Initial eye gaze to faces and its functional consequence on face identification abilities in autism spectrum disorder.
ABSTRACT: BACKGROUND:Autism spectrum disorder (ASD) is a neurodevelopmental disorder defined and diagnosed by core deficits in social communication and the presence of restricted and repetitive behaviors. Research on face processing suggests deficits in this domain in ASD but includes many mixed findings regarding the nature and extent of these differences. The first eye movement to a face has been shown to be highly informative and sufficient to achieve high performance in face identification in neurotypical adults. The current study focused on this critical moment shown to be essential in the process of face identification. METHODS:We applied an established eye-tracking and face identification paradigm to comprehensively characterize the initial eye movement to a face and test its functional consequence on face identification performance in adolescents with and without ASD (n = 21 per group), and in neurotypical adults. Specifically, we presented a series of faces and measured the landing location of the first saccade to each face, while simultaneously measuring their face identification abilities. Then, individuals were guided to look at specific locations on the face, and we measured how face identification performance varied as a function of that location. Adolescent participants also completed a more traditional measure of face identification which allowed us to more fully characterize face identification abilities in ASD. RESULTS:Our results indicate that the location of the initial look to faces and face identification performance for briefly presented faces are intact in ASD, ruling out the possibility that deficits in face perception, at least in adolescents with ASD, begin with the initial eye movement to the face. However, individuals with ASD showed impairments on the more traditional measure of face identification. CONCLUSION:Together, the observed dissociation between initial, rapid face perception processes, and other measures of face perception offers new insights and hypotheses related to the timing and perceptual complexity of face processing and how these specific aspects of face identification may be disrupted in ASD.
Project description:Speech information inherent in face movements is important for understanding what is said in face-to-face communication. Individuals with autism spectrum disorders (ASD) have difficulties in extracting speech information from face movements, a process called visual-speech recognition. Currently, it is unknown what dysfunctional brain regions or networks underlie the visual-speech recognition deficit in ASD. We conducted a functional magnetic resonance imaging (fMRI) study with concurrent eye tracking to investigate visual-speech recognition in adults diagnosed with high-functioning autism and pairwise matched typically developed controls. Compared to the control group (n?=?17), the ASD group (n?=?17) showed decreased Blood Oxygenation Level Dependent (BOLD) response during visual-speech recognition in the right visual area 5 (V5/MT) and left temporal visual speech area (TVSA) - brain regions implicated in visual-movement perception. The right V5/MT showed positive correlation with visual-speech task performance in the ASD group, but not in the control group. Psychophysiological interaction analysis (PPI) revealed that functional connectivity between the left TVSA and the bilateral V5/MT and between the right V5/MT and the left IFG was lower in the ASD than in the control group. In contrast, responses in other speech-motor regions and their connectivity were on the neurotypical level. Reduced responses and network connectivity of the visual-movement regions in conjunction with intact speech-related mechanisms indicate that perceptual mechanisms might be at the core of the visual-speech recognition deficit in ASD. Communication deficits in ASD might at least partly stem from atypical sensory processing and not higher-order cognitive processing of socially relevant information.
Project description:Face processing has been found to be impaired in autism spectrum disorders (ASD). One hypothesis is that individuals with ASD engage in piecemeal compared to holistic face processing strategies. To investigate the role of possible impairments in holistic face processing in individuals with autism, the current study investigated behavioral and electroencephalography (EEG) correlates of face processing (P1/N170 and gamma-band activity) in adolescents with ASD and sex-, age-, and IQ-matched neurotypical controls.Participants were presented with upright and inverted Mooney stimuli; black and white low information faces that are only perceived as faces when processed holistically. Participants indicated behaviorally the detection of a face. EEG was collected time-locked to the presentation of the stimuli.Adolescents with ASD perceived Mooney stimuli as faces suggesting ability to use holistic processing but displayed a lower face detection rate and slower response times. ERP components suggest slowed temporal processing of Mooney stimuli in the ASD compared to control group for P1 latency but no differences between groups for P1 amplitude and at the N170. Increases in gamma-band activity was similar during the perception of the Mooney images by group, but the ASD group showed prolonged temporal elevation in activity.Overall, our results suggest that adolescents with ASD were able to utilize holistic processing to perceive a face within the Mooney stimuli. Delays in early processing, marked by the P1, and elongated elevation in gamma activity indicate that the neural systems supporting holistic processing are slightly altered suggesting a less automatic and less efficient facial processing system.Non-applicable.
Project description:Eye-movement patterns are often utilized in studies of visual perception as indices of the specific information extracted to efficiently process a given stimulus during a given task. Our prior work, however, revealed that not only the stimulus and task influence eye-movements, but that visuomotor (start position) factors also robustly and characteristically influence eye-movement patterns to faces (Arizpe et al., 2012). Here we manipulated lateral starting side and distance from the midline of face and line-symmetrical control (butterfly) stimuli in order to further investigate the nature and generality of such visuomotor influences. First we found that increasing starting distance from midline (4°, 8°, 12°, and 16° visual angle) strongly and proportionately increased the distance of the first ordinal fixation from midline. We did not find influences of starting distance on subsequent fixations, however, suggesting that eye-movement plans are not strongly affected by starting distance following an initial orienting fixation. Further, we replicated our prior effect of starting side (left, right) to induce a spatially contralateral tendency of fixations after the first ordinal fixation. However, we also established that these visuomotor influences did not depend upon the predictability of the location of the upcoming stimulus, and were present not only for face stimuli but also for our control stimulus category (butterflies). We found a correspondence in overall left-lateralized fixation tendency between faces and butterflies. Finally, for faces, we found a relationship between left starting side (right sided fixation pattern tendency) and increased recognition performance, which likely reflects a cortical right hemisphere (left visual hemifield) advantage for face perception. These results further indicate the importance of considering and controlling for visuomotor influences in the design, analysis, and interpretation of eye-movement studies.
Project description:There is ample behavioral evidence of diminished orientation towards faces as well as the presence of face perception impairments in autism spectrum disorder (ASD), but the underlying mechanisms of these deficits are still unclear. We used face-like object stimuli that have been shown to evoke pareidolia in typically developing (TD) individuals to test the effect of a global face-like configuration on orientation and perceptual processes in young children with ASD and age-matched TD controls. We show that TD children were more likely to look first towards upright face-like objects than children with ASD, showing that a global face-like configuration elicit a stronger orientation bias in TD children as compared to children with ASD. However, once they were looking at the stimuli, both groups spent more time exploring the upright face-like object, suggesting that they both perceived it as a face. Our results are in agreement with abnormal social orienting in ASD, possibly due to an abnormal tuning of the subcortical pathway, leading to poor orienting and attention towards faces. Our results also indicate that young children with ASD can perceive a generic face holistically, such as face-like objects, further demonstrating holistic processing of faces in ASD.
Project description:Autism spectrum disorder (ASD) is characterized by deficits in social functioning and difficulties in forming social bonds. According to the social motivation theory of ASD, people with ASD fail to attend social stimuli because they do not experience them as rewarding, resulting in deficits in social cognition. In neurotypical (NT) individuals, more rewarding faces have been shown to elicit greater spontaneous facial mimicry. This association between reward and mimicry is reduced in people with high autistic traits, suggesting that altered reward processing might explain the deficits in spontaneous facial mimicry observed in individuals with ASD. In a previous study, we observed that learned reward value of a face modulates mimicry-related neural response to it and that this modulation is reduced in people with high autistic traits. Using an identical evaluative conditioning paradigm where neutral faces were conditioned with high and low rewards, we tested the modulating effect of reward value on mimicry-related brain activity in a group of adults with and without ASD. We focused on the activity in a cluster within the inferior frontal gyrus (IFG) identified through an independent meta-analysis of 139 neuroimaging studies of mimicry, in response to passively viewing videos of the conditioned faces. The blood oxygen level dependent (BOLD) response contrast of high- vs. low-reward faces was reduced in participants with ASD compared to NT controls. The extent of reward-driven modulation was negatively correlated with autistic traits across the whole sample. Our results indicate that the mimicry-related brain response is less modulated by learned reward value in individuals with ASD when compared to NT controls. In previous studies, we found in a similar sample that being mimicked by faces was associated with less reward-related brain response in individuals ASD compared to an NT sample, suggesting that the link between reward and mimicry is affected in both directions in ASD. Together, this reduced bidirectional link between reward and mimicry can point to a potential mechanism underlying some of the social cognitive features of ASD.
Project description:BACKGROUND: Autism spectrum disorder (ASD) is a neurodevelopmental disorder characterized by impairments in social cognition. The biological basis of deficits in social cognition in ASD, and their difficulty in processing emotional face information in particular, remains unclear. Atypical communication within and between brain regions has been reported in ASD. Interregional phase-locking is a neurophysiological mechanism mediating communication among brain areas and is understood to support cognitive functions. In the present study we investigated interregional magnetoencephalographic phase synchronization during the perception of emotional faces in adolescents with ASD. METHODS: A total of 22 adolescents with ASD (18 males, mean age =14.2?±?1.15 years, 22 right-handed) with mild to no cognitive delay and 17 healthy controls (14 males, mean age =14.4?±?0.33 years, 16 right-handed) performed an implicit emotional processing task requiring perception of happy, angry and neutral faces while we recorded neuromagnetic signals. The faces were presented rapidly (80 ms duration) to the left or right of a central fixation cross and participants responded to a scrambled pattern that was presented concurrently on the opposite side of the fixation point. Task-dependent interregional phase-locking was calculated among source-resolved brain regions. RESULTS: Task-dependent increases in interregional beta synchronization were observed. Beta-band interregional phase-locking in adolescents with ASD was reduced, relative to controls, during the perception of angry faces in a distributed network involving the right fusiform gyrus and insula. No significant group differences were found for happy or neutral faces, or other analyzed frequency ranges. Significant reductions in task-dependent beta connectivity strength, clustering and eigenvector centrality (all P <0.001) in the right insula were found in adolescents with ASD, relative to controls. CONCLUSIONS: Reduced beta synchronization may reflect inadequate recruitment of task-relevant networks during emotional face processing in ASD. The right insula, specifically, was a hub of reduced functional connectivity and may play a prominent role in the inability to effectively extract emotional information from faces. These findings suggest that functional disconnection in brain networks mediating emotional processes may contribute to deficits in social cognition in this population.
Project description:Individuals with autism spectrum disorder (ASD) show superior performance in processing fine detail, but often exhibit impaired gestalt face perception. The ventral visual stream from the primary visual cortex (V1) to the fusiform gyrus (V4) plays an important role in form (including faces) and color perception. The aim of this study was to investigate how the ventral stream is functionally altered in ASD. Visual evoked potentials were recorded in high-functioning ASD adults (n = 14) and typically developing (TD) adults (n = 14). We used three types of visual stimuli as follows: isoluminant chromatic (red/green, RG) gratings, high-contrast achromatic (black/white, BW) gratings with high spatial frequency (HSF, 5.3 cycles/degree), and face (neutral, happy, and angry faces) stimuli. Compared with TD controls, ASD adults exhibited longer N1 latency for RG, shorter N1 latency for BW, and shorter P1 latency, but prolonged N170 latency, for face stimuli. Moreover, a greater difference in latency between P1 and N170, or between N1 for BW and N170 (i.e., the prolongation of cortico-cortical conduction time between V1 and V4) was observed in ASD adults. These findings indicate that ASD adults have enhanced fine-form (local HSF) processing, but impaired color processing at V1. In addition, they exhibit impaired gestalt face processing due to deficits in integration of multiple local HSF facial information at V4. Thus, altered ventral stream function may contribute to abnormal social processing in ASD.
Project description:Background:Visual atypicalities in autism spectrum disorder (ASD) are a well documented phenomenon, beginning as early as 2-6 months of age and manifesting in a significantly decreased attention to the eyes, direct gaze and socially salient information. Early emerging neurobiological deficits in perceiving social stimuli as rewarding or its active avoidance due to the anxiety it entails have been widely purported as potential reasons for this atypicality. Parallel research evidence also points to the significant benefits of animal presence for reducing social anxiety and enhancing social interaction in children with autism. While atypicality in social attention in ASD has been widely substantiated, whether this atypicality persists equally across species types or is confined to humans has not been a key focus of research insofar. Methods:We attempted a comprehensive examination of the differences in visual attention to static images of human and animal faces (40 images; 20 human faces and 20 animal faces) among children with ASD using an eye tracking paradigm. 44 children (ASD n = 21; TD n = 23) participated in the study (10,362 valid observations) across five regions of interest (left eye, right eye, eye region, face and screen). Results:Results obtained revealed significantly greater social attention across human and animal stimuli in typical controls when compared to children with ASD. However in children with ASD, a significantly greater attention allocation was seen to animal faces and eye region and lesser attention to the animal mouth when compared to human faces, indicative of a clear attentional preference to socially salient regions of animal stimuli. The positive attentional bias toward animals was also seen in terms of a significantly greater visual attention to direct gaze in animal images. Conclusion:Our results suggest the possibility that atypicalities in social attention in ASD may not be uniform across species. It adds to the current neural and biomarker evidence base of the potentially greater social reward processing and lesser social anxiety underlying animal stimuli as compared to human stimuli in children with ASD.
Project description:In two experiments, we examined whether observers' eye movements distinguish studied faces from highly similar novel faces. Participants' eye movements were monitored while they viewed three-face displays. Target-present displays contained a studied face and two morphed faces that were visually similar to it; target-absent displays contained three morphed faces that were visually similar to a studied, but not tested, face. On each trial in a test session, participants were instructed to choose the studied face if it was present or a random face if it was not and then to indicate whether the chosen face was studied. Whereas manipulating visual similarity in target-absent displays influenced the rate of false endorsements of nonstudied items as studied, eye movements proved impervious to this manipulation. Studied faces were viewed disproportionately from 1,000 to 2,000 ms after display onset and from 1,000 to 500 ms before explicit identification. Early viewing also distinguished studied faces from faces incorrectly endorsed as studied. Our findings show that eye movements provide a relatively pure index of past experience that is uninfluenced by explicit response strategies, and suggest that eye movement measures may be of practical use in applied settings.
Project description:Faces convey social information such as emotion and speech. Facial emotion processing is supported via interactions between dorsal-movement and ventral-form visual cortex regions. Here, we explored, for the first time, whether similar dorsal-ventral interactions (assessed via functional connectivity), might also exist for visual-speech processing. We then examined whether altered dorsal-ventral connectivity is observed in adults with high-functioning autism spectrum disorder (ASD), a disorder associated with impaired visual-speech recognition. We acquired functional magnetic resonance imaging (fMRI) data with concurrent eye tracking in pairwise matched control and ASD participants. In both groups, dorsal-movement regions in the visual motion area 5 (V5/MT) and the temporal visual speech area (TVSA) were functionally connected to ventral-form regions (i.e., the occipital face area [OFA] and the fusiform face area [FFA]) during the recognition of visual speech, in contrast to the recognition of face identity. Notably, parts of this functional connectivity were decreased in the ASD group compared to the controls (i.e., right V5/MT-right OFA, left TVSA-left FFA). The results confirmed our hypothesis that functional connectivity between dorsal-movement and ventral-form regions exists during visual-speech processing. Its partial dysfunction in ASD might contribute to difficulties in the recognition of dynamic face information relevant for successful face-to-face communication.