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      The neural mechanisms and circuitry of the pair bond

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      Author(s): 1 , 1 , 2 , 3 , *
      Publication date PMC-release:
      Journal: Nature reviews. Neuroscience

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          Abstract

          Love is one of our most powerful emotions, inspiring some of the greatest art, literature and conquests of human history. Although aspects of love are surely unique to our species, human romantic relationships are displays of a mating system characterized by pair bonding, likely built on ancient foundational neural mechanisms governing individual recognition, social reward, territorial behaviour and maternal nurturing. Studies in monogamous prairie voles and mice have revealed precise neural mechanisms regulating processes essential for the pairbond. Here, we discuss current viewpoints on the biology underlying pair bond formation, its maintenance and associated behaviours from neural and evolutionary perspectives.

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          Social reward requires coordinated activity of accumbens oxytocin and 5HT

          Gül Dölen, Ayeh Darvishzadeh, Kee Huang … (2013)
          Social behaviors in species as diverse as honey bees and humans promote group survival but often come at some cost to the individual. Although reinforcement of adaptive social interactions is ostensibly required for the evolutionary persistence of these behaviors, the neural mechanisms by which social reward is encoded by the brain are largely unknown. Here we demonstrate that in mice oxytocin (OT) acts as a social reinforcement signal within the nucleus accumbens (NAc) core, where it elicits a presynaptically expressed long-term depression of excitatory synaptic transmission in medium spiny neurons. Although the NAc receives OT receptor-containing inputs from several brain regions, genetic deletion of these receptors specifically from dorsal raphe nucleus, which provides serotonergic (5-HT) innervation to the NAc, abolishes the reinforcing properties of social interaction. Furthermore, OT-induced synaptic plasticity requires activation of NAc 5-HT1b receptors, the blockade of which prevents social reward. These results demonstrate that the rewarding properties of social interaction in mice require the coordinated activity of OT and 5-HT in the NAc, a mechanistic insight with implications for understanding the pathogenesis of social dysfunction in neuropsychiatric disorders such as autism.
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            Oxytocin Enables Maternal Behavior by Balancing Cortical Inhibition

            Bianca Marlin, Mariela Mitre, James A D'amour … (2015)
            Oxytocin is important for social interactions and maternal behavior. However, little is known about when, where, and how oxytocin modulates neural circuits to improve social cognition. Here we show how oxytocin enables pup retrieval behavior in female mice by enhancing auditory cortical pup call responses. Retrieval behavior required left but not right auditory cortex, was accelerated by oxytocin in left auditory cortex, and oxytocin receptors were preferentially expressed in left auditory cortex. Neural responses to pup calls were lateralized, with co-tuned and temporally-precise excitatory and inhibitory responses in left cortex of maternal but not pup-naive adults. Finally, pairing calls with oxytocin enhanced responses by balancing the magnitude and timing of inhibition with excitation. Our results describe fundamental synaptic mechanisms by which oxytocin increases the salience of acoustic social stimuli. Furthermore, oxytocin-induced plasticity provides a biological basis for lateralization of auditory cortical processing.
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              Social evolution. Oxytocin-gaze positive loop and the coevolution of human-dog bonds.

              Miho Nagasawa, Shouhei Mitsui, Shiori En … (2015)
              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

                Journal
                Journal ID (nlm-journal-id): 100962781
                Journal ID (pubmed-jr-id): 22270
                Journal ID (nlm-ta): Nat Rev Neurosci
                Journal ID (iso-abbrev): Nat. Rev. Neurosci.
                Title: Nature reviews. Neuroscience
                ISSN (Print): 1471-003X
                ISSN (Electronic): 1471-0048
                Publication date Nihms-submitted: 25 October 2018
                Publication date (Print): November 2018
                Publication date PMC-release: 01 November 2019
                Volume: 19
                Issue: 11
                Pages: 643-654
                Affiliations
                [1 ]Silvio O. Conte Center for Oxytocin and Social Cognition, Center for Translational Social Neuroscience, Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA.
                [2 ]Center for Social Neural Networks, University of Tsukuba, Tsukuba, Japan.
                [3 ]Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, Atlanta, GA, USA.
                Author notes

                Author contributions

                H.W. and L.J.Y. researched data for the article and made substantial contributions to the discussion of content and to the writing, review and editing of the manuscript before submission.

                Article
                Accession ID: PMC6283620 Pmcid ID: PMC6283620 Pmc-uid ID: 6283620 Manuscript ID: nihpa994226
                DOI: 10.1038/s41583-018-0072-6
                PMC ID: 6283620
                PubMed ID: 30301953
                SO-VID: 78cf1750-6764-4bba-ba26-66cd8ce37508
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