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1.  A quantitative link between face discrimination deficits and neuronal selectivity for faces in autism☆ 
NeuroImage : Clinical  2013;2:320-331.
Individuals with Autism Spectrum Disorder (ASD) appear to show a general face discrimination deficit across a range of tasks including social–emotional judgments as well as identification and discrimination. However, functional magnetic resonance imaging (fMRI) studies probing the neural bases of these behavioral differences have produced conflicting results: while some studies have reported reduced or no activity to faces in ASD in the Fusiform Face Area (FFA), a key region in human face processing, others have suggested more typical activation levels, possibly reflecting limitations of conventional fMRI techniques to characterize neuron-level processing. Here, we test the hypotheses that face discrimination abilities are highly heterogeneous in ASD and are mediated by FFA neurons, with differences in face discrimination abilities being quantitatively linked to variations in the estimated selectivity of face neurons in the FFA. Behavioral results revealed a wide distribution of face discrimination performance in ASD, ranging from typical performance to chance level performance. Despite this heterogeneity in perceptual abilities, individual face discrimination performance was well predicted by neural selectivity to faces in the FFA, estimated via both a novel analysis of local voxel-wise correlations, and the more commonly used fMRI rapid adaptation technique. Thus, face processing in ASD appears to rely on the FFA as in typical individuals, differing quantitatively but not qualitatively. These results for the first time mechanistically link variations in the ASD phenotype to specific differences in the typical face processing circuit, identifying promising targets for interventions.
► fMRI-RA, local correlations are used to estimate neuronal tuning in the FFA in ASD. ► Both techniques reveal a link of neuronal selectivity and face discrimination ability. ► These results suggest weaker experience-driven learning in the FFA in ASD.
PMCID: PMC3777682  PMID: 24179786
Face; Autism; ASD; fMRI; fMRI-RA; Local correlation
2.  Abnormal Activation of the Social Brain Network in Children with Autism Spectrum Disorder: An fMRI Study 
Psychiatry Investigation  2014;12(1):37-45.
The aim of this study is to investigate abnormal findings of social brain network in Korean children with autism spectrum disorder (ASD) compared with typically developing children (TDC).
Functional magnetic resonance imaging (fMRI) was performed to examine brain activations during the processing of emotional faces (happy, fearful, and neutral) in 17 children with ASD, 24 TDC.
When emotional face stimuli were given to children with ASD, various areas of the social brain relevant to social cognition showed reduced activation. Specifically, ASD children exhibited less activation in the right amygdala (AMY), right superior temporal sulcus (STS) and right inferior frontal gyrus (IFG) than TDC group when fearful faces were shown. Activation of left insular cortex and right IFG in response to happy faces was less in the ASD group. Similar findings were also found in left superior insular gyrus and right insula in case of neutral stimulation.
These findings suggest that children with ASD have different processing of social and emotional experience at the neural level. In other words, the deficit of social cognition in ASD could be explained by the deterioration of the capacity for visual analysis of emotional faces, the subsequent inner imitation through mirror neuron system (MNS), and the ability to transmit it to the limbic system and to process the transmitted emotion.
PMCID: PMC4310919  PMID: 25670944
Autism spectrum disorder; Social brain network; Social cognition; fMRI
3.  It’s All in the Eyes: Subcortical and Cortical Activation during Grotesqueness Perception in Autism 
PLoS ONE  2013;8(1):e54313.
Atypical face processing plays a key role in social interaction difficulties encountered by individuals with autism. In the current fMRI study, the Thatcher illusion was used to investigate several aspects of face processing in 20 young adults with high-functioning autism spectrum disorder (ASD) and 20 matched neurotypical controls. “Thatcherized” stimuli were modified at either the eyes or the mouth and participants discriminated between pairs of faces while cued to attend to either of these features in upright and inverted orientation. Behavioral data confirmed sensitivity to the illusion and intact configural processing in ASD. Directing attention towards the eyes vs. the mouth in upright faces in ASD led to (1) improved discrimination accuracy; (2) increased activation in areas involved in social and emotional processing; (3) increased activation in subcortical face-processing areas. Our findings show that when explicitly cued to attend to the eyes, activation of cortical areas involved in face processing, including its social and emotional aspects, can be enhanced in autism. This suggests that impairments in face processing in autism may be caused by a deficit in social attention, and that giving specific cues to attend to the eye-region when performing behavioral therapies aimed at improving social skills may result in a better outcome.
PMCID: PMC3544832  PMID: 23342130
4.  Brain function and gaze-fixation during facial emotion processing in fragile-X and autism 
This research focuses on the relationship between fragile X syndrome (FXS) and autism spectrum disorders (ASD). Both of these populations have a tendency to avoid looking others in the eye, along with difficulties in communication with others and tend to be socially withdrawn. While it is clear that FXS and ASD share some common abnormal behaviors, the underlying brain mechanisms associated with the social and emotional deficits in these groups remain unclear. We showed pictures of emotional and non-emotional human faces to these groups while in a magnetic resonance scanner (MRI). We collected images of brain function along with measures of where on the faces the individuals were looking (e.g. eyes or mouth). The FXS group showed a similar yet less abnormal pattern of where they were looking on the face compared to the ASD group. The FXS group also showed a similar pattern of decreased brain function in the area of the brain typically used when looking at faces, the fusiform gyrus (FG). The amount of activation in the FG was associated with how much time the FXS and ASD individuals looked at the eyes, the more they looked at the eyes, the greater the FG activation. The FXS group also displayed more brain activation than both the ASD group and a group of typically developing control subjects in brain areas that might suggest increased task difficulty for the FXS group. These group differences in brain activation are important as they suggest there is some overlap in areas of brain function in FXS and ASD when looking at faces, but that these two groups also have unique activation in other brain areas. These findings largely support the idea that ASD characteristics in FXS are associated with partially different patterns of brain activation when looking at human faces compared to individuals with ASD.
Fragile X syndrome (FXS) is the most commonly known genetic disorder associated with autism spectrum disorder (ASD). Overlapping features in these populations include gaze aversion, communication deficits, and social withdrawal. Although the association between FXS and ASD has been well documented at the behavioral level, the underlying neural mechanisms associated with the social/emotional deficits in these groups remain unclear.
We collected functional brain images and eye-gaze fixations from 9 individuals with FXS and 14 individuals with idiopathic ASD, as well as 15 typically developing (TD) individuals, while they performed a facial-emotion discrimination task.
The FXS group showed a similar yet less aberrant pattern of gaze-fixations compared to the ASD group. The FXS group also showed fusiform gyrus (FG) hypoactivation compared to the TD control group. Activation in FG was strongly and positively associated with average eye fixation and negatively associated with ASD characteristics in the FXS group. The FXS group displayed significantly greater activation than both the TD control and ASD groups in the left hippocampus (HIPP), left superior temporal gyrus (STG), right insula (INS), and left post-central gyrus (PCG).
These group differences in brain activation are important as they suggest unique underlying face-processing neural circuitry in FXS versus idiopathic ASD, largely supporting the hypothesis that ASD characteristics in FXS and idiopathic ASD reflect partially divergent impairments at the neural level, at least in FXS individuals without a co-morbid diagnosis of ASD.
PMCID: PMC2679695  PMID: 19360673
fragile X syndrome; autism; face processing; brain function; fMRI
5.  Fusiform function in children with an ASD is a matter of “who” 
Biological psychiatry  2008;64(7):552-560.
Despite the importance of face processing for normal social development, no fMRI studies of face processing in autism have focused exclusively on the childhood years. In order to fill that gap, forty-five children between the ages of 6-12 participated in practice scans, and after exclusion due to motion, 11 children with an ASD and 11 age-matched normal controls were included in final analyses.
Stimuli consisted of pictures of a familiar adult, familiar child, stranger adult, stranger child, and objects. During the scan, children pressed a button in response to an identical face shown on two consecutive trials. Based on our prior research, masks of four anatomical ROIs including the fusiform gyrus, amygdala, anterior and posterior cingulate were created and manually edited for anatomical precision for each subject. Following deconvolution analyses, the number of voxels significantly active and % signal change values that fell within each ROI mask were calculated for each subject.
Analyses revealed normal fusiform activity in children with autism when viewing a face of their mother or other children. In contrast, looking at stranger adult faces initiated profound deficits in that the mean number of significantly active voxels in the fusiform bilaterally was approximately 25% of that shown in typically developing children.
A selective fusiform deficit in response only to the faces of adult strangers may be the result of reduced attention and interest during those conditions. Face processing abnormalities found in autism likely exists beyond the fusiform.
PMCID: PMC2673799  PMID: 18621359
Autism; face processing; fMRI; pediatric imaging; children; fusiform face area
6.  fMRI evidence of neural abnormalities in the subcortical face processing system in ASD 
NeuroImage  2010;54(1):697-704.
Recent evidence suggests that a rapid, automatic face-detection system is supported by subcortical structures including the amygdala, pulvinar, and superior colliculus. Early emerging abnormalities in these structures may be related to reduced social orienting in children with autism, and subsequently, to aberrant development of cortical circuits involved in face processing. Our objective was to determine whether functional abnormalities in the subcortical face processing system are present in adults with autism spectrum disorders (ASD) during supraliminal fearful face processing. Participants included twenty-eight individuals with ASD and 25 controls group-matched on age, IQ, and behavioral performance. The ASD group met diagnostic criteria on the ADI-R, ADOS-G, and DSM-IV. Both the ASD and control groups showed significant activation in bilateral fusiform gyri. The control group exhibited additional significant responses in the right amygdala, right pulvinar, and bilateral superior colliculi. In the direct group comparison, the controls showed significantly greater activation in the left amygdala, bilateral fusiform gyrus, right pulvinar, and bilateral superior colliculi. No brain region showed significantly greater activation in the ASD group compared to the controls. Thus, basic rapid face identification mechanisms appear to be functional in ASD. However, individuals with ASD failed to engage the subcortical brain regions involved in face detection and automatic emotional face processing, suggesting a core mechanism for impaired socioemotional processing in ASD. Neural abnormalities in this system may contribute to early emerging deficits in social orienting and attention, the putative precursors to abnormalities in social cognition and cortical face processing specialization.
PMCID: PMC3426450  PMID: 20656041
7.  Amygdala Habituation and Prefrontal Functional Connectivity in Youth With Autism Spectrum Disorders 
Amygdala habituation, the rapid decrease in amygdala responsiveness to repeated presentation of stimuli, is fundamental to the nervous system. Habituation is important for maintaining adaptive levels of arousal to predictable social stimuli and reduced habituation is associated with heightened anxiety. Input from the ventromedial prefrontal cortex (vmPFC) regulates amygdala activity. Although previous research demonstrated abnormal amygdala function in youth with autism spectrum disorders (ASD), no study had examined amygdala habituation in a young sample or whether habituation related to amygdala connectivity with the vmPFC.
Data were analyzed from 32 children and adolescents with ASD and 56 typically developing controls who underwent functional magnetic resonance imaging (fMRI) scanning while performing a gender identification task for faces that were fearful, happy, sad, or neutral. Habituation was tested by comparing amygdala activation to faces during the first half versus the second half of the session. VmPFC–amygdala connectivity was examined through psychophysiological interaction analysis.
Youth with ASD had decreased amygdala habituation to sad and neutral faces relative to controls. Moreover, reduced amygdala habituation correlated with autism severity as measured by the Social Responsiveness Scale. There was a group difference in vmPFC–amygdala connectivity while viewing sad faces, and connectivity predicted amygdala habituation to sad faces within controls.
Sustained amygdala activation to faces suggests that repeated faces are processed differently in individuals with ASD, which could contribute to social impairments. Abnormal modulation of the amygdala by the vmPFC may play a role in reduced habituation.
PMCID: PMC3530144  PMID: 23265636
fMRI; habituation; autism; adolescent; emotion
8.  Face Inversion Reduces the Persistence of Global Form and Its Neural Correlates 
PLoS ONE  2011;6(4):e18705.
Face inversion produces a detrimental effect on face recognition. The extent to which the inversion of faces and other kinds of objects influences the perceptual binding of visual information into global forms is not known. We used a behavioral method and functional MRI (fMRI) to measure the effect of face inversion on visual persistence, a type of perceptual memory that reflects sustained awareness of global form. We found that upright faces persisted longer than inverted versions of the same images; we observed a similar effect of inversion on the persistence of animal stimuli. This effect of inversion on persistence was evident in sustained fMRI activity throughout the ventral visual hierarchy, including the lateral occipital area (LO), two face-selective visual areas—the fusiform face area (FFA) and the occipital face area (OFA)—and several early visual areas. V1 showed the same initial fMRI activation to upright and inverted forms but this activation lasted longer for upright stimuli. The inversion effect on persistence-related fMRI activity in V1 and other retinotopic visual areas demonstrates that higher-tier visual areas influence early visual processing via feedback. This feedback effect on figure-ground processing is sensitive to the orientation of the figure.
PMCID: PMC3078111  PMID: 21525978
9.  Effect of Familiarity on Reward Anticipation in Children with and without Autism Spectrum Disorders 
PLoS ONE  2014;9(9):e106667.
Previous research on the reward system in autism spectrum disorders (ASD) suggests that children with ASD anticipate and process social rewards differently than typically developing (TD) children—but has focused on the reward value of unfamiliar face stimuli. Children with ASD process faces differently than their TD peers. Previous research has focused on face processing of unfamiliar faces, but less is known about how children with ASD process familiar faces. The current study investigated how children with ASD anticipate rewards accompanied by familiar versus unfamiliar faces.
The stimulus preceding negativity (SPN) of the event-related potential (ERP) was utilized to measure reward anticipation. Participants were 6- to 10-year-olds with (N = 14) and without (N = 14) ASD. Children were presented with rewards accompanied by incidental face or non-face stimuli that were either familiar (caregivers) or unfamiliar. All non-face stimuli were composed of scrambled face elements in the shape of arrows, controlling for visual properties.
No significant differences between familiar versus unfamiliar faces were found for either group. When collapsing across familiarity, TD children showed larger reward anticipation to face versus non-face stimuli, whereas children with ASD did not show differential responses to these stimulus types. Magnitude of reward anticipation to faces was significantly correlated with behavioral measures of social impairment in the ASD group.
The findings do not provide evidence for differential reward anticipation for familiar versus unfamiliar face stimuli in children with or without ASD. These findings replicate previous work suggesting that TD children anticipate rewards accompanied by social stimuli more than rewards accompanied by non-social stimuli. The results do not support the idea that familiarity normalizes reward anticipation in children with ASD. Our findings also suggest that magnitude of reward anticipation to faces is correlated with levels of social impairment for children with ASD.
PMCID: PMC4153666  PMID: 25184524
10.  Prevalence of Selectivity for Mirror-Symmetric Views of Faces in the Ventral and Dorsal Visual Pathways 
Although the ability to recognize faces and objects from a variety of viewpoints is crucial to our everyday behavior, the underlying cortical mechanisms are not well understood. Recently, neurons in a face-selective region of the monkey temporal cortex were reported to be selective for mirror-symmetric viewing angles of faces as they were rotated in depth (Freiwald & Tsao, Science 2010). This property has been suggested to constitute a key computational step in achieving full view-invariance. Here, we measured fMRI activity in nine observers as they viewed upright or inverted faces presented at five different angles (−60, −30, 0, 30, 60 degrees). Using multivariate pattern analysis (MVPA), we show that sensitivity to viewpoint mirror-symmetry is widespread in the human visual system. The effect was observed in a large band of higher-order visual areas, including the occipital face area (OFA), fusiform face area (FFA), lateral occipital cortex (LO), mid Fusiform (mFus), parahippocampal place area (PPA), and extending superiorly to encompass dorsal regions V3A/B and the posterior intraparietal sulcus (pIPS). In contrast, early retinotopic regions V1-hV4 failed to exhibit sensitivity to viewpoint symmetry, as their responses could be largely explained by a computational model of low-level visual similarity. Our findings suggest that selectivity for mirror-symmetric viewing angles may constitute an intermediate-level processing step shared across multiple higher-order areas of the ventral and dorsal streams, setting the stage for complete viewpoint-invariant representations at subsequent levels of visual processing.
PMCID: PMC3448045  PMID: 22915118
11.  Neural Bases for Impaired Social Cognition in Schizophrenia and Autism Spectrum Disorders 
Schizophrenia research  2007;99(1-3):164-175.
Schizophrenia and autism both feature significant impairments in social cognition and social functioning, but the specificity and mechanisms of these deficits remain unknown. Recent research suggests that social cognitive deficits in both disorders may arise from dysfunctions in the neural systems that underlie social cognition. We explored the neural activation of discrete brain regions implicated in social cognitive and face processing in schizophrenia subgroups and autism spectrum disorders during complex social judgments of faces. Twelve individuals with autism spectrum disorders (ASD), 12 paranoid individuals with schizophrenia (P-SCZ), 12 non-paranoid individuals with schizophrenia (NP-SCZ), and 12 non-clinical healthy controls participated in this cross sectional study. Neural activation, as indexed by blood oxygenation level dependent (BOLD) contrast, was measured in a priori regions of interest while individuals rated faces for trustworthiness. All groups showed significant activation of a social cognitive network including the amygdala, fusiform face area (FFA), superior temporal sulcus (STS), and ventrolateral prefrontal cortex (VLPFC) while completing a task of complex social cognition (i.e. trustworthiness judgments). ASD and P-SCZ individuals showed significantly reduced neural activation in the right amygdala, FFA, and left VLPFC as compared to controls and in the left VLPFC as compared to NP-SCZ individuals during this task. These findings lend support to models hypothesizing well-defined neural substrates of social cognition and suggest a specific neural mechanism that may underlie social cognitive impairments in both autism and paranoid schizophrenia.
PMCID: PMC2740744  PMID: 18053686
Amygdala; Fusiform Face Area; Paranoia; fMRI; Schizophrenia; High-functioning Autism
12.  ERP responses differentiate inverted but not upright face processing in adults with ASD 
Individuals with autism spectrum disorders (ASD) have documented deficits in face processing, face memory and abnormal activation of the neural circuitry that supports these functions. To examine speed of processing of faces in ASD, high density event-related brain potentials were recorded to images of faces, inverted faces and non-face objects from 32 high-functioning adults with ASD and controls. Participants were instructed to focus on a cross hair prior to stimulus onset; the cross-hair location directed the participant's eye gaze to the eye region at stimulus onset. Although the ASD group preformed more poorly on behavioral tests of face and object memory, both groups demonstrated similar ERP responses, characterized by greater (positive) P1 and (negative) N170 amplitude to faces vs houses. N170 speed of processing to faces did not differ between groups. However, only the control group demonstrated differential responses to upright vs inverted faces. For the ASD group, the differential response to inverted vs upright faces was associated with better performance on face memory and self-reported social skills. It is possible that the use of attention cues may facilitate face processing in high-functioning adults with ASD, suggesting that the underlying neural circuitry can be activated in adults with ASD under specific demands.
PMCID: PMC3375882  PMID: 19454620
event-related potential; P100; N170; autism; face processing
13.  Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies 
Most of our social interactions involve perception of emotional information from the faces of other people. Furthermore, such emotional processes are thought to be aberrant in a range of clinical disorders, including psychosis and depression. However, the exact neurofunctional maps underlying emotional facial processing are not well defined.
Two independent researchers conducted separate comprehensive PubMed (1990 to May 2008) searches to find all functional magnetic resonance imaging (fMRI) studies using a variant of the emotional faces paradigm in healthy participants. The search terms were: “fMRI AND happy faces,” “fMRI AND sad faces,” “fMRI AND fearful faces,” “fMRI AND angry faces,” “fMRI AND disgusted faces” and “fMRI AND neutral faces.” We extracted spatial coordinates and inserted them in an electronic database. We performed activation likelihood estimation analysis for voxel-based meta-analyses.
Of the originally identified studies, 105 met our inclusion criteria. The overall database consisted of 1785 brain coordinates that yielded an overall sample of 1600 healthy participants. Quantitative voxel-based meta-analysis of brain activation provided neurofunctional maps for 1) main effect of human faces; 2) main effect of emotional valence; and 3) modulatory effect of age, sex, explicit versus implicit processing and magnetic field strength. Processing of emotional faces was associated with increased activation in a number of visual, limbic, temporoparietal and prefrontal areas; the putamen; and the cerebellum. Happy, fearful and sad faces specifically activated the amygdala, whereas angry or disgusted faces had no effect on this brain region. Furthermore, amygdala sensitivity was greater for fearful than for happy or sad faces. Insular activation was selectively reported during processing of disgusted and angry faces. However, insular sensitivity was greater for disgusted than for angry faces. Conversely, neural response in the visual cortex and cerebellum was observable across all emotional conditions.
Although the activation likelihood estimation approach is currently one of the most powerful and reliable meta-analytical methods in neuroimaging research, it is insensitive to effect sizes.
Our study has detailed neurofunctional maps to use as normative references in future fMRI studies of emotional facial processing in psychiatric populations. We found selective differences between neural networks underlying the basic emotions in limbic and insular brain regions.
PMCID: PMC2783433  PMID: 19949718
14.  Individual differences in symptom severity and behavior predict neural activation during face processing in adolescents with autism 
NeuroImage : Clinical  2014;7:53-67.
Despite the impressive literature describing atypical neural activation in visuoperceptual face processing regions in autism, almost nothing is known about whether these perturbations extend to more affective regions in the circuitry and whether they bear any relationship to symptom severity or atypical behavior. Using fMRI, we compared face-, object-, and house-related activation in adolescent males with high-functioning autism (HFA) and typically developing (TD) matched controls. HFA adolescents exhibited hypo-activation throughout the core visuoperceptual regions, particularly in the right hemisphere, as well as in some of the affective/motivational face-processing regions, including the posterior cingulate cortex and right anterior temporal lobe. Conclusions about the relative hyper- or hypo-activation of the amygdala depended on the nature of the contrast that was used to define the activation. Individual differences in symptom severity predicted the magnitude of face activation, particularly in the right fusiform gyrus. Also, among the HFA adolescents, face recognition performance predicted the magnitude of face activation in the right anterior temporal lobe, a region that supports face individuation in TD adults. Our findings reveal a systematic relation between the magnitude of neural dysfunction, severity of autism symptoms, and variation in face recognition behavior in adolescents with autism. In so doing, we uncover brain–behavior relations that underlie one of the most prominent social deficits in autism and help resolve discrepancies in the literature.
•Adolescents with autism exhibit weak activation in core and extended face regions.•Fearful and neutral faces as well as objects elicit amygdala activation in TD adolescents.•Only fearful faces drive amygdala activation in HFA adolescents.•Individual differences in behavior predict face activation in the anterior temporal lobe.•Individual differences in symptom severity predict face activation in the fusiform gyrus.
PMCID: PMC4299957  PMID: 25610767
Fusiform gyrus; Amygdala; Development; Face recognition; fMRI; Individual differences; TD, typical developing; HFA, high functioning autism; fMRI, functional magnetic iresonance maging; BOLD, blood oxygen level dependent
15.  Association between amygdala response to emotional faces and social anxiety in autism spectrum disorders 
Neuropsychologia  2010;48(12):3665-3670.
Difficulty interpreting facial expressions has been reported in autism spectrum disorders (ASD) and is thought to be associated with amygdala abnormalities. To further explore the neural basis of abnormal emotional face processing in ASD, we conducted an fMRI study of emotional face matching in high-functioning adults with ASD and age, IQ, and gender matched controls. In addition, we investigated whether there was a relationship between self-reported social anxiety and fMRI activation. During fMRI scanning, study participants were instructed to match facial expressions depicting fear or anger. The control condition was a comparable shape - matching task. The control group evidenced significantly increased left prefrontal activation and decreased activation in the occipital lobes compared to the ASD group during emotional face matching. Further, within the ASD group, greater social anxiety was associated with increased activation in right amygdala and left middle temporal gyrus, and decreased activation in the fusiform face area. These results indicate that level of social anxiety mediates the neural response to emotional face perception in ASD.
PMCID: PMC3426451  PMID: 20655320
Autism; Asperger’s disorder; amygdala; anxiety; emotional face processing; fusiform face area
16.  Cortical Patterns of Category-Selective Activation for Faces, Places and Objects in Adults with Autism 
Autism is associated with widespread atypicalities in perception, cognition and social behavior. A crucial question concerns how these atypicalities are reflected in the underlying brain activation. One way to examine possible perturbations of cortical organization in autism is to analyze the activation of category-selective ventral visual cortex, already clearly delineated in typical populations. We mapped out the neural correlates of face, place and common object processing, using functional magnetic resonance imaging (fMRI), in a group of high-functioning adults with autism and a typical comparison group, under both controlled and more naturalistic, viewing conditions. There were no consistent group differences in place-related regions. Although there were no significant differences in the extent of the object-related regions, there was more variability for these regions in the autism group. The most marked group differences were in face-selective cortex, with individuals with autism evincing reduced activation, not only in fusiform face area but also in superior temporal sulcus and occipital face area. Ventral visual cortex appears to be organized differently in high-functioning adults with autism, at least for face-selective regions, although subtle differences may also exist for other categories. We propose that cascading developmental effects of low-level differences in neuronal connectivity result in a much more pronounced effect on later developing cortical systems, such as that for face-processing, than earlier maturing systems (those for objects and places).
PMCID: PMC2765685  PMID: 19360650
high-functioning autism; fMRI; object perception; occipito-temporal cortex; visual system
17.  Reduced Functional Integration and Segregation of Distributed Neural Systems Underlying Social and Emotional Information Processing in Autism Spectrum Disorders 
Cerebral Cortex (New York, NY)  2011;22(5):1025-1037.
A growing body of evidence suggests that autism spectrum disorders (ASDs) are related to altered communication between brain regions. Here, we present findings showing that ASD is characterized by a pattern of reduced functional integration as well as reduced segregation of large-scale brain networks. Twenty-three children with ASD and 25 typically developing matched controls underwent functional magnetic resonance imaging while passively viewing emotional face expressions. We examined whole-brain functional connectivity of two brain structures previously implicated in emotional face processing in autism: the amygdala bilaterally and the right pars opercularis of the inferior frontal gyrus (rIFGpo). In the ASD group, we observed reduced functional integration (i.e., less long-range connectivity) between amygdala and secondary visual areas, as well as reduced segregation between amygdala and dorsolateral prefrontal cortex. For the rIFGpo seed, we observed reduced functional integration with parietal cortex and increased integration with right frontal cortex as well as right nucleus accumbens. Finally, we observed reduced segregation between rIFGpo and the ventromedial prefrontal cortex. We propose that a systems-level approach—whereby the integration and segregation of large-scale brain networks in ASD is examined in relation to typical development—may provide a more detailed characterization of the neural basis of ASD.
PMCID: PMC3328339  PMID: 21784971
amygdala; connectivity; default mode network; face processing; mirror neuron system
18.  Autistic Traits and Brain Activation during Face-to-Face Conversations in Typically Developed Adults 
PLoS ONE  2011;6(5):e20021.
Autism spectrum disorders (ASD) are characterized by impaired social interaction and communication, restricted interests, and repetitive behaviours. The severity of these characteristics is posited to lie on a continuum that extends into the general population. Brain substrates underlying ASD have been investigated through functional neuroimaging studies using functional magnetic resonance imaging (fMRI). However, fMRI has methodological constraints for studying brain mechanisms during social interactions (for example, noise, lying on a gantry during the procedure, etc.). In this study, we investigated whether variations in autism spectrum traits are associated with changes in patterns of brain activation in typically developed adults. We used near-infrared spectroscopy (NIRS), a recently developed functional neuroimaging technique that uses near-infrared light, to monitor brain activation in a natural setting that is suitable for studying brain functions during social interactions.
We monitored regional cerebral blood volume changes using a 52-channel NIRS apparatus over the prefrontal cortex (PFC) and superior temporal sulcus (STS), 2 areas implicated in social cognition and the pathology of ASD, in 28 typically developed participants (14 male and 14 female) during face-to-face conversations. This task was designed to resemble a realistic social situation. We examined the correlations of these changes with autistic traits assessed using the Autism-Spectrum Quotient (AQ).
Principal Findings
Both the PFC and STS were significantly activated during face-to-face conversations. AQ scores were negatively correlated with regional cerebral blood volume increases in the left STS during face-to-face conversations, especially in males.
Our results demonstrate successful monitoring of brain function during realistic social interactions by NIRS as well as lesser brain activation in the left STS during face-to-face conversations in typically developed participants with higher levels of autistic traits.
PMCID: PMC3103507  PMID: 21637754
19.  Fusiform gyrus face-selectivity reflects facial recognition ability 
Journal of cognitive neuroscience  2010;23(7):1723-1740.
Regions of the occipital and temporal lobes, including a region in the fusiform gyrus (FG), have been proposed to comprise a “core” visual representation system for faces, in part because they show face selectivity and face repetition suppression. But recent fMRI studies of developmental prosopagnosics (DPs) raise questions about whether these measures relate to face processing skills. Although DPs manifest deficient face processing, most studies to date have not shown unequivocal reductions of functional responses in the proposed core regions. We scanned 15 DPs and 15 non-DP control participants with fMRI while employing factor analysis to derive behavioral components related to face identification or other processes. Repetition suppression specific to facial identities in FG or to expression in FG and STS did not show compelling relationships with face identification ability. However, we identified robust relationships between face selectivity and face identification ability in FG across our sample for several convergent measures, including voxel-wise statistical parametric mapping, peak face selectivity in individually defined “fusiform face areas” (FFAs), and anatomical extents (cluster sizes) of those FFAs. None of these measures showed associations with behavioral expression or object recognition ability. As a group, DPs had reduced face-selective responses in bilateral FFA when compared with non-DPs. Individual DPs were also more likely than non-DPs to lack expected face-selective activity in core regions. These findings associate individual differences in face processing ability with selectivity in core face processing regions. This confirms that face selectivity can provide a valid marker for neural mechanisms that contribute to face identification ability.
PMCID: PMC3322334  PMID: 20617881
20.  Neural Basis of Self and Other Representation in Autism: An fMRI Study of Self-Face Recognition 
PLoS ONE  2008;3(10):e3526.
Autism is a developmental disorder characterized by decreased interest and engagement in social interactions and by enhanced self-focus. While previous theoretical approaches to understanding autism have emphasized social impairments and altered interpersonal interactions, there is a recent shift towards understanding the nature of the representation of the self in individuals with autism spectrum disorders (ASD). Still, the neural mechanisms subserving self-representations in ASD are relatively unexplored.
Methodology/Principal Findings
We used event-related fMRI to investigate brain responsiveness to images of the subjects' own face and to faces of others. Children with ASD and typically developing (TD) children viewed randomly presented digital morphs between their own face and a gender-matched other face, and made “self/other” judgments. Both groups of children activated a right premotor/prefrontal system when identifying images containing a greater percentage of the self face. However, while TD children showed activation of this system during both self- and other-processing, children with ASD only recruited this system while viewing images containing mostly their own face.
This functional dissociation between the representation of self versus others points to a potential neural substrate for the characteristic self-focus and decreased social understanding exhibited by these individuals, and suggests that individuals with ASD lack the shared neural representations for self and others that TD children and adults possess and may use to understand others.
PMCID: PMC2568959  PMID: 18958161
21.  Same but different: Nine-month-old infants at average and high risk for autism look at the same facial features but process them using different brain mechanisms 
Lay Abstract
Reduced attention to the eyes and/or increased focus on the mouth have been described as features of atypical face processing in individuals with autism spectrum disorders (ASD). In this study, we examined whether 9-month-old infants at average vs. high risk for ASD differ in their detection of changes in individual facial features (eyes vs. mouth) and whether this ability is related to infants’ social and communicative skills. Eye tracking data and electrical brain activity were recorded while infants viewed repeated presentations of a smiling unfamiliar female face. Occasionally, the eyes or the mouth of that face were replaced with corresponding parts from a different face. There were no group differences in the number or duration of fixations on the eye or mouth regions for any of the face stimuli. Brain activity data revealed that all infants detected both eye and mouth changes, and that these changes were associated with changes in activity of the face-specific perception mechanisms for average-risk infants only. For all infants, the size and speed of brain responses correlated with parental reports of communication use and understanding, suggesting that differences in brain processing of faces and their features in infants are associated with individual differences in early communication skills.
Scientific Abstract
The study examined whether 9-month-old infants at average vs. high risk for autism spectrum disorder (ASD) process facial features (eyes, mouth) differently, and whether such differences are related to infants’ social and communicative skills. Eye tracking and visual event-related potentials (ERPs) were recorded in 35 infants (20 average-risk typical infants, 15 high-risk siblings of children with ASD) while they viewed photographs of a smiling unfamiliar female face. On 30% of the trials, the eyes or the mouth of that face were replaced with corresponding features from a different female. There were no group differences in the number, duration, or distribution of fixations, and all infants looked at the eyes and mouth regions equally. However, increased attention to the mouth was associated with weaker receptive communication skills and increased attention to the eyes correlated with better interpersonal skills. ERP results revealed that all infants detected eye and mouth changes but did so using different brain mechanisms. Changes in facial features were associated with changes in activity of the face perception mechanisms (N290) for the average-risk group, but not for the high-risk infants. For all infants, correlations between ERP and eye tracking measures indicated that larger and faster ERPs to feature changes were associated with fewer fixations on the irrelevant regions of stimuli. The size and latency of the ERP responses also correlated with parental reports of receptive and expressive communication skills, suggesting that differences in brain processing of human faces are associated with individual differences in social-communicative behaviors.
PMCID: PMC3422441  PMID: 22674669
Face processing; ERP; eye tracking; infants; ASD; Vineland
22.  Comparison between Face and Object Processing in Youths with Autism Spectrum Disorder: An event related potentials study 
Iranian Journal of Psychiatry  2013;8(4):179-187.
Incapability in face perception and recognition is one of the main issues in autism spectrum disorders (ASD). Event related potential (ERP) studies have revealed controversial insights on autistic brain responses to faces and objects. The current investigation examined the ERP components of young children with ASD compared to a typically developing (TD) group when looking at the upright and inverted images of faces and cars.
Fourteen children and adolescents aged between 9 and 17 diagnosed as having ASD were compared with 18 age- gender matched normally developing individuals. All participants’ ERPs were recorded while they were seeing the images of human faces and objects in both upright and inverted positions. The ERP components including N170 (latency and amplitude) were compared between the two groups in two conditions of upright and inverted using the repeated measure analysis method.
The processing speed for upright faces was faster than the inverted faces in the TD group; however, the difference was not significant. A significant difference was observed in terms of N170 latency between the two groups for different stimulus categories such as objects and faces(p<0.05). Moreover, inverted vs. upright stimuli in both groups elicited a greater response in terms of N170 amplitude in both groups, and this effect was significantly prominent in the right hemisphere (p<0.05). The N170 amplitude turned out to be greater for the inverted vs. upright stimuli irrespective of the stimuli type and group.
These data suggest youths with ASD have difficulty processing information, particularly in face perception regardless of the stimuli orientation.
PMCID: PMC4281653  PMID: 25628712
Autism; face; N170; object; event related potentials
23.  Neural circuitry of emotional face processing in autism spectrum disorders 
Autism spectrum disorders (ASD) are associated with severe impairments in social functioning. Because faces provide nonverbal cues that support social interactions, many studies of ASD have examined neural structures that process faces, including the amygdala, ventromedial prefrontal cortex and superior and middle temporal gyri. However, increases or decreases in activation are often contingent on the cognitive task. Specifically, the cognitive domain of attention influences group differences in brain activation. We investigated brain function abnormalities in participants with ASD using a task that monitored attention bias to emotional faces.
Twenty-four participants (12 with ASD, 12 controls) completed a functional magnetic resonance imaging study while performing an attention cuing task with emotional (happy, sad, angry) and neutral faces.
In response to emotional faces, those in the ASD group showed greater right amygdala activation than those in the control group. A preliminary psychophysiological connectivity analysis showed that ASD participants had stronger positive right amygdala and ventromedial prefrontal cortex coupling and weaker positive right amygdala and temporal lobe coupling than controls. There were no group differences in the behavioural measure of attention bias to the emotional faces.
The small sample size may have affected our ability to detect additional group differences.
When attention bias to emotional faces was equivalent between ASD and control groups, ASD was associated with greater amygdala activation. Preliminary analyses showed that ASD participants had stronger connectivity between the amygdala ventromedial prefrontal cortex (a network implicated in emotional modulation) and weaker connectivity between the amygdala and temporal lobe (a pathway involved in the identification of facial expressions, although areas of group differences were generally in a more anterior region of the temporal lobe than what is typically reported for emotional face processing). These alterations in connectivity are consistent with emotion and face processing disturbances in ASD.
PMCID: PMC2834792  PMID: 20184808
24.  Early neural activation during facial affect processing in adolescents with Autism Spectrum Disorder☆ 
NeuroImage : Clinical  2014;7:203-212.
Impaired social interaction is one of the hallmarks of Autism Spectrum Disorder (ASD). Emotional faces are arguably the most critical visual social stimuli and the ability to perceive, recognize, and interpret emotions is central to social interaction and communication, and subsequently healthy social development. However, our understanding of the neural and cognitive mechanisms underlying emotional face processing in adolescents with ASD is limited. We recruited 48 adolescents, 24 with high functioning ASD and 24 typically developing controls. Participants completed an implicit emotional face processing task in the MEG. We examined spatiotemporal differences in neural activation between the groups during implicit angry and happy face processing. While there were no differences in response latencies between groups across emotions, adolescents with ASD had lower accuracy on the implicit emotional face processing task when the trials included angry faces. MEG data showed atypical neural activity in adolescents with ASD during angry and happy face processing, which included atypical activity in the insula, anterior and posterior cingulate and temporal and orbitofrontal regions. Our findings demonstrate differences in neural activity during happy and angry face processing between adolescents with and without ASD. These differences in activation in social cognitive regions may index the difficulties in face processing and in comprehension of social reward and punishment in the ASD group. Thus, our results suggest that atypical neural activation contributes to impaired affect processing, and thus social cognition, in adolescents with ASD.
•The ability to recognize and interpret emotions is central to social interaction.•Deficits in social interactions are hallmarks of autism spectrum disorder (ASD).•Adolescents with and without ASD completed an emotional face task in MEG.•MEG data showed atypical neural activity in ASD to both angry and happy faces.•Insula, cingulate, temporal and orbitofrontal activities were particularly affected in the ASD group.
PMCID: PMC4300004  PMID: 25610782
Implicit face processing; Adolescents; Autism Spectrum Disorder; Magnetoencephalography; Affect processing; Anterior cingulate cortex
25.  Audiovisual speech integration in autism spectrum disorder: ERP evidence for atypicalities in lexical-semantic processing 
Lay Abstract
Language and communicative impairments are among the primary characteristics of autism spectrum disorders (ASD). Previous studies have examined auditory language processing in ASD. However, during face-to-face conversation, auditory and visual speech inputs provide complementary information, and little is known about audiovisual (AV) speech processing in ASD. It is possible to elucidate the neural correlates of AV integration by examining the effects of seeing the lip movements accompanying the speech (visual speech) on electrophysiological event-related potentials (ERP) to spoken words. Moreover, electrophysiological techniques have a high temporal resolution and thus enable us to track the time-course of spoken word processing in ASD and typical development (TD). The present study examined the ERP correlates of AV effects in three time windows that are indicative of hierarchical stages of word processing. We studied a group of TD adolescent boys (n=14) and a group of high-functioning boys with ASD (n=14). Significant group differences were found in AV integration of spoken words in the 200–300ms time window when spoken words start to be processed for meaning. These results suggest that the neural facilitation by visual speech of spoken word processing is reduced in individuals with ASD.
Scientific Abstract
In typically developing (TD) individuals, behavioural and event-related potential (ERP) studies suggest that audiovisual (AV) integration enables faster and more efficient processing of speech. However, little is known about AV speech processing in individuals with autism spectrum disorder (ASD). The present study examined ERP responses to spoken words to elucidate the effects of visual speech (the lip movements accompanying a spoken word) on the range of auditory speech processing stages from sound onset detection to semantic integration. The study also included an AV condition which paired spoken words with a dynamic scrambled face in order to highlight AV effects specific to visual speech. Fourteen adolescent boys with ASD (15–17 years old) and 14 age- and verbal IQ-matched TD boys participated. The ERP of the TD group showed a pattern and topography of AV interaction effects consistent with activity within the superior temporal plane, with two dissociable effects over fronto-central and centro-parietal regions. The posterior effect (200–300ms interval) was specifically sensitive to lip movements in TD boys, and no AV modulation was observed in this region for the ASD group. Moreover, the magnitude of the posterior AV effect to visual speech correlated inversely with ASD symptomatology. In addition, the ASD boys showed an unexpected effect (P2 time window) over the frontal-central region (pooled electrodes F3, Fz, F4, FC1, FC2, FC3, FC4) which was sensitive to scrambled face stimuli. These results suggest that the neural networks facilitating processing of spoken words by visual speech are altered in individuals with ASD.
PMCID: PMC3586407  PMID: 22162387
Auditory; ASD; ERP; Language; Multisensory; Visual

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