Attachment Reminders Trigger Widespread Synchrony across Multiple Brains.

Infant stimuli elicit widespread neural and behavioral response in human adults, and such massive allocation of resources attests to the evolutionary significance of the primary attachment. Here, we examined whether attachment reminders also trigger cross-brain concordance and generate greater neural uniformity, as indicated by intersubject correlation. Human mothers were imaged twice in oxytocin/placebo administration design, and stimuli included four ecological videos of a standard unfamiliar mother and infant: two infant/mother alone (Alone) and two mother-infant dyadic contexts (Social). Theory-driven analysis measured cross-brain synchrony in preregistered nodes of the parental caregiving network (PCN), which integrates subcortical structures underpinning mammalian mothering with cortical areas implicated in simulation, mentalization, and emotion regulation, and data-driven analysis assessed brain-wide concordance using whole-brain parcellation. Results demonstrated widespread cross-brain synchrony in both the PCN and across the neuroaxis, from primary sensory/somatosensory areas, through insular-cingulate regions, to temporal and prefrontal cortices. The Social context yielded significantly more cross-brain concordance, with PCNs striatum, parahippocampal gyrus, superior temporal sulcus, ACC, and PFC displaying cross-brain synchrony only to mother-infant social cues. Moment-by-moment fluctuations in mother-infant social synchrony, ranging from episodes of low synchrony to tightly coordinated positive bouts, were tracked online by cross-brain concordance in the preregistered ACC. Findings indicate that social attachment stimuli, representing evolutionary-salient universal cues that require no verbal narrative, trigger substantial interbrain concordance and suggest that the mother-infant bond, an icon standing at the heart of human civilization, may function to glue brains into a unified experience and bind humans into social groups.SIGNIFICANCE STATEMENT Infant stimuli elicit widespread neural response in human adults, attesting to their evolutionary significance, but do they also trigger cross-brain concordance and induce neural uniformity among perceivers? We measured cross-brain synchrony to ecological mother-infant videos. We used theory-driven analysis, measuring cross-brain concordance in the parenting network, and data-driven analysis, assessing brain-wide concordance using whole-brain parcellation. Attachment cues triggered widespread cross-brain concordance in both the parenting network and across the neuroaxis. Moment-by-moment fluctuations in behavioral synchrony were tracked online by cross-brain variability in ACC. Attachment reminders bind humans' brains into a unitary experience and stimuli characterized by social synchrony enhance neural similarity among participants, describing one mechanism by which attachment bonds provide the neural template for the consolidation of social groups.

Developmental Cascades Link Maternal-Newborn Skin-to-Skin Contact with Young Adults' Psychological Symptoms, Oxytocin, and Immunity; Charting Mechanisms of Developmental Continuity from Birth to Adulthood.

Premature birth disrupts the continuity of maternal-newborn bodily contact, which underpins the development of physiological and behavioral support systems. Utilizing a unique cohort of mother-preterm dyads who received skin-to-skin contact (Kangaroo Care, KC) versus controls, and following them to adulthood, we examined how a touch-based neonatal intervention impacts three adult outcomes; anxiety/depressive symptoms, oxytocin, and secretory immunoglobulin A (s-IgA), a biomarker of the immune system. Consistent with dynamic systems' theory, we found that links from KC to adult outcomes were indirect, mediated by its effects on maternal mood, child attention and executive functions, and mother-child synchrony across development. These improvements shaped adult outcomes via three mechanisms; (a) "sensitive periods", where the infancy improvement directly links with an outcome, for instance, infant attention linked with higher oxytocin and lower s-IgA; (b) "step-by-step continuity", where the infancy improvement triggers iterative changes across development, gradually shaping an outcome; for instance, mother-infant synchrony was stable across development and predicted lower anxiety/depressive symptoms; and (c) "inclusive mutual-influences", describing cross-time associations between maternal, child, and dyadic factors; for instance, from maternal mood to child executive functions and back. Findings highlight the long-term impact of a birth intervention across development and provide valuable insights on the mechanisms of "developmental continuity", among the key topics in developmental research.

Neural representation of the parent-child attachment from infancy to adulthood.

Attachment theory is built on the assumption of consistency; the mother-infant bond is thought to underpin the life-long representations individuals construct of attachment relationships. Still, consistency in the individual's neural response to attachment-related stimuli representing his or her entire relational history has not been investigated. Mothers and children were followed across two decades and videotaped in infancy (3-6 months), childhood (9-12 years) and young adulthood (18-24 years). In adulthood, participants underwent functional magnetic resonance imaging while exposed to videos of own mother-child interactions (Self) vs unfamiliar interactions (Other). Self-stimuli elicited greater activations across preregistered nodes of the human attachment network, including thalamus-to-brainstem, amygdala, hippocampus, anterior cingulate cortex (ACC), insula and temporal cortex. Critically, self-stimuli were age-invariant in most regions of interest despite large variability in social behavior, and Bayesian analysis showed strong evidence for lack of age-related differences. Psycho-physiological interaction analysis indicated that self-stimuli elicited tighter connectivity between ACC and anterior insula, consolidating an interface associating information from exteroceptive and interceptive sources to sustain attachment representations. Child social engagement behavior was individually stable from infancy to adulthood and linked with greater ACC and insula response to self-stimuli. Findings demonstrate overlap in circuits sustaining parental and child attachment and accord with perspectives on the continuity of attachment across human development.

Mother brain is wired for social moments.

Reorganization of the maternal brain upon childbirth triggers the species-typical maternal social behavior. These brief social moments carry profound effects on the infant's brain and likely have a distinct signature in the maternal brain. Utilizing a double-blind, within-subject oxytocin/placebo administration crossover design, mothers' brain was imaged twice using fMRI while observing three naturalistic maternal-infant contexts in the home ecology; 'unavailable', 'unresponsive', and 'social', when mothers engaged in synchronous peek-a-boo play. The social condition elicited greater neural response across the human caregiving network, including amygdala, VTA, hippocampus, insula, ACC, and temporal cortex. Oxytocin impacted neural response primarily to the social condition and attenuated differences between social and non-social stimuli. Greater temporal consistency emerged in the 'social' condition across the two imaging sessions, particularly in insula, amygdala, and TP. Findings describe how mother's brain varies by caregiving experiences and gives salience to moments of social synchrony that support infant development and brain maturation.

Synchronous caregiving from birth to adulthood tunes humans' social brain.

Mammalian young are born with immature brain and rely on the mother's body and caregiving behavior for maturation of neurobiological systems that sustain adult sociality. While research in animal models indicated the long-term effects of maternal contact and caregiving on the adult brain, little is known about the effects of maternal-newborn contact and parenting behavior on social brain functioning in human adults. We followed human neonates, including premature infants who initially lacked or received maternal-newborn skin-to-skin contact and full-term controls, from birth to adulthood, repeatedly observing mother-child social synchrony at key developmental nodes. We tested the brain basis of affect-specific empathy in young adulthood and utilized multivariate techniques to distinguish brain regions sensitive to others' distinct emotions from those globally activated by the empathy task. The amygdala, insula, temporal pole (TP), and ventromedial prefrontal cortex (VMPFC) showed high sensitivity to others' distinct emotions. Provision of maternal-newborn contact enhanced social synchrony across development from infancy and up until adulthood. The experience of synchrony, in turn, predicted the brain's sensitivity to emotion-specific empathy in the amygdala and insula, core structures of the social brain. Social synchrony linked with greater empathic understanding in adolescence, which was longitudinally associated with higher neural sensitivity to emotion-specific empathy in TP and VMPFC. Findings demonstrate the centrality of synchronous caregiving, by which infants practice the detection and sharing of others' affective states, for tuning the human social brain, particularly in regions implicated in salience detection, interoception, and mentalization that underpin affect sharing and human attachment.

Maternal depression alters stress and immune biomarkers in mother and child.

BACKGROUND: Exposure to maternal depression bears long-term negative consequences for children's well-being. Yet, no study has tested the joint contribution of maternal and child's hypothalamic pituitary axis and immune systems in mediating the effects of maternal depression on child psychopathology. METHODS: We followed a birth cohort over-represented for maternal depression from birth to 10 years (N = 125). At 10 years, mother and child's cortisol (CT) and secretory immunoglobulin A (s-IgA), biomarkers of the stress and immune systems, were assayed, mother-child interaction observed, mothers and children underwent psychiatric diagnosis, and children's externalizing and internalizing symptoms reported. RESULTS: Depressed mothers had higher CT and s-IgA levels and displayed more negative parenting, characterized by negative affect, intrusion, and criticism. Children of depressed mothers exhibited more Axis-I disorders, higher s-IgA levels, and greater social withdrawal. Structural equation modeling charted four paths by which maternal depression impacted child externalizing and internalizing symptoms: (a) increasing maternal CT, which linked with higher child CT and behavior problems; (b) augmenting maternal and child's immune response, which were associated with child symptoms; (c) enhancing negative parenting that predicted child social withdrawal and symptoms; and (d), via a combined endocrine-immune pathway suppressing symptom formation. CONCLUSIONS: Our findings, the first to test stress and immune biomarkers in depressed mothers and their children in relation to social behavior, describe mechanisms of endocrine synchrony in shaping children's stress response and immunity, advocate the need to follow the long-term effects of maternal depression on children's health throughout life, and highlight maternal depression as an important public health concern.

Affiliation, reward, and immune biomarkers coalesce to support social synchrony during periods of bond formation in humans.

Social bonds are critical for survival and adaptation and periods of bond formation involve reorganization of neurobiological systems as mediated by social behavior. Theoretical accounts and animal studies suggest similarity between parent-infant and pair bonding, a hypothesis not yet directly tested in humans. In this study, we recruited three groups of human adults (N=189); parents who had their firstborn child in the last 4-6months, new lovers who began a romantic relationship within the past 4months, and non-attached singles. We measured plasma oxytocin (OT), beta endorphin (ß-End), and interlukin-6 (IL-6), biomarkers of the affiliation, reward, and stress-response systems, and micro-coded gaze and affect synchrony between parents and infants and among new lovers during social interaction. OT significantly increased during periods of parental and romantic bonding and was highest in new lovers. In contrast, IL-6 and ß-End were highest in new parents and lowest in singles. Biomarkers became more tightly coupled during periods of bond formation and inter-correlation among hormones was highest during romantic bonding. Structural equation modeling indicated that the effects of IL-6 and ß-End on behavioral synchrony were mediated by their impact on OT, highlighting the integrative role of the oxytocinergic system in supporting human social affiliation. Findings suggest that periods of bond formation are accompanied by increased activity, as well as tighter cross-talk among systems underpinning affiliation, reward, and stress management and that research on the multidimensional process of bonding may shed further light on the effects of attachment on health.