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      Social creatures: Model animal systems for studying the neuroendocrine mechanisms of social behaviour

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          Abstract

          The interaction of animals with conspecifics, termed social behaviour, has a major impact on the survival of many vertebrate species. Neuropeptide hormones modulate the underlying physiology that governs social interactions, and many findings concerning the neuroendocrine mechanisms of social behaviours have been extrapolated from animal models to humans. Neurones expressing neuropeptides show similar distribution patterns within the hypothalamic nucleus, even when evolutionarily distant species are compared. During evolution, hypothalamic neuropeptides and releasing hormones have retained not only their structures, but also their biological functions, including their effects on behaviour. Here, we review the current understanding of the mechanisms of social behaviours in several classes of animals, such as worms, insects and fish, as well as laboratory, wild and domesticated mammals.

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          The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis.

          All animals evaluate the salience of external stimuli and integrate them with internal physiological information into adaptive behavior. Natural and sexual selection impinge on these processes, yet our understanding of behavioral decision-making mechanisms and their evolution is still very limited. Insights from mammals indicate that two neural circuits are of crucial importance in this context: the social behavior network and the mesolimbic reward system. Here we review evidence from neurochemical, tract-tracing, developmental, and functional lesion/stimulation studies that delineates homology relationships for most of the nodes of these two circuits across the five major vertebrate lineages: mammals, birds, reptiles, amphibians, and teleost fish. We provide for the first time a comprehensive comparative analysis of the two neural circuits and conclude that they were already present in early vertebrates. We also propose that these circuits form a larger social decision-making (SDM) network that regulates adaptive behavior. Our synthesis thus provides an important foundation for understanding the evolution of the neural mechanisms underlying reward processing and behavioral regulation. Copyright © 2011 Wiley-Liss, Inc.
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            The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior.

            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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              Social evolution. Oxytocin-gaze positive loop and the coevolution of human-dog bonds.

              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.
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                Author and article information

                Contributors
                mike.ludwig@ed.ac.uk
                Journal
                J Neuroendocrinol
                J. Neuroendocrinol
                10.1111/(ISSN)1365-2826
                JNE
                Journal of Neuroendocrinology
                John Wiley and Sons Inc. (Hoboken )
                0953-8194
                1365-2826
                28 November 2019
                December 2019
                : 31
                : 12 ( doiID: 10.1111/jne.v31.12 )
                : e12807
                Affiliations
                [ 1 ] Sea Mammal Research Unit Scottish Oceans Institute University of St Andrews St Andrews UK
                [ 2 ] Department of Behavioural and Molecular Neurobiology University of Regensburg Regensburg Germany
                [ 3 ] Department of Molecular Cell Biology Weizmann Institute of Science Rehovot Israel
                [ 4 ] Centre for Discovery Brain Sciences University of Edinburgh Edinburgh UK
                [ 5 ] Centre for Neuroendocrinology Department of Immunology University of Pretoria Pretoria South Africa
                Author notes
                [*] [* ] Correspondence

                Mike Ludwig, Centre for Discovery Brain Sciences, Hugh Robson Building, George Square, Edinburgh, EH8 9XD, UK.

                Email: mike.ludwig@ 123456ed.ac.uk

                Author information
                https://orcid.org/0000-0002-6212-9710
                https://orcid.org/0000-0002-0759-8143
                https://orcid.org/0000-0002-3896-1881
                https://orcid.org/0000-0001-7886-3226
                https://orcid.org/0000-0003-4036-5701
                https://orcid.org/0000-0001-9983-4950
                Article
                JNE12807
                10.1111/jne.12807
                6916380
                31679160
                c8011c0f-4f83-4daf-861b-308bc78ae1c6
                © 2019 The Authors. Journal of Neuroendocrinology published by John Wiley & Sons Ltd on behalf of British Society for Neuroendocrinology

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 28 August 2019
                : 11 October 2019
                : 30 October 2019
                Page count
                Figures: 1, Tables: 0, Pages: 12, Words: 25134
                Funding
                Funded by: Medical Research Council , open-funder-registry 10.13039/501100000265;
                Award ID: MR/N004574/1
                Funded by: Biotechnology and Biological Sciences Research Council , open-funder-registry 10.13039/501100000268;
                Award ID: BB/S000224/1
                Award ID: BB/S000801
                Funded by: Deutsche Forschungsgemeinschaft , open-funder-registry 10.13039/501100001659;
                Award ID: BO 1958/8‐2
                Award ID: GRK 2174
                Funded by: United States‐Israel Binational Science Foundation , open-funder-registry 10.13039/501100001742;
                Award ID: #2017325
                Funded by: Israel Science Foundation , open-funder-registry 10.13039/501100003977;
                Award ID: #1511/16
                Funded by: Wellcome Trust , open-funder-registry 10.13039/100004440;
                Award ID: 109614/Z/15/Z
                Categories
                Review Article
                Review Articles
                Custom metadata
                2.0
                December 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.3 mode:remove_FC converted:17.12.2019

                Endocrinology & Diabetes
                model animals,neuropeptides,oxytocin,social behaviours
                Endocrinology & Diabetes
                model animals, neuropeptides, oxytocin, social behaviours

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