The social network: Neural control of sex differences in reproductive behaviors, motivation, and response to social isolation

Abstract

Social animal species present a vast repertoire of social interactions when encountering conspecifics. Reproduction-related behaviors, such as mating, parental care, and aggression, are some of the most rewarding types of social interactions and are also the most sexually dimorphic ones. This review focuses on rodent species and summarizes recent advances in neuroscience research that link sexually dimorphic reproductive behaviors to sexual dimorphism in their underlying neuronal circuits. Specifically, we present a few possible mechanisms governing sexually-dimorphic behaviors, by hypothalamic and reward-related brain regions. Sex differences in the neural response to social isolation in adulthood are also discussed, as well as future directions for comparative studies with naturally solitary species.

Figure 1

Diversity of social strategies within the Rodentia order: the uncharted territories of social neuroscience. Within the Rodentia order, the social scale ranges from eusocial and social to solitary, even within the same subfamilies and between closely related species [42,219]. Interestingly, within these diverse social lifestyles, an additional layer of diversity exists with respect to sexual dimorphism in parental care and aggression [220]. Presented from top to bottom—eusocial rodents: naked mole-rat [219,221,222], Damaraland mole-rat (picture courtesy of Dr. Markus Zöttl) [223, 224, 225]; social group/monogamous living: house mouse [33,59,219], prairie vole (picture courtesy of Prof. Larry Young) [219,226,227]; facultatively solitary: Syrian hamster [228,229], meadow vole [219,226]; and solitary: blind mole-rat [197,199,203,230], Patagonian tuco-tuco (picture courtesy of Prof. Annaliese Beery) [231,232]. The symbols ♀ (female) and ♂ (male) denote sexual dimorphism or sex similarities for each behavior within a given species. (∗) In the eusocial naked mole-rat and Damaraland mole-rat, only the breeding indare aggressive.(#) In the Damaraland mole-rat, the level of aggression depends on the sex of the attacked individual. Toward other females, the breeding female is more aggressive compared to breeding males. In contrast, toward other males from outside the colony, the breeding males are more aggressive compared to the breeding females [225].

Figure 2

Alternative models for neural mechanisms underlying sexually dimorphic behaviors. Sexually dimorphic reproductive behaviors might be governed by at least three principal sexually dimorphic mechanisms: (a) a sexually dimorphic neuronal circuit that controls different sex-typical social behaviors in males and females [34]. (b) The same social behavior in both sexes is controlled by different neural circuits in males and females [27,95]. (c) The neural circuit that drives a behavior typically displayed by the opposite sex is present in both sexes, but is tonically repressed by external and/or internal stimuli [66,67].