01_Pheromones-Dulac - Vol 448 | 30 August 2007 |...

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ARTICLES A functional circuit underlying male sexual behaviour in the female mouse brain Tali Kimchi 1 , Jennings Xu 1 & Catherine Dulac 1 In mice, pheromone detection is mediated by the vomeronasal organ and the main olfactory epithelium. Male mice that are deficient for Trpc2, an ion channel specifically expressed in VNO neurons and essential for VNO sensory transduction, are impaired in sex discrimination and male–male aggression. We report here that Trpc2 2 / 2 female mice show a reduction in female-specific behaviour, including maternal aggression and lactating behaviour. Strikingly, mutant females display unique characteristics of male sexual and courtship behaviours such as mounting, pelvic thrust, solicitation, anogenital olfactory investigation, and emission of complex ultrasonic vocalizations towards male and female conspecific mice. The same behavioural phenotype is observed after VNO surgical removal in adult animals, and is not accompanied by disruption of the oestrous cycle and sex hormone levels. These findings suggest that VNO-mediated pheromone inputs act in wild-type females to repress male behaviour and activate female behaviours. Moreover, they imply that functional neuronal circuits underlying male-specific behaviours exist in the normal female mouse brain. Males and females within a given animal species display identifiable differences in behaviours, mostly but not exclusively pertaining to sexual and social responses. Although these represent the most obvi- ous examples of behavioural variability within a species, the basic principles underlying sexual dimorphism of brain function are lar- gely unknown. Moreover, with few exceptions, the search for unique structures and circuits in male and female brains that parallel the dimorphism of peripheral sexual organs has so far met little success 1–5 . In many animals species- and sex-specific behaviours are orche- strated by pheromonal cues. Recent studies in rodents have uncov- ered the dual role of the main olfactory epithelium and the vomeronasal organ (VNO) in pheromones controlling mating, aggression and gender identification 6 . Genetic ablation of the TRPC2 channel, a signalling component essential to VNO function, leads to indiscriminate courtship and mounting behaviour of Trpc2 2 / 2 male mice towards both males and females, suggesting an essential role of the vomeronasal system in sex identification 7–10 . Furthermore, recent recording, genetic silencing and tracing experi- ments in the mouse have revealed the involvement of the main olfact- ory epithelium and associated central pathways in pheromone- mediated responses 11–14 . To study the role of the VNO in female sexual receptivity, we introduced a sexually experienced male to the home cage of either Trpc2 1 / 1 , Trpc2 1 / 2 or Trpc2 2 / 2 females. As expected, oestrous Trpc2 1 / 1 and Trpc2 1 / 2 females were sexually receptive, allowing intensive olfactory investigation of the anogenital region by the male, leading to successful mating within minutes. However, in a striking
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01_Pheromones-Dulac - Vol 448 | 30 August 2007 |...

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