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Oculomotor Behavior in Children with Autism Spectrum Disorders

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Title: Oculomotor Behavior in Children with Autism Spectrum Disorders
Language: English
Authors: Caldani, Simona (ORCID 0000-0002-8790-6520), Steg, Sarah, Lefebvre, Aline, Atzori, Paola, Peyre, Hugo, Delorme, Richard, Bucci, Maria Pia
Source: Autism: The International Journal of Research and Practice. Apr 2020 24(3):670-679.
Availability: SAGE Publications. 2455 Teller Road, Thousand Oaks, CA 91320. Tel: 800-818-7243; Tel: 805-499-9774; Fax: 800-583-2665; e-mail: journals@sagepub.com; Web site: http://sagepub.com
Peer Reviewed: Y
Page Count: 10
Publication Date: 2020
Document Type: Journal Articles
Reports - Research
Descriptors: Psychomotor Skills, Eye Movements, Autism, Pervasive Developmental Disorders, Comparative Analysis, Matched Groups, Student Attitudes, Brain Hemisphere Functions, Attention Control, Hospitals, Foreign Countries, Observation, Diagnostic Tests, Intelligence Tests, Children, Behavior Patterns
Geographic Terms: France (Paris)
Assessment and Survey Identifiers: Autism Diagnostic Observation Schedule, Wechsler Intelligence Scale for Children
DOI: 10.1177/1362361319882861
ISSN: 1362-3613
Abstract: To identify quantitative indicators of social communication dysfunctions, we explored the oculomotor performances in subjects with autism spectrum disorders. Discordant findings in the literature have been reported for oculomotor behavior in subjects with autism spectrum disorders. This study aimed to explore reflexive and voluntary saccadic performance in a group of 32 children with autism spectrum disorders (mean age: 12.1 ± 0.5 years) compared to 32 age-, sex-, and IQ-matched typically developing children (control group). We used different types of reflexive and voluntary saccades: gap, step, overlap, and anti-saccades. Eye movements were recorded using an eye tracker (Mobile EBT®) and we measured latency, percentage of anticipatory and express saccades, errors of anti-saccades and gain. Children with autism spectrum disorders reported similar latency values with respect to typically developing children for reflexive and voluntary saccades; in contrast, they made more express and anticipatory saccades overall, as shown in paradigm testing (gap, step, overlap, and anti-saccades). Our findings support previous evidence of the atypicality of the cortical network, which is involved in saccade triggering and attentional processes in children with autism spectrum disorders.
Abstractor: As Provided
Entry Date: 2020
Accession Number: EJ1250630
Database: ERIC
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  Value: <anid>AN0142798422;f9d01apr.20;2020Apr21.04:40;v2.2.500</anid> <title id="AN0142798422-1">Oculomotor behavior in children with autism spectrum disorders </title> <p>To identify quantitative indicators of social communication dysfunctions, we explored the oculomotor performances in subjects with autism spectrum disorders. Discordant findings in the literature have been reported for oculomotor behavior in subjects with autism spectrum disorders. This study aimed to explore reflexive and voluntary saccadic performance in a group of 32 children with autism spectrum disorders (mean age: 12.1 ± 0.5 years) compared to 32 age-, sex-, and IQ-matched typically developing children (control group). We used different types of reflexive and voluntary saccades: gap, step, overlap, and anti-saccades. Eye movements were recorded using an eye tracker (Mobile EBT<sup>®</sup>) and we measured latency, percentage of anticipatory and express saccades, errors of anti-saccades and gain. Children with autism spectrum disorders reported similar latency values with respect to typically developing children for reflexive and voluntary saccades; in contrast, they made more express and anticipatory saccades overall, as shown in paradigm testing (gap, step, overlap, and anti-saccades). Our findings support previous evidence of the atypicality of the cortical network, which is involved in saccade triggering and attentional processes in children with autism spectrum disorders.</p> <p>Keywords: autism spectrum disorder; children; express saccades; inhibitory mechanism; latency</p> <p>Several cortical regions are involved in triggering and processing saccades ([<reflink idref="bib25" id="ref1">25</reflink>]). Visual inputs reaching the retina are sent to the primary visual cortex. In parallel, positional information and motor inputs are transmitted via the dorsal stream to the parietal and prefrontal cortex (for review see [<reflink idref="bib33" id="ref2">33</reflink>]). In everyday life, people make reflexive and voluntary saccades to explore their environment. However, in experimental conditions, different ocular motor paradigms are created to elicit distinct types of saccades, which may be produced more or less voluntarily. The role of cortical networks in initiating saccades is well known ([<reflink idref="bib25" id="ref3">25</reflink>]). The activation intensity of these networks shapes the saccade characteristics, such as latency, amplitude and duration ([<reflink idref="bib12" id="ref4">12</reflink>]). For example, in contrast to reflexive saccades, voluntary saccades need a larger activation of cortical structures, as well as frontal eye field (FEF) and dorsolateral prefrontal cortex (DLPFC) ([<reflink idref="bib35" id="ref5">35</reflink>]; [<reflink idref="bib48" id="ref6">48</reflink>]). The study of eye movements is a source of information to both basic scientists and clinicians: the study of eye movements control provides an opportunity to understand how the brain works and offers opportunities to understand the brain circuit of a disease process. For this reason, over the past three decades, the exploration of eye movements has increasingly been applied as an experimental tool to gain insight into brain disorders ([<reflink idref="bib25" id="ref7">25</reflink>]). Therefore, measurement of eye movements in children with autism spectrum disorder (ASD) may provide insight into the underlying neuropathology of such disorder. Indeed, in children with ASD, various paradigms have been used to investigate eye movements (i.e. reflexives and volitional saccades, pursuits). These paradigms are designed to assess basic oculomotor behaviors and to measure attentional, executive, and inhibitory functions ([<reflink idref="bib7" id="ref8">7</reflink>]; [<reflink idref="bib44" id="ref9">44</reflink>]).</p> <p>Several experimental paradigms have been developed to examine the automatic control of visual attention by manipulating the timing and appearance of visual stimuli. In a gap paradigm (where a temporal gap between the offset of the fixation target and peripheral target onset is introduced), reduced saccade latencies are observed ([<reflink idref="bib42" id="ref10">42</reflink>]). Indeed, the disappearance of the central target reduces the activity in the visual fixation system, resulting in the visual attention and saccade systems to respond more quickly to new stimuli ([<reflink idref="bib32" id="ref11">32</reflink>]). When the peripheral target is presented, the build-up activity and burst neurons effects increase proportionately to the preparing activity and triggering of saccades ([<reflink idref="bib24" id="ref12">24</reflink>]). In the step paradigm, the central fixation target disappears simultaneously to the appearance of the peripheral target. This paradigm is used to assess reflexive saccades. In contrast, in the overlap paradigm (i.e. where the central target persisted after the appearance of the peripheral cue), an increase in latency is reported since the activity in visual fixation systems is prolonged ([<reflink idref="bib41" id="ref13">41</reflink>]). Finally, concerning the fourth paradigm, known as the "anti-saccade paradigm," studies report that the activity of the fixation neurons in the superior colliculus (SC), preceding the peripheral target, increases leading to an inhibition of the activity of saccade generating neurons located in the SC caudal zone ([<reflink idref="bib12" id="ref14">12</reflink>]; [<reflink idref="bib13" id="ref15">13</reflink>]). Successful performance on anti-saccades requires two associated mechanisms: the top-down inhibition of a reflexive saccade to the onset location, and the execution of a voluntary eye movement to the opposite location of the onset.</p> <p>Under all these experimental conditions, the occurrence of express saccades (with shorter latencies) and anticipatory saccades (saccades made before the target appeared) could account for some inhibitory control deficit. The measure of express and anticipatory saccades allows to examine attention allocation, shifting, and response inhibition ([<reflink idref="bib31" id="ref16">31</reflink>]; [<reflink idref="bib36" id="ref17">36</reflink>]; [<reflink idref="bib43" id="ref18">43</reflink>]; [<reflink idref="bib54" id="ref19">54</reflink>]). The presence of these saccades could be explained by a cumulative effect of release of fixation occurring in patients, who already have a deficit of inhibition control, as observed in subjects with ASD ([<reflink idref="bib22" id="ref20">22</reflink>]). Moreover, both express and anticipatory saccades are triggered via the SC and require limited involvement of cortical areas ([<reflink idref="bib8" id="ref21">8</reflink>]). Finally, for the anti-saccades the number of errors made is also an important measure reflecting inhibitory problems linked to frontal dysfunctions ([<reflink idref="bib36" id="ref22">36</reflink>]). In the literature it had been shown that error rate for anti-saccades could be considered predictive of core ASD symptom severity ([<reflink idref="bib7" id="ref23">7</reflink>]) as well as restricted and stereotyped behaviors ([<reflink idref="bib52" id="ref24">52</reflink>]).</p> <p>ASDs are neurodevelopmental disorders characterized by social communication and social interaction deficits, associated with the presence of restricted, repetitive, and stereotyped behaviors (<emph>Diagnostic and Statistical Manual of Mental Disorders</emph> (5th edition; <emph>DSM-5</emph>; [<reflink idref="bib2" id="ref25">2</reflink>]). Numerous neuroimaging studies in ASD report atypical brain functioning in several regions associated with social functions ([<reflink idref="bib34" id="ref26">34</reflink>]; [<reflink idref="bib40" id="ref27">40</reflink>]), such as the anterior cingulate, or the anterior and posterior temporal sulci ([<reflink idref="bib39" id="ref28">39</reflink>]; [<reflink idref="bib46" id="ref29">46</reflink>]). For example, using a structural magnetic resonance imaging (MRI) method, [<reflink idref="bib56" id="ref30">56</reflink>] reported that children with ASD show a lack of normative cortical thinning and volumetric reduction, and an abnormal increase in gyrification compared with typically developing (TD) children.</p> <p>Oculomotor behavior records are frequently used to explore brain activities in ASD and could represent objective and quantitative indicators of social communication dysfunctions ([<reflink idref="bib7" id="ref31">7</reflink>]). Most studies in autism explore the oculomotor behavior in social context, such as eye contact or facial expression recognition suggesting that these individuals present atypical gaze as well as cortical activation to facially expressed emotions ([<reflink idref="bib3" id="ref32">3</reflink>]).</p> <p>In contrast, studies assessing basic oculomotor behavior and cortical circuitries in children with ASD are more scarce, presenting heterogeneous and discordant results.</p> <p>A recent meta-analysis of 27 studies recording different types of reflexive and volitional saccades in subjects with ASD show relatively few oculomotor deficiencies in subjects with ASD ([<reflink idref="bib18" id="ref33">18</reflink>]). More precisely, concerning reflexive and volitional saccades (step, gap, overlap, and anti-saccades paradigm), studies reveal that the average latency value is not statistically distinct in subjects with ASD compared to controls, even if high levels of heterogeneity have been reported. [<reflink idref="bib19" id="ref34">19</reflink>] suggested that these subjects are able to shift attention and initiate eye movements toward peripheral targets as rapidly as healthy individuals. These authors fail to observe a difference between subjects with ASD and control, when measuring the velocity values of reflexive saccades (step paradigm), suggesting a lack of abnormalities at the brainstem level ([<reflink idref="bib50" id="ref35">50</reflink>]). In contrast, the variability of the saccade gain is significantly distinct for the two groups of subjects (larger in subjects with ASD). [<reflink idref="bib19" id="ref36">19</reflink>], for example, report hypometria on reflexive saccades tasks (step paradigm) in accordance to other studies ([<reflink idref="bib29" id="ref37">29</reflink>]; [<reflink idref="bib45" id="ref38">45</reflink>]; [<reflink idref="bib49" id="ref39">49</reflink>]; [<reflink idref="bib50" id="ref40">50</reflink>]) suggesting a cerebellar dysfunction in children with ASD. Concerning volitional saccades, like anti-saccades, subjects with ASD make significantly more errors than controls ([<reflink idref="bib18" id="ref41">18</reflink>]) suggesting some difficulties to inhibit a rapid response. However, the main limits of these studies are the large age range of the participants, the absence of IQ-matched controls and the heterogeneity of paradigms used to induce saccades.</p> <p>Our study aim to record saccades objectively in a group of 32 children with ASD compared with the findings obtained in a group of 32 TD children with matching age, sex, and IQ. Different types of reflexive and volitional saccades were triggered using different conditions (gap, step, overlap, and anti-saccades) for exploring saccadic performance but also anticipatory and express saccades. By measuring several parameters of different types of saccades (reflexive and volitional), we wonder to explore whether a specific saccade parameter and/or saccade type could be a phenotypic indicator for children with ASD. Our hypothesis is that given the numerous fMRI studies that consistently identified atypical brain functioning in a number of regions commonly referred to saccadic control ([<reflink idref="bib47" id="ref42">47</reflink>]; [<reflink idref="bib56" id="ref43">56</reflink>]) we expect to find poor oculomotor performance in children with ASD with respect to TD children particularly in saccade initiation and in inhibitory control.</p> <hd id="AN0142798422-2">Materials and methods</hd> <p></p> <hd id="AN0142798422-3">Subjects</hd> <p>A total of 32 children with ASD (mean age: 12.1 ± 0.5 years) and 32 age-, sex- and IQ-matched TD children were included in the study.</p> <p>Recalling previous research works by our research group ([<reflink idref="bib5" id="ref44">5</reflink>]; [<reflink idref="bib53" id="ref45">53</reflink>]) and other research groups ([<reflink idref="bib16" id="ref46">16</reflink>]; [<reflink idref="bib17" id="ref47">17</reflink>]; [<reflink idref="bib37" id="ref48">37</reflink>]) shows that saccade performance is age-dependent and it improves during childhood until adolescence. For this reason, we decided to test children with small age variability of about 12 years old (age at which cortical structures are mostly developed see [<reflink idref="bib30" id="ref49">30</reflink>]). Moreover, in order to reduce heterogeneity in our findings we include children with ASD to that of IQ-matched TD children.</p> <p>Participants with ASD and TD were included at the Robert Debré Pediatric Hospital in Paris (France). All children enrolled in the study had to take a neurological exam in the normal range and were naïve of any psychotropic drug at the time of testing. None of them reported any personal history of sensory deficit (in any of the five senses). For subjects with ASD, the diagnosis of ASD was based on <emph>DSM</emph>-5 criteria requiring to gather clinical information from the Autism Diagnostic Interview-Revised (ADI-R) ([<reflink idref="bib28" id="ref50">28</reflink>]), the Autism Diagnostic Observation Schedule (ADOS) ([<reflink idref="bib27" id="ref51">27</reflink>]), and the clinical expertise. Their cognitive abilities were also assessed using the Wechsler Intelligence Scale for children (WISC-IV).</p> <p>TD participants and were age-, sex- and IQ-matched with subjects with ASD to avoid sampling bias. The recruitment of TD children was based on voluntary participation; they were sons and daughters of hospital employees. TD children displayed no personal history of neurological or psychiatric disorders. IQ was estimated on two sub-tests of the WISC-IV, one assessing their verbal abilities (similarities sub-test) and one assessing their performance capabilities (matrix reasoning sub-test). The scores for these two sub-tests with the two groups were not significantly distinct (<emph>F</emph>(<reflink idref="bib1" id="ref52">1</reflink>, 62) = 1.20, p = 0.3 and <emph>F</emph>(<reflink idref="bib1" id="ref53">1</reflink>, 62) = 1.55, p = 0.13 for similarity and matrix sub-tests, respectively). The clinical characteristics of children with ASD and TD children were summarized in Table 1. Note also that all children did not wear any type of optical correction.</p> <p>Graph</p> <p>Table 1. Clinical characteristics of the children with autism spectrum disorder (ASD) and typically developing (TD) children enrolled in the study.</p> <p> <ephtml> <table><colgroup><col align="left" /><col align="char" char="." /><col align="char" char="." /></colgroup><thead><tr><th /><th align="left">Children with ASD</th><th align="left">Typically developing (TD) children</th></tr><tr><th /><th align="left">N = 32</th><th align="left">N = 32</th></tr></thead><tbody><tr><td>Age (years), mean (SD)</td><td>12.1 (2.9)</td><td>11.08 (0.5)</td></tr><tr><td colspan="3">Diagnosis of ASD</td></tr><tr><td colspan="3"><italic>Autism Diagnostic Interview-Revised scores</italic></td></tr><tr><td>Social reciprocal interaction, mean (SD)</td><td>18.3 (4.9)</td><td /></tr><tr><td>Communication, mean (SD)</td><td>11.8 (4.4)</td><td /></tr><tr><td>Stereotyped patterns of behaviors, mean (SD)</td><td>4.9 (2.3)</td><td /></tr><tr><td colspan="3"><italic>Autism Diagnostic Observation Schedule Scores</italic></td></tr><tr><td>Social reciprocal interaction, mean (SD)</td><td>8.0 (3.3)</td><td /></tr><tr><td>Communication, mean (SD)</td><td>4.0 (1.6)</td><td /></tr><tr><td colspan="3">Cognitive assessment</td></tr><tr><td colspan="3"><italic>WISC-IV sub-test scores</italic></td></tr><tr><td>Verbal comprehension, mean (SD)</td><td>96.7 (27.8)</td><td /></tr><tr><td>Perceptual reasoning, mean (SD)</td><td>91.2 (23.1)</td><td /></tr><tr><td>Working memory, mean (SD)</td><td>87.5 (20.1)</td><td /></tr><tr><td>Processing speed, mean (SD)</td><td>86.2 (19.9)</td><td /></tr><tr><td>Similarities, mean (SD)</td><td>10.1 (0.9)</td><td>10.7 (0.6)</td></tr><tr><td>Matrix reasoning, mean (SD)</td><td>8.9 (0.7)</td><td>9.2 (0.5)</td></tr></tbody></table> </ephtml> </p> <p>1 WISC-IV: Wechsler Intelligence Scale, fourth version.</p> <p>The investigation followed the principles of the Declaration of Helsinki and was approved by our Institutional Human Experimentation Committee (Comité de Protection des Personnes CPP Île-de-France, Hôpital Saint-Antoine). Written consent was obtained from the children's parents after the experimental procedure was explained to them.</p> <hd id="AN0142798422-4">Eye movement recordings</hd> <p>Eye movements were recorded using the Mobile Eyebrain Tracker (Mobile EBT<sups>®</sups>, e(ye) BRAIN, SuriCog), a CE-marked medical eye-tracking device.The benefit of the Mobile EBT<sups>®</sups> is that the cameras can capture the movements of each eye independently. Recording frequency was set up to 300 Hz. The precision of this system was typically 0.25°. There was no obstruction of the visual field with this recording system. All detected saccades were manually checked by the investigator and corrected/discarded if necessary. Blinks and small amplitude saccades were eliminated automatically for the Mobile Eyebrain Tracker.</p> <hd id="AN0142798422-5">Procedure</hd> <p>Each child was seated in a chair in a dark room, their head stabilized by a headrest supporting both the forehead and the chin. Viewing was binocular; the viewing distance was 60 cm, to avoid convergence interferences during saccades. Calibration was done at the beginning of each block. During the calibration procedure, children fixated a grid of 13 points (diameter: 0.5°) mapping the screen. Point positions in degree in horizontal/vertical plan were: −20.9°/12.2°; 0°/12.2°; 20.9°/12.2°; −10.8°/6.2°; 10.8°/6.2°; −20.9°/0°; 0°/0°; 20.9°/0°; −10.8°/−6.2°; 10.8/−6.2°; −20.9°/−12.2°; 0°/−12.2°; 20.9°/−12.2°.</p> <p>Each calibration point required a fixation of 250 ms to be validated. A polynomial function with five parameters was used to fit the calibration data and to determine the visual angles. After the calibration procedure, an ocular motor task is presented to the subject. The type of task is randomly assigned. Four different paradigms are used to elicit horizontal saccades: the gap, the step paradigm (reflexive saccades), and the overlap, and the anti-saccade paradigm (voluntary saccades). Each task was kept short (lasting a couple of minutes) to avoid shift of the helmet and/or head movements of the child, but allowing for an accurate evaluation of eye movement recordings.</p> <hd id="AN0142798422-6">Ocular motor paradigms</hd> <p>Stimuli are presented on a 22″ PC screen with a resolution of 1920 × 1080 and with a refresh rate of 60 Hz. Stimuli are presented to participants on the screen at 15° to the left and to the right. The stimulus (both central and eccentric target) consists of a red filled-circle subtending a visual angle of 0.5°. The trial entail a target positioned at the screen center for a variable delay that ranged between 2000 and 3500 ms. Children are asked to fixate the target as soon as possible. The target then disappears and the central fixation point signals the beginning of the next trial.</p> <p>After the calibration procedure, an ocular motor task is presented to the subject. The type of task is randomly assigned. The four different paradigms are used to elicit horizontal saccades were: the gap, the step, the overlap paradigm, and the anti-saccade paradigm. <emph>In the gap paradigm</emph>, after the fixation period, the central target is turned off and a target appeared 200 ms later (gap period) for 1000 ms to the right or to the left side of the screen. The central fixation target then reappeared, signaling the beginning of the next trial. <emph>In the step paradigm</emph>, after a variable fixation period ranging between 2000 and 3500 ms, the central target disappears and a target at the left or at the right side of the screen simultaneously appears for 1000 ms. The central fixation target then reappears, signaling the beginning of the next trial. <emph>The overlap paradigm</emph> is started in a similar fashion, with the central fixation point illuminates between 2000 and 3500 ms. In this condition, the fixation point remains illuminated for 1000 ms while a target appears to the right or to the left side of the screen. Thus, during the overlap period, both the central fixation and the target are visible. For each of these three paradigms, children are instructed to look at the target as accurately and as rapidly as possible. The <emph>Anti-saccades paradigm</emph> is also used. The trial consists of a target positioned on the center of the screen with a variable delay period that ranged from 2000 to 3500 ms. The target then disappears in a gap interval of 200 ms. The gap paradigm is often used in the anti-saccade condition to elicit saccades with shorter latencies ([<reflink idref="bib11" id="ref54">11</reflink>]; [<reflink idref="bib37" id="ref55">37</reflink>]). Then, a lateral target appears randomly center left or center right and stayed on for 1000 ms. The central fixation target then reappears, signaling the beginning of the next trial. Children are instructed to look at the central fixation point, then to trigger a saccade as soon as possible in the opposite direction and symmetrically to the lateral target. Thus, when the target appears on the right, children had to look to the left at a distance equivalent to the central point-target distance. When the target returns to the center, children are instructed to visually follow it back to the center. An initial training block of trials is provided to ensure that the instructions are well understood.</p> <p>Each child performs two blocks of various types of eye movements. Each block is separated by a few minutes of rest. Each block contains 30 random trials: 15 target steps to the left side and 15 target steps to the right side.</p> <hd id="AN0142798422-7">Data analysis</hd> <p>Calibration factors for each eye were determined using the eye positions during the calibration procedure (for more details, see [<reflink idref="bib4" id="ref56">4</reflink>]). The algorithm used to detect saccades was described by [<reflink idref="bib38" id="ref57">38</reflink>]. The MeyeAnalysis<sups>®</sups> software (provided with the eye tracker) extracted the defining parameters of saccadic eye movements from the data. This software automatically detected both the onset and the offset of each saccade from both eyes using a built-in saccade detection algorithm.</p> <p>For each saccade recorded (gap, step, overlap, and the anti-saccade) in the different tasks, we examined its latency in millisecond (i.e. the time between the onset of the target and the beginning of the eye movements) and its gain (i.e. the ratio of the amplitude of the total movement, including corrective saccades, over the target excursion amplitude). We calculated also the percentage of anticipatory saccades (saccades with latency shorter than <80 ms) and express saccades (saccades with latency between 80 and 120 ms) ([<reflink idref="bib6" id="ref58">6</reflink>]; [<reflink idref="bib10" id="ref59">10</reflink>]). Note that for anti-saccades task, the gain was not analyzed given that the stimulus was not visible ([<reflink idref="bib18" id="ref60">18</reflink>]). Furthermore, in the anti-saccade task, the mean error rate was also examined.</p> <p>An analysis of variance (ANOVA) was performed with groups as inter-subject factor and oculomotor parameters as within subject factor. The effect of a factor is significant when p-value is below 0.05 after Bonferroni correction (for multiple comparisons). Note that for all oculomotor parameters under consideration, the leftward and rightward directions were pooled together as they did not differ significantly.</p> <hd id="AN0142798422-8">Results</hd> <p>We first explored the latency values for reflexive and voluntary saccades (Figure 1). The ANOVA showed some significant effect of the paradigm (<emph>F</emph>(<reflink idref="bib3" id="ref61">3</reflink>, 186) = 65.83, p < 0.0001, η = 0.5), which remained robust after Bonferroni correction. <emph>Post hoc</emph> analysis revealed a gradient of reduction of latency with a main decrease in the gap paradigm (compared to the step, the overlap, and the anti-saccade paradigms (all p ⩽ 0.0001)), an intermediate reduction in the step paradigm (compared to the overlap and the anti-saccade paradigms (p < 0.007; p < 0.0001, respectively)) and a slight reduction in the overlap paradigm when compared to the anti-saccade condition (p < 0.007). We found also a significant interaction between paradigm and group (<emph>F</emph>(<reflink idref="bib3" id="ref62">3</reflink>, 186) = 4.35, p < 0.006, η = 0.07) which also remained significant after Bonferroni correction. <emph>Post hoc</emph> analysis showed that the latency value in the step and the overlap paradigm in the ASD group (p = 1) was not different whereas TD subjects showed some significant difference (p < 0.0001). Also, the latency value between the overlap and the anti-sacccade paradigms was not different in the ASD and TD groups (p = 1 and p = 0.9, respectively).</p> <p>Graph: Figure 1. Mean values and standard deviations of the latency values recorded in the gap, step, overlap, and anti-saccades paradigms in both the groups of children tested (ASD, children with autism spectrum disorders; TD, typically developing children).*, §, #, and + showed statistical differences.</p> <p>In the next step, we considered the percentage of express saccades (Figure 2). The ANOVA showed some significant effect of group: the ASD group displayed more express saccades than the TD group (<emph>F</emph>(<reflink idref="bib1" id="ref63">1</reflink>, 62) = 14.12, p < 0.004, η = 0.19). We also found some significant effect of paradigm (<emph>F</emph>(<reflink idref="bib3" id="ref64">3</reflink>, 186) = 36.74, p < 0.0001, η = 0.38). <emph>Post hoc</emph> 2 × 2 analysis showed that the percentage of express saccade was higher in the gap paradigm than in the step, overlap, and anti-saccades paradigms (all p ⩽ 0.0001).</p> <p>Graph: Figure 2. Mean values and standard deviations of the percentage of express saccades recorded in the gap, step, overlap, and anti-saccades paradigms in the two groups of children tested (ASD, children with autism spectrum disorders; TD, typically developing children).* and + showed statistical differences.</p> <p>In a third step, we measured the percentage of anticipatory saccades (Figure 3). The ANOVA showed some significant effect of group. The ASD group reported more anticipatory saccades than the TD group (<emph>F</emph>(<reflink idref="bib1" id="ref65">1</reflink>, 62) = 4.61, p < 0.03, η = 0.07). We also observed some significant effect of paradigm, (<emph>F</emph>(<reflink idref="bib3" id="ref66">3</reflink>, 186) = 5.26, p < 0.002, η = 0.08), with a higher percentage of anticipatory saccades in the gap paradigm than in the step and overlap paradigms (p < 0.001 and p < 0.02, respectively).</p> <p>Graph: Figure 3. Mean values and standard deviations of the anticipatory saccade percentage recorded in the gap, step, overlap, and anti-saccades paradigms in the two groups of children tested (ASD, children with autism spectrum disorders; TD, typically developing children).* and + showed statistical differences.</p> <p>Finally, we assessed the gain (Figure 4) and error rate (Figure 5) of saccades. Statistical analysis failed to show any significant difference.</p> <p>Graph: Figure 4. Mean values and standard deviations of saccade gain recorded in the gap, step, and overlap paradigms in both the groups of children tested (ASD, children with autism spectrum disorders; TD, typically developing children).</p> <p>Graph: Figure 5. Mean and standard deviation of the percentage of error rate in the anti-saccade paradigm in both the groups of children tested (ASD, children with autism spectrum disorders; TD, typically developing children).</p> <hd id="AN0142798422-9">Discussion</hd> <p>To identify quantitative indicators of social communication dysfunctions, we explore the oculomotor behavior in subjects with ASD. We explore the latency of saccades in four distinct paradigms eliciting reflexive and voluntary saccades, and the occurrence of express and anticipatory saccades. Surprisingly, we observe that children with ASD report similar latency for reflexive and voluntary saccades (supported by the lack of any significant difference observed of latency values during the step and the overlap paradigms). In TD children, the latency values for voluntary saccades are increased leaving suppose the presence of an enlargement of the cortical network involved in the generation of saccades ([<reflink idref="bib30" id="ref67">30</reflink>]). Our results could suggest that children with ASD could display impairment in their ability to properly activate the cortical network related to initiation of saccades. In parallel, the increased prevalence of express and anticipatory saccades in all paradigms tested (gap, step, overlap, and anti-saccades) in children with ASD compared to TD children, also suggests some disability to activate the brain network which is involved in the inhibitory control of saccades triggering ([<reflink idref="bib8" id="ref68">8</reflink>]). In a recent meta-analysis ([<reflink idref="bib18" id="ref69">18</reflink>]) on individuals with ASD, a high level of heterogeneity is observed with regard to the latencies of reflexive and voluntary saccades. This may be due to the large age range (6–35 years) of the participants. The activation of cortical structures responsible for saccade triggering in TD subjects seems age-dependent ([<reflink idref="bib30" id="ref70">30</reflink>]) and may explain the impact of age on the latencies of reflexive and voluntary saccades. However, our results are parallel to those of [<reflink idref="bib55" id="ref71">55</reflink>] who examined a smaller number of children (16 children with ASD and 15 TD children). They also show no significant difference in latency values of reflexive and voluntary saccades (using gap and overlap paradigms), even though the lengthening of voluntary saccades is smaller in TD children. These results are also replicated by [<reflink idref="bib23" id="ref72">23</reflink>] and [<reflink idref="bib47" id="ref73">47</reflink>], who used similar paradigms. However, some discrepancies have been reported in the literature. For example, [<reflink idref="bib14" id="ref74">14</reflink>] reported longer latencies for reflexive and voluntary saccades in a restricted number of subjects with high functioning autism unlike [<reflink idref="bib29" id="ref75">29</reflink>] who has shown shorter latency for those saccades.</p> <p>Interestingly, [<reflink idref="bib1" id="ref76">1</reflink>] explored brain correlates of visually guided saccades (stimulated by a step paradigm) in eight subjects with ASD and in TD subjects (age range, 14–38 years) using a functional MRI. These authors reported an abnormal activation of the cerebellum in subjects with ASD with respect to TD group. Furthermore, [<reflink idref="bib51" id="ref77">51</reflink>] explored brain correlates of reflexive saccades (stimulated by a step paradigm) in subjects with ASD and in TD subjects (age range, 17–44 years) and show altered rostral frontostriatal activity suggesting the presence of neurodevelopmental perturbations.</p> <p>According to our results (similar latency for reflexive and voluntary saccades), subjects with ASD performing reflexive saccades seem to activate larger cortical network than those normally used to perform voluntary saccades in TD subjects most likely due to abnormal activity of these structures.</p> <p>In our study, we also explore the prevalence of express and anticipatory saccades in all paradigms tested (step, gap, overlap, and anti-saccade). We observe that children with ASD displayed more saccades of that kind than TD children. In the literature, a similar increased occurrence of express saccades in subjects with ASD compared to controls (seven 30-year-old adults) is reported by [<reflink idref="bib22" id="ref78">22</reflink>]. These authors suggest that these results could be related to a deficit in the attention process engagement, which could affect cortical mechanisms involved in saccades ([<reflink idref="bib15" id="ref79">15</reflink>]). The records of pre-saccade's event-related potentials in gap and overlap paradigms show that subjects with ASD report a higher pre-saccade activity during overlap paradigm ([<reflink idref="bib21" id="ref80">21</reflink>]). These results reinforce earlier evidence of a deficit in the attention process requested for these saccades paradigms. However, these results are not replicated by other groups. For example, fewer express saccades are reported in ASD in a gap paradigm ([<reflink idref="bib14" id="ref81">14</reflink>]). Additional explorations taking into account the attentional capabilities in subjects with ASD are needed to compare different types of oculomotor paradigms.</p> <p>Finally, we assess the gain and error rate of saccades throughout the four paradigms. Our results confirm previous studies exploring the gain of saccades though not for error rate (for meta-analysis see [<reflink idref="bib18" id="ref82">18</reflink>]). Methodological divergences (i.e. amplitude and time presentation of the target, age of children tested, and instructions given to subject) could explain the discrepancy in those results. Previous findings suggest that saccadic error rate is strongly age-dependent ([<reflink idref="bib29" id="ref83">29</reflink>]) and influenced by target amplitude ([<reflink idref="bib20" id="ref84">20</reflink>]).</p> <p>Based on these findings, we could advance the hypothesis that visuo-attentional capabilities and inhibitory mechanisms involved in oculomotor control maybe used as indicators for children with ASD. Note also that such poor oculomotor control affects motor capabilities as postural control as well as fine and gross motor skill impairment (see, meta-analysis of [<reflink idref="bib9" id="ref85">9</reflink>]; [<reflink idref="bib26" id="ref86">26</reflink>]). However, further studies leading with oculomotor tasks alone as well as combined with other motor tasks in ASDs will be useful in order to explore the possibility to separate different biological subgroups of patients (autism with high and low cognitive functions) on the basis of oculomotor performance.</p> <hd id="AN0142798422-10">Limitations</hd> <p>Further studies with a larger number of subjects with ASD will be necessary in order to evaluate if specific saccade parameter and/or saccade type could be considered a phenotypic indicator for children with ASD given that on-average group differences cannot be taken as individual-level markers/indicators. Other studies as machine learning analysis on eye movement's parameters could be used in order to detect ASD syndrome.</p> <hd id="AN0142798422-11">Conclusion</hd> <p>Overall, our findings suggest that children with ASD have atypical cortical network responsible for saccade triggering. Particularly, in our study, we found that attentional and inhibitory deficits would be used as phenotypic indicators for children with ASD. Knowing that ASD is characterized by a wide range of symptoms, it will be interesting to use different approaches in order to identify different subgroups within the autism spectrum. For this reason, in the future it may be interesting to explore further attentional capabilities in subjects with ASD by comparing different types of oculomotor activities. Therefore, it would be useful to combine these studies with neuroimaging data to observe the cortical activities related to eye movement's execution. This may lead to a better understanding, and even reinforce the neurophysiological hypotheses of the control and the triggering of saccades. Moreover it could be also interesting to develop oculormotor training protocols in order to improve attention process with this type of patients.</p> <p>The authors thank the children who participated in the study, the practitioners from the Child and Adolescent Psychiatry Department (Robert Debré Hospital) for the screening of children and the Paris Descartes University's Center de Langues for revising the English version of the manuscript.</p> <ref id="AN0142798422-12"> <title> References </title> <blist> <bibl id="bib1" idref="ref52" type="bt">1</bibl> <bibtext> Allen G., Courchesne E. (2003). Differential effects of developmental cerebellar abnormality on cognitive and motor functions in the cerebellum: An fMRI study of autism. The American Journal of Psychiatry, 160, 262–273.</bibtext> </blist> <blist> <bibl id="bib2" idref="ref25" type="bt">2</bibl> <bibtext> American Psychiatric Association. (2013). Diagnostic and Statistical Manual of Mental Disorders (DSM) (5th ed.). 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Molecular Autism, 7, Article 11. doi:10.1186/s13229-016-0076-x</bibtext> </blist> </ref> <ref id="AN0142798422-13"> <title> Footnotes </title> <blist> <bibtext> Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.</bibtext> </blist> <blist> <bibtext> ORCID iD Simona Caldani</bibtext> </blist> <blist> <bibtext>Graph https://orcid.org/0000-0002-8790-6520</bibtext> </blist> </ref> <aug> <p>By Simona Caldani; Sarah Steg; Aline Lefebvre; Paola Atzori; Hugo Peyre; Richard Delorme and Maria Pia Bucci</p> <p>Reported by Author; Author; Author; Author; Author; Author; Author</p> </aug> <nolink nlid="nl1" bibid="bib25" firstref="ref1"></nolink> <nolink nlid="nl2" bibid="bib33" firstref="ref2"></nolink> <nolink nlid="nl3" bibid="bib12" firstref="ref4"></nolink> <nolink nlid="nl4" bibid="bib35" firstref="ref5"></nolink> <nolink nlid="nl5" bibid="bib48" firstref="ref6"></nolink> <nolink nlid="nl6" bibid="bib44" firstref="ref9"></nolink> <nolink nlid="nl7" bibid="bib42" firstref="ref10"></nolink> <nolink nlid="nl8" bibid="bib32" firstref="ref11"></nolink> <nolink nlid="nl9" bibid="bib24" firstref="ref12"></nolink> <nolink nlid="nl10" bibid="bib41" firstref="ref13"></nolink> <nolink nlid="nl11" bibid="bib13" firstref="ref15"></nolink> <nolink nlid="nl12" bibid="bib31" firstref="ref16"></nolink> <nolink nlid="nl13" bibid="bib36" firstref="ref17"></nolink> <nolink nlid="nl14" bibid="bib43" firstref="ref18"></nolink> <nolink nlid="nl15" bibid="bib54" firstref="ref19"></nolink> <nolink nlid="nl16" bibid="bib22" firstref="ref20"></nolink> <nolink nlid="nl17" bibid="bib52" firstref="ref24"></nolink> <nolink nlid="nl18" bibid="bib34" firstref="ref26"></nolink> <nolink nlid="nl19" bibid="bib40" firstref="ref27"></nolink> <nolink nlid="nl20" bibid="bib39" firstref="ref28"></nolink> <nolink nlid="nl21" bibid="bib46" firstref="ref29"></nolink> <nolink nlid="nl22" bibid="bib56" firstref="ref30"></nolink> <nolink nlid="nl23" bibid="bib18" firstref="ref33"></nolink> <nolink nlid="nl24" bibid="bib19" firstref="ref34"></nolink> <nolink nlid="nl25" bibid="bib50" firstref="ref35"></nolink> <nolink nlid="nl26" bibid="bib29" firstref="ref37"></nolink> <nolink nlid="nl27" bibid="bib45" firstref="ref38"></nolink> <nolink nlid="nl28" bibid="bib49" firstref="ref39"></nolink> <nolink nlid="nl29" bibid="bib47" firstref="ref42"></nolink> <nolink nlid="nl30" bibid="bib53" firstref="ref45"></nolink> <nolink nlid="nl31" bibid="bib16" firstref="ref46"></nolink> <nolink nlid="nl32" bibid="bib17" firstref="ref47"></nolink> <nolink nlid="nl33" bibid="bib37" firstref="ref48"></nolink> <nolink nlid="nl34" bibid="bib30" firstref="ref49"></nolink> <nolink nlid="nl35" bibid="bib28" firstref="ref50"></nolink> <nolink nlid="nl36" bibid="bib27" firstref="ref51"></nolink> <nolink nlid="nl37" bibid="bib11" firstref="ref54"></nolink> <nolink nlid="nl38" bibid="bib38" firstref="ref57"></nolink> <nolink nlid="nl39" bibid="bib10" firstref="ref59"></nolink> <nolink nlid="nl40" bibid="bib55" firstref="ref71"></nolink> <nolink nlid="nl41" bibid="bib23" firstref="ref72"></nolink> <nolink nlid="nl42" bibid="bib14" firstref="ref74"></nolink> <nolink nlid="nl43" bibid="bib51" firstref="ref77"></nolink> <nolink nlid="nl44" bibid="bib15" firstref="ref79"></nolink> <nolink nlid="nl45" bibid="bib21" firstref="ref80"></nolink> <nolink nlid="nl46" bibid="bib20" firstref="ref84"></nolink> <nolink nlid="nl47" bibid="bib26" firstref="ref86"></nolink>
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An: EJ1250630
AccessLevel: 3
PubType: Academic Journal
PubTypeId: academicJournal
PreciseRelevancyScore: 0
IllustrationInfo
Items – Name: Title
  Label: Title
  Group: Ti
  Data: Oculomotor Behavior in Children with Autism Spectrum Disorders
– Name: Language
  Label: Language
  Group: Lang
  Data: English
– Name: Author
  Label: Authors
  Group: Au
  Data: <searchLink fieldCode="AR" term="%22Caldani%2C+Simona%22">Caldani, Simona</searchLink> (ORCID <externalLink term="https://orcid.org/0000-0002-8790-6520">0000-0002-8790-6520</externalLink>)<br /><searchLink fieldCode="AR" term="%22Steg%2C+Sarah%22">Steg, Sarah</searchLink><br /><searchLink fieldCode="AR" term="%22Lefebvre%2C+Aline%22">Lefebvre, Aline</searchLink><br /><searchLink fieldCode="AR" term="%22Atzori%2C+Paola%22">Atzori, Paola</searchLink><br /><searchLink fieldCode="AR" term="%22Peyre%2C+Hugo%22">Peyre, Hugo</searchLink><br /><searchLink fieldCode="AR" term="%22Delorme%2C+Richard%22">Delorme, Richard</searchLink><br /><searchLink fieldCode="AR" term="%22Bucci%2C+Maria+Pia%22">Bucci, Maria Pia</searchLink>
– Name: TitleSource
  Label: Source
  Group: Src
  Data: <searchLink fieldCode="SO" term="%22Autism%3A+The+International+Journal+of+Research+and+Practice%22"><i>Autism: The International Journal of Research and Practice</i></searchLink>. Apr 2020 24(3):670-679.
– Name: Avail
  Label: Availability
  Group: Avail
  Data: SAGE Publications. 2455 Teller Road, Thousand Oaks, CA 91320. Tel: 800-818-7243; Tel: 805-499-9774; Fax: 800-583-2665; e-mail: journals@sagepub.com; Web site: http://sagepub.com
– Name: PeerReviewed
  Label: Peer Reviewed
  Group: SrcInfo
  Data: Y
– Name: Pages
  Label: Page Count
  Group: Src
  Data: 10
– Name: DatePubCY
  Label: Publication Date
  Group: Date
  Data: 2020
– Name: TypeDocument
  Label: Document Type
  Group: TypDoc
  Data: Journal Articles<br />Reports - Research
– Name: Subject
  Label: Descriptors
  Group: Su
  Data: <searchLink fieldCode="DE" term="%22Psychomotor+Skills%22">Psychomotor Skills</searchLink><br /><searchLink fieldCode="DE" term="%22Eye+Movements%22">Eye Movements</searchLink><br /><searchLink fieldCode="DE" term="%22Autism%22">Autism</searchLink><br /><searchLink fieldCode="DE" term="%22Pervasive+Developmental+Disorders%22">Pervasive Developmental Disorders</searchLink><br /><searchLink fieldCode="DE" term="%22Comparative+Analysis%22">Comparative Analysis</searchLink><br /><searchLink fieldCode="DE" term="%22Matched+Groups%22">Matched Groups</searchLink><br /><searchLink fieldCode="DE" term="%22Student+Attitudes%22">Student Attitudes</searchLink><br /><searchLink fieldCode="DE" term="%22Brain+Hemisphere+Functions%22">Brain Hemisphere Functions</searchLink><br /><searchLink fieldCode="DE" term="%22Attention+Control%22">Attention Control</searchLink><br /><searchLink fieldCode="DE" term="%22Hospitals%22">Hospitals</searchLink><br /><searchLink fieldCode="DE" term="%22Foreign+Countries%22">Foreign Countries</searchLink><br /><searchLink fieldCode="DE" term="%22Observation%22">Observation</searchLink><br /><searchLink fieldCode="DE" term="%22Diagnostic+Tests%22">Diagnostic Tests</searchLink><br /><searchLink fieldCode="DE" term="%22Intelligence+Tests%22">Intelligence Tests</searchLink><br /><searchLink fieldCode="DE" term="%22Children%22">Children</searchLink><br /><searchLink fieldCode="DE" term="%22Behavior+Patterns%22">Behavior Patterns</searchLink>
– Name: Subject
  Label: Geographic Terms
  Group: Su
  Data: <searchLink fieldCode="DE" term="%22France+%28Paris%29%22">France (Paris)</searchLink>
– Name: SubjectThesaurus
  Label: Assessment and Survey Identifiers
  Group: Su
  Data: <searchLink fieldCode="SU" term="%22Autism+Diagnostic+Observation+Schedule%22">Autism Diagnostic Observation Schedule</searchLink><br /><searchLink fieldCode="SU" term="%22Wechsler+Intelligence+Scale+for+Children%22">Wechsler Intelligence Scale for Children</searchLink>
– Name: DOI
  Label: DOI
  Group: ID
  Data: 10.1177/1362361319882861
– Name: ISSN
  Label: ISSN
  Group: ISSN
  Data: 1362-3613
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: To identify quantitative indicators of social communication dysfunctions, we explored the oculomotor performances in subjects with autism spectrum disorders. Discordant findings in the literature have been reported for oculomotor behavior in subjects with autism spectrum disorders. This study aimed to explore reflexive and voluntary saccadic performance in a group of 32 children with autism spectrum disorders (mean age: 12.1 ± 0.5 years) compared to 32 age-, sex-, and IQ-matched typically developing children (control group). We used different types of reflexive and voluntary saccades: gap, step, overlap, and anti-saccades. Eye movements were recorded using an eye tracker (Mobile EBT®) and we measured latency, percentage of anticipatory and express saccades, errors of anti-saccades and gain. Children with autism spectrum disorders reported similar latency values with respect to typically developing children for reflexive and voluntary saccades; in contrast, they made more express and anticipatory saccades overall, as shown in paradigm testing (gap, step, overlap, and anti-saccades). Our findings support previous evidence of the atypicality of the cortical network, which is involved in saccade triggering and attentional processes in children with autism spectrum disorders.
– Name: AbstractInfo
  Label: Abstractor
  Group: Ab
  Data: As Provided
– Name: DateEntry
  Label: Entry Date
  Group: Date
  Data: 2020
– Name: AN
  Label: Accession Number
  Group: ID
  Data: EJ1250630
PLink https://search.ebscohost.com/login.aspx?direct=true&site=eds-live&db=eric&AN=EJ1250630
RecordInfo BibRecord:
  BibEntity:
    Identifiers:
      – Type: doi
        Value: 10.1177/1362361319882861
    Languages:
      – Text: English
    PhysicalDescription:
      Pagination:
        PageCount: 10
        StartPage: 670
    Subjects:
      – SubjectFull: Psychomotor Skills
        Type: general
      – SubjectFull: Eye Movements
        Type: general
      – SubjectFull: Autism
        Type: general
      – SubjectFull: Pervasive Developmental Disorders
        Type: general
      – SubjectFull: Comparative Analysis
        Type: general
      – SubjectFull: Matched Groups
        Type: general
      – SubjectFull: Student Attitudes
        Type: general
      – SubjectFull: Brain Hemisphere Functions
        Type: general
      – SubjectFull: Attention Control
        Type: general
      – SubjectFull: Hospitals
        Type: general
      – SubjectFull: Foreign Countries
        Type: general
      – SubjectFull: Observation
        Type: general
      – SubjectFull: Diagnostic Tests
        Type: general
      – SubjectFull: Intelligence Tests
        Type: general
      – SubjectFull: Children
        Type: general
      – SubjectFull: Behavior Patterns
        Type: general
      – SubjectFull: France (Paris)
        Type: general
      – SubjectFull: Autism Diagnostic Observation Schedule
        Type: general
      – SubjectFull: Wechsler Intelligence Scale for Children
        Type: general
    Titles:
      – TitleFull: Oculomotor Behavior in Children with Autism Spectrum Disorders
        Type: main
  BibRelationships:
    HasContributorRelationships:
      – PersonEntity:
          Name:
            NameFull: Caldani, Simona
      – PersonEntity:
          Name:
            NameFull: Steg, Sarah
      – PersonEntity:
          Name:
            NameFull: Lefebvre, Aline
      – PersonEntity:
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            NameFull: Atzori, Paola
      – PersonEntity:
          Name:
            NameFull: Peyre, Hugo
      – PersonEntity:
          Name:
            NameFull: Delorme, Richard
      – PersonEntity:
          Name:
            NameFull: Bucci, Maria Pia
    IsPartOfRelationships:
      – BibEntity:
          Dates:
            – D: 01
              M: 04
              Type: published
              Y: 2020
          Identifiers:
            – Type: issn-print
              Value: 1362-3613
          Numbering:
            – Type: volume
              Value: 24
            – Type: issue
              Value: 3
          Titles:
            – TitleFull: Autism: The International Journal of Research and Practice
              Type: main
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