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The Neurobiology of Human Attachments
Abstract
Attachment bonds are a defining feature of mammals. A conceptual framework on human attachments is presented, integrating insights from animal research with neuroimaging studies. Four mammalian bonds are described, including parent-infant, pair-bonds, peers, and conspecifics, all built upon systems shaped by maternal provisions during sensitive periods, and evolution from rodents to humans is detailed. Bonding is underpinned by crosstalk of oxytocin and dopamine in striatum, combining motivation and vigor with social focus, and their time sensitivity/pulsatility enables reorganization of neural networks. Humans' representation-based attachments are characterized by biobehavioral synchrony and integrate subcortical with cortical networks implicated in reward/motivation, embodied simulation, and mentalization. The neurobiology of love may open perspectives on the 'situated' brain and initiate dialog between science and humanities, arts, and clinical wisdom.
... According to the biobehavioral synchrony model 88,89 , children acquire the capacity for brain synchrony within the mother-infant context during sensitive, well-timed social interactions 88,89 . Consistent with the model, studies have shown that episodes of brain coupling during infancy and early childhood are aligned with the mother's or female stranger's social behavior, including touch, gaze, or vocalizations 67,85 . ...
... According to the biobehavioral synchrony model 88,89 , children acquire the capacity for brain synchrony within the mother-infant context during sensitive, well-timed social interactions 88,89 . Consistent with the model, studies have shown that episodes of brain coupling during infancy and early childhood are aligned with the mother's or female stranger's social behavior, including touch, gaze, or vocalizations 67,85 . ...
... Second, guided by the bio-behavioral synchrony model 49,88 , we hypothesized that significant longitudinal associations will be found between maternal caregiving behaviors in infancy and interbrain synchrony in adolescence. Specifically, we anticipated that higher levels of maternal sensitivity during mother-infant interactions at 3 months would be positively associated with enhanced connectivity in the right frontotemporal interbrain network during mother-adolescent interactions 12 years later. ...
Caregiving plays a critical role in children’s cognitive, emotional, and psychological well-being. In the current longitudinal study, we investigated the enduring effects of early maternal behavior on processes of interbrain synchrony in adolescence. Mother-infant naturalistic interactions were filmed when infants were 3–4 months old and interactions were coded for maternal sensitivity and intrusiveness with the Coding Interactive Behavior Manual. In early adolescence (Mean = 12.30, SD = 1.25), mother-adolescent interbrain synchrony was measured using hyperscanning EEG during a naturalistic interaction of positive valence. Guided by previous hyperscanning studies, we focused on interbrain connections within the right frontotemporal interbrain network. Results indicate that maternal sensitivity in early infancy was longitudinally associated with neural synchrony in the right interbrain frontotemporal network. Post-hoc comparisons highlighted enhancement of mother-adolescent frontal-frontal connectivity, a connection that has been implicated in parent-child social communication. In contrast, maternal intrusiveness in infancy was linked with attenuation of interbrain synchrony in the right interbrain frontotemporal network. Sensitivity and intrusiveness are key maternal social orientations that have shown to be individually stable in the mother-child relationship from infancy to adulthood and foreshadow children’s positive and negative social-emotional outcomes, respectively. Our findings are the first to demonstrate that these two maternal orientations play a role in enhancing or attenuating the child’s interbrain frontotemporal network, which sustains social communication and affiliation. Results suggest that the reported long-term impact of maternal sensitivity and intrusiveness may relate, in part, to its effects on tuning the child’s brain to sociality.
... Neural mirroring ( Inter-brain synchronization (Dumas et al., 2010) Brain-to-brain synchrony (Azhari et al., 2019) Biobehavioural synchrony (Feldman, 2017) Sensorimotor synchronization (Repp & Su, 2013) Physiological synchrony (RSA) (Abney et al., ...
... Bonding, in turn, ensures that complementary caregiving behaviours from a caregiver emerge and are efficiently directed towards the "care seeker" (Mikulincer & Shaver, 2019). Bio-behavioural synchrony (BBS) -the alignment of behaviour, physiology and brain activity during and shortly after social interaction -is regarded as a key interpersonal process -not only in the establishment and maintenance of close emotional bonds related to attachment and bonding, but also for efficient co-regulation and social allostasis (Feldman, 2017). With the emergence of hyperscanning, there has thus naturally been great interest in establishing links between attachment and bonding in child-parent and romantic partner dyads as well as BBS, and particularly IBS. ...
... A growing body of empirical evidence shows that interpersonal neural synchrony emerges early in human development and can already be observed in the early interactions of infants and their caregivers. According to the bio-behavioural synchrony (BBS) framework (Feldman, 2017; see section 2.3), the coordination of behavioural and biological (including IBS) dynamics during social contact is a fundamental characteristic of human attachment relationships with deep ontogenetic roots in the caregiver-infant bond. ...
Humans are highly social, typically without this ability requiring noticeable efforts. Yet, such social fluency poses challenges both for the human brain to compute and for scientists to study. Over the last few decades, neuroscientific research in human sociality has witnessed a shift in focus from single-brain analysis to complex dynamics occurring across several brains, posing questions about what these dynamics mean and how they relate to multifaceted behavioural models. We propose the term Relational Neuroscience to describe the interdisciplinary research field devoted to modelling the inter-brain dynamics subserving human connections, spanning from real-time joint experiences to long-term social bonds. Hyperscanning, i.e., simultaneously measuring brain activity from multiple individuals, has proven to be a highly promising technique to investigate inter-brain dynamics. Here, we discuss how hyperscanning can help investigate questions within the field of Relational Neuroscience, considering a variety of subfields, including cooperative interactions in dyads and groups, empathy, social attachment and bonding, and developmental neuroscience. While presenting Relational Neuroscience in the light of hyperscanning, our discussion also takes into account behaviour, physiology and endocrinology to properly interpret inter-brain dynamics in social contexts. We consider the strengths but also the limitations and caveats of hyperscanning to answer questions about interacting brains. The aim is to provide a framework for future work to build better theories across a variety of contexts and research subfields to model human sociality.
... Despite the short-term and long-term socioemotional and relational implications of nonverbal communication on romantic relationships [6,10], it is unclear how nonverbal connections (even brief moments) may relate to current experiences and biological mechanisms of positive feeling or love. Longstanding evidence from animals and humans suggests that loving attachments are subserved by instantaneous, biobehavioral synchrony wherein biological signals co-relate [11]. To that extent, synchronized physiology may subserve increased feelings of closeness between romantic partners engaged in nonverbal connection. ...
... Social approach and its counterpart (social avoidance) describes the neurobiological and psychological instinct to engage (or disengage) with selected people [23]. Considering the nature of affiliative pair bonding [24], neural mechanisms that modulate social approach/avoidance [25] are likely synchronized between romantic partners [11]. One important EEG measurement of social approach is known as frontal alpha asymmetry (FAA), which reflects approach or avoidant motivational states in the brain [26,27]. ...
Nonverbal connection is an important aspect of everyday communication. For romantic partners, nonverbal connection is essential for establishing and maintaining feelings of closeness. EEG hyperscanning offers a unique opportunity to examine the link between nonverbal connection and neural synchrony among romantic partners. This current study used an EEG hyperscanning paradigm to collect frontal alpha asymmetry (FAA) signatures from 30 participants (15 romantic dyads) engaged in five different types of nonverbal connection that varied based on physical touch and visual contact. The results suggest that there was a lack of FAA while romantic partners were embracing and positive FAA (i.e., indicating approach) while they were holding hands, looking at each other, or doing both. Additionally, partners’ FAA synchrony was greatest at a four second lag while they were holding hands and looking at each other. Finally, there was a significant association between partners’ weekly negative feelings and FAA such that as they felt more negative their FAA became more positive. Taken together, this study further supports the idea that fleeting moments of interpersonal touch and gaze are important for the biological mechanisms that may underlie affiliative pair bonding in romantic relationships.
... For example, the gentle touch of a loved one or caregiver is more likely to elicit positive emotional responses and higher levels of oxytocin release than the touch of a stranger. This contextual sensitivity is essential in early development, as it helps children distinguish between familiar and unfamiliar social partners, facilitating the formation of secure attachment and social learning [48]. The release of oxytocin during skin-to-skin contact or other forms of affective contact is significant for infants because their emotional regulation and physiological stability are closely linked to interactions with caregivers. ...
... In addition, the caregiver's warmth, voice, and heartbeat provide comforting stimuli by activating the infant's parasympathetic nervous system and releasing oxytocin. As discussed above, oxytocin is essential because it is a hormone associated with social bonding and stress reduction [44] and it plays a key role in establishing secure attachment, which is critical for a child's long-term emotional and social development [48]. ...
Background/Objectives: Affective touch is crucial in infant development, particularly in regulating emotional, cognitive, and physiological processes. Preterm infants are often deprived of essential tactile stimulation owing to their early exposure to the external environment, which may affect long-term developmental outcomes. This review aimed to examine the neurobiological mechanisms of affective touch and highlight effective interventions, such as skin-to-skin contact (SSC) and kangaroo care (KC), to promote development in preterm infants. Methods: This review summarizes recent studies in the literature on affective touch, the role of C-tactile fibers, and the effects of tactile interventions in neonatal care. Studies were selected based on their relevance to the care and development of preterm infants, with a focus on physiological and neurodevelopmental outcomes. Key interventions, including SSC and massage therapy, are discussed in relation to their effectiveness in the neonatal intensive care unit (NICU). Results: The results suggest that affective touch, mainly through activation of tactile C-fibers, improves caregiver-infant bonding, reduces stress responses, and supports neurodevelopment in preterm infants. Interventions such as SSC and KC have also been shown to improve physiological regulation in these infants, including heart rate, breathing, and temperature control while promoting emotional regulation and cognitive development. Conclusions: Affective touch is a key component of early development, particularly in pre-term infants admitted to the NICU. Integrating tactile interventions such as SSC and KC into neo-natal care practices may significantly improve long-term developmental outcomes. Future research should explore the epigenetic mechanisms underlying affective touch and further refine tactile interventions to optimize neonatal care.
... A core mechanism of resilience is biobehavioral synchrony, the synchronized functioning of physiological and behavioral processes between affiliative partners (Feldman, 2017). Biobehavioral synchrony develops within the mother-infant bond and involves the coordination of nonverbal behavior, synchronized release of hormones, matching of heart rhythms, and coupling of activity between the two brains (Endevelt-Shapira & Feldman, 2023;Feldman, 2007;Feldman, Gordon, & Zagoory-Sharon, 2011;Feldman, Magori-Cohen, et al., 2011). ...
... Our investigation centered on three critical aspects of the microbiome: composition, diversity, and mother-child microbial synchrony. Consistent with our biobehavioral synchrony model (Feldman, 2012(Feldman, , 2017, we explored whether mother-child microbial synchrony is associated with fewer child PTSD symptoms and may thus serve as a mechanism of resilience. ...
Objective: Identifying biomarkers that can distinguish trauma-exposed youth at risk for developing posttraumatic pathology from resilient individuals is essential for targeted interventions. As trauma can alter the microbiome with lasting effects on the host, our longitudinal, multimeasure, cross-species study aimed to identify the microbial signature of posttraumatic stress disorder (PTSD). Method: We followed children exposed to war-related trauma and matched controls from early childhood (Mage = 2.76 years, N = 232) to adolescence (Mage = 16.13 years, N = 84), repeatedly assessing posttraumatic symptomatology and maternal caregiving. In late adolescence, we collected fecal samples from mothers and youth and assessed microbiome composition, diversity, and mother–child microbial synchrony. We then transplanted adolescents’ fecal samples into germ-free mice to determine if behavioral changes are observed. Results: Youth with PTSD exhibited a distinct gut microbiome profile and lower diversity compared to resilient individuals, and microbiome diversity mediated the continuity of posttraumatic symptomatology throughout development. Low microbiome diversity correlated with more posttraumatic symptoms in early childhood, more emotional and behavioral problems in adolescence, and poor maternal caregiving. Youth with PTSD demonstrated less mother–child microbial synchrony, suggesting that low microbial concordance between mother and child may indicate susceptibility to posttraumatic illness. Germ-free mice transplanted with microbiomes from individuals with PTSD displayed increased anxious behavior. Conclusions: Our findings provide evidence that the trauma-associated microbiome profile is at least partially responsible for the anxiety component of the PTSD phenotype and highlight microbial underpinnings of resilience. Further, our results suggest that the microbiome may serve as additional biological memory of early life stress and underscore the potential for microbiome-related diagnosis and treatment following trauma.
... The attachment behavioral system is useful in maintaining physical and felt security, and its activation follows the emergence of disturbances to psychophysical balance (Bowlby, 1969(Bowlby, /1982. From a neurobiological point of view and particularly from the perspective of social neuroscience of human attachment (Coan, 2016;Feldman, 2017;White et al., 2023), the main function of attachment represented by security is closely related to organic homeostasis In this sense, the caregiver is necessary to the infant for co-regulation, this is when disturbances to a homeostatic state are managed through social-allostasis (Coan and Sbarra, 2015;Atzil et al., 2018). The caregiver serves as good regulator as long as he or she is able to cooperate with the infant in restoring homeostatic conditions, minimizing the energy the infant must expend in doing so (Atzil et al., 2018). ...
... The ventral tegmental area, substantia nigra, ventral striatum, and ventromedial prefrontal cortex are regions of the brain that play a role in reward processing, primarily through dopaminergic activity. The sense of safety is better represented by the joint action of other neurotransmitter systems, such as vasopressin, oxytocin, opioids, and serotonin (e.g., Feldman, 2017). The emotion (self-) regulation module concerns the functions of voluntary regulation of emotions, also through social behaviors. ...
Attachment is one of the foundational themes in the history of the psychological development of human beings. For this reason, we assume that it must be approached by taking into account multiple scientific perspectives. The present review aims at analyzing the state of the art regarding the genetic, neurobiological and cognitive mechanisms underlying the development of attachment bonding, considering the child as the frame of reference. We hypothesize that attachment may be present in prototypical forms even in the prenatal period, thus our analysis has a temporal origin in the intrauterine period preceding birth. The intrauterine period is assumed to be a period of maximum sensitivity to stimuli and in particular to those coming from a potential primary caregiver: the biological mother. We conclude with a reframing of the state of the art and propose that future research work would benefit from a superordinate model of attachment, capable of containing and regulating all its components and variables.
... During the infant's preverbal developmental periods, it is essential that parents possess the capacity to accurately recognise and respond to their infant's nonverbal facial expressions of emotion. This enables them to mirror expressions, interact with and form a bond with their child (Ainsworth, 1979;Feldman, 2017). In the long term, maternal EP ability also appears to be a crucial factor in maternal sensitivity. ...
... Maternal bonds set the foundation for future social bonds that an individual may form throughout development, and this is true across the mammalian realm [45][46][47][48]. There are similarities in the physiology and neurobiology of mother-infant bonds, pair bonds, and affiliative attachment bonds [49][50][51]. The physiological correlates of social attachment formation are well studied in mammals and centrally involve the neuropeptide hormone oxytocin. ...
An increasing body of evidence indicates that owning a pet dog is associated with improvements in child health and well-being. Importantly, the degree of the social bond between child and dog may mediate the beneficial outcomes of dog ownership. The formation of social bonds is an intrinsically dyadic, interactive process where each interactor’s behavior influences the other’s behavior. For this reason, it is critical to evaluate the biological mechanisms of attachment in both children and their pet dogs as a socially bonded pair. Here, we review the physical, mental, and emotional outcomes that are associated with pet dog ownership or interaction in children. We then discuss the evidence that suggests that the strength of a social bond between a child and their pet dog matters for maximizing the beneficial outcomes associated with pet dog ownership, such as possible stress-buffering effects. We review the existing literature on the neural and endocrinological mechanisms of social attachment for inter-species social bonds that form between human children and dogs, situating this emerging knowledge within the context of the mechanisms of intra-species bonds in mammals. Finally, we highlight the remaining open questions and point toward directions for future research.
... This process, in which the mother establishes a selective and lasting bond with her child, is accompanied by mental, emotional, and behavioral changes that facilitate physical and psychological intimacy. During interactions, mothers and infants showed synchronized nonverbal communication (such as eye contact, holding, calling out, touching), increased heart rate, oxytocin response, cortisol response to stress, and brain oscillations in alpha and gamma rhythms (9). Supporting kangaroo care and breastfeeding is beneficial in mother-infant bonding and supports cognitive and motor development (10). ...
Abstract
Background and Objectives: It is known that social support, especially the support given to mothers of premature babies, has a positive effect on maternal attachment. This study aims to compare the social support and the maternal attachment levels of mothers who had premature infants in NICU during the COVID-19 pandemic process and before.
Methods: This descriptive and cross-sectional study was conducted in the NICU of a university hospital in Istanbul between November 2020 and April 2021. The study sample consisted of 62 mothers who were randomly selected. Data were collected the Multidimensional Scale of Perceived Social Support (MSPSS), Maternal Attachment Inventory (MAI), and socio-demographic form.
Results: The MSPSS score of mothers (n = 43) was 98.65±8.36 before COVID-19, and the mean score of the mothers (n = 62) who had an infant in the NICU during the pandemic was 95.11±3.43 and this difference was significant (P = 0.003). The MAI scores of mothers were 54.91±7.91 in the pre-COVID-19 group and 45.53±8.53 in the COVID-19 group, and this difference was statistically significant (P < 0.001). MAI scores were found to be positively and significantly correlated with the MSPSS and perceived social support from the family.
Conclusion: The study revealed that the COVID-19 pandemic reduced the level of maternal attachment and was linked with social support. The study also suggested that mother-infant attachment during the COVID-19 outbreak was associated with perceived social support from family.
Keywords
Preterm Mother COVID-19 Maternal Attachment Social Support Nursing Nurse Midwife
... In fact, it is only recently that studies have moved beyond an exclusively behavioural approach to synchrony to incorporate hormonal, physiological and even neural information (e.g. behavioural with brain-to-brain synchrony in [11,12]), a trend that is of particular relevance when attempting to enhance the interpretability of synchrony findings across studies [13]. In the clinical context, understanding relationships between different levels of synchrony is even more crucial. ...
Interpersonal synchrony is a crucial construct in understanding social interactions, which has been used in clinical studies to measure the quality of the therapeutic alliance. However, there is a lack of studies investigating the correlation between synchrony expressed on different levels: behavioural and neurophysiological. Furthermore, there are no studies that examine how the implementation of psychodramatic role-playing techniques, when individuals adopt the persona of a different character, may influence intrinsic biobehavioural synchrony between two parties. The present study, therefore, aims to uncover the relationship between behavioural and brain-to-brain synchrony across different role-playing techniques and elucidate the impact of these synchronies on participants’ levels of anxiety and empathy. By using functional near-infrared imaging and behavioural coding in a dyadic role-playing paradigm (n = 41 dyads), the study found correlations between behavioural and brain-to-brain synchrony during naturalistic conversations, but not during role-play, implying a qualitative change in interpersonal synchrony when implementing role-playing techniques. Additionally, the study noted significant contributions of both behavioural and brain-to-brain synchrony as well as peripheral factors such as dyadic sex make-up and role immersion in predicting dyadic anxiety and empathy changes. Findings call for future studies to consider role-playing scenarios as a qualitatively different form of social interaction.
... Interbrain synchrony has been previously established as a neural indicator for social engagement, and the moment-to-moment interaction between the brains' of individuals can strengthen or diminish depending upon the degree of reciprocity of responses and mutual engagement between social partners (Czeszumski et al. 2020). Synchrony during the stress condition significantly exceeded the synchrony detected in the baseline and recovery conditions (which also incorporated collaborative tasks but without rigorous problem-solving components), suggesting that dyadic tasks that require substantial reasoning demands from both parents and children uniquely modulate the brain-to-brain network environment over and above the basic attachmentinfluenced relationship that characterizes parent-child interactions (Feldman 2017). Previous research has also detected differential neural synchrony patterns between parent-child dyads during problem-solving and cooperative contexts versus competitive contexts (Miller et al. 2019;Nguyen et al. 2021;Reindl et al. 2018Reindl et al. , 2022, further reaffirming not only the coregulatory nature of parent-child interaction, but the importance of shared intention and affect in a collaborative environment and how it may facilitate social neurodevelopment (Feldman 2015). ...
Introduction
Early child development occurs within an interactive environment, initially dominated by parents or caregivers, and is heavily influenced by the dynamics of this social context. The current study probed the neurobiology of “family personality”, or family functioning, in the context of parent–child dyadic interaction using a two‐person neuroimaging modality.
Methods
One hundred and five parent–child dyads (child mean age 5 years 4 months) were recruited. Functional near‐infrared spectroscopy (fNIRS) hyperscanning was employed to measure neural synchrony while dyads completed a mildly stressful interactive task. Family functioning was measured through the Family Adaptability and Cohesion Scale IV (FACES‐IV).
Results
Synchrony during stress was significantly greater than synchrony during both baseline and recovery conditions for all dyads. A significant interaction between neural synchrony in each task condition and familial balanced flexibility was found, such that higher levels of balanced flexibility were associated with greater changes in frontal cortex neural synchrony as dyads progressed through the three task conditions.
Discussion
Parent–child dyads from families who display heightened levels of balanced flexibility are also more flexible in their engagement of neural synchrony when shifting between social conditions. This is one of the first studies to utilize a two‐person imaging modality to explore the links between family functioning and interbrain synchrony between parents and their children.
... As one of the vital brain regions associated with the mentalizing process, the frontal area has been implicated to be responsible for understanding and predicting others' intentions and joint attention (Pan et al., 2017;Schilbach et al., 2013;Wang et al., 2018). Both mothers' and children's frontal activities have shown modulations by mother-child attachment in accumulated single-brain neuroimaging studies (Feldman, 2017;Laurent and Ablow, 2012;Minagawa-Kawai et al., 2009;Perry et al., 2017;Young et al., 2017); however, the evidence from the inter-brain network is still lacking. Though Miller et al. had tried to explore the link between attachment and the parent-child inter-brain network (Miller et al., 2019), they only found a tendency that the avoidant child attachment might associate with less cooperation-related synchrony in the right frontopolar prefrontal cortex. ...
Mother-child interaction is highly dynamic and reciprocal. Switching roles in these back-and-forth interactions serves as a crucial feature of reciprocal behaviors while the underlying neural entrainment is still not well-studied. Here, we designed a role-controlled cooperative task with dual EEG recording to study how differently two brains interact when mothers and children hold different roles. When children were actors and mothers were observers, mother-child inter-brain synchrony emerged within the theta oscillations and the frontal lobe, which highly correlated with children's attachment to their mothers. When their roles were reversed, this synchrony was shifted to the alpha oscillations and the central area and associated with mothers' perception of their relationship with their children. The results suggested an observer-actor neural alignment within the actor's oscillations, which was modulated by the actor-toward-observer emotional bonding. Our findings contribute to the understanding of how inter-brain synchrony is established and dynamically changed during mother-child reciprocal interaction.
... As equanimity engages compassion which activates the neural network of affiliation, love, reward, and positive affect (Anālayo, 2021;Desbordes et al., 2015) it actively relieves suffering, helps maintain emotional sovereignty and protects from the common occurrence of burnout due to despair and (Desbordes et al., 2015;Feldman, 2017). Samatva (Equanimity) constitutes being fully present and identifying mental occurrences -mood, thought, emotion, and sensation -without judgment or attachment. ...
This study explores the role of self-control as a mediator in the relationship between Samatva (a key Indian concept of equanimity) and thriving among emerging adults. Samatva, representing a balanced and serene state of mind, is examined for its impact on thriving through its influence on self-control. With a sample of 210 individuals aged 18-29, the study used cross-sectional surveys and Structural Equation Modeling (SEM) via AMOS software. Results indicate that higher Samatva correlates with increased self-control, which, in turn, predicts enhanced thriving. This highlights self-control as a crucial mechanism through which equanimity fosters well-being. The findings offer valuable insights for developing interventions to improve thriving by promoting Samatva and self-control.
... Such accents are a perceived phenomenon that only exists on the observer's end, and Ting et al. [12] suggest they may play a role in maintaining group identity. More broadly, interactive synchrony across multiple levels of physiological and neural activity has been proposed to support implicit mentalizing, empathy, communication, learning and social affiliation [100,108,109]. Interestingly, this list substantially overlaps with the 'disappointing failures' of ungrounded LLMs discussed in the previous section. ...
This theme issue brings together researchers from diverse fields to assess the current status and future prospects of embodied cognition in the age of generative artificial intelligence. In this introduction, we first clarify our view of embodiment as a potentially unifying concept in the study of cognition, characterizing this as a perspective that questions mind–body dualism and recognizes a profound continuity between sensorimotor action in the world and more abstract forms of cognition. We then consider how this unifying concept is developed and elaborated by the other contributions to this issue, identifying the following two key themes: (i) the role of language in cognition and its entanglement with the body and (ii) bodily mechanisms of interpersonal perception and alignment across the domains of social affiliation, teaching and learning. On balance, we consider that embodied approaches to the study of cognition, culture and evolution remain promising, but will require greater integration across disciplines to fully realize their potential. We conclude by suggesting that researchers will need to be ready and able to meet the various methodological, theoretical and practical challenges this will entail and remain open to encountering markedly different viewpoints about how and why embodiment matters.
This article is the part of this theme issue ‘Minds in movement: embodied cognition in the age of artificial intelligence’.
... Third, we quantified dynamic individual and dyadic RSA regulation via RSA return strength and parent-driven and childdriven RSA coupling from a dynamic systems perspective. Investigating dynamic RSA self-regulatory and coregulatory processes, particularly in early childhood, provides novel insight into the development of pathways from external regulation by parents to child internalized self-regulation (Feldman, 2017). Fourth, the use of a carefully crafted laboratory task allowed us to examine how proximal task stressors shape dynamic RSA selfregulation and coregulation and whether more distal life stressors exert their influences by alternating the effects of task stressors. ...
This study examined how proximal and distal familial stressors influenced the real‐time, dynamic individual and dyadic regulation of respiratory sinus arrhythmia (RSA) in mother–preschooler and father–preschooler interactions in at‐risk families ( N = 94, M age = 3.03 years, 47% males, 77% White, 20% Latinx, data collected 2013–2017). Proximal stressors were operationalized as changing task demands (baseline, challenge, recovery) across a dyadic puzzle task. Distal stressors were measured as parent‐reported stressful life events. Multilevel models revealed that greater proximal and distal stressors were related to weaker dynamic self‐regulation of RSA in mothers, fathers, and children, and more discordant mother–child and father–child coregulation of RSA. Findings affirm that stress is transmitted across levels and persons to compromise real‐time regulatory functioning in early, developmentally formative caregiver–child interactions.
... In accordance with biobehavioral models that posit a regulatory function for physiological synchrony (Feldman, 2007b(Feldman, , 2007a(Feldman, , 2012(Feldman, , 2017, this study provides evidence for a positive feedback loop (Butler & Randall, 2013) in the form of positive synchronization to the more mature regulator. For normative dyads within low-stress contexts, this likely results in relatively calmer states of the highly regulated adult being directly followed by relatively calmer infant states, thereby helping the nascent infant regulator produce and sustain the calm physiological state necessary for social engagement. ...
Human interpersonal capacities emerge from coordinated neural, biological, and behavioral activity unfolding within and between people. However, developmental research to date has allocated comparatively little focus to the dynamic processes of how social interactions emerge across these levels of analysis. Second-person neuroscience and dynamic systems approach together to offer an integrative framework for addressing these questions. This study quantified respiratory sinus arrhythmia and social behavior (∼360 observations per system) from 44 mothers and typically developing 9-month-old infants during a novel modified “still-face” (text message perturbation) task. Stochastic autoregression models indicate that the infant parasympathetic nervous system is coupled within and between people second by second and is sensitive to social context. Intraindividual, we found positive coupling between infants’ parasympathetic nervous system activity and their social behavior in the subsequent second, but only during the moments and periods of active caregiver engagement. Between people, we found a bidirectional coregulatory feedback loop: Mothers’ parasympathetic activity positively predicted that of their infant in the subsequent second, a form of synchrony that decreased during the text message perturbation and did not fully recover. Conversely, infant parasympathetic activity negatively predicted that of their mother at the subsequent second, a form of synchrony that was invariant over social context. Findings reveal unidirectional parasympathetic coupling within infants and a complementary allostatic feedback loop between mother and infant parasympathetic systems. They offer novel evidence of a dynamic, socially embedded parasympathetic system at previously undocumented timescales, contributing to both basic science and potential clinical targets to better support adaptive, multisystem social development.
... According to the biobehavioral synchrony model 88,89 , children acquire the capacity for brain synchrony within the mother-infant context during sensitive, well-timed social interactions (Feldman, 2017(Feldman, , 2020. Consistent with the model, studies have shown that episodes of brain coupling during infancy and early childhood were aligned with the mother's or female stranger's social behavior, including touch, gaze, or vocalizations 67,85 . ...
Caregiving plays a critical role in children's cognitive, emotional, and psychological well-being. In the current longitudinal study, we investigated the enduring effects of early maternal behavior on processes of interbrain synchrony in adolescence. Mother-infant naturalistic interactions were filmed when infants were 3 months old and interactions were coded for maternal sensitivity and intrusiveness using the Coding Interactive Behavior. In early adolescence (Mean = 12.30, SD = 1.25), mother-adolescent interbrain synchrony was measured using hyperscanning EEG during a naturalistic interaction of positive valance. Consistent with prior hyperscanning research, we focused on interbrain connections within the right frontotemporal network. Results indicate that maternal sensitivity in early infancy was longitudinally associated with interbrain synchrony in the right frontotemporal network. Post-hoc comparisons highlighted enhancement of mother-adolescent frontal-frontal connectivity, a connection implicated in parent-child social communication. In contrast, maternal intrusiveness in infancy linked with attenuation of interbrain synchrony in the right frontotemporal network. Sensitivity and intrusiveness are key maternal social orientations that are individually stable in the mother-child relationship from infancy to adulthood and foreshadow children's positive and negative social-emotional outcomes, respectively. Our findings are the first to demonstrate that these two maternal orientations play a role in enhancing or attenuating the child's frontotemporal interbrain network that sustains social communication and affiliation. Results suggest that the long-term impact of the mother's sensitive and intrusive style may relate, in part, to its effects on tuning the child's interbrain network to sociality.
... The approach module includes regions of the reward system. It encodes social interactions as innately rewarding and thereby counteracts fear tendencies (Feldman, 2017;Haber & Knutson, 2010). ...
Despite a growing literature, experiments directly related to attachment are still needed. We explored brain processes involved in two aspects of attachment, distress and comfort. Seventy-eight healthy adult males with different attachment styles (secure, avoidant, and anxious) viewed distress, comfort, complicity-joy and neutral images (picture database BAPS-Adult) in an fMRI block design. ROIs from the modules described in the functional Neuro-Anatomical Model of Attachment (Long et al. 2020) were studied. Secure participants used more co- and self-regulation strategies and exhibited a higher activation of the reward network in distress and comfort viewing, than insecure participants. Avoidant participants showed the lower brain activations. Their approach and reward modules were the least activated in distress and comfort. Anxious participants presented both higher activations of the approach and aversion modules during complicity-joy. In addition, comfort and complicity-joy were processed differently according to attachment styles and should be differentiated among positive stimuli to disentangle attachment processes.
... Preterm birth is associated with less effective relationship-building behaviors in parents, with mothers in particular characterized by a higher rate of maternal depression and reduced sensitivity levels towards their infants [14]. As a result, preterm birth has a negative impact on parent-infant synchrony, which serves as a critical foundation for infants' cognitive and emotional development [7], [8], [15], secure attachment [16], [17], and capacity for empathy [18]. Therefore, early intervention programs should address the family environment and caregiver's behavior as soon as possible to achieve significant long-term improvement in the child's health [19]. ...
... The primary physiological stress systems are the sympathetic-adrenal medullary (SAM) axis, inducing an immediate ght-or-ight response, and the hypothalamic-pituitary-adrenal (HPA) axis, regulating the subsequent release of the main stress hormone cortisol. Humans tend to synchronize with those around them in various situations (Feldman, 2017), including during stress (Engert et al., 2014a). This phenomenon, known as bio-behavioral synchrony (BBS), re ects how individuals' physiological and behavioral states align with those of others in their environment (Feldman, 2012). ...
Stress-related disorders are common in modern societies. What adds to the burden is empathic stress, arising when observing another’s stress elicits a stress response in the observer. In romantic couples, we investigated the association between empathic stress and adult attachment – a deep emotional bond in relationships – to understand facets of risk and resilience inherent to attachment. Psychosocial stress was induced in one partner (“target”) while the other passively observed the situation (“observer”). Stress reactivity was measured in both partners via salivary cortisol, heart rate, high-frequency heart rate variability (HF-HRV), and questionnaires. Observers’ attachment representations were assessed using the Adult Attachment Interview. As hypothesized, we found higher cortisol and HF-HRV resonance, that is, proportionality in stress reactivity in targets and observers, in dyads with securely as opposed to insecurely attached observers (specifically insecure-dismissing). Consistent with attachment as a resilience factor, our results suggest that securely attached individuals are physiologically more in tune with their partners during psychosocially stressful situations, possibly allowing for mutual understanding and triggering supportive behavior. However, suggesting a potential risk inherent to attachment security, in contexts of frequent or extreme partner stress, securely attached individuals may be prone to excessive empathic stress activation and subsequent health impairments.
... Furthermore, our bodies' dissimilarity explains a lack of empathy for floral species and why people are more likely to sympathise with animals (mammals in particular) (Jose, Wu and Kamoun, 2019). For instance, as soon as some mammals exhibit "facial expressions" and vocalisation similar to human children, it triggers some neural and hormonal mechanisms of parental behaviour (Feldman, 2017), especially if these animals are furry and small. Thus, inattention in terms of somatosensory mechanisms and attitude is the basis of plant blindness. ...
Humans constantly interact with their environment, with other humans, as well as natural and artificial non-human agents. Nevertheless, our somatosensory system limits the diversity of our ways of communicating. Such organisms as plants thus escape our notice, blending into the landscape. This phenomenon is called Plant blindness. This leads not only to indifference and lack of empathy towards plants among ordinary people but also to a deficit in funding plant conservation. We believe that it is important to develop connections and also rethink the relationship between humans and flora. This paper examines the Plant turn in the context of an art-science project titled Plantoverse. The scientific part of the project is based on a study of plant epidermis cells, which possess optical properties and function as a “lens”. The data acquired via confocal microscopy was used to construct a mathematical model of these lenses which in turn formed the basis of the artistic work. It is a representation of the plant epidermis in a digital environment. The work allows us to look at ourselves through “plant optics'' and find new tools for interacting with the vegetal world. This interdisciplinary approach can help transfer knowledge about flora from the professional environment to lay society and form a new, more empathetic view toward plants.
... Humans match each other's limb and trunk movements, facial expressions, emotional reactions, and even vocal patterns (Borrie and Delfino, 2017;Lahnakoski et al., 2020;Yokozuka et al., 2021;Shamay-Tsoory, 2022). Inside bodies, involuntary synchrony can emerge between the hearts, endocrine systems, and brains of the self and other (Feldman, 2017;Nummenmaa et al., 2018;Parkinson et al., 2018;Mayo and Gordon, 2020;De Hamilton, 2021). Generally speaking, synchrony between people is believed to support social learning and social alignment (Bandura and Adams, 1977;Fuhrmann et al., 2014;Shamay-Tsoory et al., 2019;Crone et al., Frontiers in Human Neuroscience 02 frontiersin.org ...
The process of synchronizing our body movements with others is known to enhance rapport, affect, and prosociality. Furthermore, emerging evidence suggests that synchronizing activities may enhance cognitive performance. Unknown, by contrast, is the extent to which people’s individual traits and experiences influence their ability to achieve and maintain movement synchrony with another person, which is key for unlocking the social and affective benefits of movement synchrony. Here, we take a dyad-centered approach to gain a deeper understanding of the role of embodiment in achieving and maintaining movement synchrony. Using existing data, we explored the relationship between body competence and body perception scores at the level of the dyad, and the dyad’s movement synchrony and complexity while playing a 2.5-min movement mirroring game. The data revealed that dyadic body competence scores positively correlate with movement synchrony, but not complexity, and that dyadic body perception scores are not associated with movement synchrony or complexity. Movement synchrony was greater when the more experienced member of the dyad was responsible for copying movements. Finally, movement synchrony and complexity were stable across the duration of the mirror game. These findings show that movement synchrony is sensitive to the composition of the dyad involved, specifically the dyad’s embodiment, illuminating the value of dyadic approaches to understanding body movements in social contexts.
... The ability to form and stay in couples is underpinned by a triad of love-related states: sexual desire, romantic love and companionate love (Aron et al. 2005;Feldman 2017;Acevedo et al. 2012). Combined, these characteristics define our common understanding of what a couple is. ...
Human evolutionary demography is an emerging field blending natural science with social science. This edited volume provides a much-needed, interdisciplinary introduction to the field and highlights cutting-edge research for interested readers and researchers in demography, the evolutionary behavioural sciences, biology, and related disciplines.
By bridging the boundaries between social and biological sciences, the volume stresses the importance of a unified understanding of both in order to grasp past and current demographic patterns. Demographic traits, and traits related to demographic outcomes, including fertility and mortality rates, marriage, parental care, menopause, and cooperative behavior are subject to evolutionary processes. Bringing an understanding of evolution into demography therefore incorporates valuable insights into this field; just as knowledge of demography is key to understanding evolutionary processes. By asking questions about old patterns from a new perspective, the volume—composed of contributions from established and early-career academics—demonstrates that a combination of social science research and evolutionary theory offers holistic understandings and approaches that benefit both fields.
Human Evolutionary Demography introduces an emerging field in an accessible style. It is suitable for graduate courses in demography, as well as upper-level undergraduates. Its range of research is sure to be of interest to academics working on demographic topics (anthropologists, sociologists, demographers), natural scientists working on evolutionary processes, and disciplines which cross-cut natural and social science, such as evolutionary psychology, human behavioral ecology, cultural evolution, and evolutionary medicine. As an accessible introduction, it should interest readers whether or not they are currently familiar with human evolutionary demography.
Human society is organized in structured social networks upon which large-scale cooperation among genetically unrelated individuals is favored and persists. Such large-scale cooperation is crucial for the success of the human species but also one of the most puzzling challenges. Recent work in social and behavioral neuroscience has linked human cooperation to oxytocin, an evolutionarily ancient and structurally preserved hypothalamic neuropeptide. This review aims to elucidate how oxytocin promotes nonkin cooperation in social networks by reviewing its effects at three distinct levels: individual cooperation, the formation of interpersonal relationships, and the establishment of heterogeneous network structures. We propose oxytocin as a proximate mechanism for fostering large-scale cooperation in human societies. Specifically, oxytocin plays an important role in facilitating network-wide cooperation in human societies by 1) increasing individual cooperation, mitigating noncooperation motives, and facilitating the enforcement of cooperative norms; 2) fostering interpersonal bonding and synchronization; and 3) facilitating the formation of heterogeneous network structures.
Early-life social behaviors impact an organisms further physical, socioemotional and cognitive development profoundly. In all mammalian species the mother is a central interaction partner. Disruptions in early-life mother-infant interactions have been associated with an increased risk for physical, socioemotional and cognitive development. Therefore, preclinical research is necessary to better understand underlying neural mechanisms involved in healthy and abnormal sociocommunicative development. However, establishing valid and reproducible research findings requires precise and accurate assessment tools.
The Pup Retrieval test (PRT) is the leading behavioral assay to assess the maternal behavioral response to infant isolation distress in laboratory rodents. The PRT quantifies maternal behavior of a dam by the time it needs to approach, find and carry back an isolated pup. Despite the effectiveness and usefulness of the PRT, sampling procedures are currently lab and even researcher dependent, and test output is rather limited. In this project, we developed novel phenotypes for assessment of early-life bidirectional development based on the PRT.
First, we focused on extending the level of behavioral analysis and improving test accuracy, reliability and reproducibility. Using open-access deep neural networks and machine learning technology we developed an automated procedure which is able to accurately and reliably estimate the classic PRT parameters automatically. Additionally, we extended this to quantify ethologically relevant components of maternal retrieval behavior such as maternal approach and carrying.
Second, the automated PRT was used as basis for a novel behavioral test assay: BAMBI. BAMBI is the first behavioral test assay to assess early-life bidirectionality in mother-pup dyads in mice. In contrast to existing behavioral paradigms, BAMBI simultaneously records pup isolation vocalizations and maternal behaviors to investigate the action-reaction dynamic between them. This is particularly important in preclinical research of rodent models of disorders with early-life communication deficits such as autism spectrum disorders since infant and/or maternal factors might underlie and ameliorate infant social deficits. In our experiments, for example, we showed a significant association between number of ultrasonic vocalizations of an infant during PRT and retrieval success.
Finally, we applied this early-life methodology to the prenatal valproate exposure mouse model, an established model for autism spectrum disorder (ASD). Here, we administered THIQ, a potent and selective melanocortin-4 receptor agonist, in both male and female neonates to profile its impact on early-life and adult ASD-like behaviors. We were able to show differences between treatment groups in early-life social interactions with their mother as well as long lasting behavioral alterations.
In this chapter, psychoneuroendocrinology is defined and explained, and the relevance of this scientific discipline for psychosocial and psychotherapeutic practice is made clear. The interactions between psyche, neurobiology, endocrinology, and the autonomic nervous system are demonstrated, and the enormous importance of hormones for the human psyche is made understandable. This chapter makes it clear that human behavior becomes more explainable through an increasing willingness for interdisciplinary considerations and that research benefits when various disciplines engage in interdisciplinary exchange. Therefore, several sciences are also illuminated, and disciplines relevant to this topic are explained, such as (behavioral) genetics, psychoneuroimmunology, and chronobiology. Furthermore, mental illnesses are presented in which findings from psychoneuroendocrinology are of particular relevance. Additionally, nutrition is discussed, specifically which co-factors and precursors are needed to promote the synthesis of the so-called “happiness hormones.” Ultimately, it becomes clear how the findings of psychoneuroendocrinology can be transferred into psychosocial and psychotherapeutic practice.
Caring for a person with dementia (PWD) can produce declines in caregivers’ emotional well-being and physical functioning, which could result from disruptions in the emotional linkage between PWDs and caregivers. We examined the effects of interpersonal linkage in emotional behaviors on emotional well-being and physical functioning in caregivers and control partners. Forty-five PWD–caregiver dyads and 12 control dyads had a 10-min unrehearsed conflict conversation in the laboratory. We quantified positive and negative emotional linkage as the covariation between objectively coded positive and negative emotional behaviors during the conversation. Caregivers and one partner in the control dyads completed questionnaires concerning their emotional well-being and physical functioning. We found that lower positive emotional linkage was associated with lower emotional well-being in caregivers and control partners. We did not find similar effects with negative emotional linkage or for physical functioning. We offer possible explanations for these findings and implications for assessing caregiver risk.
Introduction
Intimate domestic violence causes psychological consequences in pregnancy and maternal competency. We aimed to assess the effect of domestic violence on mental health and maternal competency with the moderating role of mother-infant attachment behavior.
Methods
This prospective longitudinal study was conducted on 254 primiparous mothers in the third trimester of pregnancy referring to selected health centers in Qazvin province, Iran. Data collection tools were questionnaires. Data were analyzed by SPSS and Smart Partial Lease Square3 software.
Results
The results of the structural equations model showed that domestic violence has a positive and significant effect on mental health disorders (β = 0.87). Mental health disorder has a negative and significant effect on parental acceptance (β = -0.55). Domestic violence has a negative and significant effect on mother-infant attachment behavior (β = -0.83), also mother-infant attachment behavior is a moderator of the relationship between pregnancy violence and maternal competency (T-value = 3.17).
Conclusion
The results revealed that domestic violence during pregnancy affects the mental health of pregnant mothers and maternal competency and mother-infant attachment behavior moderates this relationship. Therefore, it is recommended that mothers facing domestic violence be identified and receive psychological support and counseling, and also improve maternal competence and mother-infant attachment behavior in mothers exposed to violence.
According to the Learning Theory of Attachment, neuroendocrinological processes affect the association between parental support and change in attachment. The current study aimed to test this assumption for oxytocin (OT) given its role in social behavior. We conducted a three-wave longitudinal study in which 91 children (56% girls, M age = 9.55, SD age = 0.63) participated. Change in attachment was assessed from Wave 1 to Wave 3 and was indexed by measuring trust in maternal support and Secure Base Script (SBS) knowledge. Measures of salivary child OT and parental support (child and mother report) were obtained during respectively the first and last wave. Results indicated that child-reported parental support was positively related to change in trust and more so for children with high OT levels. No (moderation) effects were found for SBS knowledge. Overall, these findings illustrate the importance of considering biological factors along with experienced parenting to explain differences in attachment.
Dominant theoretical accounts of interpersonal synchrony, the temporal coordination of biobehavioral processes between several individuals, have employed a linear approach, generally considering synchrony as a positive state, and utilizing aggregate scores. However, synchrony is known to take on a dynamical form with continuous shifts in its timeline. Acting as one continuously, is not always the optimal state, due to an intrinsic tension between individualistic and synergistic forms of action that exist in many social situations. We propose an alternative theory of flexible multimodal synchrony which highlights context as a key component that defines “pulls” toward synchrony and “pulls” toward segregation inherent to the social situation. Traitlike individual differences and relationship variables then sensitize individuals to these contextual “pulls.” In this manner, context, individual differences, and relationship variables provide the backdrop to the emergence of flexible and dynamical synchrony patterns, which we consider adaptive, in several modalities—behavioral, physiological, and neural. We point to three consequences of synchrony patterns: social-, task, and self-oriented. We discuss multimodal associations that arise in different contexts considering the theory and delineate hypotheses that emanate from the theory. We then provide two empirical proofs-of-concept: First, we show how individual differences modulate the effect of context on synchrony’s outcomes in a novel dyadic motor game. Second, we reanalyze previously reported data, to show how a “flexibility” approach to synchrony data analysis improves predictive ability when testing for synchrony’s effects on social cohesion. We provide ways to standardize the characterization of context and guidelines for future synchrony research.
Some but not other studies on oxytocin for schizophrenia, particularly those using a higher dose, indicate that oxytocin improves negative symptoms of schizophrenia. We performed an add-on randomized controlled trial to examine the effect of high-dose oxytocin, social skills training, and their combination in the treatment of negative symptoms and social dysfunction in schizophrenia. Fifty-one subjects with schizophrenia were randomized, employing a two-by-two design: intranasal oxytocin (24 IU X3/day) or placebo, and social skills training or supportive psychotherapy, for 3 weeks. The primary outcome was the difference in the total score from baseline to end-of-study of a semi-structured interview which assessed patients’ social interactions in 3 scenarios: sharing a positive experience, sharing a conflict, and giving support when the experimenter shared a conflict. The interactions were scored using the Coding Interactive Behavior Manual (CIB), clinical symptoms were assessed with the Positive and Negative Syndrome Scale (PANSS). No significant difference was found between groups in the total CIB or PANSS scores. The majority of comparisons in the different social interactions between oxytocin and placebo, and between social skills training vs supportive psychotherapy, were also nonsignificant. Social skills training reduced blunted affect and gaze. In post-hoc analyses of the support interaction, oxytocin improved synchrony and decreased tension, while in the positive interaction it improved positive affect and avoidance. None of these findings remained significant when controlling for multiple comparisons. In conclusion, oxytocin did not influence participants’ social behavior, and was not effective in improving the symptoms of schizophrenia.
Clinicaltrials.gov Identifier: NCT01598623
The term ‘Perinatal’ incorporates pregnancy, birth and the postnatal period. The perinatal period is a milestone event in both the individual and familial life cycle, an experience shared by the wider social network and community. Yet, it can be a period where the impact of pre-existing and emerging mental health problems during this time could necessitate specialist Perinatal Mental Health Services (PMHS) support via the NHS. COVID-19 pandemic is considered to have exacerbated the adversity for Perinatal Mental Health (PMH), yet questions on the lived experience remain unanswered.
Interviews with expectant and new mothers were analysed using Reflexive Thematic Analysis (RTA) establishing themes of 1- Perinatal Medical Care during COVID-19 Pandemic, 2- Becoming a Parent within social isolation, iii- Managing the Perinatal Period with the Support of Perintal Mental Health Services (PMHS) and iv- Parenthood beyond the COVID-19 Pandemic.
Findings indicated that the COVID-19 Pandemic caused concerns and worries amongst pregnant, birthing, and post-partum women and that diminished opportunities for social support during the perinatal period created an adverse mental health impact upon them. Overall, COVID-19 appears to have a ripple effect on women and their families experiencing the perinatal period during COVID-19. Although participants largely did not link their poor mental well-being during the perinatal period to the COVID-19 Pandemic, they attributed the causes of their poorer experiences to the COVID-19 Pandemic, identifying the pandemic as contributor to their heightened perinatal mental distress and at times as sole cause for their referral to Perinatal Mental Health Services.
The research aim of this study is to understand the relationship between parental emotional well-being and child outcome. This study delves into the profound impact of 5Q parental education on children's emotional well-being through the intricate process of healing the inner child among parents. The 5Q framework, encompassing Intelligence Quotient (IQ), Emotional Quotient (EQ), Adversity Quotient (AQ), Social Quotient (SQ), and the innovative "You Quotient" (UQ), serves as the cornerstone of this transformative educational program. By intertwining principles of personal growth, self-awareness, and effective communication, the 5Q approach aims to empower parents to navigate the complex landscape of parenthood with confidence and competence. Central to this study is the concept of the inner child, deeply rooted in psychological theory, which symbolizes unresolved emotions and experiences from childhood that continue to influence adult behaviours and familial dynamics. Through a qualitative research methodology, this study rigorously examines the experiences of a diverse sample of 100 participants engaged in a comprehensive 6-month 5Q parental education program. Results from the qualitative analysis revealed a profound impact of the 5Q parental education program on participants' emotional well-being and parenting practices. An overwhelming majority of 82 out of 100 participants reported significant enhancements in their emotional intelligence (EQ) following the healing of their inner child. This transformation was characterized by heightened self-awareness, improved emotional regulation, improved parenting skills and strategies, strengthened parent-child relationship that foster suitability relationship. This study underscores the transformative potential of 5Q parental education in fostering nurturing family environments conducive to holistic child development. The understanding of the relationship between parental emotional well-being and child outcome is emphasized. By addressing the emotional needs of parents and facilitating the healing of their inner child, this program not only empowers individuals but also lays the foundation for resilient, empathetic, and emotionally intelligent generations to come, laying the foundation for their optimal development.
Using functional near‐infrared spectroscopy (fNIRS) hyperscanning methodology, this study investigated whether parent emotional support moderated the relation between parent–child interbrain synchrony and interaction quality (via behavioral observation and child‐report), controlling for individual emotional distress. Eighty‐eight parent–child dyads (96.6% Han ethnicity), including a school‐age child between the ages of 6 and 11 ( M age = 8.07 years, SD = 1.16 years; 58.0% boys) and their parent ( M age = 39.03 years, SD = 3.54 years; 69.3% mothers), participated in a cooperative task during which brain activity was assessed. Cluster‐based permutations indicated parent–child interbrain synchrony in the left and right temporoparietal junction (TPJ). Interbrain synchrony in the left TPJ positively related to parent–child interaction quality in the context of high parent emotional support, whereas the association was weaker and negative when parents demonstrated low emotional support. Findings suggest the emotional context of an interaction is critical when assessing interbrain synchrony.
What does it mean to become attached? Three longitudinal studies established the empirical basis for the existing four-phase model of attachment formation, a model that has remained unmodified and unexamined for over half a century. In this paper, I revisit the research questions, methods, and findings from the seminal studies to reevaluate the current model. The evidence indicates two distinct definitions of attachment onset. In the first two phases of the model, becoming attached is defined by changes in within-subject behaviors leading to the selection of a discriminated figure. Defined this way, attachment onset is analogous to how bond formation is currently defined in other mammals and how imprinting is understood in birds. In contrast, the third and fourth phases of the model define attachment onset by forming a goal-corrected relationship. This second definition is human-centric and relies on secure base behavior as the signature criterion, the same criteria used to classify secure and insecure patterns of attachment. I argue for a narrower definition of attachment by removing goal-corrected behavior as a criterion and focusing on the normative process of selection. In addition, I integrate contemporary work on pair bonding in humans and other animals to propose new avenues for conceptualizing and studying attachment formation in infancy and beyond in filial and sexual bonds.
From cradle to grave, human behaviour is greatly influenced by our emotional attachments to other people, animals, objects, places, and ideologies. In this volume, “Archaeologies of Attachment”, we seek to explore new approaches in archaeological thought to study these bonds from the Palaeolithic to the recent past. This introduction provides a basic overview of attachment, considers attachment as a more general explanatory concept for social bonds, and offers a short introduction into the rest of the chapters contained within.
Feelings of love are among the most significant human phenomena. Love informs the formation and maintenance of pair bonds, parent-offspring attachments, and influences relationships with others and even nature. However, little is known about the neural mechanisms of love beyond romantic and maternal types. Here, we characterize the brain areas involved in love for six different objects: romantic partner, one’s children, friends, strangers, pets, and nature. We used functional magnetic resonance imaging (fMRI) to measure brain activity, while we induced feelings of love using short stories. Our results show that neural activity during a feeling of love depends on its object. Interpersonal love recruited social cognition brain areas in the temporoparietal junction and midline structures significantly more than love for pets or nature. In pet owners, love for pets activated these same regions significantly more than in participants without pets. Love in closer affiliative bonds was associated with significantly stronger and more widespread activation in the brain’s reward system than love for strangers, pets, or nature. We suggest that the experience of love is shaped by both biological and cultural factors, originating from fundamental neurobiological mechanisms of attachment.
There is growing interest in understanding how sexual arousal unfolds between partners, and how this may change over the course of a relationship and in the face of sexual distress. To capture the variable, dynamic, and dyadic nature of sexual responding, this paper introduces the concept of sexual synchrony, defined as the temporal, reciprocal, and coordinated interchange between partners' subjective and genital sexual arousal. Sexual synchrony is a key mechanism for understanding how partners experience and adapt their sexual arousal responses as they evolve over time. Its relevance lies in examining the mechanisms that may disrupt and facilitate synchrony and exploring how it may contribute to sexual well-being by enabling partners to mutually regulate their sexual arousal within and across sexual interactions. The paper also discusses how sexual synchrony may evolve throughout relationship development and its potential role in sexual problems, offering valuable insights into improving sexual relationships. Suggestions are provided for future research, together with a discussion of the methodological and statistical issues involved when examining sexual dynamics. Understanding how partners jointly regulate their sexual responses allows the development of dyadic models of sexual arousal which will inform treatments for improving couples' (sexual) well-being. The study of sexual synchrony also exemplifies the importance of translational research that is relevant across disciplinary borders.
Work aimed at characterizing the biological bases of autism has revealed a multiplicity of neural and genetic factors potentially associated with the condition. Combining information from multiple modalities and focusing on a specific, more homogenous subpopulation within the spectrum will help to parse this heterogeneity. In this chapter, we first briefly review major findings regarding the neural and genetic bases of autism broadly speaking, as well as a leading theory related to the etiology of autism, specifically in persons assigned female at birth (the “female protective effect” hypothesis). Thereafter, we discuss existing literature (N = 14 studies identified via systematic review) addressing the intersection of genetic and neural factors in the emergence and expression of autism in individuals assigned female at birth. These reports implicate sex differences in striatal, oxytocinergic, and neuroimmune systems, but further research in independent cohorts is needed to replicate and extend these findings. To conclude, we briefly review ethical considerations related to autism neurogenetic work, particularly concerns raised within the autism community, and provide recommendations for neurogenetic researchers.
Introduction: Breastfeeding is a fundamental biological function in mammals, allowing the progeny to develop in a physiological way. A physical and emotional dialog between mothers and offspring during breastfeeding has been described as part of the attachment relationship, and a synchronicity between maternal and neonatal brains can be hypothesized. This study aimed to assess if neonatal and maternal cortical areas activated during breastfeeding are functionally synchronized since the second day of life. Materials and Methods: Twenty mothers and their term newborns were enrolled. Cortical activation during breastfeeding was identified by multichannel near-infrared spectroscopy, which detects changes in haemoglobin concentration from multiple cortical regions. Functional activity was simultaneously detected (hyperscanning) in mothers and newborns' frontal and motor/primary somatosensory cortical areas during the first 5 minutes of breastfeeding. Cluster analysis and Student's t test were used to detect oxygenated haemoglobin increase, as cortical activation estimate. Wavelet transform coherence (WTC) analysis was used to identify a possible synchronization between maternal and neonatal activated cortical regions. Results: Mothers showed an activation of the central motor/primary somatosensory cortex, above the sagittal fissure. In newborns, the bilateral frontal cortex was activated. WTC analysis revealed two different cyclical synchronizations between mothers and infants' activated cortical regions. Conclusions: Such evidence may reflect a very early common sharing of experiences, possibly associated with reciprocal dynamic motor adjustments, hormonal coregulation, and somatic stimulations and sensations. The observed cyclical neural synchronization, between the mother and her newborn's cortex during breastfeeding, may play an important role in promoting their bonding.
Endocrine synchronization is a biological process often associated with social bonding. The mechanisms that mediate this process have been well studied in many vertebrate clades with evolved complex social behaviors. However, studies focusing on such processes in the less neurologically complex teleost clade are surprisingly lacking. In this study, we investigated the hypothesis that mated pairs of convict cichlids (Amatitlania nigrofasciata) perform cortisol synchronization and that the disruption of this might accompany pair-bond instability. Mated pairs were subjected to both behavioral and non-invasive waterborne hormonal assays to better understand the biological complexity of endocrine synchrony and its role in pair-bonding. Baseline cortisol assays indicated a positive correlation between male and female cortisol levels. Individuals that were subjected to a prolonged separation from their mate exhibited a negative correlation in cortisol synchrony after being reunited with their mate. Cortisol synchrony was disrupted, but pairs did not show a significant variance of intrapair aggression after initial pair reunion. However, more than half of the pairs that received the stressor exhibited significantly higher levels of intrapair aggression than their time matched controls approximately 1–7 days following this reunion, indicating pair-dissolution. Concurrently, pairs who underwent the stressor but maintained their bonds did not display an increase in intrapair aggression and also re-synchronized their cortisol levels. Not only does this study provide crucial insights in regard to the role of cortisol synchrony in serially monogamous systems, but it also suggests that the mechanisms that mediate the synchronization of endocrine through the formation of social bonds are more evolutionarily conserved than originally thought.
Previous fMRI research found increased brain responses in men with pedophilic interest to non-sexual pictures of child and animal faces. This raised the question of whether an aberrant nurturing system could be linked to pedophilia. To further explore this hypothesis, 20 pedohebephilic and 23 teleiophilic men performed a target detection task with adult versus infant human and animal faces, which measured selective attention towards the baby schema by comparing reaction times to infant versus adult targets that were presented amongst distractors of the other category. Since the response to baby schema can be influenced by steroid hormones, saliva samples were additionally collected to determine endogenous testosterone, progesterone, estradiol and cortisol. Contrary to expectations, all men did not react faster to infant than adult faces. Yet, pedohebephilic men were more distracted by infant’s faces than teleiophilic men. Pedohebephilic men with higher testosterone were faster in orienting attention to infant targets in the context of adult distractors. This association was not observed in teleiophilic men. Our results support the idea of an overactive nurturing system in pedophilia, which may be influenced by the endogenous testosterone level.
Hyperscanning – the monitoring of brain activity of two or more people simultaneously – has emerged to be a popular tool for assessing neural features of social interaction. This perspective article focuses on hyperscanning studies that use functional near-infrared spectroscopy (fNIRS), a technique that is very conducive to studies requiring naturalistic paradigms. In particular, we are interested in neural features that are related to social interaction deficits among individuals with autism spectrum disorders (ASD). This population has received relatively little attention in research using neuroimaging hyperscanning techniques, compared to neurotypical individuals. The study is outlined as follows. First, we summarize the findings about brain-behavior connections related to autism from previously published fNIRS hyperscanning studies. Then, we propose a preliminary theoretical framework of inter-brain coherence (IBC) with testable hypotheses concerning this population. Finally, we provide two examples of areas of inquiry in which studies could be particularly relevant for social- emotional/behavioral development for autistic children, focusing on intergenerational relationships in family units and learning in classroom settings in mainstream schools.
The cross-generational transmission of mammalian sociality, initiated by the parent’s postpartum brain plasticity and species-typical behavior that buttress offspring’s socialization, has not been studied in humans. In this longitudinal study, we measured brain response of 45 primary-caregiving parents to their infant’s stimuli, observed parent-infant
Interactions
, and assayed parental oxytocin (OT). Intra- and inter-network connectivity were computed in three main networks of the human parental brain: core limbic, embodied simulation, and mentalizing. During preschool, two key child social competencies were observed: emotion regulation and socialization.
Parent’s network integrity in infancy predicted preschoolers’ social outcomes, with subcortical and cortical network integrity foreshadowing simple evolutionary-based regulatory tactics versus complex self-regulatory strategies and advanced socialization
. Parent-infant synchrony mediated the links between connectivity of the parent’s embodied simulation network and preschoolers’ ability to use cognitive/executive emotion regulation strategies, highlighting the inherently dyadic nature of this network and its long-term effects on tuning young to social life. Parent’s inter-network core limbic-embodied simulation connectivity predicted children’s OT as moderated by parental OT. Findings challenge solipsistic neuroscience perspectives by demonstrating how the parent-offspring interface enables the brain of one human to profoundly impact long-term adaptation of another.
Enduring social bonds play an essential role in human society. These bonds positively affect psychological, physiological, and behavioral functions. Here, we review the recent literature on the neurobiology, particularly the role of oxytocin and dopamine, of pair bond formation, bond disruption, and social buffering effects on stress responses, from studies utilizing the socially monogamous prairie vole (Microtus ochrogaster).
Although children's social development is embedded in social interaction, most developmental neuroscience studies have examined
responses to non-interactive social stimuli (e.g., photographs of faces). The neural mechanisms of real-world social behavior
are of special interest during middle childhood (roughly ages 7-13), a time of increased social complexity and competence
coinciding with structural and functional social brain development. Evidence from adult neuroscience studies suggests that
social interaction may alter neural processing, but no neuroimaging studies in children have directly examined the effects
of live social-interactive context on social cognition. In the current study of middle childhood, we compare the processing
of two types of speech: speech that children believed was presented over a real-time audio-feed by a social partner and speech
that they believed was recorded. Although in reality all speech was prerecorded, perceived live speech resulted in significantly
greater neural activation in regions associated with social cognitive processing. These findings underscore the importance
of using ecologically-valid and interactive methods to understand the developing social brain.
When people observe one another, behavioural alignment can be detected at many levels, from the physical to the mental. Likewise, when people process the same highly complex stimulus sequences, such as films and stories, alignment is detected in the elicited brain activity. In early sensory areas, shared neural patterns are coupled to the low-level properties of the stimulus (shape, motion, volume, etc.), while in high-order brain areas, shared neural patterns are coupled to high-levels aspects of the stimulus, such as meaning. Successful social interactions require such alignments (both behavioural and neural), as communication cannot occur without shared understanding. However, we need to go beyond simple, symmetric (mirror) alignment once we start interacting. Interactions are dynamic processes, which involve continuous mutual adaptation, development of complementary behaviour and division of labour such as leader–follower roles. Here, we argue that interacting individuals are dynamically coupled rather than simply aligned. This broader framework for understanding interactions can encompass both processes by which behaviour and brain activity mirror each other (neural alignment), and situations in which behaviour and brain activity in one participant are coupled (but not mirrored) to the dynamics in the other participant. To apply these more sophisticated accounts of social interactions to the study of the underlying neural processes we need to develop new experimental paradigms and novel methods of data analysis.
Unlabelled:
Initiating a reward-seeking behavior involves deciding on an action, how fast to initiate the action (initiation vigor), as well as how much effort to exert. These processes are thought to involve the mesolimbic dopamine system. Dopamine levels in the ventral striatum rise before initiating a reliably reinforced behavior. However, it is unknown whether dopamine is similarly involved with unreinforced actions (inactive lever presses, premature food port entries, insufficient number of active lever presses). Furthermore, does the dopamine response when initiating an action reflect specific aspects of motivated behavior, such as initiation vigor and exerted effort? Here, we analyzed voltammetry recordings of dopamine levels in the nucleus accumbens (NAcc) core and shell in rats working for food under a progressive ratio reinforcement schedule. We examined dopamine levels when rats initiated distinct actions (active lever presses, inactive lever presses, food port entries) that were temporally separated from cue- and reward-evoked dopamine release. Active lever pressing bouts were preceded by elevated dopamine release in the NAcc shell, as well as in the NAcc core, although only when rats exhibited high initiation vigor. Dopamine levels were transiently reduced in the NAcc core following an unreinforced food port entry and were unchanged throughout the NAcc when initiating inactive lever presses. The effort exerted and vigor to initiate a bout of active lever presses were signaled by dopamine transmission in the NAcc core, but not in the NAcc shell. These results demonstrate that the dopamine response when initiating a behavior is both region- and action-specific.
Significance statement:
Exogenous activation of the mesolimbic dopamine system facilitates motivated behavior. However, a direct relationship has not been established between endogenous phasic dopamine transmission and measures of motivation, such as the vigor to initiate an action and the effort exerted in a bout of activity. The present work demonstrates that the dopamine response when initiating an action depends both upon where dopamine is released and what action is performed. Furthermore, dopamine reflects measures of motivated behavior selectively within the nucleus accumbens core.
Besides their fundamental movement function evidenced by Parkinsonian deficits, the basal ganglia are involved in processing closely linked non-motor, cognitive and reward information. This review describes the reward functions of three brain structures that are major components of the basal ganglia or are closely associated with the basal ganglia, namely midbrain dopamine neurons, pedunculopontine nucleus, and striatum (caudate nucleus, putamen, nucleus accumbens). Rewards are involved in learning (positive reinforcement), approach behavior, economic choices and positive emotions. The response of dopamine neurons to rewards consists of an early detection component and a subsequent reward component that reflects a prediction error in economic utility, but is unrelated to movement. Dopamine activations to non-rewarded or aversive stimuli reflect physical impact, but not punishment. Neurons in pedunculopontine nucleus project their axons to dopamine neurons and process sensory stimuli, movements and rewards and reward-predicting stimuli without coding outright reward prediction errors. Neurons in striatum, besides their pronounced movement relationships, process rewards irrespective of sensory and motor aspects, integrate reward information into movement activity, code the reward value of individual actions, change their reward-related activity during learning, and code own reward in social situations depending on whose action produces the reward. These data demonstrate a variety of well-characterized reward processes in specific basal ganglia nuclei consistent with an important function in non-motor aspects of motivated behavior.
Significance
The subcortical striatum is critical for the planning and execution of motor behavior, and its dysfunction is associated with disorders such as Parkinson’s disease. More recently, the human striatum has also been reported to be involved in heterogeneous nonmotor psychological functions. However, detailed functional mappings of human psychological processes to striatal regions have been bound by theoretical and methodological limitations, including a strong focus on experimental paradigms derived from animal research, and the tendency to infer function from anatomical connectivity, rather than task-related activation. To overcome these limitations, we used a large-scale, unbiased, data-driven approach, and generated a precise, comprehensive functional map, directly associating striatal zones with the broadest range of psychological processes to date.
Information in neurons flows from synapses, through the dendrites
and cell body (soma), and, finally, along the axon as spikes
of electrical activity that will ultimately release neurotransmitters
from the nerve terminals. However, the dendrites of many
neurons also have a secretory role, transmitting information
back to afferent nerve terminals1–4. In some central nervous
system neurons, spikes that originate at the soma can travel
along dendrites as well as axons, and may thus elicit secretion
from both compartments1. Here, we show that in hypothalamic
oxytocin neurons, agents that mobilize intracellular Ca21 induce
oxytocin release from dendrites without increasing the electrical
activity of the cell body, and without inducing secretion from the
nerve terminals. Conversely, electrical activity in the cell bodies
can cause the secretion of oxytocin from nerve terminals with
little or no release from the dendrites. Finally, mobilization of
intracellular Ca21 can also prime the releasable pool of oxytocin
in the dendrites. This priming action makes dendritic oxytocin
available for release in response to subsequent spike activity.
Priming persists for a prolonged period, changing the nature of
interactions between oxytocin neurons and their neighbours.
Loss of a partner can have severe effects on mental health. Here we explore the neural mechanisms underlying increased passive stress-coping, indicative of depressive-like behavior, following the loss of the female partner in the monogamous male prairie vole. We demonstrate that corticotropin-releasing factor receptor 2 (CRFR2) in the nucleus accumbens shell mediates social loss-induced passive coping. Further, we show that partner loss compromises the oxytocin system through multiple mechanisms. Finally, we provide evidence for an interaction of the CRFR2 and oxytocin systems in mediating the emotional consequences of partner loss. Our results suggest that chronic activation of CRFR2 and suppression of striatal oxytocin signaling following partner loss result in an aversive emotional state that may share underlying mechanisms with bereavement. We propose that the suppression of oxytocin signaling is likely adaptive during short separations to encourage reunion with the partner and may have evolved to maintain long-term partnerships. Additionally, therapeutic strategies targeting these systems should be considered for treatment of social loss-mediated depression.
Functional neuroimaging studies have suggested the existence of 2 largely distinct social cognition networks, one for theory of mind (taking others' cognitive perspective) and another for empathy (sharing others' affective states). To address whether these networks can also be dissociated at the level of brain structure, we combined behavioral phenotyping across multiple socio-cognitive tasks with 3-Tesla MRI cortical thickness and structural covariance analysis in 270 healthy adults, recruited across 2 sites. Regional thickness mapping only provided partial support for divergent substrates, highlighting that individual differences in empathy relate to left insular-opercular thickness while no correlation between thickness and mentalizing scores was found. Conversely, structural covariance analysis showed clearly divergent network modulations by socio-cognitive and -affective phenotypes. Specifically, individual differences in theory of mind related to structural integration between temporo-parietal and dorsomedial prefrontal regions while empathy modulated the strength of dorsal anterior insula networks. Findings were robust across both recruitment sites, suggesting generalizability. At the level of structural network embedding, our study provides a double dissociation between empathy and mentalizing. Moreover, our findings suggest that structural substrates of higher-order social cognition are reflected rather in interregional networks than in the the local anatomical markup of specific regions per se.
People are embedded in social interaction that shapes their brains throughout lifetime. Instead of emerging from lower-level cognitive functions, social interaction could be the default mode via which humans communicate with their environment. Should this hypothesis be true, it would have profound implications on how we think about brain functions and how we dissect and simulate them. We suggest that the research on the brain basis of social cognition and interaction should move from passive spectator science to studies including engaged participants and simultaneous recordings from the brains of the interacting persons.
Genes and social experiences interact to create variation in social behavior and vulnerability to develop disorders of the social domain. Socially monogamous prairie voles display remarkable diversity in neuropeptide receptor systems and social behavior. Here, we examine the interaction of early-life adversity and brain oxytocin receptor (OTR) density on adult social attachment in female prairie voles. First, pups were isolated for 3 h per day, or unmanipulated, from postnatal day 1-14. Adult subjects were tested on the partner preference (PP) test to assess social attachment and OTR density in the brain was quantified. Neonatal social isolation impaired female PP formation, without affecting OTR density. Accumbal OTR density was, however, positively correlated with the percent of time spent huddling with the partner in neonatally isolated females. Females with high accumbal OTR binding were resilient to neonatal isolation. These results are consistent with the hypothesis that parental nurturing shapes neural systems underlying social relationships by enhancing striatal OTR signaling. Thus, we next determined whether early touch, mimicking parental licking and grooming, stimulates hypothalamic OT neuron activity. Tactile stimulation induced immediate-early gene activity in OT neurons in neonates. Finally, we investigated whether pharmacologically potentiating OT release using a melanocortin 3/4 agonist, melanotan-II (10 mg kg(-1) subcutaneously), would mitigate the social isolation-induced impairments in attachment behavior. Neonatal melanotan-II administration buffered against the effects of early isolation on partner preference formation. Thus, variation in accumbal OTR density and early OT release induced by parental nurturing may moderate susceptibility to early adverse experiences, including neglect.
Early mother-infant relationships play important roles in infants' optimal development. New mothers undergo neurobiological changes that support developing mother-infant relationships regardless of great individual differences in those relationships. In this article, we review the neural plasticity in human mothers' brains based on functional magnetic resonance imaging (fMRI) studies. First, we review the neural circuits that are involved in establishing and maintaining mother-infant relationships. Second, we discuss early postpartum factors (e.g., birth and feeding methods, hormones, and parental sensitivity) that are associated with individual differences in maternal brain neuroplasticity. Third, we discuss abnormal changes in the maternal brain related to psychopathology (i.e., postpartum depression, posttraumatic stress disorder, substance abuse) and potential brain remodeling associated with interventions. Last, we highlight potentially important future research directions to better understand normative changes in the maternal brain and risks for abnormal changes that may disrupt early mother-infant relationships.
Copyright © 2015. Published by Elsevier Inc.
The number of papers about the orbitofrontal cortex (OFC) has grown from 1 per month in 1987 to a current rate of over 50 per month. This publication stream has implicated the OFC in nearly every function known to cognitive neuroscience and in most neuropsychiatric diseases. However, new ideas about OFC function are typically based on limited data sets and often ignore or minimize competing ideas or contradictory findings. Yet true progress in our understanding of an area's function comes as much from invalidating existing ideas as proposing new ones. Here we consider the proposed roles for OFC, critically examining the level of support for these claims and highlighting the data that call them into question.
Human-like modes of communication, including mutual gaze, in dogs may have been acquired during domestication with humans. We show that gazing behavior from dogs, but not wolves, increased urinary oxytocin concentrations in owners, which consequently facilitated owners' affiliation and increased oxytocin concentration in dogs. Further, nasally administered oxytocin increased gazing behavior in dogs, which in turn increased urinary oxytocin concentrations in owners. These findings support the existence of an interspecies oxytocin-mediated positive loop facilitated and modulated by gazing, which may have supported the coevolution of human-dog bonding by engaging common modes of communicating social attachment.
Copyright © 2015, American Association for the Advancement of Science.
Nearly 40 years of research on the function of the nucleus accumbens (NAc) has provided a wealth of information on its contributions to behavior but has also yielded controversies and misconceptions regarding these functions. A primary tenet of this review is that, rather than serving as a "reward" center, the NAc plays a key role in action selection, integrating cognitive and affective information processed by frontal and temporal lobe regions to augment the efficiency and vigor of appetitively or aversively motivated behaviors. Its involvement in these functions is most prominent when the appropriate course of action is ambiguous, uncertain, laden with distractors, or in a state of flux. To this end, different subregions of the NAc play dissociable roles in refining action selection, promoting approach toward motivationally relevant stimuli, suppressing inappropriate actions so that goals may be obtained more efficiently, and encoding action outcomes that guide the direction of subsequent ones. Expected final online publication date for the Annual Review of Psychology Volume 66 is November 30, 2014. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
Social isolation has been recognized as a major risk factor for morbidity and mortality in humans for more than a quarter of a century. Although the focus of research has been on objective social roles and health behavior, the brain is the key organ for forming, monitoring, maintaining, repairing, and replacing salutary connections with others. Accordingly, population-based longitudinal research indicates that perceived social isolation (loneliness) is a risk factor for morbidity and mortality independent of objective social isolation and health behavior. Human and animal investigations of neuroendocrine stress mechanisms that may be involved suggest that (a) chronic social isolation increases the activation of the hypothalamic pituitary adrenocortical axis, and (b) these effects are more dependent on the disruption of a social bond between a significant pair than objective isolation per se. The relational factors and neuroendocrine, neurobiological, and genetic mechanisms that may contribute to the association between perceived isolation and mortality are reviewed. Expected final online publication date for the Annual Review of Psychology Volume 66 is November 30, 2014. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
Von Economo neurons (VENs) are a recently evolved cell type which may be involved in the fast intuitive assessment of complex situations. As such, they could be part of the circuitry supporting human social networks. We propose that the VENs relay an output of fronto-insular and anterior cingulate cortex to the parts of frontal and temporal cortex associated with theory-of-mind, where fast intuitions are melded with slower, deliberative judgments. The VENs emerge mainly after birth and increase in number until age 4 yrs. We propose that in autism spectrum disorders the VENs fail to develop normally, and that this failure might be partially responsible for the associated social disabilities that result from faulty intuition.
Significance
Intergroup conflicts are among the world’s most imminent problems, particularly with the shift of battlefields into the heart of civilian locations and the participation of increasingly younger adolescents in intergroup conflict. We found that Israeli and Palestinian adolescents reared in a climate of long-standing strife shut down the brain’s automatic response to outgroup pain. This neural modulation characterized a top-down process superimposed upon an automatic response to the pain of all and was sensitive to hostile behavior toward outgroup, uncompromising worldviews, and brain-to-brain synchrony among group members. Findings pinpoint adolescents’ sociocognitive top-down processes as targets for intervention.
Objective:
Exposure to maternal depression across the first years of life markedly increases children's susceptibility to psychopathology, yet no study has tested its effects on the maturation of children's social brain.
Method:
Using a birth cohort of mothers with no contextual risk (N = 1,983), families were followed at 7 time points from birth to 11 years and repeatedly assessed for maternal depression across the first 6 years to form 2 cohorts: mothers continuously depressed from birth to 6 years and controls without depression. At 11 years of age, children's (n = 72; depressed, n = 27; nondepressed, n = 45) brain response to others' pain was measured by magnetoencephalography.
Results:
Preadolescents displayed a unique oscillatory pattern with higher alpha power to pain versus no pain expressing as alpha rebound, not alpha suppression, at a late time window (1,100-1,300 ms post-stimulus) in the supplementary motor area. This suggests that top-down processing in areas of the pain matrix can underpin the maturation of vicarious empathy. Children of mothers with depression showed enhanced alpha rebound to pain in the right posterior superior temporal gyrus, which was unrelated to emotion detection abilities, pointing to decreased late processing of others' overwhelming experiences in socio-cognitive areas. Alpha power in the posterior superior temporal gyrus was predicted by higher maternal intrusiveness and lower synchrony across early childhood.
Conclusion:
These findings, from the first study to examine maternal depression and early caregiving as long-term predictors of children's neural empathic response, pinpoint a decrease in top-down socio-cognitive mechanisms as potential pathways for the cross-generational transfer of vulnerability from mothers with depression to their offspring and highlight the need for early interventions focused on enhancing maternal attunement.
Summary Oxytocin promotes social interactions and recognition of conspecifics that rely on olfaction in most species. The circuit mechanisms through which oxytocin modifies olfactory processing are incompletely understood. Here, we observed that optogenetically induced oxytocin release enhanced olfactory exploration and same-sex recognition of adult rats. Consistent with oxytocin’s function in the anterior olfactory cortex, particularly in social cue processing, region-selective receptor deletion impaired social recognition but left odor discrimination and recognition intact outside a social context. Oxytocin transiently increased the drive of the anterior olfactory cortex projecting to olfactory bulb interneurons. Cortical top-down recruitment of interneurons dynamically enhanced the inhibitory input to olfactory bulb projection neurons and increased the signal-to-noise of their output. In summary, oxytocin generates states for optimized information extraction in an early cortical top-down network that is required for social interactions with potential implications for sensory processing deficits in autism spectrum disorders.
In the extant literature examining the brain mechanisms implicated in pain perception, researchers have theorized that the overlapping responses to pain in the self and in others mark the human capacity for empathy. Here we investigated how prior exposure to extreme pain affects pain perception, by assessing the dynamics of pain processing in veterans who were previously exposed to severe injury. Forty-three participants (28 pain-exposed and 15 controls) underwent whole-head magnetoencephalography (MEG) while viewing photographs of limbs in painful and nonpainful (neutral) conditions. Among controls, an early (0-220 ms) "pain effect" in the posterior cingulate and sensorimotor cortices, and a later (760-900 ms) "pain effect" in the posterior cingulate cortex, superior temporal gyrus/insula, and fusiform gyrus were found, indicated by enhanced alpha suppression to the pain versus nonpain conditions. Importantly, pain-exposed participants exhibited an atypical pain response in the posterior cingulate cortex, indicated by a normative response to pain, but no pain-to-no-pain differentiation. This may suggest that individuals exposed to extreme pain may perceive neutral stimuli as potentially threatening. Our findings demonstrate alterations in pain perception following extreme pain exposure, chart the sequence from automatic to evaluative pain processing, and emphasize the importance of considering past experiences in studying the neural response to others' states.
Existing evidence suggests that interval timing, processing of temporal information in the hundredth of milliseconds-to-minutes range, recruits broad brain regions such as cortico-striatal circuits via dopaminergic–glutamatergic pathways. In this review, we summarize recent findings on the neurobiological basis of interval timing with a special focus on dopaminergic modulations of temporal information. Two properties of interval timing — accuracy and precision — are used to examine recent results from manipulations of dopaminergic signaling and the resulting distortions in temporal processing.
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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 4-6 months, new lovers who began a romantic relationship within the past 4 months, and non-attached singles. We measured plasma oxytocin (OT), beta endorphin (β-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 β-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 β-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.
The neurohormone oxytocin (OT) is positively involved in the regulation of parenting and social bonding in mammals, and may thus also be important for the mediation of alloparental care. In cooperatively breeding marmosets, infants are raised in teamwork by parents and adult and sub-adult non-reproductive helpers (usually older siblings). Despite high intrinsic motivation, which may be mediated by hormonal priming, not all individuals are always equally able to contribute to infant-care due to competition among care-takers. Among the various care-taking behaviors, proactive food sharing may reflect motivational levels best, since it can be performed ad libitum by several individuals even if competition among surplus care-takers constrains access to infants. Our aim was to study the link between urinary OT levels and care-taking behaviors in group-living marmosets, while taking affiliation with other adults and infant age into account. Over eight reproductive cycles, 26 individuals were monitored for urinary baseline OT, care-taking behaviors (baby-licking, -grooming, -carrying, and proactive food sharing), and adult-directed affiliation. Mean OT levels were generally highest in female breeders and OT increased significantly in all individuals after birth. During early infancy, high urinary OT levels were associated with increased infant-licking but low levels of adult-affiliation, and during late infancy, with increased proactive food sharing. Our results show that, in marmoset parents and alloparents, OT is positively involved in the regulation of care-taking, thereby reflecting the changing needs during infant development. This particularly included behaviors that are more likely to reflect intrinsic care motivation, suggesting a positive link between OT and motivational regulation of infant-care.
Let me comfort you
Consolation behavior promotes stress reduction of one by another. We know that consolation occurs in humans and apes. Burkett et al. observed that within a pair of monogamous prairie voles, an unstressed partner increased its grooming of a stressed partner. Furthermore, the unstressed partner matched the stressed partner in its stress hormone response. Thus, consolation may be more common than assumed in animals, and prairie voles may prove a useful model for understanding the physical and neural mechanisms underlying consolation behavior.
Science , this issue p. 375
Oxytocin (OT) is a deeply conserved nonapeptide that acts both peripherally and centrally to modulate reproductive physiology and sociosexual behavior across divergent taxa, including humans. In vertebrates, the distribution of the oxytocin receptor (OTR) in the brain is variable within and across species, and OTR signaling is critical for a variety of species-typical social and reproductive behaviors, including affiliative and pair bonding behaviors in multiple socially monogamous lineages of fishes, birds, and mammals. Early work in prairie voles suggested that the endogenous OT system modulates mating-induced partner preference formation in females but not males; however, there is significant evidence that central OTRs may modulate pair bonding behavior in both sexes. In addition, it remains unclear how transient windows of central OTR signaling during sociosexual interaction modulate neural activity to produce enduring shifts in sociobehavioral phenotypes, including the formation of selective social bonds. Here we re-examine the role of the central OT system in partner preference formation in male prairie voles using a selective OTR antagonist delivered intracranially. We then use the same antagonist to examine how central OTRs modulate behavior and immediate early gene (Fos) expression, a metric of neuronal activation, in males during brief sociosexual interaction with a female. Our results suggest that, as in females, OTR signaling is critical for partner preference formation in males and enhances correlated activation across sensory and reward processing brain areas during sociosexual interaction. These results are consistent with the hypothesis that central OTR signaling facilitates social bond formation by coordinating activity across a pair bonding neural network.
Emotions are powerful determinants of behaviour, thought and experience, and they may be regulated in various ways. Neuroimaging studies have implicated several brain regions in emotion regulation, including the ventral anterior cingulate and ventromedial prefrontal cortices, as well as the lateral prefrontal and parietal cortices. Drawing on computational approaches to value-based decision-making and reinforcement learning, we propose a unifying conceptual framework for understanding the neural bases of diverse forms of emotion regulation.
This article is part of a Special Issue "Parental Care". Research on the neurobiology of attachment, pioneered by scholars in the generation that followed the discovery of social bonding, examined the biological basis of mammalian parenting through systematic experiments in animal models and their application to theories on human attachment. This paper argues for the need to construct a theory on the neurobiology of human attachment that integrates findings in animal models with human neuroscience research to formulate concepts based on experimental, not only extrapolative data. Rosenblatt's (2003) three characteristics of mammalian parenting - rapid formation of attachment, behavioral synchrony, and mother-offspring attachment as basis of social organization - are used to guide discussion on mammalian general versus human-specific attributes of parental care. These highlight specific components of attachment in rodents, primates, and humans that chart the evolution from promiscuous, nest-bound, olfactory-based bonds to exclusive, multi-sensory, and representation-based attachments. Following, three continua are outlined in parental behavior, hormones, and brain, each detailing the evolution from rodents to humans. Parental behavior is defined as a process of trophallaxis - the reciprocal multisensory exchange that supports approach orientation and enables collaboration in social species - and includes human-specific features that enable behavioral synchrony independent of tactile contact. The oxytocin system incorporates conserved and human-specific components and is marked by pulsatile activity and dendritic release that reorganize neural networks on the basis of species-specific attachment experiences. Finally, the subcortical limbic circuit underpinning mammalian mothering extends in humans to include multiple cortical networks implicated in empathy, mentalizing, and emotion regulation that enable flexible, goal-directed caregiving. I conclude by presenting a philosophical continuum from Hobbes to Lorenz, which illustrates how research on the neurobiology of attachment can put in the forefront the social-collaborative elements in human nature and afford a new perspective on the mind-brain polarity.
I propose that synchronization affects communication between neuronal groups. Gamma-band (30-90 Hz) synchronization modulates excitation rapidly enough that it escapes the following inhibition and activates postsynaptic neurons effectively. Synchronization also ensures that a presynaptic activation pattern arrives at postsynaptic neurons in a temporally coordinated manner. At a postsynaptic neuron, multiple presynaptic groups converge, e.g., representing different stimuli. If a stimulus is selected by attention, its neuronal representation shows stronger and higher-frequency gamma-band synchronization. Thereby, the attended stimulus representation selectively entrains postsynaptic neurons. The entrainment creates sequences of short excitation and longer inhibition that are coordinated between pre- and postsynaptic groups to transmit the attended representation and shut out competing inputs. The predominantly bottom-up-directed gamma-band influences are controlled by predominantly top-down-directed alpha-beta-band (8-20 Hz) influences. Attention itself samples stimuli at a 7-8 Hz theta rhythm. Thus, several rhythms and their interplay render neuronal communication effective, precise, and selective.
What roles do mesolimbic and neostriatal dopamine systems play in reward? Do they mediate the hedonic impact of rewarding stimuli? Do they mediate hedonic reward learning and associative prediction? Our review of the literature, together with results of a new study of residual reward capacity after dopamine depletion, indicates the answer to both questions is 'no'. Rather, dopamine systems may mediate the incentive salience of rewards, modulating their motivational value in a manner separable from hedonia and reward learning. In a study of the consequences of dopamine loss, rats were depleted of dopamine in the nucleus accumbens and neostriatum by up to 99% using 6-hydroxydopamine. In a series of experiments, we applied the 'taste reactivity' measure of affective reactions (gapes, etc.) to assess the capacity of dopamine-depleted rats for: 1) normal affect (hedonic and aversive reactions), 2) modulation of hedonic affect by associative learning (taste aversion conditioning), and 3) hedonic enhancement of affect by non-dopaminergic pharmacological manipulation of palatability (benzodiazepine administration). We found normal hedonic reaction patterns to sucrose vs. quinine, normal learning of new hedonic stimulus values (a change in palatability based on predictive relations), and normal pharmacological hedonic enhancement of palatability. We discuss these results in the context of hypotheses and data concerning the role of dopamine in reward. We review neurochemical, electrophysiological, and other behavioral evidence. We conclude that dopamine systems are not needed either to mediate the hedonic pleasure of reinforcers or to mediate predictive associations involved in hedonic reward learning. We conclude instead that dopamine may be more important to incentive salience attributions to the neural representations of reward-related stimuli. Incentive salience, we suggest, is a distinct component of motivation and reward. In other words, dopamine systems are necessary for 'wanting' incentives, but not for 'liking' them or for learning new 'likes' and 'dislikes'.
Oxytocin (OT), a nonapeptide signaling molecule originating from an ancestral peptide, appears in different variants across all vertebrate and several invertebrate species. Throughout animal evolution, neuropeptidergic signaling has been adapted by organisms for regulating response to rapidly changing environments. The family of OT-like molecules affects both peripheral tissues implicated in reproduction, homeostasis, and energy balance, as well as neuromodulation of social behavior, stress regulation, and associative learning in species ranging from nematodes to humans. After describing the OT-signaling pathway, we review research on the three genes most extensively studied in humans: the OT receptor (OXTR), the structural gene for OT (OXT/neurophysin-I), and CD38. Consistent with the notion that sociality should be studied from the perspective of social life at the species level, we address human social functions in relation to OT-pathway genes, including parenting, empathy, and using social relationships to manage stress. We then describe associations between OT-pathway genes with psychopathologies involving social dysfunctions such as autism, depression, or schizophrenia. Human research particularly underscored the involvement of two OXTR single nucleotide polymorphisms (rs53576, rs2254298) with fewer studies focusing on other OXTR (rs7632287, rs1042778, rs2268494, rs2268490), OXT (rs2740210, rs4813627, rs4813625), and CD38 (rs3796863, rs6449197) single nucleotide polymorphisms. Overall, studies provide evidence for the involvement of OT-pathway genes in human social functions but also suggest that factors such as gender, culture, and early environment often confound attempts to replicate first findings. We conclude by discussing epigenetics, conceptual implications within an evolutionary perspective, and future directions, especially the need to refine phenotypes, carefully characterize early environments, and integrate observations of social behavior across ecological contexts.
An ever-growing body of evidence suggests that the hypothalamic neuropeptide oxytocin plays a central role in the regulation of mammalian social behavior and relationships. Yet, mammalian social interactions are extremely complex, involving both approach and avoidance behaviors toward specific individuals. While in the past oxytocin was conceived merely as a prosocial molecule that nonselectively facilitated affiliative emotions and behavior, it is now recognized that oxytocin plays a role in a wide range of social relationships, some of which involve negative emotions such as fear, aggression, and envy and lead to avoidance behavior. However, the way by which a single molecule such as oxytocin contributes to contrasting emotions and opposite behaviors is yet to be discovered. Here, we discuss the role of oxytocin in the modulation of emotional memories in rodents, focusing on two paradigms: social recognition and fear conditioning, representing approach and avoidance behaviors, respectively. We review recent pioneering studies that address the complex effects of oxytocin in a mechanistic approach, using genetic animal models and brain region-specific manipulations of oxytocin activity. These studies suggest that the multiple roles of oxytocin in social and fear behavior are due to its local effects in various brain areas, most notably distinct regions of the amygdala. Finally, we propose a model explaining some of the contradictory effects of oxytocin as products of the balance between two networks in the amygdala that are controlled by the medial prefrontal cortex.
Mother-infant bonding is a characteristic of virtually all mammals. The maternal neural system may have provided the scaffold upon which other types of social bonds in mammals have been built. For example, most mammals exhibit a polygamous mating system, but monogamy and pair bonding between mating partners occurs in ~5% of mammalian species. In mammals, it is plausible that the neural mechanisms that promote mother-infant bonding have been modified by natural selection to establish the capacity to develop a selective bond with a mate during the evolution of monogamous mating strategies. Here we compare the details of the neural mechanisms that promote mother-infant bonding in rats and other mammals with those that underpin pair bond formation in the monogamous prairie vole. Although details remain to be resolved, remarkable similarities and a few differences between the mechanisms underlying these two types of bond formation are revealed. For example, amygdala and nucleus accumbens-ventral pallidum (NA-VP) circuits are involved in both types of bond formation, and dopamine and oxytocin action within NA appears to promote the synaptic plasticity that allows either infant or mating partner stimuli to persistently activate NA-VP attraction circuits, leading to an enduring social attraction and bonding. Further, although the medial preoptic area is essential for maternal behavior, its role in pair bonding remains to be determined. Our review concludes by examining the broader implications of this comparative analysis, and evidence is provided that the maternal care system may have also provided the basic neural foundation for other types of strong social relationships, beyond pair bonding, in mammals, including humans.
Copyright © 2015. Published by Elsevier Inc.