Visualizing the invisible tie: Linking parent-child neural synchrony to parents' and children's attachment representations.

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 (𝛸2(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 (𝛸2(3) = 9.18, p = 0.027). Conversely, secure daughter attachment representations were related to higher daughter-parent INS within temporal regions (𝛸2(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.

Attachment and inter-individual differences in empathy, compassion, and theory of mind abilities.

Social processing, namely the ability to understand others' cognitive and affective states, is crucial for successful social interaction. It encompasses socio-affective abilities such as empathy and compassion, as well as socio-cognitive abilities such as theory of mind (ToM). This study examined the link between social processing and attachment. Our study goes beyond previous research in that social processing abilities were assessed in a single, state-of-the-art behavioral paradigm using video narratives, the EmpaToM. Attachment was captured with the Adult Attachment Interview (N = 85; 50.60% women, Mage = 25.87 ± 4.50 years) measuring participants' present-day capacity to think about and communicate attachment-relevant information about the past. Additionally, a self-report attachment questionnaire was employed (N = 158). We found that AAI-based attachment security (vs. insecurity) was associated with higher behavioral ToM abilities. Furthermore, self-reported attachment avoidance was negatively correlated with behavioral compassion abilities. Our findings provide further evidence that interview-based and self-reported attachment measures do not converge, but may rather be understood as capturing different facets of attachment that relate to different components of social processing. We conclude that individuals with secure, non-avoidant attachment show social abilities that allow them to better understand others' thoughts and generate positive, caring emotions in face of others' distress.

Attachment is differentially associated with distinct behavioral social processing abilities, that is, compassion and theory of mind.Higher attachment security in the Adult Attachment Interview (AAI) is linked to higher behavioral theory of mind abilities.Increased self-reported attachment avoidance is linked to lower behavioral compassion.

Precursors and Effects of Self-reported Parental Reflective Functioning: Links to Parental Attachment Representations and Behavioral Sensitivity.

Parental reflective functioning is thought to provide a missing link between caregivers' own attachment histories and their ensuing parenting behaviors. The current study sought to extend research on this association involving 115 parents, both mothers and fathers, of 5-to-6-year-old preschoolers using the German version of the Parental Reflective Functioning Questionnaire (PRFQ). Our study was the first to combine Adult Attachment Interview classifications of parental attachment, behavioral observations of parental sensitivity and PRFQ ratings while drawing on a sizable father subsample. We found theoretically consistent significant relations between all measures, while our results particularly highlighted the role of dismissing attachment for decreases in parenting quality on both cognitive and behavioral levels as the dismissing status differentially affected specific components of self-reported parental reflective functioning and observed sensitivity. Interestingly, these patterns were largely comparable in mothers and fathers. Exploratory mediation analyses further suggested that decreased parental reflective functioning may partially mediate the relationship between parents' dismissing attachment and decreased parental sensitivity. Thus, for prevention and intervention programs targeting parental sensitivity and thus children's long term healthy mental development, the interplay between parental reflective functioning and parents' own attachment history emerges as a key mechanism. Finally, our study served as a further validation of the PRFQ given the caveat that the pre-mentalizing subscale may need further revision in the German version.

Association between attachment anxiety and the gaze direction-related N170.

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.

Charting the social neuroscience of human attachment (SoNeAt).

This introduction aims to set out the potential as well as some of the pitfalls of the newly emerging area of the Social Neuroscience of Human Attachment (SoNeAt). To organize and interconnect the burgeoning empirical studies in this line of research, including those in this special issue, we outline a programmatic framework including an extension of our conceptual proposals NAMA and NAMDA to guide future research. We hope that this special issue will act as a stimulus for redoubling our efforts advancing the newly emerging SoNeAt area bridging attachment theory and social neuroscience.

Longitudinal associations between self-reported attachment dimensions and neurostructural development from adolescence to early adulthood.

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.

Deactivating attachment strategies associate with early processing of facial emotion and familiarity in middle childhood: an ERP study.

Neurophysiological evidence suggests associations between attachment and the neural processing of emotion expressions. This study asks whether this relationship is also evident in middle childhood, and how it is affected by facial familiarity. Attachment strategies (deactivation, hyperactivation) were assessed in 51 children (9 - 11 years) using a story stem completion task. Event-related potentials (ERPs) were recorded during children's passive viewing of mother and stranger emotional faces (angry/happy). At the stage of facial information encoding (N250), attachment deactivation was associated with a pattern pointing to increased vigilance towards angry faces. Further, the attention-driven LPP was increased to happy mother faces as highly salient stimuli overall, but not in children scoring high on deactivation. These children did not discriminate between mothers' facial emotions and showed a general attentional withdrawal from facial stimuli. While our results on attachment deactivation support a two-stage processing model, no effect of hyperactivation was found.

Emotional maltreatment and neglect impact neural activation upon exclusion in early and mid-adolescence: An event-related fMRI study.

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.

Contemplative Mental Training Reduces Hair Glucocorticoid Levels in a Randomized Clinical Trial.

OBJECTIVE: This study aimed to investigate the effect of regular contemplative mental training on endocrine and psychological indices of long-term stress. METHODS: An open-label efficacy trial that comprised three distinct 3-month long modules targeting attention and interoception, socioaffective, or sociocognitive abilities through dyadic exercises and secularized meditation practices was conducted with healthy adults. Participants underwent the training for 3 or 9 months, or were assigned to a retest control cohort. Chronic stress indices were assayed at four time points: pretraining and after 3, 6, and 9 months. The main outcome measures were cortisol (HC) and cortisone (HE) concentration in hair and self-reported long-term stress. RESULTS: Of 362 initially randomized individuals, 30 dropped out before study initiation (n = 332; mean [SD] age = 40.7 [9.2] years; 197 women). Hair-based glucocorticoid assays were available from n = 227, and questionnaire data from n = 326. Results from three separate training cohorts (TC1-3) revealed consistent decreases in HC and HE levels over the first three (TC3) to 6 months (TC1 and TC2) of training, with no further reduction at the final 9-month mark (baseline to end of training differences, HC, TC1: t(355) = 2.59, p = .010, contrast estimate (est.) [SE] = 0.35 [0.14]; HC, TC2: t(363) = 4.06, p < .001, est. = 0.48 [0.12]; HC, TC3: t(368) = 3.18, p = .002, est. = 0.41 [0.13]; HE, TC1: t(435) = 3.23, p = .001, est. = 0.45 [0.14]; HE, TC2: t(442) = 2.60, p = .010, est. = 0.33 [0.13]; HE, TC3: t(446) = 4.18, p < .001, est. = 0.57 [0.14]). Training effects on HC increased with individual compliance (practice frequency), and effects on both HC and HE were independent of training content and unrelated to change in self-reported chronic stress. Self-reported stress, and cortisol-to-dehydroepiandrosterone ratios as an exploratory endpoint, were also reduced, albeit less consistently. CONCLUSIONS: Our results point to the reduction of long-term cortisol exposure as a mechanism through which meditation-based mental training may exert positive effects on practitioners' health.Trial Registration: ClinicalTrials.gov identifier: NCT01833104.

Interpersonal Neural Synchrony During Father-Child Problem Solving: An fNIRS Hyperscanning Study.

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.

Exclusion Expected? Cardiac Slowing Upon Peer Exclusion Links Preschool Parent Representations to School-Age Peer Relationships.

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.

A Guide to Parent-Child fNIRS Hyperscanning Data Processing and Analysis.

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.

Neural bases of social feedback processing and self-other distinction in late childhood: The role of attachment and age.

Attachment plays a key role in how children process information about the self and others. Here, we examined the neural bases of interindividual differences in attachment in late childhood and tested whether social cognition-related neural activity varies as function of age. In a small sample of 8-year-old to 12-year-old children (n = 21/19), we used functional magnetic resonance imaging to measure neural responses during social feedback processing and self-other distinction. Attachment was assessed using child self-report. The social feedback processing task presented smiling and angry faces either confirming or disconfirming written information about participant performance on a perceptual game. In addition to observing main effects of facial emotion and performance, an increase in age was related to a shift from negative (i.e., angry faces/bad performance) to positive (i.e., smiling faces/good performance) information processing in the left amygdala/hippocampus, bilateral fusiform face area, bilateral anterior temporal pole (ATP), and left anterior insula. There were no effects of attachment on social feedback processing. The self-other distinction task presented digital morphs between children's own faces and faces of their mother or stranger females. We observed differential activation in face processing and mentalizing regions in response to self and mother faces versus morphed faces. Furthermore, left ATP activity was associated with attachment anxiety such that greater attachment anxiety was related to a shift from heightened processing of self and mother faces to morphed faces. There were no effects of age on self-other distinction. We discuss our preliminary findings in the context of attachment theory and previous work on social evaluation and self-other processing.

Spatiotemporal pattern of appraising social and emotional relevance: Evidence from event-related brain potentials.

Social information is particularly relevant for the human species because of its direct link to guiding physiological responses and behavior. Accordingly, extant functional magnetic resonance imaging (fMRI) data suggest that social content may form a unique stimulus dimension. It remains largely unknown, however, how neural activity underlying social (versus nonsocial) information processing temporally unfolds, and how such social information appraisal may interact with the processing of other stimulus characteristics, particularly emotional meaning. Here, we presented complex visual scenes differing in both social (vs. nonsocial) and emotional relevance (positive, negative, neutral) intermixed with scrambled versions of these pictures to N = 24 healthy young adults. Event-related brain potentials (ERPs) to intact pictures were examined for gaining insight to the dynamics of appraisal of both dimensions, implemented within the brain. Our main finding is an early interaction between social and emotional relevance due to enhanced amplitudes of early ERP components to emotionally positive and neutral pictures of social compared to nonsocial content, presumably reflecting rapid allocation of attention and counteracting an overall negativity bias. Importantly, our ERP data show high similarity with previously observed fMRI data using the same stimuli, and source estimations located the ERP effects in overlapping occipitotemporal brain areas. Our novel data suggest that relevance detection may occur already as early as around 100 ms after stimulus onset and may combine relevance checks not only examining intrinsic pleasantness/emotional valence but also social content as a unique, highly relevant stimulus dimension.

The neural basis of humour processing.

Humour is a vital component of human socio-affective and cognitive functioning. Recent advances in neuroscience have enabled researchers to explore this human attribute in children and adults. Humour seems to engage a core network of cortical and subcortical structures, including temporo-occipito-parietal areas involved in detecting and resolving incongruity (mismatch between expected and presented stimuli); and the mesocorticolimbic dopaminergic system and the amygdala, key structures for reward and salience processing. Examining personality effects and sex differences in the neural correlates of humour may aid in understanding typical human behaviour and the neural mechanisms underlying neuropsychiatric disorders, which can have dramatic effects on the capacity to experience social reward.

Epigenetic modification of the oxytocin and glucocorticoid receptor genes is linked to attachment avoidance in young adults.

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.

Brain activity underlying negative self- and other-perception in adolescents: The role of attachment-derived self-representations.

One of teenagers' key developmental tasks is to engage in new and meaningful relationships with peers and adults outside the family context. Attachment-derived expectations about the self and others in terms of internal attachment working models have the potential to shape such social reorientation processes critically and thereby influence adolescents' social-emotional development and social integration. Because the neural underpinnings of this developmental task remain largely unknown, we sought to investigate them by functional magnetic resonance imaging. We asked n = 44 adolescents (ages 12.01-18.84 years) to evaluate positive and negative adjectives regarding either themselves or a close other during an adapted version of the well-established self-other trait-evaluation task. As measures of attachment, we obtained scores reflecting participants' positive versus negative attachment-derived self- and other-models by means of the Relationship Questionnaire. We controlled for possible confounding factors by also obtaining scores reflecting internalizing/externalizing problems, schizotypy, and borderline symptomatology. Our results revealed that participants with a more negative attachment-derived self-model showed increased brain activity during positive and negative adjective evaluation regarding the self, but decreased brain activity during negative adjective evaluation regarding a close other, in bilateral amygdala/parahippocampus, bilateral anterior temporal pole/anterior superior temporal gyrus, and left dorsolateral prefrontal cortex. These findings suggest that a low positivity of the self-concept characteristic for the attachment anxiety dimension may influence neural information processing, but in opposite directions when it comes to self- versus (close) other-representations. We discuss our results in the framework of attachment theory and regarding their implications especially for adolescent social-emotional development and social integration.

Mother-infant interaction characteristics associate with infant falling reactivity and child peer problems at pre-school age.

This longitudinal study investigated the associations between mother-infant interaction characteristics at 9 months of age, maternal mental health, infant temperament in the first year postpartum, and child behaviour at 3 years of age. The infants (N = 54, 22 females) mainly had White British ethnic backgrounds (85.7%). Results showed that i) mother-infant dyadic affective mutuality positively correlated with infant falling reactivity, suggesting that better infant regulatory skills are associated with the dyad's ability to share and understand each other's emotions; and ii) maternal respect for infant autonomy predicted fewer child peer problems at 3 years of age, suggesting that maternal respect for the validity of the infant's individuality promotes better social and emotional development in early childhood.

A narrative on the neurobiological roots of attachment-system functioning.

Attachment theory is one of the most comprehensive frameworks in social and developmental psychology. It describes how selective, enduring emotional bonds between infants and their caregivers are formed and maintained throughout life. These attachment bonds exhibit distinct characteristics that are intimately tied to fundamental aspects of mammalian life, including pregnancy, birth, lactation, and infant brain development. However, there is a lack of a cohesive biological narrative that explains the psychological forces shaping attachment behavior and the emergence and consolidation of attachment patterns at a neurobiological level. Here, we propose a theoretical narrative focusing on organized attachment patterns that systematically link the two primary purposes of the attachment behavioral system: the provision of tangible protection or support and the corresponding subjective feeling of safety or security. We aim for this detailed delineation of neurobiological circuits to foster more comprehensive and interdisciplinary future research.

Plasma oxytocin is modulated by mental training, but does not mediate its stress-buffering effect.

Based on its role in social processing and stress, oxytocin has been suggested to mediate stress reduction of socio-affective, compassion-based mental training. We tested this hypothesis in the ReSource Project, a 9-month longitudinal mental training study. Participants practiced three different types of mental training, targeting either attentional abilities (Presence Module), socio-affective or socio-cognitive abilities (Affect and Perspective Modules). We investigated plasma oxytocin levels, and their link to cortisol and subjective reactivity to acute psychosocial stress as a function of previous mental training (n = 313). In a subsample (n = 113), to better understand oxytocin's involvement in the effects of socio-affective training, we explored oxytocin, cortisol and subjective experiential responses to a single Loving-kindness Meditation (LKM) conducted after three months of Affect training (versus rest without prior training). We found that, independent of mental training, stress triggered acute oxytocin release. Following a single LKM, however, acute oxytocin release was unaffected. Training effects were only found in overall oxytocin release during both, stress and LKM. Compared to no training, 3-month compassion-based Affect training decreased overall oxytocin levels in the context of psychosocial stress, but increased overall oxytocin levels during LKM. Training-induced changes in overall oxytocin were unrelated to cortisol and subjective stress reactivity. Based on Quintana and Guastella's (2020) theory of oxytocin as an allostatic hormone with anticipatory properties, we interpret training-induced changes in overall oxytocin levels as alterations in the anticipated emotional relevance of specific events. After training socio-affective skills for three months, the stressful situation may have lost its emotional saliency, whereas the meditation technique itself gained emotional relevance. We conclude that changes in peripheral oxytocin release do not mediate stress reduction after mental training, and encourage the investigation of an allostatic concept of oxytocin in future research.