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Social Decision-Making in Animals

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Front. Behav. Neurosci. | doi: 10.3389/fnbeh.2018.00272

Oxytocin manipulation alters neural activity in response to social stimuli in eusocial naked mole-rats

 Mariela Faykoo-Martinez1*,  Melissa M. Holmes1, 2 and Skyler J. Mooney2, 3
  • 1University of Toronto, Canada
  • 2University of Toronto Mississauga, Canada
  • 3Sunnybrook Research Institute (SRI), Canada

The social decision-making network is a conserved neural circuit that modulates a range of social behaviors via context-specific patterns of activation that may be controlled in part by oxytocinergic signalling. We have previously characterized oxytocin’s influence on prosociality in the naked mole-rat, a eusocial mammalian species, and its altered neural distribution between animals of differing social status. Here, we asked two questions: 1) do patterns of activation in the social decision-making network vary by social context and 2) is functional connectivity of the social decision-making network altered by oxytocin manipulation? Adult subordinate naked mole-rats were exposed to one of three types of stimuli (three behavioral paradigms: familiar adult conspecific, unfamiliar adult conspecific, or familiar pups) while manipulating oxytocin (three manipulations: saline, oxytocin, or oxytocin antagonist). Immediate early gene c-Fos activity was quantified using immunohistochemistry across social decision-making network regions. Network analyses indicated that the social decision-making network is conserved in naked mole-rats and functions in a context-dependent manner. Specific brain regions were recruited with each behavioral paradigm suggesting a role for the nucleus accumbens in social valence and sociosexual interaction, the prefrontal cortex in assessing/establishing social dominance, and the hippocampus in pup recognition. Furthermore, while oxytocin manipulation was generally disruptive to coordinated neural activity, the specific effects were context-dependent supporting the hypothesis that oxytocinergic signalling promotes context appropriate social behaviors by modulating co-ordinated activity of the social decision-making network.

ACC=Anterior cingulate cortex, AH=Anterior hypothalamus, AntPVN=Anterior paraventricular nucleus, AON=Anterior olfactory nucleus, BLA=Basolateral amygdala, BNST=Bed nucleus of the stria terminalis, CeA=Central amygdala, CG=Cingulate cortex, CA1=Cornu ammonis 1, CA2=Cornu ammonis 2, CA3=Cornu ammonis 3, Caudate=Caudate putamen, dDG=dorsal dentate gyrus, IL=Infralimbic cortex, LS=Lateral septum, MeA=Medial amygdala, MOB=Main olfactory bulb, MS=Medial septum, NAcc=Nucleus accumbens, PG=periaqueductal grey, PIC=Piriform cortex, PO=Pre-optic area, PostPVN=Posterior paraventricular nucleus, PrL=Pre-limbic cortex, SON=Supraoptic nucleus, Tu=Olfactory tubercle, vDG=Ventral dentate gyrus, VMH=Ventromedial hypothalamus, VP=Ventral pallidum, VTA=Ventral tegmental area

Keywords: Social decision-making network, naked mole-rat, eusociality, Immediate early Gene, Social Behavior, functional connectivity

Received: 12 Jul 2018; Accepted: 23 Oct 2018.

Edited by:

James P. Curley, University of Texas at Austin, United States

Reviewed by:

Kevin D. Broad, Institute of Ophthalmology, University College London, United Kingdom
David A. Freeman, University of Memphis, United States  

Copyright: © 2018 Faykoo-Martinez, Holmes and Mooney. 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) and the copyright owner(s) 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.

* Correspondence: Ms. Mariela Faykoo-Martinez, University of Toronto, Toronto, Canada, m.faykoomartinez@mail.utoronto.ca