Early rearing history influences oxytocin receptor epigenetic regulation in rhesus macaques

Baker, Mairead; Lindell, Stephen G.; Driscoll, Carlos A.; Zhou, Zhifeng; Yuan, Qiaoping; Schwandt, Melanie L.; Miller-Crews, Isaac; Simpson, Elizabeth A.; Paukner, Annika; Ferrari, Pier Francesco; Sindhu, Ravi Kumar; Razaqyar, M.; Sommer, Wolfgang; López, Juan F.; Thompson, Robert C.; Goldman, David; Heilig, Markus; Higley, J. Dee; Suomi, Stephen J.; Barr, Christina S.

doi:10.1073/pnas.1706206114

Cited by 52 publications

(41 citation statements)

References 61 publications

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“…Oxytocin‐expressing neurons include a wide variety of cell types, such as GABAergic interneurons, glutamatergic pyramidal cells, and other peptidergic cells 34,37,38 . Oxytocin integrates brain and periphery, incorporates massive epigenetic inputs, and is particularly related to attachment experiences 39,40 . It increases plasticity in the hippocampal network to increase salience of the attachment target 41 , and attachment experiences shape oxytocin receptors availability 42 .…”

Section: Core Components Of the Neurobiology Of Affiliationmentioning

confidence: 99%

What is resilience: an affiliative neuroscience approach

2020

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Resilience – a key topic in clinical science and practice – still lacks a clear conceptualization that integrates its evolutionary and human‐specific features, refrains from exclusive focus on fear physiology, incorporates a developmental approach, and, most importantly, is not based on the negation (i.e., absence of symptoms following trauma). Building on the initial condition of mammals, whose brain matures in the context of the mother's body and caregiving behavior, we argue that systems and processes that participate in tuning the brain to the social ecology and adapting to its hardships mark the construct of resilience. These include the oxytocin system, the affiliative brain, and biobehavioral synchrony, all characterized by great flexibility across phylogenesis and ontogenesis. Three core features of resilience are outlined: plasticity, sociality and meaning. Mechanisms of sociality by which coordinated action supports diversity, endurance and adaptation are described across animal evolution. Humans' biobehavioral synchrony matures from maternal attuned behavior in the postpartum to adult‐adult relationships of empathy, perspective‐taking and intimacy, and extends from the mother‐child relationship to other affiliative bonds throughout life, charting a fundamental trajectory in the development of resilience. Findings from three high‐risk cohorts, each tapping a distinct disruption to maternal‐infant bonding (prematurity, maternal depression, and early life stress/trauma), and followed from birth to adolescence/young adulthood, demonstrate how components of the neurobiology of affiliation confer resilience and uniquely shape the social brain.

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Section: Core Components Of the Neurobiology Of Affiliationmentioning

confidence: 99%

What is resilience: an affiliative neuroscience approach

2020

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“…116 On the other hand, deprivation of early maternal care in rhesus macaques has been reported to suppress expression of the oxytocin receptor in the hippocampus via epigenetic regulation and induce higher separation anxiety, which was rescued by a certain oxytocin receptor gene single nucleotide polymorphism (SNP). 117 Neonatal maternal separation has also been shown to induce larger responses to noxious stimuli in an oxytocinand histone deacetylase-dependent manner in rats. 118 All of these reported findings suggest that expression of the oxytocin receptor is influenced by early experiences and modulates stress responsiveness in adulthood.…”

Section: Influence Of Early-life Experiences On Stress Responsesmentioning

confidence: 99%

Role of oxytocin in the control of stress and food intake

Onaka

Takayanagi

2019

J Neuroendocrinology

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Oxytocin neurones in the hypothalamus are activated by stressful stimuli and food intake. The oxytocin receptor is located in various brain regions, including the sensory information‐processing cerebral cortex; the cognitive information‐processing prefrontal cortex; reward‐related regions such as the ventral tegmental areas, nucleus accumbens and raphe nucleus; stress‐related areas such as the amygdala, hippocampus, ventrolateral part of the ventromedial hypothalamus and ventrolateral periaqueductal gray; homeostasis‐controlling hypothalamus; and the dorsal motor complex controlling intestinal functions. Oxytocin affects behavioural and neuroendocrine stress responses and terminates food intake by acting on the metabolic or nutritional homeostasis system, modulating emotional processing, reducing reward values of food intake, and facilitating sensory and cognitive processing via multiple brain regions. Oxytocin also plays a role in interactive actions between stress and food intake and contributes to adaptive active coping behaviours.

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“…Maternal care, or lack thereof, also seems to impact the expression of OXTR in rhesus monkeys. Indeed, peer-reared infants, compared to their mother-reared counterparts, showed altered epigenetic regulation of the OXTR gene (resulting in decreased OXTR mRNA in the hippocampus), and higher levels of separation anxiety and arousal (Baker et al, 2017). Subsequently it was shown that a naturally occurring gain-of-function nonsynonymous OXTR polymorphism partially rescued these behavioral differences.…”

Section: Studies Of Oxytocin In Non-human Primatesmentioning

confidence: 99%

Bridging the gap between rodents and humans: The role of non‐human primates in oxytocin research

Putnam

Young²,

Gothard

2018

American J Primatol

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Oxytocin (OT), a neuropeptide that acts in the brain as a neuromodulator, has been long known to shape maternal physiology and behavior in mammals, however its role in regulating social cognition and behavior in primates has come to the forefront only in the recent decade. Many of the current perspectives on the role of OT in modulating social behavior emerged first from studies in rodents, where invasive techniques with a high degree of precision have permitted the mechanistic dissection of OT-related behaviors, as well as their underlying neural circuits in exquisite detail. In parallel, behavioral and imaging studies in humans have suggested that brain OT may similarly influence human social behavior and neural activity. These studies in rodents and humans have spurred interest in the therapeutic potential of targeting the OT system to remedy deficits in social cognition and behavior that are present across numerous psychiatric disorders. Yet there remains a tremendous gap in our mechanistic understanding of the influence of brain OT on social neural circuitry between rodents and man. In fact, very little is known regarding the neural mechanisms by which exogenous or endogenous OT influences human social cognition, limiting its therapeutic potential. Here we discuss how non-human primates (NHPs) are uniquely positioned to now bridge the gaps in knowledge provided by the precise circuit-level approaches widely used in rodent models and the behavioral, imaging, and clinical studies in humans. This review provides a perspective on what has been achieved, and what can be expected from exploring the role of OT in shaping social behaviors in NHPs in the coming years.

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Early rearing history influences oxytocin receptor epigenetic regulation in rhesus macaques

Cited by 52 publications

References 61 publications

What is resilience: an affiliative neuroscience approach

What is resilience: an affiliative neuroscience approach

Role of oxytocin in the control of stress and food intake

Bridging the gap between rodents and humans: The role of non‐human primates in oxytocin research

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