Self-oriented neural circuitry predicts other-oriented adaptive risks in adolescence: a longitudinal study

Adolescence is marked by changes in decision-making and perspective-taking abilities. Although adolescents make more adaptive decisions with age, little is understood about how adolescents take adaptive risks that impact others and how this behavior changes developmentally. Functional coupling between reward [e.g., ventral striatum (VS)] and ‘social brain’ [e.g. temporal parietal junction (TPJ)/ posterior superior temporal sulcus (pSTS), medial prefrontal cortex (mPFC)] systems may be differentially shape adaptive risks for the self and other. A total of 173 participants completed between one and three sessions across three waves [a total of 433 behavioral and 403 functional magnetic resonance imaging (fMRI) data points]. During an fMRI scan, adolescents completed a risky decision-making task where they made risky decisions to win money for themselves and their parent. The risky decisions varied in their expected value (EV) of potential reward. Results show that from the 6th through 9th grades, adolescents took increasingly more adaptive risks for themselves than for their parent. Additionally, greater VS–TPJ/pSTS and VS–mPFC connectivity that tracks EV when making risky decisions for themselves in 6th grade, but a lower VS–mPFC connectivity in 9th grade, predicted greater adaptive risk-taking for their parent. This study contributes to our understanding of the self as a neural proxy for promoting adaptive social behaviors in youth.     

Beyond the average brain: individual differences in social brain development are associated with friendship quality

We tested whether adolescents differ from each other in the structural development of the social brain and whether individual differences in social brain development predicted variability in friendship quality development. Adolescents (N = 299, M_age T1 =13.98 years) were followed across three biannual waves. We analysed self-reported friendship quality with the best friend at T1 and T3, and bilateral measures of surface area and cortical thickness of the medial prefrontal cortex (mPFC), posterior superior temporal sulcus (pSTS), temporoparietal junction (TPJ) and precuneus across all waves. At the group level, growth curve models confirmed non-linear decreases of surface area and cortical thickness in social brain regions. We identified substantial individual differences in levels and change rates of social brain regions, especially for surface area of the mPFC, pSTS and TPJ. Change rates of cortical thickness varied less between persons. Higher levels of mPFC surface area and cortical thickness predicted stronger increases in friendship quality over time. Moreover, faster cortical thinning of mPFC surface area predicted a stronger increase in friendship quality. Higher levels of TPJ cortical thickness predicted lower friendship quality. Together, our results indicate heterogeneity in social brain development and how this variability uniquely predicts friendship quality development.     

Developmental changes in the structure of the social brain in late childhood and adolescence

Social cognition provides humans with the necessary skills to understand and interact with one another. One aspect of social cognition, mentalizing, is associated with a network of brain regions often referred to as the ‘social brain.’ These consist of medial prefrontal cortex [medial Brodmann Area 10 (mBA10)], temporoparietal junction (TPJ), posterior superior temporal sulcus (pSTS) and anterior temporal cortex (ATC). How these specific regions develop structurally across late childhood and adolescence is not well established. This study examined the structural developmental trajectories of social brain regions in the longest ongoing longitudinal neuroimaging study of human brain maturation. Structural trajectories of grey matter volume, cortical thickness and surface area were analyzed using surface-based cortical reconstruction software and mixed modeling in a longitudinal sample of 288 participants (ages 7–30 years, 857 total scans). Grey matter volume and cortical thickness in mBA10, TPJ and pSTS decreased from childhood into the early twenties. The ATC increased in grey matter volume until adolescence and in cortical thickness until early adulthood. Surface area for each region followed a cubic trajectory, peaking in early or pre-adolescence before decreasing into the early twenties. These results are discussed in the context of developmental changes in social cognition across adolescence.     

fNIRS detects temporal lobe response to affective touch

Touch plays a crucial role in social–emotional development. Slow, gentle touch applied to hairy skin is processed by C-tactile (CT) nerve fibers. Furthermore, ‘social brain’ regions, such as the posterior superior temporal sulcus (pSTS) have been shown to process CT-targeted touch. Research on the development of these neural mechanisms is scant, yet such knowledge may inform our understanding of the critical role of touch in development and its dysfunction in disorders involving sensory issues, such as autism. The aim of this study was to validate the ability of functional near-infrared spectroscopy (fNIRS), an imaging technique well-suited for use with infants, to measure temporal lobe responses to CT-targeted touch. Healthy adults received brushing to the right forearm (CT) and palm (non-CT) separately, in a block design procedure. We found significant activation in right pSTS and dorsolateral prefrontal cortex to arm > palm touch. In addition, individual differences in autistic traits were related to the magnitude of peak activation within pSTS. These findings demonstrate that fNIRS can detect brain responses to CT-targeted touch and lay the foundation for future work with infant populations that will characterize the development of brain mechanisms for processing CT-targeted touch in typical and atypical populations.     

Reduced functional connectivity within and between ‘social’ resting state networks in autism spectrum conditions

Individuals with Autism Spectrum Conditions (ASC) have difficulties in social interaction and communication, which is reflected in hypoactivation of brain regions engaged in social processing, such as medial prefrontal cortex (mPFC), amygdala and insula. Resting state studies in ASC have identified reduced connectivity of the default mode network (DMN), which includes mPFC, suggesting that other resting state networks incorporating ‘social’ brain regions may also be abnormal. Using Seed-based Connectivity and Group Independent Component Analysis (ICA) approaches, we looked at resting functional connectivity in ASC between specific ‘social’ brain regions, as well as within and between whole networks incorporating these regions. We found reduced functional connectivity within the DMN in individuals with ASC, using both ICA and seed-based approaches. Two further networks identified by ICA, the salience network, incorporating the insula and a medial temporal lobe network, incorporating the amygdala, showed reduced inter-network connectivity. This was underlined by reduced seed-based connectivity between the insula and amygdala. The results demonstrate significantly reduced functional connectivity within and between resting state networks incorporating ‘social’ brain regions. This reduced connectivity may result in difficulties in communication and integration of information across these networks, which could contribute to the impaired processing of social signals in ASC.     

An fMRI study of simple ethical decision-making

Recent functional neuroimaging studies suggest that ventromedial prefrontal cortex (vmPFC), left posterior superior temporal sulcus (pSTS) and posterior cingulate cortex are engaged during moral decision-making on complex dilemmatic or salient emotional stimuli. In this fMRI study we investigated which of these brain regions are activated during simple ethical decision-making about unambiguous scenarios not containing direct bodily harm or violence. Simple moral decisions compared to semantic decisions resulted in activation of left pSTS and middle temporal gyrus, bilateral temporal poles, left lateral PFC and bilateral vmPFC. These results suggest that pSTS and vmPFC are a common neuronal substrate of decision-making about complex ethical dilemmas, processing material evocative of moral emotions and simple ethical decision-making about scenarios devoid of violence and direct bodily harm.     

Differential responses of the dorsomedial prefrontal cortex and right posterior superior temporal sulcus to spontaneous mentalizing

Previous research suggests a role of the dorsomedial prefrontal cortex (dmPFC) in metacognitive representation of social information, while the right posterior superior temporal sulcus (pSTS) has been linked to social perception. This study targeted these functional roles in the context of spontaneous mentalizing. An animated shapes task was presented to 46 subjects during functional magnetic resonance imaging. Stimuli consisted of video clips depicting animated shapes whose movement patterns prompt spontaneous mentalizing or simple intention attribution. Based on their differential response during spontaneous mentalizing, both regions were characterized with respect to their task‐dependent connectivity profiles and their associations with autistic traits. Functional network analyses revealed highly localized coupling of the right pSTS with visual areas in the lateral occipital cortex, while the dmPFC showed extensive coupling with instances of large‐scale control networks and temporal areas including the right pSTS. Autistic traits were related to mentalizing‐specific activation of the dmPFC and to the strength of connectivity between the dmPFC and posterior temporal regions. These results are in good agreement with the hypothesized roles of the dmPFC and right pSTS for metacognitive representation and perception‐based processing of social information, respectively, and further inform their implication in social behavior linked to autism. Hum Brain Mapp 38:3791–3803, 2017. © 2017 Wiley Periodicals, Inc.     

The person within: memory codes for persons and traits using fMRI repetition suppression

Neuroimaging studies on trait inference demonstrated that the ventral medial prefrontal cortex (mPFC) houses neural representations of memory codes for traits . In this study, we investigate the neural code not only of traits, but also of persons who exemplify these traits. We used repetition suppression, which is a rapid suppression of the neuroimaging signal upon repeated presentation of the same stimulus or core stimulus characteristics—in this case, the implied trait and person. Participants inferred familiar person’s traits. At each trial, a critical (target) sentence described a behavior that implied a trait, and was preceded by a (prime) sentence that implied the same trait and portrayed the same person, the same trait but portrayed a different person or did not imply a trait and portrayed a different person. As predicted, we found partly overlapping repetition suppression areas in the ventral mPFC when persons and traits were repeated, indicating that not only traits but also familiar persons have a neural code in the ventral mPFC. We also found a negative correlation between activation when reading about a new person and participants’ social network size, indicating that experience with larger social groups results in less recruitment of a person code.     

Social preferences correlate with cortical thickness of the orbito-frontal cortex

Humans differ in their preferences for personal rewards, fairness and others’ welfare. Such social preferences predict trust, public goods provision and mutual gains bargaining and have been linked to neural activity in regions involved in reward computation, cognitive control and perspective-taking. Although shaped by culture, social preferences are relatively stable across time, raising the question whether differences in brain anatomy predict social preferences and their key components—concern for personal outcomes and concern for others’ outcomes. Here, we examine this possibility by linking social preferences measured with incentivized economic games to 74 cortical parcels in 194 healthy humans. Neither concerns for personal outcomes nor concerns for the outcomes of others in isolation were related to anatomical differences. However, fitting earlier findings, social preferences positively scaled with cortical thickness in the left olfactory sulcus, a structure in the orbital frontal cortex previously shown to be involved in value-based decision-making. Consistent with work showing that heavier usage corresponds to larger brain volume, findings suggest that pro-social preferences relate to cortical thickness in the left olfactory sulcus because of heavier reliance on the orbital frontal cortex during social decision-making.     

Functional connectivity during a social emotion task in adolescents and in adults

In this fMRI study we investigated functional connectivity between components of the mentalising system during a social emotion task, using psychophysiological interaction (PPI) analysis. Ten adults (22–32 years) and 18 adolescents (11–18 years) were scanned while thinking about scenarios in which a social or a basic emotion would be experienced. Unlike basic emotions (such as disgust and fear), social emotions (such as embarrassment and guilt) require the representation of another's mental states. In both adults and adolescents, an anterior rostral region of medial prefrontal cortex (arMPFC) involved in mentalising showed greater connectivity with the posterior superior temporal sulcus (pSTS) bordering on the temporo-parietal junction (TPJ) and with anterior temporal cortex (ATC) during social than during basic emotion. This result provides novel evidence that components of the mentalising system interact functionally during a social emotion task. Furthermore, functional connectivity differed between adolescence and adulthood. The adolescent group showed stronger connectivity between arMPFC and pSTS/TPJ during social relative to basic emotion than did the adult group, suggestive of developmental changes in functional integration within the mentalising system.     

From moral to legal judgment: the influence of normative context in lawyers and other academics

Various kinds of normative judgments are an integral part of everyday life. We extended the scrutiny of social cognitive neuroscience into the domain of legal decisions, investigating two groups, lawyers and other academics, during moral and legal decision-making. While we found activation of brain areas comprising the so-called ‘moral brain’ in both conditions, there was stronger activation in the left dorsolateral prefrontal cortex and middle temporal gyrus particularly when subjects made legal decisions, suggesting that these were made in respect to more explicit rules and demanded more complex semantic processing. Comparing both groups, our data show that behaviorally lawyers conceived themselves as emotionally less involved during normative decision-making in general. A group × condition interaction in the dorsal anterior cingulate cortex suggests a modulation of normative decision-making by attention based on subjects’ normative expertise.     

Corticostriatal connectivity is associated with the reduction of intergroup bias and greater impartial giving in youth

Although prosocial behavior is preferentially directed toward the in-group across many species, prioritizing the outcomes of both the in- and out-group earlier in development can reduce intergroup biases. The current study examined the role of corticostriatal recruitment and connectivity in buffering the effect of intergroup bias on costly giving behavior during childhood and adolescence, a period when other-oriented preferences and associated brain functions undergo significant change. During functional magnetic resonance imaging, youth (n = 51; 8–16 years) made decisions that could potentially benefit in-group and out-group peers at a cost to themselves. Youth were more prosocial toward in-group relative to out-group peers, but were relatively more prosocial to out-group peers when there was a greater discrepancy between potential rewards for others over oneself (i.e., higher reward inequity). Although they showed no differences in corticostriatal activation, youth evinced greater connectivity between the ventral striatum (VS) and posterior superior temporal sulcus (pSTS) when considering more inequitable prosocial decisions that favored the outcomes of out-group peers, which attenuated intergroup biases in prosocial behavior. We found no age-related differences at the behavioral or neural level, suggesting that in-group preferences already bias prosocial behavior and its neurocognitive processes by late childhood and do not change across adolescence.     

Engagement of amygdala in third-person view of face-to-face interaction

Humans often watch interactions between other people without taking part in the interaction themselves. Strikingly little is, however, known about how gestures and expressions of two interacting humans are processed in the observer's brain, since the study of social cues has mostly focused on the perception of solitary humans. To investigate the neural underpinnings of the third-person view of social interaction, we studied brain activations of subjects who observed two humans either facing toward or away from each other. Activations within the amygdala, posterior superior temporal sulcus (pSTS), and dorsomedial prefrontal cortex (dmPFC) were sensitive to the interactional position of the observed people and distinguished humans facing toward from humans facing away. The amygdala was most sensitive to face-to-face interaction and did not differentiate the humans facing away from the pixelated control figures, whereas the pSTS dissociated both human stimuli from the pixel figures. The results of the amygdala reactivity suggest that, in addition to regulating interpersonal distance towards oneself, the amygdala is involved in the assessment of the proximity between two other persons.     

Schizophrenia and Autism as Contrasting Minds: Neural Evidence for the Hypo-Hyper-Intentionality Hypothesis

Both schizophrenia (SCZ) and autism spectrum disorder (ASD) are characterized by mentalizing problems and associated neural dysfunction of the social brain. However, the deficits in mental state attribution are somehow opposed: Whereas patients with SCZ tend to over-attribute intentions to agents and physical events (“hyper-intentionality”), patients with autism treat people as devoid of intentions (“hypo-intentionality”). Here we aimed to investigate whether this hypo-hyper-intentionality hypothesis can be supported by neural evidence during a mentalizing task. Using functional magnetic resonance imaging (fMRI), we investigated the neural responses and functional connectivity during reading others intention. Scanning was performed in 23 individuals with ASD, 18 with paranoid SCZ and 23 gender and IQ matched control subjects. Both clinical groups showed reduced brain activation compared to controls for the contrast intentional vs physical information processing in left posterior superior temporal sulcus (pSTS) and ventral medial prefrontal cortex (vMPFC) for SCZ, and right pSTS in ASD. As predicted, these effects were caused in a group specific way: Relative increased activation for physical information processing in SCZ that was also correlated with positive PANNS score and relative decreased activation for intentional information processing in ASD. Additionally, we could demonstrate opposed connectivity patterns between the right pSTS and vMPFC in the clinical groups, ie, increased for SCZ, decreased for ASD. These findings represent opposed neural signatures in key regions of the social brain as predicted by the hyper-hypo-intentionality hypothesis.     

Eyes on me: an fMRI study of the effects of social gaze on action control

Previous evidence suggests that ‘social gaze’ can not only cause shifts in attention, but also can change the perception of objects located in the direction of gaze and how these objects will be manipulated by an observer. These findings implicate differences in the neural networks sub-serving action control driven by social cues as compared with nonsocial cues. Here, we sought to explore this hypothesis by using functional magnetic resonance imaging and a stimulus–response compatibility paradigm in which participants were asked to generate spatially congruent or incongruent motor responses to both social and nonsocial stimuli. Data analysis revealed recruitment of a dorsal frontoparietal network and the locus coeruleus for the generation of incongruent motor responses, areas previously implicated in controlling attention. As a correlate for the effect of ‘social gaze’ on action control, an interaction effect was observed for incongruent responses to social stimuli in sub-cortical structures, anterior cingulate and inferior frontal cortex. Our results, therefore, suggest that performing actions in a—albeit minimal—social context significantly changes the neural underpinnings of action control and recruits brain regions previously implicated in action monitoring, the reorienting of attention and social cognition.     

Neural mechanisms of social influence in adolescence

During the transformative period of adolescence, social influence plays a prominent role in shaping young people’s emerging social identities, and can impact their propensity to engage in prosocial or risky behaviors. In this study, we examine the neural correlates of social influence from both parents and peers, two important sources of influence. Nineteen adolescents (age 16–18 years) completed a social influence task during a functional magnetic resonance imaging (fMRI) scan. Social influence from both sources evoked activity in brain regions implicated in mentalizing (medial prefrontal cortex, left temporoparietal junction, right temporoparietal junction), reward (ventromedial prefrontal cortex), and self-control (right ventrolateral prefrontal cortex). These results suggest that mental state reasoning, social reward and self-control processes may help adolescents to evaluate others’ perspectives and overcome the prepotent force of their own antecedent attitudes to shift their attitudes toward those of others. Findings suggest common neural networks involved in social influence from both parents and peers.     

Network structure underlying resolution of conflicting non-verbal and verbal social information

Social judgments often require resolution of incongruity in communication contents. Although previous studies revealed that such conflict resolution recruits brain regions including the medial prefrontal cortex (mPFC) and posterior inferior frontal gyrus (pIFG), functional relationships and networks among these regions remain unclear. In this functional magnetic resonance imaging study, we investigated the functional dissociation and networks by measuring human brain activity during resolving incongruity between verbal and non-verbal emotional contents. First, we found that the conflict resolutions biased by the non-verbal contents activated the posterior dorsal mPFC (post-dmPFC), bilateral anterior insula (AI) and right dorsal pIFG, whereas the resolutions biased by the verbal contents activated the bilateral ventral pIFG. In contrast, the anterior dmPFC (ant-dmPFC), bilateral superior temporal sulcus and fusiform gyrus were commonly involved in both of the resolutions. Second, we found that the post-dmPFC and right ventral pIFG were hub regions in networks underlying the non-verbal– and verbal–content-biased resolutions, respectively. Finally, we revealed that these resolution-type–specific networks were bridged by the ant-dmPFC, which was recruited for the conflict resolutions earlier than the two hub regions. These findings suggest that, in social conflict resolutions, the ant-dmPFC selectively recruits one of the resolution-type–specific networks through its interaction with resolution-type–specific hub regions.