Reward of tactile genital stimulation is sexually equivalent, but mechanistically differentiated in mice

Gonadal steroid hormones are thought to activate sexual behavior by actions on multiple organ systems, including the nervous system and genitalia. We previously characterized ovarian hormone dependent behavioral and neural responses to clitoral stimulation in female mice. Here we investigate whether sex differences exist in the responses to tactile genital stimulation, and whether these might depend on gonadal androgens. We measured conditioned place preference (CPP) in response to manual tactile stimulation of either the prepuce or dorsum and subsequently measured neural activation. Behavioral and neural responses to genital stimulation were sexually equivalent in gonadally intact mice, with males exhibiting CPP and neural activation responses similar to those previously reported in females, with the exception of the Arcuate nucleus, which was activated to a greater extent in females. An unexpected sex difference in response to dorsal stimulation was observed, with only males developing CPP and increased FOS expression in the nucleus accumbens. Unlike females, the reward value of tactile stimulation was unaffected by gonadectomy in males. However, neural responses to tactile stimulation were disrupted by gonadectomy in both sexes. Testosterone treatment was only partially effective in restoring neural responses to genital stimulation and did so in a sexually diffentiated manner. We conclude that behavioral and neural responses of sexually-naïve mice to genital stimulation are largely similar between males and females, but that non-genital tactile stimulation is more reinforcing to males. Further, the relationship between gonadal steroid hormones and genital reward is sexually differentiated.