A Specialized Neural Circuit Gates Social Vocalizations in the Mouse

Vocalizations are fundamental to mammalian communication, but the underlying neural circuits await detailed characterization. Here, we used an intersectional genetic method to label and manipulate neurons in the midbrain periaqueductal gray (PAG) that are transiently active in male mice when they produce ultrasonic courtship vocalizations (USVs). Genetic silencing of PAG-USV neurons rendered males unable to produce USVs and impaired their ability to attract females. Conversely, activating PAG-USV neurons selectively triggered USV production, even in the absence of any female cues. Optogenetic stimulation combined with axonal tracing indicates that PAG-USV neurons gate downstream vocal-patterning circuits. Indeed, activating PAG neurons that innervate the nucleus retroambiguus, but not those innervating the parabrachial nucleus, elicited USVs in both male and female mice. These experiments establish that a dedicated population of PAG neurons gives rise to a descending circuit necessary and sufficient for USV production while also demonstrating the communicative salience of male USVs. [Display omitted] [Display omitted] •Specialized midbrain neurons are active when mice produce courtship vocalizations•Silencing these neurons blocks vocalization but does not impair non-vocal courtship•Activating these neurons elicits vocalization, even in the absence of social cues•Activation and tracing show that these neurons gate premotor patterning circuits Tschida et al. use an intersectional method to identify specialized midbrain neurons whose activity is necessary and sufficient for the production of social vocalizations in the mouse, affording an entry point for genetically dissecting the brain-wide circuits for vocal communication.