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Humans are strongly dependent upon social resources for allostasis and emotion regulation. This applies especially to early childhood because humans-as an altricial species-have a prolonged period of dependency on support and input from caregivers who typically act as sources of co-regulation. Accordingly, attachment theory proposes that the history and quality of early interactions with primary caregivers shape children's internal working models of attachment. In turn, these attachment models guide behavior, initially with the set goal of maintaining proximity to caregivers but eventually paving the way to more generalized mental representations of self and others. Mounting evidence in non-clinical populations suggests that these mental representations coincide with differential patterns of neural structure, function, and connectivity in a range of brain regions previously associated with emotional and cognitive capacities. What is currently lacking, however, is an evidence-based account of how early adverse attachment-related experiences and/or the emergence of attachment disorganization impact the developing brain. While work on early childhood adversities offers important insights, we propose that how these events become biologically embedded crucially hinges on the context of the child-caregiver attachment relationships in which the events take place. Our selective review distinguishes between direct social neuroscience research on disorganized attachment and indirect maltreatment-related research, converging on aberrant functioning in neurobiological systems subserving aversion, approach, emotion regulation, and mental state processing in the wake of severe attachment disruption. To account for heterogeneity of findings, we propose two distinct neurobiological phenotypes characterized by hyper- and hypo-arousal primarily deriving from the caregiver serving either as a threatening or as an insufficient source of co-regulation, respectively.

It is a central tenet of attachment theory that individual differences in attachment representations organize behavior during social interactions. Secure attachment representations also facilitate behavioral synchrony, a key component of adaptive parent–child interactions. Yet, the dynamic neural processes underlying these interactions and the potential role of attachment representations remain largely unknown. A growing body of research indicates that interpersonal neural synchrony (INS) could be a potential neurobiological correlate of high interaction and relationship quality. In this study, we examined whether interpersonal neural and behavioral synchrony during parent–child interaction is associated with parent and child attachment representations. In total, 140 parents (74 mothers and 66 fathers) and their children (age 5–6 years; 60 girls and 80 boys) engaged in cooperative versus individual problem‐solving. INS in frontal and temporal regions was assessed with functional near‐infrared spectroscopy hyperscanning. Attachment representations were ascertained by means of the Adult Attachment Interview in parents and a story‐completion task in children, alongside video‐coded behavioral synchrony. Findings revealed increased INS during cooperative versus individual problem solving across all dyads (훸2(2) = 9.37, p = 0.009). Remarkably, individual differences in attachment representations were associated with INS but not behavioral synchrony (p > 0.159) during cooperation. More specifically, insecure maternal attachment representations were related to higher mother–child INS in frontal regions (훸2(3) = 9.18, p = 0.027). Conversely, secure daughter attachment representations were related to higher daughter–parent INS within temporal regions (훸2(3) = 12.58, p = 0.006). Our data thus provide further indication for INS as a promising correlate to probe the neurobiological underpinnings of attachment representations in the context of early parent–child interactions. Research Highlights: We assessed attachment representations using narrative measures and interpersonal neural synchrony (INS) during parent‐child problem‐solving.Dyads including mothers with insecure attachment representations showed higher INS in left prefrontal regions.Dyads including daughters with secure attachment representations showed higher INS in right temporo‐parietal regions.INS is a promising correlate to probe the neurobiological underpinnings of attachment representations in the context of parent‐child interactions, especially within the mutual prediction framework. [ABSTRACT FROM AUTHOR]

Attachment theory suggests that interindividual differences in attachment security versus insecurity (anxiety and avoidance) contribute to the ways in which people perceive social emotional signals, particularly from the human face. Among different facial features, eye gaze conveys crucial information for social interaction, with a straight gaze triggering different cognitive and emotional processes as compared to an averted gaze. It remains unknown, however, how interindividual differences in attachment associate with early face encoding in the context of a straight versus averted gaze. Using electroencephalography (EEG) and recording event-related potentials (ERPs), specifically the N170 component, the present study (N = 50 healthy adults) measured how the characteristics of attachment anxiety and avoidance relate to the encoding of faces with respect to gaze direction and head orientation. Our findings reveal a significant relationship between gaze direction (irrespective of head orientation) and attachment anxiety on the interhemispheric (i.e. right) asymmetry of the N170 and thus provide evidence for an association between attachment anxiety and eye gaze processing during early visual face encoding. [ABSTRACT FROM AUTHOR]

The existing literature suggests that individual differences in attachment may be associated with differential trajectories of structural brain development. In addition to maturation during infancy and childhood, developmental trajectories are characteristic of adolescence, a period marked by increasingly complex interpersonal relationships and significant neurostructural and functional plasticity. It remains to be examined whether attachment prospectively relates to neurostructural developmental trajectories during adolescence. In this longitudinal study, we investigated whether self-reported attachment dimensions of anxiety (AX) and avoidance (AV) could predict elements of cortical thickness (CT) and subcortical volume (SV) trajectories in 95 typically developing adolescents (12–19 years old at study baseline). Self-reported scores of AX and AV were obtained at study baseline, and neurostructural development was assessed at baseline and three timepoints over the four following years. Self-reported AX and AV were associated with steeper CT decreases in prefrontal cortical and cortical midline structures as well as anterior temporal cortex, particularly in participants younger at study baseline. Regarding SV, preliminary differential associations were observed between developmental trajectories and attachment dimensions. Our study suggests that interindividual differences in attachment contribute to shaping neurodevelopmental trajectories for several cortical and subcortical structures during adolescence and young adulthood. [ABSTRACT FROM AUTHOR]

Child maltreatment gives rise to atypical patterns of social functioning with peers which might be particularly pronounced in early adolescence when peer influence typically peaks. Yet, few neuroimaging studies in adolescents use peer interaction paradigms to parse neural correlates of distinct maltreatment exposures. This fMRI study examines effects of abuse, neglect, and emotional maltreatment (EM) among 98 youth (n = 58 maltreated; n = 40 matched controls) using an event-related Cyberball paradigm affording assessment of both social exclusion and inclusion across early and mid-adolescence (≤13.5 years, n = 50; >13.5 years, n = 48). Younger adolescents showed increased activation to social exclusion versus inclusion in regions implicated in mentalizing (e.g., superior temporal gyrus). Individual exposure-specific analyses suggested that neglect and EM coincided with less reduction of activation to social exclusion relative to inclusion in the dorsal anterior cingulate cortex/pre-supplementary motor area (dACC/pre-SMA) among younger versus older adolescents. Integrative follow-up analyses showed that EM accounted for this dACC/pre-SMA activation pattern over and above other exposures. Moreover, age-independent results within respective exposure groups revealed that greater magnitude of neglect predicted blunted exclusion-related activity in the parahippocampal gyrus, while EM predicted increased activation to social exclusion in the precuneus/posterior cingulate cortex. [ABSTRACT FROM AUTHOR]

Attachment theory proposes that children's representations of interactions with caregivers guide information‐processing about others, bridging interpersonal domains. In a longitudinal study (N = 165), preschoolers (Mage = 5.19 years) completed the MacArthur Story Stem Battery to assess parent representations. At school‐age (Mage = 8.42 years), children played a virtual ballgame with peers who eventually excluded them to track event‐related cardiac slowing, a physiological correlate of rejection, especially when unexpected. At both ages, parents and teachers reported on peer and emotional problems. During exclusion versus inclusion‐related events, cardiac slowing was associated with greater positive parent representations and fewer emerging peer problems. Cardiac slowing served as a mediator between positive parent representations and peer problems, supporting a potential psychophysiological mechanism underlying the generalization of attachment‐related representations to peer relationships. [ABSTRACT FROM AUTHOR]

Interpersonal neural synchrony (INS) has been previously evidenced in mother–child interactions, yet findings concerning father–child interaction are wanting. The current experiment examined whether fathers and their 5‐ to 6‐year‐old children (N = 66) synchronize their brain activity during a naturalistic interaction, and addressed paternal and child factors related to INS. Compared to individual problem solving and rest, father–child dyads showed increased INS in bilateral dorsolateral prefrontal cortex and left temporo‐parietal junction during cooperative problem solving. Furthermore, the father's attitude toward his role as a parent was positively related to INS during the cooperation condition. These results highlight the implication of the father's attitude to parenting in INS processes for the first time. [ABSTRACT FROM AUTHOR]

Conversations are an essential form of communication in daily family life. Specific patterns of caregiver–child conversations have been linked to children's socio-cognitive development and child-relationship quality beyond the immediate family environment. Recently, interpersonal neural synchronization has been proposed as a neural mechanism supporting conversation. Here, we present a functional near-infrared spectroscopy (fNIRS) hyperscanning study looking at the temporal dynamics of neural synchrony during mother–child conversation. Preschoolers (20 boys and 20 girls, M age 5;07 years) and their mothers (M age 36.37 years) were tested simultaneously with fNIRS hyperscanning while engaging in a free verbal conversation lasting for 4 min. Neural synchrony (using wavelet transform coherence analysis) was assessed over time. Furthermore, each conversational turn was coded for conversation patterns comprising turn-taking, relevance, contingency and intrusiveness. Results from linear mixed-effects modeling revealed that turn-taking, but not relevance, contingency or intrusiveness predicted neural synchronization during the conversation over time. Results are discussed to point out possible variables affecting parent–child conversation quality and the potential functional role of interpersonal neural synchronization for parent–child conversation. [ABSTRACT FROM AUTHOR]

Humans are strongly dependent upon social resources for allostasis and emotion regulation. This applies especially to early childhood because humans—as an altricial species—have a prolonged period of dependency on support and input from caregivers who typically act as sources of co-regulation. Accordingly, attachment theory proposes that the history and quality of early interactions with primary caregivers shape children's internal working models of attachment. In turn, these attachment models guide behavior, initially with the set goal of maintaining proximity to caregivers but eventually paving the way to more generalized mental representations of self and others. Mounting evidence in non-clinical populations suggests that these mental representations coincide with differential patterns of neural structure, function, and connectivity in a range of brain regions previously associated with emotional and cognitive capacities. What is currently lacking, however, is an evidence-based account of how early adverse attachment-related experiences and/or the emergence of attachment disorganization impact the developing brain. While work on early childhood adversities offers important insights, we propose that how these events become biologically embedded crucially hinges on the context of the child–caregiver attachment relationships in which the events take place. Our selective review distinguishes between direct social neuroscience research on disorganized attachment and indirect maltreatment-related research, converging on aberrant functioning in neurobiological systems subserving aversion, approach, emotion regulation, and mental state processing in the wake of severe attachment disruption. To account for heterogeneity of findings, we propose two distinct neurobiological phenotypes characterized by hyper- and hypo-arousal primarily deriving from the caregiver serving either as a threatening or as an insufficient source of co-regulation, respectively. [ABSTRACT FROM AUTHOR]

Attachment in the context of intimate pair bonds is most frequently studied in terms of the universal strategy to draw near, or away, from significant others at moments of personal distress. However, important interindividual differences in the quality of attachment exist, usually captured through secure versus insecure - anxious and/or avoidant - attachment orientations. Since Bowlby’s pioneering writings on the theory of attachment, it has been assumed that attachment orientations are influenced by both genetic and social factors - what we would today describe and measure as gene by environment interaction mediated by epigenetic DNA modification - but research in humans on this topic remains extremely limited. We for the first time examined relations between intra-individual differences in attachment and epigenetic modification of the oxytocin receptor (OXTR) and glucocorticoid receptor (NR3C1) gene promoter in 109 young adult human participants. Our results revealed that attachment avoidance was significantly and specifically associated with increased OXTR and NR3C1 promoter methylation. These findings offer first tentative clues on the possible etiology of attachment avoidance in humans by showing epigenetic modification in genes related to both social stress regulation and HPA axis functioning. [ABSTRACT FROM AUTHOR]

Objective The establishment of an accurate understanding of one's social context is a central developmental task during adolescence. A critical component of such development is to learn how to integrate the objective evaluation of one's behavior with the social response to the latter-here referred to as social feedback processing. Case report We measured brain activity by means of fMRI in 33 healthy adolescents (12-19 years old, 14 females). Participants played a difficult perceptual game with integrated verbal and visual feedback. Verbal feedback provided the participants with objective performance evaluation (won vs. lost). Visual feedback consisted of either smiling or angry faces, representing positive or negative social evaluations. Together, the combination of verbal and visual feedback gave rise to congruent versus incongruent social feedback combinations. In addition to assessing sex differences, we further tested for the effects of age and attachment style on social feedback processing. Results revealed that brain activity during social feedback processing was significantly modulated by sex, age, and attachment style in prefrontal cortical areas, ventral anterior cingulate cortex, anterior insula, caudate, and amygdala/hippocampus. We found indication for heightened activity during incongruent social feedback processing in females, older participants, and individuals with an anxious attachment style. Conversely, we observed stronger activity during processing of congruent social feedback in males and participants with an avoidant attachment style. Conclusion Our findings not only extend knowledge on the typical development of socio-emotional brain function during adolescence, but also provide first clues on how attachment insecurities, and particularly attachment avoidance, could interfere with the latter mechanisms. [ABSTRACT FROM AUTHOR]

In the past, the amygdala has generally been conceptualized as a fear-processing module. Recently, however, it has been proposed to respond to all stimuli that are relevant with respect to the current needs, goals, and values of an individual. This raises the question of whether the human amygdala may differentiate between separate kinds of relevance. A distinction between emotional (vs. neutral) and social (vs. non-social) relevance is supported by previous studies showing that the human amygdala preferentially responds to both emotionally and socially significant information, and these factors might even display interactive encoding properties. However, no investigation has yet probed a full 2 (positive vs. negative valence) × 2 (social vs. non-social content) processing pattern, with neutral images as an additional baseline. Applying such an extended orthogonal factorial design, our fMRI study demonstrates that the human amygdala is (1) more strongly activated for neutral social vs. non-social information, (2) activated at a similar level when viewing social positive or negative images, but (3) displays a valence effect (negative vs. positive) for non-social images. In addition, this encoding pattern is not influenced by cognitive or behavioral emotion regulation mechanisms, and displays a hemispheric lateralization with more pronounced effects on the right side. Finally, the same valence × social content interaction was found in three additional cortical regions, namely the right fusiform gyrus, right anterior superior temporal gyrus, and medial orbitofrontal cortex. Overall, these findings suggest that valence and social content processing represent distinct kinds of relevance that interact within the human amygdala as well as in a more extensive cortical network, likely subserving a key role in relevance detection. [ABSTRACT FROM AUTHOR]

Adult attachment style (AAS) refers to individual differences in the way people experience and regulate their social relationships and corresponding emotions. Based on developmental and psychological research, it has been hypothesized that avoidant attachment style (AV) entails deactivating strategies in social contexts, whereas anxious attachment style (AX) involves hyper vigilance and up-regulation mechanisms. However, the neural substrates of differences in social emotion regulation associated with AAS have not been systematically investigated. Here we used fMRI in 19 healthy adults to investigate the effect of AAS on the processing of pleasant or unpleasant social and nonsocial scenes. Participants were asked either to naturally attend (NAT), cognitively reappraise (REAP), or behaviorally suppress (ESUP) their emotional responses. Avoidantly attached participants showed increased prefrontal and anterior cingulate activation to social negative scenes when making spontaneous emotion judgments. They also exhibited persistent increases in dorsolateral prefrontal cortex and left amygdala activity for the same stimuli during reappraisal, as well as additional activation in supplementary motor area and ventral caudate during the suppression of social positive emotions. These results suggest that AV may imply less efficient reappraisal strategies to regulate social negative emotions, and lead to higher conflict or effortful control when suppression cannot be employed. In contrast, anxiously attached participants showed differential increases in the right amygdala and left parahippocampal cortex for social negative and positive stimuli, respectively, but only when making spontaneous emotion judgments. No effect of AX was found during down-regulation conditions. This suggests heightened arousal to negative information without difficulty in down-regulating emotions through cognitive re-evaluation or suppression. Taken together, these findings reveal for the first time the neural underpinnings of attachment-related differences in social emotion regulation. [ABSTRACT FROM AUTHOR]

Since its first description four decades ago, attachment theory (AT) has become one of the principal developmental psychological frameworks for describing the role of individual differences in the establishment and maintenance of social bonds between people. Yet, still little is known about the neurobiological underpinnings of attachment orientations and their well-established impact on a range of social and affective behaviors. In the present review, we summarize data from recent studies using cognitive and imaging approaches to characterize attachment styles and their effect on emotion and social cognition. We propose a functional neuroanatomical framework to integrate the key brain mechanisms involved in the perception and regulation of social emotional information, and their modulation by individual differences in terms of secure versus insecure (more specifically avoidant, anxious, or resolved versus unresolved) attachment traits. This framework describes how each individual's attachment style (built through interactions between personal relationship history and predispositions) may influence the encoding of approach versus aversion tendencies (safety versus threat) in social encounters, implicating the activation of a network of subcortical (amygdala, hippocampus, striatum) and cortical (insula, cingulate) limbic areas. These basic and automatic affective evaluation mechanisms are in turn modulated by more elaborate and voluntary cognitive control processes, subserving mental state attribution and emotion regulation capacities, implicating a distinct network in medial prefrontal cortex (mPFC), superior temporal sulcus (STS), and temporo-parietal junction (TPJ), among others. Recent neuroimaging data suggest that affective evaluation is decreased in avoidantly but increased in anxiously attached individuals. In turn, although data on cognitive control is still scarce, it points toward a possible enhancement of mental state representations associated with attachment insecurity and particularly anxiety. Emotion regulation strategies such as reappraisal or suppression of social emotions are also differentially modulated by attachment style. This research does not only help better understand the neural underpinnings of human social behavior, but also provides important insights on psychopathological conditions where attachment dysregulation is likely to play an important (causal) role. [ABSTRACT FROM AUTHOR]

Attachment theory describes how people emotionally bond with others, utilize their social interactions to regulate affective needs, and how they differ in their attachment style. However, it remains unknown whether anxious or avoidant attachment is linked to more general differences in emotional processing for negative and positive stimuli, and whether such differences depend on stimulus content. Here we tested how social or non-social positive or negative emotional scenes were rated for pleasantness, arousal, and control, as a function of individual attachment style, in a sample of 54 female participants. Our results show that avoidant attachment was associated with a selective reduction of pleasantness ratings for positive social images, whereas anxious attachment was associated with higher arousal and lower control ratings for negative social images, besides higher arousal ratings for all remaining stimulus categories. These findings reveal that adult attachment style is associated with differences in the perception of emotion-laden stimuli, even when unfamiliar and not directly attachment-related, and such differences may also affect positive scenes, particularly when they contain social information, rather than just socially negative or threatening information. In addition, our results support the notion that anxious attachment is not only associated with hyperactivating tendency during the appraisal of social threat, but may also involve an ambivalence influencing the judgments of both positive and negative information. [ABSTRACT FROM AUTHOR]

Every day we encounter new people, interact with them, and form person impressions based on quick and automatic inferences from minimal contextual information. Previous studies have identified an extensive network of brain areas involved in familiar face recognition, but there is little evidence to date concerning the neural bases of negative vs. positive person impressions. In the present study, participants were repeatedly exposed to 16 unfamiliar face identities within a pseudo-interactive game context to generate a perception of either “friends” or “foes”. Functional magnetic resonance imaging (fMRI) was then performed during an old/new memory task to assess any difference in brain responses to these now familiar face identities, relative to unfamiliar faces. Importantly, whereas facial expressions were always emotional (either smiling or angry) during the encoding phase, they were always neutral during the memory task. Our results reveal that several brain regions involved in familiar face recognition, including fusiform cortex, posterior cingulate gyrus, and amygdala, plus additional areas involved in motivational control such as caudate and anterior cingulate cortex, were differentially modulated as a function of a previous encounter, and generally more activated when faces were perceived as “foes” rather than “friends”. These findings underscore that a key dimension of social judgments, based on past impressions of who may be supportive or hostile, may lead to long-lasting effects on memory for faces and thus influence affective reactions to people during a subsequent encounter even in a different (neutral) context. [ABSTRACT FROM AUTHOR]

Adult attachment style refers to individual personality traits that strongly influence emotional bonds and reactions to social partners. Behavioral research has shown that adult attachment style reflects profound differences in sensitivity to social signals of support or conflict, but the neural substrates underlying such differences remain unsettled. Using functional magnetic resonance imaging (fMRI), we examined how the three classic prototypes of attachment style (secure, avoidant, anxious) modulate brain responses to facial expressions conveying either positive or negative feedback about task performance (either supportive or hostile) in a social game context. Activation of striatum and ventral tegmental area was enhanced to positive feedback signaled by a smiling face, but this was reduced in participants with avoidant attachment, indicating relative impassiveness to social reward. Conversely, a left amygdala response was evoked by angry faces associated with negative feedback, and correlated positively with anxious attachment, suggesting an increased sensitivity to social punishment. Secure attachment showed mirror effects in striatum and amygdala, but no other specific correlate. These results reveal a critical role for brain systems implicated in reward and threat processing in the biological underpinnings of adult attachment style, and provide new support to psychological models that have postulated two separate affective dimensions to explain these individual differences, centered on the ventral striatum and amygdala circuits, respectively. These findings also demonstrate that brain responses to face expressions are not driven by facial features alone but determined by the personal significance of expressions in current social context. By linking fundamental psychosocial dimensions of adult attachment with brain function, our results do not only corroborate their biological bases but also help understand their impact on behavior. [ABSTRACT FROM AUTHOR]

The use of functional near-infrared spectroscopy (fNIRS) hyperscanning during naturalistic interactions in parent–child dyads has substantially advanced our understanding of the neurobiological underpinnings of human social interaction. However, despite the rise of developmental hyperscanning studies over the last years, analysis procedures have not yet been standardized and are often individually developed by each research team. This article offers a guide on parent–child fNIRS hyperscanning data analysis in MATLAB and R. We provide an example dataset of 20 dyads assessed during a cooperative versus individual problem-solving task, with brain signal acquired using 16 channels located over bilateral frontal and temporo-parietal areas. We use MATLAB toolboxes Homer2 and SPM for fNIRS to preprocess the acquired brain signal data and suggest a standardized procedure. Next, we calculate interpersonal neural synchrony between dyads using Wavelet Transform Coherence (WTC) and illustrate how to run a random pair analysis to control for spurious correlations in the signal. We then use RStudio to estimate Generalized Linear Mixed Models (GLMM) to account for the bounded distribution of coherence values for interpersonal neural synchrony analyses. With this guide, we hope to offer advice for future parent–child fNIRS hyperscanning investigations and to enhance replicability within the field. [ABSTRACT FROM AUTHOR]