Circuit-based mechanism for object craving and ultrasonic vocalization

Abstract

The medial preoptic area (MPA) is a hypothalamic region that mediates various innate behaviors including social interaction and parental behaviors. There have still been more elusive behavioral functions controlled by neural circuits, as MPA is extremely heterogeneous and intensely connected to other hypothalamic regions. We have discovered other previously unknown behavioral functions of a specific population of neurons in MPA and its output projections to ventral periaqueductal gray (vPAG), by using optognetic manipulations specifically targeting that particular circuit. First, we found that a subset of neurons in MPA induce a strong craving for three-dimensional (3D) objects via neuronal projections to vPAG. Exploiting this observation, we devised a learning-free method to precisely steer animals’ moving directions based on eliciting this strong craving for 3D objects. We made a head-mounted 3D object, the direction of which and timing of photostimulation were wirelessly controlled. Using this MPA-induced drive assisted steering (MIDAS) system we were able to precisely control the navigation pathway of mice in real time without prior training through a programmed route in a complex maze. Second, we found that ultrasonic vocalizations were elicited by photostimulation of MPA. Interestingly, such USVs were emitted in the absence of social targets and the pattern of USVs was modulated according to the frequency and intensity of photostimulation. Therefore, we discover two novel functions of MPA in mediating object craving as an innate behavior and affecting ultrasonic vocalization in mice.