Encoding of female mating dynamics by a hypothalamic line attractor
Nature volume 634, pages 901–909 (2024 )Cite this article
Females exhibit complex, dynamic behaviours during mating with variable sexual receptivity depending on hormonal status1,2,3,4. However, how their brains encode the dynamics of mating and receptivity remains largely unknown. The ventromedial hypothalamus, ventrolateral subdivision contains oestrogen receptor type 1-positive neurons that control mating receptivity in female mice5,6. Here, unsupervised dynamical system analysis of calcium imaging data from these neurons during mating uncovered a dimension with slow ramping activity, generating a line attractor in neural state space. Neural perturbations in behaving females demonstrated relaxation of population activity back into the attractor. During mating, population activity integrated male cues to ramp up along this attractor, peaking just before ejaculation. Activity in the attractor dimension was positively correlated with the degree of receptivity. Longitudinal imaging revealed that attractor dynamics appear and disappear across the oestrus cycle and are hormone dependent. These observations suggest that a hypothalamic line attractor encodes a persistent, escalating state of female sexual arousal or drive during mating. They also demonstrate that attractors can be reversibly modulated by hormonal status, on a timescale of days.
Mating is a complex social interaction whose success is essential to the survival of a species. In rodents, female mating receptivity has been considered as a binary behaviour defined by lordosis7,8,9,10, a reflexive acceptance posture. In fact, however, female receptivity is highly dynamic, exhibiting variability both within a mating interaction and across different physiological states2. Nevertheless, the important contribution of a female to the dynamics of successful mating has been underappreciated and understudied, relative to the male.
