females = 3) participated in this study. Three male PD patients were excluded from statistical analyses: two patients score d above 19 on the BDI and one patient scored below 26 on the MOCA. Thus, after the removal of these participants the PD group included 23 individuals. A summary of demographic, affective state and trait, and clinical characteris tics are presented in Table 1. As shown, the PD and control groups did not differ statistically with respect to age, mass, cognitive dysfunction, trait anxiety, and positive and negative affect. PD patients obtained significantly higher scores than controls on the BDI 2, Apathy Scale and state version of the STAI. However, both groups had mean BDI scores in the non depressed range and mean STAI S scores indicating a low to moderate level of state anxiety. All participants reported being free of neurological disorders (other than PD for the Parkinson group), major psychiatric disturbances, and medications affecting balance or alertness/attention. The PD patients were in the middle stages of their disease (Hoehn and Yahr stage of 2 or 3) and demonstrated a moderate degree of disease se verity based on the UPDRS (Fa hn, Elton, & Committee, 1987). These staging and severity indices were obtained within six months of participation in the current study. Data points 3 SDs from the mean were considered extreme scores and were removed prior t o analysis. Additionally, trials in which participants did not initiate gait following picture offset (i.e., did not initiate gait at all or initiated gait prior to picture offset) were removed. Participants missing one or more scores were completely

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143 remov ed from each separate analysis. Consequently, 2 PD participants and 2 control participants were removed from the COP analyses and the step length/velocity analyses, and 2 PD participants and 1 control participant were removed from the RT analyses. Technica l problems also led to the exclusion of reaction time data from 3 participants. Table 4 1 Demographic, affective, and clinical characteristics by group. Primary Statistical Results Reaction Time Raw RT scores The 2 way ANOVA revealed a significant ma in effect of Group [ F (1, 38) = 4.83, p = .034, = .113] and Category [ F (3.63, 137.95) = 3.24, p = .017, = .08]. The control group ( M = 331 ms, SD = 21) exhibited faster reaction times on the gait initiation task compared to the PD group ( M = 400 ms, SD = 23). Across all participants, exposure to the attack pictures speeded reaction times on the GI task compared to all other categories expect for the blank (attack = 320 ms ( SD = 104),

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144 mutilation = 370 ms ( SD = 134), contamination = 398 ms ( SD = 160), erotic = 383 ( SD = 149), happy people = 369 ( SD = 135), neutral = 344 ms (SD = 98), blank = 354 ( SD = 138). Additionally, reaction time was slower following exposure to the contamination, mutilation, erotic, and happy people pictures compared to the neutr al pictures (See Figure 4 1a). The group by categ ory interaction was not significant ( p > .05). RT percent change scores The 2 way ANOVA conducted on the reaction time percent change scores similarly showed a significant main effect of category [ F (2.84, 113.76) = 6.43, p = .001, = .14], confirming t hat reaction time was faster following the presentation of the attack pictures compared to all other affective picture categories (See Figure 4 1b). The main effect of group and the group by category interaction were not significant ( p S1 Region of the COP Trace Raw COP scores The MANOVA conducted on the pre and post trials showed a significant main effect of time, = .612, F (4, 34.00) = 5.38, p = .002, = .39. The follow up tests were significant for the AP displacement, F (1, 37) = 12.24, p = .001, = .25 [means: pre = 2.04 cm (.16), post = 2.52 cm (.23)], ML displacement, F (1, 37) = 8.20, p = .007, = .18 [means: pre = 1.70 cm (.25), post = 2.37 cm (.20)], and AP velocity, F (1, 37) = 7.01, p = .012, = .16 [means: pre = 2.58 cm/s (.32), post = 3.38 cm (.41)]. For all participants the displacement and velocity of the posterior COP movement, as well as the lateral COP displacement in the S1 regi on significantly increased from the pre trials to the post trials, indicating that fatigue was likely not a factor influencing the S1 COP variables du ring the experimental session. The main effect of group and the group by time interaction were not signifi cant ( > .05).

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145 The 2 way MANOVA conducted on the experimental trials revealed significant main effects of category = .832, F (24, 828.00) = 1.87, p = .007, = .05 and group = .619, F (4, 37) = 5.70, p = .001, = .38. Figure 4 2 presents the displacement and velocity of the COP movement in the posterior and lateral directions. The respective follow up ANOVAs for the main effect of category p roduced significant effects for the displacement [ F (6, 240) = 4.30, p > .001, = .10] and velocity [ F (4.04, 161.68) = 3.565, p = .008, = .08] of the COP movement in the AP direction As hypothesized, exposure to the erotic and happy people pictures re sulted in a significant increase in the magnitude of the COP displacement in the posterior direction compared to the attack, mutilation, contamination, and neutral pictures (Figure 4 2a). Similarly, exposure to the erotic pictures compared to the attack, c ontamination, and neutral ( p = .077) pictures resulted in greater velocity of the posterior COP movement (Figure 4 2b). Additionally, the posterior COP velocity was 1) greater following exposure to the happy people pictures compared to the contamination pi ctures and 2) reduced following exposure to the attack, mutilation, contamination, and neutral pictures c ompared to the blank pictures. The follow up ANOVAs for the displacement ( p = .083; Figure 4 2c) and velocity ( p = .077; Figure 4 2d) of the COP moveme nt in the lateral direction were not significant. The follow up ANOVAs for the main effect of group were significant for each COP measure in the S1 phase: posterior displacement, F (1, 40) = 21.73, p > .001, = .35 [means: Control = 4.88 cm (.32), PD = 2.70 cm (.35)]; posterior velocity, F (1, 40) = 13.92, p = .001, = .26 [means: Control = 7.47 cm/s (.64), PD = 3.93 cm/s (.70)]; lateral displacement, F (1, 40) = 6.19, p = .017, = .13 [means: Control = 3.50 cm

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146 (.23), PD = 2.66 cm (.25)]; lateral velocity, F (1, 40) = 7.05, p = .011, = .150 [means: Control = 5.31 cm/s (.41), PD = 3.68 cm/s (.46)]. As expected, these results showed that the magnitude of the displacement and velocity of the COP move ment in each direction was greater for the control g roup compared to the PD group. The group by category interaction was not significant ( p = .165). COP percent change scores The 2 way MANOVA on the percent change scores revealed a significant main effec t of category for the variables in the S1 region of the COP curve, = .823, F (16, 480.00) = 1.98, p = .013, = .05. Figure 4 3 presents the percent change scores for displacement and velocity of the COP movement in the posterior and lateral directions. The respective follow up ANOVAs showed a significant effect of category for the displacement of the COP movem ent in the posterior direction, F (2.84, 113.60) = 5.73, p = .001, = .13 The posterior COP displacement percent change scores for the happy people and erotic pictures were significantly greater than the percent change scores for the attack and contamin a tion pictures (Figure 4 3a). The ANOVA conducted on the velocity of the posterior COP approached significance, F (2.56, 102.49) = 2.66, p = .06, = .06, with the erotic and happy people pictures resulting in greater posterior velocity percent change score s compared to the attack and contamination pictures (Figure 4 3b). The ANOVAs also showed a significant effect of category for the COP displacement in the lateral direction, F (4, 160) = 3.11, p = .017, = .07. The percent change scores for 1) the erotic pictures were significantly greater than the mutilation pictures and 2) the happy people pictures were significantly greater than the mutilation and contami nation pictures (Figure 4 3c). The ANOVA conducted on the lateral COP velocity percent change scores was not

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147 significant ( p = .182; Figure 4 3d). The main effect of group and the group by category interaction were not significant ( > .05). S2 Region of the COP Trace Raw COP scores The MANOVA conducted on the pre and post trials showed a significa nt main effect of group, = .716, F (4, 34.00) = 2.67, p = .049, = .24 and time, = .611, F (4, 34.00) = 5.41, p = .002, = .39. Significant group differences were found for AP displacement, F (1, 37) = 5.70, p = .022, = .13 [means: Control = 0.98 cm (.51), PD = 0.80 cm (.55)], ML displacement, F (1, 37) = 5.17, p = .029, = .12 [means: Control = 11.03 cm (.45), PD = 9.53 cm (.48)], and ML velocity, F (1, 37) = 4.90, p = .033, = .12 [means: Control = 10.91 cm/s (.70), PD = 8.64 cm/s (.75)]. Across all trials the control group exhibited greater displacement and velocity of the medial COP movement in the S2 region compared to the PD group. The follow up tests for time were significant for the AP displacement, F (1, 37) = 8.91, p = .005, = .19 [means: pre = .60 cm (.37), post = .42 cm (.45)] and ML velocity, F (1, 37) = 11.17, p = .002, = .23 [means: pre = 9.17 cm/s (.54), post = 10.38 cm/s (.55)]. The velocity of the medial COP movement in the S2 region significantly increased from the pre tri als to the post trials. The group by time interaction was not significant ( > .05). The 2 way MANOVA conducted on the experimental trials revealed a significant main effect of group, = .584, F (4, 37) = 6.60, p > .001, = .416 The follow up ANOVAs produced a significant effect of group for the AP COP displacement, F (1, 40) = 7.60, p = .009, = .16 [means: Control = .21 cm (.32), PD = 1.81 cm (.43)]; the ML COP displacement, F (1, 40) = 9.54, p = .004, = .19 [means: Contro l = 11.87 cm (.45), PD = 9.81cm (.49)]; and the ML COP velocity, F (1, 40) = 11.49, p = .002, = .22 [means: Control = 1.44 cm/s (.08), PD = 1.06 cm/s (.08)]. Across picture categories,

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148 the control group displayed greater displacement and velocity of th e medial COP movement in the S2 region compared to the PD group (See Figure 4 4) The main effect of category and the interaction were not significant ( > .05). COP percent changes scores The main effect of category approached significance, da = .853, F (16.00, 480.28) = 1.60, p = .065, = .039, and was driven by a significant ANOVA for the velocity of the COP trajectory in the ML direction, F (4, 160) = 3.35, p = .011, = .052. While such findings must be considered with caution due to the lack of omnibus significance, the data sugges t that exposure to 1) erotic and happy people pictures lead to greater ML velocity percent change scores compared to mutilation pictures and 2) happy people pictures resulted in greater ML velocity percent change scores compared to contamination pictures ( See Figure 4 5) The main effect of group and the interaction were not significant ( > .05). S3 Region of the COP Trace Raw COP scores The MANOVA conducted on the pre and post trials showed a significant main effect of time, = .375, F (4, 34.00) = 14.17, p < .001, = .63. The follow up tests were significant for only the AP displacement, F (1, 37) = 4.83, p = .034, = .12 [means: pre = 14.56 cm (. 98), post = 13.26 cm (1.12)]. The magnitude of the anterior displacement of the COP mo vement in the S3 region significantly decreased from the pre trials to the post trials. The main effect of group and the group by time interaction were not significant ( > .05). The MANOVA conducted on the experimental trials showed no significant effec ts for the S3 portion of the COP trajectory ( > .05). COP percent change scores No significant effects were found for the percent change scores during the S3 portion of the COP trajectory ( > .05).

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149 Average Step Length and Step Velocity of the 1 st and 2 nd S teps Raw Step length and velocity scores The MANOVA conducted on the pre and post trials showed a significant main effect of time = .430, F (5, 35.00) = 9.30, p < .001, = .57. The follow up tests were significant for the len gth of step 1, F (1, 39) = 8.86, p = .005, = .19 [means: pre = 51.53 cm (1.31), post = 53.85 cm (1.48)], stride length, F (1, 39) = 5.23, p = .028, = .12 [means: pre = 105.66 cm (2.33), post = 108.53 cm (2.77)], velocity of step 1, F (1, 39) = 10.00, p = .003, = .20 [means: pre = 47.18 cm/s (2.15), post = 53.41 cm/s (2.38)], and velocity of step 2, F (1, 39) = 19.39, p > .001, = .19 [means: pre = 80.93 cm/s (2.5 4), post = 87.45 cm/s (3.07)]. The length and velocity of step 1, stride length, and the velocity of step 2 significantly increased from the pre trials to the post trials, indicating that fatigue was not likely a factor influencing the step execution component of GI du ring the experimental session. The main effect of group and the group by tim e interaction were not significant ( > .05). The 2 way MANOVA conducted on the experimental trials revealed a significant main of effect of group, = .698, F (5, 38) = 3.29, p = .014, = .30. The follow up tests revealed significant group differences for each dependent variable: length of step 1, F (1, 42) = 16.28, p > .001, = .28 [mean: Control = 57.02 cm/s (1.74), PD = 46.90 cm/s (1.82)]; length of step 2, F (1, 42) = 10.22, p = 003, = .20 [mean: Control = 58.85 cm/s (1.68), PD = 51.07 cm/s (1.68)]; stride length, F (1, 42) = 14.63, p > .001, = .26 [mean: Control = 115.87 cm/s (3.24), PD = 97.92 cm/s (3.39)]; velocity of step 1, F (1, 42) = 14.63, p = .001, = .25 [mean: C ontrol = 64.45 cm/s (2.72), PD = 49.66 cm/s (2.84)]; velocity of step 2, F (1, 42) = 5.55, p = .023, = .12 [mean: Control = 95.47 cm/s (3 .90), PD = 82.16 cm/s (4.09)]. As hypothesized the control group exhibited longer step and stride lengths and great er step velocities

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150 compared to the PD group (See Figure 4 6) The main effect of category and the interaction were not significant ( > .05). Step length and velocity percent change scores The 2 way MANOVA conducted on the percent change scores produced a significant category by group interaction, = .825, F (20, 544.88) = 1.62, p = .043, = .047. Figure 4 7 presents the percent change scores for length and velocity of the first and second step. The follow up tests revealed a significant interaction for the velocity of the first step, F (4, 168) = 3.49, p = .009, = .08. Exposure to muti lation pictures for the PD group resulted in reduced step velocity percent changes scores compared to mutilation and erotic pictures for the control group and happy people pictures for both groups. The group and category main effects were not significant ( > .05). Additionally, no significant findings were found for step 2. Instantaneous Velocity of the 1 st and 2 nd S teps Raw Instantaneous step velocity scores Instantaneous velocity was measured to index the velocity at heel strike of the first and seco nd steps. The MANOVA conducted on the pre and post trials showed a significant main effect of group = .857, F (2, 38.00) = 3.16, p = .05, = .14 and time, = .434, F (2, 38.00) = 24.80, p < .001, = .57. Significant group dif ferences were found for velocity of step 1, F (1, 39) = 6.38, p = .016, = .14 [means: Control = 81.25 cm/s (3.64), PD = 68.09 cm/s (3.73)] and step 2, F (1, 39) = 3.94, p = .05, = .09 [means: Control = 106.14 cm/s (4.02), PD = 94.70 cm/s (4.12)]. Acros s all trials the control group exhibited greater instantaneous velocity at heel strike for step 1 and 2 compared to the PD group. The follow up tests for the main effect of time were also significant for the velocity of step 1, F (1, 39) = 42.68, p < .001, = .52 [means: pre = 71.13 cm/s (2.58), post = 78.21 cm/s

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151 (2.73)] and the velocity of step 2, F (1, 39) = 18.72, p < .001, = .32 [means: pre = 97.41 cm/s (2.77 ), post = 103.43 cm/s (3.14)]. Similar to the average step velocity results, the instantaneou s velocity of step 1 and 2 significantly increased from the pre trials to the post trials. The group by time interaction was not significant ( p > .05). The MANOVA conducted on the instantaneous velocity of the first and second steps for the experimental trials revealed a significant main of effect of group Lambda = .862, F (3.27, 41.00) = 3.27, p = .048, = .14. The follow up tests revealed significant group differences for velocity of step 1, F (1, 42) = 6.70, p = .013, = .14 [mean: Control = 83.10 cm/s (3.65), PD = 69.44 cm/s (3.82)] and velocity of step 2, F (1, 42) = 4.64, p = .037, = .10 [mean: Control = 127.77 cm/s (4. 19), PD = 99.70 cm/s (43.89)]. The control group exhibited greater instantaneous velocity for step 1 and 2 compared to the PD group. The main effect of category and the group by category interaction were not significant ( > .0 5). Instantaneous step velocity percent change scores The MANOVA conducted on the instantaneous step velocity percent change scores revealed no significant effects ( > .05). SAM R atings The 2 way ANOVA conducted on the valence ratings revealed a si gnificant main effect of category F (2.97, 121.70) = 305.85, p > .001, = .882. As expected all participants rated the erotic and happy people pictures as significantly more pleasant than the mutilation, attack, contamination, and neutral pictures (Figur e 4 8 a). The mutilation pictures were rated significantly more unpleasant than all other picture categories, and the attack and contamination pictures were rated as more unpleasant

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152 than the neutral pictures. The main effect of group and the interaction wer e not significant ( > .05). The 2 way ANOVA conducted on the arousal ratings also demonstrated a significant main effect of category, F (2.96, 121.29) = 41.81, p > .001, = .51. As demonstrated in Figure 4 8 b, the erotic pictures were rated significantly more arousing than all other picture categories and mutilation pictures were rated more arousing than all categories except for erotic. Attack pictures were rated signi ficantly more arousing than the happy people, contam ination, and neutral pictures. Finally, the contamination and happy people pictures were rated significantly more arousing than neutral pictures. The main effect of group and the interaction were not sig nificant ( > .05). Secondary Statistical Results R eaction T ime reaction time on the gait initiation task ( p < .001). However, the MAO model revealed that the variation in rea ction time was not significantly predicted by any of the level 2 variables ( > .05). The RRC model also showed that no significant relationship existed between self reported valence/ arousal and reaction time ( > .05). This analysis also revealed tha t the relationship between the level 1 variables and reaction time did not vary significantly between participants ( > .05); thus the data were not analyzed with an IASO model. S1 Region of the COP Trace The RA model indicated significant variation exi sted among individuals in their posterior and lateral displacement and velocity of the COP movements in the S1 region on the gait initiation task ( < .001). The MAO model showed that the presence of PD

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153 significantly predicted the posterior displacement, 03 = 1.70, SE = 0.55; t (40) = 3.08, p = 0.004, and posterior velocity of the COP movement, 03 = 0.025, SE = 0.116; t (40) = 2.17, p = 0.036. Confirming the MANOVA results, individuals with PD exhibited reduced COP displacement and velocity in the po sterior direction compared to healthy control individuals, eve n after controlling for height. The RRC models showed that each COP variable in the S1 region had a significant relationship with self reported valence, AP displacement 10 = 0.036, SE = 0.009; t (1240) = 4.09, p < 0.001; AP velocity 10 = 0.007, SE = 0.003; t (44) = 2.36, p = 0.023; ML displacement 10 = 0.021, SE = 0.008; t (1241) = 2.53, p = 0.019; ML velocity 10 = 0.005, SE = 0.002; t (1241) = 2.70, p = 0.008. Supporting the MANOVA results exposure to pictures which were rated more pleasant, relative to unpleasant, resulted in greater magnitude of the COP displacement and velocity in the pos terior and lateral directions. The RRC models also revealed that the level 1 slope for arousal and M L COP displacement ( p = .049) and the slope for valence and AP COP velocity ( p = .015) significant ly varied between participants. However, the IASO models indicated that no level 2 variables predicted the relationship between arousal and ML COP displacemen t or valence and AP COP velocity ( > .05). S2 Region of the COP Trace The RA model indicated significant variation existed among individuals in their AP and ML displacement and velocity of the COP movements in the S2 region on the gait initiation tas k ( < .001). significantly predicted the medial COP displacement, 04 = 0.117, SE = 0.041; t (40) = 2.86, p = 0.007. As expected, participants who were taller demonstrated greater medial COP displacement in the S2 region. The presence of PD significantly predicted the

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154 medial COP velocity, 04 = 0.299, SE = 0.140; t (40) = 2.13, p = 0.039. Individuals with PD were more likely to exhibit reduced medial COP velocity compared to those without PD. The remaining MAO models pr oduced no significant effects. Additionally, the RRC models revealed that self reported valence and ar ousal did not significantly predict the COP variables and that the relationship between the level 1 variables and COP movement did not vary sign ificantly across participants. Thus, the IASO models were not conducted for the COP variables in the S2 region. S3 Region of the COP Trace The RA models indicated significant variation existed among individuals in their AP and ML displacement and velocity of the COP movements in the S3 region on the gait initiation task ( < .001). The MAO model showed that the p significantly predicted the anterior COP displacement, 04 = 0.226, SE = 0.088; t (40) = 2.58, p = 0.014. As expected, participants who were taller displayed greater anterior COP displacement in the S3 region. All the remaining models conducted produced no significant results ( > .05). Average Step Length and Step Velocity of the 1 st and 2 nd S teps The RA models showed that significant variation existed among individuals in their length and velocity of the first and se cond steps of gait initiation. The MAO models revealed that PD predicted the length of st ep 1, 03 = 67.45, SE = 25.95; t (41) = 2.60, p = 0.013, and the velocity of step 1 03 = 101.53, SE = 46.44; t (41) = 2.19, p = 0.034. Individuals with PD displayed shorter step lengths and slower step velocity compared to those individuals without PD. He ight also predicted the length of step 1, 04 = 4.43, SE = 1.71; t (41) = 2.60, p = 0.013, as well as the length of step 2 (Ht: 04 = 4.26, SE = 1.38; t (41) = 3.08, p = 0.004). Individuals who were taller exhibited longer step lengths.

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155 The RRC model dem onstrated that a significant relationship existed between self reported valence and velocity of the first step, 10 = 1.57, SE = 0.56; t (45) = 2.78, p = 0.008. Exposure to images rated more pleasant, relative to unpleasant, resulted in greater step veloci ty for the first step of gait initiation. The remaining RRC models were not significant ( > .05). Additionally the RRC models revealed that the relationship between the level 1 variables and step length/velocity did not vary significantly across parti cipants so the data were not analyzed with an IASO model.

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156 Figure 4 1. Mean reaction time (Figure 4 1a) and mean percent change scores for reaction time (Figure 4 1b) across category conditions for the PD and Control groups. A=att ack, M=mutilation, CM=contamination, E=erotic, HP=happy people, N=neutral, B=blank.

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157 Figure 4 2. COP movement in the S1 region across category conditions for the PD and Control groups for the mean displacement in the posterior direction (Figure 4 2a), mean velocity in the posterior direction (Figure 4 2b), mean displacement in the lateral direction (Figure 4 2c), and mean velocity in the lateral direction (Figure 4 2d). A=attack, M=mutilation, CM=contamination, E=erotic, HP=happy people, N=neutral, B=b lank.

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158 Figure 4 3. COP movement percent change scores in the S1 region across category conditions for the PD and Control groups for the mean percent change displacement in the posterior direction (Figure 4 3a), mean percent change velocity in the poste rior direction (Figure 4 3b), mean percent change displacement in the lateral direction (Figure 4 3c), and mean percent change velocity in the lateral direction (Figure 4 3d). A=attack, M=mutilation, CM=contamination, E=erotic, HP=happy people.

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159 Figure 4 4 COP movement in the S 2 region across category conditions for the PD and Control groups for the mean displacement in the posterior direction (Figure 4 4 a), mean velocity in the posterior direction (Figure 4 4 b), mean displacement in the medial (Figure 4 4 c), and mean velocity in the medial direction (Figure 4 4 d). A=attack, M=mutilation, CM=contamination, E=erotic, HP=happy people, N=neutral, B=blank.

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160 Figure 4 5 COP movement percent change scores in the S2 region across category conditions for th e PD and Control groups for the mean percent change displacement in the posterior direction (Figure 4 5 a), mean percent change velocity in the posterior direction (Figure 4 5 b), mean percent change displacement in the medial direction (Figure 4 5 c), and me an percen t change velocity in the medial direction (Figure 4 5 d). A=attack, M=mutilation, CM=contamination, E=erotic, HP=happy people.

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161 Figure 4 6 Mean length of step 1 (Figure 4 6a), mean velocity of step 1 (Figure 4 b), mean stride length (Figure 4 6c), mean length of step 2 (Figure 4 6d) and mean velocity of step 2 (Figure 4 6e) across category conditions for the PD and Control groups. A=attack, M=mutilation, CM=contamination, E=erotic, HP=happy people, N=neutral, B=blank.

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162 Figure 4 7. Mean perc ent change scores across category conditions for the PD and Control groups for length of step 1 (Figure 4 7a), velocity of step 1 (Figure 4 7b), length of step 2 (Figure 4 7c), and velocity of step 2 (Figure 4 7d). A=attack, M=mutilation, CM=contamination, E=erotic, HP=happy people.

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163 Figure 4 8. Mean SAM valence ratings (Figure 4 8a) and arousal ratings (Figure 4 8b) across category conditions for the PD and Control groups. The higher a es as being pleasant or arousing, respectively. A=attack, M=mutilation, CM=contamination, E=erotic, HP=happy people, N=neutral.

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164 CHAPTER 5 DISCUSSION Individuals with PD experience difficulty initiating gait which is often highly disabling and can inter fere with many facet s of daily living. C urrent therapies for patients with PD have shown clear but limited benefits for the treatment of gait disturbances A pressing need remains to develop novel and complimentary therapeutic strategies to treat these dis abling gait symptoms. Gamble and colleagues (in review) r ecent ly demonstrated that pleasant emotional states improve the quality of gait initiation in healthy young adults M anipulation of emotional state may therefore be a viable strategy for optimizing t he quality of gait initiation in individuals suffering from P D. T he primary aim of the present experiment was to determine the impact of emotional state on the quality of gait initiation in persons wit h PD and healthy older adults. To address this aim par ticipants with PD and healthy aged matched older adults were required to initiate gait and walk several steps following exposure to affective stimuli representing specific emotional categories. Three novel contributions emerged : 1) threatening stimuli spee d the initiation of gait for PD patients and healthy older adults, 2) pleasant emotional stimuli facilitate the anticipatory postural adjustments of gait initiation as well as the velocity of the first step for PD patients and healthy older adults, and 3) exposure to emotional stimuli modulates gait initiation parameters in PD patients to the same degree as healthy older adults. Following discussion of these findings, limitations of the present study are addressed, practical implications are suggested, and recommendations for future research are offered.

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165 Reaction Time Persons with PD have consistently shown deficits on simple reaction time tasks (Gauntlett Gilbert & Brown, 1998; Burleigh Jacobs, et al., 1997; Dibble, Nicholson, Shultz, MacWilliams, Marcus & Moncur, 2004 ). I therefore hypothesized that PD patients would exhibit slower reaction times on the gait initiation task across all picture conditions relative to the age matched control group In line with expectations PD pa tients reacted more slowl y to initiate gait in response to the target initiating stimulus (i.e., picture onset) compared to healthy older adults. While the underlying mechanisms of this deficit have been debated, the delay in movement is likely due to a deficit in central process ing of the initiating stimulus (Kutukcu, Marks, Jr., Goodin, & Aminoff, 1998; Cooper, Sagar, Tidwell, & Jordan, 1994). These results support the notion that PD is characterized by the inability to initiate movement (i.e., akinesia) and slowness of willed m ovement (i.e., bradykinesia). Consistent with the second hypothesis, exposure to attack pictures speeded the initiation of gait compared to all other pictures categories. The current data support and extend previous evidence showing that exposure to th reatening stimuli speeds the initiation of the motor response on a gait initiation task in healthy young adults (Gamble et al., in review), as well as on upper extremity movement tasks (e.g., ballistic precision pinch grip: Coombes, et al., 2009; wrist ext ension: Coombes et al., 2007a). Threatening contexts theoretically prime the motor system for action, accelerating motor responses and thereby providing organisms the advantage of efficient fight or flight response (hman, et al., 2000; hman & Soare s 19 98). Furthermore, Coombes et al. (2007a) showed that activating defensive emotional circuitry speeds the initiation of the appropriate motor action by facilitating the central processes that precede overt

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166 movement (i.e., perceptual and cognitive processes necessary to perceive the onset cue and formulate the appropriate motor response). Evidence from the current project corroborates this position and importantly, suggests that the neural circuitry underlying th e survival function of the primitive emotion s ystem remains preserved in healthy older adults and those with PD Indeed, a similar reduction in reaction time (~6%) was observed for PD and control participants in response to attack pictures relative to neutral pictures. While cons istent with data acquired from projects that have involved young, healthy subjects, the current findings conflict with those reported in prior research showing that PD patients exhibit blunted reactivity to highly arousing aversive pictures, as indexed by reduced startle eye blink magnitude (Bowers et al. 1996; Miller et al. 2009). Although such evidence might appear contradictory, Miller and colleagues (2009) later specified that the diminished startle potentiation occurred in response to a single subcateg ory of aversive pictures ; namely mutilations. Similar startle reactivity in response to attack, contamination, pleasant and neutral pictures was observed fo r control and PD participants. Furthermore, Miller et al. were interested in emotion modulation of i nvoluntary movement, which is controlled by different circuits than voluntary movement. Taken together, the findings indicate that PD patients with moderate disease severity experience similar motor and physiological reactivity to threatening stimuli compa red to healthy older adults. Exposure to all other affective pictures led to increased reaction times compared to the neutral pictures for all participants. Prior work has shown that viewing emotional arousing pictures relative to un arousing neutral pic tures uses more attentional resources (Bradley, Greenwald, Petry, & Lang, 1992; Cuthbert et al., Schupp, Bradley,

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167 Birbaumer, & Lang, 2000 ; Lang, Bradley, & Cuthbert, 1998). All participants in the current study rated the affective pictures categories (i.e. erotic, happy people, mutilation, attack, contamination) higher in arousal than the neutral pictures. Thus, even though participants initiated gait following picture offset, the attentional demand of viewing arousing stimuli may have interfered with cent ral processes devoted to movement production, thereby slowing Importantly, attack pictures expedited motor responses on the gait initiation task despite also being rated more arousing and potentially more attentionally demandi ng than the neutral pictures Future work should aim to delineate the emotional and attentional contributions to the changes in movement that result from picture viewing contexts. Preparatory Postural Adjustments The quality of preparatory postural adjus tments was indexed via displacement and velocity of the COP movement within the three regions of the COP trajectory during gait initiation. N umerous studies indicat e that PD is characterized by inefficient anticipatory postural adjustments during the gait initiation process (Burleigh Jacobs, et al., 1997; Crenna et al., 1990; Halliday et al., 1998; Gantchev et a l, 1996; Hass et al., 2005). Compared to control participants, PD patients in the current study exhibited reduced displacement and velocity of the C OP movement in the posterior and lateral directions across al l conditions in the S1 region. Furthermore, PD patients exhibited reduced d isplacement and velocity of the medial COP shift during the weight shift phase compared to control participants. However the HLM analyses revealed that the differences in medial displacement may have been driven by differences in average height. These results corroborate previous evidence (e.g., Halliday et al., 1998; Crenna et al., 1990) showing that persons with PD have similar qualitative patterns of COP

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168 movement during gait initiation with reduced COP movement amplitude and velocity particularly during the APAs, ultimately causing a lack forward momentum needed to initiate gait. I also anticipated that exposure to the approach related picture categories erotic and happy people, in the PD and control participants A previous study found that high and low arousing pleasant pictures relative to unpleasant pictures led to g reater displacement and velocity of the posterior and lateral COP movements in the S1 region in healthy young adul ts (Gamble et al., in review). Furthermore, physiological reactivity to pleasant stimuli has been shown to be similar between persons with PD and healthy older adults (Bowers et al., 1996; Miller et al., 2009). The current study extended these findings showing that PD and control participants displayed similar increases in posterior displacement of the COP movement following exposure to happy p eople and erotic pictures compared to attack, mutilation, contam ination, and neutral pictures. Furthermore, exposure to both of these approach related categories enhanced the velocity of the posterior movement compared to atta ck and contamination pictures. The HLM results showed that self reported judgments of valence pre dicted posterior COP movement, thereby providing additional confirmation for the facilitati ng effect of pleasant stimuli. Specifically, pleasant rated images, relative to unpleasant and neu tral, were associated with greater posterior COP displacement and velocity. I mportantly, this effect was not modulated by the presence of PD. T h e initial backward shift of the COP movement caused by the deactivation of the gastrocnemii and soleus muscles (Winter, 1995), drives the COM forward and thus is responsible for producing the forward momentum needed to initiate gait (Crenna et al.,

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169 1990; Massion, 1992; Polcyn, Lipsitz, Kerrigan, & Collins, 1998). The current results suggest that exposure to approac h oriented stimuli may help individuals produce forward momentum during the gait initiation process by augmenting the magnitude and speed of the initial posterior COP movement. T he pleasant picture categories also enhanced the lateral COP movement in the S1 region for all participants. Specifically, the results revealed increased displacement of the lateral movement following exposure to the 1) erotic and happy people pictures compared to mutilation pictures and, 2) happy people pictures compared to the co ntamination pictures. T he HLM analyses supported my hypothesis; revealing greater magnitude and velocity of the lateral COP movement in response to pictures rated more pleasant compared to unpleasant The initial lateral shift toward the swing limb, caused by the momentary loading of the swing leg by the hip abductors (Winter, 1995), propels the COM toward the stance limb in preparation for single limb support and preserves lateral stability during step execution (Polcyn et al., 1998; Jian et al., 1993; Z et tel, Mcllroy, & Maki, 2002). Thus, the lateral COP movement in the S1 region is c ritical to the generation of stance side momentum. The present data indicate that approach oriented stimuli (i.e., pleasant images) facilitate the momentum needed to reach sin gle limb support during forward gait initiation for both persons with PD and healthy older adults. The purpose of the COP movement in the S2 and S3 regions is to complete the positioning of body weight over the initial stance limb and then to propel the COM forward, accelerating it away from the stance limb (Jian, Winter, Ishac, & Gilchrist, 1993) The step execution phase of gait initiation is considered to begin when weight

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170 has been transferred from the initial swing limb to the stance limb (Crenna et al., 1990). Compared to the anticipatory postural adjustments ( which are more centrally controlled ) the S2 and S3 regions represent the beginning of the locomotor phase of gait initiation which is generally regulated by lower level spinal processes (Mass ion, 1992; Rocchi et al., 2006). Nonetheless, we hypothesized that the approach related picture categories would facilitate the velocity of the medial COP movement in the S2 region and the velocity of the anterior COP movement in the S3 region compared to all other p icture categories. This hypothesis was not supported, as exposure to the affective pictures produce d no significant changes in the COP movement in the S2 or S3 region Gamble et al. (in review) similarly found no impact of emotion in the S2 or S3 regions o f the COP trajectory in healthy young adults Thus, the existing evidence suggests that t he effect of emotion on the COP movement during gait initiation i s regulated by the anticipatory postural adjustments occurring during the S1 component of GI Two exp lanations are offered to account for the diminished impact of emotion on the COP movement in S2 and S3. First, within the current protocol and in Gamble et (in review) prior as poss instructed to initiate gait an d walk as quickly as possible. Hence, participants were required to focus more on the planning aspect of the movement rather than on the locomoto r component of the movement. on S1 of the COP trajectory and RT, the two measures most reflecti ve of motor planning

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171 processes. Perhaps requiring participants to focus on the locomotor aspect of the task (e.g., be gin walking as quickly as possible) would lead to modulation of S2 and S3. may vary between the APA phase and locomotor phase is supported by animal and human studies. Resear are largely controlled by the SMA, premotor cortex, and basal ganglia (Massion, 1992, Rocchi et al., 2006; Yazaea et al., 1997 ; Takakusaki et al., 2003 ), whereas the more automatic locomotor components of gait initiation (i .e., S2, S3) are controlled more so by the brainstem and spinal processes ( i.e., CPGs: Takakusaki et al., 2003) Thus, the collective processes controlling the APAs are dissimilar from those that control the locomotor phase of the COP movement. As such the neural circuits regulating the different phases of gait initiation may interact differently with the neural circuits underlying emotional processing. The results of the current study are in line with evidence suggesting that emotion modulation of moveme nt likely involves higher cortical and subcortical processes. Behavioral work (Coombes et al., 2007a, 2007b) has shown that emotion impacts the speed with which ballistic force is initiated as a function of the impact on centrally driven processes (i.e., cognition, perception), as compared to peripheral processes (i.e., musculature and moto r unit recruitment processes). Furthermore, animal retrograde and anterograde tracing studies ( Haber, 2003; Haber et al., 2003 ) and human imaging work (Doron & Goehman, 2010 ; Schmidt et al., 2009 ) suggests circuits involving the basal ganglia and frontal cortex are critical to the integration of limbic and motor circuits. N on reciprocal cortico cortical and corticothalamic pathways may link multiple frontal cortical

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172 areas and functional basal ganglia cortical loops, respectively (McFarland & Haber, 2002; Haber & Calzavara 2009; Schmidt et al., 2009). Thus, information can be relayed from the limbic basal ganglia cortical loop to the motor basal ganglia cortical loop allow ing emotion to shape motor processes. Moreover the SN, as well as the STN, have been identified as potential brain structure s which will allow emotion to influence motor processes (Coombes, Corcos, Pavuluri, & Vaillancourt, submitted ; Haber, Fudge, & McFa rland, 2000 ). Specifically, it is thought that the different functional regions of the striatum (i.e., limbic, cognitive, motor) are connected via midbrain dopamine neurons, allowing the ventral limbic region of the striatum to interact with the dorsal mot or region. Hence, the collective evidence indicates that the neural circuits underlying the APAs involving cortical and subcortical structures as compared to the locomotor components of gait initiation, are more likely to be influenced by emotion. It sho uld be noted that the integration of the emotion and motor systems has been evaluated almost exclusively with simple hand movements, and/or in studies that have not differentiated between upper and lower extremity control. Importantly, voluntary movement of different body parts engages distinct and somatotopically organized sections of the primary motor cortex (Ehrsson, Geyer, & Nai to, 2003; Ghosh et al., 1987). Furthermore, different cerebral control mechanisms may exist for the planning of upper and lowe r limb movements. For example, mapping of the premotor cortex has demonstrated clear activation differences between hand and foot movements (Wheaton, Carpenter, Mizelle, & Forrester, 2008). Specifically, wrist extension movements elicited activity of the rostral ventral premotor cortex, while ankle dorsiflexion movement elicite d activation of dorsal area 6. Similarly, Luft and colleagues

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173 (2002) showed that the distribution of activation across the motor areas substantially differs for isolated elbow and kn ee movements that share mechanical properties (e.g., corresponding one dimensional joints, frequency, range). Knee movement evoked greater SMA proper activation, but less lateralization in M1 compared to the elbow movement. In contrast, other research has shown some common motor representations for isolated flexion and extension movements of the wrist and ankle in the ventral premotor area and parts of the SMA (Ehresson, Fagergren, Jonsson, et al., 1999; Ehresson, Naito, Geyer, et al., 2000). Even so, there appears to be precise effector specific mapping of motor areas related to planning. Given the distinct effector dependent representations in the motor cortices, future research may want to specify whether different linkages exist between the emotion and motor systems for upper and lower extremity movements. Furthermore, future work should investigate whether emotional input similarly modulates comparable upper and lower extremity movements. Nonetheless, our results suggest that the mechanisms integrating emotion into the motor processes that regulate gait initiation remain intact in PD patients with moderate Step E xecution As hypothesized, PD patients exhibited smaller and slower steps during the initiation of gait compared to the healthy older adults. I also predicted that exposure to the approach related erotic and happy people pictures would increase the length and velocity of the first two steps compared to all other picture categori es. The percent change scores and the HLM analyses partially supported this hypothesis. PD patients showed a greater increase in step velocity of the first step following exposure to the happy people pictures compared to the mutilation pictures (which decreased ve locity

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174 compared to ne utral). Furthermore, control participants demonstrated a greater increase in step velocity of the first step in response to the erotic, happy people, and mutilation ation pictures. In line with the hypothesis, t he HLM analyses revealed that pictures rated more pleasant relative to unpleasant led to great er velocity of the first step. These findings again mirror those of (in review) results in healthy young adults, in wh ich exposure t o pleasant images facilitated the velocity of the first step and no effect was found on the second step During the step execution phase of gait initiation, individuals achieve a velocity close to steady state velocity (Brunt et al., 1991; Elble, M oody, L effler, & Sinha, 1994). Prior research has shown that the amplitude and velocity of the posterior COP at the end of the first step. Thus, the step velocity results, which were relatively small in magnitude, may have been driven by the emotion modulation fou found following exposure to the happy people and erotic pictures likely enabled a quicker first step. While the current data collectively indic ate a lesser impact of emotion on the stepping components of gait initiation in PD patients and healthy older adults, it would be perfunctory to conclude that emotion has no impact on steady state walking in this population Prior work has shown emotional influences on steady walking in young adults (Gamble et al. in review; Michalak, Troje, Fischer, Vollmar, Heidenreich, & Schulte, 2009). For example, Gamble and colleagues found that encountering stimuli that clearly motivated a disgust emotional response (i.e., contamination) significantly

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175 shortened stride length and step velocity, whereas stimuli eliciting appetitive responses enhanced step velocity during forward walking. A number of methodological explanations may account for the different effects of e motion on the locomotor parameters in the Gamble et al. study and the present one First, t he effect of emotion on locomotion may depend on the component of gait being evaluated (i.e., planning of the initiation of gait v. regulation of ongoing gait) as we ll as the nature of the task walk as quickly Secondly, the temporal dynamics of picture presentation and walking differed between the two studies (i.e., walking at p icture offset v. w alking while viewing picture). F uture research should investigate whether emotional state impacts steady state walking in individuals with PD. Summary Collectively, the current findings indicated successful integration of the emotion and movement systems in persons with PD of moderate severity. Threatening pictures speeded the initial motor response on the gait initiation task, while the approach related pictures clearly facilitated gait initiation in all participants as evidenced by the APAs. These results support the long held premise that emotions are action dispositions (Frijda, Kuipers, & ter Schure, 1989; Lang, 1995) and further support the neurobiological evidence suggesting the emotion and motor systems are integrated in primitive brain circuits to ensure appropriate motor reactions occur in response to environmental stimuli (e.g., Pessiglione, et al., 2007; Schmidt, Clery Melin, Lafarque et al., 2009). As such, investigating the utilization of the emotion system to optimize movemen t in PD could be a promising n ew avenue for future research. Specifically, inducing pleasant emotional states to drive improvements in gait initiation may be a viable strategy to

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176 complement existing gait therapies for PD patients w ith moderate disease seve rity. These practical implications and future directions are discussed in more detail following the Limitations section. Limitations Several limitations to the current study sho uld be acknowledged. First a n imbalance of men and women existed in e ach group (3 women, > 20 men). Previous work has shown that emotional reactivity to picture stimuli as evidenced by modulation in the human motor system is similar between men and women (Coombes et al., 2008; Gamble et al., in review). Furthermore, with few excepti ons ( e.g., Bradley, Codispoti, Sabatinelli, & Lang, 2001; Sabatinelli, Flaisch, Bradley, Fitzimmons, & Lang, 2004) research has demonstrated that reactions to affective pictures in the autonomic, somatic, reflex, visual, and evaluative systems are similar between men and women. W omen occasion greater defensive reactivity to aversive cues as indexed by facial EMG activity, cardiac deceleration, and judgments of valence and arousal, whereas men are more reactive to pictures with erotic content as evidenced b y judgments of valence and arousal and skin condu ctance (Bradley et al., 2001). Given that (1) the and (2) exposure to erotic pictures drove many of the improvements in gait initiation, replication of thes e findings in a sample of female PD patients is critical to the generalizability of the results. Importantly, however, gait initiation was similarly facilitated by pictures of happy people which generate no know n gender based response differences in the e valuative, physiological, or motor systems. As such, we are reasonably confident that the current studies results would be replicated in larger sample of female older adults and PD patients.

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177 Another limitation of the study was the range of disease severit y within the current PD sample. Most PD patients were in Hoehn and Yahr stages 2 or 3 and had 41), indicating a moderate level of disease severity. The HLM analyses indicated that disease severity (UPDRS score) did not influence on gait initiation. However, this finding may be limited by the lack of patients in the severe stages of the disease as well as a lack of sufficient power at the between subj ect level for the HLM analysis. Pathological changes i n limbic structures (e.g., reduction in amygdala volume; Harding et al., 2002; Ouchi et al., 1999) and dopaminergic denervation of limbic basal ganglia pathways (Braak & Braak, 2000; German et al., 1989; Satton et al., 1982) found in patients with PD likel y incre ase as the disease progresses. Given that midbrain dopamine neurons are likely crucial to the integration of emotional information into motor circuits (Haber, 2003), future studies should include patients with a broader range of disease severity to more comprehensively examine the effect of disease progression on the successful integration of emotion into the functional motor system. A third limitation centers on the dispositional affect that character ized the sample tested herein. As previously men tioned PD is increasingly linked with emotional dysfunction particularly greater symptoms of depression and apathy (Leentjens et al., 2003; Rojo et al., 2003). Such was the case with the current sample. A growing body of research has shown that depressio n is linked to blunted physiological and motor reactivity to pleasant stimuli (Gamble, Coombes, et al., in review; Larson et al., 2007). Though the HLM analyses revealed, that levels of apathy and depression did not impact on gait initiation participants with severe levels of

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178 depression were not included in the study Our results may not, therefore generalize to severely depressed PD patients. Fourth, the data revealed a potential attentional effect of picture viewing o n gait initiation performance. Specifically COP values in the S1 region were primarily reduced in all picture categories relative to the blank condition in which no picture was viewed. Consequently the direct comparison of movement following the presentat ion of the affective pictures to the no picture condition likely reflects both attentional and emotional processes Importantly the neutral condition was considered to represent the effect of viewing the pictures without the affective component. Hence th is limitation should not compromise the impact of the should be primarily reflected in comparisons between the affective pictures and the neutral pictures (i.e., percent change scores). Future resear ch could extend the current findings by integrating attentional measures or through the use of emotion manipulations of a different modality (i.e., emotionally evocative sounds: Bradley & Lang, 2000). Additionally, a formal assessment of the COM movement during gait initiation was not conducted, preventing direct inferences to be made regarding the rel ation between the COP and COM. However, the exclusion of COM data should not detract from the contribution of the current findings. Extensive evidence exis ts for the interaction between the COP and COM during the preparatory phase of gait initiation (e.g., Breniere et al., 1987; Hass et al., 2005; Martin et al., 2002), allowing for strong inferences to be made from the COP data regarding the influence of emo tion on dynamic postural control.

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179 Practical Implications and Future Directions The findings of the current study provide several potential avenues for fu ture research. First, the results demonstrate that the presentation of pleasant emotional stimuli faci litated gait initiation in PD. Thus, further exploration of emotion manipulations as a strategy to optimize the efficacy of therapeutic interventions to improve gait disturbances may be a promising avenue for future research. For example, researchers shoul d investigate whether emotion manipulations of different modalities can produce similar changes in gait paramete rs as picture viewing methods. In particular, emotion induction techniques more easily transferable to clinical/real world settings should be ex plored, such as emotionally evocative sounds, imagery based techniques, or even virtual reality modalities C ommon neural representations are known to exist for perceiving emotion in another, feeling an emotion, and imagining an emotion (Holmes, Mathews, M ackintosh, & Dalgleish, 2008; Jabbi, Bastiaansen, & Keysers, 2008). As such, mental imagery may be a particularly effective route to modify em otion in the clinical setting. Furthermore, future research could test interventions designed to up regulate posi tive emotional experiences, as well as techniques to facilitate emotional awareness and experience. Emotion awareness and emotion regulation skills could be important, inexpensive tools that persons with PD could use to improve the quality of their movemen ts in any setting. The present study was a single acute assessment o f how emotion influences gait. While the emotion induced effects on acute bouts of gait initiation may appear to hold little clinical significance (despite their statistical significance ), future research could test a chronic intervention in which persons with PD consistently operated in a pleasant, approach oriented environment. Perhaps the cumulative effects of these small

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180 improvements in movement could lead to more clinically significa nt and observable changes over time. As such, it will also be important to investigate how clinical settings can be tailored to induce positive emotional states during gait training to maximize improvements in gait. Alternatively, comparison of gait initia tion performance on the pre and post trials may indicate that repeated heightened activation of the emotion system, regardless of the specific emotion being elicited, e nhances motor system activity. T he pre and post trial comparison was originally condu cted to ensure that participants did not experience fatigue, which could have hindered performance on the gait initiation task as the ex perimental session progressed. Interestingly, all participants improved performance from the pre trials to the post tria ls, as evidenced by greater displacement and velocity of the COP movement during the anticipatory postural adjustments, greater velocity of COP shift from the swing limb to stance limb, and longer and quicker steps. Two likely explanations may account for this change in performance from pre to post trials ; motivation to finish the experimental sessio n or physiological mechanisms. With regard to the latter possibility increased temperature or circulation from the repetitive walking trials could have reduce d myofacial restriction and increased joint motion thus allowing for increased gait initiation parameters (Prentice, 2004; Wenos & Konin, 2004) Concerning the former explanation broadly increased emotional experience was likely induced during the experim ental session. Emotions have long been described as motivational tuned states of readiness (Lang et al., 1998). R epeated activation of the emotion circuits regardless of the specific emotion elicited, may increase the intensity of an individual current motivational state. In turn, this increased level of

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181 arousal or activation could intensify activation of other response systems, thereby causing a general pattern of heighte ned motor system excitability. Perhaps gait initiation parameters, which ar e slower, smaller and less forceful in individuals with PD, can be amplified simply by prolonging or intensifying the experience of emotion. I ndividuals with PD in the advanced stage commonly experience freezing of gait ; the sudden and transient inabilit y to initiate or continue locomotion (Chee, Murphy, Danoudis, Georgi o Karistianis & Iansek, 2009). While the FOG phenomenon is one of the least understood symptoms of PD, clinicians and researchers agree that FOG does n ot occur randomly. Indeed, a potentia l trigger of freezing is thought to be intense emotional stress or threatening situations (Chee, et al., 2009; Rahman, Griffin, Quinn, & Jahanshahi, 2008; Okuma, 2006). This notion has been primarily based upon PD patient reports, rather than systematic in vestigation. The PD patients in the current study were primarily non different manner than those PD patient s in the current study. It is possible that rather than speeding the initiation of movement, threatening stimuli may induce freezing episodes. Future research needs to systematically investigate the role of emotion as a trigger for FOG in PD. A greater un derstanding of the factors that induce FOG is crucial to the optimal management of this debilitating mobility problem. Finally, i n the past decade strides have been made toward greater understanding of the mechanisms allowing emotion to influence motor pr ocesses (Coombes et al., in review; Haber, 2003; Revital et al., 2008; Schmidt et al., 2008). Nonetheless, the neural system that allows emotional reactivity to modify and guide

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182 motor behavior remains poorly understo od. Future work could manipulate neuros urgical and pharmacological techniques in persons with PD to further investigate the extent to which basal ganglia function and dopamine are integral to the integration o f emotion into motor circuits. Past research suggest s that basal ganglia pathways cons ist of two potential neural networks linking emotion and motor circuits via complex nonreciprocal connections which allow a continuous feedfo r ward mechanism of information flow from limbic to motor circuits (Haber, 2003; Haber & Calzavara, 2009). One neura l network involves parallel basal gangli thalamocortical circuits interconnected through feedfo r ward thalamic cortico thalamic pathways, while the other network functions via midbrain dopamine neurons of the striato nigral striatal pathway interconnecting the functional regions of the striatum (i. e., limbic, cognitive, motor). Individuals with PD medication and DBS of critical basal ganglia structures, such as the STN and SN. Giv en that a pathological hallmark of PD is the degeneration of dopaminergic cells, medication would provide additional confirmation for the importance of functioning dopaminergic pathways in connecting these two circuits in the brain. Additionally, con cerning the role of specific basal ganglia structures in emotion and movement integration. For information into motor systems controlling gait initiation.

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183 Conclusion The purpose of this inves tigation was to examine how emotional state alters critical gait parameters in persons wit h PD and healthy older adults. As hypothesized, patients with PD exhibited slower and diminished amplitude of movement during the gait initiation task compared with t he healthy older adults. Despite these expected between group differences, the two groups displayed comparable modulation of gait under emotionally evocative conditions, with both groups respond ing similarly to the pre sentation of emotional stimuli. Exposu re to threatening stimuli speeded the initiation of the motor response on the gait initiation task, while the approach related emotional states induced by pleasant pictures clearly facilitated the anticipatory postural adjustments needed to initiate forwar d gait. The current study provides the first evidence indicating that manipulating the activation of emotional circuits may be a viable strategy to improve the quality of g ait initiation in PD patients. With continued empirical efforts, researchers will be able to inform the development of novel emotion based interventions that may be integrated with other behavioral, pharmacological, and genetic interventions to optimize motor therapy for medication refractory gait dysfunction in PD.

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184 APPENDIX PERMISSION TO USE FIGURES Figure 2 10 ELSEVIER LICENSE TERMS AND CONDITIONS Oct 06, 2009 This is a License Agreement between Kelly M Gamble ("You") and Elsevier ("Elsevier") provided by Copyright Clearance Center ("CCC"). The license consists of your order det ails, the terms and conditions provided by Elsevier, and the payment terms and conditions. All payments must be made in full to CCC. For payment instructions, please see information listed at the bottom of this form. Supplier Elsevier Limited The Boulev ard,Langford Lane Kidlington,Oxford,OX5 1GB,UK Registered Company Number 1982084 Customer name Kelly M Gamble Customer address 1048A SW 14th Ave Gainesville, FL 32601 License Number 2283290721694 License date Oct 06, 2009 Licensed content publishe r Elsevier Licensed content publication Gait & Posture Licensed content title The initiation of gait in young, elderly, and Parkinson's disease subjects Licensed content author Suzanne E. Halliday, David A. Winter, James S. Frank, Aftab E. Patla an d Franois Prince Licensed content date August 1998 Volume number 8

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190 Figure 2 11 Attention: Springer Customer Service Please note below information pertaining to a customer request for reuse o f Springer content. This request is being forwarded to you by Copyright Clearance Center's Rightslink Service as established by Springer. Please contact the customer below regarding this request and to provide a corresponding price quote. Customer informa tion: Name: Kelly Gamble Email: mailto:kmgamble@hhp.ufl.edu Article information: Publication: Journal of Neurology Pages: 19 29 Volume number: 255 Issue number: 0 Publication date: 08/01/2008 Title: Substrat es for normal gait and pathophysiology of gait disturbances with respect to the basal ganglia dysfunction Author: Kaoru Takakusaki Order Details: Type of use: Thesis/Dissertation Requester type: Not specified Distribution/Circulation: ${CIRCULATION} Port ion Used: Figures Redirect Reason: Conent for this journal is not currently an available through Rightslink. Please contact Permissions.heidelberg@springer .com directly to submit the details of your request. Dear Ms. Gamble, Thank you for getting back to us. With reference to your request (copy herewith) to re use material on which Springer controls the copyright, our permission is granted free of charge, on the following conditions: it concerns original material which does not carry references to other sources, if material in question appears with credit to another sourc e, authorization from and reference to that source is required as well, permission is also obtained from the author (address is given on the imprint page or with the article); allows you non exclusive reproduction rights throughout the world, permiss ion includes use in an electronic form, on the condition that content is password protected, at Intranet or in CD ROM/E book;

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191 full credit (journal title, volume, year of publication, page, chapter/article title, name(s) of a uthor(s), figure number(s), original copyright notice) is given to the publication in which the material was originally published by adding: With kind permission of Springer Science+Business Media. Permission free of charge does not prejudice any rights w e might have to charge for reproduction of our copyrighted material in the future. Kind regards, Alice Essenpreis Springer Rights and Permissions Tiergartenstrasse 17 | 69121 Heidelberg GERMANY FAX: +49 6221 487 8223 permissions.Heidelberg@springer.com www.springer.com/rights From: "Gamble,Kelly M" >> To: >> Date: 2010 06 10 22:48:27 >> Subject : kusaki@asahikawa med.ac.jp >> >> Hi Dr. Takakusaki, >> >> I would like to get your permission to use a figure in one of your articles in the literature review (Chapter 2) in my dissertation. The dissertation will be available electronically online to Faculty and students at the University of Florida, who it is published through. I have obtained permission from the publisher of the article, Springer Science+Business (the below email). Now I just need permission from you. The article is Takakusaki, To mita, & Yano, 2008. Substrates for normal gait and pathophysiology of gait disturbances with respect to the basal ganglia. Journal of Neurology, 255, Suppl 4. I would like the permission to use Figure 4 on page 25 in my dissertation. >> >> Thank you, >> Kelly Gamble Re: kusaki@asahikawa med.ac.jp Hello, Kelly Gamble This is Kaoru Takakusaki, Off course! YES. Please use the figure in the paper. Please let me know if you need my assistance. All the best, Kaoru

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223 BIOGR APHICAL SKETCH Kelly Gamble was born in Fort Wayne, IN in 1979, to Mariette and Gary Gamble. Growing up, Kelly was taught that through hard work and a positive attitude she could b e successful in all endeavors. nabled her to be succ essful in her academic career. Kelly graduated from Scecina Memorial High school in 1997 as valedictorian of her class. Kelly went on to earn a BS in psychology and MA in clinical psychology from t he University of Indianapolis. Kelly t hen enrolled at Ball State University, where she earned a MS i n physical e ducation with a speci alization in sport psychology. Kelly attended the University of Florida to complete her PhD in health and human p erformance in 2006. While pursuing her doctorat e, Kelly has worked as a research assistant in the Performance Psychology lab and was blessed with great mentors who supported this dream of becoming a Doctor of Philosophy.