Chronic Childhood Peer Rejection is Associated with Heightened Neural Responses to Social Exclusion During Adolescence

This functional Magnetic Resonance Imaging (fMRI) study examined subjective and neural responses to social exclusion in adolescents (age 12–15) who either had a stable accepted (n?=?27; 14 males) or a chronic rejected (n?=?19; 12 males) status among peers from age 6 to 12. Both groups of adolescents reported similar increases in distress after being excluded in a virtual ball-tossing game (Cyberball), but adolescents with a history of chronic peer rejection showed higher activity in brain regions previously linked to the detection of, and the distress caused by, social exclusion. Specifically, compared with stably accepted adolescents, chronically rejected adolescents displayed: 1) higher activity in the dorsal anterior cingulate cortex (dACC) during social exclusion and 2) higher activity in the dACC and anterior prefrontal cortex when they were incidentally excluded in a social interaction in which they were overall included. These findings demonstrate that chronic childhood peer rejection is associated with heightened neural responses to social exclusion during adolescence, which has implications for understanding the processes through which peer rejection may lead to adverse effects on mental health over time.     

Adolescents’ neural response to social reward and real-world emotional closeness and positive affect

Feeling emotionally close to others during social interactions is a ubiquitous and meaningful experience that can elicit positive affect. The present study integrates functional magnetic resonance imaging (fMRI) and ecological momentary assessment (EMA) to investigate whether neural response to social reward (1) is related to the experience of emotional closeness and (2) moderates the association between emotional closeness and positive affect during and following social interactions. In this study, 34 typically developing adolescents (ages 14–18 years) completed a social-reward fMRI task, a monetary-reward fMRI task, and a 2-week EMA protocol regarding their social and affective experiences. Adolescents with greater right posterior superior temporal sulcus/temporoparietal junction (pSTS/TPJ) response to social reward reported greater mean momentary emotional closeness. Neural response to social reward in the right pSTS/TPJ moderated how strongly momentary emotional closeness was associated with both concurrent positive affect and future peak happiness, but in different ways. Although emotional closeness had a significant positive association with concurrent positive affect among adolescents at both high and low right pSTS/TPJ response based on a follow-up simple slopes test, this association was stronger for adolescents with low right pSTS/TPJ response. In contrast, emotional closeness had a significant positive association with future peak happiness among adolescents with high right pSTS/TPJ response, but not among those with low right pSTS/TPJ response. These findings demonstrate the importance of neural response to social reward in key social processing regions for everyday experiences of emotional closeness and positive affect in the context of social interactions.     

The push of social pain: Does rejection’s sting motivate subsequent social reconnection?

Physical pain motivates the healing of somatic injuries, yet it remains unknown whether social pain serves a similarly reparative function toward social injuries. Given the substantial overlap between physical and social pain, we predicted that social pain would mediate the effect of rejection on greater motivation for social reconnection and affiliative behavior toward rejecters. In Study 1, the effect of rejection on an increased need to belong was mediated by reports of more intense social pain. In Study 2, three neural signatures of social pain (i.e., activity in the dorsal anterior cingulate cortex, left and right anterior insula during social rejection), each predicted greater behavioral proximity to rejecters. Our findings reify the overlap between social and physical pain. Furthermore, these results are some of the first to demonstrate the reparative nature of social pain and lend insight into how this process may be harnessed to promote postrejection reconnection.     

Gut feelings and the reaction to perceived inequity: The interplay between bodily responses, regulation, and perception shapes the rejection of unfair offers on the ultimatum game

It has been robustly demonstrated using the ultimatum game (UG) that individuals frequently reject unfair financial offers even if this results in a personal cost. One influential hypothesis for these rejections is that they reflect an emotional reaction to unfairness that overrides purely economic decision processes. In the present study, we examined whether the interplay between bodily responses, bodily regulation, and bodily perception ("interoception") contributes to emotionally driven rejection behavior on the UG. Offering support for bodily feedback theories, interoceptive accuracy moderated the relationship between changes in electrodermal activity to proposals and the behavioral rejection of such offers. Larger electrodermal responses to rejected relative to accepted offers predicted greater rejection in those with accurate interoception but were unrelated to rejection in those with poor interoception. Although cardiovascular responses during the offer period were unrelated to rejection rates, greater resting heart rate variability (linked to trait emotion regulation capacity) predicted reduced rejection rates of offers. These findings help clarify individual differences in reactions to perceived unfairness, support previous emotion regulation deficit accounts of rejection behavior, and suggest that the perception and regulation of bodily based emotional biasing signals ("gut feelings") partly shape financial decision making on the UG.     

The effects of the behavioral inhibition and activation systems on social inclusion and exclusion

Human beings have a strong fundamental need to form and maintain relationships. Social exclusion therefore evokes social pain in excluded individuals, whereas social inclusion evokes pleasure in those individuals who are included. The present study used near-infrared spectroscopy (NIRS) to investigate whether individual differences in personality, specifically differences in behavioral inhibition and activation system (BIS and BAS) functioning, affect the experiences of social pleasure and pain. Thirty-seven undergraduates participated in an NIRS session that involved both social rejection and inclusion during an online ball-tossing game. People with greater BIS sensitivity experienced more social pain during social exclusion, while people with greater BAS sensitivity reported more social pleasure during social inclusion. BIS sensitivity was negatively correlated with ventrolateral prefrontal cortex (VLPFC) activity during social exclusion. Finally, VLPFC activity partially mediated the relationship between BIS sensitivity and social pain experienced during social exclusion.     

Identifying the neural substrates of intrinsic motivation during task performance

Intrinsic motivation is the inherent tendency to seek out novelty and challenge, to explore and investigate, and to stretch and extend one’s capacities. When people imagine performing intrinsically motivating tasks, they show heightened anterior insular cortex (AIC) activity. To fully explain the neural system of intrinsic motivation, however, requires assessing neural activity while people actually perform intrinsically motivating tasks (i.e., while answering curiosity-inducing questions or solving competence-enabling anagrams). Using event-related functional magnetic resonance imaging, we found that the neural system of intrinsic motivation involves not only AIC activity, but also striatum activity and, further, AIC–striatum functional interactions. These findings suggest that subjective feelings of intrinsic satisfaction (associated with AIC activations), reward processing (associated with striatum activations), and their interactions underlie the actual experience of intrinsic motivation. These neural findings are consistent with the conceptualization of intrinsic motivation as the pursuit and satisfaction of subjective feelings (interest and enjoyment) as intrinsic rewards.     

Kin rejection: social signals,neural response and perceived distress during social exclusion

Across species, kin bond together to promote survival. We sought to understand the dyadic effect of exclusion by kin (as opposed to non‐kin strangers) on brain activity of the mother and her child and their subjective distress. To this end, we probed mother–child relationships with a computerized ball‐toss game Cyberball. When excluded by one another, rather than by a stranger, both mothers and children exhibited a significantly pronounced frontal P2. Moreover, upon kin rejection versus stranger rejection, both mothers and children showed incremented left frontal positive slow waves for rejection events. Children reported more distress upon exclusion than their own mothers. Similar to past work, relatively augmented negative frontal slow wave activity predicted greater self‐reported ostracism distress. This effect, generalized to the P2, was limited to mother‐ or child‐rejection by kin, with comparable magnitude of effect across kin identity (mothers vs. children). For both mothers and children, the frontal P2 peak was significantly pronounced for kin rejection versus stranger rejection. Taken together, our results document the rapid categorization of social signals as kin relevant and the specificity of early and late neural markers for predicting felt ostracism.     

Brain activation while forming memories of fearful and neutral faces in women and men

Event-related functional MRI (fMRI) was used to assess brain activity during encoding of fearful and neutral faces in 12 women and 12 men. In a subsequent memory analysis, the authors separated successful from unsuccessful encoding of both types of faces, based on whether they were remembered or forgotten in a later recognition memory test. Overall, women and men recruited overlapping neural circuitries. Both sexes activated right-sided medial-temporal regions during successful encoding of fearful faces. Successful encoding of neutral faces was associated with left-sided lateral prefrontal and right-sided superior frontal activation in both sexes. In women, relatively greater encoding related activity for neutral faces was seen in the superior parietal and parahippocampal cortices. By contrast, men activated the left and right superior/middle frontal cortex more than women during successful encoding of the same neutral faces. These findings suggest that women and men use similar neural networks to encode facial information, with only subtle sex differences observed for neutral faces.     

Neural correlates of feigned memory impairment are distinguishable from answering randomly and answering incorrectly: an fMRI and behavioral study

Previous functional magnetic resonance imaging (fMRI) studies have identified activation in the prefrontal-parietal-sub-cortical circuit during feigned memory impairment when comparing with truthful telling. Here, we used fMRI to determine whether neural activity can differentiate between answering correctly, answering randomly, answering incorrectly, and feigned memory impairment. In this study, 12 healthy subjects underwent block-design fMRI while they performed digit task of forced-choice format under four conditions: answering correctly, answering randomly, answering incorrectly, and simulated feigned memory impairment. There were three main results. First, six areas, including the left prefrontal cortex, the left superior temporal lobe, the right postcentral gyrus, the right superior parietal cortex, the right superior occipital cortex, and the right putamen, were significantly modulated by condition type. Second, for some areas, including the right superior parietal cortex, the right postcentral gyrus, the right superior occipital cortex, and the right putamen, brain activity was significantly greater in feigned memory impairment than answering randomly. Third, for the areas including the left prefrontal cortex and the right putamen, brain activity was significantly greater in feigned memory impairment than answering incorrectly. In contrast, for the left superior temporal lobe, brain activity was significantly greater in answering incorrectly than feigned memory impairment. The results suggest that neural correlates of feigned memory impairment are distinguishable from answering randomly and answering incorrectly in healthy subjects.     

I Did OK,but Did I Like It? Using Ecological Momentary Assessment to Examine Perceptions of Social Interactions Associated With Severity of Social Anxiety and Depression

Socially anxious and depressed individuals tend to evaluate their social interactions negatively, but little is known about the specific real-time contributors to these negative perceptions. The current study examined how affect ratings during social interactions predict later perceptions of those interactions, and whether this differs by social anxiety and depression severity. Undergraduate participants (N = 60) responded to a smartphone application that prompted participants to answer short questions about their current affect and social context up to 6 times a day for 2 weeks. At the end of each day, participants answered questions about their perceptions of their social interactions from that day. Results indicated that the link between negative affective experiences reported during social interactions and the end-of-day report of enjoyment (but not effectiveness) of those experiences was more negative when social anxiety was more severe. The link between negative affective experiences rated during social interactions and the end-of-day report of effectiveness (but not enjoyment) during those social encounters was more negative when depression was more severe. These findings demonstrate the importance of examining self-perceptions of social interactions based both on the extent to which individuals think that they met the objective demands of an interaction (i.e., effectiveness, mastery) and the extent to which they liked or disliked that interaction (i.e., enjoyment, pleasure). These findings also highlight how real-time assessments of daily social interactions may reveal the key experiences that contribute to negative self-evaluations across disorders, potentially identifying critical targets for therapy.     

Separable neural components in the processing of black and white faces

In a study of the neural components of automatic and controlled social evaluation, White participants viewed Black and White faces during event-related functional magnetic resonance imaging. When the faces were presented for 30 ms, activation in the amygdala-a brain region associated with emotion-was greater for Black than for White faces. When the faces were presented for 525 ms, this difference was significantly reduced, and regions of frontal cortex associated with control and regulation showed greater activation for Black than White faces. Furthermore, greater race bias on an indirect behavioral measure was correlated with greater difference in amygdala activation between Black and White faces, and frontal activity predicted a reduction in Black-White differences in amygdala activity from the 30-ms to the 525-ms condition. These results provide evidence for neural distinctions between automatic and more controlled processing of social groups, and suggest that controlled processes may modulate automatic evaluation.     

Role of the hippocampus and orbitofrontal cortex during the disambiguation of social cues in working memory

Human social interactions are complex behaviors requiring the concerted effort of multiple neural systems to track and monitor the individuals around us. Cognitively, adjusting our behavior on the basis of changing social cues such as facial expressions relies on working memory and the ability to disambiguate, or separate, the representations of overlapping stimuli resulting from viewing the same individual with different facial expressions. We conducted an fMRI experiment examining the brain regions contributing to the encoding, maintenance, and retrieval of overlapping identity information during working memory using a delayed match-to-sample task. In the overlapping condition, two faces from the same individual with different facial expressions were presented at sample. In the nonoverlapping condition, the two sample faces were from two different individuals with different expressions. fMRI activity was assessed by contrasting the overlapping and nonoverlapping conditions at sample, delay, and test. The lateral orbitofrontal cortex showed increased fMRI signal in the overlapping condition in all three phases of the delayed match-to-sample task and increased functional connectivity with the hippocampus when encoding overlapping stimuli. The hippocampus showed increased fMRI signal at test. These data suggest that lateral orbitofrontal cortex helps encode and maintain representations of overlapping stimuli in working memory, whereas the orbitofrontal cortex and hippocampus contribute to the successful retrieval of overlapping stimuli. We suggest that the lateral orbitofrontal cortex and hippocampus play a role in encoding, maintaining, and retrieving social cues, especially when multiple interactions with an individual need to be disambiguated in a rapidly changing social context in order to make appropriate social responses.     

Spatial and temporal episodic memory retrieval recruit dissociable functional networks in the human brain

Imaging, electrophysiological studies, and lesion work have shown that the medial temporal lobe (MTL) is important for episodic memory; however, it is unclear whether different MTL regions support the spatial, temporal, and item elements of episodic memory. In this study we used fMRI to examine retrieval performance emphasizing different aspects of episodic memory in the context of a spatial navigation paradigm. Subjects played a taxi-driver game ("yellowcab"), in which they freely searched for passengers and delivered them to specific landmark stores. Subjects then underwent fMRI scanning as they retrieved landmarks, spatial, and temporal associations from their navigational experience in three separate runs. Consistent with previous findings on item memory, perirhinal cortex activated most strongly during landmark retrieval compared with spatial or temporal source information retrieval. Both hippocampus and parahippocampal cortex activated significantly during retrieval of landmarks, spatial associations, and temporal order. We found, however, a significant dissociation between hippocampal and parahippocampal cortex activations, with spatial retrieval leading to greater parahippocampal activation compared with hippocampus and temporal order retrieval leading to greater hippocampal activation compared with parahippocampal cortex. Our results, coupled with previous findings, demonstrate that the hippocampus and parahippocampal cortex are preferentially recruited during temporal order and spatial association retrieval--key components of episodic "source" memory.     

Neural mechanisms underlying subsequent memory for personal beliefs:An fMRI study

Many fMRI studies have examined the neural mechanisms supporting emotional memory for stimuli that generate emotion rather automatically (e.g., a picture of a dangerous animal or of appetizing food). However, far fewer studies have examined how memory is influenced by emotion related to social and political issues (e.g., a proposal for large changes in taxation policy), which clearly vary across individuals. In order to investigate the neural substrates of affective and mnemonic processes associated with personal opinions, we employed an fMRI task wherein participants rated the intensity of agreement/disagreement to sociopolitical belief statements paired with neural face pictures. Following the rating phase, participants performed an associative recognition test in which they distinguished identical versus recombined face–statement pairs. The study yielded three main findings: behaviorally, the intensity of agreement ratings was linked to greater subjective emotional arousal as well as enhanced high-confidence subsequent memory. Neurally, statements that elicited strong (vs. weak) agreement or disagreement were associated with greater activation of the amygdala. Finally, a subsequent memory analysis showed that the behavioral memory advantage for statements generating stronger ratings was dependent on the medial prefrontal cortex (mPFC). Together, these results both underscore consistencies in neural systems supporting emotional arousal and suggest a modulation of arousal-related encoding mechanisms when emotion is contingent on referencing personal beliefs.     

Contributions of the medial temporal lobe to declarative memory retrieval: manipulating the amount of contextual retrieval

We investigated how the hippocampus and its adjacent mediotemporal structures contribute to contextual and noncontextual declarative memory retrieval by manipulating the amount of contextual information across two levels of the same contextual dimension in a source memory task. A first analysis identified medial temporal lobe (MTL) substructures mediating either contextual or noncontextual retrieval. A linearly weighted analysis elucidated which MTL substructures show a gradually increasing neural activity, depending on the amount of contextual information retrieved. A hippocampal engagement was found during both levels of source memory but not during item memory retrieval. The anterior MTL including the perirhinal cortex was only engaged during item memory retrieval by an activity decrease. Only the posterior parahippocampal cortex showed an activation increasing with the amount of contextual information retrieved. If one assumes a roughly linear relationship between the blood-oxygenation level-dependent (BOLD) signal and the associated cognitive process, our results suggest that the posterior parahippocampal cortex is involved in contextual retrieval on the basis of memory strength while the hippocampus processes representations of item-context binding. The anterior MTL including perirhinal cortex seems to be particularly engaged in familiarity-based item recognition. If one assumes departure from linearity, however, our results can also be explained by one-dimensional modulation of memory strength.     

Community structure analysis of rejection sensitive personality profiles: A common neural response to social evaluative threat?

Monitoring social threat is essential for maintaining healthy social relationships, and recent studies suggest a neural alarm system that governs our response to social rejection. Frontal-midline theta (4–8 Hz) oscillatory power might act as a neural correlate of this system by being sensitive to unexpected social rejection. Here, we examined whether frontal-midline theta is modulated by individual differences in personality constructs sensitive to social disconnection. In addition, we examined the sensitivity of feedback-related brain potentials (i.e., the feedback-related negativity and P3) to social feedback. Sixty-five undergraduate female participants (mean age = 19.69 years) participated in the Social Judgment Paradigm, a fictitious peer-evaluation task in which participants provided expectancies about being liked/disliked by peer strangers. Thereafter, they received feedback signaling social acceptance/rejection. A community structure analysis was employed to delineate personality profiles in our data. Results provided evidence of two subgroups: one group scored high on attachment-related anxiety and fear of negative evaluation, whereas the other group scored high on attachment-related avoidance and low on fear of negative evaluation. In both groups, unexpected rejection feedback yielded a significant increase in theta power. The feedback-related negativity was sensitive to unexpected feedback, regardless of valence, and was largest for unexpected rejection feedback. The feedback-related P3 was significantly enhanced in response to expected social acceptance feedback. Together, these findings confirm the sensitivity of frontal midline theta oscillations to the processing of social threat, and suggest that this alleged neural alarm system behaves similarly in individuals that differ in personality constructs relevant to social evaluation.     

Regional gray matter volume is associated with rejection sensitivity: A voxel-based morphometry study

Rejection sensitivity (RS) can be defined as the disposition that one tends to anxiously expect, readily perceive, and intensely react to rejection. High-RS individuals are more likely to suffer mental disorders. Previous studies have investigated brain activity during social rejection using different kinds of rejection paradigms and have provided neural evidence of individual differences in response to rejection cues, but the association between individual differences in RS and brain structure has never been investigated. In this study, voxel-based morphometry (VBM) was used to investigate the relationship between gray matter volume (GMV) and RS in a large healthy sample of 150 men and 188 women. The participants completed the RS Questionnaire and underwent an anatomical magnetic resonance imaging scan. Multiple regression was used to analyze the correlation between regional GMV and RS scores, adjusting for age, sex, and total brain GMV. These results showed that GMV in the region of the posterior cingulate cortex/precuneus was negatively associated with RS, and GMV in the region of the inferior temporal gyrus was positively correlated with RS. These findings suggest a relationship between individual differences in RS and GMV in brain regions that are primarily related to social cognition.     

Brain activations associated with shifts in response criterion on a recognition test.

Sensitivity and bias can be manipulated independently on a recognition test. The goal of this fMRI study was to determine whether neural activations associated with manipulations of a decision criterion would be anatomically distinct from neural activations associated with manipulations of memory strength and episodic retrieval. The results indicated that activations associated with shifting criteria (a manipulation of bias) were located in bilateral regions of the lateral cerebellum, lateral parietal lobe, and the dorsolateral prefrontal cortex extending from the supplementary motor area. These regions were anatomically distinct from activations in the prefrontal cortex produced during memory-based retrieval processes (manipulations of sensitivity), which tended to be more medial and anterior. These later activations are consistent with previous studies of episodic retrieval. Determining patterns of neural activations associated with decision-making processes relative to memory processes has important implications for Cognitive Neuroscience, including the use of these patterns to compare memory models in different paradigms.     

The role of empathy in the neural responses to observed human social touch

One of the ways in which individuals convey feelings and thoughts to one another is through touch. Although the neural responses to felt and observed tactile stimuli between an inanimate object and a part of the human body have been vastly explored, the neural responses to observed human interaction involving touch are not well understood. Considering that the observation of social touch involves vicarious sharing of emotions, we hypothesized that levels of empathic traits modulate the neural responses to observed touch and focused on the attenuation in the mu\alpha rhythm (8–13Hz), a neural marker that has been related to sensorimotor resonance. Fifty-four participants observed photos depicting social touch, nonsocial touch, or no touch while their electroencephalography (EEG) activity was recorded. Results showed that interindividual differences in levels of empathic traits modulated both behavioral and electrophysiological responses to human social touch, such that highly empathic participants evaluated human social touch as inducing more pleasant emotions and exhibited greater mu suppression upon observation of human social touch compared to less empathic participants. Specifically, both the behavioral and the electrophysiological responses to observed social touch were predicted by levels of personal distress, a measure of emotional contagion. These findings indicate that the behavioral and electrophysiological responses to observed social touch are modulated by levels of empathy.     

Individual differences in working memory capacity predict action monitoring and the error-related negativity

Neuroscience suggests that the anterior cingulate cortex (ACC) is responsible for conflict monitoring and the detection of errors in cognitive tasks, thereby contributing to the implementation of attentional control. Though individual differences in frontally mediated goal maintenance have clearly been shown to influence outward behavior in interference-rich contexts, it is unclear whether corresponding differences exist in neural responses that arise out of the ACC. To investigate this possibility, we conducted an electrophysiological study using a variant of the Simon Task, recording event-related potentials (ERPs) in healthy normal individuals with varying working memory capacity (high vs. low spans; a behavioral proxy for variability in goal maintenance). Primary analyses focused on the magnitude of the error-related negativity (ERN), a response-locked ERP component associated with the commission of errors thought to arise because of action monitoring in the ACC. Our results revealed that frontally mediated working memory capacity may alter error monitoring by the ACC, with high spans showing a greater ERN than low spans. These individual differences were also observed in the posterror positivity, a response-locked ERP component associated with updating cognitive strategies, suggesting greater awareness of errors with increased working memory capacity. These results are interpreted within 2-process models of attentional control, suggesting individuals with greater working memory capacity may better maintain task goals by more strongly biasing neural activity in frontal-executive networks.