Atypical spatiotemporal activation of cerebellar lobules during emotional face processing in adolescents with autism

Autism spectrum disorder (ASD) is characterized by social deficits and atypical facial processing of emotional expressions. The underlying neuropathology of these abnormalities is still unclear. Recent studies implicate cerebellum in emotional processing; other studies show cerebellar abnormalities in ASD. Here, we elucidate the spatiotemporal activation of cerebellar lobules in ASD during emotional processing of happy and angry faces in adolescents with ASD and typically developing (TD) controls. Using magnetoencephalography, we calculated dynamic statistical parametric maps across a period of 500 ms after emotional stimuli onset and determined differences between group activity to happy and angry emotions. Following happy face presentation, adolescents with ASD exhibited only left‐hemispheric cerebellar activation in a cluster extending from lobule VI to lobule V (compared to TD controls). Following angry face presentation, adolescents with ASD exhibited only midline cerebellar activation (posterior IX vermis). Our findings indicate an early (125–175 ms) overactivation in cerebellar activity only for happy faces and a later overactivation for both happy (250–450 ms) and angry (250–350 ms) faces in adolescents with ASD. The prioritized hemispheric activity (happy faces) could reflect the promotion of a more flexible and adaptive social behavior, while the latter midline activity (angry faces) may guide conforming behavior.     

Negative emotional face perception is diminished on a very early level of processing in autism spectrum disorder

Deficits in facial affect recognition (FAR) are often reported in autism spectrum disorder (ASD) due to inappropriate visual search strategies. It is unclear, however, whether or not deficits in subliminal FAR are still present in autism when visual focus is controlled. Thirteen persons with ASD and 13 healthy participants took part in this experiment. Supraliminal FAR was assessed using a standardized, computer-aided test. Subliminal FAR was obtained by an emotional face priming paradigm. By using an eye-tracking technique, it was assured that the initial visual focus was on the eyes of the prime. Persons with ASD showed worse FAR in supraliminal face recognition. Although controlled for initial gaze direction, participants also showed reduced negative face priming. These data confirm that FAR is disturbed already on a pre-attentive level in autism.     

Altered fusiform connectivity during processing of fearful faces in social anxiety disorder

Social anxiety disorder (SAD) has been associated with hyper-reactivity in limbic brain regions like the amygdala, both during symptom provocation and emotional face processing tasks. In this functional magnetic resonance imaging study we sought to examine brain regions implicated in emotional face processing, and the connectivity between them, in patients with SAD (n=14) compared with healthy controls (n=12). We furthermore aimed to relate brain reactivity and connectivity to self-reported social anxiety symptom severity. SAD patients exhibited hyper-reactivity in the bilateral fusiform gyrus in response to fearful faces, as well as greater connectivity between the fusiform gyrus and amygdala, and decreased connectivity between the fusiform gyrus and ventromedial prefrontal cortex. Within the SAD group, social anxiety severity correlated positively with amygdala reactivity to emotional faces, amygdala-fusiform connectivity and connectivity between the amygdala and superior temporal sulcus (STS). These findings point to a pivotal role for the fusiform gyrus in SAD neuropathology, and further suggest that altered amygdala-fusiform and amygdala-STS connectivity could underlie previous findings of aberrant socio-emotional information processing in this anxiety disorder.     

Diminished social reward anticipation in the broad autism phenotype as revealed by event-related brain potentials

Diminished responsivity to reward incentives is a key contributor to the social-communication problems seen in autism spectrum disorders (ASDs). Social motivation theories suggest that individuals with ASD do not experience social interactions as rewarding, leading to negative consequences for the development of brain circuitry subserving social information. In this study, we examined neural responses to social and non-social reward anticipation in 35 typically developing young adults, examining modulation of reward sensitivity by level of autistic traits. Using an Event-related potential incentive-delay task incorporating novel, more ecologically valid forms of reward, higher expression of autistic traits was associated with an attenuated P3 response to the anticipation of social (simulated real-time video feedback from an observer), but not non-social (candy), rewards. Exploratory analyses revealed that this was unrelated to mentalizing ability. The P3 component reflects motivated attention to reward signals, suggesting attenuated motivation allocation specific to social incentives. The study extends prior findings of atypical reward anticipation in ASD, demonstrating that attenuated social reward responsiveness extends to autistic traits in the range of typical functioning. Results support the development of innovative paradigms for investigating social and non-social reward responsiveness. Insight into vulnerabilities in reward processing is critical for understanding social function in ASD.     

Abnormal activation of face processing systems at early and intermediate latency in individuals with autism spectrum disorder: a magnetoencephalographic study

The neurological basis of developmental psychopathology in autism is a matter of intense debate. Magnetoencephalography (MEG) was used to study the neuronal responses associated with the processing of faces in 12 able adults with autism spectrum disorders (ASD), performing image categorization and image identification tasks. The neuromagnetic data were analysed using nonparametric time-series analysis and equivalent current dipole estimation. Comparison data were obtained from 22 normally developing adults. In individuals with ASD, the neural responses to images of faces, observed in right extrastriate cortices at approximately 145 ms after stimulus onset, were significantly weaker, less lateralized and less affected by stimulus repetition than in control subjects. Early latency (30-60 ms) responses to face images, over right anterior temporal regions, differed significantly between the two subject groups in the image identification task. No such difference was observed for images of mugs or meaningless geometrical patterns. These findings suggest that, during the course of development in individuals with ASD, the cortical activity associated with the processing of human faces assumes a different-from-normal localization in extrastriate brain regions. This abnormal localization may be associated with unusual, but nevertheless face-specific, fast processing pathways.     

Development of an audiovisual speech perception app for children with autism spectrum disorders

Perception of spoken language requires attention to acoustic as well as visible phonetic information. This article reviews the known differences in audiovisual speech perception in children with autism spectrum disorders (ASD) and specifies the need for interventions that address this construct. Elements of an audiovisual training program are described. This researcher-developed program delivered via an iPad app presents natural speech in the context of increasing noise, but supported with a speaking face. Children are cued to attend to visible articulatory information to assist in perception of the spoken words. Data from four children with ASD ages 8–10 are presented showing that the children improved their performance on an untrained auditory speech-in-noise task.     

An investigation of the relationship between activation of a social cognitive neural network and social functioning

Previous work examining the neurobiological substrates of social cognition in healthy individuals has reported modulation of a social cognitive network such that increased activation of the amygdala, fusiform gyrus, and superior temporal sulcus are evident when individuals judge a face to be untrustworthy as compared with trustworthy. We examined whether this pattern would be present in individuals with schizophrenia who are known to show reduced activation within these same neural regions when processing faces. Additionally, we sought to determine how modulation of this social cognitive network may relate to social functioning. Neural activation was measured using functional magnetic resonance imaging with blood oxygenation level dependent contrast in 3 groups of individuals--nonparanoid individuals with schizophrenia, paranoid individuals with schizophrenia, and healthy controls--while they rated faces as either trustworthy or untrustworthy. Analyses of mean percent signal change extracted from a priori regions of interest demonstrated that both controls and nonparanoid individuals with schizophrenia showed greater activation of this social cognitive network when they rated a face as untrustworthy relative to trustworthy. In contrast, paranoid individuals did not show a significant difference in levels of activation based on how they rated faces. Further, greater activation of this social cognitive network to untrustworthy faces was significantly and positively correlated with social functioning. These findings indicate that impaired modulation of neural activity while processing social stimuli may underlie deficits in social cognition and social dysfunction in schizophrenia.     

Abnormal superior temporal connectivity during fear perception in schizophrenia

Patients with schizophrenia have difficulty in decoding facial affect. A study using event-related functional neuroimaging indicated that errors in fear detection in schizophrenia are associated with paradoxically higher activation in the amygdala and an associated network implicated in threat detection. Furthermore, this exaggerated activation to fearful faces correlated with severity of flat affect. These findings suggest that abnormal threat detection processing may reflect disruptions between nodes that comprise the affective appraisal circuit. Here we examined connectivity within this network by determining the pattern of intercorrelations among brain regions (regions of interest) significantly activated during fear identification in both healthy controls and patients using a novel procedure CORANOVA. This analysis tests differences in the interregional correlation strength between schizophrenia and healthy controls. Healthy subjects' task activation was principally characterized by robust correlations between medial structures like thalamus (THA) and amygdala (AMY) and middle frontal (MF), inferior frontal (IF), and prefrontal cortical (PFC) regions. In contrast, schizophrenia patients displayed no significant correlations between the medial regions and either MF or IF. Further, patients had significantly higher correlations between occipital lingual gyrus and superior temporal gyrus than healthy subjects. These between-group connectivity differences suggest that schizophrenia threat detection impairment may stem from abnormal stimulus integration. Such abnormal integration may disrupt the evaluation of threat within fronto-cortical regions.     

Visual scanning of faces in autism

The visual scanpaths of five high-functioning adult autistic males and five adult male controls were recorded using an infrared corneal reflection technique as they viewed photographs of human faces. Analyses of the scanpath data revealed marked differences in the scanpaths of the two groups. The autistic participants viewed nonfeature areas of the faces significantly more often and core feature areas of the faces (i.e., eyes, nose, and mouth) significantly less often than did control participants. Across both groups of participants, scanpaths generally did not differ as a function of the instructions given to the participants (i.e., Please look at the faces in any manner you wish. vs. Please identify the emotions portrayed in these faces.). Autistic participants showed a deficit in emotion recognition, but this effect was driven primarily by deficits in the recognition of fear. Collectively, these results indicate disorganized processing of face stimuli in autistic individuals and suggest a mechanism that may subserve the social information processing deficits that characterize autism spectrum disorders.     

Right lateral fusiform gyrus dysfunction during facial information processing in schizophrenia.

BACKGROUND: Patients with schizophrenia exhibit facial information processing deficits that likely contribute to their social dysfunction. Whether the deficits involve facial affect and/or identity processing or result from other cognitive abnormalities in schizophrenia remains controversial, and a brain dysfunction specifically related to them has never been reported. If such dysfunction existed, it should be consistently observed across groups of patients and during performance of different facial information processing tasks, independently of whether such tasks demand working memory (WM), semantic, or other cognitive processes. We hypothesized that the right lateral fusiform gyrus (rLFG), one of several human brain areas involved in facial information processing, would consistently show activation abnormalities during both facial affect and identity discrimination in schizophrenia. METHODS: We used functional magnetic resonance imaging to measure brain activation in two groups of six chronic, stable schizophrenic outpatients and two of six age- and gender-matched healthy controls. One group of patients and one of controls performed facial affect-with or without semantic processing-and identity discrimination tasks, and the other two groups WM tasks with facial expression cues and varying attentional demands. RESULTS: Patients from either group failed to activate the rLFG when compared to controls in any task. Other activation abnormalities were task-specific (i.e., seen only during performance of one set of tasks) and not consistently observed in both groups of patients, and thus could not be directly and solely linked to facial information discrimination. CONCLUSIONS: These results indicate a specific rLFG dysfunction during early facial information--identity or affect--processing, independent from other cognitive deficits, in schizophrenia.     

Abnormal magnocellular pathway visual processing in infants at risk for autism.

BACKGROUND: A wealth of data has documented impairments in face processing in individuals with autism spectrum disorders (ASD). Recently, the suggestion has been made that these impairments may arise from abnormal development of a subcortical system involved in face processing that originates in the magnocellular pathway of the primate visual system. METHODS: To test this developmental hypothesis, we obtained visual perceptual data from 6-month-old infants who were at risk for ASD because they had an older sibling diagnosed with the disorder ("high-risk infants"). To measure sensitivity of the magnocellular (M) pathway and, for comparison, of the parvocellular (P) visual pathway, we employed visual stimuli designed to selectively stimulate the two. Sensitivity data from high-risk infants (n = 13) were compared with data from matched control infants (i.e., "low-risk" infants with no family history of ASD, n = 26). RESULTS: On the P pathway stimulus, high-risk infants exhibited sensitivities that were identical to those of control infants. By contrast, on the M pathway stimulus, high-risk infants exhibited sensitivities nearly twofold greater than those of control infants. CONCLUSIONS: Given that ASD and its symptoms are known to run in families, these preliminary results suggest that ASD may be associated with abnormal M pathway function early in infancy, which may aid in early diagnosis of the disorder.     

Personally familiar faces are perceived categorically in face-selective regions other than the fusiform face area

Neuroimaging studies of humans have provided inconsistent evidence with respect to the response properties of the fusiform face area (FFA). It has been claimed that neural populations within this region are sensitive to subtle differences between individual faces only when they are perceived as distinct identities [P. Rotshtein et al. (2005) Nature Neuroscience, 8 , 107–113]. However, sensitivity to subtle changes of identity was found in previous studies using unfamiliar faces, for which categorical perception is less pronounced. Using functional magnetic resonance adaptation and morph continua of personally familiar faces, we investigated sensitivity to subtle changes between faces that were located either on the same or opposite sides of a categorical perceptual boundary. We found no evidence for categorical perception within the FFA, which exhibited reliable sensitivity to subtle changes of face identity whether these were perceived as distinct identities, or not. On the contrary, both the posterior superior temporal sulcus and prefrontal cortex exhibited categorical perception, as subtle changes between faces perceived as different identities yielded larger release from adaptation than those perceived as the same identity. These observations suggest that, whereas the FFA discriminates subtle physical changes of personally familiar faces, other regions encode faces in a categorical fashion.     

Neural correlates of eye-gaze detection in young children with autism

Various reports have demonstrated difficulties in eye-gaze processing in older children and adults with autism. However, little is known about the neural or developmental origin of such difficulties. In the present study, we used high-density Event-Related Potentials (HD-ERPs) to record the neural correlates of gaze processing in young children with autism, and their age-matched controls. In addition, to determine normal gaze processing development we also tested a non-autism adult group. The data obtained from the children with autism resembled that previously observed in typical 4-month old infants. In contrast, the control group showed the same pattern as typical adults. These findings suggest that the neural correlates of gaze direction processing may be delayed in young children with autism.     

Neuronal correlates of social cognition in borderline personality disorder

Patients with borderline personality disorder (BPD) have severe problems in social interactions that might be caused by deficits in social cognition. Since the findings about social-cognitive abilities in BPD are inhomogeneous, ranging from deficits to superior abilities, we aimed to investigate the neuronal basis of social cognition in BPD. We applied a paradigm with three social cognition tasks, differing in their complexity: basal processing of faces with a neutral expression, recognition of emotions, and attribution of emotional intentions (affective ToM). A total of 13 patients with BPD and 13 healthy matched controls (HCs) were included in a functional magnet resonance imaging study. BPD patients showed no deficits in social cognition on the behavioral level. However, while HCs showed increasing activation in areas of the mirror neuron system with increasing complexity in the social-cognitive task, BPD patients had hypoactivation in these areas and hyperactivation in the amygdala which were not modulated by task complexity. This activation pattern seems to reflect an enhanced emotional approach in the processing of social stimuli in BPD that allows good performance in standardized social-cognitive tasks, but might be the basis of social-cognitive deficits in real-life social interactions.     

Learning faces as concepts improves face recognition by engaging the social brain network

Face recognition benefits from associating social information to faces during learning. This has been demonstrated by better recognition for faces that underwent social than perceptual evaluations. Two hypotheses were proposed to account for this effect. According to the feature-elaboration hypothesis, social evaluations encourage elaborated processing of perceptual information from faces. According to a social representation hypothesis, social evaluations convert faces from a perceptual representation to a socially meaningful representation of a person. To decide between these two hypotheses, we ran a functional magnetic resonance imaging (fMRI) study in which we functionally localized the posterior face-selective brain areas and social processing brain areas. Participants watched video-clips of young adults and were asked to study them for a recognition test, while making either perceptual evaluations or social evaluations about them. During the fMRI scan, participants performed an old/new recognition test. Behavioural findings replicated better recognition for faces that underwent social then perceptual evaluations. fMRI results showed higher response during the recognition phase for the faces that were learned socially than perceptually, in the social-brain network but not in posterior face-selective network. These results support the social-representation hypothesis and highlight the important role that social processing mechanisms, rather than purely perceptual processes, play in face recognition.     

Altered automatic face processing in individuals with high-functioning autism spectrum disorders: Evidence from visual evoked potentials

Individuals with autism spectrum disorders (ASDs) have different automatic responses to faces than typically developing (TD) individuals. We recorded visual evoked potentials (VEPs) in 10 individuals with high-functioning ASD (HFASD) and 10 TD individuals. Visual stimuli consisted of upright and inverted faces (fearful and neutral) and objects presented subliminally in a backward-masking paradigm. In all participants, the occipital N1 (about 100 ms) and P1 (about 120 ms) peaks were major components of the evoked response. We calculated “subliminal face effect (SFE)” scores by subtracting the N1/P1 amplitudes and latencies of the object stimuli from those of the face stimuli. In the TD group, the SFE score for the N1 amplitude was significantly higher for upright fearful faces but not neutral faces, and this score was insignificant when the stimuli were inverted. In contrast, the N1 amplitude of the HFASD subjects did not show this SFE in the upright orientation. There were no significant group differences in SFE scores for P1 amplitude, latency, or N1 latency. Our findings suggest that individuals with HFASD have altered automatic visual processing for emotional faces within the lower level of the visual cortex. This impairment could be a neural component of the disrupted social cognition observed in individuals with HFASD.     

Mechanisms of face perception in humans: A magneto‐ and electro‐encephalographic study

We have been studying the underlying mechanisms of face perception in humans using magneto‐ (MEG) and electro‐encephalography (EEG) including (1) perception by viewing the static face, (2) differences in perception by viewing the eyes and whole face, (3) the face inversion effect, (4) the effect of gaze direction, (5) perception of eye motion, (6) perception of mouth motion, and (7) the interaction between auditory and visual stimuli related to the vowel sounds. In this review article, we mainly summarize our results obtained on 3, 5, and 6 above. With the presentation of both upright and inverted unfamiliar faces, the inferior temporal cortex (IT) centered on the fusiform gyrus, and the lateral temporal cortex (LT) near the superior temporal sulcus were activated simultaneously, but independently, between 140 and 200 ms post‐stimulus. The right hemisphere IT and LT were both active in all subjects, and those in the left hemisphere in half of the subjects. Latencies with inverted faces relative to those with upright faces were longer in the right hemisphere, and shorter in the left hemisphere. Since the activated regions under upright and those under inverted face stimuli did not show a significant difference, we consider that differences in processing upright versus inverted faces are attributable to temporal processing differences rather than to processing of information by different brain regions. When viewing the motion of the mouth and eyes, a large clear MEG component, 1M (mean peak latency of approximately 160 ms), was elicited to both mouth and eye movement, and was generated mainly in the occipito‐temporal border, at human MT/V5. The 1M to mouth movement and the 1M to eye movement showed no significant difference in amplitude or generator location. Therefore, our results indicate that human MT/V5 is active in the perception of both mouth and eye motion, and that the perception of movement of facial parts is probably processed similarly.     

Visual local and global processing in low-functioning deaf individuals with and without autism spectrum disorder

Background The ComFor study has indicated that individuals with intellectual disability (ID) and autism spectrum disorder (ASD) show enhanced visual local processing compared with individuals with ID only. Items of the ComFor with meaningless materials provided the best discrimination between the two samples. These results can be explained by the weak central coherence account. The main focus of the present study is to examine whether enhanced visual perception is also present in low‐functioning deaf individuals with and without ASD compared with individuals with ID, and to evaluate the underlying cognitive style in deaf and hearing individuals with ASD. Method Different sorting tasks (selected from the ComFor) were administered from four subsamples: (1) individuals with ID (n = 68); (2) individuals with ID and ASD (n = 72); (3) individuals with ID and deafness (n = 22); and (4) individuals with ID, ASD and deafness (n = 15). Differences in performance on sorting tasks with meaningful and meaningless materials between the four subgroups were analysed. Age and level of functioning were taken into account. Results Analyses of covariance revealed that results of deaf individuals with ID and ASD are in line with the results of hearing individuals with ID and ASD. Both groups showed enhanced visual perception, especially on meaningless sorting tasks, when compared with hearing individuals with ID, but not compared with deaf individuals with ID. Conclusions In ASD either with or without deafness, enhanced visual perception for meaningless information can be understood within the framework of the central coherence theory, whereas in deafness, enhancement in visual perception might be due to a more generally enhanced visual perception as a result of auditory deprivation.     

Examining the utilisation and usefulness of social support for mothers with young children with autism spectrum disorder

ABSTRACT

Background Social support has been described as a vital resource for families with children with disability. Although the benefits of social support have been described, little is known about the utilisation patterns in families of young children with autism spectrum disorder (ASD).

Method In a community sample of 78 American families with children (2–6 years) with ASD, this study examined the utilisation and usefulness of social support. Child, family, and service variables related to social support were explored.

Results Mothers of children with ASD reported using a combination of formal and informal supports, and these were perceived to be helpful. Sociodemographic variables, child behaviour problems, satisfaction with the autism diagnostic process, and access to information about ASD predicted social support utilisation.

Conclusion Social support utilisation varies as a function of different child, family, and service variables. Understanding these variables may help professionals guide families in access to and use of social support.