In the field of social neuroscience, major branches of research have been instrumental in describing independent components of typical and aberrant social information processing, but the field as a whole lacks a comprehensive model that integrates different branches. We review existing research related to the neural basis of three key neural systems underlying social information processing: social perception, action observation, and theory of mind. We propose an integrative model that unites these three processes and highlights the posterior superior temporal sulcus (pSTS), which plays a central role in all three systems. Furthermore, we integrate these neural systems with the dual system account of implicit and explicit social information processing. Large-scale meta-analyses based on Neurosynth confirmed that the pSTS is at the intersection of the three neural systems. Resting-state functional connectivity analysis with 1000 subjects confirmed that the pSTS is connected to all other regions in these systems. The findings presented in this review are specifically relevant for psychiatric research especially disorders characterized by social deficits such as autism spectrum disorder.

C-tactile (CT) afferents encode caress-like touch that supports social-emotional development, and stimulation of the CT system engages the insula and cortical circuitry involved in social-emotional processing. Very few neuroimaging studies have investigated the neural mechanisms of touch processing in people with autism spectrum disorder (ASD), who often exhibit atypical responses to touch. Using functional magnetic resonance imaging, we evaluated the hypothesis that children and adolescents with ASD would exhibit atypical brain responses to CT-targeted touch. Children and adolescents with ASD, relative to typically developing (TD) participants, exhibited reduced activity in response to CT-targeted (arm) versus non-CT-targeted (palm) touch in a network of brain regions known to be involved in social-emotional information processing including bilateral insula and insular operculum, the right posterior superior temporal sulcus, bilateral temporoparietal junction extending into the inferior parietal lobule, right fusiform gyrus, right amygdala, and bilateral ventrolateral prefrontal cortex including the inferior frontal and precentral gyri, suggesting atypical social brain hypoactivation. Individuals with ASD (vs. TD) showed an enhanced response to non-CT-targeted versus CT-targeted touch in the primary somatosensory cortex, suggesting atypical sensory cortical hyper-reactivity.

Atypicality of N170-particularly latency-to faces appears to be a specific biomarker of social-communicative dysfunction in ASD and may relate to differential developmental experiences and use of compensatory cognitive mechanisms. Future research should examine phenotypic differences that contribute to N170 heterogeneity, as well as specificity of N170 differences in ASD versus non-ASD clinical populations, and N170 malleability with treatment.

Growing evidence suggests that posterior cerebellar lobe contributes to social perception in healthy adults. However, we know little about how this process varies across age and with development. Using cross-sectional fMRI data, we examined cerebellar response to biological (BIO) versus scrambled (SCRAM) motion within typically developing (TD) and autism spectrum disorder (ASD) samples (age 4–30 y), characterizing cerebellar response and BIO > SCRAM-selective effective connectivity, as well as associations with age and social ability. TD individuals recruited regions throughout cerebellar posterior lobe during BIO > SCRAM, especially bilateral lobule VI, and demonstrated connectivity with right posterior superior temporal sulcus (RpSTS) in left VI, Crus I/II, and VIIIb. ASD individuals showed BIO > SCRAM activity in left VI and left Crus I/II, and bilateral connectivity with RpSTS in Crus I/II and VIIIb/IX. No between-group differences emerged in well-matched subsamples. Among TD individuals, older age predicted greater BIO > SCRAM response in left VIIb and left VIIIa/b, but reduced connectivity between RpSTS and widespread regions of the right cerebellum. In ASD, older age predicted greater response in left Crus I and bilateral Crus II, but decreased effective connectivity with RpSTS in bilateral Crus I/II. In ASD, increased BIO > SCRAM signal in left VI/Crus I and right Crus II, VIIb, and dentate predicted lower social symptomaticity; increased effective connectivity with RpSTS in right Crus I/II and bilateral VI and I-V predicted greater symptomaticity. These data suggest that posterior cerebellum contributes to the neurodevelopment of social perception in both basic and clinical populations.

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Deficient social communication and interaction behaviors are a hallmark feature of individuals with autism spectrum disorder. These social communication and interaction deficits potentially stem from problems with explicit social cognition (i.e. processes that are controlled and largely conscious) as well as with implicit social cognition (i.e. processes that are fast, spontaneous, and primarily unconscious). This study aimed to investigate the relative contributions of implicit and explicit social cognition factors as predictors of multi-informant measures of social communication and interaction behaviors in a sample of 34 youth with clinical diagnoses of autism spectrum disorder. Behavioral, cognitive, and electrophysiological indices of implicit and explicit social cognition were entered into partial least squares regression models designed to identify latent factors that optimally predict parent-report, observer-coded, and clinician-rated social communication, and interaction outcomes. Results indicated that while both implicit and explicit social cognition factors optimally predicted outcomes, implicit social cognition factors were relatively more predictive. Findings have important implications for the conceptualization and measurement of social functioning as well as the development of targeted social interventions in autism spectrum disorder populations. Lay abstract Difficulties with social communication and interaction are a hallmark feature of autism spectrum disorder. These difficulties may be the result of problems with explicit social cognition (effortful and largely conscious processes) such as learning and recalling social norms or rules. Alternatively, social deficits may stem from problems with implicit social cognition (rapid and largely unconscious processes) such as the efficient integration of social information. The goal of this study was to determine how problems in explicit and implicit social cognition relate to social behavior in 34 youth with autism spectrum disorder. We measured aspects of implicit and explicit social cognition abilities in the laboratory using behavioral, cognitive, and brain (electrophysiological) measures. We then used those measures to predict “real-world” social behavior as reported by parents, clinicians, and independent observers. Results showed that overall better aspects of implicit and explicit social cognition predicted more competent social behavior. In addition, the ability to fluidly integrate social information (implicit social cognition) was more frequently related to competent social behavior that merely knowing what to do in social situations (explicit social cognition). These findings may help with the development of interventions focusing on improving social deficits.

Females versus males are less frequently diagnosed with autism spectrum disorder (ASD), and while understanding sex differences is critical to delineating the systems biology of the condition, female ASD is understudied. We integrated functional MRI and genetic data in a sex-balanced sample of ASD and typically developing youth (8–17 years old) to characterize female-specific pathways of ASD risk. Our primary objectives were to: (i) characterize female ASD (n = 45) brain response to human motion, relative to matched typically developing female youth (n = 45); and (ii) evaluate whether genetic data could provide further insight into the potential relevance of these brain functional differences. For our first objective we found that ASD females showed markedly reduced response versus typically developing females, particularly in sensorimotor, striatal, and frontal regions. This difference between ASD and typically developing females does not resemble differences between ASD (n = 47) and typically developing males (n = 47), even though neural response did not significantly differ between female and male ASD. For our second objective, we found that ASD females (n = 61), versus males (n = 66), showed larger median size of rare copy number variants containing gene(s) expressed in early life (10 postconceptual weeks to 2 years) in regions implicated by the typically developing female > female functional MRI contrast. Post hoc analyses suggested this difference was primarily driven by copy number variants containing gene(s) expressed in striatum. This striatal finding was reproducible among n = 2075 probands (291 female) from an independent cohort. Together, our findings suggest that striatal impacts may contribute to pathways of risk in female ASD and advocate caution in drawing conclusions regarding female ASD based on male-predominant cohorts.

A common interpretation of the face-processing deficits associated with autism spectrum disorder (ASD) is that they arise from a failure to develop normative levels of perceptual expertise. One indicator of perceptual expertise for faces is the own-age bias, operationalized as a processing advantage for faces of one's own age, presumably due to more frequent contact and experience. This effect is especially evident in domains of face recognition memory but less commonly investigated in social-emotional expertise (e.g., facial emotion recognition; FER), where individuals with ASD have shown consistent deficits. In the present study, we investigated whether a FER task would elicit an own-age bias for individuals with and without ASD and explored how the magnitude of an own-age bias may differ as a function of ASD status and symptoms. Ninety-two adolescents (63 male) between the ages of 11 and 14 years completed the child-and adult-face subtests of a standardized FER task. Overall FER accuracy was found to differ by ASD severity, reflecting poorer performance for those with increased symptoms. Results also indicated that an own-age bias was evident, reflecting greater FER performance for child compared to adult faces, for all adolescents regardless of ASD status or symptoms. However, the strength of the observed own-age bias did not differ by ASD status or severity. Findings suggest that face processing abilities of adolescents with ASD may be influenced by experience with specific categories of stimuli, similar to their typically developing peers.