Grasping the Intentions of Others: The Perceived Intentionality of an Action Influences Activity in the Superior Temporal Sulcus during Social Perception

An explication of the neural substrates for social perception is an important component in the emerging field of social cognitive neuroscience and is relevant to the field of cognitive neuroscience as a whole. Prior studies from our laboratory have demonstrated that passive viewing of biological motion (Pelphrey, Mitchell, et al., 2003; Puce et al., 1998) activates the posterior superior temporal sulcus (STS ) region. Furthermore, recent evidence has shown that the perceived context of observed gaze shifts (Pelphrey, Singerman, et al., 2003; Pelphrey et al., 2004) modulates STS activity. Here, using event-related functional magnetic resonance imaging at 4 T, we investigated brain activity in response to passive viewing of goal- and nongoal-directed reaching-to-grasp movements. Participants viewed an animated character making reaching-to-grasp movements either toward (correct) or away (incorrect) from a blinking dial. Both conditions evoked significant posterior STS activity that was strongly right lateralized. By examining the time course of the blood oxygenation level-dependent response from areas of activation, we observed a functional dissociation. Incorrect trials evoked significantly greater activity in the STS than did correct trials, while an area posterior and inferior to the STS (likely corresponding to the MT/ V5 complex) responded equally to correct and incorrect movements. Parietal cortical regions, including the superior parietal lobule and the anterior intraparietal sulcus, also responded equally to correct and incorrect movements, but showed evidence for differential responding based on the hand and arm (left or right) of the animated character used to make the reaching-to-grasp movement. The results of this study further suggest that a region of the right posterior STS is involved in analyzing the intentions of other people's actions and that activity in this region is sensitive to the context of observed biological motions

Developmental Continuity and Change in Responses to Social and Nonsocial Categories in Human Extrastriate Visual Cortex

It is well known that adult human extrastriate visual cortex contains areas that respond in a selective fashion to specific categories of visual stimuli. Three regions have been identified with particular regularity: the fusiform face area (FFA), which responds to faces more than to other objects; the parahippocampal place area (PPA), which responds selectively to images of houses, places, and visual scenes; and the extrastriate body area (EBA), which responds specifically to images of bodies and body parts. While the presence of these regions in the mature human brain is well-established, the degree to which children possess these areas and the degree of functional specialization of these areas in children of various ages has thus far remained unclear. This functional magnetic resonance imaging study examined the development of the FFA, EBA, and PPA in healthy, typically developing 7- to 11-year-old children and adults. Our results revealed a right FFA and a bilateral EBA and PPA in the children that were localized in a way consistent with these same regions in adults. In addition, the response profiles of these regions were very similar in adults and children with comparable levels of functional specificity at all of the ages tested. We discuss the implications of this research for understanding abnormal regional specialization for social and nonsocial object categories in individuals with autism spectrum disorders

Developmental neuroscience of time and number: implications for autism and other neurodevelopmental disabilities

Estimations of time and number share many similarities in both non-humans and man. The primary focus of this review is on the development of time and number sense across infancy and childhood, and neuropsychological findings as they relate to time and number discrimination in infants and adults. Discussion of these findings is couched within a mode-control model of timing and counting which assumes time and number share a common magnitude representation system. A basic sense of time and number likely serves as the foundation for advanced numerical and temporal competence, and aspects of higher cognition—this will be discussed as it relates to typical childhood, and certain developmental disorders, including autism spectrum disorder. Directions for future research in the developmental neuroscience of time and number (NEUTIN) will also be highlighted

Disrupted action perception in autism: Behavioral evidence, neuroendophenotypes, and diagnostic utility

AbstractDisruptions in the visual perception of biological motion are emerging as a hallmark of autism spectrum disorder (ASD), consistent with the pathognomonic social deficits of this neurodevelopmental disorder. Accumulating evidence suggests an early and marked divergence in ASD from the typical developmental tuning of brain regions to process social information. In this review, we discuss a relatively recent yet substantial literature of behavioral and neuroimaging studies that consistently indicates impairments in biological motion perception in ASD. We then illustrate the fundamental disruption in this form of social perception in autism, drawing connections between a genetic liability to develop autism and disrupted associated brain mechanisms, as we describe neuroendophenotypes of autism derived from an fMRI study of biological motion perception in children with autism and their unaffected siblings. Finally, we demonstrate the diagnostic utility of brain responses to biological motion. With the ability to measure brain function in the first year of life comes the potential to chart the development of disrupted biological motion processing in ASD and to specify the gene–brain–behavior interactions shaping this atypical trajectory. We propose that a comprehensive understanding of the development of impaired responses to biological motion in ASD can inform future diagnosis and treatment approaches

Brain responses to biological motion predict treatment outcome in young children with autism

Autism spectrum disorders (ASDs) are common yet complex neurodevelopmental disorders, characterized by social, communication and behavioral deficits. Behavioral interventions have shown favorable results—however, the promise of precision medicine in ASD is hampered by a lack of sensitive, objective neurobiological markers (neurobiomarkers) to identify subgroups of young children likely to respond to specific treatments. Such neurobiomarkers are essential because early childhood provides a sensitive window of opportunity for intervention, while unsuccessful intervention is costly to children, families and society. In young children with ASD, we show that functional magnetic resonance imaging-based stratification neurobiomarkers accurately predict responses to an evidence-based behavioral treatment—pivotal response treatment. Neural predictors were identified in the pretreatment levels of activity in response to biological vs scrambled motion in the neural circuits that support social information processing (superior temporal sulcus, fusiform gyrus, amygdala, inferior parietal cortex and superior parietal lobule) and social motivation/reward (orbitofrontal cortex, insula, putamen, pallidum and ventral striatum). The predictive value of our findings for individual children with ASD was supported by a multivariate pattern analysis with cross validation. Predicting who will respond to a particular treatment for ASD, we believe the current findings mark the very first evidence of prediction/stratification biomarkers in young children with ASD. The implications of the findings are far reaching and should greatly accelerate progress toward more precise and effective treatments for core deficits in ASD

Individual Differences in Personality Predict How People Look at Faces

Determining the ways in which personality traits interact with contextual determinants to shape social behavior remains an important area of empirical investigation. The specific personality trait of neuroticism has been related to characteristic negative emotionality and associated with heightened attention to negative, emotionally arousing environmental signals. However, the mechanisms by which this personality trait may shape social behavior remain largely unspecified.We employed eye tracking to investigate the relationship between characteristics of visual scanpaths in response to emotional facial expressions and individual differences in personality. We discovered that the amount of time spent looking at the eyes of fearful faces was positively related to neuroticism.This finding is discussed in relation to previous behavioral research relating personality to selective attention for trait-congruent emotional information, neuroimaging studies relating differences in personality to amygdala reactivity to socially relevant stimuli, and genetic studies suggesting linkages between the serotonin transporter gene and neuroticism. We conclude that personality may be related to interpersonal interaction by shaping aspects of social cognition as basic as eye contact. In this way, eye gaze represents a possible behavioral link in a complex relationship between genes, brain function, and personality

Hemodynamic signals of mixed messages during a social exchange

The present study used functional magnetic resonance imaging (fMRI) to characterize hemodynamic activation patterns recruited when participants view mixed social communicative messages during a common interpersonal exchange. Mixed messages were defined as conflicting sequences of biological motion and facial affect signals that are unexpected within a particular social context (for example, observing the reception of a gift). Across four social vignettes, valenced facial expressions were crossed with rejecting and accepting gestures in a virtual avatar responding to presentation of a gift from the participant. Results indicate that conflicting facial affect and gesture activated superior temporal sulcus, a region implicated in expectancy violations, as well as inferior frontal gyrus and putamen. Scenarios conveying rejection differentially activated the insula and putamen, regions implicated in embodied cognition and motivated learning, as well as frontoparietal cortex. Characterizing how meaning is inferred from integration of conflicting nonverbal communicative cues is essential to understand nuances and complexities of human exchange

Tactile Perception in Adults with Autism: a Multidimensional Psychophysical Study

Although sensory problems, including unusual tactile sensitivity, are heavily associated with autism, there is a dearth of rigorous psychophysical research. We compared tactile sensation in adults with autism to controls on the palm and forearm, the latter innervated by low-threshold unmyelinated afferents subserving a social/affiliative submodality of somatosensation. At both sites, the groups displayed similar thresholds for detecting light touch and innocuous sensations of warmth and cool, and provided similar hedonic ratings of the pleasantness of textures. In contrast, increased sensitivity to vibration was seen in the autism group on the forearm, along with increased sensitivity to thermal pain at both sites. These findings suggest normal perception along with certain areas of enhanced perception in autism, consistent with previous studies

Brain Activity Evoked by the Perception of Human Walking: Controlling for Meaningful Coherent Motion

Many functional neuroimaging studies of biological motion have used as stimuli point-light displays of walking figures and compared the resulting activations with those evoked by the same display elements moving in a random or noncoherent manner. Although these studies have established that biological motion activates the superior temporal sulcus (STS), the use of random motion controls has left open the possibility that coordinated and meaningful nonbiological motion might activate these same brain regions and thus call into question their specificity for processing biological motion. Here we used functional magnetic resonance imaging and an anatomical region-of-interest approach to test a hierarchy of three questions regarding activity within the STS. First, by comparing responses in the STS with animations of human and robot walking figures, we determined (1) that the STS is sensitive to biological motion itself, not merely to the superficial characteristics of the stimulus. Then we determined that the STS responds more strongly to biological motion (as conveyed by the walking robot) than to (2) a nonmeaningful but complex nonbiological motion (a disjointed mechanical figure) and (3) a complex and meaningful nonbiological motion (the movements of a grandfather clock). In subsequent whole-brain voxel-based analyses, we confirmed robust STS activity that was strongly right lateralized. In addition, we observed significant deactivations in the STS that differentiated biological and nonbiological motion. These voxel-based analyses also revealed regions of motion-related positive activity in other brain regions, including MT or V5, fusiform gyri, right premotor cortex, and the intraparietal sulci