Functional Brain Correlates of Social and Nonsocial Processes in Autism Spectrum Disorders: An Activation Likelihood Estimation Meta-Analysis

Phyllis Green and Randolph Cowen Institute for Pediatric Neuroscience at the New York University (NYU) Child Study Center, New York, New York 10016, USA.
Biological psychiatry (Impact Factor: 10.26). 11/2008; 65(1):63-74. DOI: 10.1016/j.biopsych.2008.09.022
Source: PubMed


Functional neuroimaging studies of autism spectrum disorders (ASD) have examined social and nonsocial paradigms, although rarely in the same study. Here, we provide an objective, unbiased survey of functional brain abnormalities in ASD, related to both social and nonsocial processing.
We conducted two separate voxel-wise activation likelihood estimation meta-analyses of 39 functional neuroimaging studies consisting of 24 studies examining social processes (e.g., theory of mind, face perception) and 15 studies examining nonsocial processes (e.g., attention control, working memory). Voxel-wise significance threshold was p<.05, corrected by false discovery rate.
Compared with neurotypical control (NC) subjects, ASD showed greater likelihood of hypoactivation in two medial wall regions: perigenual anterior cingulate cortex (ACC) in social tasks only and dorsal ACC in nonsocial studies. Further, right anterior insula, recently linked to social cognition, was more likely to be hypoactivated in ASD in the analyses of social studies. In nonsocial studies, group comparisons showed greater likelihood of activation for the ASD group in the rostral ACC region that is typically suppressed during attentionally demanding tasks.
Despite substantial heterogeneity of tasks, the rapidly increasing functional imaging literature showed ASD-related patterns of hypofunction and aberrant activation that depended on the specific cognitive domain, i.e., social versus nonsocial. These results provide a basis for targeted extensions of these findings with younger subjects and a range of paradigms, including analyses of default mode network regulation in ASD.

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    • "Although functional imaging studies of emotionprocessing in ASD have yielded inconsistent findings, several have reported hypofunctioning in ASD in regions associated with socio-emotional processing (e.g., INS, AMYG) [Di Martino et al., 2009], in extrastriate cortices [Deeley et al., 2007], ventral PFC [Ashwin et al., 2007; Hadjikhani et al., 2006], medial-frontal and orbito-frontal cortices [Bachevalier and Loveland, 2006; Loveland et al., 2008; Ogai et al., 2003], ACC and FG [Hall et al., 2003], striatum, and IFG [Dapretto et al., 2006] compared to TD controls. Conversely, studies have found increased activity for ASD compared to TD groups in STS, ACC [Ashwin et al., 2007; Hall et al., 2003; Pelphrey et al., 2007], and parieto-occipital regions [Dapretto et al., 2006; Hubl et al., 2003; Wang et al., 2004] when viewing facial emotions. "
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    ABSTRACT: Individuals with autism spectrum disorders (ASD) often have difficulty recognizing and interpreting facial expressions of emotion, which may impair their ability to navigate and communicate successfully in their social, interpersonal environments. Characterizing specific differences between individuals with ASD and their typically developing (TD) counterparts in the neural activity subserving their experience of emotional faces may provide distinct targets for ASD interventions. Thus we used functional magnetic resonance imaging (fMRI) and a parametric experimental design to identify brain regions in which neural activity correlated with ratings of arousal and valence for a broad range of emotional faces. Participants (51 ASD, 84 TD) were group-matched by age, sex, IQ, race, and socioeconomic status. Using task-related change in blood-oxygen-level-dependent (BOLD) fMRI signal as a measure, and covarying for age, sex, FSIQ, and ADOS scores, we detected significant differences across diagnostic groups in the neural activity subserving the dimension of arousal but not valence. BOLD-signal in TD participants correlated inversely with ratings of arousal in regions associated primarily with attentional functions, whereas BOLD-signal in ASD participants correlated positively with arousal ratings in regions commonly associated with impulse control and default-mode activity. Only minor differences were detected between groups in the BOLD signal correlates of valence ratings. Our findings provide unique insight into the emotional experiences of individuals with ASD. Although behavioral responses to face-stimuli were comparable across diagnostic groups, the corresponding neural activity for our ASD and TD groups differed dramatically. The near absence of group differences for valence correlates and the presence of strong group differences for arousal correlates suggest that individuals with ASD are not atypical in all aspects of emotion-processing. Studying these similarities and differences may help us to understand the origins of divergent interpersonal emotional experience in persons with ASD. Hum Brain Mapp, 2015. © 2015 Wiley Periodicals, Inc.
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    • "It is reported that amnestic mild cognitive impairment (aMCI) patients had greater decreases in low frequency oscillation amplitude in the PCC/precuneus and parahippocampal gyrus in Slow-5 band than in Slow-4 band (Han et al., 2011), and patients with schizophrenia had widespread abnormalities of low frequency oscillation amplitudes in the Slow-4 frequency band (Hoptman et al., 2010). Another study indicated greater diagnostic information for children with attention-deficit hyperactivity disorder in the Slow-4 band rather than other bands (Di Martino et al., 2009). In our study, we showed that the FC-connections which have the most potential to discriminate ASD from HCs are concentrated in the Slow-4 frequency band (Fig. 3A). "
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    • "For example, in autism literature, the distinction between social and non-social stimuli is clearly articulated and the difference between individuals with autism and neurotypical participants emerges in their differential responses to social and non-social stimuli. Social stimuli show processing advantages compared to non-social stimuli in healthy individuals, but in individuals with autism, such advantages are abolished and there may even be a processing benefit for non-social stimuli (e.g., Dawson et al., 1998; Sasson et al., 2008; South et al., 2008; Di Martino et al., 2009; Baranek et al., 2013). In the present manuscript, we focus on the effects of the social nature of stimuli on emotion experience, and whether social and non-social stimuli evoke different emotional experiences in SZ versus control participants. "
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    ABSTRACT: Adaptive emotional responses are important in interpersonal relationships. We investigated self-reported emotional experience, physiological reactivity, and micro-facial expressivity in relation to the social nature of stimuli in individuals with schizophrenia (SZ). Galvanic skin response (GSR) and facial electromyography (fEMG) were recorded in medicated outpatients with SZ and demographically matched healthy controls (CO) while they viewed social and non-social images from the International Affective Pictures System. Participants rated the valence and arousal, and selected a label for experienced emotions. Symptom severity in the SZ and psychometric schizotypy in CO were assessed. The two groups did not differ in their labeling of the emotions evoked by the stimuli, but individuals with SZ were more positive in their valence ratings. Although self-reported arousal was similar in both groups, mean GSR was greater in SZ, suggesting differential awareness, or calibration of internal states. Both groups reported social images to be more arousing than non-social images but their physiological responses to non-social vs. social images were different. Self-reported arousal to neutral social images was correlated with positive symptoms in SZ. Negative symptoms in SZ and disorganized schizotypy in CO were associated with reduced mean fEMG. Greater corrugator mean fEMG activity for positive images in SZ indicates valence-incongruent facial expressions. The patterns of emotional responses differed between the two groups. While both groups were in broad agreement in self-reported arousal and emotion labels, their mean GSR, and fEMG correlates of emotion diverged in relation to the social nature of the stimuli and clinical measures. Importantly, these results suggest disrupted self awareness of internal states in SZ and underscore the complexities of emotion processing in health and disease.
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