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Attentional Resource Allocation and Swallow Function in Parkinson's Disease

Permanent Link: http://ufdc.ufl.edu/UFE0041073/00001

Material Information

Title: Attentional Resource Allocation and Swallow Function in Parkinson's Disease
Physical Description: 1 online resource (107 p.)
Language: english
Creator: Troche, Michelle
Publisher: University of Florida
Place of Publication: Gainesville, Fla.
Publication Date: 2009

Subjects

Subjects / Keywords: aspiration, attention, disease, dual, parkinsons, penetration, swallow, task, videofluoroscopy
Communication Sciences and Disorders -- Dissertations, Academic -- UF
Genre: Communication Sciences and Disorders thesis, Ph.D.
bibliography   ( marcgt )
theses   ( marcgt )
government publication (state, provincial, terriorial, dependent)   ( marcgt )
born-digital   ( sobekcm )
Electronic Thesis or Dissertation

Notes

Abstract: The goal of this study was to test whether swallow safety could be disrupted by increasing cognitive demands during the motor task of swallowing. To achieve this end, twenty participants with Parkinson s disease (PD) and dysphagia were tested completing a dual task experimental paradigm under videofluoroscopy. Results revealed that there were differential effects to swallow safety based on baseline scores on measures of cognitive flexibility and attention. Participants who were mildly impaired in cognitive flexibility and attention demonstrated cognitive-motor interference with worsening of both swallow and cognitive performance. Participants who were most impaired in the domains of cognitive flexibility and attention actually had improvements in swallow safety in the dual task condition. Additionally, decreased swallow timing durations were found overall when comparing single and dual task conditions, but no significant changes were found in measures of airway coordination. The results of this study support the hypothesis that fronto-limbic top-down drive can influence the swallow plan resulting in changes to swallow performance (in this case, swallow safety). Future studies should focus on further specifying the cognitive mechanisms influencing the swallow plan and focus on use of cognitive targets for the treatment of swallow dysfunction.
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 Michelle Troche.
Thesis: Thesis (Ph.D.)--University of Florida, 2009.
Local: Adviser: Sapienza, Christine M.

Record Information

Source Institution: UFRGP
Rights Management: Applicable rights reserved.
Classification: lcc - LD1780 2009
System ID: UFE0041073:00001

Permanent Link: http://ufdc.ufl.edu/UFE0041073/00001

Material Information

Title: Attentional Resource Allocation and Swallow Function in Parkinson's Disease
Physical Description: 1 online resource (107 p.)
Language: english
Creator: Troche, Michelle
Publisher: University of Florida
Place of Publication: Gainesville, Fla.
Publication Date: 2009

Subjects

Subjects / Keywords: aspiration, attention, disease, dual, parkinsons, penetration, swallow, task, videofluoroscopy
Communication Sciences and Disorders -- Dissertations, Academic -- UF
Genre: Communication Sciences and Disorders thesis, Ph.D.
bibliography   ( marcgt )
theses   ( marcgt )
government publication (state, provincial, terriorial, dependent)   ( marcgt )
born-digital   ( sobekcm )
Electronic Thesis or Dissertation

Notes

Abstract: The goal of this study was to test whether swallow safety could be disrupted by increasing cognitive demands during the motor task of swallowing. To achieve this end, twenty participants with Parkinson s disease (PD) and dysphagia were tested completing a dual task experimental paradigm under videofluoroscopy. Results revealed that there were differential effects to swallow safety based on baseline scores on measures of cognitive flexibility and attention. Participants who were mildly impaired in cognitive flexibility and attention demonstrated cognitive-motor interference with worsening of both swallow and cognitive performance. Participants who were most impaired in the domains of cognitive flexibility and attention actually had improvements in swallow safety in the dual task condition. Additionally, decreased swallow timing durations were found overall when comparing single and dual task conditions, but no significant changes were found in measures of airway coordination. The results of this study support the hypothesis that fronto-limbic top-down drive can influence the swallow plan resulting in changes to swallow performance (in this case, swallow safety). Future studies should focus on further specifying the cognitive mechanisms influencing the swallow plan and focus on use of cognitive targets for the treatment of swallow dysfunction.
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 Michelle Troche.
Thesis: Thesis (Ph.D.)--University of Florida, 2009.
Local: Adviser: Sapienza, Christine M.

Record Information

Source Institution: UFRGP
Rights Management: Applicable rights reserved.
Classification: lcc - LD1780 2009
System ID: UFE0041073:00001


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1 ATTENTIONAL RESOURCE ALLOCATION AND SWALLOW FUNCTION IN PARKINSONS DISEASE By MICHELLE SHEVON TROCHE-MORENO A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORID A IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2009

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2 2009 Michelle Shevon Troche-Moreno

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3 To all those who have journeyed with me on the road to graduation: your faithfulness and love have not gone unnotic ed. This document is dedicated to each of you.

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4 ACKNOWLEDGMENTS It takes a village seems to fall short as I write these acknowledgm ents. I have been immensely blessed throughout my educational trajectory with amazing people who have been placed in my path; people who have changed my professional and personal life in ways which I cannot begin to express in these few words. To God I am thankful for the grace given each of t hose special people and given me during this journey. I must thank my parents who always advised that I should stay in school until I ran out of degrees and who provided me with all the lo ve, guidance, and care that I would need to achieve that end. To my brother, who is my greatest pride, I give many thanks for standing close during every peak and valley, especially in the last sprint towards this degree. The roller coaster would never have been bearable or as enjoyable without him. Many thanks to Lali and Heather, for listening ears, giving hearts, and for being pillars during this process; I am eternally grateful to both of them. I must also thank Bethany, Leidi, Vivi and the rest of t he corillo through whom I have learned many invaluable life lessons; especially the true definit ion of work hard, play hard. For every moment of escape and for your selflessness I am so thankful. Y ou are much more than friends, you are family. Many thanks go out to the small army of graduate students: Lauren, Sarah, April, Katie, and Stacie, who made data acquisition possible, a joy, and seamless for the participants. I am also thank ful to my labmates, the exc eptional women of the laryngeal function lab (past and present), who poured so many resources into making my completion of this document possible, thei r friendship and support have been invaluable through the years. Much apprec iation to my dissertation co mrade and partner in crime,

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5 Christina del Toro, who is the best classm ate, roommate, and friend any nerd could ask for. My heartfelt thanks go to my dissertati on committee, the members of which have seen me grow from an eager undergraduate, to an excited Masters student with many questions, to a doctoral candidate and studen t. The educational journey would never have been as fruitful as it was without their diehard support and guidance. To Christine Sapienza I give many thanks. She always sa w potential in me and provided me with all the resources I would need to have a well-rounded educational experience: she has been much more than a scientif ic mentor, she has been a fr iend. I look forward to many more years of collaborat ion and friendship. To Jay Rosenbek, I am appreciative for all the lessons learned as a student and o ffice mate, through him I have been taught the delicate balance of mixing science and heart into every research and clinical experience. In Lori Altmann I found a mentor who helped me learn the language lingo and whose statistical expertise and empathetic, caring spirit were essential to my formation as a researcher. Since I stepped foot on Movement Disorders soil Michael Okun was available to assist in every research endeavor. His willingness to offer expertise and resources was essential to the successful completion of this project. Very special thanks also go to the parti cipants and families who were enrolled in this study. It was their willingness and openness to research which made this project possible and a joy to complete.

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6 TABLE OF CONTENTS page ACKNOWLEDG MENTS .................................................................................................. 4LIST OF TABLES ............................................................................................................ 9LIST OF FIGURES ........................................................................................................ 10LIST OF ABBR EVIATIONS ........................................................................................... 11ABSTRACT ................................................................................................................... 13 CHA PTER 1 INTRODUCTION AND REVI EW OF LITERATURE ............................................... 15Swallow Fu nction .................................................................................................... 15Physiology of H ealthy Sw allow ......................................................................... 15Neural Substrates of Swallow ........................................................................... 16Respiratory-Swallo w Relations hips .................................................................. 20Sensation and Swallowing ................................................................................ 20Cognition and Swallowing ................................................................................ 22A Proposed Theoretical Framework of Sensorimotor Sw allow Control ................... 24Cognitive-Affective Input ................................................................................... 25Swallow Plan .................................................................................................... 28Swallow Execution ........................................................................................... 28Central Pattern Generator (CPG ) ..................................................................... 29Feedback .......................................................................................................... 29Swallow Framework in a Pathological Model .......................................................... 30Parkinsons Dis ease (Gener al) ......................................................................... 31Parkinsons Diseas e and Dysphagia ................................................................ 32Parkinsons Diseas e and Cogn ition .................................................................. 34Cognitive-Affe ctive In put ............................................................................ 36Swallow Plan .............................................................................................. 37Swallow Execution ..................................................................................... 38Feedback ................................................................................................... 38Swallow Framework: Influences on Evaluation and Management of Dysphagia .... 39Evaluation of Swa llowing Disor ders ................................................................. 39Cognitive-Affe ctive In put ............................................................................ 40Swallow Planning ....................................................................................... 40Swallow Execution ..................................................................................... 40Feedback ................................................................................................... 40Treatment of Swallowing Disor ders .................................................................. 40

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7 Specific Aims and Hypothes es ............................................................................... 41Specific Aim 1 ................................................................................................... 42Specific Aim 2 ................................................................................................... 42Explorator y Aim ................................................................................................ 432 METHODS .............................................................................................................. 49Participants ............................................................................................................. 49Inclusion/Exclus ion Crit eria .............................................................................. 49Diagnosis and Clinical Assessment of PD ........................................................ 50Research Design .................................................................................................... 50Overvi ew .......................................................................................................... 50Phase 1: Cognitive Testing Pr ocedures ........................................................... 50Training on experimental proc edures ............................................................... 53Phase 2 : Experiment al Proc edures ................................................................. 53Videofluoroscopi c procedur es .................................................................... 53Cognitiv e task ............................................................................................ 54Motor task .................................................................................................. 54Dual ta sk .................................................................................................... 55Data Analysis and Outcome Meas ures ................................................................... 55Primary Outcome : Swallow Sa fety .................................................................. 56Physiological Measures of Swa llow Timing and C oordination .......................... 56Measures of Sw allow Ti ming ............................................................................ 56Measures of Airw ay Coordi nation ..................................................................... 57Dual Task Response ........................................................................................ 57Reliabi lity .......................................................................................................... 58Statistical Analyses ................................................................................................. 59Reliabi lity .......................................................................................................... 593 RESULTS ............................................................................................................... 66Reliabi lity ................................................................................................................ 66Baseline Cognitive Measures ................................................................................. 66Primary Outcome: Penetra tion-Aspirati on Scor e .................................................... 66Comparison of Single versus D ual Task........................................................... 66Dual Task Response ........................................................................................ 66Baseline Cognitive Function by Dual Ta sk Response ...................................... 67Secondary Outcome ............................................................................................... 68Swallow Timing ................................................................................................ 68Airway Coor dination ......................................................................................... 68Explorator y Aim ...................................................................................................... 684 DISCUSSI ON ......................................................................................................... 74Dual Task Effects on Swallow Sa fety ..................................................................... 75Dual Task Effects of Swallow Timing and Airway Coordination .............................. 78

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8 Implications for the Proposed Framew ork Of Sensorimotor Oropharyngeal Swallo wing ........................................................................................................... 81Implications for Evaluation and Treatment of Dysphagia ........................................ 82Strengths and Li mitations ....................................................................................... 85Future Re search ..................................................................................................... 87Summary ................................................................................................................ 88LIST OF RE FERENCES ............................................................................................... 91BIOGRAPHICAL SKETCH .......................................................................................... 107

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9 LIST OF TABLES Table page 2-1 Demographic information, including sex, age, UPDRS, Hoehn & Yahr (H & Y) score, years since diagnosis (PD Dx), and education for each participant. Compiled from medical record review and responses from participant inquiry. .. 602-2 List of stimuli used for each participant during the experimental dual task paradigm completed under videofluorosc opy during phase II of the study. ........ 612-3 Penetration-Aspiration Scale (Ros enbek, et al., 1996) used as the primary outcome m easure. .............................................................................................. 622-4 Measurement tags of physiological swallow f unction completed by the principal investigator who was blinded to participant identity and experimental dual/single task condition. Measur es of swallow timing and airway coordination were deriv ed from thes e tags. ........................................................ 632-5 Description of calculations used to derive swallow timing measures from swallow event tags descr ibed in Tabl e 2-4. ........................................................ 632-6 Description of calculations used to derive airway coordination measures. Both calculations and definitions of measures are delin eated. ........................... 643-1 Raw scores, means, and standard deviations for baseline cognitive measures (i.e. Dementia Rating Scale, Stroop XXXs & color words, digit span forward (DSF), digit span backward (DSB), digit ordering (DO), Trails A & B) .................................................................................................................... 693-2 Average PA scores for each participant, along with group means and standard deviations. ........................................................................................... 703-3 Differences scores (single minus dual task) and corresponding groups by participant for cognitive and swallo w tasks. For response code, 1=no change, 2=worsened, 3=impr oved ..................................................................... 713-4 Means, standard deviations, significance based on Kruskal Wallis nonparametric statistical analyses of score s on baseline cognitive scores by dual task respons e groups. ........................................................................................ 723-5 Means, standard deviations and pvalues for swallow timing measures by conditi on. ............................................................................................................ 733-6 Means, standard deviations and pvalues for airway coordination measures by condi tion. ....................................................................................................... 73

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10 LIST OF FIGURES Figure page 1-1 Proposed theoretical fram ework of sensorimotor sw allow control whereby the CPG represents the patterned brainstem control of swallow and the domains of 1) cognitive-affective input, 2) swallo w plan, 3) swallow exec ution, and 4) feedback are proposed to understand the mechanisms modulating swallow functi on. .............................................................................................................. 441-2 Neural correlates of the proposed framework of sens orimotor swallow control. ................................................................................................................ 451-3 A proposed fram ework of sensorimotor swallo w control: a PD pathological model. It is proposed that PD results in changes of all the domains of the proposed fram ework. .......................................................................................... 461-4 A proposed framewor k of sensorimotor swallo w control: Evaluation of Dysphag ia. ......................................................................................................... 471-5 A proposed framewor k of sensorimotor swallo w control: Treatment of Dysphag ia. ......................................................................................................... 482-1 Still radiographic image representing one frame of sw allow sequence (lateral view) as visualized on the Kay Elemetrics Digital Swallow Station program. ..... 654-1 The results of t he current study overlaid on the proposed model of sensorimotor orophar yngeal d ysphagia .............................................................. 90

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11 LIST OF ABBREVIATIONS PD Parkinsons disease CPG Central pattern generator EEG Electroencephalogram SMA Supplemental motor area fMRI Functional magnetic resonance imaging DSG Dorsal swallow group VSG Ventral swallow group NTS Nucleus tractus solitarius NA Nucleus ambiguous UES Upper esophageal sphincter L-Dopa Levodopa VFES Videofluoroscopic evaluation of swallowing EMST Expiratory muscle strength training PA score Penetration-aspiration score VAMC Veterans Administration Medical Center UPDRS Unified Parkinsons Disease Rating Scale H&Y score Hoehn & Yahr score DBS Deep brain stimulation MDC Movement Disorders Centers UK United Kingdom BRRC Brain Rehabilitation Research Center UF University of Florida DRS Dementia Rating Scale

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12 SPSS Statistical Package for the Social Sciences Dx Diagnosis OOT Onset oral transit BHR Bolus head passed ramus of the mandible BTR Bolus tail passed ramus of the mandible BV Bolus at vallecula AEE Arytenoids elevate AEC Arytenoid cartil age contacts epiglottis OTT Oral Transit Time PTT Pharyngeal Transit Time TSD Total Swallow Duration DSF Digit span forward DSB Digit span backward DO Digit Ordering

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13 Abstract of Dissertation Pr esented to the Graduate School of the University of Florida in Partial Fulf illment of the Requirements for t he Degree of Doctor of Philosophy ATTENTIONAL RESOURCE ALLOCATION AND SWALLOW FUNCTION IN PARKINSONS DISEASE By Michelle Shevon Troche-Moreno December 2009 Chair: Christine M. Sapienza Major: Communication Sciences and Disorders The goal of this study was to test whether swallow safety could be disrupted by increasing cognitive demands during the motor ta sk of swallowing. To achieve this end, twenty participants with Parkinsons di sease (PD) and dysphagia were tested completing a dual task experimental par adigm under videofluoroscopy. Results revealed that there were differential effects to swallow safety based on baseline scores on measures of cognitive flexibility and attenti on. Participants who were mildly impaired in cognitive flexibility and attention dem onstrated cognitive-motor interference with worsening of both swallow and cognitive per formance. Participants who were most impaired in the domains of cognitive flex ibility and attention actually had improvements in swallow safety in the dual task condition. Additional ly, decreased swallow timing durations were found overall when compar ing single and dual task conditions, but no significant changes were found in measures of airway coordination. The results of this study support the hypothesis that fronto-limbic top-down dr ive can influence the swallow plan resulting in changes to swallow performanc e (in this case, swallow safety). Future studies should focus on further specifyi ng the cognitive mechanisms influencing the

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14 swallow plan and focus on use of cognitive targets for the treatment of swallow dysfunction.

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15 CHAPTER 1 INTRODUCTION AND REVI EW OF LITERATURE Dysphagia, or disordered swallowing, can lead to significant deterioration of health and quality of life. Of particular concern is the associated ri sk of aspiration or ingestion of foreign particles into the airway, a pot ential cause of aspiration pneumonia resulting in high morbidity and mortalit y (Langmore, Skarupski, Park, & Fries, 2002; Langmore, et al., 1998). Studies suggest t hat 40% of adults aged 60 year s and older have dysphagia (Doggett, Turkelson, & Coates, 2002; Feinberg, Knebl, Tully, & Segall, 1990). Additionally, pneumonia is the 5t h leading cause of death in persons 65 years or older and the 3rd leading cause of death in perso ns 85 years and older (LaCroix, Lipson, Miles, & White, 1989). In fa ct, aspiration pneumonia is oft en the leading cause of death in persons with neurodegenerative diseases including Parkinsons disease (PD; Fernandez & Lapane, 2002; Gorell, Peterson, Rybicki, & Johnson, 2004; Hoehn, 1967; Shill & Stacy, 1998; Singer, 1992) By the year 2010 an esti mated 18 million adults will require care for dysphagia-re lated impairment (Feinberg, et al., 1990; Robbins, et al., 2008). Despite the staggering statistics, ther e is an incomplete understanding of the mechanisms underlying swallow function and dysfunction, its assessment, and management. A more comprehensive unders tanding of these mechanisms should result in improved assessment and manage ment techniques for dysphagia. Swallow Function Physiology of Healthy Swallow Swallowing is a complex process during whic h the bolus, a cohesive mass of food/liquid, is successfully tr ansported from the oral cavity to the esophagus and into the stomach. Traditionally the proce ss of swallowing has been considered to be

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16 comprised of three main phases: 1) the oral phase, 2) pharyngeal phase, and 3) esophageal phase. The oral phase can be par sed into the oral-preparatory and oral transit phases (Perlman, Booth, Grayhack, 1994). In the oral -preparatory phase, food is brought to the mouth and manipulated in the oral cavity preparing the bolus for swallowing (Kahrilas & Logemann, 1993). The oral transit phase follows with transport of the bolus to the oropharynx (Blitz er, 1990; Dodds, Stewart, & Logemann, 1990). More specifically, the tongue tip elevates or dips, the soft palate raises, and the posterior tongue depresses (Dodds, et al., 1990; Shaker, Cook, Dodds, & Hogan, 1988). Classically, these swallow phase ha ve been considered to be under voluntary control (e.g., Leopold & Kagel, 1983). The pharyngeal phase involves various laryngeal airway protective mechanisms incl uding adduction of the true and false vocal folds and inversion of the epiglottis, ultimately resulting in transport of the bolus from the oropharynx, passed a closed laryngeal ve stibule, and through the upper esophageal sphincter (Logemann, 1983; Perlman & Christensen, 1997). During the esophageal phase peristalsis transports the bolus thro ugh the esophagus and into the stomach (Logemann, 1983). The latter tw o stages are classically considered to be under involuntary control, but there is a literature to suggest t hat voluntary mechanisms can influence these phases (Leopold & Kagel 1997a; Leopold & Kagel, 1983; Logemann, 1983; McGuire & Rothenberg, 1986; Pimental & Kingsbury, 1989), at least in part. Neural Substrates of Swallow From initiation to completion, swallowin g is a patterned sensorimotor process controlled by both automatic and volitional control system s within a complex neural network (Hamdy, et al ., 1996; Hamdy, et al ., 1999; Hamdy, Xue, Valdez, & Diamant, 2001; Martin, Goodyear, Gati, & Menon, 2001; Ma rtin & Sessle, 1993; Mosier, et al.,

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17 1999; Zald & Pardo, 1999). Literature s uggests the involvement of the cortex, subcortical structures, brai nstem, and cerebellum in the production of a healthy, safe swallow. Studies have reported activation of neural structures including the cingulate cortex, insula, inferior frontal gyrus, s upplementary motor area, sensorimotor cortex, supplementary sensory area, premotor co rtex, antereolateral and posterior parietal cortex, basal ganglia, thalamus, and cerebellum (Hamdy, et al., 1996; Hamdy, et al., 1999; Hamdy, et al., 2001; Martin, et al., 2001; Martin, Murray, Kemppainen, Masuda, & Sessle, 1997; Martin & Sessle, 1993; Mosier, et al., 1999; Zald & Pardo, 1999) as well as indirect pathways between cortical mo tor planning regions and lower motor neurons (Huckabee, Deecke, Cannito, Gould, & Mayr, 2003). These data have been accepted in part, but not without controve rsy as some of the activation identified in these studies may be representative of innervations of the tongue and face which are not necessarily specific to swallowing (Martin, et al., 2001). Cortical areas (e.g. inferior fr ontal gyrus, supplementary motor area, sensorimotor cortex, supplementary sensory area, premotor cortex antereolateral and posterior parietal cortex) involved in sw allowing have been implicat ed in sensorimotor integration, motor planning, and execution of t he swallow. The function of subcortical structures for swallowing is le ss clear, but these are considered essential for refining the swallow pattern. The thalamus, for instance, is bilaterally activated during swallowing (Malandraki, Sutton, Perlman, Karampinos, & Conway, 2009) and it is considered that this activation is suggestive of sensory and motor input processing through thalamic connections with cortical and striat al structures resulting in tr ansfer of this information to higher cortical structures (Mosier, et al., 1999; Simonyan, Saad, Loucks, Poletto, &

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18 Ludlow, 2007). Pharyngeal stage components of swallowing, specifically laryngeal closure, result in yet higher activation of subc ortical areas (i.e. posterior insula). Albeit limited evidence, Malandrak i and colleagues (2009) suggest that more automatic components of swallowing rely more heavily on subcortical networks. Additionally, the insular cortex, also highly activated during swallowing, has been c onsidered essential to sensory-motor integration between primary cortical and subcortical sites (Augustine, 1996; Mosier, et al., 1999). Mosier and colleagues (1999) also described the importance of the insular co rtex to regulation of kinem atic movement and temporal sequencing of events during swallowing. Studies describing the neural substrates of swallowing have not parsed out the effects of motor planning/progra mming from motor execution; this may be due in part to the complex interaction of t hese processes and their interact ion with the central pattern generator (CPG; which will be further described below). Huckabee and colleagues (2003) investigated cortical activation during swallow planning versus swallow execution using electroencephalography (EEG) in 20 healthy older adults through identification of a premotor potential. EEG activity was found in the supplementary motor cortex with a rapid declination before the initiation of movement, suggesting the role of the supplemental motor area (SMA) during swallo w planning. Malandraki and colleagues (2009) addressed swallow plann ing vs. execution in an experimental design using functional magnetic resonance imaging (fMRI) during swallowing and throat clearing tasks. Their results supported those of previous studies fi nding activation of pericentral and perisylvian areas, the cingulate gyrus, the insula, the thal amus, premotor and prefrontal regions, parieto-occipital areas, and the cerebellum during swallow (Hamdy et

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19 al., 1999; Hartnick, et al., 2001; Kern et al ., 2001a,b; Martin et al., 2001, 2004, 2007; Mosier & Bereznaya, 2001; Mosier et al ., 1999; Suzuki et al., 2003; Toogood et al., 2005; Zald & Pardo, 1999). There were no statistical differences in activation during the planning (throat clearing, tongue tapping) and the execution of the swallow. Further support for the presence of a swallow plan is the occurrence of swallow specific apraxia most commonly occurring in persons with stroke (Daniels, 2000; Robbins & Levin, 1988; Robbins, Levine, Maser, Rosenbek, & Kempster, 1993). Unique from other motor acts, swallo wing can occur independent of cortical control. Decerebrate animals are able to sustain functional swallowing patterns (Janczewski & Karczewski, 1990; Mitchell & Berger, 1975; Zheng, Barillot, & Bianchi, 1991). This is attributed to the presence of a CPG for swallowing located in the brainstem (Yajima & Larson, 1993). CPGs are groups of neurons which can fire in a rhythmic and patterned manner independent of sensory or central input. The swallow CPG is hypothesized to be made up of two distinct groups of neurons, the dorsal swallow group (DSG) in the rostrocaudal nucleus tractu s solitarius (NTS) and the ventral swallow group (VSG) in the nucleus ambiguous (NA; Broussard & Altschuler, 2000a, 2000b; Zheng, et al., 1991) It appears that the DSG are a group of premotor neurons which send information to the VSG whic h then transmit information to selected cranial and spinal motor nuclei resulting in the execution of the swallow (Wheeler & Sapienza, 2005). Further description of the CPG is to follow. The swallowing and respiratory CPGs are in clos e proximity within the brainste m, likely improving efficiency and coordination of swallo w and respiration.

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20 Respiratory-Swallow Relationships Sharing upper airway anatomic and neur o-anatomic space, respiratory and swallow functions are intricately linked. Both respiratory and swallow function are susceptible to modification based on changes to oropharyngeal and laryngeal structures. To date, the majority of the literature assessing respiratory-swallow relationships has focused on respiratory pat tern during swallow; most often assessed through the use of nasal cannulas during vid eofluoroscopic evaluation. These studies suggest that although the swa llow can be triggered during the inspiratory or expiratory phases of respiration, the vast majority of people expire prior to swallowing and end the swallow with expiration (Fer oah, et al., 2002; Klahn & Perlm an, 1999; Martin-Harris, et al., 2005; Martin-Harris, Brod sky, Price, Michel, & Walt ers, 2003; Martin, Logemann, Shaker, & Dodds, 1994; Perlman, He Barkmeier, & Van Leer, 2005). There is also mounting evi dence that sensory information from the upper airways influences lung volume and subglottal pre ssure during swallowing. Wheeler and colleagues (Wheeler Hegland, Huber, Pitts, & Sapienza, 2009) found that lung volume at swallow onset ranges from 50 55% vi tal capacity in healthy young adults, and remains unchanged during effortful swallow (W heeler, 2007). Lung volume initiation is higher for thin boluses than thick boluses. Additionally, swallow safety improves with increased subglottal pressure during swallo w (Gross, Steinhauer, Zajac, & Weissler, 2006). The effects of perturbati ons to these factors are not we ll understood as of yet. Sensation and Swallowing An exquis itely coordinated process, sw allowing is an integrated sensory-motor experience, and therefore is highly modifiable based on sensory input. Sensory receptors responsible for identifying changes in taste, smell, visual appearance, and

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21 temperature, in addition to mechanoreceptor s which identify changes in the respiratory and deglutitive systems, among others, are likely responsible for modifying the motor act of swallowing (Ding, Logemann, Larson, & Rademak er, 2003; Gross, Atwood, Grayhack, & Shaiman, 2003; Gross, et al ., 2006; Hiss, Strauss, Treole, Stuart, & Boutilier, 2004; Logemann, et al., 1995; Mistry, Rothwell, Thompson, & Hamdy, 2006; Sciortino, Liss, Case, Gerritsen, & Katz, 2003). There is evidence, that increasing bolus volume, viscosity, and changing taste will result in physiological changes of the swallowing act (Chee, Arshad, Singh, Mistry, & Hamdy, 2005; Dantas & Dodds, 1990; Ertekin, et al., 1997; Kuhl emeier, Palmer, & Rosenber g, 2001; Leow, Huckabee, Sharma, & Tooley, 2007; Raut, McKee, & Johns ton, 2001; Shaker, et al., 1993; Smith, Logemann, Burghardt, Zecker, & Rademaker 2006; Troche, Sapienza, & Rosenbek, 2008; Wheeler Hegland, et al., 2009). Additionally, changes in lung volume and respiratory pattern also result in functional changes to swallow (Gross, Atwood, et al., 2003; Gross, et al., 2008; Gr oss, Atwood, Ross, Olszewski & Eichhorn, 2009; Gross, Mahlmann, & Grayhack, 2003; Gross, et al., 2006; Wheeler Heglan d, et al., 2009; Wheeler, 2007). While the data suggest that t he swallow motor plan/program is highly plastic and modifiable based on sensory informa tion; significant empirical study is needed. This is of particular importanc e as changes in bolus consistency and stimulation of oral structures are often utilized in clinical practice for improvement of swallow function (Bulow, Olsson, Ekberg, 2003; Dantas & Dodds, 1990; Kendall, Leonard, McKenzie, 2001; Kuhlemeier, Palmer, Rosenberg, 2001; Power, Fraser, et al., 2006; Troche, Sapienza & Rosenbek, 2008).

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22 Cognition and Swallowing The influence of cognitive systems on motor functioning has recently garnered signific ant research interest (e.g., Bensoussan, et al., 2007; Plummer-D'Amato, et al., 2008; Singhal, Culham, Chinellato, & G oodale, 2007; Yogev-Seligmann, Hausdorff, & Giladi, 2008). There is some literature, mainly deductive in nature, describing the effects of cognitive changes on swallow fu nction, with an emphasis on the influence of cognition on the oral-preparat ory phase of swallowing. T hese changes include, but are not limited to, the development of hyperphagia and feedi ng aversion secondary to impulsiveness, altered attention, disinhibition, and poor judgmen t (Leopold & Kagel, 1997a; Leopold & Kagel, 1983; Logemann, 1983; McGuire & Rothenberg, 1986; Pimental & Kingsbury, 1989). Very little controlle d investigation exists into the effects of cognitive processes on the pharyngeal phase of swallow, and only one study has empirically tested the effects of varying co gnitive load on any phase of swallow. There is one study which experimentally ex plored the involvement of attentional processes on oral-pharyngeal swallowing and reaction times utilizing a dual task paradigm. There was no inclus ion of videofluoroscopy or other more direct swallow visualization measures. The results of this study (Brod sky, 2006), a dissertation which is not yet published, demonstrated differentia l changes in swallow function during single and dual task conditions. Baseline durational measures of oral-preparatory and oropharyngeal phases of swallow were comp leted (single task condition). Following this, a dual task condition was completed du ring which participants listened for a target non-word presented aurally while swallowing 5 ml of water from a cup. These aural stimuli were presented during the oral -preparatory and oropharyngeal phases of swallow. Durational measures of oral -preparatory and oropharyngeal phases and

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23 reaction times revealed that the oral-pr eparatory phase was more highly influenced by changes in attention than was the oral-pharyngeal phase of sw allow, but both the oralpreparatory and oropharyngeal phases of swallowing increased in duration during the dual task condition. The paradigm used in th is study had durational measures of oralpreparatory and oropharyngeal phas es of swallow and reacti on time as its primary outcomes. Additionally, no meas ures of swallow safety were completed. Despite this, the results suggest that although the pharyngeal phase of swallow has long been considered reflexive it can be influenced by other mechanisms, including cognition, as evidenced by increased latency in r eaction times during the pharyngeal phase and differential effects on dur ational measures. Other evidence supporting the involvement of cognitive systems during swallow include the activation of fronto-cortical stru ctures during swallowing (Earles, Vardaxis, & Koceja, 2001; Martin, et al., 1999) and the presence of dysphagia in persons with cognitive disorders, independent of neuromuscular deficit (Langmore, Olney, LomenHoerth, & Miller, 2007). Nonetheless, direct empirical study testing the influence of cognitive factors on the pharyngeal phase of swallow specifically has not been completed to date. A more complete understanding of t he mechanisms underlying a healthy vs. dysfunctional swallow along with the development and testing of evidence/physiologically-based treatment paradigms for dys phagia is hindered by the absence of a model/framework of swallow functi on. Currently there is no framework of sensorimotor swallow control which acc ounts for both motor and nonmotor aspects of swallowing; more specifically, cognitive functioning, motor planning/programming, motor

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24 execution, and sensory feedback. The following section wil l elaborate on the development of a proposed framework for studying swallow func tion. A Proposed Theoretical Framework of Se nsorimotor Swallow Control The proposed framework presented here (Fi gure 1-1) is based on the literature related to healthy swallow physiology and that from participants with dysphagia. The motor control literature with specific att ention to motor speech and Van der Merwes model of speech production was also util ized to shape the proposed framework (Van der Merwe, 1997). Such a model has utilit y for the description of healthy swallow processes. A sound theoretical framework is also necessary for the characterization and appropriate management of pathological swallow sens orimotor control; issues which will be expounded upon later in this c hapter. The following section will provide information regarding: 1) the function of each of the specified domains comprising the framework; 2) the literature to support the presence of thes e domains; and 3) the neural areas which likely contribute to the function co mpleted by each domain. It is important to note that the proposed framework is theor etical and hypothetical and as such, there are many unanswered questions whose solutions will provide further support for the proposed domains and insight related to the factors influencing the domains. This theoretical framework of swallow function includes four main domains: 1) cognitive-affective; 2) swallow plan; 3) swa llow execution; and 4) CPG. The influence of feedback throughout the swallow syst em is also specified. Each of the domains will be explained in further detail below Arrows indicate the possi bility of top down and bottom up processing. This framework allows for the production of swa llow independent of cortical control: CPG to Execution and swallowing influenced by cortical control which

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25 would involve Cognitive-Affective Input Motor Planning and Execution the latter of which are also influenced by the presence of the CPG. Cognitive-Affective Input Literature suggests that limbic drives are essential to the development and implement ation of motor goals; processes which likely take place in the higher association cortex (Brooks, 1986). The fronto-limbic syst ems which are essential to various cognitive processes may gain a ccess to the motor systems via the nucleus accumbens (Mogenson, Jones, & Yim, 1980). In an alert and awake person, cognitiveaffective input (including motivation, awar eness, etc) will influence the drive for swallowing. There is evidence of dementia inducing dysphagia (Langmor e, et al., 2007) and clinically it seems that mood, arousal, memory, at tention and other cognitiveaffective factors often influence swallow performance. Additi onally, persons with swallow dysfunction may develop marked fear or anxiety of swallowing resulting in changes to swallow function (i.e. posturing of swallow structures, aversion; adverse reactions to eating or to specific foods). Cognitive-Affective input for swallowing can be susceptible to change via feedback in various ways: varying taste, smell, and visual appeal, for instance, may trigger an association which may result in an adverse limbic response to swallowing. Although there is no direct evidence testing the effects of cognition or affect on the safe execution of a swallow, patients wil l often report worsening swallow function with increased distraction, implicating cognitive-affective systems in the production of a safe swallow. The influence of cognitive processe s on motor performance has garnered increased research support in recent years; particularly in the area of gait and balance (e.g., Bensoussan, et al., 2007; Plumme r-D'Amato, et al., 2008; Singhal, Culham,

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26 Chinellato, & Goodale, 2007; Yogev-Seligmann, H ausdorff, & Giladi, 20 08). Since there has been no empirical testing of the effect s of cognitive-affective system changes on swallow function, the gait and balance literatu re can be used to inform the framework of swallow functioning, especially given the invo lvement of a CPG for gait. The effects of cognitive processes on gait function have been studied, in large part, through the use of dual task paradigms. In these paradigms, a person performs two tasks simultaneously. The performance in the dual task condition is then compared to the performance in the single task condition. Cognitive motor in terference refers to the phenomenon in which simultaneous performance of a cognitive ta sk and a motor task interferes with the performance of one or more tasks. This in terference is presumed to occur because of competing demands for attentional resources. The dual task paradigm is a wellrespected paradigm for assessing shared attentional resources among two cognitive tasks or cognitive and motor tasks (e.g., B ensoussan, et al., 2007; Kemper, McDowd, Pohl, Herman, & Jackson, 2006; Melzer, Benjuya, & Kaplanski, 2001; PlummerD'Amato, et al., 2008; Riby, Perfect, & St ollery, 2004; Singhal, Culham, Chinellato, & Goodale, 2007; Yogev-Seligmann, Hausdorff, & Giladi, 2008). The concept of attention has been modified si gnificantly over the years. It is now considered essential for the distribution/allocation of res ources to given cognitive and motor tasks. At times termed c ognitive effort, resources, or capacity it is influenced by internal and external stimuli, result ing in bottom-up and top-down modulation of function. There are still various theories as to what attention really is, how much attention exists, and how the resources are allocated (McNe il, Odell, & Tseng, 1990). There is relative agreement, though, that cognitive-motor interference, a phenomenon

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27 often observed during dual task paradigms, can be explained utilizing capacity-sharing models of attention allocation where two func tions are competing for similar resources; therefore, when these functions are completed at the same time, there are decrements in one or both of the functions Kahneman (1973, p. 8) expan ds on this idea; describing two assumptions: 1) there is general limit on capacity to perform mental work and 2) this limited capacity can be allocated wit h considerable freedom among concurrent activities. This has implications for swallo w given that it is a life sustaining function and thus should result in prioritizati on within allocated resources. McNeil and colleagues (1990) identify se veral other factors associated with attention from which theories regarding allocation of resources for swallowing can be extrapolated: Attentional allocation is influenced by arousal. If a person is not sufficiently aroused, the ability to allocate attent ion to a given task and/or the amount of attentional resources available is r educed. This phenomenon might explain the increased incidence of dysphagia related to dementia (Langmore, et al., 2007) or the increased incidence of aspiration pneumonia in nursing home residents (Langmore, et al., 2002; Langm ore, et al., 1998). Attention is organized in a dynamic m anner. Attention can therefore be shared across cognitive and potentially motor domai ns, and this might result in unequally distributed attentional resources across domains. The attentional system has the capacity to evaluate task demands, therefore, allocating the appropriate amount of resources to a task. This might result in tasks which are cognitively underdriven, not because of reduced amounts of cognitive effort or attention but secondary to defic ient analysis of task demands. This may be of particular concern in persons with sensory-motor involvement. Additionally, this might result in variability of performance secondary to varying feedback influencing decisions relative to task demands. The more complex and less automatic a task, the more cognitive e ffort is required. Swallowing is a complex task, but relatively automatic in nature. It is possible that in pathological cases, there is a decrement in the automaticity of the task resulting in the need for additional attentional resources for successful completion of the task.

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28 Swallow Plan Common understanding in the area of motor c ontrol describes several hierarchical levels of organization, including planning, programming, and execution for successful motor control (e.g., Gracco & Abbs, 1987; Sc hmidt, 1975, Van der Merw e, 1997). In the speech motor control l iterature, it has been suggested that a clinical distinction cannot be made between motor planning and progra mming (Van der Merwe, 1997). In the swallowing literature, little to no distinction has been made between motor execution and the swallow plan therefore, this model, for now, will join planning and programming into one domain termed swallow plan. The term s wallow plan has been used very limitedly in the swallow literature (Huckabee et al., 2003; Malandraki et al., 2009). Therefore, the s wallow plan will involve both the motor plan and motor program. Evidence for the presence of this domain in clude EEG and fMRI studies (Huckabee, et al., 2003; Malandraki, et al ., 2009), the occurrence of swallow apraxia (Daniels, 2000; Robbins & Levin, 1988; Robbi ns, et al., 1993), and the extensive motor control literature (e.g., Gra cco & Abbs, 1987; Schmidt, 1975). This domain is essential to understanding the coordinated and modifi able nature of swallowing function secondary to feedback. Changes in the motor plan/program which are sent to the motor units are highly dependent upon sensory informa tion from the bolus (e.g. changes in bolus size, viscosity, consistency) or inter nal changes in the resp iratory or deglutative systems, for instance. This sw allowing plan is then executed. Swallow Execution In the execution phas e of swallowing, the swallow plan is transformed into automatic reflexive motor movements (Brooks, 1986). There is evid ence from the motor control literature that despite the relatively reflexive nat ure of this domain there may be

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29 influence of feedback on the execution of a mo tor plan/program (Crutcher & Alexander, 1990; Eccles, 1977). This may occur with unex pected (especially transient) changes in peripheral muscle strength or range of motion or perhaps secondary to afferent information being relayed from mechanorecept ors within the swallow mechanism. Central Pattern Generator (CPG) The CPG, defined as, premotor neurons or interneurons which can initiate or organize the swallowing motor sequence (Ertekin & Aydogdu, 2003, pg. 2233) has mainly been studied in non-human mammal s. These neurons are located in the NTS and the reticular formations surrounding the NTS (dorsal swallowing group DSG) and the nucleus ambiguous (ventral swallowing group VSG) (Jean, 1984, 2001; Kessler and Jean 1985; Broussard & Altschuler, 200 0b). The involvement of the CPG on execution and motor planning is not completely clear, although it has been suggested that the DSG may be more closely linked to motor planning and the VSG to execution driving motorneuron pools of cranial nerves V, VII, IX, X, and XII (Ertekin & Aydogdu, 2003; Holstege, Kuypers, & Dekker, 1977; Jean et al., 1983; Jean, 2001; Wheeler & Sapienza, 2005). The extent of its in volvement on motor planning/programming and execution during automatic swallowing (i.e. sleep) versus swallowing in an awake, aware state is unclear and an empirical question. The neural correlates of the various dom ains of swallow function as per the proposed framework are identified in Figure 1-2. These are based on the motor control literature and areas activated during fMRI and EEG st udies of swallowing. Feedback Unarguable is the role of feedback via various sensory systems for proper motor control of swallowing. Feedback can influence cognitiv e-affective input, motor

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30 planning/programming, and execution as descr ibed above and each of the domains can subsequently provide information which will al ter future swallowing performance (Ding, et al., 2003; Gross, Atwood, et al., 2003; Gross, et al., 2006; Hiss, et al., 2004; Logemann, et al., 1995; Mistry, et al., 2006; Sciortino, et al., 2003). Examples of feedback mechanisms vi a baroreceptors, chemoreceptors, hydroreceptors, mechanoreceptors (and muscle spindles), nociceptors, proprioceptors, thermoreceptors, etc. are listed below: Bolus Taste Bolus Smell Visual appearance of bolus Bolus size Bolus consistency Bolus temperature Auditory cue from a clinician or caretaker Kinesthetic information from oral structures Kinesthetic information from the hands as food is manipulat ed, cut, etc. Receptors within the gastrointestinal tracts detecting hunger Mechanoreceptors in the airways Swallow Framework in a Pathological Model The propos ed framework of swallow function has implications for the understanding of dysphagia. The proposed framework can be utilized to define loci of dysfunction secondary to pathology. This leads to specific research questions used to examine factors which can influence swallow function in a given population. Following, the proposed model will be considered in light of pathology, in this case, PD. PD was selected as it is the population of interest in the current study. PD results in changes to both motor and non-motor functions. The su sceptibility to cognitive and swallow dysfunction in PD, specifically, is of par ticular importance for this study. Further description of motor and non-motor symptoms secondary to PD is to follow.

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31 Parkinsons Disease (General) PD has long been considered an illness caused by dopamine depletion in the substantia nigra that affected only motor function, but the current conceptualiz ation of PD acknowledges that it affects distributed neuroanatomical regions, disrupting multiple motor and non-motor systems (Braak, Ghebre medhin, Rub, Bratzke, & Del Tredici, 2004). The cardinal symptoms include brady kinesia, rigidity, resting tremor, and postural instability. In addition to basal gan glia specific changes, it is now considered that the PD process begins in the dorsal mo tor nucleus of the vagal nerve and, from there, proceeds upward until it ar rives at the cerebral cortex (Braak et al., 2004). This conceptualization of PD progression has particu lar implications for swallowing, given the particular involvement of brainstem structur es. Braak and colleagues (Braak, et al., 2004) delineate six stages in the progression of PD; in the firs t of which the dorsal motor nucleus of the vagal nerve in the brain stem is always involved. Involvement of the substantia nigra follows the pat hology of the medulla. It is nt until stages 3 and 4 of the disease that the clinical presentation of PD may begin. In stage 3, there is an upward moving process of the disease into the forebrain and development of pathological changes to the striatal loop centers. The 4t h stage, results in bilateral impairment with dysfunction in memory and cognition. It is in stages 5 and 6 that the substantia nigra appears unmistakably pale. Braaks model has not been accepted without controversy, but provides support for the understanding of pathology secondary to PD which is not solely dependent on basal gangl ia mediated functions (i.e. swallow, speech, cognition, autonomic systems, etc).

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32 Parkinsons Disease and Dysphagia James Parkinson (1817) in his firs t published description of the PD, An Essay on the Shaking Palsy, identified swallow di sturbance. He r eported prepharyngeal abnormalities of ingestion, including difficulty initiating the swallow, maintaining selffeeding, impaired oral cont ainment of both saliva and food, and labored lingual movements. His observations have proven quite accurate (Ardran & Kemp, 1967; Blonsky, Logemann, Boshes, & Fisher 1975; Bosma, 1957; Logemann, 1983). The incidence of dysphagia in persons with PD has been reported to be anywhere between 18.5% to 100% of the patients studied (Bassotti, et al., 1998; Coates & Bakheit, 1997; Hunter, Crameri, A ust in, Woodward, & Hughes, 1997; Logemann, Blonsky, & Boshes, 1975) with silent aspiration in at least a third of pat ients (Mari, et al., 1997) many of which are asymptomatic (Bushmann, Dobmeyer, Leeker, & Perlmutter, 1989). Additionally, there is six times great er risk of death secondary to pneumonia in PD (Morgante, et al., 2000), with aspiration pneumonia being the leading cause of death (Fernandez & Lapane, 2002; Gorell, et al., 20 04; Hoehn, 1967; Shill & Stacy, 1998; Singer, 1992). This is t hought to be a consequence of a combination of chronic immobilization and swallow impai rment (Fall, Saleh, Fredr ickson, Olsson, & Granerus, 2003). Widespread impairment in PD results in swallow deficits of every stage of swallow. Dysfunction is commonly seen in oral mani pulation of the bolus including lingual pumping, labial bolus leakag e, lingual tremor, slowed or limited mandibular function, piecemeal deglutition, pre-swallow spill, delayed swallow triggering, and post swallow residue (Ali, et al., 1996; Blonsky, et al., 1975; Born, Harned, Rikkers, Pfeiffer, & Quigley, 1996; Coates & Bakheit, 1997; Erte kin, et al., 2002; Leopold & Kagel, 1996,

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33 1997b, 1997c; Nagaya, Kachi, Yamada, & Igat a, 1998; Stroudley & Walsh, 1991). Changes to the pharyngeal phase of swa llow include slow pharyngeal transit, abnormal/delayed contraction of the pharyngeal wall, coating of the pharyngeal walls with bolus material, deficient epiglottic posit ioning, decreased epiglottic range of motion, stasis in the vallecula and pyriform sinuses, slow laryngeal elevation and excursion, penetration, aspiration, and upper esophageal sphincter (UES) discoordination (Ali, et al., 1996; Blonsky, et al., 1975; Born, et al ., 1996; Bushmann, et al., 1989; Coates & Bakheit, 1997; Eadie & Tyrer, 1965; Erte kin, et al., 2002; Leopold & Kagel, 1996, 1997b, 1997c; Nagaya, et al., 1998; Stroudl ey & Walsh, 1991). Other associated impairments include vocal fold bowing, drooling and difficulty swallowing saliva in up to 78% of persons with PD, and deficits in swallow-respiratory relationships as evidenced by more swallowing during inha lation and swallowing at low ti dal volume (Gross, et al., 2008; Lim, Leow, Huckabee, Frampton, & Anderson, 2008; Pinn ington, Muhiddin, Ellis, & Playford, 2000). The etiology of swallow dysfunction in persons with PD has not been well defined. Changes have been attributed to the cardinal symptoms of PD with decline in motoric abilities due to rigidity, hypokinesia, and tremor; processes controlled by dopaminergic pathways (Lieberman, et al., 1980). Rigidity and bradykinesia have been implicated specifically as responsible for difficulty chewing and drooling. Eadier & Tyrer (1965) and Ertekin et al. (2002) hypothesized t hat the hypokinetic, reduced rate of spontaneous swallowing movements, and the slowness of segmented but coordinated sequential movements (pg 948), may be the most significant cause of swallow dysfunction in PD. Lastly, swallow dysfunc tion in PD has also been attributed to

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34 involvement of the dorsal motor nucleus of the vagus nerve and of Lewy bodies in the myenteric plexus of the es ophagus (Edwards, Quigley, & Pfeiffer, 1992, pg. 730). Severity and degree of motor involvement in PD do not necessarily correlate with severity of swallow dysfunction (Ali, et al., 1 996). Similarly, clinical staging does not predict swallow difficulty (Bushmann, et al., 1989). In fact, Ali et al. (1996) found no relation between limb tremor and lingual tremor and no relation between muscular rigidity and dysmotility of the pharyngeal wa ll. Additionally, Levodopa (L-Dopa), the gold standard for the treatm ent of PD related symptoms, has not been found to be efficacious for the treatment of dysphagia in PD (Born, et al., 1996; Hunter, et al., 1997; Leopold & Kagel, 1997c); nor does L-Dopa improve/influence respiratory-swallow relationships (Lim, et al., 2008). Parkinsons Disease and Cognition Concurrent cognitive and motoric dysfunc tion is inevitable in PD. Cognitive deficits in PD have long been identified in the literature. Subtle cognitive impairments exist in most of the population (Brown & Marsden, 1984) and changes which are often unidentifiable clinically but can be evidenc ed with comprehensive neuropsychological testing (Muslimovic, Post, Speelman, & Schmand, 2005). Dementia has deleterious effects on quality of life, prognosis, and incr eases risk for placement in a nursing home (which also happens to be a risk factor for development of aspiration pneumonia) (Aarsland, Zaccai, & Brayne, 2005; Langmor e, et al., 2002; Nussbaum, Treves, Inzelberg, Rabey, & Korczyn, 1998). A recent study in a large cohort of newly diagnosed persons with PD reveal ed cognitive dysfunction in 24% of patients. Deficits in the domains of memory, attention, and executive function constituted the core dysfunction (Muslimovic, et al., 2005). Other studies have identified a yet higher

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35 prevalence of cognitive dysfunction in per sons with PD (Williams-Gray, Foltynie, Brayne, Robbins, & Barker, 2007). More specifically, cognitive deficits have been reported in the areas of language, memory, visuospatial function, and concept formation and behavioral regulation, with executive functioning being the first affected and visuospatial dysfunction most fr equently reported (for a review see Owen, 2004) Deficits in the domain of memory incl ude deficits in episodic memory, paired associate learning, auditory verbal learning, and visual reproduction of geometric designs (Beatty, Staton, Weir, Monson, & Whitaker, 1989; Bowen, Burns, Brady, & Yahr, 1976; Huber, Shuttlewor th, & Paulson, 1986; Huber, Shuttleworth, Paulson, Bellchambers, & Clapp, 1986; Massman, Delis, Butters, Levin, & Salmon, 1990). Impaired verbal and nonverbal short and l ong term recall have also been observed with preserved long term recognition. At the le vel of executive func tion, anticipation, planning, initiation, and moni toring of goal-directed behaviors are negatively affected. Additionally, there is evidenc e supporting decrements in att entional processes (Litvan, Mohr, Williams, Gomez, & Chase, 1991; Taylor, et al., 2008). The pathophysiology of dement ia in PD is not completely defined but has been thought to involve limbic and neocortical Lew y body deposition, neurofibrillary tangles, senile plaques, and dysfunction of non-dopam inergic neurotransmi tter systems, most specifically the cholinergic system (review Williams-Gray et al., 2007). Additionally, later onset disease has been found to predict cognitive dysfunction (Muslimovic, et al., 2005). In the section below PD is presented as a pathological model in light of the proposed framework (F igure 1-3).

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36 Cognitive-Affective Input Persons with PD have been found to have deficits in multiple cognitive and affective domains as described in the liter ature (Aarsland, et al., 2003; Altgassen, Phillips, Kopp, & Kliegel, 2007; Bayles, et al ., 1996; Beatty, et al., 1989; Berg, Bjornram, Hartelius, Laakso, & Johnels, 2003; Braak, R ub, Jansen Steur, Del Tredici, & de Vos, 2005; Brown, MacCarthy, Gotham, Der, & Marsden, 1988; Brown & Marsden, 1990; Elwan, et al., 1996; Lees & Sm ith, 1983; Levin, Llabre, & Weiner, 1989; Levin, Tomer, & Rey, 1992; McDonald, Richard, & DeLong, 2003; Menza, Forman, Goldstein, & Golbe, 1990; Morti mer, Pirozzolo, Hansch, & Webste r, 1982; Muslimovic, et al., 2005; Okun & Watts, 2002; Owen, 2004; Pirozzolo, Hansch Mortimer, Webster, & Kuskowski, 1982; Richard, 2007; A. E. Taylor & Saint-Cyr, 1995; Veazey, Aki, Cook, Lai, & Kunik, 2005). These changes may influence the amount and allocation of attentional resources or cognitive effort for swallow performance in persons with PD. The following theories will be specific to attentional resource allocation for swallowing in PD given the use of a dual task paradigm as was utilized in the current study. A reduction in the total amount of resour ces may result in less resources allocated overall and therefore less available resources for swallowing. Reductions in level of arousal might re sult in an inability to properly allocate resources to swallowing at any given time. Deficient sensory processing may pr ovide inaccurate information regarding swallowing task demands at any given time, resulting in an impr oper allocation of resources to swallowing. Reductions in attentional resources and ex ecutive function deficits may result in improper prioritization of re sources for swallowing. It may also be the case that for persons with motor disturbance a given motor task may require more attentional resources or cognitive effort resu lting in insufficient resources for swallowing. In this case the deficit may not be caused by reduced attentional resources, but by increased task demands secondary to motor deficits.

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37 It is likely that persons with cognitive and motor dysfunction will be especially vulnerable to dual task effects on swallow fu nction. This discussion will focus on the influence of attentional mechanisms on swallow function given the aims of the proposed study, but dysfunction in other cognitive domains and affective changes (i.e., apathy, depression, anxiety, etc) will inevitably intera ct to influence swal low performance as well. Although this has only been studied once in the area of swallow function (Brodsky, 2006), these assumptions are also supported by the gait and balance literature which has found decrements in speed and accuracy of gait function with concurrent cognitive and motor tasks (Bensoussan, et al., 2007; Plummer-D'Amato, et al., 2008; Singhal, Culham, Chinellato, & Goodale, 2007; YogevSeligmann, Hausdorff, & Giladi, 2008); with results being exaggerated in populations with known cognitive-motor deficits, such as PD (Rochester, et al., 2004; Yogev-S eligmann, et al., 2008). These changes have been attributed to: 1) exceedi ng the limited attentional resource capacity, 2) less automaticity compared with normal controls, and 3) deficits in central executive function. Swallow Plan The basal ganglia are an important structure for the development of the motor plan/program; therefore, dysf unction of the basal ganglia may inherently result in changes to motor plans/programs. In addi tion, sensory disturbanc e associated with basal ganglia impairment may also further influence motor plans/programs. Swallow planning/programming can be altered due to several changes which occur secondary to PD: Inappropriate feedback or defic ient sensory information resu lts in the selection of an inappropriate motor plan/progr am within a given context. Distorted or inappropriate knowledge of results or performance over time reinforces an inappropriate or deficient motor plan/program.

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38 Difficulty integrating sensory information results in an inability to modify the motor plan/program online. Swallow Execution Although weakness of peripheral structures is not always implicated in the early stages of motor dysfunction sec ondary to PD there is evidence suggesting that muscle strength weakness is common (Falvo, Schilli ng, & Earhart, 2008; Koll er & Kase, 1986). There is evidence, for instance, of vocal fold bowing in PD which may be secondary to reduced drive to the thyrovocalis muscle over time (Blumin, Pcolinsky, & Atkins, 2004). Similarly, maximum range of motion of orophar yngeal and laryngeal structures may also decrease over time (Nagaya, Kachi, Yamada & Igata, 1998). Therefore, execution level deficits secondary to weakness and reduc ed range of motion may occur. The CPG will not be discussed specifically, but evidence from Braak et al, 1994 would suggest that the nucleus ambiguous and nucleus tractus solitarius are not implicated in the brainstem lesions identifie d in the progression of PD; these may exist but have not yet been identified. Feedback Feedback is without a doubt impaired in PD; def icits may be present at the level of the receptors or in the int egration of sensory information in the basal ganglia. The impact of sensory disturbance on swallow function in PD is not completely un derstood. Evidence suggesting a high prevalence of silent aspiration provides additional support for influence of sensory dysfunction on swallow impairment (Mari, et al., 1997). Other identified changes in PD which might infl uence the feedback loop necessary for safe swallowing include changes in taste, ability to self feed, and changes in smell, among others (Simuni & Sethi, 2008). Additionally, there is evidence that external cuing

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39 improves dual task cost in persons with PD suggesting that feedback, in this case, can improve function (Baker, Roches ter, & Nieuwboer, 2008). Swallow Framework: Influences on Evalua tion and Management of Dy sphagia Evaluation of Swallowing Disorders Proper evaluation of swallow impairment is necessary fo r refined identification of dysfunction and selection of salient therapeutic targets. The videofluoroscopic evaluation of swallowing (VFES) is consi der ed by many to be the gold standard for assessment of swallowing function. This is especially the case in neurodegenerative disease which often involves dysfunction of all the phases of swallow and is also associated with sensory impairm ent. VFES allows for the vi sualization of the swallow mechanism before, during, and after the swallo w. VFES is completed in a radiographic suite. VFES only provides a snapshot of swallowing function as repeated ingestion of barium and radiation exposure for patient s limits the acquisition of longer more elaborate samples of swallow function. Care ful attention should be directed towards the development of clinical assessment protoc ols which evaluate all domains of swallow function. Assessment protocols should be guided by detailed medical history and patient report, and during instrumental a ssessment (be it with VFES or swallow endoscopy), the swallowing mechanism should be taxed and challenged in order to properly identify loci of dysfunction. Figure 1-4 provides examples of possible questions which should be answered utilizing current assessment methods in orde r to address changes at the various levels of swallow function and enhance assessment improving the comprehensiveness of evaluative techniques. Methods for asse ssment of the proposed domains of swallow are delineated below.

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40 Cognitive-Affective Input Administer cognitive screening or obtai n information regarding cognitive function from the medical record/history; Have patient complete dual cognit ive and motor (swallow) task and assess changes in cognitive performance in single vs. dual task conditions; Have patient complete dual cognit ive and motor (swallow) task and assess changes in swallow performance in single vs. dual task conditions; Assess whether an external cue to priori tize swallow improves swallow function Swallow Planning Assess variability of performance over several trials Assess coordination of structures Swallow Execution Test the strength of the muscles of sw allowing in a task other than swallowing Test the strength of the muscles of swallow during swallowing Test the range of motion of swallow st ructures in tasks ot her than swallowing Test the movement of swallo w structures during swallowing Feedback Assess patients awareness of the bolus in the oral and pharyngeal cavities Note patient awareness of penetration/aspiration Note patients ability to self-feed (or lack thereof) Ask or assess patient awareness of changes in smell or taste Treatment of Swallowing Disorders Most techniques for clinical management of dysphagia lack empirical evidence for their use. There have been only two randomized clinical trials specific to dysphagia management; one of a compensatory technique (Robbins, et al., 2008) and the second a recent study exp loring the utility of expiratory muscle strength training (EMST), a restorative technique, for the management of dysphagia in PD (Troche, WheelerHegland, Musson, Rosenbek, Okun, & Sapienza, 2008). As evidence has mounted regarding peripheral and central plasticity, rehabilitative and restorative techniques have

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41 received more research and clinical attention (Ludlow, et al., 2008). These techniques often target improved strength and/or coordination, but an incomplete understanding of the factors and domains in fluencing dysphagia limit the specif icity of training to identified loci of dysfunction. Dysfunction of varying domains of the pr oposed theoretical framework will require adaptation of selected therapeutic techniques. More specif ic treatment targets should allow for greater exploitation of plasticity resulting in robust change/improvement to swallow function. In cases of persons wit h cognitive-motor impairment, for example, training to dual task, training to prioritize the more important ta sk, or training to attend to swallowing when swallowing, may be most appr opriate. Training to improve cognition overall, may also improve swallow performanc e in these cases. Dysfunction in swallow planning, for instance, may require treat ments which are very task-specific in conjunction with enhanced and specific knowledge of performance and results in order to strengthen appropriate motor plans/programs. Repetition in varying contexts specific to those encountered in everyday feeding conditions may also be necessary. Dysfunction in execution may rely more heavily on the principle of overload; therefore resulting in improved str ength and range of motion of t he swallow mechanism thus improving swallow func tion (Figure 1-5). Specific Aims and Hypotheses The repercussions of dysphagia in populat ions with cognitive-motor involvement, particularly PD, are often deadly s econdar y to the development of aspiration pneumonia. Currently, there is an inco mplete understanding of the factors which contribute to a safe and timely swallow. No studies have tested the effects of increased cognitive load on swallow safety and physi ology under direct visualization with

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42 videofluoroscopy. The mechanisms controlling swallow safety have long been considered to be mainly reflexive in nature mediated by processes of the swallow CPG in the brainstem (e.g., Ertekin & Aydogdu, 2003; Holstege, Kuypers, & Dekker, 1977; Jean et al., 1983; Jean, 2001; Wheeler & Sapienza, 2005). The expectation that swallowing function might be influenced by c ognitive changes is not unfounded as other processes like gait, also mediated via a CPG, have demonstrated dual cognitive-motor task effects (e.g., Bensoussan, et al., 2007; Plummer-D'Amato, et al., 2008; Singhal, Culham, Chinellato, & Goodale, 2007; Yogev-Seligmann, Hausdorff, & Giladi, 2008). A more comprehensive understand ing of the mechanisms influencing and modulating swallow function is important for the developm ent of appropriate interventions for the remediation of swallow impairm ents. Therefore, the primar y goal of this study was to assess the influence of attentional resource allocation on swallow performance in PD by testing the effects of completing a cognitive task while swallowing on swallow safety. Specific Aim 1 To test the hypothesis that performing concurrent cognitive (digit span forward) and swallow tasks would result in decrement s of swallow safety (as measured by penetration-aspiration score, PA score) (Rosenbek Robbins, Roecker, Coyle, & Wood, 1996) secondary to increased at tentional demands via dual task paradigm. It was predicted that persons with PD and dyspha gia would have significantly higher PA scores in the dual task versus single task conditions. Specific Aim 2 To test the hypothesis that performing concurrent cognitive (digit span forward) and swallow tasks would result in disruptions of swallow timing and swallow coordination (a proxy of the swallow plan/program). It wa s predicted that persons with

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43 PD and dysphagia would demonstrate significantly shorter oral transit times, pharyngeal transit times, and total swallow duration and would also have less swallow coordination in the dual task versus single task conditions. Exploratory Aim To test the hypothesis that performing a more complex concurrent cognitive task (digit span backward) would result in greater disruptions to swallo w safety, as measured by PA score, when performing a less complex c ognitive task or no concurrent cognitive task. It was predicted that PA scores would be significantly higher for the dual task with digits span backward than the single task and dual task digits forward conditions.

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44 Figure 1-1. Proposed theoretical framework of sensorimotor swallow control whereby the CPG represents the patterned brai nstem control of swallow and the domains of 1) cognitive-affective input, 2) swallow plan, 3) swallow execution, and 4) feedback are proposed to understand the mechanisms modulating swallow function.

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45 Figure 1-2. Neural correlates of the proposed framework of sensorimotor swallow control.

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46 Figure 1-3. A proposed framework of sensorimotor swallow control: a PD pathological model. It is proposed that PD results in changes of all the domains of the proposed framework.

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47 Figure 1-4. A proposed framework of sensorimotor swallow cont rol: Evaluation of Dysphagia.

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48 Figure 1-5. A proposed framework of sensorimotor swallow cont rol: Treatment of Dysphagia.

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49 CHAPTER 2 METHODS Participants Twenty participants with idiopathic PD were recruited and participated in this study. There were 4 females (ages 72 to 77, mean=75) and 16 males (ages 65 to 80, mean=70.5). Persons with PD we re recruited from the U niver sity of Florida (UF) and Malcom Randall Veterans Administration Medical Center Movement Dis order Centers. All participants had complaints of dysphagia with evidence of penetration of thin liquid barium on videofluoroscopic evaluation of swallowing (VFES) as assessed by a licensed and certified speech-la nguage pathologist. Demographic information, including age, Unified Parkinsons Disease Rating Sc ale (UPDRS), Hoehn &Yahr (H&Y) score, years since diagnosis, and education, is presented in Table 2-1. Inclusion/Exclusion Criteria Criteria for inclus ion in the study included: Diagnosis of Idiopathic Parkinsons Disea se (either tremor-predominant or rigidpredominant) by a certified mo vement disorders neurologist Hoehn & Yahr ( 1967) stage II-III Stabilized on one or more anti-PD meds Adult between the ages of 60 and 85 years Non-demented as measured by the Dem entia Rating Scale-II (DRS-II; Jurica, Leitten, & Mattis, 2001) Willing and capable of providing informed consent Normal hearing thresholds for the par ticipants age or appropriately aided Criteria for exclusion fr om the study included: History of Deep Brain Stimulation (DBS), pallidot omy, or thalamotomy History of any other neurological disorder

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50 History of developmental speech or language disorder History of any other motor speech or language disorder Diagnosis of Alzheimers dis ease or semantic dementia History of severe depression, anxiety, or apathy History of attention deficit disorder Diagnosis and Clinical Assessment of PD Fellowship trained Movement Disorders N eurologists from the UF and Malcom Randall VAMC Movement Disorders Center s (MDC) diagnosed PD using the United Kingdom (UK) brain bank crit eria (Hughes, et al., 1992). Research Design Overview The following protocol was developed and implemented in order to test the hypothesis that attentional resour ce allocation plays an important role in a safe, timely, and coordinated swallow in PD. To achieve this end, a group of participants with PD and known dysphagia were enrolled. All par ticipants underwent two different phases of study. Phase one included complete baselin e testing of cognitive functioning and training on the experiment al paradigm and phase two included the dual task experimental paradigm completed in the radiologic suite under videofluoroscopy. Both phases were completed on the same day. Pa rticipants with PD were tested within the window of optimized medication functi on (i.e. one hour after taking anti-PD medications). Phase 1: Cognitive T esting Procedures The first half of the experimental visit included assessment of study eligibility and neuropsychological status and took place in the Oral Motor Performance Lab at the Malcom Randall VAMC, Brain R ehabilitation Research Center (BRRC), Gainesville, FL. Prior to completion of any tests, the par ticipant signed the info rmed consent form for

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51 project IRB# 518-2008 which wa s approved by University of Florida (UF) and Malcom Randall VAMC Institutional/Scientific Review boards and accompanying radiation safety committees. The participants medical histories were obtained through chart review and query of the UF Movement Disorders Database, which maintains complete data on all neuropsychological function, UPDRS scores, Hoehn & Yahr scores, Mini Mental Status Examination, and scores related to depre ssion, anxiety, and apathy (e.g., Beck Depression Index and Mari n Apathy Index). Given the novelty of the research ques tions, a comprehensive neuropsychological screening was necessary in order to identify any possible covariates contributing to the obtained results. The neuropsychol ogical testing included: 1) DRS-II (Jurica, Leitten, & Mattis, 2001); 2) digit s pan forward/backward (Wechsler, 1987); 3) digit ordering (Hoppe, Muller, Werheid, Thone, & von Cramon, 2000); 4) Trails A & B (Spreen & Strauss, 1998); and 5) Stroop color XXXs and color words. The DRS-II is a valid mental screening test of cognitive functioning in patients with PD (Brown, et al., 1999) and was used to as sess eligibility for study inclusion. Administration of the DRS-II results in a gl obal measure of dementia. Subtests, which were designed to mirror bedside examinations of cognitive fu nctioning, test attention, initiation and perseveration, construction, conceptualization, and verbal and nonverbal short term memory. Digit s pan, performance of alternating movements, design copying, description of similarities, sentence recall and design recognition are among the tasks included in the DRS (Jurica, Leitten, & Mattis, 2001). The Wechsler Memory Scale Revised (Wechsler, 1987) was used to assess working memory. The subtests administered were digit span forward, digit span backward, and digit ordering. For all

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52 three, stimuli gradually increas ed in length and digits were read at a rate of one per second. For digit span forward and backward participants were instructed to listen to the string of digits and then repeat the numbers either forward or backward depending on the task. There were tw o sets of stimuli for each corresponding length/amount of numbers. The test was stopped once the participant failed both sets of a given length. For digit ordering, participants were present ed with a string of numbers which they were then to place in ascending order. There were four sets of stimuli at each selected length. Cognitive flexibility and a ttention was assessed using the Trails A & B tests and the Stroop color XXXs and color words tests. For the Trails A, participants were presented with a sheet containi ng numbers one through 25. T hey were then instructed to draw lines from number to number in asc ending order. For Trails B, participants were to alternate numbers and letters in ascending or der. For both Trails tests, total time to complete the test was determined. Lastly, t he Stroop test, also a measure of attention and cognitive flexibility, consisted of a sheet of paper containing five rows of ten items each. For the Stroop color XXXs the particip ants read the color names (i.e. blue, green, red) of the XXXs which were pr inted in colored ink. Participants were then administered the Stroop color words, in this case, partici pants were presented with five rows of ten color words each. The color words were prin ted in a color other than the one printed. Participants were asked to disregard the color word, and instead say the color of the ink the word was printed in. For both parts, participants were given 45 seconds to list as many of the colors correctly as possible. The investigator and/or trained graduate

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53 research assistants administered all tests to the participants. This phase of the experimental protocol lasted approximately 45 minutes per participant. Training on experimental procedures Prior to the experimental videofluoroscopic evaluation of swallowing, participants were trained on the experimental task. Participants were then given small cups (identical to the ones used in the experiment al design) filled with water (instead of barium) to swallow. They were instructed to keep their heads as still as possible, tiling the cup more than their heads when swallowing. They were also instructed to hold the cup, listen for the numbers, swallow, and then repeat the numbers as requested following the swallow in the dual task condition. They practiced taking single and dual task swallows. They were trained to 90% success prior to enrollment in the experimental paradigm described below. Phase 2 : Experimental Procedures Videofluoroscopic procedures The experimental dual task procedures took place in the department of radiology at the Malcom Randall VAMC, Ga inesville, Fl. using videofl uoroscopy. Participants were seated upright and images of barium swallows were recorded in the lateral view. A properly collimated Ph illips Radiographic/ Fluoroscopic unit t hat provides a 63-kV, 1.2m-A type output for full field of view mode was utilized. Fluoroscopic images were recorded to a Kay Elemetrics Swallowing Si gnals Lab (Kay Elemetrics, Lincoln Park, NJ) using a digital scan converter and electronica lly recorded at 30 frames per second. It was requested of the resident radiologist that the field of view include, at the very least, the lips and teeth anteriorly, nasal spin e superiorly, cervical spine posteriorly, and upper esophageal sphincter inferiorly, allowing fo r a complete visualization of the oral

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54 and pharyngeal structures involved in swallow. Specifically, the structures needing to be visualized for measurement included the tongue, ramus of the mandible, hyoid bone, and upper esophageal sphincter. Figure 2-1 prov ides a still picture as visualized on the Kay Elemetrics Digital Swal low Station program. Cognitive task The cognitive task used in the experimental paradigm was a modified digit span. Digits forw ard using six digits and digits ba ckward with five digits were both completed in the dual task condition. The participants were instructed to listen to the aurally presented span of digits and then provide the digits back in a forward or backward order, depending on the trial. Accuracy of responses was assessed by determining number of correctly recalled digits over tota l number of digits which should have been recalled. Previous studies (Troche, Altm ann, Hudson, et al., 2008; Troche, Altmann, Rosenbek, & Sapienza, 2008) revealed that participants began to demonstrate greatest breakdown in digit span forward following pres entation of five digits. Therefore, six digits were chosen in order to challenge participants, while stil l allowing sufficient success to determine dual task effects. Responses were transcribed online and accuracy was assessed following the exper imental paradigm. Online information regarding accuracy of responses was not provided to the participants. Motor task The motor task for the dual task paradigm was the swallowing of 10 ccs of thi n barium contrast by small cup (Liquid E-Z Paque Barium Sulfate Suspension; 60% w/v, 41% w/w; from E-Z-EM). The cup for self-f eeding was selected in order to approximate everyday feeding conditions despite the fact that the swallow study was taking place in a synthetic environment; the radiological suite. In the si ngle swallow task participants

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55 were instructed to empty the barium in to [your] mouth and swallow when [youre] ready. Participants were instructed to k eep their heads as still as possible during all swallows in order to reduce any movement artifact. Dual task The experimental paradigm cons isted of single (cognitive and swallow) and dual task (cognitive plus swallow) conditions. Pa rticipants at times completed the cognitive task independent of the swallow task (single task cognitive condition) or the swallow task independent of the cognitive task (single task swallow c ondition). Under dual task conditions, the participants were given the cup of barium to hold and instructed, I will now read you [six or five] numbers, please gi ve me the numbers [forward or backward] after you swallow. The numbers were then r ead aloud by the examiner, at a rate of approximately one per second. Single task and dual task conditions were randomized. Each single task (digits forward and swallow) was completed five times, the dual task (digits forward while swallowing) was comp leted five times, and the dual task (digits backward while swallowing) was completed thr ee times. The number of total possible swallows was limited so as not to create over exposure to radiation and excessive ingestion of barium for participants. Tabl e 2-2 presents the stimuli used for each participant. The same stimuli were used for all participants, but recall that the trials were randomized. Data Analysis and Outcome Measures All swallow measurements were completed by an examiner trained in the analy sis of modified barium swallow studies and blin ded to participant identity and condition. Swallow-related measures were completed on swallow studies which were recorded to

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56 the Kay Elemetrics Swallow station. Analysis was completed frame by frame to ensure accuracy and reliability of measurement. Primary Outcome : Swallow Safety Swallow safety in the single versus dual task conditions, was quantif ied using the PA scale (Table 2-3; Rosenbek et al., 1996). Each swallow was measured individually and assigned a PA score. The P-A Scale is a validated, ordinal scale used to measure whether or not material entered the airway and if it did, whether the residue remained or was expelled. Physiological Measures of Swa llow Timing and Coordination The Kay Elemetrics Swallow st ation software allows for t he electronic tagging of videofluoroscopic swallow studies upon frame-by-f rame playback. This in turn allows for the tagging of specific sw allow events with extraction of time-specific information. The following swallow event tags were placed in order to assess swallow timing and airway coordination changes in response to dual task conditions. The following tags were made by the principal investigator who was blinded to participant identity and experimental dual/single ta sk condition (Table 2-4). Measures of Swallow Timing Measures of swallow timing included oral transit time, pharyngeal t ransit time, and total swallow duration (e.g., Ali, Laundl, Wall ace, deCarle, & Cook, 1996; Cook, et al., 1989; Kendall, 2002; Kendall, Leonard, & McKenzie, 2003; Kendall, McKenzie, Leonard, Goncalves, & Walker, 2000; Power, et al., 2009; Troche, Sapienza, & Rosenbek, 2008). These measures were determined from the swallow event tags described above. Oral transit time was def ined as the duration of time it took a participant to clear the bolus from the oral ca vity. Initiation of or al transit time was

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57 defined as the point when the tongue tip was raised and the bolus began posterior movement in the oral cavity with the end of oral transit time being defined by the point when the bolus tail passed the level of the ra mus of the mandible. Pharyngeal transit time was defined as the time it took the bol us to clear the pharyngeal cavity. Onset of pharyngeal transit was defined as the point when the bolus head passed the level of the ramus of the mandible and offset when the bolus tail pass ed through the UES. Total swallow duration was defined as the amount of time it took the bolus to move through the oral cavity and clear the pharyngeal cavi ty. Onset of total swallow duration was defined as the point when the tongue tip wa s raised and the bolus began posterior movement in the oral cavity and the offs et when the bolus tail cleared the UES. Calculation of swallow timing measures from swallow event tags is described in Table 2-5. Measures of Airway Coordination Airway coordination (Table 2-6) was assessed using a measurement scheme defined by Kendall & Leonard ( 2001). Measurements were based on swallow event tags listed above in T able 2-4. The four se lected airway coordinat ion measures allowed for, in theory, the description o f: 1) onset of aryepiglottic fo ld elevation relative to the initiation of the pharyngeal swallo w, 2) the time required for aryepiglottic folds to elevate in order to achieve glottic closur e, 3) aryepiglottic fold elevat ion relative to location of the bolus in the pharynx, and 4) aryepiglottic fold closure relative to location of the bolus in the pharynx. Dual Task Response Comparisons between single and dual task performance within cognitive and swallow measures was completed by participant in order to assess whether participants

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58 were responders to the dual task condi tion. Difference scores (single task performance minus dual task performance) were calculated for each trial completed by each participant. These scores were then averaged by participant within condition. To assess cognitive response to dual task conditi ons, percent correct for digits forward in the dual task was subtracted from percent correct for digits forward in the single task. To assess swallow (motor) response to dual task conditions, PA score in the dual task condition was subtracted from PA score in th e single task condition. A score of zero placed participants in the no change group for both swallow and cognitive performance. Participants who worsened in cognitive task performance in the dual vs. single task condition were identified as those with pos itive difference scores. Those with negative difference scores were identified as par ticipants who had improved in cognitive performance in the dual vs. single task condition. Participants who worsened in swallow safety in the dual vs. singl e task condition were identif ied as those with negative difference scores. Those with positive differ ence scores were identified as participants who had improved in swallow safety in the dual vs. single task condition. Based on these difference scores participants were divided into groups based on dual task response for both cognitive and swallow tasks (i .e. no response, worsening in dual task, improvement in dual ta sk condition). Reliability Inter and Intra-rater reliability for the primary out come measure, PA score, was completed on 25% of the obtained swallow dat a. The primary rate r was the principal investigator and the intra rater reliability was completed by a trained graduate speechlanguage pathology student.

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59 Statistical Analyses Reliability Statistical analysis of the data was comple ted using the Statistical Package for the Socia l Sciences (SPSS) software version 17.0. Both inter and intra-rater reliability was completed on 25% of the sample for the pr imary outcome measure and were assessed statistically using intraclass correlational ana lyses providing a Cronbachs alpha. Given the ordinal nature of the primary outcome of PA score, a Wilcoxon signed rank test for two related samples was utilized to test differences in the single vs. dual task conditions. Baseline cognitive scores were then separated by dual task swallow response group (i.e. no change, worsened, improved) in order to identify any differences in baseline cognitive func tioning which may have influenced dual task response. Analysis of cognitive measur es by dual task response group was completed using nonparametric Kruskal Wallis testing. Paired samples t-tests were utilized to test any difference in the single and dual tasks fo r transit time measures and measures of airway coordination. Lastly, for the exploratory aim, non-paramet ric Friedman test for related samples was completed comparing PA scores in the single, dual-forward, and dual-backward conditions. Statis tical significance was set at p .05.

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60 Table 2-1. Demographic information, including sex, age, UPDRS, Hoehn & Yahr (H & Y) score, years since diagnosis (PD Dx), and education for each participant. Compiled from medical record review and responses from participant inquiry. Participant Code Sex Age UPDRS H & Y PD Diagnosis Education 1 M 66 32 2 1998 14 2 M 74 23 2 2003 20 3 M 65 58 3 2000 20 4 M 80 37 3 2000 20 5 M 65 22 2 2005 20 6 M 66 43 2 1999 20 7 F 76 33 2 2001 12 8 F 77 29 2 2005 12 9 M 60 27 2.5 2001 16 10 M 80 44 2 2004 16 11 M 71 25 2 2008 11 12 F 75 24 2 2005 16 13 M 74 25 2 2008 20 14 M 75 48 3 1999 20 15 M 70 28 2 2004 16 16 M 73 33 3 1998 20 17 M 67 24 2 2007 20 18 F 72 35 3 1998 16 19 M 75 29 2 2001 16 20 M 67 42 2.5 1999 12

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61 Table 2-2. List of stimuli used for each participant during the experimental dual task paradigm completed under videofluoroscopy during phase II of the study. Task Condition Stimuli Cognitive (single) 7 9 6 3 5 8 Cognitive (single) 2 5 6 1 8 3 Cognitive (single) 3 2 8 5 9 6 Cognitive (single) 5 8 9 2 4 3 Cognitive (single) 3 7 2 4 1 5 Swallow (single) n/a Swallow (single) n/a Swallow (single) n/a Swallow (single) n/a Swallow (single) n/a Dual task (forward) 4 5 9 7 3 6 Dual task (forward) 9 1 5 2 7 3 Dual task (forward) 3 8 2 6 9 1 Dual task (forward) 8 7 3 2 6 4 Dual task (forward) 2 4 1 7 5 8 Dual task (backward) 2 7 5 4 6 Dual task (backward) 5 7 1 3 4 Dual task (backward) 8 5 3 4 1

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62 Table 2-3. Penetration-Aspiration Scale (Rosenbek, et al., 1996) used as the primary outcome measure. 1 Contrast does not enter the airway 2 Contrast enters the airway, remains above the vocal folds 3 Contrast remains above the vocal folds with visible residue 4 Contrast contacts vocal folds, no residue 5 Contrast contacts vocal folds, visible residue 6 Contrast passes glottis, no sub-glottic residue 7 Contrast passes glottis, visible sub-glottic residue despite patient response 8 Contrast passes glottis, visible sub-glottic residue, absent of patient response

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63 Table 2-4. Measurement t ags of physiological swallow function completed by the principal investigator who was blinded to participant identity and experimental dual/single task condition. Measur es of swallow timing and airway coordination were derived from these tags. Tag Description OOT Onset of posterior movement by the bolus in the oral cavity. Point at which the tongue tip was raised and the bolus began posterior movement towards the posterior aspect of the oral cavity. BHR Point at which the leading edge of the bolus passed the level of the ramus of the mandible. BTR Point at which the tail of the bolus passed the level of the ramus of the mandible BV Point at which the bolus arrived at the level of the vallecula. If the bolus did not appear to arrive in the vallecula BV was identified as the point when the bolus passed the leve l of the base of the vallecula. UES Point at which the tail of the bolus passed through the UES. AEE Point when the most superior part of the arytenoids began to elevate. AEC Point when the Arytenoid cartila ge made contact with the inverting epiglottis. Table 2-5. Description of calculations used to derive swallow timing measures from swallow event tags described in Table 2-4. Timing Measures Calculation Oral Transit Time BTR OOT Pharyngeal Transit Time UES BHR Total Swallow Duration UES OOT

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64 Table 2-6. Description of calculations us ed to derive airway coordination measures. Both calculations and definitions of measures ar e delineated. AEE BHR Onset of aryepiglottic fold elevation relative to start of swallow AEC AEE Time required for aryepigl ottic fold elevation to achieve supraglottic closure BV-AEE Aryepiglottic fold elevation rela tive to location of the bolus in the pharynx AEC-BV Aryepiglottic fold closure relative to location of the bolus in the pharynx

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65 Figure 2-1. Still radiographic im age representing one frame of swallow sequence (lateral view) as visualized on the Kay Elemetri cs Digital Swallow St ation program.

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66 CHAPTER 3 RESULTS Reliability Intraclass correlation analyses revealed that interrater reliab ility was excellent with a Cronbachs alpha of .968, p< .001. Intrarater re liability was also found to be excellent with a Cronbachs alpha of .966, p< .001. Baseline Cognitive Measures Table 3-1 contains raw scores, means and standard deviations for baseline cognitive measures (i.e. DRS, Stroop 1 & 2, DS F, DSB, Digit orderi ng, Trails A & B). Participant 20 was excluded from further analysi s given that his DRS score was in the demented range (DRS = 116). Participants 1-19 all performed within the nondemented range (DRS 130) and all further result s excluded participant 20 from analysis. Primary Outcome: Penetration-Aspiration Score Comparison of Single versus Dual Task Table 3-2 shows average PA scores for each participant, group means and standard deviations. Wilcoxon signed rank test revealed that PA scores were not signific antly different in the single versus dual task conditions (Z=-1.259, p= -.208 ) Dual Task Response Fourteen of 20 participants worsened in their cognitive performance (percent correct on digits forward) in the dual task condition, 3 of 20 had no change in percent correct in the two conditions, and 3 of 20 had an improvement in percent correct on digits forward in the single vs. dual task conditions.

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67 8 of 20 participants worsened in swallow safety in the dual vs. single task conditions, 5 of 20 participants demonstrated no change in swallow safety in the two conditions, and 7 of 20 participants demonstrat ed an improvement in swallow safety in the dual task condition. Table 3-3 present s difference scores and corresponding groups (for groups: 1=no change, 2= worsened, 3=improved). Baseline Cognitive Function by Dual Task Response Table 3-4 displays means and standard dev iations of all baseline c ognitive measures by dual task swallow response group. Non-parametric Kruskal Wallis testing revealed significant differences among dual ta sk response groups for several cognitive measures (Table 3-4). The measures which demonstrated significant differences or trends towards significant differences were those which measured co gnitive flexibility and attention (i.e. Trails and Stroop). Signifi cant differences were found for Stroop color XXXs (Chi-square=9.430, p=.009) and Trails A (Chi-square=12.20, p=.002 ). In both cases, least impaired scores were f ound for the group which demonstrated no change in the dual vs. single task conditions and most impaired scores were found for the group which improved in swallow safety in the dual vs. single task conditions. Trends towards significance were found for Stro op color words (Chi-square=9.430, p=.088 ) and Trails B (Chi-square=4.852, p=.088 ). Again, in this case, leas t impaired scores were found for the group which demonstrated no change in the dual vs. single task conditions and most impaired scores were found for the group which improved in swallow safety in the dual vs. single task conditions.

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68 Secondary Outcome Swallow Timing Table 3-5 presents means, standard deviations, and pvalues. Paired samples ttests assessing change in swallow timi ng secondary to task condition revealed a signific ant shortening of OTT (t=2.524, df =17, p=.022) PTT ( t =2.141, df =17, p=.047) and TSD ( t =2.731, df =17, p=.014) in the dual task condition. Airway Coordination Means, standard deviations, and pvalues can be found in Table 3-6. Pairedsamples t-tests completed to assess changes in airway coordination secondar y to task condition demonstrated no significant differences in the single vs. dual task conditions. There was a trend towards change in airway coordination (aryepiglottic fold closure relative to location of the bolus in the pharynx) ( t =1.807, df =17, p=.088). Exploratory Aim A non-parametric Friedman Te st for related samples revealed no s ignificant difference in PA score in the single, dual forward, and dual backward conditions between groups (Chi-square=.241, p= .886). Given no signific ant difference in PA, timing and airway coordination m easures were not tested.

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69 Table 3-1. Raw scores, means, and standard deviations for baseline cognitive measures (i.e. Dementia Rating Scale, Stroop XXXs & color words, digit span forward (DSF), digit span backward (DSB) digit ordering (DO), Trails A & B) Participant DRS Stroop XXXs Stroop Color Words DSF DSB DO Trails A Trails B 1 143 83 47771991 140 2 139 76 5612142064 90 3 140 66 32841375 239 4 135 55 299714188 192 5 142 47 3210614108 148 6 137 57 349714145 227 7 142 30 227612197 219 8 139 46 167611188 485 9 139 58 51743125 148 10 142 19 278717120 260 11 139 64 28751482 197 12 137 80 3610313147 176 13 130 64 337613152 309 14 141 43 266414164 284 15 140 73 325612214 687 16 137 46 318812222 413 17 141 77 32341194 122 18 142 69 396716109 204 19 131 83 22649101 364 20 116 27 13623344 629 Means 137.60 58.15 31.907. 405.8512.70146.50 276.65 StDevs 6.18 18.93 10.601.982.504.2366.35 163.87

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70 Table 3-2. Average PA scores for eac h participant, along with group means and standard deviations. Participant PA Mean Single PA Mean Dual PA SD Single PA SD Dual 1 1.00 1.00 0 0 2 1.00 1.00 0 0 3 5.00 5.60 0 1.34 4 2.80 1.00 1.48 0 5 2.80 4.80 1.48 0.45 6 2.25 2.80 1.89 2.05 7 1.20 1.00 0.45 0 8 4.00 3.80 0 0.45 9 1.20 2.20 0.45 1.64 10 2.20 2.60 1.79 2.19 11 1.40 1.40 0.89 0.89 12 1.00 1.25 0 0.50 13 1.20 1.00 0.45 0 14 2.20 2.00 1.30 1.22 15 2.00 2.40 0.71 0.55 16 3.40 2.80 1.52 1.30 17 1.00 1.00 0 0 18 3.00 4.20 1.22 1.79 19 1.00 1.00 0 0

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71 Table 3-3. Differences scores (single mi nus dual task) and corresponding groups by participant for cognitive and swallow ta sks. For response code, 1=no change, 2=worsened, 3=improved Participant Cog Dual Task Cognitive Response Code Swallow Dual Task Swallow Response Code 1 0.00 1 0.00 1 2 0.00 1 0.00 1 3 0.03 2 -0.60 2 4 0.00 1 1.80 3 5 0.10 2 -2.00 2 6 0.23 2 -0.55 2 7 0.23 2 0.20 3 8 0.23 2 0.20 3 9 -0.03 3 -1.00 2 10 0.10 2 -0.40 2 11 -0.13 3 0.00 1 12 0.01 2 -0.25 2 13 0.13 2 0.20 3 14 0.03 2 0.20 3 15 0.01 2 -0.40 2 16 0.10 2 0.65 3 17 0.03 2 0.00 1 18 -0.03 3 -1.20 2 19 0.10 2 0.00 1 20 0.13 2 0.30 3

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72 Table 3-4. Means, standard deviations, significance based on Kruskal Wallis non-param etric statistical analyses of scores on baseline cognitive scores by dual task response groups. Dual Task Motor Response Cog Perf UPDRS DRS Stroop 1Stroop 2DSF DSB DO Trails A Trails B No change 0.00 26.60 138.60 76.60 37.00 7.00 6.80 14.60 86.40 182.60 0.09 3.78 4.56 7.77 14. 07 3.24 4.21 4.83 14.26 108.60 Worsened 0.05 35.13 139.88 58.63 35.38 7. 88 5.50 12.75 130.38 261.13 0.09 12.40 2.11 19.03 7. 21 1.81 1.60 4.27 40.79 176.93 Improved 0.12 34.40 137.33 47.33 26.17 7.33 6.17 12 .67 185.17 317.00 0.10 8.82 4.412 11.48 6. 31 1.03 1.33 1.21 24.74 112.98 Chi-square 3.907 2.711 1.345 9.4304. 8651.052.429.74812.20 4.852 Asymp. Sig .142 .258 .510 .009.088. 591.807.688.002 .088

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73 Table 3-5. Means, standard deviations and pvalues for swallow timing measures by condition. Single Task Dual Task p-values Oral Transit Time 0.4982 0.449 .022 0.1610 0.1337 Pharyngeal Transit Time 0.8443 0.7771 .047 0.1944 0.1550 Total Swallow Duration 1.0213 0.9381 .014 0.2125 0.1997 Table 3-6. Means, standard deviations and pvalues for airway coordination measures by condition. Airway Coordination Measures Single Task Dual Task pvalues AEE BHR 0.8419 0.8091 .261 0.2194 0.1768 AEC AEE 0.6700 0.6428 .186 0.1497 0.1374 BV-AEE 0.9749 1.0058 .293 0.2162 0.1976 AEC-BV 0.7939 0.7370 .088 0.2255 0.1940

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74 CHAPTER 4 DISCUSSION The current study was designed to test the hypothesis that changes to oropharyngeal swallowing occu r with increasing cognitiv e demand in persons with PD. Despite the fact that the mechanisms controlling swallow safety have long been considered to be mainly under involuntary control, the expectation that swallowing function might be influenced by changes in cogni tive drives is not unfounded. Gait, for example, also mediated via a CPG, has dem onstrated dual cognitive-motor task effects (Bensoussan, et al., 2007; Plummer-D'Amato, et al., 2008; Singhal, Culham, Chinellato, & Goodale, 2007; Yogev-Seligmann, Hausdorf f, & Giladi, 2008), wh ich are exaggerated in populations with cognitive-motor dysfunc tion (Rochester, et al., 2004; YogevSeligmann, et al., 2008). With the progressi on of PD, cognitive an d swallow dysfunction worsen, with death usually occurring sec ondary to dysphagia related changes (i.e. aspiration pneumonia) (Fernandez & Lapane, 2002; Gorell, Peterson, Rybicki, & Johnson, 2004; Hoehn, 1967; Mari, et al., 1997; Shill & Stacy, 1998; Singer, 1992). Therefore, the current project was timely in that the findings provide insight for improvements in evaluation and management of dysphagia in persons with PD. The design of the current study is novel as it is the first study to use a dual task paradigm to test swallow function under videofluoroscopy in those with PD. The study involved 20 persons with PD whose baseline cognitive function was tested extensively prior to completing a digit span task wh ile swallowing. The following discussion highlights the results of the st udy in light of their clinical and research implications, particularly addressing their influence on the proposed theoretical framework for sensorimotor oropharyngeal sw allowing which was present ed in Chapter one.

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75 Dual Task Effects on Swallow Safety The primary aim of this study was to te st the hypothesis that swallow safety would worsen, as measured by PA score, when persons with PD completed a concurrent motor (swallowing) and cognitive (digit span fo rward) task as compared to swallowing without the cognitive task. The results of this study did not demonstrate a signific ant worsening of swallow safety when comparing the two task c onditions. In fact, seven participants were found to improve in swallow safety when in the dual task condition. This is compared to eight participants who worsened under the dual task condition and five which demonstrated no change in the dual task vs. single task conditions. Further, post-hoc statistical anal yses were completed in order to determine whether baseline cognitive functioning influenced dual task response/effect. Once baseline cognitive scores were separated by group (i.e. no change, worsened, improved) differential effects of cognition on dual task swallow response were revealed. On average, participants with no change in swallow performance in the dual vs. single task conditions (i.e. non-responders), also had no change in cognitive performance between the two conditions. Basi cally, these participants were nonresponders to the cognitive and motor aspect s of the dual task paradigm. It can be hypothesized that in order for cognitive inpu t to result in decre ments of the swallow plan, there must be a given degree of swallow and cognitive impairment, making both more susceptible to change. It is possibl e that the swallow plan does not become disrupted by cognitive input until a certai n threshold of motor and/or cognitive impairment is reached. This apparently was not achieved with the simple digit span forward task in the five participant s who were non-responders.

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76 Significant differences in baseline cognitive functioning were found among the three dual task swallow response groups on two measures of cognition. The Stroop color XXXs and Trails A tests showed significant differences between groups (as a function of dual task response). Additionally, trends toward s significance were found for the Stroop Color words and Trails B. In all four case s, non-responders were least impaired, followed by those who wors ened in the dual task, and with those who improved in the dual task performing the wo rst on these measures. These cognitive tests are considered to test cognitive flexibility and attent ion, specifically (Spreen and Strauss, 1998). This result provides insight into the domains of cognition which when dysfunctional, may cause most significant change to swallow performance. For Stroop color XXXs, persons who worsened in the dual task condition demonstrated a 23.5 percentage reduction in Str oop and those who improved in the dual task condition a 38.2 percentage worsening as compared to the non responders. For Trails A, persons who worsened in the dual task condition de monstrated a 50.9 percentage reduction in Stroop and those who improved a 114.3 percentage worsening as compared to the non responders. Our prediction of higher PA scores (less sa fe swallow) in the dual task condition was supported in the subgroup of the tested sample who demonstrated mild impairment in cognitive flexibility and attention. T hese findings are consistent with the gait and balance dual task literature, where per sons with PD have been found to have breakdowns in postural stability and gait in the dual task versus single task conditions (Rochester, et al., 2004; Yogev-Seligmann, et al., 2008). This subgroup of participants demonstrated cognitive-motor interference, s upporting the theory that the modified digit

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77 span task and the swallowing task shared attentiona l resources; therefor e, resulting in a breakdown in both swallowing safety and digit span performance in the dual task condition. It was unexpected that a group would actually benefit from the dual task conditions and it was even more surprising that t he group with the most impaired scores on cognitive testing showed this benefit. It is po ssible that for those with the most impaired cognitive flexibility and a ttention the dual task condition served as a treatment for improved swallowing. The simple fact that the participant knew they would be completing a more difficult task may have in creased arousal during the dual task, thus increasing available attentional resources for the swallow and cognitive tasks. This is compatible with the McNeil et al., (1990) description of at tention. As described in Chapter 1, the amount of available attentional resource s is highly dependent upon the level of arousal. Increased arousal results in increased amount of att entional resources. Similarly, the dual task condition may have resulted in increased arousal thus leading to improved allocation of attentional resources. Or, perhaps prioritization of the swallowing task was improved in the dual task condition as compared to the single task condition. Prioritization of a task is considered important fo r resource allocation. A task which is more highly prioritized is likely to receive more resources quicker, than a less prioritized task. Prioritization, along with amount of resources available for allocation, fluctuate with arousal level. In the case of this study both the cognitive task and the swallow task were competing for resources. Swallow, being a bi ological function necessary for survival, should be prioritized. It is possible that bringing greater attention to the task resulted in just that prioritization of swallow.

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78 Regardless, the fact that a change in swallow safety was observed in a cohort of persons with dysphagia as a function of co mpleting a concurrent motor (swallowing) and cognitive task supports the hypothesis t hat varying cognitive load results in changes to swallow safety. This has signific ant research and clinical implications given that the pharyngeal phase of swallowing has long been thought to be controlled completely or at least in large part by in voluntary processes with little susceptibility to change from top-down mechanisms. Furthe r description of these mechanisms will be described below when implications for t he framework of sens orimotor oropharyngeal swallow are addressed. Dual Task Effects of Swallow Timing and Airw ay Coordination In order to better understand any physi ological adjustments which might have occurred with the dual task condition, m easures of swallow timing and airway coordination were completed. It was hypot hesized that timing measures would shorten in the dual task condition and airway coordination measures would reveal diminished swallow coordination in the dual task condition. Oral transit time, pharyngeal transit time, and swallow duration were all signific antly shortened in the dual vs. single task conditions. Historically, shorter transi t times have been associated with improved swallow function but more recently this t heory has been refuted. Many researchers have revised this idea and instead consider t hat faster swallowing is not necessarily more functional or safe (Kendall, 2002; Kenda ll & Leonard, 2001). Rather it may be that there is a minimum time requirement for coordination of airway protection and bolus propulsion/flow through the oropharynx and lary ngopharynx. It is very possible that shorter transit times particularly in a neuropathological condition (model) may be indicative of reduced coordination of or opharyngeal swallowing. Unfortunately, the

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79 literature on swallow transit times is not comp lete enough to allow for the comparison of transit times obtained in this study to expec ted values in healthy elderly and/or persons with PD for a 10 cc bolus of thin liquid barium. Oral transit times shortened from .498 to .449 seconds in the dual task condition, a reduction of ten percent from the single task condition. Tota l swallow duration shortened from 1.0213 to 0.9381 seconds in the dual task condition, an 8% reduction from the single task condition. Lastly, pharyngeal transit time shortened from .844 to .777 seconds in the dual task condition, an 8 % reduction from the single to dual tasks. Current literature suggests that the oral phase of swallow is completely under voluntary control and should therefore be more highly in fluenced by intrinsic and extrinsic factors, like cognitive load, affect, and motor disrupt ion (e.g., Leopold & Kagel, 1983). Therefore the fact that oral transit time was most su sceptible to change in the dual task condition is not unfounded. Brodsky (2006) tested the effects of a dual task on durational measures of swallow and reaction times during a gono go task with swallowing. During the dual task participants listened for a ta rget non-word while swallowing 5 cc of water from a cup. Videofluoroscopy was no t completed but reaction times as well as durational measures were completed. Br odsky found that duration of oral preparatory transit was much more su sceptible to change than was duration of oropharyngeal transit. Interestingly, Brodsky (2006) found that transit times significantly increased in duration. The current study found that there was a significant decrease in transit times. in the current study. These differences ma y be explained by diffe rent methodologies. Both the cognitive and motor tasks were quite different be tween studies. In the Brodsky

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80 (2006) study participants were swallowing a smaller bolus (5 cc) but were also required to react motorically (by switch ) to the target stimuli. Additionally, the cognitive task required attentional resources to be prioritized to the cognitive task as stimuli were being presented aurally during the act of swa llowing. In the current study, the bolus size was larger but no motoric response was r equired in response to the cognitive task. Additionally, the cognitive task allowed for prioritization of either t he cognitive or motor task during swallow, as digits were pr esented before swallow and response following swallow. Direct visualization of swallow in the current study shoul d have also allowed for more exact assessment of duration of swallow phases. Despite the methodological differences, the fact that phar yngeal transit time, in both Brodsky (2006) and the current study, were significantly influenced by task condition, although less so than oral transit time, is further support for the hypothesis t hat mechanisms of swallow, which have been historically perceived to be reflexive in nature, are influenced by cognitive factors and are much more modifiable and adaptable to change than historic ally thought. It is likely that these factors disturb the development of the proper swallow plan, particularly in a neuropathological model. The pharyngeal mechanisms of swallow were further described through the measures of airway/swallow coordinati on. The selected measures have been described by Kendall and Leonard (2001) but have not received extensive study by other researchers. Of the measures de scribed by Kendall and Leonard (2001) we selected the measures which provided specific information pertaining to airway coordination. These measures in cluded: 1) onset of aryepiglotti c fold elevation, 2) time required for glottal closure, 3) aryepiglottic fo ld closure relative to bolus position in the

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81 pharynx, and 4) onset of aryepiglottic fold elevation relative to bolus arrival in the vallecula. Of those, only one measure demons trated a trend towards significant change in the dual task as compared to the single task: the onset of aryepiglottic fold elevation relative to bolus arrival in the vallecula. The fact that no significant change was demonstrated in any of the airway coordi nation measures, may be their lack of sensitivity or specificity to detect these subtle changes change rather than a lack of change in airway/swallow coordi nation in the dual vs. single task conditions. The same may be true of PA score. Further discussion of these measurement issues follows. Implications for the Proposed Framew ork Of Sensorimotor Orophar yngeal Swallowing The results of this study support the impor tance of including a domain specific to cognition in the framework of sensorimotor oropharyngeal sw allowing. In the case of this study, completing a digits forward ta sk while swallowing resulted in changes to swallow transit times with differential effects on swallow safe ty as a function of baseline cognitive functioning. It can be suggest ed that in an awake and alert human, the function of the CPG is not enough to overco me the descending drive from fronto-limbic systems which can influence/shape/disrupt the swallow plan and subsequently disturb swallow performance. The im provement in swallow safety observed in those with most impaired cognitive functioning provides insight for swallow therapy. It can be hypothesized that increasing descending cognitive drive in persons with baseline reductions/impairments in arousal, amount of attentional resource, or attentional resource allocation can result in normalizati on of swallow function. Further study should test what person-specific or task-specific fa ctors cause some to improve in function in the dual task and others to worsen.

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82 Although the current study pr ovides support for the hypo thesis that attentional resources are important for a safe, timely swal low, less is clear as to the mechanism of action. The most likely explanation would be that dysfunctional attentional processes result in a deficient swallow plan. Some theories include: Reduced attentional resources result in faulty prioritization and therefore faulty allocation of resources to swallowing during swallowing. Reduced attentional resources results in an under driven motor system which results in global changes to motor functioning, including swallowing. Reduced attentional resources impair feedback loops which result in the inappropriate selection of a swa llow plan within a given context. Reduced attentional resources impair t he swallow mechanisms ability to modify the swallow plan online. Increased motoric task demands for swallo wing may result in an insufficiency of attentional resources for safe swallowing. Therefore, in summary, when asleep the pathway for swallow function is CPG to swallow execution (possibly through swallo w planning) directly. When awake the cognitive/affective system increases its in fluence on the swallow pl an, with the CPG still essential for swallow execution and function. Figure 4-1 depict s the results of this study in relation to the proposed framework. Implications for Evaluation and Treatment of Dy sphagia Despite the fact that the repercussions of dysphagia (i.e. aspiration pneumonia, malnutrition, and dehydration) are life thr eatening and often the leading cause of death in populations with neurodegenerative disease, there are few treatments for dysphagia which have been identified and studied appr opriately. There are currently no effectiveness studies for any dysphagia rehabi litation paradigm and the only efficacy studies have been for diet modification te chniques (Robbins et al., 2008) and most

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83 recently, expiratory muscle strength training (e.g., Troche et al., 2008). Additionally, even less is known about the long term outco mes associated with dysphagia treatment. In fact, most studies testing outcomes of dysphagia rehabilitation involve very small sample sizes and effect sizes. It may be that dysphagia rehabilitation is hindered not only by a lack of understanding of the factors influencing dysphagia, but also by restricted evaluation methods which do not proper ly locate the loci of dysfunction. Moreover, the act of swallowing does not o ccur in isolation. Swallowing usually surrounds a social event often taking place in the context of multiple cognitive and motor distractions and require ments. At home, eating is rarely a silent, solitary experience. Instead, families gather, discuss their day and share stories, sometimes while the television is on in the background and the dog is barking. At a restaurant, yet more affective, cognitive, and motor load is added as background noise, social pressures, and distractions are enhanced. A dditionally, the sole act of eating is cognitively loaded. One must decide on bolus sizes, order of bolus presentation, and then complete the motor task of bringing the food to the mouth successfully. Current evaluation methods for dysphagia do not cons ider the cognitive and affective complexity surrounding eating and thus swallowing. Instead patients are in an isolated, usually quiet, environment when ev aluated. During the time of evaluation patients are usually completely focused/conc entrated on swallowing; the task at hand. Patients are then presented with a controlled set of boluses, the type and size of which are usually selected by the c linician. The evaluation loses ecological validity as it no longer represents the rea lity of the swallowing/eating exper ience. This study highlights the need for cognitive taxing during swallow evaluation in order to elucidate changes

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84 which may be occurring during a real meal. It is only through more complete and specific evaluation of swallowing that we can identify true lo ci of dysfunction influencing everyday swallow changes. The results of this study also provide pr eliminary evidence fo r the utility of dual tasks or tasks of varying cognitive load as treat ment for dysphagia. In the case of this cohort of participants with PD, a subst antial group of parti cipants demonstrated improvement in swallow function in the dual task. Further research must identify the bounds of how much cognitive load is enou gh and when it is too much. These are empirical questions which must be answered in order to identify what cognitive tasks are most effective in increasing arousal and improving the amount of available attentional resources for swallowing. Furt her study is also needed in order to identify whether swallow or cognitive therapy, particu larly in more impaired populations, results in improvement to swallow function, particula rly in swallowing situations which are more highly loaded cognitively. Additionally, it is possible that pharmacological management may also be of benefit in these situations. A survey-based pilot study of 8 persons with PD revealed that persons with lower levels of arousal were more likely to have dysphagia, a finding which supports the results of this study (S engupta et al., 2007). In these cases, it has been suggested that pharmacol ogical agents targeting incr eased arousal, may improve swallowing function. This requires signifi cant study in order to identify whether pharmacological agents can improve arous al for swallowing and identify which pharmacological agent is most appropriate.

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85 Strengths and Limitations While still e xploratory the current studys implementat ion and design were quite novel. Each participant underwent the same number of swallows, as participants were not cued to swallow more than normal in order to reduce differential effects of fatigue from participant to participant. Additionally, single/dual task conditions were randomized. Although the same stimuli were us ed for all participants, the order in which the stimuli were presented changed in order to, again, control for possible swallow fatigue, a phenomenon which may not be uncomm on in persons with known dysphagia. All participants underwent extensive base line cognitive testing allowing for the identification of cognitive fact ors which should receive further testing; factors which may very well contribute to increased susceptibil ity to worsening of swallow function. Additionally, disease severity was controlled in this group of persons with PD and testing was completed when participants were opt imized ON their medi cations. This is especially essential in this population w here heterogeneity of pr esentation is not uncommon. Although participants had swallow d ysfunction it was mild to moderate in severity, in order to minimi ze floor and ceiling effects and the need to bail out prior to completion of the protocol. Ensuring that participants were non-demented further homogenized our experimental sample. Lastly, all measures were made by raters who were blinded to participant and swallow condition. This study was not without limitation. T he small sample size of 20 persons with PD, may have limited the degree to which subtle changes could be assessed statistically secondary to reduced power. This is particularly influential given that the outcome measures selected may not have been sensitive enough to detect the level and intricacy of change associated with phary ngeal coordination. The PA scale is a

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86 valid, and clinically relevant tool fo r assessing swallow safety. Evaluating presence/absence of penetration/aspiration is essential for determining an appropriate management plan in dysphagia. This being said, further development of measurement tools/schemes to completely, accurately, and precisely describe the physiology of swallow are needed. Current me asures are quite gross in their assessment of swallow physiology. Although measures of timing and airway coordination are important to swallow physiology, it is t he interplay between swallow phas e durations, coordination of swallow structures, timing of key swallow events, location of bolus material, and respiratory-swallow relationshi ps together which truly provide insight into physiology. The development of new measures and improvement of curr ent measures of swallow physiology are necessary for the proper iden tification of change in swallow physiology secondary to perturbat ion and treatment. More bolus types/sizes should be tested in future experimental designs. The bolus type/size selected was 10 cc of thin liquid barium. This is a relatively small bolus size compared to the bolus sizes present in everyday eating conditions, but is one often utilized in the swallow literatur e. The smaller bolus size allowed for the relative control of bolus residue in these participants with known oropharyngeal dysphagia. Too much residue could have obscured measurement, maki ng it more difficult to reliably assess safety and coordination of swallow. It was also thought t hat the selected bolus size would diminish the possibility of a floor effect by restrict ing the incidence of aspiration during the swallow exams and control the ceil ing effect, by allowing for enough swallow deterioration. An empirical question to be a ssessed in the future is whether varying

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87 bolus size from swallow to swallow creates changes in swallow safety given the need to rapidly change the swallow plan. Another limitation of the study is that each participants cognitive system was likely taxed to a different degree with the digit sp an forward task. For instance, a person whose baseline function only allowed for the recalling of 6 digits forward was taxed maximally by our experimental task, but a person who could recall 11 digits maximally on baseline cognitive functioning was taxed less so in the digits forward design. It is also possible that the select ed cognitive task (i.e. modified digit span) was not difficult enough to truly tax the attentional system. This concern is mitigated by the results showing cognitive-motor interference in a subgroup of the tested sample. Despite this we believe that the current desig n was most appropriate for this first study using a dual task paradigm for swallowing under videofluor oscopy. Future studies should test differential effects on swallow function when varying the degree to which an individuals cognitive system is taxed during the dual task paradigm (i.e. basing the cognitive task within the dual task paradigm on baseline cognitive functioning). The exploratory aim of this study was to test whether there would be differential e ffects on swallow safety if a more cognitively taxing task was utilized in t he dual task condition. In the case of this study, digits backward vs. digits forward did not result in differential effects on swallow safety. Future Research This study serves as impetus for fu rther research testing the non-motor contributions to dysphagia. What may seem clinically intuitive to some requires substantial examination to answer the questi ons surrounding this topic and

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88 subsequently enhance the care of persons with dysphagia. The following topics and questions require study: Can the results of this study be r eplicated in a larger sample size? Do the phenomena elucidated in this study also exist in healthy older and younger adults? Or are they specific to populations with some sort of pathology? Or do they only occur in populations with concomit ant cognitive and swallow disturbance? How impaired does baselin e cognitive functioning have to be to result in decrements of swallow safety when in the dual task? What is the dual task cost for swallow sa fety when the cognitive task is made more difficult? Can a simple distraction task lead to reductions in swallow safety? Is there truly a population in which dual tasking can function as a treatment for dysphagia? Can cognitive treatment (specifically treatment for atte ntion and cognitive flexibility) improve swallowing indirectly? Can pharmacological agents be used for the improvement of arousal and subsequently, the reduction in incidence of swallow dysfunction in persons with PD? Can combined modality treatments (i.e cognitive rehabilitation + swallow exercises or swallow exercises + pharmaco logical management) result in more maintainable and generalizable outcomes for swallow? How can dysphagia evaluation methods be improved in a way which more appropriately mirrors the rea lities of everyday meals? Summary The goal of this study was to test whether swallow safety could be disrupted by increasing cognitive demands during the motor ta sk of swallowing. To achieve this end, 20 participants with PD and dysphagia were tested completing a dual task experimental paradigm under videofluoroscopy. Results rev ealed that there were differential effects to swallow safety based on baseline scores of cognitive flexibility and attention.

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89 Participants who were mildly impaired in cognitive flexibility and attention demonstrated cognitive-motor interference with worsening of both swallow and cognitive performance. Participants who were most impaired in the dom ains of cognitive flexibility and attention actually had improvements in swallow safety in the dual task condition. Additionally, shorter transit times were found over all when comparing single and dual task conditions, but no significant changes were f ound to measures of airway coordination. The results from this study support the hypot hesis that fronto-limbic top-down drive can influence the swallow plan resulting in subs equent change to swallo w performance.

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90 A. Single Task Swallow Performance B. Dual Task Swallow Pe rformance in those with most impaired cognitive functioning Figure 4-1. The results of the current study overlaid on the proposed model of sensorim otor oropharyngeal dysphagia

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105 Troche, M.S., Altmann, L.J.P., Rosenbek, J.C., & Sapienza, C.M. Exploring sentence production in PD: Effects of conceptual and task complexity. Accepted for presentation at 2008 Clinica l Aphasiology Conference. May 2008: Jackson Hole, WY. Troche, M. S., Sapienza, C. M., & Rosenbek, J. C. (2008). Effects of bolus consistency on timing and safety of swallow in patients with Parkinson's disease. Dysphagia, 23(1), 26-32. Troche, M. S., Wheeler-Hegland, K. M., Musson, N., Rosenbek J. C., Okun, M. S., & Sapienza, C. M. (2008). Treatment outcomes of Expiratory Muscle Strength Training (EMST) on swallow function in Parkinson's disease Paper presented at the Movement Disorders Society International Congress. Van der Merwe, A. (1997). A theoretical framework for the characterization of pathological speech sensor imotor control. In M. R. McNeil (Ed.), Clinical Management of Sensorim otor Speech Disorders New York Thieme Medical Pub. Veazey, C., Aki, S. O., Cook, K. F., Lai, E. C., & Kunik, M. E. (2005). Prevalence and treatment of depression in Parkinson's disease. J Neuropsychiatry Clin Neurosci, 17(3), 310-323. Wechsler, D. (1987). Wechsler Adult Intelligence Scales-Revised Manual New York: The Psychological Corporation. Wheeler, K. M. (2007). Invest igation of the respiratoryswallow relationship during effortful swallowing. Paper presented at the ASHA conference. Wheeler, K. M., Huber, J. E., Pitts, T., & S apienza, C. M. (submitted). Lung volume during swallowing: single bolus swallows in healthy young adults. Journal of Speech Language & Hearing Research Wheeler, K.K. & Sapienza, C.M. (2005). Sw allowing and respirat ion: shared neural substrates. Speechpathology.com. Williams-Gray, C. H., Foltynie, T., Brayne, C. E., Robbins, T. W., & Ba rker, R. A. (2007). Evolution of cognitive dysfunction in an incident Parkinson's disease cohort. Brain, 130 (Pt 7), 1787-1798. Yajima, Y., & Larson, C. R. (1993). Multifunctional proper ties of ambiguous neurons identified electrophysiologically during vocalization in the awake monkey. J Neurophysiol, 70 (2), 529-540. Yogev-Seligmann, G., Hausdorff, J. M., & Giladi, N. (2008) The role of executive function and attention in gait. Movement Disorders, 23 (3), 329-342; quiz 472.

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106 Zald, D. H., & Pardo, J. V. (1999). The functional neuroanatomy of voluntary swallowing. Ann Neurol, 46 (3), 281-286. Zheng, Y., Barillot, J. C., & Bianchi, A. L. (1991). Patterns of membrane potentials and distributions of the medullary respir atory neurons in the decerebrate rat. Brain Res, 546 (2), 261-270.

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107 BIOGRAPHICAL SKETCH Michelle Troche receiv ed her bachelors and masters degrees in communication sciences and disorders from the University of Florida in 2004 and 2006, respectively. Clinically, she currently wo rks as an adult outpatient and inpatient Speech-Language Pathologist at Shands Hospital. She has coordinated several expiratory muscle strength training (EMST) research protoc ols working in the UF Movement Disorders Center and Brain Rehabilita tion Research Centers since her undergraduate years. Her research interests include dysphagia rehabilit ation and effects of cognitive factors on speech and swallow production. She plans to continue the interface between research, teaching, and the clinic as an academician.