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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.
... Early experiences with primary caregivers, particularly mothers, shape reward anticipation throughout life [17]. Specifically, maternal warmth and encouragement in childhood and adolescence is perceived as integral for developing healthy reward processing [18,19]. ...
... Furthermore, previous research has focused on monetary rewards, although for humans social stimuli, such as smiling faces and positive feedback during social interactions, are one of the most powerful incentives motivating behavior [43,44]. This is particularly relevant, as maternal antipathy more specifically shapes the formation of values and expectations of social reinforcers during development [17]. Thus, the question arises whether maternal antipathy may have a particularly strong association with social reward anticipation. ...
... Total scores range from 0 to 63 with higher scores indicating more severe depressive symptoms. Criteria have been proposed to interpret the total score as reflecting mild (14)(15)(16)(17)(18)(19), moderate (20-28), or severe (29-63) depression [60]. SSD symptomatology was measured with the Somatic Symptom Disorder-B-Criteria Scale [61], assessing the three psychological sub-criteria of SSD with four items each on a five-point Likert scale ranging from 0 (never) to 4 (very often). ...
Aberrant activation in the ventral striatum (VS) during reward anticipation may be a key mechanism linking adverse childhood experiences (ACE) to transdiagnostic psychopathology. This study aimed to elucidate whether retrospectively reported ACE, specifically maternal antipathy, relate to monetary and social reward anticipation in a transdiagnostic adult sample. A cross-sectional neuroimaging study was conducted in 118 participants with varying levels of ACE, including 25 participants with posttraumatic stress disorder (PTSD), 32 with major depressive disorder (MDD), 29 with somatic symptom disorder (SSD), and 32 healthy volunteers (HVs). Participants underwent functional magnetic resonance imaging during a monetary and social incentive delay task, and completed a self-report measure of ACE, including maternal antipathy. Neural correlates of monetary and social reward anticipation and their association with ACE, particularly maternal antipathy, were analyzed. Participants showed elevated activation in brain regions underlying reward processing, including the VS, only while anticipating social, but not monetary rewards. Participants reporting higher levels of maternal antipathy exhibited reduced activation in the brain reward network, including the VS, only during social, but not monetary reward anticipation. Group affiliation moderated the association between maternal antipathy and VS activation to social reward anticipation, with significant associations found in participants with PTSD and HVs, but not in those with MDD and SSD. Results were not associated with general psychopathology or psychotropic medication use. Childhood maternal antipathy may confer risk for aberrant social reward anticipation in adulthood, and may thus be considered in interventions targeting reward expectations from social interactions.
... Developmentally, INS might be rooted early in human life, with synchronous caregiver-infant interactions being critical for establishing affiliative bonds (Feldman, 2017) and impacting long-term developmental outcomes (Atzil and Gendron, 2017). In the brain, on both cognitive and functional levels, INS has been embedded in a predictive coding framework (social alignment system), mediated by a three-component feedback loop consisting of an observation-execution/alignment, an error-monitoring, and a reward system thought to be activated by and to reinforce successful alignment (Shamay-Tsoory et al., 2019). ...
... Here, the cortical activity of one subject engaged in a certain behavior would translate into the cortical activity of an interacting subject, with the repetition of this social interaction reshaping interbrain functional connectivity not only in dyads but potentially in entire social groups (Ramakrishnan et al., 2015). On the neurochemical level, oxytocin and dopamine have been discussed as the key neurotransmitter systems involved (Feldman, 2017;Gvirts and Perlmutter, 2020;Mu et al., 2016) given their pivotal roles in social functions (MacDonald and MacDonald, 2010), reward processing (Glimcher, 2011), and reciprocal interactions between the two systems in the mesolimbic tract (Baskerville and Douglas, 2010). Related to the social alignment system (Shamay-Tsoory et al., 2019), these mesolimbic neurotransmitter systems may regulate a mutual social attention system located in the PFC and TPJ, possibly enabling selective attention in social interactions through reward-related feedback mechanisms (Gvirts and Perlmutter, 2020). ...
... Here, we could not confirm the involvement of oxytocin and dopamine in neurobiobehavioral synchrony that was hypothesized previously (Feldman, 2017;Gvirts and Perlmutter, 2020;Mu et al., 2016). In contrast, we consider our findings to be more in line with the hypothesis that INS relies on neurobiological mechanisms similar to those previously reported for within-brain synchronization processes: GABA-mediated E/I balance (Sears and Hewett, 2021). ...
Humans synchronize with one another to foster successful interactions. Here, we use a multimodal data fusion approach with the aim of elucidating the neurobiological mechanisms by which interpersonal neural synchronization (INS) occurs. Our meta-analysis of 22 functional magnetic resonance imaging and 69 near-infrared spectroscopy hyperscanning experiments (740 and 3,721 subjects) revealed robust brain-regional correlates of INS in the right temporoparietal junction and left ventral prefrontal cortex. Integrating this meta-analytic information with public databases, biobehavioral and brain-functional association analyses suggested that INS involves sensory-integrative hubs with functional connections to mentalizing and attention networks. On the molecular and genetic levels, we found INS to be associated with GABAergic neurotransmission and layer IV/V neuronal circuits, protracted developmental gene expression patterns, and disorders of neurodevelopment. Although limited by the indirect nature of phenotypic-molecular association analyses, our findings generate new testable hypotheses on the neurobiological basis of INS.
... Scientific evidence shows how the initiation and maintenance of parental behaviour require coordination of the hormonal and neurochemical system, thus highlighting the sensitivity of the human female brain to physiological changes in pregnancy (Kim et al., 2010). In particular, maternal care, both in its initiation and in its maintenance, is influenced by oxytocin (Feldman, 2017). The transition to motherhood changes women's assessment and management of infant signals at different levels, both implicit and explicit. ...
... A critically implicated process in human parenting is the bio-behavioural synchrony that takes place between the partners of the relationship during social exchanges (Feldman, 2012a(Feldman, , 2012b(Feldman, , 2015b(Feldman, , 2016Romero-Fernandez et al., 2013). Bio-behavioural synchrony implies the involvement of multiple systems: behavioural, anatomical, hormonal and cerebral and is observed in the reactions between caregiver and child and in romantic relationships and in friendship (Feldman, 2017). Therefore, neural synchrony is configured as a multimodal phenomenon, reflecting distinct context-dependent processes (Reindl et al., 2022). ...
... Through the self-regulation ability of the parent, bio-behavioural synchrony favours an adequate physiological response, positive development and modelling of the social brain of the child. Indeed, longitudinal studies indicate that the bio-behavioural synchrony between caregiver and child is a predictor of emotional regulation, self-control and bonding security, management of stress and empathy in childhood and adolescence (Dumas et al., 2010;Feldman, 2006Feldman, , 2015bFeldman, , 2017. ...
The quality of the relationship between caregiver and child has long‐term effects on the cognitive and socio‐emotional development of children. A process involved in human parenting is the bio‐behavioural synchrony that occurs between the partners in the relationship during interaction. Through interaction, bio‐behavioural synchronicity allows the adaptation of the physiological systems of the parent to those of the child, promotes the positive development and modelling of the child’s social brain. The role of bio‐behavioural synchrony in building social bonds could be investigated using functional near‐infrared spectroscopy (fNIRS). In this paper we have (a) highlighted the importance of the quality of the caregiver‐child relationship for the child’s cognitive and socio‐emotional development, as well as the relevance of infantile stimuli in the activation of parenting behaviour, (b) discussed the tools used in the study of the neurophysiological substrates of the parental response, (c) proposed fNIRS as a particularly suitable tool for the study of parental responses, (d) underlined the need for a multi‐systemic psychobiological approach to understand the mechanisms that regulate caregiver‐child interactions and their bio‐behavioural synchrony. We propose to adopt a multi‐system psychobiological approach to the study of parental behaviour and social interaction.
... nals. As such, empathy is an ability crucial for communication as well as formation and maintenance of the parent-infant bond (Bos, 2017;Decety, 2011b;Feldman, 2017). OXT seems to affect certain aspects of empathy, such as the recognition of emotions (Bartz et al., 2010;Leppanen et al., 2017) and the recognition of internal states of others (Domes et al., 2010;Hurlemann et al., 2010), and has further shown to increase empathy for pain on a subjective level, although only in specific contexts (Abu-Akel et al., 2015;Shamay-Tsoory et al., 2013). ...
... Overall, the results suggest that in individuals who experienced emotional neglect, OXT boosts emotion and salience perception of socially rewarding and neutral images of children by increasing activity in amygdala and hippocampus and simultaneously decreasing activity in the vmPFC and sPFC. Being responsive to reward signals from children is highly relevant for communication and bonding, and therefore a crucial aspect of caregiving behavior (Bos, 2017;Feldman, 2017). Although negative cues are already highly salient (as is demonstrated by strong activation of amygdala and hippocampus in the task-related effects), for high-emotional-neglect individuals positive or neutral images might be less salient in comparison. ...
... We found no effects in areas involved in response to watching physical pain stimuli with a high aversive component (Bos et al., 2015) such as the AI, ACC, or sensorimotor cortices, whereas we do show strong activation of the amygdala, hippocampus, thalamus, and prefrontal areas involved in the processing of negative emotions. Sensitivity of these regions to distress is highly relevant for caregiving behavior as it reflects increased emotion processing and possibly empathic responses Feldman, 2017). That we did not find activation in the aforementioned regions involved in empathy for pain might reflect that our stimuli indeed induce feelings of compassion, but are not emotionally aversive, such as the sound of an infant crying, which robustly activates the insula (Witteman et al., 2019). ...
Sensitivity for rewarding cues and distress signals from children is fundamental to human caregiving and modulated by the neuropeptide oxytocin. In a functional magnetic resonance imaging study, we investigated whether oxytocin regulates neural responses to reward or distress cues form children. In a placebo‐controlled, within‐subject design, we measured neural responses to positive, negative, and neutral cues from children in 22 healthy female subjects who received oxytocin (24 IU) versus placebo. Further, based on current literature, we hypothesized that oxytocin effects are modulated by experiences of childhood trauma. The task elicited valence‐specific effects—positive images activated the ventromedial prefrontal cortex, left anterior cingulate cortex, and right putamen, and images of children in distress activated the bilateral amygdala, hippocampus, and right medial superior frontal cortex. The effects of oxytocin depended on subjective reports of childhood emotional neglect. Self‐reported neglect interacted with oxytocin administration in the amygdala, hippocampus, and prefrontal areas. In individuals with higher scores of emotional neglect, oxytocin increased neural reactivity of limbic structures to positive and neutral images. Our findings need replication in larger samples and can therefore be considered preliminary but are in line with the recent literature on the modulating effect of childhood adversity on the sensitivity to oxytocin administration.
... It was amongst the ancestors of modern mammals, hamster-like cynodonts living around 250 million years ago, however, that a more pronounced infant dependence and maternal willingness to respond to the vulnerability and distress of their infant formed the basis of mammalian empathy (Brethel-Haurwitz et al. 2017;Marsh 2019). The brain structures and hormonal responses that allow us to sense others' feelings are common across all mammals (Feldman 2017). ...
... Marmosets and tamarins, for example, show not only a concern for fairness (Yasue et al. 2018) and capacities to share but also loyalty to their mate and great investments in efforts in shared care of offspring. Certain brain areas in males are active when recognising their mate (Bales et al. 2007), associated with pleasurable hormonal responses due to the release of the hormones oxytocin and dopamine, as we also see in humans (Abraham and Feldman 2018;Feldman 2017). Many argue that, in their willingness to be generous and in the sharing of care, they are a better analogy for early humans than are much more closely related chimpanzees (Burkart and Finkenwirth 2015;Erb and Porter 2017). ...
... Subtle changes in inherited genetics that influence hormones like oxytocin (such as oxytocin receptor densities in the brain) can have quick and farreaching effects on emotional responses and social behaviours. Many speculate, for example, that hormonal changes in oxytocin and in vasopressin are likely to have been key to changes in the role of fathers in infant development in human evolution (Abraham and Feldman 2018;Feldman 2017) and other changes in these hormones, later in human evolution, may have been important in changes in intergroup tolerance (discussed in Part 2). ...
In Hidden Depths, Professor Penny Spikins explores how our emotional connections have shaped human ancestry. Focusing on three key transitions in human origins, Professor Spikins explains how the emotional capacities of our early ancestors evolved in response to ecological changes, much like similar changes in other social mammals. For each transition, dedicated chapters examine evolutionary pressures, responses in changes in human emotional capacities and the archaeological evidence for human social behaviours. Starting from our earliest origins, in Part One, Professor Spikins explores how after two million years ago, movement of human ancestors into a new ecological niche drove new types of collaboration, including care for vulnerable members of the group. Emotional adaptations lead to cognitive changes, as new connections based on compassion, generosity, trust and inclusion also changed our relationship to material things. Part Two explores a later key transition in human emotional capacities occurring after 300,000 years ago. At this time changes in social tolerance allowed ancestors of our own species to further reach out beyond their local group and care about distant allies, making human communities resilient to environmental changes. An increasingly close relationship to animals, and even to cherished possessions, appeared at this time, and can be explained through new human vulnerabilities and ways of seeking comfort and belonging. Lastly, Part Three focuses on the contrasts in emotional dispositions arising between ourselves and our close cousins, the Neanderthals. Neanderthals are revealed as equally caring yet emotionally different humans, who might, if things had been different, have been in our place today. This new narrative breaks away from traditional views of human evolution as exceptional or as a linear progression towards a more perfect form. Instead, our evolutionary history is situated within similar processes occurring in other mammals, and explained as one in which emotions, rather than ‘intellect’, were key to our evolutionary journey. Moreover, changes in emotional capacities and dispositions are seen as part of differing pathways each bringing strengths, weaknesses and compromises. These hidden depths provide an explanation for many of the emotional sensitivities and vulnerabilities which continue to influence our world today.
... Developmentally, INS might be rooted early in human life, with synchronous caregiver-infant interactions being critical for establishing affiliative bonds (37) and impacting long-term developmental outcomes (38). In the brain, on both cognitive and functional levels, INS has been embedded in a predictive coding framework (social alignment system), mediated by a three-component feedback loop consisting of an observation-execution/alignment, an error-monitoring, and a reward system thought to be activated by and to reinforce successful alignment (34). ...
... Here, the cortical activity of one subject engaged in a certain behavior would translate into the cortical activity of an interacting subject, with the repetition of this social interaction reshaping interbrain functional connectivity not only in dyads but potentially in entire social groups (40). On the neurochemical level, oxytocin and dopamine have been discussed as the key neurotransmitter systems involved (12,37,41) given their pivotal roles in social functions (42), reward processing (43), and reciprocal interactions between the two systems in the mesolimbic tract (44). Related to the social alignment system (34), these mesolimbic neurotransmitter systems may regulate a mutual social attention system located in the PFC and TPJ, possibly enabling selective attention in social interactions through reward-related feedback mechanisms (41). ...
... Here, we could not confirm the involvement of oxytocin and dopamine in neurobiobehavioral synchrony that was hypothesized previously (12,37,41). In contrast, we consider our findings to be more in line with the hypothesis that INS relies on neurobiological mechanisms similar to those previously reported for within-brain synchronization processes: GABA-mediated E/I balance (16). ...
Humans synchronize with one another to foster successful interactions. Here, we use a multimodal data fusion approach with the aim of elucidating the neurobiological mechanisms by which interpersonal neural synchronization (INS) occurs. Our meta-analysis of 22 functional magnetic resonance imaging and 69 near-infrared spectroscopy hyperscanning experiments (740 and 3,721 subjects) revealed robust brain-regional correlates of INS in the right temporoparietal junction and left ventral prefrontal cortex. Integrating this meta-analytic information with public databases, biobehavioral and brain-functional association analyses suggested that INS involves sensory-integrative hubs with functional connections to mentalizing and attention networks. On the molecular and genetic levels, we found INS to be associated with GABAergic neurotransmission and layer IV/V neuronal circuits, protracted developmental gene expression patterns, and disorders of neurodevelopment. Although limited by the indirect nature of phenotypic-molecular association analyses, our findings generate new testable hypotheses on the neurobiological basis of INS.
Associated GitHub repository: https://github.com/LeonDLotter/MAsync
... Otro análisis significativo de la interacción genambiente fue revelado por un análisis de los datos de consumo de alcohol. Los monos criados en patrones de apego no seguros con el alelo LS presentaron mayor dependencia al consumo de alcohol que los monos criados en el mismo patrón de crianza con el alelo LL (30). Resumiendo, el alelo LS parecía representar un factor de riesgo significativo para el consumo excesivo de alcohol entre los monos con experiencias adversas de apego temprano, pero un factor protector significativo para los sujetos criados por madres en experiencias de apego positivas con sus madres. ...
... La oxitocina está implicada en la maternidad humana, la paternidad, el coparenting, el apego romántico y la amistad cercana. La oxitocina tiene un papel fundamental a través de sus receptores en el núcleo accumbens en la formación del apego y en la continuidad del mismo a largo plazo (30). Los estudios también describen el papel de la oxitocina en la regulación de la respuesta de la amígdala a los estímulos sociales aversivos, favoreciendo de esta manera las conductas de acercamiento necesarias para el desarrollo del apego y reduciendo las respuestas de miedo. ...
... Este sistema integra todos los componentes y determina la correcta formación de relaciones de apego y el mantenimiento de las mismas (29). Estudios longitudinales que siguen a humanos desde la infancia hasta la edad adulta describen la participación de la oxitocina no solo en el establecimiento del apego sino también en la transferencia del mismo en las relaciones de amistad que se establecen en la edad adulta y en las relaciones de pareja (30). Las conexiones surgen integradas en respuesta a señales relacionadas con la vinculación e implican tanto a la oxitocina como la dopamina. ...
El sistema vincular del apego es fundamental en la comprensión de las relaciones que se establecen entre diferentes individuos de una especie, así como de la relación de las madres con su progenie. El sistema de apego tiene un componente evolutivo a lo largo de las diferentes especies y un patrón de transmisión intergeneracional. En la siguiente revisión se desarrolla un marco para poder entender este sistema de apego, tanto desde la propia perspectiva evolutiva como neurobiológica. Revisar el apego en diferentes especies ha permitido profundizar en el sustrato biológico subyacente y su correspondencia con la neurobiología del mismo en humanos, así como su implicación en la respuesta al estrés y las similitudes y diferencias evolutivas de las relaciones vinculares en distintas especies de mamíferos.
... Other researchers have investigated the neurobiology of love, namely, the role of oxytocin, vasopressin, dopamine, serotonin, testosterone or cortisol in love and attachment relations (DeBoer et al., 2012;Seshadri, 2016;Feldman, 2017). Based on neuroimaging studies, some scholars even proposed that love represents a form of positive addiction when feelings are mutual (Fisher et al., 2016) and a negative addiction when love is unrequited, when people feel rejected or experience heartbreak (Fisher et al., 2010(Fisher et al., , 2016. ...
... For example, they were shown to be important for parent-child relations or friendships. Feldman (2017) describes the relevance of neural networks for attachment, including the interaction of oxytocin and dopamine in the striatum. Attachment implies the maintenance of proximity, seeking safety and security and preventing separation anxiety (Berscheid, 2010). ...
Our love relationships define us as individuals and shape our personal growth across the lifespan in all developmental domains (i.e. cognitive, emotional, physical, social, personality). Love relations evolve across the later stages of life as the individuals within a couple change. In this chapter, I will focus on romantic relationships and their impact on individual development in midlife and older age. First, I will discuss definitions of love and marital satisfaction, theories that explain love and what instruments were developed to measure love and fulfilled romantic relations. Second, I will examine what middle-aged and older people think about love and relationships and what are the positive and negative characteristics of romantic relationships in midlife and older age. In this context, I will discuss the potentials and pitfalls of the empty nest syndrome, grey divorces and bereavement. Third, I will analyse the relation between romantic relationships and personal development in all life domains. Finally, I will reflect on how positive psychology principles and developmental resources can be applied to help middle-aged and older individuals to achieve their desired relationships as well as foster their developmental potential.
... Within the mother-infant bond, which occurs in all mammals, a variety of physiological and behavioral phenomena have been described, so the system is today known in great detail revealing common structures and functional similarities to other types of mammalian affective bonds -sexual partner pair bonds, peer-group bonds and social bonds with same community and species individuals -with measurable and observable features in rodents, nonhuman primates and humans (Donaldson & Young, 2008, Feldman et al., 2007Feldman, 2017). The study of what seems to be the original "mother system" to the subsystems underpinning other social bonds -tagged as the neurobiology of love -has shown that these bonds have in common the strong and interactive mediation of oxytocin and dopamine -and re-markable synchronization (not only of behavior, a common observation for ethologists) but of autonomic nervous system activity, with measurable coordination in heart and respiratory rate, brain activity synchrony especially in alpha rhythms, and coordinated response to events in brain temporoparietal structures involved in emotional and cognitive empathy (Feldman, 2017). ...
... Within the mother-infant bond, which occurs in all mammals, a variety of physiological and behavioral phenomena have been described, so the system is today known in great detail revealing common structures and functional similarities to other types of mammalian affective bonds -sexual partner pair bonds, peer-group bonds and social bonds with same community and species individuals -with measurable and observable features in rodents, nonhuman primates and humans (Donaldson & Young, 2008, Feldman et al., 2007Feldman, 2017). The study of what seems to be the original "mother system" to the subsystems underpinning other social bonds -tagged as the neurobiology of love -has shown that these bonds have in common the strong and interactive mediation of oxytocin and dopamine -and re-markable synchronization (not only of behavior, a common observation for ethologists) but of autonomic nervous system activity, with measurable coordination in heart and respiratory rate, brain activity synchrony especially in alpha rhythms, and coordinated response to events in brain temporoparietal structures involved in emotional and cognitive empathy (Feldman, 2017). The strength of both mother-infant and pair bonds is correlated with oxytocin levels, with cross-species mother postpartum behavior and, in addition, positive representations of motherhood in humans (Feldman et al., 2007). ...
The socioemotional lives of animals have been brought to light over the years by studies seeking to address specific topics in animal emotion, cognition and behavior. Breakthrough information has been provided by field work with natural communities, and notable advances have stemmed from non-invasive research with captive animals and from laboratory work entailing varying degrees of invasiveness. But there is a source of information on animals that has not always been integrated in the knowledge on animals’ emotional lives: the outputs of studies where animals served as models of human emotional processes but that were seldom published as literature on animals. This article proposes an integrated view whereby the vast amount of information amassed by the brain and behavioral sciences over the course of the last 30 years on the affective experiences of animals, their triggers, biomarkers and behavioral correlates is fully integrated in an account of animal emotions. Topics where this knowledge can accommodate further integration from studies with animals models of the human mind are the parental care and different types of affective bonds; the experience of empathic reactions, the association between emotions, expressive behavior and affective bonds, and conscience. Fostering further connection between these neuroscience and behavioral studies might contribute to 1) widening the breath of measures used in assessing the well-being of animals, 2) widening criteria used by ethical committees considering studies with animals, and 3) to review some common practices that by those who have key roles in the management of wild or captive animals.
... However, in everyday life a variety of outcomes can serve as rewards, shaping and maintaining behavior. Social affiliation and food are basic human needs and universal motivators (Feldman, 2017;Sescousse et al., 2013). In typically developing adults, striatal activation to affiliative (Feldman, 2017;Moll and de Oliveira-Souza, 2009) and food stimuli (Beaver et al., 2006;Cornier et al., 2007;Pursey et al., 2014;Rothemund et al., 2007;Tang et al., 2012) have been reported. ...
... Social affiliation and food are basic human needs and universal motivators (Feldman, 2017;Sescousse et al., 2013). In typically developing adults, striatal activation to affiliative (Feldman, 2017;Moll and de Oliveira-Souza, 2009) and food stimuli (Beaver et al., 2006;Cornier et al., 2007;Pursey et al., 2014;Rothemund et al., 2007;Tang et al., 2012) have been reported. There is also some evidence that striatal responses to the anticipation of affiliative and food rewards are similar to anticipatory responses to monetary rewards (Bortolini et al., 2021;Goerlich et al., 2017;Rademacher et al., 2010;Simon et al., 2015;Spreckelmeyer et al., 2009). ...
Altered reward sensitivity has been proposed to underlie symptoms of attention deficit hyperactivity disorder (ADHD). Functional magnetic resonance imaging (fMRI) studies have reported hypoactivation to reward-predicting cues in the ventral striatum among individuals with ADHD, using experimental designs with and without behavioral response requirements. These studies have typically used monetary incentives as rewards; however, it is unclear if these findings extend to other reward types. The current study examined striatal responses to anticipation and delivery of both affiliative and food reward images using a classical conditioning paradigm. Data from 20 typically developing young adults, and 20 individuals diagnosed with ADHD were included in a region-of-interest analysis for a priori striatal regions. Consistent with findings from studies using monetary rewards, individuals with ADHD showed decreased activation to cues predicting affiliative rewards in the bilateral ventral and dorsal striatum and increased activation to the delivery of affiliative rewards in the ventral striatum. No group differences were found in striatal responses to food reward cues or images. These results suggest hyposensitivity to reward-predicting cues in ADHD extends to affiliative rewards, with important implications for understanding and managing the learning and social functioning of those with ADHD.
... The idea of children being born biologically driven and neurologically wired to form relationships and connect with the world around them is not new (Golding, 2007;Feldman, 2017). From birth babies are active and relationally engaged beings, seeking closer reciprocal relationships and relational experiences as they begin to make sense of their world (Trevarthen, 2005;Music, 2017). ...
... Research into bio-behavioural exchanges within the womb and babies' face-to-face interactions from birth, provide a growing evidence base for these innate relational connections (Feldman, 2017). Behaviour synchronicity for example, is expressed through physical actions and behaviours, gestures and so forth, which build social connections. ...
Within this literature-based article the authors consider the importance and power of relationships, within the field of early years education and care (ECEC). Drawing on the lenses of attachment and development theory, alongside current literature and research, the authors critically explore the significance of relationships in child development, including the crucial role that they play in general physical and emotional health and development, as well as more long-term mental health and wellbeing. Children’s relational worlds have recently been challenged by the pandemic and subsequent lockdowns, social isolation and safety measures. This article argues that while the full implications of the pandemic have yet to be realised, the relational implications for children are more important than ever before. Dominant discourses regarding attachment and early bonding are discussed, alongside the lesser explored discourses around companionship attachment and how this connects to relational pedagogy, and wider notions of genetic heritage and ecocultural literacy.
... Selection on neuroendocrine pathways, including oxytocin and serotonin, are associated with differences in social behaviour between chimpanzees and bonobos, for example (Kovalaskas, Rilling, and Lindo 2020). Changes in oxytocin and beta endorphins are likely to have played a role in the expansion of compassion towards a broader set of group members that we saw occurring between 2 and 1.5 million years ago (Feldman 2017;Gordon et al. 2010). Oxytocin, in particular, is involved in social touch, grooming, and behaviours that facilitate strong emotional bonds, motivate generosity and altruism, and reduce stress (Snowdon 2011). ...
... Close friendships are thus a particular form of bond, extending from maternal attachment and romantic attachments (Feldman et al. 2013). Oxytocin increases following contact with friends (Feldman 2017 Other related hormone changes are also significant, and attention has also particularly been drawn to changes in serotonin pathways. Serotonin is another hormone influencing our mood and social behaviour that is likely to have been subject to selection pressures in human evolution. ...
In Hidden Depths, Professor Penny Spikins explores how our emotional connections have shaped human ancestry. Focusing on three key transitions in human origins, Professor Spikins explains how the emotional capacities of our early ancestors evolved in response to ecological changes, much like similar changes in other social mammals. For each transition, dedicated chapters examine evolutionary pressures, responses in changes in human emotional capacities and the archaeological evidence for human social behaviours. Starting from our earliest origins, in Part One, Professor Spikins explores how after two million years ago, movement of human ancestors into a new ecological niche drove new types of collaboration, including care for vulnerable members of the group. Emotional adaptations lead to cognitive changes, as new connections based on compassion, generosity, trust and inclusion also changed our relationship to material things. Part Two explores a later key transition in human emotional capacities occurring after 300,000 years ago. At this time changes in social tolerance allowed ancestors of our own species to further reach out beyond their local group and care about distant allies, making human communities resilient to environmental changes. An increasingly close relationship to animals, and even to cherished possessions, appeared at this time, and can be explained through new human vulnerabilities and ways of seeking comfort and belonging. Lastly, Part Three focuses on the contrasts in emotional dispositions arising between ourselves and our close cousins, the Neanderthals. Neanderthals are revealed as equally caring yet emotionally different humans, who might, if things had been different, have been in our place today. This new narrative breaks away from traditional views of human evolution as exceptional or as a linear progression towards a more perfect form. Instead, our evolutionary history is situated within similar processes occurring in other mammals, and explained as one in which emotions, rather than ‘intellect’, were key to our evolutionary journey. Moreover, changes in emotional capacities and dispositions are seen as part of differing pathways each bringing strengths, weaknesses and compromises. These hidden depths provide an explanation for many of the emotional sensitivities and vulnerabilities which continue to influence our world today.
... An infant is fully dependent on their caregiver for all aspects of physiological regulation, including body temperature, feeding and sleeping. Caregivers are actively entraining the developing child's physiology in ways that will ultimately support or undermine their ability to effectively regulate physiologically (Feldman, 2015(Feldman, , 2017. These multiple forms of regulation include physiological responses to stress, which will ultimately decide the balance through which reactive versus reflective responses to stimulation are prioritized (Blair and Cybele Raver, 2015;Brandes-Aitken et al., 2020). ...
... This is seen in the vast empirical literature demonstrating the centrality of the caregiverchild relationship in child social-emotional and cognitive development, particularly for children who experience neglect and marginalization on the basis of their race/ethnicity or income (McLoyd, 1998). It is also seen in a burgeoning literature on the neuroscience of relationships in which hormones, neuropeptides and catecholamines organize and shape connections between cortical and subcortical networks in ways that influence relations between caregivers and children (Feldman, 2017). ...
The overall goal of the ISEE Assessment is to pool multi-disciplinary expertise on educational systems and reforms from a range of stakeholders in an open and inclusive manner, and to undertake a scientifically robust and evidence based assessment that can inform education policy-making at all levels and on all scales. Its aim is not to be policy prescriptive but to provide policy relevant information and recommendations to improve education systems and the way we organize learning in formal and non-formal settings. It is also meant to identify information gaps and priorities for future research in the field of education.
... These two lines of research propose a novel anti-phase synchrony of the mother-infant dyads. While many reports have identified several instances of in-phase synchrony in the mother-infants in emotional interactions like eye gaze, emotional regulations and verbal and non-verbal communications and social play [11,30,38] these passive "inactions" are interesting because it enables physiological and behavioral turn-taking: while the major actor of the dyad is engaging in a necessary duty for survival (such as transport or suckling), the counterpart should restrict their own activity and stay calm for a while, not to disturb the main actor. This type of inhibitory cooperation may not be as conspicuous as active role-taking and thus may have been understudied. ...
The mother–infant relation is key to infant physical, cognitive and social development. Mutual regulation and cooperation are required to maintain the dyadic system, but the biological foundation of these responses remains to be clarified. In this study, we report the maternal calming responses to infant suckling during breastfeeding. Using behavioral measures and a Holter electrocardiogram as a readout of the maternal autonomic nervous system, the maternal activities during resting, sitting with her infant on her lap, and breastfeeding were assessed. We found that during breastfeeding, mothers talked less and maternal heart rate was lower than during sitting with the infant without breastfeeding. Congruently, maternal heart rate variability measurements indicated a higher parasympathetic activity during breastfeeding. Time-locked analyses suggested that this maternal calming response was initiated by the tactile stimulation at the breast by the infant face or mouth latch, which preceded the perceived milk ejection. These findings suggest that somatosensory stimuli of breastfeeding activate parasympathetic activity in mothers. Just as how the infant Transport Response facilitates the carrying of infants, the maternal calming responses during breastfeeding may promote efficient milk intake by inhibiting spontaneous maternal activities.
... The Social Baseline Theory posits that humans have evolved to be social creatures and that social interactions are essential for the efficient regulation of physiological and psychological processes (17,18). Biobehavioral synchrony refers to the coordination of physiological and psychological processes during social interactions, such as the coordination of nonverbal behaviour, autonomic regulation, heart rhythms, brain-to-brain synchrony, and the release of neurotransmitters like oxytocin (19,20). Research has shown that when these systems are sufficiently coupled, they exhibit similar dynamic neuronal structures, including matching activations in the parietal and frontal cortices, particularly during therapeutic touch (21,22). ...
Therapeutic affective touch has been recognized as essential for survival, nurturing supportive interpersonal interactions, accelerating recovery-including reducing hospitalisations, and promoting overall health and building robust therapeutic alliances. Through the lens of active inference, we present an integrative model, combining therapeutic touch and communication, to achieve biobehavioural synchrony. This model speaks to how the brain develops a generative model required for recovery, developing successful therapeutic alliances, and regulating allostasis within paediatric manual therapy. We apply active inference to explain the neurophysiological and behavioural mechanisms that underwrite the development and maintenance of synchronous relationships through touch. This paper foregrounds the crucial role of therapeutic touch in developing a solid therapeutic alliance, the clinical effectiveness of paediatric care, and triadic synchrony between health care practitioner, caregiver, and infant in a variety of clinical situations. We start by providing a brief overview of the significance and clinical role of touch in the development of social interactions in infants; facilitating a positive therapeutic alliance and restoring homeostasis through touch to allow a more efficient process of allostatic regulation. Moreover, we explain the role of CT tactile afferents in achieving positive clinical outcomes and updating prior beliefs. We then discuss how touch is implemented in treatment sessions to promote cooperative interactions in the clinic and facilitate theory of mind. This underwrites biobehavioural synchrony, epistemic trust, empathy, and the resolution of uncertainty. The ensuing framework is underpinned by a critical application of the active inference framework to the fields of pediatrics and neonatology.
... The study was guided by the biobehavioral synchrony conceptual frame, which suggests that maternal behavior characterized by ongoing coordination with the infant's nonverbal signals and couched within a well-adapted, fluent, and reciprocal dialogue (i.e., maternal sensitivity) provides the template for the coordination of the physiological processes between mother and child, including heart rhythms, hormonal release, or interbrain synchrony [37][38][39]. Such biobehavioral linkage is a critical social input the infant must experience during the first months of life, prior to the onset of language and the first major reorganization of the prefrontal cortex [37,40]. Here, we examined the hypothesis that the mother's sensitive style is associated with greater inter-brain synchrony, whereas the intrusive style is linked with diminished neural synchrony, and that such differences in coordinated neural input may exert a lasting effect on the infant's brain and behavior. ...
Biobehavioral synchrony, the coordination of physiological and behavioral signals between mother and infant during social contact, tunes the child’s brain to the social world. Probing this mechanism from a two-brain perspective, we examine the associations between patterns of mother–infant inter-brain synchrony and the two well-studied maternal behavioral orientations—sensitivity and intrusiveness—which have repeatedly been shown to predict positive and negative socio-emotional outcomes, respectively. Using dual-electroencephalogram (EEG) recordings, we measure inter-brain connectivity between 60 mothers and their 5- to 12-month-old infants during face-to-face interaction. Thirty inter-brain connections show significantly higher correlations during the real mother–infant face-to-face interaction compared to surrogate data. Brain–behavior correlations indicate that higher maternal sensitivity linked with greater mother–infant neural synchrony, whereas higher maternal intrusiveness is associated with lower inter-brain coordination. Post hoc analysis reveals that the mother-right-frontal–infant-left-temporal connection is particularly sensitive to the mother’s sensitive style, while the mother-left-frontal–infant-right-temporal connection indexes the intrusive style. Our results support the perspective that inter-brain synchrony is a mechanism by which mature brains externally regulate immature brains to social living and suggest that one pathway by which sensitivity and intrusiveness exert their long-term effect may relate to the provision of coordinated inputs to the social brain during its sensitive period of maturation.
... OXT promotes synchronisation in the mother-child, father-child and other relationships (Feldman, 2017), whereas T inhibits synchronisation (Gordon et al., 2017). Rhythmic synchronisation is associated with cooperative, collaborative and pro-social behaviours (Cirelli, 2018). ...
Since the time of Darwin, theories have been proposed on the origin and functions of music; however, the subject remains enigmatic. The literature shows that music is closely related to important human behaviours and abilities, namely, cognition, emotion, reward and sociality (co-operation, entrainment, empathy and altruism). Notably, studies have deduced that these behaviours are closely related to testosterone (T) and oxytocin (OXT). The association of music with important human behaviours and neurochemicals is closely related to the understanding of reproductive and social behaviours being unclear. In this paper, we describe the endocrinological functions of human social and musical behaviour and demonstrate its relationship to T and OXT. We then hypothesised that the emergence of music is associated with behavioural adaptations and emerged as humans socialised to ensure survival. Moreover, the proximal factor in the emergence of music is behavioural control (social tolerance) through the regulation of T and OXT, and the ultimate factor is group survival through co-operation. The “survival value” of music has rarely been approached from the perspective of musical behavioural endocrinology. This paper provides a new perspective on the origin and functions of music.
... In normative development, the attachment system is activated in response to threat (24,25), leading the individual to seek proximity to responsive attachment figures, which leads in turn to a down-regulation of distress and discomfort. At the neurobiological level, this response is mediated by a mesocorticolimbic dopaminergic "reward system" that plays an essential role in downregulating the stress system and is responsible for feeling supported, validated, and understood by close others (26,27). Trauma typically disrupts the virtuous cycle associated with proximity seeking in the face of stress and adversity, as the individual begins to rely excessively either on attachment hyperactivating or deactivating strategies, or a combination of both. ...
Background: Recent meta-analyses suggest that many patients with borderline personality disorder (BPD) have a history of (complex) trauma. Although trauma is central in mentalization-based approaches to the understanding of BPD, surprisingly little is known about the effects of trauma on treatment outcomes in Mentalization-based treatment (MBT). This paper investigates the prevalence and impact of childhood trauma in BPD patients in MBT in the context of a randomized controlled trial comparing MBT day hospital (MBT-DH) and intensive outpatient MBT (MBT-IOP). Methods. All 114 patients from the original multicenter RCT were included. Childhood trauma was assessed at baseline by the Childhood Trauma Questionnaire and its impact on symptom severity, interpersonal functioning and borderline pathology was investigated over a time horizon of 36 months after start of treatment using multilevel modeling. Results. Childhood trauma was very common in BPD patients referred to MBT, with more than 85% of patients meeting cut-off criteria for substantial childhood trauma. However, childhood trauma had little impact on outcome in both MBT-DH and MBT-IOP in terms of improvements in BPD features and interpersonal functioning, although patients with high levels of childhood trauma seemed to improve more rapidly in MBT-DH compared with MBT-IOP in terms of symptom severity. Patients with a history of emotional neglect also showed more rapid changes in BPD symptoms in MBT-DH compared with MBT-IOP. Conclusions. Findings are discussed in the context of a social communicative approach to BPD, with a focus on the need to address trauma in (MBT) treatment for BPD.
... Infantile facial features of babies and toddlers, such as big eyes, short nose, narrow chin, and high forehead, are perceived as cute, grab attention, induce pleasant feelings, and promote caregiving behaviors [28][29][30][31][32][33]. Infantile (Kindchenschema) characteristics related to the perception of vulnerability, innocence, and the need for care activate the parenting system, known as the baby schema effect [30,[33][34][35][36][37]. Brain areas associated with social-emotional, reward, and motivational processing are activated when watching visual cues of baby cuteness [34,38,39]. To reiterate, infants' and young children's infantile physical characteristics are visually attractive and effective in inducing nurturing motivations and behaviors in adults. ...
The current empirical evidence regarding the effects of personality on physical attractiveness is limited to adult faces. In two preregistered studies, we demonstrated that personality descriptions influenced perceived cuteness, warmth, competence of young children, and female adults' nurturing motivation toward them. Study 1 showed that participants rated children accompanied by positive personality descriptions as cuter, friendlier, and more intelligent than their initial ratings. Negative personality descriptions reduced perceived cuteness in children, which in turn reduced nurturing motivation. Study 2 showed that negative personality descriptions consistently reduced perceived cuteness and warmth ratings after manipulation, regardless of the initial level of perceived cuteness. After one week, cuteness and warmth ratings in the positive personality condition tended to return to their initial ratings. However, the effect of negative personality descriptions on cuteness ratings persisted for all children. Together, our findings suggest that female adults' perception of cuteness and nurturing motivation are induced not only by children's appearance but also their personality.
... Previous research has indicated that empathy emerges in early life and develops for a long period after that through abundant interactions with caregivers (De Haan and Gunnar, 2009). The parent-child attachment bond provides a template for children to understand and resonate with the pain, feelings, and thoughts of others (Feldman, 2017). However, being abused or neglected by caregivers in early life, could disrupt the normal development of empathy. ...
Background
Childhood abuse and neglect are typically considered as two different forms of maltreatment. Previous international studies have found differential effects of abuse and neglect on prosocial behavior, but this and the mediating pathway underlying these associations have not been examined in a Chinese sample. Our study aims to examine the effects of childhood abuse and neglect on prosocial behavior in Chinese participants and test the unique mediating roles of different empathic components in these associations.
Methods
A total of 1,569 young adults (average age = 18.17 years) were recruited from a college that enrolls students from all provinces of China. Participants completed a series of questionnaires, including the Childhood Trauma Questionnaire, Interpersonal Reactivity Index, and Prosocial Tendencies Measure. Path analysis was conducted to determine the mediational relationships.
Results
Emotional neglect had significant direct effect on prosocial behavior ( β = −0.108, p < 0.001), and could also impact prosocial behavior through the mediating roles of perspective-taking and empathic concern (effect size = −0.091 and −0.097 respectively, p < 0.001). Emotional abuse affected prosocial behavior only through personal distress (effect size = −0.072, p < 0.001). Physical abuse, sexual abuse and physical neglect have little effect on prosocial behavior and empathy.
Conclusion
Childhood abuse and neglect have distinct influences on prosocial behavior. Emotional abuse and emotional neglect affect prosocial behavior through distinct pathways. This conclusion could help to establish precise interventions for improving prosocial behavior in maltreated individuals.
... Recent studies on children with autism spectrum disorder (ASD) indicate that intranasal OT administration is generally well tolerated with few side effects (23-26). Inreasing evidence supports the important role of neuropeptide OT in regulating mother-infant bonding and attachment in humans (27,28), and atypical OT levels in plasma, cerebrospinal fluid, and saliva have been found in children subjected to maltreatment and lacking attachment or bonding with a primary caregiver (29)(30)(31)(32)(33)(34). OT acts both as a neurotransmitter and neuromodulator, regulating neuroendocrine, psychophysiological, and socioemotional responses in animals and humans (22,28,35,36). ...
Reactive attachment disorder (RAD) is associated with socially and emotionally withdrawn/inhibited behaviors and reduced neural responses to rewards. Children and adolescents with RAD show aberrant attachment behaviors, and existing psychotherapies are difficult to maintain; therefore, pharmacological interventions to aid and boost treatment responses are needed. Oxytocin (OT) administration is known to promote reward functioning. We investigated whether single-use intranasal OT administration improved neural responses during reward processing in patients with RAD compared with healthy controls. Twenty-four male children and adolescents with RAD (10–18 years old) and 27 age- and sex-matched typically developing individuals (10–17 years old) were included in this randomized, double-blind, placebo-controlled, cross-over, functional magnetic resonance imaging study. Following a single intranasal OT (24 IU) or placebo administration, neural responses were investigated using a monetary reward task. In the RAD group, OT significantly increased subjective motivation scores, significantly enhanced activation in the right middle frontal gyrus, and reduced activation in the right precentral gyrus during the monetary reward task. Additional analyses revealed increased activation in the bilateral caudate at a more lenient threshold. Under placebo conditions, the severity of internalizing problems in patients with RAD was negatively correlated with ventral striatal activity. Moreover, the effect of OT on ventral striatum activity was positively associated with the severity of internalizing problems in patients with RAD. Intranasal OT administration enhanced activity in the reward pathway in male children and adolescents with RAD, suggesting that exogenous OT promotes reward processing and reward-related motivational behavior in these individuals. Further investigation is needed to fully understand the neural mechanisms of intranasal OT and identify novel targets for pediatric cases with RAD.
Clinical trial registration: UMIN-CTR; UMIN000013215. URL: https://upload.umin.ac.jp/cgi-open-bin/ctr/ctr_view.cgi?recptno=R000015419
... Similarly, the original focus on attachment to parental figures has been expanded to encompass romantic partners, parents, siblings, children and friends (Doherty and Feeney, 2004), adult relationships (Allen and Land, 1999;Heffernan and Fraley, 2015;Overall et al., 2015) and the ways in which attachment influences parenting styles (Jones et al., 2015;Young et al., 2017). The neuroscience of attachment has also been progressively developed (Insel and Young, 2001;Insel and Fernald, 2004;Montague and Lohrenz, 2007;Coan, 2008;Neumann, 2008;Coan, 2010;Panksepp, 2011;Gillath, 2015;Feldman, 2017). Attachment theory is now central to research and academic agendas within clinical applications (Fonagy and Campbell, 2015), adult psychopathology (Ein-Dor and Doron, 2015), and more recently learning (Luyten et al., 2017a,b) and pedagogy (Csibra and Gergely, 2009). ...
Attachment theory is one of the key theoretical constructs that underpin explorations of human bonding, taking its current form in John Bowlby's amalgamation of ideas from psychoanalysis, developmental psychology and ethology. Such a period of interdisciplinary exchange, and Bowlby's interest in Lorenz' concept of imprinting in particular, have been subject to rather historical and biographical studies, leaving a fine-grained theoretical scrutiny of the exact relationship between imprinting and attachment still pending. This paper attempts to remedy such an omission by exploring the relationships between these two constructs. It critically reviews the theories of imprinting in general, of human imprinting in particular, and of attachment; analysis of the links between these processes bring to the foreground the distinction between supra-individual vs. individual aspects of bonding, the relevance of 'proto-attachment' phases before 'proper' Bowlbyan attachment is attained, and the role of communicative signals during such early phases. The paper outlines potential benefits of considering such elements in the study of early social cognition, particularly in respect of the study of the gaze and the infant-directed communicative register.
... Par la suite, la théorie de l'attachement a été transférée à d'autres situations de la vie d'un animal, avec notamment le développement, à partir des années quatre-vingt, d'études concernant « l'attachement social », c'est-à-dire la mise en place et le maintien de liens affectifs particuliers durables entre partenaires autres que les parents et leurs enfants (Brent et al. 2014, Feldman 2017, Hazan & Shaver 1987, Young & Wang 2004 Par exemple, les comportements qui suscitent l'attachement sont des activités gratifiantes, qui procurent du plaisir. De récentes observations s'appuyant sur la neuro-imagerie humaine confirment l'implication, dans les phénomènes d'attachement social, de régions nerveuses impliquées dans le circuit de la récompense (Bartels & Zeki 2004, Fisher et al. 2006, Fisher et al. 2010). ...
Dans une société où les animaux compagnons sont intégrés au cercle familial, beaucoup d’humains les considèrent comme des membres de la famille à part entière. La recherche doit suivre cette tendance et s’attacher à appréhender les mécanismes de relations qui se construisent entre différentes espèces amenées à cohabiter. L’objectif de cette thèse est d’enrichir et d’approfondir les connaissances scientifiques sur l’éthologie du chat compagnon (Felis catus), afin de mieux appréhender ses besoins et réponses comportementales, au sein d’un environnement souvent imposé par l’humain. Les travaux restitués sont principalement centrés sur la communication interspécifique entre l’humain et le chat. Soucieux d’explorer aussi bien la perspective de l’humain que celle du chat, nous avons étudié la façon dont chacun s’exprime et décode les messages de l’autre. Ainsi, nous nous sommes intéressés à la communication vocale et visuelle entre ces deux espèces différentes qui partagent un même milieu - et doivent apprendre à communiquer efficacement pour cohabiter sereinement. Nos études ont mis en évidence que les humains utilisaient un discours spécifique pour s’adresser à leur compagnons félins, caractérisé par l’utilisation d’une voix plus aiguë. Nous avons également rapporté que les chats étaient plus attentifs à ce type de discours, mais seulement lorsqu’il était prononcé par leur compagnon humain et non par un étranger. Dans une troisième étude, nous avons observé que les chats venaient plus volontiers au contact d’un humain peu familier si celui-ci proposait un contact bimodal ou visuel, plutôt que vocal. Enfin, nous avons vu que les humains comprenaient mieux les chats dans leurs expressions bimodales et visuelles que vocales. Ainsi, bien que communément utilisée par chaque émetteur de cette communication interspécifique, la modalité vocale ne semble pas être suffisante pour la transmission et la réception d’un signal clair. Ces résultats sont discutés à la lumière des notions d’attachement, d’anthropomorphisme et de bien-être animal.
... Throughout life, human attachment promotes homeostasis, health, and well-being. Social attachment promotes health and happiness, whereas social isolation promotes stress, health issues, and mortality (Feldman, 2017). Psychologists categorize three stages of romantic relationships as companionate love, being in love, and passionate love. ...
Unification theory seeks to gain a comprehensive understanding of something. The goal of unification theory is to bring together multiviews on love. If “Love” is not understood from multiple perspectives, it will be difficult to understand and easy to misinterpret. This paper expresses Nurcholish Madjid's "Love" thoughts based on his works. Given the scope of the issue, Love will be examined through the lens of neuroparemiofenomenology, or the collaboration of neuroscience, paremiology, and phenomenology. The term "Love" was searched using "Nurcholish Madjid's Complete Works," edited by Dr. Budhy Munawar-Rachman. The neuroparemiopheno menological perspective is hoped to reveal the fundamental meaning of "love" in a comprehensive and complete manner. Teori unifikasi berusaha untuk memperoleh pemahaman yang komprehensif tentang sesuatu. Tujuan dari teori unifikasi adalah untuk menyatukan berbagai pandangan tentang cinta. Cinta akan sulit dipahami dan mudah disalahtafsirkan bila tidak dimengerti melalui multiperspektif. Tulisan ini mengungkapkan pemikiran "Cinta" ala Nurcholish Madjid berdasarkan karya-karyanya. Mengingat luasnya problematika, maka Cinta akan dibahas berdasarkan perspektif neuroparemiofenomenologi, yakni: kolaborasi antara neurosains, paremiologi, dan fenomenologi. Terminologi "Cinta" dicari berdasarkan "Karya Lengkap Nurcholish Madjid" dengan Dr. Budhy Munawar-Rachman selaku ketua penyunting. Diharapkan perspektif neuroparemiofenomenologi dapat mengungkapkan makna fundamental "cinta" secara komprehensif dan paripurna.
... The baby's brain is a sponge toward environmental stimulation and cues. Indeed, the environment can act on the brain and influence its future development through many mechanisms: statistical learning [14], stress regulation [15], epigenetic mechanisms and transgenerational transmission of behavioral patterns [16], gene/environment interactions [17], synchronous interactive signals taking on the valence of a social signal amplified by certain hormones (e.g., oxytocin) [18], and cultural recycling of brain areas to promote learning [19]. ...
... The evolution of varied complex social systems and affiliative behaviors, including social attachment behavior, has intriguingly converged upon the nonapeptide hormones oxytocin (Oxt) and arginine vasopressin (AVP), and their homologues, despite arising in the context of diverse ecological pressures and social constraints (Bielsky & Young, 2004;Carter, 2017;Carter & Perkeybile, 2018;Donaldson & Young, 2008;Feldman, 2017;Insel et al., 1998;Opie et al., 2013;Reichard & Boesch, 2003). Following the initial establishment of Oxt function in the physiology surrounding parturition, namely uterine contraction and milk ejection, investigations of its role in maternal behaviors revealed that Oxtr signaling modulates a range of attachment behaviors across species (Lee et al., 2008;Nishimori et al., 1996;Pinto et al., 1967;Reynolds et al., 1950;Rich et al., 2014;Shapiro & Insel, 1992;Wakerley et al., 1973;Young et al., 1996). ...
Social attachments, the enduring bonds between individuals and groups, are essential to health and well-being. The appropriate formation and maintenance of social relationships depend upon a number of affective processes, including stress regulation, motivation, reward, as well as reciprocal interactions necessary for evaluating the affective state of others. A genetic, molecular, and neural circuit level understanding of social attachments therefore provides a powerful substrate for probing the affective processes associated with social behaviors. Socially monogamous species form long-term pair bonds, allowing us to investigate the mechanisms underlying attachment. Now, molecular genetic tools permit manipulations in monogamous species. Studies using these tools reveal new insights into the genetic and neuroendocrine factors that design and control the neural architecture underlying attachment behavior. We focus this discussion on the prairie vole and oxytocinergic signaling in this and related species as a model of attachment behavior that has been studied in the context of genetic and pharmacological manipulations. We consider developmental processes that impact the demonstration of bonding behavior across genetic backgrounds, the modularity of mechanisms underlying bonding behaviors, and the distributed circuitry supporting these behaviors. Incorporating such theoretical considerations when interpreting reverse genetic studies in the context of the rich ethological and pharmacological data collected in monogamous species provides an important framework for studies of attachment behavior in both animal models and studies of human relationships.
... Although the way in which attachment dimensions derive from the features of caregiving (intergenerational transmission) is still controversial in attachment theory (Verhage et al., 2016;van Ijzendoorn and Bakermans-Kranenburg, 2019), the dimensionality of attachment suggests a possible corresponding Frontiers in Psychology 03 frontiersin.org dimensionality of caregiving (Harrist and Waugh, 2002;Skinner et al., 2005;Bernier et al., 2014;Feldman, 2017;Hollenstein et al., 2017;Gagliardi, 2021). In other words, if several attachment dimensions can be identified as characterizing the child (or any "attacher"), some corresponding caregiving features should be identified as characterizing the mother (or any caregiver). ...
Attachment is an emotional bond between two people where one seeks care from the other. In the prototypical case, the child attaches to their mother. The most recent theoretical developments point out that attachment is multidimensional – meaning that the phenomenon pertains to multiple domains related to the relationship with the caregiver. However, researchers have so far modeled attachment computationally by mostly adopting a classical categorical (as opposed to dimensional) standpoint that sees the system as controlling caregiver proximity. In contrast, we adopt here a dimensional perspective (DP) and consider dimensions to be the system’s set-goals. We hypothesize that the resulting multidimensional controller should lead to valid (or even better) models of the phenomenon. To start testing this hypothesis, we built a DP-informed agent-based model of attachment inspired by the widely-studied Strange Situation Procedure. In this context, child and mother show the nature of attachment bonds through their behavioral and emotional expressions. By modeling them as point-agents moving in a two-dimensional arena, we simulated child-mother interactions for the avoidant and ambivalent attachment dimensions. The generated dynamical patterns – characterized by the alternation between approach and exploration – matched those described in the attachment literature, thereby confirming the implementability and validity of the DP.
... Acts of generosity tend to spread to people down the line, as people feel differently after hearing about or witnessing them and 'pay it forwards' (Fowler and Christakis 2010). Moreover, we have extraordinary levels of biological attunement to each other -the heart rate and gamma brain wave oscillations of mothers and babies and couples even coordinate in tune with each other, as well as their emotions and movements (Feldman 2017 There have even been many changes to the human face since our split with other apes which reflect our need to display our feelings and identify the feelings of others. These include the emergence of blushing and crying as signs of genuine emotions (Evans 2002), as well as changes in face shape and appearance (Bastir 2018;Godinho, Spikins, and O'Higgins 2018;Lacruz et al. 2019). ...
In Hidden Depths, Professor Penny Spikins explores how our emotional connections have shaped human ancestry. Focusing on three key transitions in human origins, Professor Spikins explains how the emotional capacities of our early ancestors evolved in response to ecological changes, much like similar changes in other social mammals. For each transition, dedicated chapters examine evolutionary pressures, responses in changes in human emotional capacities and the archaeological evidence for human social behaviours. Starting from our earliest origins, in Part One, Professor Spikins explores how after two million years ago, movement of human ancestors into a new ecological niche drove new types of collaboration, including care for vulnerable members of the group. Emotional adaptations lead to cognitive changes, as new connections based on compassion, generosity, trust and inclusion also changed our relationship to material things. Part Two explores a later key transition in human emotional capacities occurring after 300,000 years ago. At this time changes in social tolerance allowed ancestors of our own species to further reach out beyond their local group and care about distant allies, making human communities resilient to environmental changes. An increasingly close relationship to animals, and even to cherished possessions, appeared at this time, and can be explained through new human vulnerabilities and ways of seeking comfort and belonging. Lastly, Part Three focuses on the contrasts in emotional dispositions arising between ourselves and our close cousins, the Neanderthals. Neanderthals are revealed as equally caring yet emotionally different humans, who might, if things had been different, have been in our place today. This new narrative breaks away from traditional views of human evolution as exceptional or as a linear progression towards a more perfect form. Instead, our evolutionary history is situated within similar processes occurring in other mammals, and explained as one in which emotions, rather than ‘intellect’, were key to our evolutionary journey. Moreover, changes in emotional capacities and dispositions are seen as part of differing pathways each bringing strengths, weaknesses and compromises. These hidden depths provide an explanation for many of the emotional sensitivities and vulnerabilities which continue to influence our world today.
... A novel way of assessing dyadic interaction quality is the alignment of mothers' and infants' physiological processes-a construct called bio-behavioral synchrony (DiLorenzo et al., 2021;Feldman, 2012b;Reyna & Pickler, 2009). Synchronization of physiological rhythms emerges in late pregnancy and is suggested to be a critical component of human attachment, shaping later coordination of social behavior (Feldman, 2007;Feldman, 2017). Synchronization of biological processes can aid mother-infant dyads in the regulation of distress (DiLorenzo et al., 2021;Reyna & Pickler, 2009). ...
Skin‐to‐skin contact (SSC) between mothers and their infants has beneficial effects in both preterm and full‐term infants. Underlying mechanisms are largely unknown. This randomized controlled trial assessed whether daily SSC in full‐term mother–infant dyads: (1) decreases infants’ cortisol and behavioral reactivity to a mild naturalistic stressor, and (2) facilitates interaction quality between infants and mothers (i.e., improved maternal caregiving behavior and mother–infant adrenocortical synchrony). Pregnant Dutch women (N = 116) were recruited and randomly allocated to an SSC or care‐as‐usual condition. The SSC condition performed 1 h of SSC daily, from birth until postnatal week 5. In week 5, mothers bathed the infant (known mild stressor). Infant and maternal cortisol was sampled at baseline, 25 and 40 min after bathing, and infant and maternal behavior was rated. Results did not indicate effects of SSC on infant behavioral and cortisol reactivity to the bathing session. Similarly, no effect of SSC was found on maternal caregiving behavior and mother–infant adrenocortical synchrony. In conclusion, the findings provide no evidence that daily mother–infant SSC is associated with full‐term infants’ behavioral and adrenocortical stress reactivity or mother–infant interaction quality. Future studies should replicate these findings and unveil other potential mechanisms underlying beneficial effects of SSC.
Sadness regulation is crucial for maintaining the romantic relationships of couples. Interpersonal emotion regulation, including affective engagement (AE) and cognitive engagement (CE), activates social brain networks. However, it is unclear how AE and CE regulate sadness in couples through affective bonds. We recruited 30 heterosexual couple dyads and 30 heterosexual stranger dyads and collected functional near-infrared spectroscopy hyperscanning data while each dyad watched sad or neutral videos and while the regulator regulated the target's sadness. Then, we characterized interbrain synchronization (IBS) and Granger causality (GC). The results indicated that AE and CE were more effective for couples than for strangers and that sadness evaluation of female targets was lower than that of male targets. CE-induced IBS at CH13 (BA10, right middle frontal gyrus) was lower for female targets than for male targets, while no gender difference in AE was detected. GC change at CH13 during CE was lower in the sad condition for male targets than for female targets, while no gender difference in AE was discovered. These observations suggest that AE and CE activate affective bonds but that CE was more effective for regulating sadness in female targets, revealing different neural patterns of cognitive and affective sadness regulation in couples.
The fuzzy nature of categories of psychopathology, such as autism, leads to significant research challenges. Alternatively, focusing research on the study of a common set of important and well-defined psychological constructs across psychiatric conditions may make the fundamental etiological processes of psychopathology easier to discern and treat (Cuthbert, 2022). The development of the research domain criteria (RDoC) framework is designed to guide this new research approach (Insel et al., 2010). However, progress in research may be expected to continually refine and reorganize the understanding of the specifics of these mental processes (Cuthbert & Insel, 2013). Moreover, knowledge gleaned from the study of both normative and atypical development can be mutually informative in the evolution of our understanding of these fundamental processes. A case in point is the study of social attention. This Autism 101 commentary provides an educational summary of research over the last few decades indicates that social attention is major construct in the study of human social-cognitive development, autism and other forms of psychopathology. The commentary also describes how this research can inform the Social Process dimension of the RDoC framework.
In the recent years, discoveries in neuroscience have greatly impacted upon the
need to modify therapeutic practice starting from the evidence showing some
cerebral mechanisms capable of coping with mental health crisis and traumatic
events of the individual’s life history by redesigning the narrative plot and the
person’s sense of the Self. The emerging dialogue between neuroscience and
psychotherapy is increasingly intense and modern psychotherapy cannot ignore the
heritage deriving from studies about neuropsychological modification of memory
traces, neurobiology of attachment theory, cognitive mechanisms involved in
psychopathology, neurophysiology of human empathy, neuroimaging evidence
about psychotherapeutic treatment, and somatoform disorders connecting the brain
and the body. In the present article, we critically examined sectorial literature and
claimed that psychotherapy has to referred to a neuroscience-based approach in
order to adopt the most tailored interventions for specific groups of patients or
therapy settings. We also provided recommendations for care implementation in
clinical practice and illustrated challenges of future research.
This introduction aims to set out the potential as well as some of the pitfalls of the newly emerging area of the Social Neuroscience of Human Attachment (SoNeAt). To organize and interconnect the burgeoning empirical studies in this line of research, including those in this special issue, we outline a programmatic framework including an extension of our conceptual proposals NAMA and NAMDA to guide future research. We hope that this special issue will act as a stimulus for redoubling our efforts advancing the newly emerging SoNeAt area bridging attachment theory and social neuroscience.
Historical evidence from stimulation and lesion studies in animals and humans demonstrated a close association between the hypothalamus and typical and atypical socioemotional behavior. A central hypothalamic contribution to regulation of socioemotional responses was also provided indirectly by studies on oxytocin and arginine vasopressin. However, a limited number of studies have so far directly investigated the contribution of the hypothalamus in human socioemotional behavior. To reconsider the functional role of the evolutionarily conserved hypothalamic region in regulating human social behavior, here I provide a synthesis of neuroimaging investigations showing that the hypothalamus is involved in multiple and diverse facets of human socioemotional behavior through widespread functional interactions with other cortical and subcortical regions. These neuroimaging findings are then integrated with recent optogenetics studies in animals demonstrating that the hypothalamus plays a more active role in eliciting socioemotional responses and is not simply a downstream effector of higher-level brain systems. Building on the aforementioned evidence, the hypothalamus is argued to substantially contribute to a continuum of human socioemotional behaviors promoting survival and preservation of the species that extends from exploratory and approaching responses facilitating social bonding to aggressive and avoidance responses aimed to protect and defend formed relationships.
Compassion is a warm response of care and concern for those who are suffering, which drives individuals to devote their resources for the sake of others. A prominent neuroevolutionary framework grounds compassion in the neurobiology of the mammalian caregiving system. Accordingly, it has been suggested that the oxytocinergic system, which plays a central role in parental caregiving and bonding, provides the neurobiological foundation for compassion towards strangers. Yet, the specific role of oxytocin in compassion is far from clear. The current paper aims to target this gap and offer a theoretical framework that integrates the state-of-the-art literature on oxytocin with research on compassion. We suggest that oxytocin mediates compassion by enhancing the saliency of cues of pain and distress and discuss the plausible underlying neurobiological substrates. We further demonstrate how the proposed framework can account for individual differences in compassion, focusing on the effects of attachment on caregiving and support. The proposed framework integrates the current scientific understanding of oxytocin function with compassion-related processes. It thus highlights the largely ignored attentional processes in compassion and taps into the vast variability of responses in social contexts involving pain and suffering.
Myths, drama, and sacred texts have warned against the fragile nature of human love; the closer the affiliative bond, the quicker it can turn into hatred, suggesting similarities in the neurobiological underpinnings of love and hatred. Here, I offer a theoretical account on the neurobiology of hatred based on our model on the biology of human attachments and its three foundations; the oxytocin system, the "affiliative brain", comprising the neural network sustaining attachment, and biobehavioral synchrony, the process by which humans create a coupled biology through coordinated action. These systems mature in mammals in the context of the mother‐infant bond and then transfer to support life within social groups. During this transition, they partition to support affiliation and solidarity to one's group and fear and hatred toward out‐group based on minor variations in social behavior. I present the Tools of Dialogue© intervention for outgroup members based on social synchrony. Applied to Israeli and Palestinian youth and implementing RCT, we measured social behavior, attitudes, hormones, and social brain response before and after the 8‐session intervention. Youth receiving the intervention increased reciprocity and reduced hostile behavior toward outgroup, attenuated the neural marker of prejudice and increased neural empathic response, reduced cortisol and elevated oxytocin, and adapted attitudes of compromise. These neural changes predicted peacebuilding support 7 years later, when young adults can engage in civil responsibilities. Our intervention, the first to show long‐term effects of inter‐group intervention on brain and behavior, demonstrates how social synchrony can tilt the neurobiology of hatred toward the pole of affiliation.
Background
Whereas the maternal ‘blues’ has been widely researched, comparatively less is known about the “highs” following childbirth, and the relation between mothers and fathers’ mood in this early period. We aimed to investigate the association between maternal ‘blues’ and ‘highs’ with paternal postpartum mood (here described as ‘lows’ and ‘highs’) in the early postpartum and their associations with the quality of child bonding.
Methods
Women and their cohabitating male partners, fathers of the index child (N = 98 couples), attending an obstetric hospital unit completed questionnaires on mood, bonding and socio-demographics between the 3rd and the 5th postpartum day. We used generalised estimating equations to analyse the data.
Results
The ‘blues’ scores were higher in mothers, whereas ‘highs’ and bonding were higher in fathers. Maternal ‘blues’ were significantly correlated with paternal ‘lows’ (rs = .23, p < .05) and maternal ‘highs’ were also associated with paternal ‘highs’ (rs = .22, p < .05). Parental ‘highs’ were significantly associated with better baby bonding (B = .13, p = .02).
Conclusions
Our study demonstrates moderate associations between both ‘blues/lows’ and ‘highs’ in mothers and fathers shortly after the birth of the child. Associations between mood, particularly ‘highs’, and bonding were similar for mothers and fathers. Greater consideration of ‘blues/lows’ and ‘highs’ in both parents is needed to promote adjustment in the postpartum period.
Biobehavioral frameworks of attachment posit that mother–child dyads engage in physiological synchrony that is uniquely formative for children's neurobiological, social, and emotional development. Much of the work on mother–child physiological synchrony has focused on respiratory sinus arrhythmia (RSA). However, the strength of the existing evidence for mother–child RSA synchrony during interaction is unclear. Using meta‐analysis, we summarized results from 12 eligible studies comprising 14 samples and 1201 children ranging from infancy to adolescence (Mage = 5.68 years, SD = 4.13, range = 0.4–17 years) and their mothers. We found that there was a statistically significant, albeit modest, positive within‐dyad association between mother and child fluctuations in RSA. There also was evidence for significant heterogeneity across studies. Less mother–child RSA synchrony was observed in high‐risk samples characterized by clinical difficulties, history of maltreatment, or socioeconomic disadvantage. We did not find that mother–child RSA synchrony significantly differed by task context, mean child age, or by epoch length for computing RSA. Collectively, these findings suggest that mother–child dyads show correspondence in their fluctuations in RSA, and that RSA synchrony is disrupted in high‐risk contexts. Future directions and implications for the study of parent–child physiological synchrony are discussed.
Infants are born predisposed to develop strong relationships to those most likely to protect them; this emotional connection from the child to the protective adult is described as attachment (Ainsworth, 1979; Bowlby, 1983; Crittenden, 2006; Spierling et al., 2019). In turn, parents’ behavioral and physiological responses prime them to respond to attachment behaviors, such as crying, with protective behaviors (Ainsworth, 1979; Bowlby, 1983; Cong et al., 2015). This emotional connection from the attachment figure to the child is described as bonding (Scatliffe et al., 2019). Parental bonding is more often studied in biological mothers, but similar processes of bonding can occur in fathers and other caregivers who act in the role of parents (Bowlby, 1983; Cong et al., 2015; Dayton, Malone, & Brown, 2020). Relationships are a dyadic experience, influenced by both the parent and the child, dynamically changing over time, and shaped by the family context (Ainsworth, 1979; Crittenden, 2006; Wilson et al., 2000). Bonding and attachment are distinct concepts, even though the labels are sometimes used interchangeably (Habib & Lancaster, 2006; McNamara, Townsend, & Herbert, 2019).
Parenting is a critical influence on the development of children across the globe. This handbook brings together scholars with expertise on parenting science and interventions for a comprehensive review of current research. It begins with foundational theories and research topics, followed by sections on parenting children at different ages, factors that affect parenting such as parental mental health or socioeconomic status, and parenting children with different characteristics such as depressed and anxious children or youth who identify as LGBTQ. It concludes with a section on policy implications, as well as prevention and intervention programs that target parenting as a mechanism of change. Global perspectives and the cultural diversity of families are highlighted throughout. Offering in-depth analysis of key topics such as risky adolescent behavior, immigration policy, father engagement, family involvement in education, and balancing childcare and work, this is a vital resource for understanding the most effective policies to support parents in raising healthy children.
The mu opioid receptor (MOR) and the orphan GPR151 receptor are inhibitory G protein coupled receptors that are enriched in the habenula, a small brain region involved in aversion processing, addiction and mood disorders. While MOR expression in the brain is widespread, GPR151 expression is restricted to the habenula. In a previous report, we created conditional ChrnB4-Cre × Oprm1fl/fl (so-called B4MOR) mice, where MORs are deleted specifically in Chrnb4-positive neurons restricted to the habenula, and shown a role for these receptors in naloxone aversion. Here we characterized the implication of habenular MORs in social behaviors. B4MOR−/− mice and B4MOR+/+ mice were compared in several social behavior measures, including the chronic social stress defeat (CSDS) paradigm, the social preference (SP) test and social conditioned place preference (sCPP). In the CSDS, B4MOR−/− mice showed lower preference for the social target (unfamiliar mouse of a different strain) at baseline, providing a first indication of deficient social interactions in mice lacking habenular MORs. In the SP test, B4MOR−/− mice further showed reduced sociability for an unfamiliar conspecific mouse. In the sCPP, B4MOR−/− mice also showed impaired place preference for their previous familiar littermates after social isolation. We next created and tested Gpr151−/− mice in the SP test, and also found reduced social preference compared to Gpr151+/+ mice. Altogether our results support the underexplored notion that the habenula regulates social behaviors. Also, our data suggest that the inhibitory habenular MOR and GPR151 receptors normally promote social reward, possibly by dampening the aversive habenula activity.
Much has been documented on the association between stress and health. Both direct and indirect pathways have been identified and explored extensively, helping us understand trajectories from healthy individuals to reductions in well-being, and development of preclinical and disease states. Some of these pathways are well established within the field; physiology, affect regulation, and social relationships. The purpose of this review is to push beyond what is known separately about these pathways and provide a means to integrate them using one common mechanism. We propose that social touch, specifically affective touch, may be the missing active ingredient fundamental to our understanding of how close relationships contribute to stress and health. We provide empirical evidence detailing how affective touch is fundamental to the development of our stress systems, critical to the development of attachment bonds and subsequent social relationships across the life course. We will also explore how we can use this in applied contexts and incorporate it into existing interventions.
The absence of a healthy parent is not only an adverse childhood experience (ACE); it can result in multiple ACEs and complex trauma throughout a child’s life. Mental and physical illness, substance misuse, and trauma in the life of parents, caregivers, and significant others are described here. Mental health and substance use during pregnancy and parenting are discussed. Because of the complex links between genetics, epigenetics, and environmental exposures such as ACEs and other traumas, trauma survivors may be more likely to have a mental illness during parenting compared to those who have not experienced trauma. Trauma-informed mental healthcare is critical for breaking the cycle of intergenerational trauma. The >6 million deaths worldwide from COVID-19 represent children who lost a parent and/or other loved ones. Incarceration or other loss of a parent, caregiver, or significant others is discussed in relation to healthy bonding and attachment.KeywordsAdverse childhood experiencesACEsParental mental illnessParental illnessParental substance misuseParental traumaTraumaMental healthSubstance use during pregnancySubstance useFetal substance exposureGeneticsEpigeneticsIncarcerated parentLoss of a parentBondingAttachmentMaternal infant attachment
The interactions between species-specific predispositions and cultural plasticity in the development of human musical behavior have recently become the rationale for a possible Baldwinian origin of human musicality. In the previously suggested Baldwinian scenarios of music origin, social bonding has been indicated as the crucial adaptive value that became the main cause of the co-evolutionary process that led to our musicality. However, the adaptive value of social bonding does not explain the cultural variability of musical expressions that enabled the Baldwinian evolution of musicality. The main aim of this article is to show that free rider recognition, along with social bonding and signaling commitment, could have been a possible adaptive function of hominin musical rituals. In the proposed scenario, free rider recognition became a “flywheel” of the arms race between deception and cooperation. As a result, the interplay between the canalization and plasticity of musical learning became a part of music evolution. This process created a cultural niche in which hominin vocal learning was specialized in the imitation of discrete pitch and rhythm.
The transition to technologically-assisted communication has permeated all facets of human social life; yet, its impact on the social brain is still unknown and the effects may be particularly intense during periods of developmental transitions. Applying a two-brain perspective, the current preregistered study utilized hyperscanning EEG to measure brain-to-brain synchrony in 62 mother-child pairs at the transition to adolescence (child age; M = 12.26, range 10-14) during live face-to-face interaction versus technologically-assisted remote communication. The live interaction elicited 9 significant cross-brain links between densely inter-connected frontal and temporal areas in the beta range [14-30 Hz]. Mother's right frontal region connected with the child's right and left frontal, temporal, and central regions, suggesting its regulatory role in organizing the two-brain dynamics. In contrast, the remote interaction elicited only 1 significant cross-brain-cross-hemisphere link, attenuating the robust right-to-right-brain connectivity during live social moments that communicates socio-affective signals. Furthermore, while the level of social behavior was comparable between the two interactions, brain-behavior associations emerged only during the live exchange. Mother-child right temporal-temporal synchrony linked with moments of shared gaze and the degree of child engagement and empathic behavior correlated with right frontal-frontal synchrony. Our findings indicate that human co-presence is underpinned by specific neurobiological processes that should be studied in depth. Much further research is needed to tease apart whether the "Zoom fatigue" experienced during technological communication may stem, in part, from overload on more limited inter-brain connections and to address the potential cost of social technology for brain maturation, particularly among youth.
Se revisaron los principales cambios realizados por el psicoanálisis en la comprensión del desarrollo y
funcionamiento mental, mostrando que desde hace varias décadas algunas de sus propuestas armonizancon otras ciencias. Destacamos los enfoques de Stern, Sander y Trevarthen, quienes consideran que los
fenómenos mentales emergen en el marco de una matriz intersubjetiva al sincronizar tiempos
compartidos entre los cuidadores primarios y el bebé. Ello deriva en la regulación de funciones
fisiológicas básicas, considerando la crianza humana como un sistema biológico compartido. Estas
formulaciones se explayan en un nuevo campo científico denominado neurociencia social, el que
valiéndose del análisis interdisciplinario multinivel provee evidencias de que estructuras y funciones del
sistema nervioso están influidas por el entorno social. Desde esta perspectiva se destaca un nuevo marcoconceptual propuesto por Feldman, quien explicita los fundamentos neurobiológicos del apego, basados
en la sincronía bioconductual, el sistema oxitocina y el cerebro parental, revelando aspectos cruciales de
la interfaz mente-cuerpo y del pasaje de ritmos biológicos a ritmos sociales. Al demostrar que los circuitos
neurobiológicos constituidos en las relaciones tempranas son los mismos que se activan en los demás
vínculos significativos a lo largo de la vida, abre caminos promisorios para intervenciones preventivas y
terapéuticas en los más diversos ámbitos. Asimismo, se destaca que el psicoanálisis como estudio de la
subjetividad, al salir de su aislamiento inicial, presenta propuestas que contribuyen a otras disciplinas y al
mismo tiempo son enriquecidas por ella, abriendo vías promisorias para la investigación e intervenciones
preventivas y clínicas.
In Hidden Depths, Professor Penny Spikins explores how our emotional connections have shaped human ancestry. Focusing on three key transitions in human origins, Professor Spikins explains how the emotional capacities of our early ancestors evolved in response to ecological changes, much like similar changes in other social mammals. For each transition, dedicated chapters examine evolutionary pressures, responses in changes in human emotional capacities and the archaeological evidence for human social behaviours. Starting from our earliest origins, in Part One, Professor Spikins explores how after two million years ago, movement of human ancestors into a new ecological niche drove new types of collaboration, including care for vulnerable members of the group. Emotional adaptations lead to cognitive changes, as new connections based on compassion, generosity, trust and inclusion also changed our relationship to material things. Part Two explores a later key transition in human emotional capacities occurring after 300,000 years ago. At this time changes in social tolerance allowed ancestors of our own species to further reach out beyond their local group and care about distant allies, making human communities resilient to environmental changes. An increasingly close relationship to animals, and even to cherished possessions, appeared at this time, and can be explained through new human vulnerabilities and ways of seeking comfort and belonging. Lastly, Part Three focuses on the contrasts in emotional dispositions arising between ourselves and our close cousins, the Neanderthals. Neanderthals are revealed as equally caring yet emotionally different humans, who might, if things had been different, have been in our place today. This new narrative breaks away from traditional views of human evolution as exceptional or as a linear progression towards a more perfect form. Instead, our evolutionary history is situated within similar processes occurring in other mammals, and explained as one in which emotions, rather than ‘intellect’, were key to our evolutionary journey. Moreover, changes in emotional capacities and dispositions are seen as part of differing pathways each bringing strengths, weaknesses and compromises. These hidden depths provide an explanation for many of the emotional sensitivities and vulnerabilities which continue to influence our world today.
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.
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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http://www.sciencedirect.com/science/article/pii/S2352154616300365
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.
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.
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.