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      Oxytocin and the Neurobiology of Prosocial Behavior

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          Abstract

          Humans are an unusually prosocial species, who engage in social behaviors that include altruism—whereby an individual engages in costly or risky acts to improve the welfare of another person—care, and cooperation. Current perspectives on the neurobiology of human prosociality suggest that it is deeply rooted in the neuroendocrine architecture of the social brain and emphasize the modulatory role of the neuropeptide hormone oxytocin. In this review, we provide a conceptual overview of the neurobiology of prosocial behavior with a focus on oxytocin’s modulatory role in human prosociality. Specifically, we aim to encourage a better understanding of the peptide’s susceptibility to diverse factors that produce heterogeneity in outcomes and the resulting methodological implications for measuring the behavioral effects of oxytocin in humans. After providing an overview of the state-of-the-art research on oxytocin’s exogenous use, we elaborate on the peptide’s modulatory role in the context of care-based altruism, cooperation, and conflict and discuss its potential for therapeutic interventions in psychiatric disorders characterized by social dysfunction.

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          Most cited references153

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          Oxytocin, vasopressin, and the neurogenetics of sociality.

          There is growing evidence that the neuropeptides oxytocin and vasopressin modulate complex social behavior and social cognition. These ancient neuropeptides display a marked conservation in gene structure and expression, yet diversity in the genetic regulation of their receptors seems to underlie natural variation in social behavior, both between and within species. Human studies are beginning to explore the roles of these neuropeptides in social cognition and behavior and suggest that variation in the genes encoding their receptors may contribute to variation in human social behavior by altering brain function. Understanding the neurobiology and neurogenetics of social cognition and behavior has important implications, both clinically and for society.
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            Oxytocin modulates neural circuitry for social cognition and fear in humans.

            In non-human mammals, the neuropeptide oxytocin is a key mediator of complex emotional and social behaviors, including attachment, social recognition, and aggression. Oxytocin reduces anxiety and impacts on fear conditioning and extinction. Recently, oxytocin administration in humans was shown to increase trust, suggesting involvement of the amygdala, a central component of the neurocircuitry of fear and social cognition that has been linked to trust and highly expresses oxytocin receptors in many mammals. However, no human data on the effects of this peptide on brain function were available. Here, we show that human amygdala function is strongly modulated by oxytocin. We used functional magnetic resonance imaging to image amygdala activation by fear-inducing visual stimuli in 15 healthy males after double-blind crossover intranasal application of placebo or oxytocin. Compared with placebo, oxytocin potently reduced activation of the amygdala and reduced coupling of the amygdala to brainstem regions implicated in autonomic and behavioral manifestations of fear. Our results indicate a neural mechanism for the effects of oxytocin in social cognition in the human brain and provide a methodology and rationale for exploring therapeutic strategies in disorders in which abnormal amygdala function has been implicated, such as social phobia or autism.
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              Neuroendocrine perspectives on social attachment and love.

              The purpose of this paper is to review existing behavioral and neuroendocrine perspectives on social attachment and love. Both love and social attachments function to facilitate reproduction, provide a sense of safety, and reduce anxiety or stress. Because social attachment is an essential component of love, understanding attachment formation is an important step toward identifying the neurobiological substrates of love. Studies of pair bonding in monogamous rodents, such as prairie voles, and maternal attachment in precocial ungulates offer the most accessible animal models for the study of mechanisms underlying selective social attachments and the propensity to develop social bonds. Parental behavior and sexual behavior, even in the absence of selective social behaviors, are associated with the concept of love; the analysis of reproductive behaviors, which is far more extensive than our understanding of social attachment, also suggests neuroendocrine substrates for love. A review of these literatures reveals a recurrent association between high levels of activity in the hypothalamic pituitary adrenal (HPA) axis and the subsequent expression of social behaviors and attachments. Positive social behaviors, including social bonds, may reduce HPA axis activity, while in some cases negative social interactions can have the opposite effect. Central neuropeptides, and especially oxytocin and vasopressin have been implicated both in social bonding and in the central control of the HPA axis. In prairie voles, which show clear evidence of pair bonds, oxytocin is capable of increasing positive social behaviors and both oxytocin and social interactions reduce activity in the HPA axis. Social interactions and attachment involve endocrine systems capable of decreasing HPA reactivity and modulating the autonomic nervous system, perhaps accounting for health benefits that are attributed to loving relationships.
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                Author and article information

                Journal
                Neuroscientist
                Neuroscientist
                NRO
                spnro
                The Neuroscientist
                SAGE Publications (Sage CA: Los Angeles, CA )
                1073-8584
                1089-4098
                26 September 2020
                December 2021
                : 27
                : 6
                : 604-619
                Affiliations
                [1 ]Department of Psychiatry, Carl von Ossietzky University Oldenburg, Oldenburg, Lower Saxony, Germany
                [2 ]Department of Psychology, Georgetown University, Washington, DC, USA
                [3 ]Clinical Psychoneuroendocrinology and Neuropsychopharmacology Section, National Institute on Drug Abuse Intramural Research Program, Baltimore, MD, USA
                [4 ]National Institute on Alcohol Abuse and Alcoholism Division of Intramural Clinical and Biological Research, National Institutes of Health, Bethesda, MD, USA
                [5 ]Research Center Neurosensory Science, Carl von Ossietzky University Oldenburg, Oldenburg, Lower Saxony, Germany
                Author notes
                [*]René Hurlemann, Department of Psychiatry, Head, NEMO (Neuromodulation of Emotion) Lab, School of Medicine & Health Sciences, Carl von Ossietzky University of Oldenburg, Oldenburg, Lower Saxony, Germany. Email: renehurlemann@ 123456icloud.com
                [*]

                Nina Marsh and Abigail A. Marsh contributed equally to this work and have shared first authorship.

                Article
                10.1177_1073858420960111
                10.1177/1073858420960111
                8640275
                32981445
                0ce9c34b-d914-4813-b436-4e57bd47a371
                © The Author(s) 2020

                This article is distributed under the terms of the Creative Commons Attribution 4.0 License ( https://creativecommons.org/licenses/by/4.0/) which permits any use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access page ( https://us.sagepub.com/en-us/nam/open-access-at-sage).

                History
                Funding
                Funded by: National Institute on Drug Abuse, FundRef https://doi.org/10.13039/100000026;
                Funded by: National Institute on Alcohol Abuse and Alcoholism, FundRef https://doi.org/10.13039/100000027;
                Funded by: German Research Foundation, ;
                Award ID: HU 1302/11-1
                Categories
                Reviews
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                oxytocin,prosocial behavior,altruism,care,social neuroscience

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