Electrophysiological evidence for selective impairment of optic flow perception in autism spectrum disorder

People with autism spectrum disorder (ASD) often show inferior global motion performance with superior performance in detail form perception, suggesting dysfunction of the dorsal visual stream. To elucidate the neural basis of impaired global motion perception in ASD, we measured psychophysical threshold and visual event-related potentials (ERPs) with a 128-channel system in 12 ASD and 12 healthy control adults. Radial optic flow (OF) and horizontal motion (HO) were used as the visual stimuli. The former was related to the ventro-dorsal stream formed by the inferior parietal lobule, while the latter was conveyed from the dorso-dorsal stream formed by the superior parietal lobule. No significant group differences were observed in the motion thresholds for both OF and HO. N170 and P200 were elicited as major components of ERPs in both groups. However, the latencies of both components for OF but not HO were significantly prolonged in ASD compared with the control group. Our ERP results suggest that ASD has a selective impairment for OF processing even though the psychophysical thresholds are preserved. Therefore, we provide the first electrophysiological evidence for altered function of the higher-level dorsal visual stream in ASD, specifically the ventro-dorsal stream closely related to OF perception.     

Contrast sensitivity for motion detection and direction discrimination in adolescents with autism spectrum disorders and their siblings

The magnocellular (M) pathway hypothesis proposes that impaired visual motion perception observed in individuals with Autism Spectrum Disorders (ASD) might be mediated by atypical functioning of the subcortical M pathway, as this pathway provides the bulk of visual input to cortical motion detectors. To test this hypothesis, we measured luminance and chromatic contrast sensitivity, thought to tap M and Parvocellular (P) pathway processing, respectively. We also tested the hypothesis that motion processing is impaired in ASD using a novel paradigm that measures motion processing while controlling for detectabilty. Specifically, this paradigm compares contrast sensitivity for detection of a moving grating with contrast sensitivity for direction-of-motion discrimination of that same moving grating. Contrast sensitivities from adolescents with ASD were compared to typically-developing adolescents, and also unaffected siblings of individuals with ASD (SIBS). The results revealed significant group differences on P, but not M, pathway processing, with SIBS showing higher chromatic contrast sensitivity than both participants with ASD and TD participants. This atypicality, unique to SIBS, suggests the possible existence of a protective factor in these individuals against developing ASD. The results also revealed impairments in motion perception in both participants with ASD and SIBS, which may be an endophenotype of ASD. This impairment may be driven by impairments in motion detectors and/or by reduced input from neural areas that project to motion detectors, the latter possibility being consistent with the notion of reduced connectivity between neural areas in ASD.     

Disrupted action perception in autism: behavioral evidence, neuroendophenotypes, and diagnostic utility

Disruptions in the visual perception of biological motion are emerging as a hallmark of autism spectrum disorder (ASD), consistent with the pathognomonic social deficits of this neurodevelopmental disorder. Accumulating evidence suggests an early and marked divergence in ASD from the typical developmental tuning of brain regions to process social information. In this review, we discuss a relatively recent yet substantial literature of behavioral and neuroimaging studies that consistently indicates impairments in biological motion perception in ASD. We then illustrate the fundamental disruption in this form of social perception in autism, drawing connections between a genetic liability to develop autism and disrupted associated brain mechanisms, as we describe neuroendophenotypes of autism derived from an fMRI study of biological motion perception in children with autism and their unaffected siblings. Finally, we demonstrate the diagnostic utility of brain responses to biological motion. With the ability to measure brain function in the first year of life comes the potential to chart the development of disrupted biological motion processing in ASD and to specify the gene-brain-behavior interactions shaping this atypical trajectory. We propose that a comprehensive understanding of the development of impaired responses to biological motion in ASD can inform future diagnosis and treatment approaches.     

Perception of biological motion in autism spectrum disorders

In individuals with autism or autism-spectrum-disorder (ASD), conflicting results have been reported regarding the processing of biological motion tasks. As biological motion perception and recognition might be related to impaired imitation, gross motor skills and autism specific psychopathology in individuals with ASD, we performed a functional MRI study on biological motion perception in a sample of 15 adolescent and young adult individuals with ASD and typically developing, age, sex and IQ matched controls. Neuronal activation during biological motion perception was compared between groups, and correlation patterns of imitation, gross motor and behavioral measures with neuronal activation were explored. Differences in local gray matter volume between groups as well as correlation patterns of psychopathological measures with gray matter volume were additionally compared. On the behavioral level, recognition of biological motion was assessed by a reaction time (RT) task. Groups differed strongly with regard to neuronal activation and RT, and differential correlation patterns with behavioral as well as with imitation and gross motor abilities were elicited across and within groups. However, contrasting with the initial hypothesis, additional differences between groups were observed during perception and recognition of spatially moving point lights in general irrespective of biological motion. Results either point towards difficulties in higher-order motion perception or in the integration of complex motion information in the association cortex. This interpretation is supported by differences in gray matter volume as well as correlation with repetitive behavior bilaterally in the parietal cortex and the right medial temporal cortex. The specific correlation of neuronal activation during biological motion perception with hand-finger imitation, dynamic balance and diadochokinesis abilities emphasizes the possible relevance of difficulties in biological motion perception or impaired self-other matching for action imitation and gross motor difficulties in individuals with ASD.     

Coherent motion processing in autism spectrum disorder (ASD): An fMRI study

A deficit in global motion processing caused by a specific dysfunction of the visual dorsal pathway has been suggested to underlie perceptual abnormalities in subjects with autism spectrum disorders (ASD). However, the neural mechanisms associated with abnormal motion processing in ASD remain poorly understood. We investigated brain responses related to the detection of coherent and random motion in 15 male subjects with ASD and 15 age- and IQ-matched healthy controls (aged 13-19 years) using event-related functional magnetic resonance imaging (fMRI). Behaviorally, no significant group differences were observed between subjects with ASD and controls. Neurally, subjects with ASD showed increased brain activation in the left primary visual cortex across all conditions compared with controls. A significant interaction effect between group and condition was observed in the right superior parietal cortex resulting from increased neural activity in the coherent compared with the random motion conditions only in the control group. In addition, neural activity in area V5 was not differentially modulated by specific motion conditions in subjects with ASD. Functional connectivity analyses revealed positive correlations between the primary visual cortex and area V5 within both hemispheres, but no significant between-group differences in functional connectivity patterns along the dorsal stream. The data suggest that motion processing in ASD results in deviant activations in both the lower and higher processing stages of the dorsal pathway. This might reflect differences in the perception of visual stimuli in ASD, which possibly result in impaired integration of motion signals.     

Right Temporoparietal Gray Matter Predicts Accuracy of Social Perception in the Autism Spectrum

Individuals with an autism spectrum disorder (ASD) show hallmark deficits in social perception. These difficulties might also reflect fundamental deficits in integrating visual signals. We contrasted predictions of a social perception and a spatial–temporal integration deficit account. Participants with ASD and matched controls performed two tasks: the first required spatiotemporal integration of global motion signals without social meaning, the second required processing of socially relevant local motion. The ASD group only showed differences to controls in social motion evaluation. In addition, gray matter volume in the temporal–parietal junction correlated positively with accuracy in social motion perception in the ASD group. Our findings suggest that social–perceptual difficulties in ASD cannot be reduced to deficits in spatial–temporal integration.     

Attentional effects of gaze shifts are influenced by emotion and spatial frequency, but not in autism

ObjectiveImpaired gaze following is an important hallmark of autism spectrum disorders (ASDs) in clinical settings. Yet, ASD subjects perform normally on laboratory tasks involving gaze shifts. We investigated this contradiction, hypothesizing that impaired gaze following in ASDs is not related to basic impairments in attention orienting but to impaired emotion perception and abnormal processing of spatial frequencies (i.e., local and global information).MethodWe tested 30 high-functioning, school-age children with ASDs and 30 age- and IQ-matched controls on a task involving gaze shifts that cue the location of targets. The cueing faces differed in emotionality and were filtered for different spatial frequencies. We recorded behavioral responses (reaction times) and brain responses (event-related potentials).ResultsASD subjects performed normally when neutral faces were used. However, emotional faces elicited modified face and gaze cue processing in control subjects, but not in the ASD subjects. Furthermore, the control group was biased toward the use of low spatial frequencies (global information) to process gaze cues, whereas the ASD group was biased toward the use of high spatial frequencies (local information).ConclusionsWe conclude that impaired gaze following in ASDs is related to impaired emotion processing. Moreover, ASD subjects show an abnormal reliance on local information to process gaze cues.     

Direction-specific motion blindness induced by focal stimulation of human extrastriate cortex

Motion blindness (MB) or akinetopsia is the selective disturbance of visual motion perception while other features of the visual scene such as colour and shape are normally perceived. Chronic and transient forms of MB are characterized by a global deficit of direction discrimination (pandirectional), which is generally assumed to result from damage to, or interference with, the motion complex MT+/V5. However, the most characteristic feature of primate MT-neurons is not their motion specificity, but their preference for one direction of motion (direction specificity). Here, we report that focal electrical stimulation in the human posterior temporal lobe selectively impaired the perception of motion in one direction while the perception of motion in other directions was completely normal (unidirectional MB). In addition, the direction of MB was found to depend on the brain area stimulated. It is argued that direction specificity for visual motion is not only represented at the single neuron level, but also in much larger cortical units.     

IQ Predicts Biological Motion Perception in Autism Spectrum Disorders

Biological motion is easily perceived by neurotypical observers when encoded in point-light displays. Some but not all relevant research shows significant deficits in biological motion perception among those with ASD, especially with respect to emotional displays. We tested adults with and without ASD on the perception of masked biological motion and the perception of direction from coherent and scrambled biological motion. Within the autism spectrum group, there was a large and statistically significant relationship between IQ and the ability to perceive directionality in masked biological motion. There were no group differences in sensitivity to biological motion or the ability to identify the direction of motion. Possible explanations are discussed, including the possible use of compensatory strategies in high IQ ASD.     

Children with autism spectrum disorders are less proficient in action identification and lacking a preference for upright point-light biological motion displays

Recent studies demonstrated impaired biological motion perception in children with autism spectrum disorder (ASD), who are characterized by deficits in social interactions and communication. Using point-light displays, the present study intended to examine the looking preferences for human and non-human biological motion paired with non-biological scrambled motion (Exp. 1) and the performance on the action identification task (Exp. 2) in typically developing (TD) children and children with ASD. Forty-two participants (21 ASD and 21 TD children) aged 3–7 years were included in this study. In Exp. 1, we found that children with ASD did not preferentially attend to biological motion as TD children did. The ASD group also exhibited shorter overall fixation time for all the point-light displays than did the TD group. In the action identification task of Exp. 2, children with ASD made more errors in naming and needed more time to respond than did TD children. Nevertheless, the actions that were likely to be correctly identified by TD children were also likely to be correctly identified by children with ASD. In conclusion, children with ASD are lacking the preference TD children have for biological motion stimuli over the scrambled motion. Moreover, such impairment might be due to an overall deficit in processing biological motion information and may explain the poor performance on action recognition in the ASD group.     

A review of behavioural and electrophysiological studies on auditory processing and speech perception in autism spectrum disorders

This literature review aims to interpret behavioural and electrophysiological studies addressing auditory processing in children and adults with autism spectrum disorder (ASD). Data have been organised according to the applied methodology (behavioural versus electrophysiological studies) and according to stimulus complexity (pure versus complex tones versus speech sounds). In line with the weak central coherence (WCC) theory of autism we aimed to investigate whether individuals with ASD show a more locally and less globally oriented processing style in the auditory modality. To avoid the possible confound of stimulus complexity, this influence was taken into account as an additional hypothesis. The review reveals that the identification and discrimination of isolated acoustic features (in particular pitch processing) is generally intact or enhanced in individuals with ASD, for pure as well as for complex tones and speech sounds. It thus appears that the local processing advantage is not influenced by stimulus complexity. Individuals with ASD are also less susceptible to global interference of speech-like material. A deficit in global auditory processing, however, is less universally confirmed. We propose that the observed pattern of auditory enhancements and deficits in ASD may be related to an atypical pattern of right hemisphere dominance. As the right and left hemisphere are relatively more specialized in spectral versus temporal auditory processing, respectively, right hemisphere dominance in ASD could provoke enhanced pitch and vowel processing, whereas left hemisphere deficiencies might explain speech perception problems and temporal processing deficits.     

Selective impairment in visual perception of biological motion in obsessive-compulsive disorder

Obsessive-compulsive disorder (OCD) is associated with a variety of well-documented cognitive deficits such as deficits in memory and executive functioning, but little is known about basic perceptual concomitants of OCD. This study investigated global, configural processing in OCD using dynamic (moving) and static stimuli with minimal demands on cognitive function. Twenty OCD patients and 16 age- and education-matched healthy control subjects were tested on four perceptual tasks: two motion tasks involved detection and discrimination of human activity portrayed by point-light animations ("biological" motion). The other two tasks involved detection of coherent, translational motion defined by random-dot cinematograms and detection of static global shape defined by spatially distributed contours. OCD patients exhibited impaired performance on biological motion tasks; in contrast, their performance on tasks of coherent motion detection and global form perception were comparable to those of healthy controls. These results indicate that OCD patients have a specific deficit in perceiving biological motion signals, whereas their perception of non-biological coherent motion and static global shape is intact. Because efficient social interactions depend on accurate and rapid perception of subtle socially relevant cues, deficits in biological motion perception may compromise social functioning in people with OCD.     

Role of primary visual cortex in the binocular integration of plaid motion perception

This study assessed the early mechanisms underlying perception of plaid motion. Thus, two superimposed gratings drifting in a rightward direction composed plaid stimuli whose global motion direction was perceived as the vector sum of the two components. The first experiment was aimed at comparing the perception of plaid motion when both components were presented to both eyes (dioptic) or separately to each eye (dichoptic). When components of the patterns had identical spatial frequencies, coherent motion was correctly perceived under dioptic and dichoptic viewing condition. However, the perceived direction deviated from the predicted direction when spatial frequency differences were introduced between components in both conditions. The results suggest that motion integration follows similar rules for dioptic and dichoptic plaids even though performance under dichoptic viewing did not reach dioptic levels. In the second experiment, the role of early cortical areas in the processing of both plaids was examined. As convergence of monocular inputs is needed for dichoptic perception, we tested the hypothesis that primary visual cortex (V1) is required for dichoptic plaid processing by delivering repetitive transcranial magnetic stimulation to this area. Ten minutes of magnetic stimulation disrupted subsequent dichoptic perception for approximately 15 min, whereas no significant changes were observed for dioptic plaid perception. Taken together, these findings suggest that V1 is not crucial for the processing of dioptic plaids but it is necessary for the binocular integration underlying dichoptic plaid motion perception.     

Temporal characteristics of global motion processing revealed by transcranial magnetic stimulation

The ability to detect the motion of objects is critical to survival, and understanding the cortical mechanisms involved in this process remains a key challenge in sensory neuroscience. A relatively new approach to this problem is to temporarily disrupt processing at specific cortical sites and measure the behavioural consequences. Several previous studies have shown that transcranial magnetic stimulation (TMS) of human visual area V5/MT disrupts global motion perception, but reports vary widely in the timescale of this effect. To resolve this issue we employed psychophysical techniques to investigate how discrimination of translational, rotational and radial global motion is affected by TMS. Prior to applying TMS we established baseline coherence thresholds for global motion perception. Adopting each observer’s coherence level at threshold we examined how TMS delivered to V5/MT modulated performance. Importantly, we measured the influence of single‐pulse TMS over a broad temporal range to reveal the fine temporal structure of the disruption profile for global motion perception. Results show that the disruption profile consisted of two distinct epochs during which global direction judgments were reliably impaired, separated by an interval in which performance was unaffected. The bimodal nature of the distribution profiles is consistent with feedforward and feedback processing between visual areas mediating global motion processing. We present a novel quantitative model that characterizes the contribution of each process to visual motion perception.     

Impaired Timing and Frequency Discrimination in High-functioning Autism Spectrum Disorders

Individuals with autism spectrum disorders (ASD) frequently demonstrate preserved or enhanced frequency perception but impaired timing perception. The present study investigated the processing of spectral and temporal information in 12 adolescents with ASD and 15 age-matched controls. Participants completed two psychoacoustic tasks: one determined frequency difference limens, and the other determined gap detection thresholds. Results showed impaired frequency discrimination at the highest standard frequency in the ASD group but no overall difference between groups. However, when groups were defined by auditory hyper-sensitivity, a group difference arose. For the gap detection task, the ASD group demonstrated elevated thresholds. This supports previous research demonstrating a deficit in ASD in temporal perception and suggests a connection between hyper-sensitivity and frequency discrimination abilities.     

Monitoring in language perception in high-functioning adults with autism spectrum disorder: Evidence from event-related potentials

ObjectivesAutism spectrum disorder (ASD) is characterized by impaired global language processing, whereas local language processing often appears intact. Recent psycholinguistic research suggests that the quality of language perception relies on monitoring, an aspect of executive control. The aim of the study was to examine monitoring in people with ASD of (a) local, orthographic violations, and (b) global, syntactic violations, when provided with single level versus dual level task instructions.MethodsWe recorded event-related potentials and compared P600 effects to the linguistic violations relative to correct words in 14 adults with ASD and 14 matched controls.ResultsIn control participants, local errors elicited a monitoring response as tapped by the P600 effect in both conditions. For global errors, the P600 effect was present only at one centroposterior site in the single level condition, whereas in the dual level condition a broadly distributed effect was obtained. People with ASD, however, showed a monitoring response to local and global errors both in the single and dual level condition.ConclusionsThe main ERP finding suggests that when instructed people with ASD monitor global aspects of language already under simple circumstances, whereas people without ASD mainly do so under more complex circumstances.SignificanceResults suggest that language problems in ASD should not be studied in terms of a linguistic dysfunction as such, but in light of the use of executive resources during language comprehension.     

Impaired visual recognition of biological motion in schizophrenia

BACKGROUND: Motion perception deficits have been suggested to be an important feature of schizophrenia but the behavioral consequences of such deficits are unknown. Biological motion refers to the movements generated by living beings. The human visual system rapidly and effortlessly detects and extracts socially relevant information from biological motion. A deficit in biological motion perception may have significant consequences for detecting and interpreting social information. METHODS: Schizophrenia patients and matched healthy controls were tested on two visual tasks: recognition of human activity portrayed in point-light animations (biological motion task) and a perceptual control task involving detection of a grouped figure against the background noise (global-form task). Both tasks required detection of a global form against background noise but only the biological motion task required the extraction of motion-related information. RESULTS: Schizophrenia patients performed as well as the controls in the global-form task, but were significantly impaired on the biological motion task. In addition, deficits in biological motion perception correlated with impaired social functioning as measured by the Zigler social competence scale [Zigler, E., Levine, J. (1981). Premorbid competence in schizophrenia: what is being measured? Journal of Consulting and Clinical Psychology, 49, 96-105.]. CONCLUSION: The deficit in biological motion processing, which may be related to the previously documented deficit in global motion processing, could contribute to abnormal social functioning in schizophrenia.     

Parvocellular pathway impairment in autism spectrum disorder: Evidence from visual evoked potentials

In humans, visual information is processed via parallel channels: the parvocellular (P) pathway analyzes color and form information, whereas the magnocellular (M) stream plays an important role in motion analysis. Individuals with autism spectrum disorder (ASD) often show superior performance in processing fine detail, but impaired performance in processing global structure and motion information. To date, no visual evoked potential (VEP) studies have examined the neural basis of atypical visual performance in ASD. VEPs were recorded using 128-channel high density EEG to investigate whether the P and M pathways are functionally altered in ASD. The functioning of the P and M pathways within primary visual cortex (V1) were evaluated using chromatic (equiluminant red–green sinusoidal gratings) and achromatic (low contrast black–white sinusoidal gratings) stimuli, respectively. Unexpectedly, the N1 component of VEPs to chromatic gratings was significantly prolonged in ASD patients compared to controls. However, VEP responses to achromatic gratings did not differ significantly between the two groups. Because chromatic stimuli preferentially stimulate the P-color but not the P-form pathway, our findings suggest that ASD is associated with impaired P-color pathway activity. Our study provides the first electrophysiological evidence for P-color pathway impairments with preserved M function at the V1 level in ASD.     

Differential electrophysiological responses to biological motion in children and adults with and without autism spectrum disorders

Although atypical processing of biological motion (BM) in individuals with autism spectrum disorder (ASD) has been reported, the temporal profile of the neural response to BM is not well explored. In the current study, event-related potentials (ERPs) were measured in 12 individuals with ASD, aged 8–22 years, and 12 age- and gender-matched normal controls, to investigate the electrophysiological response to BM and a control visual stimulus. By introducing a novel experimental paradigm that can dissociate the electrophysiological responses to motion processing and the global shape processing of BM, we found that: (1) the timing of the response was preserved in ASD groups, whereas (2) the ERP response to BM was significantly enhanced compared with scrambled point-light motion (SM) in normal controls; the responses to both BM and SM were not significantly different in subjects with ASD. Because we did not find a significant group effect on the peak and mean amplitude induced by BM, it is presumed that this atypical response in individuals with ASD was due to over-sensitivity to the local motion signals. This experimental paradigm showed atypical local motion processing of BM in individuals with ASD.     

The perception of social and mechanical causality in young children with ASD

This study investigated perceptual causality in launch and reaction events in children with ASD (CA = 8.4, VMA = 5.1) and mental age matched controls with typical development and learning difficulties. This is of interest because difficulties with global processing in autism suggest that individuals with ASD may not ‘see’ causal Gestalts in general, and specific difficulties with reaction perception could be related to difficulties with TOM. Participants matched pictures depicting mechanical and psychological cause and non-causality to computer animated launch and reaction events and delayed control events. Children with ASD showed the typical response to reaction events, matching them with the picture for psychological cause, but they were impaired in launch perception compared to control participants. We discuss the possibility that event duration may be the critical difference between the causal events. The information allowing identification of a reaction is conveyed over a longer time frame (600 ms here) than in launching (21 ms here). This may allow for the deployment of global processes and/or attentional shifts in reaction, but not launch perception.