James C. Thompson

Shared understanding of common experiences can foster feelings of social closeness and friendship, and help us understand those experiences. Recent work has suggested that patterns of neural activity shared across individuals, especially throughout the default mode network, may underlie shared representations. Here we used repetitive transcranial magnetic stimulation (rTMS) and functional magnetic resonance imaging during movie watching to show that shared neural patterns to common experiences rely on the encoding of social information from the environment by the right posterior superior temporal sulcus (rpSTS). An encoding model of movie features showed that rTMS selectively degraded social feature encoding in rpSTS, leaving low-level visual encoding in early visual cortex intact. Using natural language processing (NLP)-based analysis, we found that rpSTS stimulation was associated with reduced memory and intersubject pattern similarity across DMN and limbic networks during scenes central to the movie narrative. Projecting scene embeddings onto NLP-based concept axes revealed reductions in memory and neural pattern similarity for scenes conveying helplessness and empathy following rTMS. These findings provide causal evidence that the rpSTS is a key region that encodes shared social information into common neural representations, and suggest that disrupting its input leads DMN representations to become idiosyncratic.

Even in our highly interconnected modern world, geographic factors play an important role in human social connections. Similarly, social relationships influence how and where we travel, and how we think about our spatial world. Here, we review the growing body of neuroscience research that is revealing multiple interactions between social and spatial processes in both humans and non-human animals. We review research on the cognitive and neural representation of spatial and social information, and highlight recent findings suggesting that underlying mechanisms might be common to both. We discuss how spatial factors can influence social behaviour, and how social concepts modify representations of space. In so doing, this review elucidates not only how neural representations of social and spatial information interact but also similarities in how the brain represents and operates on analogous information about its social and spatial surroundings. This article is part of the theme issue ‘The spatial–social interface: a theoretical and empirical integration’.

Humans can rapidly encode information from faces to support social judgments and facilitate interactions with others. We can also recall complex knowledge about those individuals, such as their social relationships with others, but the timecourse of this process has not been examined in detail. This study addressed the temporal dynamics of emerging visual and social relationship information using electroencephalography (EEG) and representational similarity analysis (RSA). Participants became familiar with a 10-person social network, and were then shown faces of that network’s members while EEG was recorded. To examine the temporal dynamics of the cognitive processes related to face perception, we compared the similarity structure of neural pattern responses to models of visual processing, face shape similarity, person identity, and social connectedness. We found that all types of information are associated with neural patterns after a face is seen. Visual and identity models became significant early after image onset, but only the identity model stayed associated with neural patterns until 400 ms. Models representing social connections were also present beginning around 200 ms, even in the absence of an explicit task to think about the friendships among the network members. A partial correlation showed that visual and social information contribute uniquely to person perception, although differences were found between models of social connection. This study highlights the speed and salience of social information relating to group dynamics that are present in the brain during person perception.Significance Statement: We live our lives in social groups where complex relationships form among and around us. It is likely that some of the information about social relationships that we observe is integral during person perception, to better help us interact in differing situations with a variety of people. However, when exactly this information becomes relevant has been unclear. In this study, we present evidence that information reflecting observed relationships among a social network is spontaneously represented in whole-brain patterns shortly following visual perception, and is uniquely present around 400 ms. These results are consistent with neuroimaging studies showing spontaneous spatial representation of social network characteristics, and contribute novel insights into the timing of these neural processes.

Understanding the emotions of others through nonverbal cues is critical for successful social interactions. The right posterior superior temporal sulcus (pSTS) is one brain region thought to be key in the recognition of the mental states of others based on body language and facial expression. In the present study, we temporarily disrupted functional activity of the right pSTS by using continuous, theta-burst transcranial magnetic stimulation (cTBS) to test the hypothesis that the right pSTS plays a causal role in emotion recognition from body movements. Participants ( N = 23) received cTBS to the right pSTS, which was individually localized using fMRI, and a vertex control site. Before and after cTBS, we tested participants’ ability to identify emotions from point-light displays (PLDs) of biological motion stimuli and a nonbiological global motion identification task. Results revealed that accurate identification of emotional states from biological motion was reduced following cTBS to the right pSTS, but accuracy was not impaired following vertex stimulation. Accuracy on the global motion task was unaffected by cTBS to either site. These results support the causal role of the right pSTS in decoding information about others’ emotional state from their body movements and gestures.

Socially appropriate behavior involves learning actions that are valued by others and those that have a social cost. Facial expressions are one way that others can signal the social value of our actions. The rewarding or aversive properties of signals such as smiles or frowns also evoke automatic approach or avoidance behaviors in receivers, and a Pavlovian system learns cues that predict rewarding or aversive outcomes. In this study, we examined the computational and neural mechanisms underlying interactions between Pavlovian and Instrumental systems during social reinforcement learning. We found that Pavlovian biases to approach cues predicting social reward and avoid cues predicting social punishment interfered with Instrumental learning from social feedback. While the computations underlying Pavlovian and Instrumental interactions remained the same as when learning from monetary feedback, Pavlovian biases from social outcomes to approach or withdraw were not significantly correlated with biases from money. Trial-by-trial measures of alpha (8-14Hz) EEG power was associated with suppression of Pavlovian bias to social outcomes, while suppression of bias from money was associated with theta (4-7Hz) EEG power. Our findings demonstrate how emotional reactions to feedback from others are balanced with the instrumental value of that feedback to guide social behavior. Significance statement: A smile from another can be a signal to continue what we are doing, while an angry scowl is a sure sign to stop. Feedback from others such as this plays an important role in shapeing social behavior. The rewarding nature of a smile (or the aversive nature of a scowl) can also lead to automatic tendencies to approach (or avoid), and we can learn situations that predict positive or negative social outcomes. In this study, we examined the brain mechanisms that come into play when the instrumental demands of a situation are in conflict with our automatic biases to approach or withdraw, such as when we have to approach someone who is scowling at us or withdraw from someone who is smiling.

Social functioning involves learning about the social networks in which we live and interact; knowing not just our friends, but also who is friends with our friends. Here we utilized a novel incidental learning paradigm and representational similarity analysis (RSA), a functional MRI multivariate pattern analysis technique, to examine the relationship between learning social networks and the brain's response to the faces within the networks. We found that accuracy of learning face pair relationships through observation is correlated with neural similarity patterns to those pairs in the left temporoparietal junction (TPJ), the left fusiform gyrus, and the subcallosal ventromedial prefrontal cortex (vmPFC), all areas previously implicated in social cognition. This model was also significant in portions of the cerebellum and thalamus. These results show that the similarity of neural patterns represent how accurately we understand the closeness of any two faces within a network, regardless of their true relationship. Our findings indicate that these areas of the brain not only process knowledge and understanding of others, but also support learning relations between individuals in groups. Significance Statement: Knowledge of the relationships between people is an important skill that helps us interact in a highly social world. While much is known about how the human brain represents the identity, goals, and intentions of others, less is known about how we represent knowledge about social relationships between others. In this study, we used functional neuroimaging to demonstrate that patterns in human brain activity represent memory for recently learned social connections.

Bulimia nervosa (BN) is a serious psychiatric illness defined by preoccupation with weight and shape, episodic binge-eating and compensatory behaviors. Although diagnosed BN has been associated with diffuse grey matter volume reductions, characterization of brain structure alterations in women with a range of BN symptoms has yet to be made. This study examined whether changes in cortical thickness (CT) scaled with BN symptom severity in a sample of 33 adult women (n = 10 BN; n = 5 EDNOS-BN). Our second objective was to assess global structural connectivity (SC) of CT and to determine if individual differences in global SC relate to BN symptom severity. We used the validated Eating Disorder Examination Questionnaire (EDE-Q; Fairburn & Beglin, 1994) as a continuous measure of BN symptom severity. Increased EDE-Q score was negatively related to global CT and local CT in the left middle frontal gyrus, right superior frontal gyrus and bilateral orbitofrontal cortex (OFC) and temporoparietal regions. Moreover, analysis of global SC indicated that BN-related cortical thinning preferentially occurred in regions with high global connectivity. Finally, we showed that individuals’ contribution to global SC at the group level were significantly related to EDE-Q score, where increased EDE-Q score correlated with reduced connectivity of the left OFC and middle temporal cortex and increased connectivity of the right superior parietal lobule. Our findings offer novel insight into CT alterations in BN and further suggest that the combination of CT and structural connectivity measures may be sensitive to individual differences in BN symptom severity.

Humans have evolved to thrive in large and complex social groups, and it is likely that this increase in group complexity has come with a greater need to decode and respond to complex and uncertain communicatory signals. In this functional MRI study, we examined whether complexity of social networks in humans is related to the functioning of brain regions key to the perception of basic, nonverbal social stimuli. Greater activation to biological than to scrambled motion in the right posterior superior temporal sulcus (pSTS) and right amygdala were positively correlated with the diversity of social-network roles. In the pSTS, in particular, this association was not due to a relationship between network diversity and network size. These findings suggest that increased functioning of brain regions involved in decoding social signals might facilitate the detection and decoding of subtle signals encountered in varied social settings.

Rhythms are an essential characteristic of our lives and auditory-motor coupling affects a variety of behaviors. Previous research has shown that neural regions associated with motor system processing are coupled to perceptual rhythmic processing, such that the perception of rhythmic stimuli can entrain motor responses. However, the degree to which individual preference modulates the motor system is unknown. Recent work has shown that passively listening to metrically strong rhythms increases corticospinal excitability, as indicated by transcranial magnetic stimulation (TMS). Furthermore, neuroimaging evidence suggests that premotor activity increases while listening to tempos occurring within a preferred tempo category. Preferred tempo (PT) refers to the rate of a hypothetical endogenous oscillator that may be indicated by spontaneous motor tempo (SMT) and preferred perceptual tempo (PPT) measurements. The present study investigated whether listening to a rhythm at an individual's PT preferentially modulates motor excitability. SMT was obtained in human participants through a tapping task, in which subjects were asked to tap a response key at their most comfortable rate. Subjects listened to tone sequences at 11 log-spaced tempos and rated their preference for each (PPT). SMT and PPT measurements were correlated, indicating that preferred and produced tempos occurred at a similar rate. Crucially, single-pulse TMS delivered to left M1 during PPT judgments revealed that corticospinal excitability, measured by motor-evoked potentials, was modulated by tempos traveling closer to individual PT. However, the specific nature of this modulation differed across individuals, with some exhibiting an increase in excitability around PT and others exhibiting a decrease. These findings suggest that auditory-motor coupling induced by rhythms is preferentially modulated by rhythms occurring at a preferred rate, and that individual differences can alter the nature of this coupling.