Early-Stage Visual Processing Abnormalities in ASD by Investigating Erps Elicited in a Visual of Medicine, Louisville, KY 40202 Oddball Task Using Illusory Figures
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Communication • DOI: 10.2478/v10134-010-0024-9 • Translational Neuroscience • 1(2) •2010 •177–187 Translational Neuroscience EARLy-stAGE VISUAL PROCESSING ABNORMALITIES Joshua M. Baruth1*, Manuel F. Casanova1,2, Lonnie Sears3, IN high-funcTIONING AUTISM 2 SPECTRUM DISORDEr (ASD) Estate Sokhadze Abstract 1Department of Anatomical Sciences and It has been reported that individuals with autism spectrum disorder (ASD) have abnormal responses to the Neurobiology, University of Louisville sensory environment. For these individuals sensory overload can impair functioning, raise physiological School of Medicine, Louisville, KY 40202 stress, and adversely affect social interaction. Early-stage (i.e. within 200 ms of stimulus onset) auditory 2 processing abnormalities have been widely examined in ASD using event-related potentials (ERP), while Department of Psychiatry and Behavioral ERP studies investigating early-stage visual processing in ASD are less frequent. We wanted to test the Sciences, University of Louisville School hypothesis of early-stage visual processing abnormalities in ASD by investigating ERPs elicited in a visual of Medicine, Louisville, KY 40202 oddball task using illusory figures. Our results indicate that individuals with ASD have abnormally large 3Department of Pediatrics, University of cortical responses to task irrelevant stimuli over both parieto-occipital and frontal regions-of-interest Louisville School of Medicine, (ROI) during early stages of visual processing compared to the control group. Furthermore, ASD patients showed signs of an overall disruption in stimulus discrimination, and had a significantly higher rate of Louisville, KY 40202 motor response errors. Keywords Autism • Event-related potentials • EEG • Visual processing • Evoked potentials Received 8 June 2010 © Versita Sp. z o.o. accepted 24 June 2010 1. Introduction Event-related potentials (ERP) provide a Auditory processing abnormalities have unique method of characterizing the magnitude been widely examined in ASD using ERPs (see Autism Spectrum Disorder (ASD) includes and time course of brain activity associated [14] for review). Briefly, individuals with ASD three conditions sharing a similar core with both auditory and visual perception. ERPs have been shown to have normal brainstem symptomatology: Autism, Asperger syndrome, represent transient changes in the electrical auditory evoked potentials (AEPs) [15,16]. and Pervasive Developmental Disorder Not activity of the brain in response to a given However, the most consistently reported Otherwise Specified (PDD-NOS). ASD is stimulus or event [6] and consist of component auditory ERP abnormality is attenuated characterized by severe disturbances in reciprocal waveforms spanning from as early as 50 ms post- amplitude of the centroparietal P300 in social relations, varying degrees of language stimulus to up to 600-1000 ms post-stimulus. various auditory stimulus presentation and communication difficulty, and restricted, For example, in the components N100 and paradigms in ASD patients of all ages [17] . repetitive and stereotyped behavioral patterns P200 the letter indicates the polarity and the Also, the short-latency fronto-central N100 [1]. It has also been suggested that individuals number indicates the period after onset of the has reliably been found to be attenuated with ASD have sensory abnormalities indicated by stimulus, i.e. 100 is in the 100-200 ms period in amplitude and latency during tasks hypersensitivity and an extraordinary interest in (or earlier) and 200 is in the 200-300 ms period involving target detection and tones of certain sensations [2]. In fact, it has been proposed [7,8]. Generally components in the first 50- varying frequency and intensity [18-21]. that sensory-perceptual abnormalities are 200 ms are considered early, exogenous field Furthermore, the mismatch negativity present in approximately 90% of individuals with potentials reflecting ‘pre-attentive’ processes (MMN), a large negative deflection occurring autism [3]. An avoidance of external stimulation and the processing of physical attributes of when frequent stimuli are subtracted from in ASD may be due to altered inhibitory control a stimulus [9,10] while those after 200 ms infrequent stimuli, has commonly been of sensory intake [4], and for these individuals represent endogenous field potentials reflecting found to be prolonged in latency in response sensory overload can impair functioning, raise polymodal associative processing and later- to pitch deviants [22-24]. physiological stress, and adversely affect social stage attentional processes (e.g. sustained ERP studies investigating early-stage visual interaction [5]. attention, perceptual closure) [11-13]. processing in ASD are less frequent (see [6] * E-mail: [email protected] 177 Translational Neuroscience for review) especially in comparison to other cortex [51] with a contribution from parieto- disrupt stimulus discrimination as compared to psychopathologies like schizophrenia [25-29]. occipital and occipito-temporal areas [49,52]; the control group. ERP studies of visual processing commonly while the visual N100 over frontal electrode sites employ an ‘oddball’ discrimination task in which most likely is reflective of frontal generators 2. Experimental Procedures the participant responds to an infrequent [43]. The visual N100 generally is augmented target stimulus among more frequent non- during attentional stimulus processing, which 2.1 Participants target stimuli [30]. Most investigations into is also know as the ‘N1-effect’ [53], and is larger Participants with autism spectrum disorder visual processing in ASD have focused on towards task-relevant target stimuli [7,48]. (ASD) (age range 9 to 20 years) were recruited higher-level, long-latency ERPs, like the P300 The visual P200 over frontal electrode sites through the University of Louisville Weisskopf [31-39]. In brief centroparietal P300 amplitude is generally found in a latency range of 180– Child Evaluation Center (WCEC). Diagnosis has been found to be similar [31-33,38,39] 320 ms poststimulus and has been reported was made according to the Diagnostic and reduced [34,37] and augmented [36] in ASD in working memory and attention tasks. Statistical Manual of Mental Disorders (DSM- patients to target stimuli compared to controls. Kenemans, Kok, & Smulders [54] described this IV-TR) [1] and further ascertained with the Remarkably to our knowledge there have only frontal positivity as a component that indexes Autism Diagnostic Interview – Revised (ADI-R) been two studies reporting on short-latency the hierarchical selection of task-relevant [57]. They also had a medical evaluation by a (i.e., 50-200 ms) visual ERPs in ASD and one features for further processing. Over inferior developmental pediatrician. All subjects had was by our group [40]; Courchesne et al. [32] frontal recording sites source localization normal hearing based on past hearing screens. included the N100 and P200 among later places dipoles of this component in the Participants either had normal vision or wore components in their analysis. orbito-frontal cortex [55,56]. The visual P200 corrective lenses. Participants with a history Visual processing is based on a core system over posterior regions has been less studied of seizure disorder, significant hearing or visual consisting of occipito-temporal regions in but likely is associated with generators in the impairment, a brain abnormality conclusive extrastriate visual cortex [41] although parietal primary visual cortex and extrastriate areas from imaging studies or an identified genetic [42] and frontal [43] regions also play a role in reflecting visual categorization processes. disorder were excluded. All participants were directing visual attention. The earliest electrical The present study was designed to evaluate high-functioning persons with ASD with full- sign of cortical activity observed in humans the cortical responses of Kanizsa visual stimuli scale IQ > 80 assessed using the Wechsler (commonly referred to the P100) during visual evoked at short latencies over frontal and Intelligence Scale for Children, Fourth Edition tasks [44] can occur as early as 50 ms post parieto-occipital regions-of-interest (ROI) [58] or the Wechsler Abbreviated Scale of stimulus [45] to as late as 160 ms depending on in both children with ASD and typical age- Intelligence [59]. topography and visual task and reflects early matched controls: Kanizsa stimuli consist of Controls were recruited through categorization and recognition processes [46]. inducer disks of a shape feature and either advertisements in the local media. All control The visual P100 likely has posterior generators constitute an illusory figure (square, triangle) participants were free of neurological or in the primary visual cortex, extrastriate areas or not (colinearity feature). For the purposes significant medical disorders, had normal [29] and fusiform gyrus [47], while the anterior of this study the stimuli consisted of Kanizsa hearing and vision, and were free of psychiatric, P100 likely reflects the activation of frontal targets, Kanizsa non-targets, and non-Kanizsa learning, or developmental disorders generators [43]. The P100 may reflect early stimuli. We focused our analysis on short- based on self- and parent reports. Subjects sensory processing of attended stimuli [41] and latency field potentials, P50, N100, and were screened for history of psychiatric or is generally larger to attended visual stimuli