Limbic Neurons Shape Sex Recognition and Social Behavior in Sexually Naive Males

• Published in: Cell 2019-02, Vol.176 (5), p.1190-1205.e20
• Main Authors: Bayless, Daniel W., Yang, Taehong, Mason, Matthew M., Susanto, Albert A.T., Lobdell, Alexandra, Shah, Nirao M.
• Format: Article
• Language: English
• Subjects: aggression; Amygdala - physiology; Animals; aromatase; Aromatase - metabolism; bed nucleus of the stria terminalis; Brain - physiology; emotional behavior; gender recognition; innate behavior; Limbic System - metabolism; Male; mating; Mice; Mice, Inbred C57BL; Neural Pathways - metabolism; Neurons - metabolism; Pheromones - metabolism; Septal Nuclei - physiology; Sex Characteristics; sexual behavior; Sexual Behavior, Animal - physiology; sexual dimorphism; Social Behavior
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2018.12.041

Sexually naive animals have to distinguish between the sexes because they show species-typical interactions with males and females without meaningful prior experience. However, central neural pathways in naive mammals that recognize sex of other individuals remain poorly characterized. We examined the role of the principal component of the bed nucleus of stria terminalis (BNSTpr), a limbic center, in social interactions in mice. We find that activity of aromatase-expressing BNSTpr (AB) neurons appears to encode sex of other animals and subsequent displays of mating in sexually naive males. Silencing these neurons in males eliminates preference for female pheromones and abrogates mating success, whereas activating them even transiently promotes male-male mating. Surprisingly, female AB neurons do not appear to control sex recognition, mating, or maternal aggression. In summary, AB neurons represent sex of other animals and govern ensuing social behaviors in sexually naive males. [Display omitted] •In sexually naive males, activity of AB neurons encodes sex of conspecifics•Male AB neurons are required for sexual preference, mating, and aggression•Activation of male AB neurons promotes male-male sexual behavior•Females use other, non-AB neurons for sex recognition, mating, and maternal care Aromatase-expressing BNSTpr neurons govern sex recognition and social behavior in naive male mice.