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Summary: Social interactions involve both approach and avoidance toward specific individuals. Currently, the brain regions subserving these behaviors are not fully recognized. The anterior hypothalamic nucleus (AHN) is a poorly defined brain area, and recent studies have yielded contradicting conclusions regarding its behavioral role. Here we explored the role of AHN neuronal activity in regulating approach and avoidance actions during social interactions. Using electrophysiological recordings from behaving mice, we revealed that theta rhythmicity in the AHN is enhanced during affiliative interactions, but decreases during aversive ones. Moreover, the spiking activity of AHN neurons increased during the investigation of social stimuli, as compared to objects, and was modulated by theta rhythmicity. Finally, AHN optogenetic stimulation during social interactions augmented the approach toward stimuli associated with the stimulation. These results suggest the role for AHN neural activity in regulating approach behavior during social interactions, and for theta rhythmicity in mediating the valence of social stimuli.

Summary: The survival of individuals of gregarious species depends on their social interactions. In humans, atypical social behavior is a hallmark of several psychopathological conditions, many of which have sex-specific manifestations. Various laboratory mouse strains are used to reveal the mechanisms mediating typical and atypical social behavior in mammals. Here, we used three social discrimination tests to characterize social behavior in males and females of three widely used laboratory mouse strains (C57BL/6J, BALB/c, and ICR). We found marked sex- and strain-specific differences in the behavior exhibited by subjects, in a test-dependent manner. Interestingly, some characteristics were strain-dependent, while others were sex-dependent. We then crossbred C57BL/6J and BALB/c mice and found that offspring of such crossbreeding exhibit social behavior which differs from both parental strains and depends on the specific combination of parental strains. Thus, social behavior of laboratory mice is sex- and strain-specific and depends on both genetic and environmental factors.