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.     

The development of the social brain in human infancy

Much research has focused on how the adult human brain processes the social world, yet until recently little was known about the early development of these abilities. Developmental studies inform debates about the specificity of social functions in the adult cortex. This review highlights recent work, mainly based on electroencephalography/event-related potential methods, examining the precursors of the human social brain network during infancy in several domains such as face and eye gaze processing, the perception of emotions, decoding biological motion, perceiving human actions and joint attention. The findings illustrate that the human brain is fundamentally adapted to develop within a social context, and that this context contributes to many of the specializations seen in the adult cortex.     

A longitudinal analysis of neural regions involved in reading the mind in the eyes

The ability to perceive social intentions from people’s eyes is present from an early age, yet little is known about whether this skill is fully developed in childhood or that subtle changes may still occur across adolescence. This fMRI study investigated the ability to read mental states by using an adapted version of the Reading the Mind in the Eyes task within adolescents (aged 12–19 years) over a 2-year test–retest interval. This longitudinal setup provides the opportunity to study both stability over time as well as age-related changes. The behavioral results showed that participants who performed well in the mental state condition at the first measurement also performed well at the second measurement. fMRI results revealed positive test–retest correlations of neural activity in the right superior temporal sulcus and right inferior frontal gyrus for the contrast mental state > control, suggesting stability within individuals over time. Besides stability of activation, dorsal medial prefrontal cortex showed a dip in mid-adolescence for the mental state > control condition and right inferior frontal gyrus decreased linearly with age for the mental state > control condition. These findings underline changes in the slope of the developmental pattern depending on age, even in the existence of relatively stable activation in the social brain network.     

Different types of Internet use, depression, and social anxiety: The role of perceived friendship quality

The current study examined the longitudinal associations of time spent on Internet activities for communication purposes (i.e., IM-ing) versus time spent on Internet activities for non-communication purposes (i.e., surfing) with depression and social anxiety, as well as the moderating role of perceived friendship quality in these associations. Questionnaire data were gathered from 307 Dutch middle adolescents (average age 15 years) on two waves with a one-year interval. For adolescents who perceive low friendship quality, Internet use for communication purposes predicted less depression, whereas Internet use for non-communication purposes predicted more depression and more social anxiety. These results support social compensation effects of IM-ing on depression and poor-get-poorer effects of surfing on depression and social anxiety, respectively.     

Moral values are associated with individual differences in regional brain volume

Moral sentiment has been hypothesized to reflect evolved adaptations to social living. If so, individual differences in moral values may relate to regional variation in brain structure. We tested this hypothesis in a sample of 70 young, healthy adults examining whether differences on two major dimensions of moral values were significantly associated with regional gray matter volume. The two clusters of moral values assessed were "individualizing" (values of harm/care and fairness) and "binding" (deference to authority, in-group loyalty, and purity/sanctity). Individualizing was positively associated with left dorsomedial pFC volume and negatively associated with bilateral precuneus volume. For binding, a significant positive association was found for bilateral subcallosal gyrus and a trend to significance for the left anterior insula volume. These findings demonstrate that variation in moral sentiment reflects individual differences in brain structure and suggest a biological basis for moral sentiment, distributed across multiple brain regions.     

Experiences of sexual harassment are associated with high self-esteem and social anxiety among adolescent girls

Abstract

Introduction: Subjection to sexual harassment among adolescents have been associated with negative mental health outcomes, such as depression and social anxiety. Self-esteem and social support may modify these associations.

Methods: The Adolescent Mental Health Cohort 10-year replication data were used. It is a cross-sectional classroom survey involving 656 girls and 636 boys aged (mean (sd)) 15.6 (0.4) years and 15.7 (0.4) years, respectively. Subjection to sexual harassment was elicited with five questions. Depression was measured by the Beck’s 13-item Depression Inventory, social anxiety by the SPIN-Fin Inventory, self-esteem by Rosenberg’s Self-Esteem Scale and social support by the PSSS-R scale. The data were analysed using cross-tabulations with chi-square statistics and logistic regressions.

Resutls: Among girls, social anxiety and higher self-esteem were positively associated with experiencing subjection to sexual harassment in multivariate models. No statistically significant associations were detected among boys between experiences of sexual harassment and any of the four variables.

Conclusion: Experiences of being sexually harassed correlate among adolescents with high social anxiety but also with high self-esteem. Sexual harassment among adolescents may partly be explained as inept ways of showing interest, but it may nevertheless have detrimental effects on the well-being of the those subjected to it.     

Extensive individual differences in brain activations associated with episodic retrieval are reliable over time

The localization of brain functions using neuroimaging techniques is commonly dependent on statistical analyses of groups of subjects in order to identify sites of activation, particularly in studies of episodic memory. Exclusive reliance on group analysis may be to the detriment of understanding the true underlying cognitive nature of brain activations. In the present study, we found that the patterns of brain activity associated with episodic retrieval are very distinct for individual subjects from the patterns of brain activity at the group level. These differences go beyond the relatively small variations due to cyctoarchitectonic differences or spatial normalization. We quantify this individual variability by cross-correlating volumes of brain images. We demonstrate that individual patterns of brain activity are reliable over time despite their extensive variability. We suggest that varied but reliable individual patterns of significant brain activity may be indicative of different cognitive strategies used to produce a recognition response. We believe that individual analysis in conjunction with group analysis may be critical to fully understanding the relationship between retrieval processes and underlying brain regions.     

Developmental differences in the neural mechanisms of facial emotion labeling

Adolescence is a time of increased risk for the onset of psychological disorders associated with deficits in face emotion labeling. We used functional magnetic resonance imaging (fMRI) to examine age-related differences in brain activation while adolescents and adults labeled the emotion on fearful, happy and angry faces of varying intensities [0% (i.e. neutral), 50%, 75%, 100%]. Adolescents and adults did not differ on accuracy to label emotions. In the superior temporal sulcus, ventrolateral prefrontal cortex and middle temporal gyrus, adults show an inverted-U-shaped response to increasing intensities of fearful faces and a U-shaped response to increasing intensities of happy faces, whereas adolescents show the opposite patterns. In addition, adults, but not adolescents, show greater inferior occipital gyrus activation to negative (angry, fearful) vs positive (happy) emotions. In sum, when subjects classify subtly varying facial emotions, developmental differences manifest in several ‘ventral stream’ brain regions. Charting the typical developmental course of the brain mechanisms of socioemotional processes, such as facial emotion labeling, is an important focus for developmental psychopathology research.     

Gray matter volumes of early sensory regions are associated with individual differences in sensory processing

Sensory processing (i.e., the manner in which the nervous system receives, modulates, integrates, and organizes sensory stimuli) is critical when humans are deciding how to react to environmental demands. Although behavioral studies have shown that there are stable individual differences in sensory processing, the neural substrates that implement such differences remain unknown. To investigate this issue, structural magnetic resonance imaging scans were acquired from 51 healthy adults and individual differences in sensory processing were assessed using the Sensory Profile questionnaire (Brown et al.: Am J Occup Ther 55 (2001) 75–82). There were positive relationships between the Sensory Profile modality‐specific subscales and gray matter volumes in the primary or secondary sensory areas for the visual, auditory, touch, and taste/smell modalities. Thus, the present results suggest that individual differences in sensory processing are implemented by the early sensory regions. Hum Brain Mapp 38:6206–6217, 2017. © 2017 Wiley Periodicals, Inc.     

Genetic influences on individual differences in longitudinal changes in global and subcortical brain volumes: Results of the ENIGMA plasticity working group

Structural brain changes that occur during development and ageing are related to mental health and general cognitive functioning. Individuals differ in the extent to which their brain volumes change over time, but whether these differences can be attributed to differences in their genotypes has not been widely studied. Here we estimate heritability (h²) of changes in global and subcortical brain volumes in five longitudinal twin cohorts from across the world and in different stages of the lifespan (N = 861). Heritability estimates of brain changes were significant and ranged from 16% (caudate) to 42% (cerebellar gray matter) for all global and most subcortical volumes (with the exception of thalamus and pallidum). Heritability estimates of change rates were generally higher in adults than in children suggesting an increasing influence of genetic factors explaining individual differences in brain structural changes with age. In children, environmental influences in part explained individual differences in developmental changes in brain structure. Multivariate genetic modeling showed that genetic influences of change rates and baseline volume significantly overlapped for many structures. The genetic influences explaining individual differences in the change rate for cerebellum, cerebellar gray matter and lateral ventricles were independent of the genetic influences explaining differences in their baseline volumes. These results imply the existence of genetic variants that are specific for brain plasticity, rather than brain volume itself. Identifying these genes may increase our understanding of brain development and ageing and possibly have implications for diseases that are characterized by deviant developmental trajectories of brain structure. Hum Brain Mapp 38:4444–4458, 2017. © 2017 Wiley Periodicals, Inc.     

Impact of traumatic brain injury on social cognition in adolescents and contribution of other higher order cognitive functions

Social cognition impairments can contribute to social participation difficulties following traumatic brain injury (TBI). However, little attention has been given to these impairments during adolescence, a period of life when peer relationships are central. The aim of the current study was to examine the impact of a moderate to severe TBI sustained in adolescence on multiple facets of social cognition. Twenty-three adolescents who had sustained a moderate-to-severe TBI were compared with a group of 23 typically developing peers. The Integrated Social Cognition Battery (mentalising, social knowledge, emotion recognition) and the Interpersonal Reactivity Index were administered, along with non-social cognition tests (selective attention, working memory, executive functions), IQ estimation, and a socio-demographic questionnaire. Adolescents with TBI reported having a significantly lower ability to take other people's perspectives versus controls. They also presented significantly lower levels of mentalising. After controlling for non-social higher-order cognitive variables, the group effect on mentalising remained marginally significant, whereas the effect on perspective taking remained significant. Our findings suggest the presence of primary deficits in social cognition following TBI in adolescence. These deficits could partially underlie the social reintegration difficulties encountered following TBI. A systematic assessment of social cognition in clinical practice is necessary.     

Non-invasive stimulation of the social brain: the methodological challenges

Use of non-invasive brain stimulation methods (NIBS) has become a common approach to study social processing in addition to behavioural, imaging and lesion studies. However, research using NIBS to investigate social processing faces challenges. Overcoming these is important to allow valid and reliable interpretation of findings in neurotypical cohorts, but also to allow us to tailor NIBS protocols to atypical groups with social difficulties. In this review, we consider the utility of brain stimulation as a technique to study and modulate social processing. We also discuss challenges that face researchers using NIBS to study social processing in neurotypical adults with a view to highlighting potential solutions. Finally, we discuss additional challenges that face researchers using NIBS to study and modulate social processing in atypical groups. These are important to consider given that NIBS protocols are rarely tailored to atypical groups before use. Instead, many rely on protocols designed for neurotypical adults despite differences in brain function that are likely to impact response to NIBS.     

Invited Review: Factors associated with atypical brain development in preterm infants: insights from magnetic resonance imaging

Preterm birth (PTB) is a leading cause of neurodevelopmental and neurocognitive impairment in childhood and is closely associated with psychiatric disease. The biological and environmental factors that confer risk and resilience for healthy brain development and long-term outcome after PTB are uncertain, which presents challenges for risk stratification and for the discovery and evaluation of neuroprotective strategies. Neonatal magnetic resonance imaging reveals a signature of PTB that includes dysconnectivity of neural networks and atypical development of cortical and deep grey matter structures. Here we provide a brief review of perinatal factors that are associated with the MRI signature of PTB. We consider maternal and foetal factors including chorioamnionitis, foetal growth restriction, socioeconomic deprivation and prenatal alcohol, drug and stress exposures; and neonatal factors including co-morbidities of PTB, nutrition, pain and medication during neonatal intensive care and variation conferred by the genome/epigenome. Association studies offer the first insights into pathways to adversity and resilience after PTB. Future challenges are to analyse quantitative brain MRI data with collateral biological and environmental data in study designs that support causal inference, and ultimately to use the output of such analyses to stratify infants for clinical trials of therapies designed to improve outcome.     

Cortical brain development in schizophrenia: insights from neuroimaging studies in childhood-onset schizophrenia

Childhood-onset schizophrenia (COS; defined as onset by age 12 years) is rare, difficult to diagnose, and represents a severe and chronic phenotype of the adult-onset illness. A study of childhood-onset psychoses has been ongoing at the National Institute of Mental Health (NIMH) since 1990, where children with COS and severe atypical psychoses (provisionally labeled "multidimensionally impaired" or MDI by the NIMH team) are studied prospectively along with all first-degree relatives. COS subjects have robust cortical gray matter (GM) loss during adolescence, which appears to be an exaggeration of the normal cortical GM developmental pattern and eventually mimics the pattern seen in adult-onset cases as the children become young adults. These cortical GM changes in COS are diagnostically specific and seemingly unrelated to the effects of medications. Furthermore, the cortical GM loss is also shared by healthy full siblings of COS probands suggesting a genetic influence on the abnormal brain development.     

Altered structure and functional connectivity of the hippocampus are associated with social and mathematical difficulties in nonverbal learning disability

The hippocampus is known to play a critical role in a variety of complex abilities, including visual‐spatial reasoning, social functioning, and math. Nonverbal learning disability (NVLD) is a neurodevelopmental disorder characterized by deficits in visual‐spatial reasoning that are accompanied by impairment in social function or mathematics, as well as motor or executive function skills. Despite the overlap between behaviors supported by the hippocampus and impairments in NVLD, the structure and function of the hippocampus in NVLD has not been studied. To address this gap in the literature, we first compared hippocampal volume and resting‐state functional connectivity in children with NVLD (n = 24) and typically developing (TD) children (n = 20). We then explored associations between hippocampal structure, connectivity, and performance on measures of spatial, social, and mathematical ability. Relative to TD children, those with NVLD showed significant reductions in left hippocampal volume and greater hippocampal‐cerebellar connectivity. In children with NVLD, reduced hippocampal volume associated with worse mathematical problem solving. Although children with NVLD exhibited more social problems (social responsiveness scale [SRS]) and higher hippocampal‐cerebellar connectivity relative to TD children, greater connectivity was associated with fewer social problems among children with NVLD but not TD children. Such an effect may suggest a compensatory mechanism. These structural and functional alterations of the hippocampus may disrupt its putative role in organizing conceptual frameworks through cognitive mapping, thus contributing to the cross‐domain difficulties that characterize NVLD.     

Immediate early gene activation throughout the brain is associated with dynamic changes in social context

Social competence is dependent on successful processing of social context information. The social opportunity paradigm is a methodology in which dynamic shifts in social context are induced through removal of the alpha male in a dominance hierarchy, leading to rapid ascent in the hierarchy of the beta male and of other subordinate males in the social group. In the current study, we use the social opportunity paradigm to determine what brain regions respond to this dynamic change in social context, allowing an individual to recognize the absence of the alpha male and subsequently perform status-appropriate social behaviors. Replicating our previous work, we show that following removal of the alpha male, beta males rapidly ascend the social hierarchy and attain dominant status by increasing aggression towards more subordinate individuals. Analysis of patterns of Fos immunoreactivity throughout the brain indicates that in individuals undergoing social ascent, there is increased activity in regions of the social behavior network, as well as the infralimbic and prelimbic regions of the prefrontal cortex and areas of the hippocampus. Our findings demonstrate that male mice are able to respond to changes in social context and provide insight into the how the brain processes these complex behavioral changes.     

Large-scale investigation of white matter structural differences in bilingual and monolingual children: An adolescent brain cognitive development data study

Emerging research has provided valuable insights into the structural characteristics of the bilingual brain from studies of bilingual adults; however, there is a dearth of evidence examining brain structural alterations in childhood associated with the bilingual experience. This study examined the associations between bilingualism and white matter organization in bilingual children compared to monolingual peers leveraging the large-scale data from the Adolescent Brain Cognitive Development (ABCD) Study. Then, 446 bilingual children (ages 9–10) were identified from the participants in the ABCD data and rigorously matched to a group of 446 monolingual peers. Multiple regression models for selected language and cognitive control white matter pathways were used to compare white matter fractional anisotropy (FA) values between bilinguals and monolinguals, controlling for demographic and environmental factors as covariates in the models. Results revealed significantly lower FA values in bilinguals compared to monolinguals across established dorsal and ventral language network pathways bilaterally (i.e., the superior longitudinal fasciculus and inferior frontal-occipital fasciculus) and right-hemispheric pathways in areas related to cognitive control and short-term memory (i.e., cingulum and parahippocampal cingulum). In contrast to the enhanced FA values observed in adult bilinguals relative to monolinguals, our findings of lower FA in bilingual children relative to monolinguals may suggest a protracted development of white matter pathways associated with language and cognitive control resulting from dual language learning in childhood. Further, these findings underscore the need for large-scale longitudinal investigation of white matter development in bilingual children to understand neuroplasticity associated with the bilingual experience during this period of heightened language learning.     

Co-ordinated structural and functional covariance in the adolescent brain underlies face processing performance

Our ability to process complex social cues presented by faces improves during adolescence. Using multivariate analyses of neuroimaging data collected longitudinally from a sample of 38 adolescents (17 males) when they were 10, 11.5, 13 and 15 years old, we tested the possibility that there exists parallel variations in the structural and functional development of neural systems supporting face processing. By combining measures of task-related functional connectivity and brain morphology, we reveal that both the structural covariance and functional connectivity among ‘distal’ nodes of the face-processing network engaged by ambiguous faces increase during this age range. Furthermore, we show that the trajectory of increasing functional connectivity between the distal nodes occurs in tandem with the development of their structural covariance. This demonstrates a tight coupling between functional and structural maturation within the face-processing network. Finally, we demonstrate that increased functional connectivity is associated with age-related improvements of face-processing performance, particularly in females. We suggest that our findings reflect greater integration among distal elements of the neural systems supporting the processing of facial expressions. This, in turn, might facilitate an enhanced extraction of social information from faces during a time when greater importance is placed on social interactions.     

The awareness of social inference test: development of a shortened version for use in adults with acquired brain injury

Objective: The Awareness of Social Inference Test (TASIT) is an ecologically valid test of complex social perception. Despite its utility for detecting social perception deficits in clinical groups, its lengthy administration time has limited its routine use in clinical practice. This paper describes the development and validation of a shortened version of the TASIT (TASIT-S) in 160 individuals (males = 129) with moderate to severe acquired brain injury (ABI).

Method: Both Rasch and confirmatory factor analysis modeling were used to create the TASIT-S, which, consistent with the original test, included the following subtests: (1) Emotion Evaluation Test (10 items), assessing basic emotion recognition; (2) Social Inference (Minimal) Test (9 items), assessing understanding of sincere and sarcastic exchanges; and (3) Social Inference (Enriched) Test (9 items), assessing comprehension of lies and sarcasm.

Results: The TASIT-S demonstrated excellent construct validity as evidenced by its high correlations with the original TASIT and correlations with social cognition and cognitive neuropsychological measures. Importantly, the TASIT-S also successfully differentiated between ABI participants and healthy controls (n = 43).

Conclusions: The new shortened version of the TASIT is a promising new tool with excellent psychometric properties that can assist clinicians with the detection of complex social perception deficits in ABI.