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      Sensitive Periods, Vasotocin-Family Peptides, and the Evolution and Development of Social Behavior

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          Abstract

          Nonapeptides, by modulating the activity of neural circuits in specific social contexts, provide an important mechanism underlying the evolution of diverse behavioral phenotypes across vertebrate taxa. Vasotocin-family nonapeptides, in particular, have been found to be involved in behavioral plasticity and diversity in social behavior, including seasonal variation, sexual dimorphism, and species differences. Although nonapeptides have been the focus of a great deal of research over the last several decades, the vast majority of this work has focused on adults. However, behavioral diversity may also be explained by the ways in which these peptides shape neural circuits and influence social processes during development. In this review, I synthesize comparative work on vasotocin-family peptides during development and classic work on early forms of social learning in developmental psychobiology. I also summarize recent work demonstrating that early life manipulations of the nonapeptide system alter attachment, affiliation, and vocal learning in zebra finches. I thus hypothesize that vasotocin-family peptides are involved in the evolution of social behaviors through their influence on learning during sensitive periods in social development.

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          Most cited references 159

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          Attachments beyond infancy.

           M D Ainsworth (1989)
          Attachment theory is extended to pertain to developmental changes in the nature of children's attachments to parents and surrogate figures during the years beyond infancy, and to the nature of other affectional bonds throughout the life cycle. Various types of affectional bonds are examined in terms of the behavioral systems characteristic of each and the ways in which these systems interact. Specifically, the following are discussed: (a) the caregiving system that underlies parents' bonds to their children, and a comparison of these bonds with children's attachments to their parents; (b) sexual pair-bonds and their basic components entailing the reproductive, attachment, and caregiving systems; (c) friendships both in childhood and adulthood, the behavioral systems underlying them, and under what circumstances they may become enduring bonds; and (d) kinship bonds (other than those linking parents and their children) and why they may be especially enduring.
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            Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress.

            Variations in maternal care affect the development of individual differences in neuroendocrine responses to stress in rats. As adults, the offspring of mothers that exhibited more licking and grooming of pups during the first 10 days of life showed reduced plasma adrenocorticotropic hormone and corticosterone responses to acute stress, increased hippocampal glucocorticoid receptor messenger RNA expression, enhanced glucocorticoid feedback sensitivity, and decreased levels of hypothalamic corticotropin-releasing hormone messenger RNA. Each measure was significantly correlated with the frequency of maternal licking and grooming (all r's > -0.6). These findings suggest that maternal behavior serves to "program" hypothalamic-pituitary-adrenal responses to stress in the offspring.
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              The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior.

               Thomas Insel (2010)
              Social neuroscience is rapidly exploring the complex territory between perception and action where recognition, value, and meaning are instantiated. This review follows the trail of research on oxytocin and vasopressin as an exemplar of one path for exploring the "dark matter" of social neuroscience. Studies across vertebrate species suggest that these neuropeptides are important for social cognition, with gender- and steroid-dependent effects. Comparative research in voles yields a model based on interspecies and intraspecies variation of the geography of oxytocin receptors and vasopressin V1a receptors in the forebrain. Highly affiliative species have receptors in brain circuits related to reward or reinforcement. The neuroanatomical distribution of these receptors may be guided by variations in the regulatory regions of their respective genes. This review describes the promises and problems of extrapolating these findings to human social cognition, with specific reference to the social deficits of autism. (c) 2010 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Front Endocrinol (Lausanne)
                Front Endocrinol (Lausanne)
                Front. Endocrinol.
                Frontiers in Endocrinology
                Frontiers Media S.A.
                1664-2392
                02 August 2017
                2017
                : 8
                Affiliations
                1Department of Psychology, Cornell University , Ithaca, NY, United States
                2School of Biological Sciences, Georgia Institute of Technology , Atlanta, GA, United States
                Author notes

                Edited by: Aras Petrulis, Georgia State University, United States

                Reviewed by: Bice Chini, Consiglio Nazionale Delle Ricerche (CNR), Italy; Illana Gozes, Tel Aviv University, Israel; Sean Veney, Kent State University, United States

                *Correspondence: Nicole M. Baran, nicole.baran@ 123456biology.gatech.edu

                Specialty section: This article was submitted to Neuroendocrine Science, a section of the journal Frontiers in Endocrinology

                Article
                10.3389/fendo.2017.00189
                5539493
                Copyright © 2017 Baran.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 1, Tables: 2, Equations: 0, References: 167, Pages: 12, Words: 11175
                Funding
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: IOS – 1310908, IOS – 1146891
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: 5T32HD055177-05
                Categories
                Endocrinology
                Review

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