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Oculomotor Performance in Children with High-Functioning Autism Spectrum Disorders

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Title:
Oculomotor Performance in Children with High-Functioning Autism Spectrum Disorders
Creator:
Wilkes, Bradley J
Place of Publication:
[Gainesville, Fla.]
Florida
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University of Florida
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Language:
english
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1 online resource (28 p.)

Thesis/Dissertation Information

Degree:
Master's ( M.S.)
Degree Grantor:
University of Florida
Degree Disciplines:
Psychology
Committee Chair:
WHITE,KEITH D
Committee Co-Chair:
LEWIS,MARK HENRY
Committee Members:
VOLLMER,TIMOTHY RAYMOND
Graduation Date:
5/2/2015

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Subjects / Keywords:
Asperger syndrome ( jstor )
Autistic disorder ( jstor )
Child psychology ( jstor )
Disabilities ( jstor )
Eye movements ( jstor )
Eyes ( jstor )
Intelligence quotient ( jstor )
Saccades ( jstor )
Smooth pursuit ( jstor )
Social communication ( jstor )
Psychology -- Dissertations, Academic -- UF
autism -- disorders -- oculomotor
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bibliography ( marcgt )
theses ( marcgt )
government publication (state, provincial, terriorial, dependent) ( marcgt )
born-digital ( sobekcm )
Electronic Thesis or Dissertation
Psychology thesis, M.S.

Notes

Abstract:
Sensorimotor issues are of increasing focus in the assessment and treatment of Autism Spectrum Disorders (ASD). The oculomotor system is a sensorimotor network that can provide insights into functional neurobiology and has well-established methodologies for investigation. In this study, we assessed oculomotor performance among children with high functioning ASD and typically developing children, ages 6-12 years. Children with ASD exhibited greater horizontal saccade latency and greater phase lag during vertical smooth pursuit. Saccades and smooth pursuit are mediated by spatially distant brain regions and the long-fiber tracts connecting them, many of which are implicated in ASD. Training paradigms for oculomotor deficits have shown positive outcomes in other clinical populations, and deficits described here may provide useful targets for interventions. ( en )
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In the series University of Florida Digital Collections.
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Includes vita.
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Includes bibliographical references.
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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.
Thesis:
Thesis (M.S.)--University of Florida, 2015.
Local:
Adviser: WHITE,KEITH D.
Local:
Co-adviser: LEWIS,MARK HENRY.
Statement of Responsibility:
by Bradley J Wilkes.

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UFRGP
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Copyright Wilkes, Bradley J. Permission granted to the University of Florida to digitize, archive and distribute this item for non-profit research and educational purposes. Any reuse of this item in excess of fair use or other copyright exemptions requires permission of the copyright holder.
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OCULOMOTOR PERFORMANCE IN CHILDREN WITH HIGH FUNCTIONING AUTISM SPECTRUM DISORDERS By BRADLEY JAMES WILKES A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MAST ER OF SCIENCE UNIVERSITY OF FLORIDA 2015

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2 © 2015 Bradley James Wilkes

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3 ACKNOWLEDGEMENTS T his research supported by Autism Idea Award W81XWH 10 1 0382 from the US Department of Defense Congressionally Di rected Medical Research Program. I would especially like to thank Dr. Keith D. White, Dr. Tana Bleser Carson, Dr. Mark H. Lewis, Dr. Jill Welsh, Kunal Patel , and Brittany Jesewitz.

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4 TABLE OF CONTENTS Page 3 LIST OF TABLES LIST OF FIGURE ABSTRACT CHAPTER 1 INTRODUCTION 2 METHODS 3 2.1 Participants . . 3 2.2 Experimental Setting: Space Theme . 3 2.3 Neuropsychological Assessment 1 4 2.4 Equipment ... .1 4 2.5 Calibration and Oculomotor Tests .. 5 2.6 Statistical Analysis . 6 3 RESULTS .. 1 7 3.1 Saccades 7 3.2 Smooth Pursuit 8 4 .. . 1 9 25 8

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5 LIST OF TABLES Table page 1 Mean and standard deviation for age, IQ, and neuropsychological assessment scores of .. 6

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6 LIST OF FIGURES Figure page 1 17 2 Mean phase (in degrees) for horizontal and vertical visually guided smooth pursuit .. 18

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7 Abstract of Thesis P resented to the Graduate School o f the University of Florida in Partial F ulfillment of the R eq uirements for the D egree Master of Science OCULOMOTOR PERFORMANCE IN CHILDREN WITH HIGH FUNCTIONING AUTISM SPECTRUM DISORDERS By Bradley James Wilkes May 2015 Chair: Keith D. White Major: Psychology Sensorimotor issues are of increasing focus in the assessment and treatment of a utism s pectrum d isorders (ASD). The oculomotor system is a sensorimotor network that can provide insights into functional neurobiology and has well established methodologies for investigation. In this study, we assessed oculom otor performance among children with high functionin g ASD and typically developing children , ages 6 12 years. Children with ASD exhibited greater horizontal saccade latency and greater phase lag during vertical smooth pursuit. Saccades and smooth pursuit a re mediated by spatially distant brain regions and the long fiber tracts connecting them, many of which are implicated in ASD. Training paradigms for oculomotor deficits have shown positive outcomes in other clinical populations , and deficits described here may provide useful targets for intervention s .

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8 CHAPTER 1 INTRODUCTION Autism s pectrum d isorders (ASD ) are a group of neurodevelopmental disorders characterized and diagnosed by deficits in communication and social skills, as well as the presence of restrict ed and/or repetitive behaviors ( DSM V ; America n Psychiatric Association, 20 13 ). Abnormal responses to sensory stimuli are included in the DSM V criteria for ASD with relation to restrictive and/or repetitive behaviors, yet abnormal sensorimotor processes appear to be more pervasive , as evidenced by findings such as deficits in postural stability (Minshew , Sung, Jones, and Furman, 2004 ) and vestibulo ocular reflex abnormalities (Ritvo , Ornitz, Eviatar, Markham, Brown, and Mason, 1969; Ornitz , Constance, Kaplan, and Westlake , 1985) . Estimates of the prevalence for sensory abnormalities in ASD range between 42 88% (Tomcheck and Dunn, 2007). Although there is a high prevalence of sensory abnormalities in ASD, there is a rela tive lack of sensorimotor research in ASD, as compared to investigations of other diagnostic features or comorbid problems (e.g. hyperactivity, anxiety ) . S ensory integrative and sensory based therapies , the goal of which is to modify arousal and abnormal responses to sensory stimuli, are a common intervention for individuals wi th ASD, yet there is a lack of evidence based approaches . Before such issues can be adequately addressed , there is a need for thorough characterization of sensory systems and sensorimotor behaviors in ASD . A sensorimotor system that has received increasing attention in the research of developmental disorders is the oculomotor system. The oculomotor system controls volitional eye movements by incorporating visual information in to appropriate motor output s to the extraocular muscle s . Oculomotor assessments are useful in the study of neurodevelopmental disorders, as abnormal outcomes measures can provide insights into aberrant neural circuitry in

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9 these populations (Sweeney, Takarae, Macmillan, Luna, and Minshew, 2004). The developmental trajectory and neural circuitry underlying the oculomotor system have been thoroughly characterized in typical individuals and methodologies for objective quantific ation of this system early in life are reliable and well established (for a review see Luna, Velanova, and Geier, 2008 ) . Oculomotor outcomes and their potential associations with core features of ASD could provide insights into the underlying features of these phenomena and provide targets for s ensorimotor interventions among individuals with ASD. Two of the most common oculomotor assessments are those of saccades and visual smooth pursuit. A s accade is a quick, darting ey e movement that occur s for both eyes in unison, typically to center a target on the retina. Saccades are characterized by fast acceleration to high velocity, followed by a quick deceleration of equal magnitude. Two parameters of saccades which are commonly studied are gain and latency. Saccade gain is the degree of displacement of the eye as compared to the degree of displacement for the target visual stimulus. Saccade latency is the time lag between appearance o f a target visual stimulus and onset of saccadic eye movement to that stimulus. Visual s mooth pursuit entails a slower, gradual eye movement that serves to stabilize images on the retina during object motion. Smooth pursuit eye movements have much slower acceleratio n and velocity than do saccades, and cannot be performed in the absence of a moving visual stimulus. Two parameters of smooth pursuit which are commonly studied are gain and phase lead/lag. Smooth pursuit gain is the maximum degree of displaceme nt of the eye as compared to the maximum degree of displacement of the target visual stimulus , w hereas smooth mean degree of displacement by which the eye leads or lags behind the target stimulus during a trial.

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10 Oculomotor assessments among individuals with ASD have yielded mixed results. Rosenhall, Johansson, and Gillberg (1988) reported saccade hypometria (reduced gain) in 6 of 11 young adolescent participants with autism. However, Minshew, Luna, and Sweeney (1 999) reported no difference in saccade gain or latency among young adults with high functioning ASD . More recently Takarae, Minshew, Luna, Krisky, and Sweeney (2004 ) as well as Takarae, Luna, Minshew, and Sweeney ( 2008) found that participants with high functioning ASD do not have significantly different saccade gain from control participants, although ASD participants did have greater variance in saccade gain s . In addition, Kemner, van der Geest, Verbaten, and van Engeland (2 004) report ed that children with high functioning pervasive developmental disorder not otherwise specified (PDD NOS) have typical saccade function. Takarae et al. (2004 ; 2008) have demonstrated that participants with high functioning ASD display significa nt abnormalities in visual smooth pursuit gain and latency (similar to phase, except measured in time as opposed to degrees). Rosenhall et al. (1988) reported that although smooth pursuit function was found to be normal in 4 out of 11 participants with autism, 7 could not perform the task as instructed. Scharre and Creedon (1992) also attempted to assess voluntary s mooth pursuit in children with autism, but 29 out of 34 participants displayed a series of saccades, rather than smooth pur suit, while t racking the target. O nly 5 out of 34 children were able to successfully perform the task, but those data were not reported by the authors. Together t hese studies show that high functioning adults with ASD have relatively typical, if more varied saccade function, but abnormal visual smooth pursuit. I t is unclear the extent to which children with high functioning ASD have altered saccade and smooth pursuit function , as these studies have focused on adult populations with high functioning ASD, or child populations without controlling for intellectual disability . It may be that saccade hypometria is

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11 present in those with ASD at younger ages, and that this deficit resolves through maturation. The diffic ulty participants with autism had completing visual smooth pursuit tasks in Rosenhall et al. (1988) and Scharre and Creedon (1992) could have been related to intellectual disability, in that they had trouble understanding and following instructions. Howeve r, in light of the findings from Takarae et al. (2004; 2008), it could be that those participants were performing the ta sk to the best of their ability and saccadic intrusions in the visual smooth pursuit task are part of the ASD po deficits, rather than a confound of low IQ reflecting gross central nervous system damage. Oculomotor systems are optimal targets for sensorimotor research in ASD because they can be reliably assessed, have well understood neural circuitry, and well develo ped m ethodologies for investigation. Oculomotor behaviors are established early in development and remain modifiable. T raining paradigms targeting oculomotor deficits in human subjects have shown positive outcomes (Ciuffreda, Han, Kapoor, and Ficarra, 2006 ) . A s such, these systems are amenable to early identification and intervention, which has been shown to significantly improve the prognosis of children with ASD among other types of interventions (Dawson, Rogers, Munson, Smith, Winter, Greenson, Donaldson , and Varley, 2010; Rogers , 1998). Saccade and visual smooth pursuit behaviors are also functional at birth and can be reliably assessed in infants at 4 weeks of age (Roucoux, Culee, and Roucoux , 1983). The focus of this investigation was to assess saccade and smooth pursuit function in children with ASD, but without intellectual disability (IQ>70). A number of neuropsychological assessments commonly used among individuals ASD were also performed, and we explored associations between oculomotor and n europsychological function . In addition to replicating recent investigations of oculomotor function in high functioning adults with A SD (Takarae et al.,

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12 2004; 2008), the present work extend ed studies of oculomotor function into the vertical plane, which ha s not previously been performed in a population with developmental disability .

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13 CHAPTER 2 METHODS 2.1 Participants Participants include d 1 6 children with ASD and 2 4 typically developing controls . Children were bet ween 6 to 12 years of age at the time of testing. Children were recruited through advertisements distributed to Alachua county public schools, local clinics, and the University of Florida Center for Autism and Related Disabilities (CARD). Experimental protocol was approved by the Institutional R eview Board at the University of Florida. Informed consent participants. Diagnoses were confirmed with the Autism Diagnostic Observa tion Schedule (ADOS; Lord, Risi , Lambrecht, Cook, Leventhal, DiLavore, Pickles, and Rutter , 2000) and Social Communication Questionnaire (SCQ; Rutter, Bayley, Lord, and Berument, 2003) administered by a clinical psychologist. Exclusion criteria for the ASD group were diagnosis of Fragile X, Rett Syndrome, tuberous sclerosis, seizure disorder or fetal cytomegalovirus infection. Exclusion criteria for the control group were any current or past history of psychiatric disorders. None of the children included in the study were prescribe d medications known to alter oculomotor function (e.g. Risperdal). Mean age for the ASD group was 104(±23) months , and mean IQ was 104(±20), with one high outlier of 159 . For typically developing controls, mean age was 110(±21) months , and mean IQ was 106 ( ±14) . Children with an IQ below 70 were not included in this sample, in order to control for intellectual disability as a potential confound. 2.2 Experimental Setting: Space Theme Given the number of assessments performed and their duration, some degree of participant attrition was expected. We sought to increase the s compliance and motivation to participate by providing a stimulating experimental setting. Walls in the room

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14 where oculomotor testing were carried out were painted with a space theme, with the planets of the s olar system and a space shuttle . Children generally reported enjoying the experience, and parents described that children were excited to return if an additional session was needed to complete testing. 2.3 Neuropsych ological Assessment For children included in the ASD group, diagnoses were confirmed with the ADOS administered by a clinical psychologist, and SCQ completed by a parent or primary caregiver. A p a rent or primary caregiver of the participants in both groups was asked to complete the Repetitive Behavior s Scale Revised (RBS R; Bodfish, Symons, Parker, and Lewis, 2000) and the Sensory Profile Careg iver Questionnaire (Dunn, 1999). Although there were several outcome variables derived from the questions in the Se nsory Profile Careg iver Questionnaire, only the Visual Processing sub score was used in this investigation. See Table 1 for a summary of neuropsychological outcome measures. 2.4 Equipment Video oculo graphy (VOG) was performed with the I Portal® system from Neuro Kinetics, Inc. (NKI). This system include d VOG goggles, computer hardware, and VEST 6.8 softwar e for acquisition and analysis. This system sample d from both eyes , in real time , at a rate of 100 Hz. Visual stimuli were presented as a red laser light, generated by NKI Pursuit Tracker® laser . The Pursuit Tracker® laser was mounted on the underside of the circular platform to which the seating apparatus is mounted, and project ed o n a cylindrical arc of h eight 48 inches, with a radius of 76.5 inches. The chair and seating arrangement were created by the authors for pediatric use and include a padded chair, safety harness, and head stabilizers with occipital head

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1 5 rest a nd support arms placed on the temporal region of the participant to prevent head movement during testing . 2.5 Calibration and Oculomotor Tests Calibration and oculomotor tests were performed in darkness, so that only the red laser stimulus was visible to participants. Participants were individually cali brated to the testing equipment by projecting the red laser stimulus onto the cylindrical screen and providing a fixed target at + 10 º in both the horizontal and vertical directions (e.g., 10º to the left, then right, then up and then down) . Calibration values were averaged across two trials. Two oculomotor tasks were then performed, saccades and smooth pursuit, which are described in the next section. During saccade testing, parti cipants were instructed to focus on the red laser stimulus projected onto the cylindrical screen, and to re focus on the stimulus when it appeared at another location. Saccade testing included one trial of horizontal saccades with no vertical component , an d one trial of vertical saccades with no horizontal component . In both horizontal and vertical conditions, 30 saccades were generated with random position between + 25º an d duration between 1 2 seconds; the same randomly generated set of saccades was used for each participant. Mean saccade gain and latency for each participant were determined using VEST 6.8 software. During visual smooth pursuit testing, participants wer e instructed to red stimulus projected onto the cylindrical screen, and to while it The stimulus for smooth pursuit testing moved in an oscillatory fashion ; trials were p erformed at .10 Hz and .50 Hz for 6 cycles , between + 10 º . At each frequency, a trial was performed once in the horizontal direction and once in the vertical direction. Gain and phase lag /lead were determined for each smooth pursuit trial using VEST 6.8 software.

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16 2.6 Statistical Analysis Statistical analyses were performed using IBM SPSS Statistics 21 software. T tests were used to compare group differences in saccade gain, saccade latency, smooth pursuit gain, and smooth pursuit phase lead/lag . Subsequently, a stepwi se linear r egression was used to investigate whether outcome variables from neuropsychological assessments could predict oculomotor parameters that were found to be significantly different between groups. = .05 was used for both t tests and linear regressions. Table 1. Mean and standard deviation for a ge, IQ, and neuropsychological assessment scores of participants. ASD TD Measure Mean ± SD Mean ± SD Age a 104 ± 23 110 ± 21 IQ b 104 ± 20 106 ± 14 SCQ c 21 ± 7 2 ± 2 RBS R d 38 ± 24 3 ± 4 Sensory Profile (visual) e 32 ± 6 40 ± 4 ADOS (CS) f 11 ± 5 ADOS (R) g 2 ± 2 ADOS (total) h 13 ± 7 a Age in months b Leiter non verbal intelligence quotient c Social Communication Questionnaire. d Repetitive Behaviors Scale Revised. e Sensory Profile visual processing sub score. f Autism diagnostic observation schedule (communication + social). g Autism diagnostic observation schedule (repetitive behavior). h Autism diagnostic observation schedule (total score).

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17 CHAPTER 3 RESULTS 3.1 Saccades A significant group difference was identified for horizontal saccade latency (see F igure 1) [ t ( 25.130 ) = 2. 32 , p <0.05] . No significant difference was identified between groups for vertical saccade latency, or saccade gain in either horizontal or vertical conditions. A stepwise linear regression was performed among ASD participants to investigate whether horizontal saccade lat ency could be predicted by ADOS communication plus social composite score, ADOS repetitive behavior composite score, ADOS combined score, RBS R score, SCQ score, or Sensory Profile visual processing sub score. From this regression, it was determined that S CQ score was a significant predictor [ = 0.70 , t ( 12)= 3.288 , p < .05 ] of horizontal saccade laten cy among participants with ASD, with an adjusted R 2 = .45 for the model. Figure 1. Mean latency (in seconds) for horizontal and vertical saccades. A significant group difference was identified between groups for horizontal (p<.05), but not vertical saccades. *

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18 3.2 Smooth Pursuit A significant group difference was identified for vertical smooth pursuit phase at 0.10 Hz [ t ( 14.88 ) = 2. 2 2 , p < 0.05] (see Figure 2) . There was a trending group difference for vertical smooth pursuit phase at 0. 5 0 Hz [ t ( 20.06 ) = 1.86 , p = 0.0 8 ] (see Figure 2) . No significant group differences were identified for horizontal smooth pursuit gain or phase at either .10 Hz or .50 Hz . S tepwise linear regressions were performed among ASD participants to investigate whether either vertical smooth pursuit phase at .10 Hz could be predicted by ADOS communication plus social composite score, ADOS repetitive behavior composite score, ADOS comb ined score, RBS R score, SCQ score, or Sensory Profile visual processing sub score. This regression did not find any significant predictors for vertical smooth pursuit at . 10 Hz . Figure 2 . Mean phase (in degrees) for horizontal and vertical visually guided smooth pursuit at .10 Hz and .50 Hz. A significant group difference was identified for vertical smooth pursuit at .10 Hz (p<.05). *

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19 CHAPTER 4 CONCLUSIONS This study was the first to use VOG to investigate saccade and smooth pursuit function in children with high functioning ASD, without intellectual disability (IQ>70). By controlling for intellectual disability, results from this experiment reflect neurodevelopmental abnormalities specifically r elevant to ASD, rather than general intellectual deficits. In addition, this study is the first to characterize vertical saccade and smooth pursuit in the ASD popul ation. We found evidence of abnormal visual smooth pursuit phase in high functioning c hildren with ASD. We also found evidence that high functioning children with ASD have a greater latency for initiating saccades . W e found participants with ASD had significant ly greater mean phase lag for vertical smooth pursuit at .10 Hz. We did not find significant differences in mean gain or phase for horizontal smooth pursuit conditions . In light of previous findings of reduced gain during pursuit tasks among ASD participants older than 16 years (Takarae et al., 2004), i t is not surprising that we found no group difference for pursuit gain in our sample, since all participants in this investigation wer e between 6 and 12 years of age. Our findings regarding pursuit phase are similar to those of Takarae et al. (2004; 2008) of pursuit latency (similar to phase, except measured in time as opposed to degrees) . Their work suggests that differences in pursuit latency were only detectable after controlling for language delay (i.e. those with languag e delay have lower pursuit latency) . Our findings of greater variance among ASD participants for horizontal smooth pursuit phase, but no group difference in mean horizontal smooth pursuit phase makes sense, as we did not control for language delay in this study .

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20 Our finding of greater mean vertical smooth pursuit phase among children with ASD are novel as we are, to our knowledge, the first investigators to measure vertical smooth pursuit in children with developmental disability. This pronounced difference in group means for phase in verti cal, but not horizontal conditions, could relate to the relatively infrequent use of visual pursuit in the vertical plane. In other words, both populations have less experience tracking objects with continuous motion in the vertical plane , as moving stimuli with motion in the vertical plane are less common than those with motion in the horizontal plane in daily experience . Smooth pursuit is a complex sensorimotor behavior that involves several spatially distant brain regions such as the frontal eye f ields, lateral intra parietal area, medial superior temporal area, caudate, superior colliculus, cerebellar vermis, brainstem premotor nuclei, and vestibular nuclei (for a review see Krauzlis, 200 4 ). Several of these structures have evidence of abnormality among individuals with ASD (for a review see Courchesne , Pierce, Schum ann, Redcay, Buckwalter, Kenned y, and Morgan, 2007) . There is also evidence that individuals with ASD have abnormalities in long fiber tracts between distal brain regions ( Courchesne, Redcay, Morgan, and Kennedy, 2005 ). Local abnormalities in the above brain regions implicated in smooth pursuit, or aberrations in long fiber tracts connecting them could both play a role in abnormal smooth pursuit function among some individuals with ASD. For some ASD participants pursuit phase lag was 10 º in horizontal, or up to 20º in vertical conditions. Interestingly, t he group difference s in horizontal smooth pursuit phase variance and vertical smooth pursuit mean phase were more pronounced at the slower frequency of .10 Hz, where pursuit is typically more accurate (i.e. less phase difference between eye and target). This implies that for some participants the fovea was not on target, but rather, that the

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21 target was in the per iphery. Participants from this study were part of a larger investigation characterizing vestibulo ocular reflex function , performed with the same equipment. Remarkably , ASD participants were unable to significantly suppress post rotary nystagmus with a fov eal target stimulus displayed inside otherwise dark VOG goggles, but were able to suppress post rotary nystagmus normally when the entire room was visible (Bleser Carson et al., unpublished). Taken together, these results may indicate that foveal and perip heral visual streams may be utilized differently in people with ASD. Such difficulties in integrating foveal and peripheral visual information meshes well with sensory integration difficulties described in ASD ( Tomcheck and Dunn, 2007 ). Future investigatio ns among individuals with ASD to directly ascertain whether foveal and peripheral visual streams can be utilized in an integrative fashion, comparable to neurologically typical individuals, seem warranted. It is possible that abnormalities in smooth pursuit could cause functional impairments among individuals with ASD, such as altered spatial awareness in environments with moving stimuli. Indeed, previous work has shown that ASD participants with language de lay had poorer performance than controls on a visual motion discrimination task , correlated with visual smooth pursuit performance (Takarae et al., 2008 ). I t has been demonstrated that adaptive changes in smooth pursuit can be induced by training in non h uman primates (Fuk ushima, Wells, Yamanobe, Takeichi, Shinmei, and Fukushima, 2001) and in humans following brain injury (Ciuffreda et al., 2006) . The adaptive benef its of smooth pursuit training could also potentially improve deficits in visual motion discrimination in the ASD population . Regarding saccades, this investigation found evidence that children with high functioning ASD have a significantly greater latency for initiating horizontal saccades. This group diff erence in mean saccade latency did not extend to the vertical plane. Children with ASD had similar

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22 saccade latency for both horizontal and vertical conditions, whereas typically developing controls initiated saccades more quickly in the horizontal conditio n. The se findings are in contrast with previous work indicating typical saccade function among high functioning individuals with ASD (Minshew et al., 1999; Kemner et al., 2004). Although these previous investigations used random order of presentation for saccade stimuli, each included only three potential target locations, mirrored on each side, and a constant duration of presentation for each stimulus. In t he current investigation, each saccade had a unique, randomly generated position and duration of pre sentation. Perhaps the greater difficulty of the saccade task in this investigation revealed mild deficits in latency to initiate a horizontal saccade in children with ASD that would not be detectable with more predictable stimuli. Deficits in latency to initiate saccades in monkeys occurred after lesions to the frontal eye fields (Lync h, 1992) . Among individuals with ASD, there is evidence of reduced functional connectivity from frontal eye fields and dorsal anterior cingulate cortex (Kenet, Orekhova, Bha radwaj, Shetty, Israeli, Lee, Agam, Elam, Joseph, Hämäläinen, and Manoach, 2012 ) , both of which are regions c ritical in oculomotor control . Perhaps horizontal saccade latency deficits observed in this study are a reflection of neurodevelopmental abnormalit ies in frontal eye fields, or efferent targets. As to why these latency deficits did not extend to vertical saccades, it may be that the circuit implicated in vertical saccades includes some structures that do not overlap with the circuit involved in horiz ontal saccades, and that these are unaffected in this population. Work in monkeys show that lesions to the superior temporal poly sensory area, which receives indirect afferents from the frontal eye fields via the medial pulvinar, negatively affected horizontal saccade latency but not vert ical saccade latency (Scalaidhe, Albright, Rodman, and Gross, 1995).

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23 We performed stepwise linear regression to investigate whether neuropsychological outcome measures could predict those oculomotor parameters found to be significantly different between groups . SCQ score was found to be a significant predictor of horizontal saccade latency, explaining 45% of the variation in horizontal saccade latency among participants with ASD. T he direction of this relationship was unexpected as higher SCQ scores, which indicate greater deficits, predicted lower horizontal saccade latency, where lower latency indicates more typical saccade function. Perhaps it is adaptive for individuals with greater social and communication deficit s to develop shorter latency for initiating visually guided saccades, in order to derive more information about their surroundings from visual stimuli. Other neuropsychological measures from this investigation were not found to be significant predictors fo r those oculomotor parameters that differ ed between groups. It may be that the degree of severity of ASD diagnostic symptoms, indexed by ADOS scores, does not directly affect performance on these oculomotor parameters. Many of the neuropsychological measur es included in these regression models were completed with the aid of parents or caregivers, and thus may not be sensitive enough to function as predictor variables for those oculomotor parameters found to be a b normal in this study. Future studies of oculomotor function in ASD should seek to confirm findings from this investigation regarding saccade and smooth pursuit function in the vertical plane . Although the current investigation focused on individuals with high functioning ASD in order to control for general intellectual disability , the inclusion of participants with lower functioning ASD will help to elucidate whether such oculomotor abnormalities general ize to all individuals with ASD . Clinicians could also develop targeted ther apeutic interventions for patients with ASD who show smooth pursuit phase lag in order to improve smooth pursuit function. Furthermore, the

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24 selectivity of oculomotor abnormalities to ASD can be addressed by future studies that include comparisons of oculom otor abnormalities among other developmentally disabled populations (e.g. Down syndrome ) alongside individuals with ASD.

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25 REFERENCES American Psychiatric Association. (20 13 ). Diagnostic and statistical manual of mental disorders ( 5 th ed .). Washington, DC . Bodfish, J.W., Symons, F.J., Parker, D.E., and Lewis, M.H. (2000). Varieties of Repetitive Behavior in Autism: Comparisons to Mental Retardation. Journal of Autism and Developmental Disorders , 30(3) , 237 243 . Ciuffreda, K.J., Han, Y., Kapoor, N., and F icarra, A.P. (2006). Oculomotor rehabilitation for reading in acquired brain injury. NeuroRehabilitation , 21(1), 9 21. Courchesne, E., Pierce, K., Schumann, C.M., Redcay, E., Buckwalter, J.A., Kennedy, D.P., and Morgan, J. (2007). Mapping early brain development in autism. Neuron , 56(2) , 399 413. Courchesne, E., Redcay, E., Morgan, J.T., Kennedy, D.P. (2005). Autism at the beginning: Microstructural and growth abnormalities underlying the cognitive and behavioral phenotype of autism. Development and P sychology , 17(3) , 577 597. Dawson, G., Rogers, S., Munson, J., Smith, M., Winter, J., Greenson, J., Donaldson, A., and Varley, J. (2010). Randomized Controlled Trial of an Intervention for Toddlers With Autism: The Early Start Denver Model. Pediatrics , 1 25 , 17 23. Fukushima, K., Wells, S.G., Yamanobe, T., Takeichi, N., Shinmei, Y., and Fukushima, J. (2001). Adaptive changes in smooth pursuit eye movements induced by croxx axis pursuit vestibular interaction training in monkeys. Experimental Brain Research , 139(4) , 473 481. Haishi, K., Okuzumi, H., and Kokubun, M. (2011). Effects of age, intelligence, and executive control function on saccadic reaction time in persons with intellectual disabilities. Research in Developmental Disabilities , 32(6) , 26 44 2650. Jacobs, M., Harris, C., Shawkat, F., and Taylor, D. (1992). The objective assessment of abnormal eye movements in infants and young children. Australian and New Zealand Journal of Ophthalmology , 20(3) , 185 195. Kemner, C., van der Geest, J.N., Verbaten, M.N., and van Engeland, H. (2004). In search of neurophysiological markers of pervasive developmental disorders: smooth pursuit eye movements? Journal of Neural Transmission , 111(12) , 1617 1626. Kenet, T., Orekhova, E.V., Bharadwaj, H., Shetty, N.R., Israeli, E., Lee, A.K., Agam, Y., Elam, M., Joseph, R.M., Hämäläinen, M.S., and Manoach, D.S. (2012). Disconnectivity of the cortical ocular motor control network in autism spectrum disorders. NeuroImage , 61(4) , 1226 1234.

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26 Krauzlis, R.J. (2004). Re casting the Smooth Pursuit Eye Movement System. Journal of Neurophysiology , 91(2) , 591 603. Lord, C., Risi, S., Lambrecht, L., Cook, E.H., Leventhal, B.L., DiLavore, P.C., Pickles, A., and Rutter, M. (2000). The Autism Diagnostic Observation Schedule Gene ric: A Standard Measure of Social and Communication Deficits Associated with the Spectrum of Autism. Journal of Autism and Developmental Disorders , 30(3) , 205 223. Lynch, J.C. (1992). Saccade initiation and latency deficits after combined lesions of the frontal and posterior eye fields in monkeys. Journal of Neurophysiology , 68(5) , 1913 1916. Luna, B., Velanova, K., and Geier, C. (2008). Development of eye movement control. Brain and Cognition , 68(3), 293 308. Minshew, N.J., Luna, B., and Sweeney J.A. (1999). Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism. Neurology , 52(5), 917 922 . Minshew, N.J., Sung, K., Jones, B.L., and Furman, J.M. (2004). Underdevelopment of the postural control system in autism. Neurology , 63(11), 2056 2061. Ornitz, E.M., Constance, W.A., Kaplan, A.R., Westlake, J.R. (1985) Brain stem Dysfunction in Autism: results of vestibular stimulation. Archives of General Psychiatry , 42, 1018 1025. Phillips, J.O. and Backous, D.D. (2002) Evaluation of vestibular function in young children. Otolaryngology Clinics of North America , 35 (4), 765 790. Ritvo, E.R., Ornitz, E.M., Eviatar, A., Markham, C.H., Brown, M.B., and Mason, A. (1969). Decreased post rotatory nystagmus in early infantile autism. Ne urology , 19, 653 658. Rogers, S.J., (1998). Empirically supported comprehensive treatments for young children with autism. Journal of Clinical Child Psychology , 27, 168 179. Rosenhall, U., Johannson, E., and Gillberg, C. (1988). Oculomotor findings in a utistic children. The Journal of Laryngology & Otology , 102(5), 435 439. Roucoux, A., Culee, C., and Roucoux, M. (1983). Development of Fixation and Pursuit Eye Movements in Human Infants. Behavioural Brain Research , 10 (1), 133 139 . Rutter, M., Bailey, A., Lord, C., and Berument, S.K. (2003). Social Communication Questionnaire . Los Angeles, CA: Western Psychological Services. Scalaidhe, S.P., Albright, T.D., Rodman, H.R., and Gross, C.G. (1995). Effects of superior temporal polysensory area lesions on the eye movements in the macaque monkey. Journal of Neurophysiology , 73(1), 1 19.

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27 Scharre, J.E. and Creedon, M.P. (1992). Assessment of Visual Function in Autistic Children. Optometry and Vision Science , 69(6), 433 439. Sweeney, J.A., Takarae, Y., Macmil lan, C., Luna, B., and Minshew N.J. (2004). Eye movements in neurodevelopmental disorders. Current Opinions in Neurology , 17(1), 37 42. Takarae, Y., Luna, B., Minshew, N.J., and Sweeney, J.A. (2008). Patterns of visual sensory and sensorimotor abnormaliti es in autism vary in relation to history of early language delay. Journal of the International Neuropsychological Society , 14(6), 980 989. Takarae, Y., Minshew, N.J., Luna, B., Krisky, C.M. and Sweeney, J.A. (2004). Pursuit eye movement deficits in autism . Brain , 127(12), 2584 2594. Tomcheck, S.D. and Dunn, W. (2007.) Sensory Processing in Children With and Without Autism: A Comparative Study Usign the Short Sensory Profile. The American Journal of Occupational Therapy , 61(2), 190 200.

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28 BIOGRAPHICAL SKETCH Bradley James Wilkes was born in Orlando, Florida. In Orlando, h e attended Dr. Phillips High School, gradu ating in the summer of 2006. In t he fall of 2006 , he began attendance at the University of Florida . In August 2011, Bradley graduated summa cu m laude with a Bachelor of Science in n eurobiological s ciences , and cum laude with a Bachelor of Arts in a nthropology. In the fall o f 2011, Bradley began a PhD in p sychology, in the b ehavioral and c ognitive n euroscience area within the Department of Psycho logy with a research focus on sensorimotor processing in a utism s pectrum d isorders. Bradley was awarded his Master of Science in p sychology in the area of b ehavioral and c ognitive n euroscience in 2015 . Bradley is continuing his PhD in p sychology at the Uni versity of Florida , with a research focus on neural mechanisms regulating restrictive and repetitive behavior s , a diagnostic feature of a utism s pectrum d isorders.