Neural and affective responses to prolonged eye contact with parents in depressed and nondepressed adolescents.

Eye contact improves mood, facilitates connectedness, and is assumed to strengthen the parent-child bond. Adolescent depression is linked to difficulties in social interactions, the parent-child bond included. Our goal was to elucidate adolescents' affective and neural responses to prolonged eye contact with one's parent in nondepressed adolescents (HC) and how these responses are affected in depressed adolescents. While in the scanner, 59 nondepressed and 19 depressed adolescents were asked to make eye contact with their parent, an unfamiliar peer, an unfamiliar adult, and themselves by using videos of prolonged direct and averted gaze, as an approximation of eye contact. After each trial, adolescents reported on their mood and feelings of connectedness, and eye movements and BOLD-responses were assessed. In HCs, eye contact boosted mood and feelings of connectedness and increased activity in inferior frontal gyrus (IFG), temporal pole, and superior frontal gyrus. Unlike HCs, eye contact did not boost the mood of depressed adolescents. While HCs reported increased mood and feelings of connectedness to the sight of their parent versus others, depressed adolescents did not. Depressed adolescents exhibited blunted overall IFG activity. These findings show that adolescents are particularly sensitive to eye contact and respond strongly to the sight of their parents. This sensitivity seems to be blunted in depressed adolescents. For clinical purposes, it is important to gain a better understanding of how the responsivity to eye contact in general and with their parents in particular, can be restored in adolescents with depression.

Sticky criticism? Affective and neural responses to parental criticism and praise in adolescents with depression.

BACKGROUND: Parent-adolescent interactions, particularly parental criticism and praise, have previously been identified as factors relevant to self-concept development and, when negative, to adolescent depression. Yet, whether adolescents with depression show aberrant emotional and neural reactivity to parental criticism and praise is understudied. METHODS: Adolescents with depression (n = 20) and healthy controls (n = 59) received feedback supposedly provided by their mother or father in the form of negative ('untrustworthy'), neutral ('chaotic'), and positive ('respectful') personality evaluations while in an MRI-scanner. After each feedback word, adolescents reported their mood. Beforehand, adolescents had rated whether these personality evaluations matched their self-views. RESULTS: In both groups, mood decreased after criticism and increased after praise. Adolescents with depression reported blunted mood responses after praise, whereas there were no mood differences after criticism. Neuroimaging analyses revealed that adolescents with depression (v. healthy controls) exhibited increased activity in response to criticism in the subgenual anterior cingulate cortex, temporal pole, hippocampus, and parahippocampal gyrus. Praise consistent with adolescents' self-views improved mood independent of depression status, while criticism matching self-views resulted in smaller mood increases in adolescents with depression (v. healthy controls). Exploratory analyses indicated that adolescents with depression recalled criticism (v. praise) more. CONCLUSIONS: Adolescents with depression might be especially attentive to parental criticism, as indexed by increased sgACC and hippocampus activity, and memorize this criticism more. Together with lower positive impact of praise, these findings suggest that cognitive biases in adolescent depression may affect how parental feedback is processed, and may be fed into their self-views.

Looking into troubled waters: Childhood emotional maltreatment modulates neural responses to prolonged gazing into one's own, but not others', eyes.

One of the most prevalent nonverbal, social phenomena known to automatically elicit self- and other-referential processes is eye contact. By its negative effects on the perception of social safety and views about the self and others, childhood emotional maltreatment (CEM) may fundamentally affect these processes. To investigate whether the socioaffective consequences of CEM may become visible in response to (prolonged) eye gaze, 79 adult participants (mean [M]age = 49.87, standard deviation [SD]age = 4.62) viewed videos with direct and averted gaze of an unfamiliar other and themselves while we recorded self-reported mood, eye movements using eye-tracking, and markers of neural activity using fMRI. Participants who reported higher levels of CEM exhibited increased activity in ventromedial prefrontal cortex to one's own, but not to others', direct gaze. Furthermore, in contrast to those who reported fewer of such experiences, they did not report a better mood in response to a direct gaze of self and others, despite equivalent amounts of time spent looking into their own and other peoples' eyes. The fact that CEM is associated with enhanced neural activation in a brain area that is crucially involved in self-referential processing (i.e., vmPFC) in response to one's own direct gaze is in line with the chronic negative impact of CEM on a person's self-views. Interventions that directly focus on targeting maladaptive self-views elicited during eye gaze to self may be clinically useful.

Aberrant neural network activation during reliving of autobiographical memories in adolescent depression.

BACKGROUND: Adolescents with depression exhibit negative biases in autobiographical memory with detrimental consequences for their self-concept and well-being. Investigating how adolescents relive positive autobiographical memories and activate the underlying neural networks could reveal mechanisms that drive such biases. This study investigated neural networks when reliving positive and neutral memories, and how neural activity is modulated by valence and vividness in adolescents with and without depression. METHODS: Adolescents (N = 69; n = 17 with depression) retrieved positive and neutral autobiographical memories. On a separate day, they relived these memories during fMRI scanning, and reported on pleasantness and vividness after reliving each memory. We used a multivariate, data-driven approach - event-related independent component analysis (eICA) - to characterize neural networks supporting autobiographical recollection. RESULTS: Adolescents with depression reported their positive memories as significantly less pleasant compared to healthy controls, while subjective vividness was unaffected. Using eICA, we identified a broad autobiographical memory network, and subnetworks related to reliving positive vs neutral memories. These subnetworks comprised a 'self-referential processing network' including medial prefrontal cortex, posterior cingulate cortex/precuneus, and temporoparietal junction, anti-correlating with parts of the central executive network and salience network. Adolescents with depression exhibited aberrant activation in this self-referential network, but only when reliving relatively 'low' pleasant memories. CONCLUSIONS: Our findings provide first insights into how the quality of reliving autobiographical memories in adolescents with depression may relate to aberrant self-referential neural network activation, and underscore the potential of targeting memory reliving in therapeutic interventions to foster self-esteem and diminish depressive symptoms.

Low self-esteem and the formation of global self-performance estimates in emerging adulthood.

High self-esteem, an overall positive evaluation of self-worth, is a cornerstone of mental health. Previously we showed that people with low self-esteem differentially construct beliefs about momentary self-worth derived from social feedback. However, it remains unknown whether these anomalies extend to constructing beliefs about self-performance in a non-social context, in the absence of external feedback. Here, we examined this question using a novel behavioral paradigm probing subjects' self-performance estimates with or without external feedback. We analyzed data from young adults (N = 57) who were selected from a larger community sample (N = 2402) on the basis of occupying the bottom or top 10% of a reported self-esteem distribution. Participants performed a series of short blocks involving two perceptual decision-making tasks with varying degrees of difficulty, with or without feedback. At the end of each block, they had to decide on which task they thought they performed best, and gave subjective task ratings, providing two measures of self-performance estimates. We found no robust evidence of differences in objective performance between high and low self-esteem participants. Nevertheless, low self-esteem participants consistently underestimated their performance as expressed in lower subjective task ratings relative to high self-esteem participants. These results provide an initial window onto how cognitive processes underpinning the construction of self-performance estimates across different contexts map on to global dispositions relevant to mental health such as self-esteem.

Neural and Affective Responses to Prolonged Eye Contact with One's Own Adolescent Child and Unfamiliar Others.

Eye contact is crucial for the formation and maintenance of social relationships, and plays a key role in facilitating a strong parent-child bond. However, the precise neural and affective mechanisms through which eye contact impacts on parent-child relationships remain elusive. We introduce a task to assess parents' neural and affective responses to prolonged direct and averted gaze coming from their own child, and an unfamiliar child and adult. While in the scanner, 79 parents (n = 44 mothers and n = 35 fathers) were presented with prolonged (16-38 s) videos of their own child, an unfamiliar child, an unfamiliar adult, and themselves (i.e., targets), facing the camera with a direct or an averted gaze. We measured BOLD-responses, tracked parents' eye movements during the videos, and asked them to report on their mood and feelings of connectedness with the targets after each video. Parents reported improved mood and increased feelings of connectedness after prolonged exposure to direct versus averted gaze and these effects were amplified for unfamiliar targets compared to their own child, due to high affect and connectedness ratings after videos of their own child. Neuroimaging results showed that the sight of one's own child was associated with increased activity in middle occipital gyrus, fusiform gyrus and inferior frontal gyrus relative to seeing an unfamiliar child or adult. While we found no robust evidence of specific neural correlates of eye contact (i.e., contrast direct > averted gaze), an exploratory parametric analysis showed that dorsomedial prefrontal cortex (dmPFC) activity increased linearly with duration of eye contact (collapsed across all "other" targets). Eye contact-related dmPFC activity correlated positively with increases in feelings of connectedness, suggesting that this region may drive feelings of connectedness during prolonged eye contact with others. These results underline the importance of prolonged eye contact for affiliative processes and provide first insights into its neural correlates. This may pave the way for new research in individuals or pairs in whom affiliative processes are disrupted.

Self-esteem depends on beliefs about the rate of change of social approval.

A major challenge in understanding the neurobiological basis of psychiatric disorders is rigorously quantifying subjective metrics that lie at the core of mental illness, such as low self-esteem. Self-esteem can be conceptualized as a 'gauge of social approval' that increases in response to approval and decreases in response to disapproval. Computational studies have shown that learning signals that represent the difference between received and expected social approval drive changes in self-esteem. However, it is unclear whether self-esteem based on social approval should be understood as a value updated through associative learning, or as a belief about approval, updated by new evidence depending on how strongly it is held. Our results show that belief-based models explain self-esteem dynamics in response to social evaluation better than associative learning models. Importantly, they suggest that in the short term, self-esteem signals the direction and rate of change of one's beliefs about approval within a group, rather than one's social position.

Adolescents' affective and neural responses to parental praise and criticism.

Social feedback from parents has a profound impact on the development of a child's self-concept. Yet, little is known about adolescents' affective and neural responses to parental social feedback, such as criticism or praise. Adolescents (n = 63) received standardized social feedback supposedly provided by their mother or father in the form of appraisals about their personality (e.g., 'respectful', 'lazy') during fMRI scanning. After each feedback word, adolescents reported their mood. Additionally, adolescents had rated whether feedback words matched their self-views on an earlier occasion. In line with preregistered hypotheses, negative parental feedback worsened adolescents' mood, which was exacerbated when feedback did not match adolescents' self-views. Negative feedback was associated with increased activity in the neural 'saliency network', including anterior insula, anterior cingulate cortex and dorsomedial prefrontal cortex. Positive feedback improved mood and increased activity in brain regions supporting social cognition, including temporoparietal junction, posterior superior temporal sulcus, and precuneus. A more positive general self-view and perceived parental warmth were associated with elevated mood, independent of feedback valence, but did not impact neural responses. Taken together, these results enhance our understanding of adolescents' neural circuitry involved in the processing of parental praise and criticism, and the impact of parental feedback on well-being.

Neural signatures of parental empathic responses to imagined suffering of their adolescent child.

Empathy is deemed indispensable for sensitive caregiving. Neuroimaging studies have identified canonical empathy networks consisting of regions supporting cognitive and affective aspects of empathy. However, not much is known about how these regions support empathy towards one's own offspring and how this neural activity relates to parental caregiving. We introduce a novel task to assess affective and neural responses to the suffering of one's own adolescent child. While in the scanner, 60 parents (n = 35 mothers, n = 25 fathers) were confronted with unpleasant situations involving their own child, an unfamiliar child, and themselves. Parents were asked to vividly imagine these situations and indicate their levels of distress. Parents reported higher levels of distress when imagining suffering for their own child relative to an unfamiliar child or themselves. Neuroimaging results showed increased activation within the cognitive empathy network (i.e., temporoparietal junction, dorsomedial- and ventromedial prefrontal cortex) when contrasting suffering of one's own child versus an unfamiliar child or the self. The task also engaged regions of the affective empathy network (i.e., anterior insula and anterior mid-cingulate cortex), which was however not modulated by whether suffering was for the self, one's own child, or an unfamiliar child. Parental care did not co-vary with activity in the empathy networks, but parents who were perceived as less caring exhibited increased activity in anterior prefrontal regions when imagining their own child suffering. These results provide new insights into neural processes supporting parental empathy, highlighting the importance of regions in the cognitive empathy network when confronted with the suffering of their own adolescent child, and suggest that additional (i.e., emotion regulation) networks may be relevant for parental caring behavior in daily life.

Vicarious praise and pain: parental neural responses to social feedback about their adolescent child.

Social feedback, such as praise or critique, profoundly impacts our mood and social interactions. It is unknown, however, how parents experience praise and critique about their child and whether their mood and neural responses to such 'vicarious' social feedback are modulated by parents' perceptions of their child. Parents (n = 60) received positive, intermediate and negative feedback words (i.e. personality characteristics) about their adolescent child during a magnetic resonance imaging scan. After each word, parents indicated their mood. After positive feedback their mood improved and activity in ventromedial prefrontal cortex and posterior cingulate cortex/precuneus increased. Negative feedback worsened parents' mood, especially when perceived as inapplicable to their child, and increased activity in anterior cingulate cortex, anterior insula, dorsomedial prefrontal cortex and precuneus. Parents who generally viewed their child more positively showed amplified mood responses to both positive and negative feedback and increased activity in dorsal striatum, inferior frontal gyrus and insula in response to negative feedback. These findings suggest that vicarious feedback has similar effects and engages similar brain regions as observed during feedback about the self and illustrates this is dependent on parents' beliefs of their child's qualities and flaws. Potential implications for parent-child dynamics and children's own self-views are discussed.

Multi-Round Trust Game Quantifies Inter-Individual Differences in Social Exchange from Adolescence to Adulthood.

Investing in strangers in a socio-economic exchange is risky, as we may be uncertain whether they will reciprocate. Nevertheless, the potential rewards for cooperating can be great. Here, we used a cross sectional sample (n = 784) to study how the challenges of cooperation versus defection are negotiated across an important period of the lifespan: from adolescence to young adulthood (ages 14 to 25). We quantified social behaviour using a multi round investor-trustee task, phenotyping individuals using a validated model whose parameters characterise patterns of real exchange and constitute latent social characteristics. We found highly significant differences in investment behaviour according to age, sex, socio-economic status and IQ. Consistent with the literature, we showed an overall trend towards higher trust from adolescence to young adulthood but, in a novel finding, we characterized key cognitive mechanisms explaining this, especially regarding socio-economic risk aversion. Males showed lower risk-aversion, associated with greater investments. We also found that inequality aversion was higher in females and, in a novel relation, that socio-economic deprivation was associated with more risk averse play.

Neurocomputational mechanisms underpinning aberrant social learning in young adults with low self-esteem.

Low self-esteem is a risk factor for a range of psychiatric disorders. From a cognitive perspective a negative self-image can be maintained through aberrant learning about self-worth derived from social feedback. We previously showed that neural teaching signals that represent the difference between expected and actual social feedback (i.e., social prediction errors) drive fluctuations in self-worth. Here, we used model-based functional magnetic resonance imaging (fMRI) to characterize learning from social prediction errors in 61 participants drawn from a population-based sample (n = 2402) who were recruited on the basis of being in the bottom or top 10% of self-esteem scores. Participants performed a social evaluation task during fMRI scanning, which entailed predicting whether other people liked them as well as the repeated provision of reported feelings of self-worth. Computational modeling results showed that low self-esteem participants had persistent expectations that others would dislike them, and a reduced propensity to update these expectations in response to social prediction errors. Low self-esteem subjects also displayed an enhanced volatility in reported feelings of self-worth, and this was linked to an increased tendency for social prediction errors to determine momentary self-worth. Canonical correlation analysis revealed that individual differences in self-esteem related to several interconnected psychiatric symptoms organized around a single dimension of interpersonal vulnerability. Such interpersonal vulnerability was associated with an attenuated social value signal in ventromedial prefrontal cortex when making predictions about being liked, and enhanced dorsal prefrontal cortex activity upon receipt of social feedback. We suggest these computational signatures of low self-esteem and their associated neural underpinnings might represent vulnerability for development of psychiatric disorder.

Turning a Blind Eye? Punishment of Friends and Unfamiliar Peers After Observed Exclusion in Adolescence.

In order to decrease the occurrence of social exclusion in adolescence, we need to better understand how adolescents perceive and behave toward peers involved in exclusion. We examined the role of friendships in treatment of perpetrators and victims of social exclusion. Eighty-nine participants (aged 9-16) observed exclusion of an unfamiliar peer (victim) by their best friend and another unfamiliar peer. Subsequently, participants could give up valuable coins to altruistically punish or help peers. Results showed that participants altruistically compensated victims and punished unfamiliar excluders, but refrained from punishing their friends. Our findings show that friendship with excluders modulates altruistic punishment of peers and provide mechanistic insight into how friendships may influence treatment of peers involved in social exclusion during adolescence.

Annual Research Review: Developmental computational psychiatry.

Most psychiatric disorders emerge during childhood and adolescence. This is also a period that coincides with the brain undergoing substantial growth and reorganisation. However, it remains unclear how a heightened vulnerability to psychiatric disorder relates to this brain maturation. Here, we propose 'developmental computational psychiatry' as a framework for linking brain maturation to cognitive development. We argue that through modelling some of the brain's fundamental cognitive computations, and relating them to brain development, we can bridge the gap between brain and cognitive development. This in turn can lead to a richer understanding of the ontogeny of psychiatric disorders. We illustrate this perspective with examples from reinforcement learning and dopamine function. Specifically, we show how computational modelling deepens an understanding of how cognitive processes, such as reward learning, effort learning, and social learning might go awry in psychiatric disorders. Finally, we sketch the promises and limitations of a developmental computational psychiatry.

Friend versus foe: Neural correlates of prosocial decisions for liked and disliked peers.

Although the majority of our social interactions are with people we know, few studies have investigated the neural correlates of sharing valuable resources with familiar others. Using an ecologically valid research paradigm, this functional magnetic resonance imaging study examined the neural correlates of prosocial and selfish behavior in interactions with real-life friends and disliked peers in young adults. Participants (N = 27) distributed coins between themselves and another person, where they could make selfish choices that maximized their own gains or prosocial choices that maximized outcomes of the other. Participants were more prosocial toward friends and more selfish toward disliked peers. Individual prosociality levels toward friends were associated negatively with supplementary motor area and anterior insula activity. Further preliminary analyses showed that prosocial decisions involving friends were associated with heightened activity in the bilateral posterior temporoparietal junction, and selfish decisions involving disliked peers were associated with heightened superior temporal sulcus activity, which are brain regions consistently shown to be involved in mentalizing and perspective taking in prior studies. Further, activation of the putamen was observed during prosocial choices involving friends and selfish choices involving disliked peers. These findings provide insights into the modulation of neural processes that underlie prosocial behavior as a function of a positive or negative relationship with the interaction partner.

Longitudinal links between childhood peer acceptance and the neural correlates of sharing.

Childhood peer acceptance is associated with high levels of prosocial behavior and advanced perspective taking skills. Yet, the neurobiological mechanisms underlying these associations have not been studied. This functional magnetic resonance imaging study examined the neural correlates of sharing decisions in a group of adolescents who had a stable accepted status (n = 27) and a group who had a chronic rejected status (n = 19) across six elementary school grades. Both groups of adolescents played three allocation games in which they could share money with strangers with varying costs and profits to them and the other person. Stably accepted adolescents were more likely to share their money with unknown others than chronically rejected adolescents when sharing was not costly. Neuroimaging analyses showed that stably accepted adolescents, compared to chronically rejected adolescents, exhibited higher levels of activation in the temporo-parietal junction, posterior superior temporal sulcus, temporal pole, pre-supplementary motor area, and anterior insula during costly sharing decisions. These findings demonstrate that stable peer acceptance across childhood is associated with heightened activity in brain regions previously linked to perspective taking and the detection of social norm violations during adolescence, and thereby provide insight into processes underlying the widely established links between peer acceptance and prosocial behavior.

Neural and computational processes underlying dynamic changes in self-esteem.

Self-esteem is shaped by the appraisals we receive from others. Here, we characterize neural and computational mechanisms underlying this form of social influence. We introduce a computational model that captures fluctuations in self-esteem engendered by prediction errors that quantify the difference between expected and received social feedback. Using functional MRI, we show these social prediction errors correlate with activity in ventral striatum/subgenual anterior cingulate cortex, while updates in self-esteem resulting from these errors co-varied with activity in ventromedial prefrontal cortex (vmPFC). We linked computational parameters to psychiatric symptoms using canonical correlation analysis to identify an 'interpersonal vulnerability' dimension. Vulnerability modulated the expression of prediction error responses in anterior insula and insula-vmPFC connectivity during self-esteem updates. Our findings indicate that updating of self-evaluative beliefs relies on learning mechanisms akin to those used in learning about others. Enhanced insula-vmPFC connectivity during updating of those beliefs may represent a marker for psychiatric vulnerability.

Neural correlates of retaliatory and prosocial reactions to social exclusion: Associations with chronic peer rejection.

Social exclusion is a distressing experience and can lead to both retaliatory and prosocial reactions toward the sources of exclusion. The way people react to social exclusion has been hypothesized to be shaped through chronic exposure to peer rejection. This functional Magnetic Resonance Imaging study examined associations between chronic peer rejection and retaliatory (i.e. punishing) and prosocial (i.e. forgiving) reactions to social exclusion and the neural processes underlying them. Chronically rejected (n=19) and stably highly accepted adolescents (n=27) distributed money between themselves and unknown others who previously included or excluded them in a virtual ball-tossing game (Cyberball). Decreasing the excluders' monetary profits (i.e., punishment) was associated with increased activity in the ventral striatum, dorsolateral prefrontal cortex (PFC) and parietal cortex in both groups. Compared to stably highly accepted adolescents, chronically rejected adolescents exhibited higher activity in the dorsal striatum and lateral prefrontal cortex - brain regions implicated in cognitive control - when they refrained from punishment and shared their money equally with (i.e. forgave) the excluders. These results provide insights into processes that might underlie the maintenance of peer rejection across development, such as difficulties controlling the urge to retaliate after exclusion.

Effects of Testosterone Administration on Strategic Gambling in Poker Play.

Testosterone has been associated with economically egoistic and materialistic behaviors, but -defensibly driven by reputable status seeking- also with economically fair, generous and cooperative behaviors. Problematically, social status and economic resources are inextricably intertwined in humans, thus testosterone's primal motives are concealed. We critically addressed this issue by performing a placebo-controlled single-dose testosterone administration in young women, who played a game of bluff poker wherein concerns for status and resources collide. The profit-maximizing strategy in this game is to mislead the other players by bluffing randomly (independent of strength of the hand), thus also when holding very poor cards (cold bluffing). The profit-maximizing strategy also dictates the players in this poker game to never call the other players' bluffs. For reputable-status seeking these materialistic strategies are disadvantageous; firstly, being caught cold bluffing damages one's reputation by revealing deceptive intent, and secondly, not calling the other players' bluffs signals submission in blindly tolerating deception. Here we show that testosterone administration in this game of bluff poker significantly reduces random bluffing, as well as cold bluffing, while significantly increasing calling. Our data suggest that testosterone in humans primarily motivates for reputable-status seeking, even when this elicits behaviors that are economically disadvantageous.