Neural mechanisms of vocal control

Abstract

Vocal communication is a key behavior by which mammals form social bonds and convey information about social status and mating fitness. However, the cellular and synaptic nature of the neural circuits that adaptively regulate vocalization as a function of the individual’s social and environmental context remain unknown. Here, I helped pioneer the use of an intersectional genetic method to identify a subpopulation of neurons in the midbrain periaqueductal gray (PAG) of the mouse that act on downstream vocal-patterning circuits to gate ultrasonic courtship vocalizations. Next, I used transsynaptic tracing to identify two populations of inhibitory neurons that lie upstream of these PAG-USV neurons that exert opposing effects on USV production. I used molecular profiling, optogenetics, and circuit dissection in brain slices to establish that PAG-projecting GABAergic neurons in the preoptic hypothalamus promote USV production. In contrast, I found that PAG-projecting GABAergic neurons in the central-medial boundary zone of the amygdala suppress USV production without disrupting non-vocal social behavior. Finally, I used fiber photometry during free behaviors to reveal that affiliative social and sexual interactions excite USV-promoting preoptic neurons while innately aversive stimuli activate USV-suppressing amygdala neurons. These experiments provide an important step forward in mapping the brain-wide networks that regulate vocalizations as a function of social and environmental contexts.