Nested circuits mediate the decision to vocalize

Abstract

Vocalizations facilitate mating and social affiliation, but may also inadvertently alert predators and rivals. Consequently, the decision to vocalize depends on brain circuits that can weigh and compare these potential benefits and risks. Male mice produce ultrasonic vocalizations (USVs) during courtship to facilitate mating and female mice produce USVs to promote social affiliation with each other. Previously we showed that a specialized set of neurons in the midbrain periaqueductal gray (PAG) are an obligatory gate for USV production in both male and female mice, and that both PAG-USV neurons and USVs can be switched on by their inputs from the preoptic area (POA) of the hypothalamus and switched off by their inputs from neurons on the border between the central and medial amygdala (AmgC/M-PAG neurons) (Michael et al., 2020). Here we show that the USV-suppressing AmgC/M-PAG neurons are strongly activated by predator cues or during social contexts that suppress USV production in male and female mice. Furthermore, a subset of USV-promoting POA neurons that provide input to the PAG-USV region also extend axon collaterals to the amygdala, where they directly inhibit AmgC/M-PAG neurons. Accordingly, AmgC/M-PAG neurons, along with POAPAG and PAG-USV neurons, form a nested hierarchical circuit in which environmental and social information converges to influence the decision to vocalize.