Face Processing In Autism Spectrum Disorder Research Articles

Diminished Repetition Suppression Reveals Selective and Systems-Level Face Processing Differences in ASD.

Repeated exposure to a stimulus results in reduced neural response, or repetition suppression, in brain regions responsible for processing that stimulus. This rapid accommodation to repetition is thought to underlie learning, stimulus selectivity, and strengthening of perceptual expectations. Importantly, reduced sensitivity to repetition has been identified in several neurodevelopmental, learning, and psychiatric disorders, including autism spectrum disorder (ASD), a neurodevelopmental disorder characterized by challenges in social communication and repetitive behaviors and restricted interests. Reduced ability to exploit or learn from repetition in ASD is hypothesized to contribute to sensory hypersensitivities, and parallels several theoretical frameworks claiming that ASD individuals show difficulty using regularities in the environment to facilitate behavior. Using fMRI in autistic and neurotypical human adults (females and males), we assessed the status of repetition suppression across two modalities (vision, audition) and with four stimulus categories (faces, objects, printed words, and spoken words). ASD individuals showed domain-specific reductions in repetition suppression for face stimuli only, but not for objects, printed words, or spoken words. Reduced repetition suppression for faces was associated with greater challenges in social communication in ASD. We also found altered functional connectivity between atypically adapting cortical regions and higher-order face recognition regions, and microstructural differences in related white matter tracts in ASD. These results suggest that fundamental neural mechanisms and system-wide circuits are selectively altered for face processing in ASD and enhance our understanding of how disruptions in the formation of stable face representations may relate to higher-order social communication processes.SIGNIFICANCE STATEMENT A common finding in neuroscience is that repetition results in plasticity in stimulus-specific processing regions, reflecting selectivity and adaptation (repetition suppression [RS]). RS is reduced in several neurodevelopmental and psychiatric conditions including autism spectrum disorder (ASD). Theoretical frameworks of ASD posit that reduced adaptation may contribute to associated challenges in social communication and sensory processing. However, the scope of RS differences in ASD is unknown. We examined RS for multiple categories across visual and auditory domains (faces, objects, printed words, spoken words) in autistic and neurotypical individuals. We found reduced RS in ASD for face stimuli only and altered functional connectivity and white matter microstructure between cortical face-recognition areas. RS magnitude correlated with social communication challenges among autistic individuals.

Asynchronous neural oscillations associated with subliminal affective face priming in autism spectrum disorder.

Autism spectrum disorder (ASD) is characterized by social communicative disturbance. Social communication requires rapid processing and accurate cognition regarding others' emotional expressions. Previous electrophysiological studies have attempted to elucidate the processes underlying atypical face-specific N170 responses to emotional faces in ASD. The present study explored subliminal affective priming effects (SAPEs) on the N170 response and time-frequency analysis of intertrial phase coherence (ITPC) for the N170 in ASD. Fifteen participants [seven participants with ASD and eight typically developing (TD) controls] were recruited for the experiment. Event-related potentials were recorded with a 128-channel electroencephalography device while participants performed an emotional face judgment task. The results revealed enhanced N170 amplitude for supraliminal target-face stimuli when they were preceded by subliminal fearful-face stimuli, in both the ASD and TD groups. Interestingly, TD participants exhibited higher alpha-ITPC in the subliminal fearful-face priming condition in the right face-specific area in the N170 time window. In contrast, there were no significant differences in ITPC in any frequency bands between the subliminal fearful and neutral priming conditions in the ASD group. Asynchronous phase-locking neural activities in the face-specific area may underlie impaired nonconscious face processing in ASD, despite the presence of common features of SAPEs for the N170 component in both the ASD and TD groups.

Atypical gaze patterns to facial feature areas in autism spectrum disorders reveal age and culture effects: A meta-analysis of eye-tracking studies.

Children and adults with autism spectrum disorder (ASD) often present with atypical gaze patterns to others' faces, a finding substantiated throughout the literature. Yet, a quantification of atypical gaze patterns to different facial regions (e.g., eyes versus mouth) in ASD remains controversial. Also few study has investigated how age and culture impacted the pattern of gaze abnormalities in ASD. This research therefore conducted a meta-analysis of eye-tracking studies to evaluate age and culture effect on atypical gaze patterns of face processing in ASD. A total of 75 articles (91 studies) and 4209 individuals (ASD: 2027; controls: 2182) across all age ranges (i.e., childhood through to adulthood) from both Eastern and Western cultures were included in this meta-analysis. Individuals with ASD yielded shorter fixation durations to the eyes than individuals without ASD. Group differences in the time spent fixating on the eyes were not modulated by age, but affected by culture. Effect size in the eastern culture was larger than that in the western culture. In contrast, group differences on time spent looking at the mouth were not significant, but changed with age and modulated by culture. Relative to the neurotypical controls, Western individuals with ASD spent more time looking at the mouth from school age, whereas Eastern individuals with ASD did not gaze longer on mouth until adulthood. These results add to the body of evidence supporting atypical gaze behaviors to eyes in ASD and provide new insights into a potential mouth compensation strategy that develops with age in ASD. LAY SUMMARY: Individuals with autism spectrum disorder (ASD) often show atypical gaze patterns when looking at others' faces compared to neurotypical individuals. This paper examines the role of age and culture on pattern of gaze abnormalities in individuals with ASD. Results show that reduction of gaze on eyes in ASD is stable across all ages and cultures, while increase of gaze on mouth emerges as individuals with ASD get older. The findings provide a developmental insight to the gaze patterns on the autism spectrum across culture.

Face perception predicts affective theory of mind in autism spectrum disorder but not schizophrenia or typical development.

Autism spectrum disorder (ASD) and schizophrenia spectrum disorder (SCZ) have overlapping symptomatology related to difficulties with social cognition. Yet, few studies have directly compared social cognition in ASD, SCZ, and typical development (TD). The current study examined individual differences in face recognition and its relation to affective theory of mind (ToM) in each diagnostic group. Adults with ASD (n = 31), SCZ (n = 43), and TD (n = 47) between the ages of 18 and 48 years-old with full scale IQ above 80 participated in this study. The Reading the Mind in the Eyes Test (RMET) measured affective ToM, and the Benton Facial Recognition Test (BFRT) measured face perception. Adults with ASD and SCZ did not differ in their affective ToM abilities, and both groups showed affective ToM difficulties compared with TD. However, better face recognition ability uniquely predicted better affective ToM ability in ASD. Results suggest that affective ToM difficulties may relate to face processing in ASD but not SCZ. By clarifying the complex nature of individual differences in affective ToM and face recognition difficulties in these disorders, the present study suggests there may be divergent mechanisms underlying pathways to social dysfunction in ASD compared with SCZ. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

The N170 event-related potential reflects delayed neural response to faces when visual attention is directed to the eyes in youths with ASD.

Atypical neural response to faces is thought to contribute to social deficits in autism spectrum disorder (ASD). Compared to typically developing (TD) controls, individuals with ASD exhibit delayed brain responses to upright faces at a face-sensitive event-related potential (ERP), the N170. Given observed differences in patterns of visual attention to faces, it is not known whether slowed neural processing may simply reflect atypical looking to faces. The present study manipulated visual attention to facial features to examine whether directed attention to the eyes normalizes N170 latency in ASD. ERPs were recorded in 30 children and adolescents with ASD as well as 26 TD children and adolescents. Results replicated prior findings of shorter N170 latency to the eye region of the face in TD individuals. In contrast, those with ASD did not demonstrate modulation of N170 latency by point of regard to the face. Group differences in latency were most pronounced when attention was directed to the eyes. Results suggest that well-replicated findings of N170 delays in ASD do not simply reflect atypical patterns of visual engagement with experimental stimuli. These findings add to a body of evidence indicating that N170 delays are a promising marker of atypical neural response to social information in ASD. LAY SUMMARY: This study looks at how children's and adolescents' brains respond when looking at different parts of a face. Typically developing children and adolescents processed eyes faster than other parts of the face, whereas this pattern was not seen in ASD. Children and adolescents with ASD processed eyes more slowly than typically developing children. These findings suggest that observed inefficiencies in face processing in ASD are not simply reflective of failure to attend to the eyes.

Neural responses to viewing human faces in autism spectrum disorder: A quantitative meta-analysis of two decades of research

The human face communicates a wealth of socially relevant information such as person identity, emotion, and intention. A consistent behavioral finding in autism spectrum disorder (ASD) is reduced attention to or difficulty drawing meaning from faces. However, neuroimaging research into the neural correlates of face processing differences in ASD has returned mixed results. While many studies find hypo-activation or hypo-connectivity of core and extended face network regions, others show hyper-activation, equal activation, or even activation shifted to object-selective fusiform gyrus (FG) regions in ASD during face processing. This study consolidates two decades of literature to reveal common and consistent patterns of brain activation when viewing human faces in ASD. It also addresses whether face processing in ASD is routinely shifted to object-centric regions of the FG. To do so, we conducted an extensive search of the neuroimaging literature according to PRISMA guidelines. Peak activation coordinates from a final set of 23 studies, yielding a sample of 713 participants (338 ASD), were included for quantitative meta-analysis using Activation Likelihood Estimation (ALE). ASD within-group results across studies revealed a single activation cluster in the left FG, which presented laterally to the mid-fusiform sulcus (MFS). Typically developing groups displayed common activations across core and extended face network regions. Exploratory analysis of between group findings from the literature did not yield significant results. Overall, our results suggest that individuals with ASD consistently activate at least one typical face network region, the left FG, when processing faces and this activation is not routinely shifted to object-centric areas of the FG.

Neural and behavioural indices of face processing in siblings of children with autism spectrum disorder (ASD): A longitudinal study from infancy to mid-childhood

Impaired face processing is proposed to play a key role in the early development of autism spectrum disorder (ASD) and to be an endophenotypic trait which indexes genetic risk for the disorder. However, no published work has examined the development of face processing abilities from infancy into the school-age years and how they relate to ASD symptoms in individuals with or at high-risk for ASD. In this novel study we investigated neural and behavioural measures of face processing at age 7 months and again in mid-childhood (age 7 years) as well as social-communication and sensory symptoms in siblings at high (n = 42) and low (n = 35) familial risk for ASD. In mid-childhood, high-risk siblings showed atypical P1 and N170 event-related potential correlates of face processing and, for high-risk boys only, poorer face and object recognition ability compared to low-risk siblings. These neural and behavioural atypicalities were associated with each other and with higher social-communication and sensory symptoms in mid-childhood. Additionally, more atypical neural correlates of object (but not face) processing in infancy were associated with less right-lateralised (more atypical) N170 amplitudes and greater social-communication problems in mid-childhood. The implications for models of face processing in ASD are discussed.

Rapid neural categorization of angry and fearful faces is specifically impaired in boys with autism spectrum disorder.

BackgroundDifficulties with facial expression processing may be associated with the characteristic social impairments in individuals with autism spectrum disorder (ASD). Emotional face processing in ASD has been investigated in an abundance of behavioral and EEG studies, yielding, however, mixed and inconsistent results.MethodsWe combined fast periodic visual stimulation (FPVS) with EEG to assess the neural sensitivity to implicitly detect briefly presented facial expressions among a stream of neutral faces, in 23 boys with ASD and 23 matched typically developing (TD) boys. Neutral faces with different identities were presented at 6 Hz, periodically interleaved with an expressive face (angry, fearful, happy, sad in separate sequences) every fifth image (i.e., 1.2 Hz oddball frequency). These distinguishable frequency tags for neutral and expressive stimuli allowed direct and objective quantification of the expression‐categorization responses, needing only four sequences of 60 s of recording per condition.ResultsBoth groups show equal neural synchronization to the general face stimulation and similar neural responses to happy and sad faces. However, the ASD group displays significantly reduced responses to angry and fearful faces, compared to TD boys. At the individual subject level, these neural responses allow to predict membership of the ASD group with an accuracy of 87%. Whereas TD participants show a significantly lower sensitivity to sad faces than to the other expressions, ASD participants show an equally low sensitivity to all the expressions.ConclusionsOur results indicate an emotion‐specific processing deficit, instead of a general emotion‐processing problem: Boys with ASD are less sensitive than TD boys to rapidly and implicitly detect angry and fearful faces. The implicit, fast, and straightforward nature of FPVS‐EEG opens new perspectives for clinical diagnosis.

The pupil: a window on social automatic processing in autism spectrum disorder children.

Faces are crucial social stimuli, eliciting automatic processing associated with increased physiological arousal in observers. The level of arousal can be indexed by pupil diameter (the 'Event-Related Pupil Dilation', ERPD). However, many parameters could influence the arousal evoked by a face and its social saliency (e.g. virtual vs. real, neutral vs. emotional, static vs. dynamic). A few studies have shown an atypical ERPD in autism spectrum disorder (ASD) patients using several kinds of faces but no study has focused on identifying which parameter of the stimulus is the most interfering with face processing in ASD. In order to disentangle the influence of these parameters, we propose an original paradigm including stimuli along an ecological social saliency gradient: from static objects to virtual faces to dynamic emotional faces. This strategy was applied to 186 children (78 ASD and 108 typically developing (TD) children) in two pupillometric studies (22 ASD and 47 TD children in the study 1 and 56 ASD and 61 TD children in the study 2). Strikingly, the ERPD in ASD children is insensitive to any of the parameters tested: the ERPD was similar for objects, static faces or dynamic faces. On the opposite, the ERPD in TD children is sensitive to all the parameters tested: the humanoid, biological, dynamic and emotional quality of the stimuli. Moreover, ERPD had a good discriminative power between ASD and TD children: ASD had a larger ERPD than TD in response to virtual faces, while TD had a larger ERPD than ASD for dynamic faces. This novel approach evidences an abnormal physiological adjustment to socially relevant stimuli in ASD.

Representational similarity analysis reveals atypical age-related changes in brain regions supporting face and car recognition in autism

Autism Spectrum Disorder (ASD) is associated with atypical activation in the ventral stream during face processing. The current study further characterizes the development of face processing in ASD using a multivoxel pattern analysis, which assesses the similarity in the representation of exemplars from the same category. Ninety-two children, adolescents and adults - with and without ASD - performed the Cambridge Face Memory Test, the Australian Face Memory Test, and a matched car memory test. Regions of interest during these tasks included Fusiform Face Area (FFA), based on the literature, and additional, structurally-defined regions in the ventral stream. Group differences in the patterns of activity within these ROIs when memorizing exemplars were examined using a representational similarity analysis (RSA). The RSA revealed significant interactions between age group and diagnostic group in R FFA, with increasing similarity within a category (faces, cars) into adulthood typically but not in those with ASD. This pattern was also evident in structurally defined ventral stream regions, namely L inferior frontal gyrus (IFG), bilateral temporoparietal junction (TPJ), L inferior temporal lobule, and the R fusiform gyrus. The specialization of face and object processing from adolescence to adulthood evident in typical development may be impaired in ASD, undermining the ability to reach adult-level visual processing in those with ASD.

Emotional face processing in autism spectrum disorder: Effects in gamma connectivity

Impairments in social functioning are characteristic of autism spectrum disorder (ASD). Differences in functional networks during face processing in ASD compared to controls have been reported; however, the spatial-temporal dynamics of networks underlying affective processing are still not well understood. The current magnetoencephalography study examined whole-brain functional connectivity to implicit happy and angry faces in 104 adults with and without ASD. A network of reduced gamma band (30–55 Hz) phase synchrony occurring 80–308 ms following angry face presentation was found in adults with ASD compared to controls. The network involved widespread connections primarily anchored in frontal regions, including bilateral orbitofrontal areas, bilateral inferior frontal gyri, and left middle frontal gyrus extending to occipital, temporal, parietal, and subcortical regions. This finding suggests disrupted long-range neuronal communication to angry faces. Additionally, reduced gamma band-specific connectivity may reflect altered E/I balance in brain regions critical for emotional face processing in ASD.

Slow segmentation of faces in Autism Spectrum Disorder

Atypical visual segmentation, affecting object perception, might contribute to face processing problems in Autism Spectrum Disorder (ASD). The current study investigated impairments in visual segmentation of faces in ASD. Thirty participants (ASD: 16; Control: 14) viewed texture-defined faces, houses, and homogeneous images, while electroencephalographic and behavioral responses were recorded. The ASD group showed slower face-segmentation related brain activity and longer segmentation reaction times than the control group, but no difference in house-segmentation related activity or behavioral performance. Furthermore, individual differences in face-segmentation but not house-segmentation correlated with score on the Autism Quotient. Segmentation is thus selectively impaired for faces in ASD, and relates to the degree of ASD traits. Face segmentation relates to recurrent connectivity from the fusiform face area (FFA) to the visual cortex. These findings thus suggest that atypical connectivity from the FFA might contribute to delayed face processing in ASD.

Enhanced Early Visual Responses During Implicit Emotional Faces Processing in Autism Spectrum Disorder.

Research on Autism Spectrum Disorder (ASD) has focused on processing of socially-relevant stimuli, such as faces. Nonetheless, before being 'social', faces are visual stimuli. The present magnetoencephalography study investigated the time course of brain activity during an implicit emotional task in visual emotion-related regions in 19 adults with ASD (mean age 26.3 ± 4.4) and 19 typically developed controls (26.4 ± 4). The results confirmed previously-reported differences between groups in brain responses to emotion and a hypo-activation in the ASD group in the right fusiform gyrus around 150ms. However, the ASD group also presented early enhanced activity in the occipital region. These results support that impaired face processing in ASD might be sustained by atypical responses in primary visual areas.

Young Adults with Autism Spectrum Disorder Show Early Atypical Neural Activity during Emotional Face Processing.

Social cognition is impaired in autism spectrum disorder (ASD). The ability to perceive and interpret affect is integral to successful social functioning and has an extended developmental course. However, the neural mechanisms underlying emotional face processing in ASD are unclear. Using magnetoencephalography (MEG), the present study explored neural activation during implicit emotional face processing in young adults with and without ASD. Twenty-six young adults with ASD and 26 healthy controls were recruited. Participants indicated the location of a scrambled pattern (target) that was presented alongside a happy or angry face. Emotion-related activation sources for each emotion were estimated using the Empirical Bayes Beamformer (pcorr ≤ 0.001) in Statistical Parametric Mapping 12 (SPM12). Emotional faces elicited elevated fusiform, amygdala and anterior insula and reduced anterior cingulate cortex (ACC) activity in adults with ASD relative to controls. Within group comparisons revealed that angry vs. happy faces elicited distinct neural activity in typically developing adults; there was no distinction in young adults with ASD. Our data suggest difficulties in affect processing in ASD reflect atypical recruitment of traditional emotional processing areas. These early differences may contribute to difficulties in deriving social reward from faces, ascribing salience to faces, and an immature threat processing system, which collectively could result in deficits in emotional face processing.

Testing the effects of expression, intensity and age on emotional face processing in ASD

Individuals with autism spectrum disorder (ASD) commonly show global deficits in the processing of facial emotion, including impairments in emotion recognition and slowed processing of emotional faces. Growing evidence has suggested that these challenges may increase with age, perhaps due to minimal improvement with age in individuals with ASD. In the present study, we explored the role of age, emotion type and emotion intensity in face processing for individuals with and without ASD. Twelve- and 18–22- year-old children with and without ASD participated. No significant diagnostic group differences were observed on behavioral measures of emotion processing for younger versus older individuals with and without ASD. However, there were significant group differences in neural responses to emotional faces. Relative to TD, at 12 years of age and during adulthood, individuals with ASD showed slower N170 to emotional faces. While the TD groups’ P1 latency was significantly shorter in adults when compared to 12 year olds, there was no significant age-related difference in P1 latency among individuals with ASD. Findings point to potential differences in the maturation of cortical networks that support visual processing (whether of faces or stimuli more broadly), among individuals with and without ASD between late childhood and adulthood. Finally, associations between ERP amplitudes and behavioral responses on emotion processing tasks suggest possible neural markers for emotional and behavioral deficits among individuals with ASD.

Restoring effects of oxytocin on the attentional preference for faces in autism

Reduced attentional preference for faces and symptoms of social anxiety are common in autism spectrum disorders (ASDs). The neuropeptide oxytocin triggers anxiolytic functions and enhances eye gaze, facial emotion recognition and neural correlates of face processing in ASD. Here we investigated whether a single dose of oxytocin increases attention to faces in ASD. As a secondary question, we explored the influence of social anxiety on these effects. We tested for oxytocin’s effects on attention to neutral faces as compared to houses in a sample of 29 autistic individuals and 30 control participants using a dot-probe paradigm with two different presentation times (100 or 500 ms). A single dose of 24 IU oxytocin was administered in a randomized, double-blind placebo-controlled, cross-over design. Under placebo, ASD individuals paid less attention to faces presented for 500 ms than did controls. Oxytocin administration increased the allocation of attention toward faces in ASD to a level observed in controls. Secondary analyses revealed that these oxytocin effects primarily occurred in ASD individuals with high levels of social anxiety who were characterized by attentional avoidance of faces under placebo. Our results confirm a positive influence of intranasal oxytocin on social attention processes in ASD. Further, they suggest that oxytocin may in particular restore the attentional preference for facial information in ASD individuals with high social anxiety. We conclude that oxytocin’s anxiolytic properties may partially account for its positive effects on socio-cognitive functioning in ASD, such as enhanced eye gaze and facial emotion recognition.

自闭症谱系障碍患者的梭状回面孔区(FFA)研究进展

本文主要从两个角度综述自闭症谱系障碍(ASD)患者的FFA研究进展。首先是FFA的面孔加工功能，研究发现与正常人相比，自闭症患者FFA神经元对面孔的选择性存在定量的区别，而不是定性的区别：即ASD患者的面孔缺陷很可能与其自身FFA神经元对面孔的选择性密切相关，选择性越低，面孔加工能力越弱；此外，前人将FFA的功能从面孔加工拓展到了视觉专家，近来也有研究者发现ASD患者的有限兴趣可以增强其视觉专家的能力。未来的研究可以从FFA的面孔加工功能出发，结合其他脑区，探讨ASD患者大脑面孔加工网络的机制；也可从采用ASD被试，结合奖赏回路等其他相关脑区，进一步探究FFA的面孔加工和视觉专家功能背后共同的神经机制。 This paper reviews the studies of Fusiform Face Area (FFA) in patients with Autism Spectrum Dis-orders (ASD) from two perspectives. First, we reviewed fMRI researches about face processing and FFA on patients with ASD. It’s found that face processing in ASD appears to rely on FFA as in typical individuals, differing quantitatively but not qualitatively. That is, face processing deficits of ASD may correlate with FFA neural selectivity and the little selectivity, the worse performance. In ad-dition, previous study extended the function of FFA from face processing to expertise. Recent re-search showed that restricted interest in patients with ASD could enhance expertise through FFA study. From the perspective of face processing of FFA, future research could combine FFA with other brain regions to explore the network mechanism of face processing in patients with ASD. Also, researchers can integrate FFA with reward circuits or other related brain areas to explore corporate mechanism of face processing and visual expertise by recruiting ASD patients.

Neural networks related to dysfunctional face processing in autism spectrum disorder.

One of the most consistent neuropsychological findings in autism spectrum disorders (ASD) is a reduced interest in and impaired processing of human faces. We conducted an activation likelihood estimation meta-analysis on 14 functional imaging studies on neural correlates of face processing enrolling a total of 164 ASD patients. Subsequently, normative whole-brain functional connectivity maps for the identified regions of significant convergence were computed for the task-independent (resting-state) and task-dependent (co-activations) state in healthy subjects. Quantitative functional decoding was performed by reference to the BrainMap database. Finally, we examined the overlap of the delineated network with the results of a previous meta-analysis on structural abnormalities in ASD as well as with brain regions involved in human action observation/imitation. We found a single cluster in the left fusiform gyrus showing significantly reduced activation during face processing in ASD across all studies. Both task-dependent and task-independent analyses indicated significant functional connectivity of this region with the temporo-occipital and lateral occipital cortex, the inferior frontal and parietal cortices, the thalamus and the amygdala. Quantitative reverse inference then indicated an association of these regions mainly with face processing, affective processing, and language-related tasks. Moreover, we found that the cortex in the region of right area V5 displaying structural changes in ASD patients showed consistent connectivity with the region showing aberrant responses in the context of face processing. Finally, this network was also implicated in the human action observation/imitation network. In summary, our findings thus suggest a functionally and structurally disturbed network of occipital regions related primarily to face (but potentially also language) processing, which interact with inferior frontal as well as limbic regions and may be the core of aberrant face processing and reduced interest in faces in ASD.

Neural responses to emotional expression information in high- and low-spatial frequency in autism: evidence for a cortical dysfunction

Despite an overall consensus that Autism Spectrum Disorder (ASD) entails atypical processing of human faces and emotional expressions, the role of neural structures involved in early facial processing remains unresolved. An influential model for the neurotypical brain suggests that face processing in the fusiform gyrus and the amygdala is based on both high-spatial frequency (HSF) information carried by a parvocellular pathway, and low-spatial frequency (LSF) information separately conveyed by a magnocellular pathway. Here, we tested the fusiform gyrus and amygdala sensitivity to emotional face information conveyed by these distinct pathways in ASD individuals (and matched Controls). During functional Magnetical Resonance Imaging (fMRI), participants reported the apparent gender of hybrid face stimuli, made by merging two different faces (one in LSF and the other in HSF), out of which one displayed an emotional expression (fearful or happy) and the other was neutral. Controls exhibited increased fusiform activity to hybrid faces with an emotional expression (relative to hybrids composed only with neutral faces), regardless of whether this was conveyed by LSFs or HSFs in hybrid stimuli. ASD individuals showed intact fusiform response to LSF, but not HSF, expressions. Furthermore, the amygdala (and the ventral occipital cortex) was more sensitive to HSF than LSF expressions in Controls, but exhibited an opposite preference in ASD. Our data suggest spared LSF face processing in ASD, while cortical analysis of HSF expression cues appears affected. These findings converge with recent accounts suggesting that ASD might be characterized by a difficulty in integrating multiple local information and cause global processing troubles unexplained by losses in low spatial frequency inputs.

Reduced beta connectivity during emotional face processing in adolescents with autism.

BackgroundAutism 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.MethodsA 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.ResultsTask-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.ConclusionsReduced 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.Electronic supplementary materialThe online version of this article (doi:10.1186/2040-2392-5-51) contains supplementary material, which is available to authorized users.