Auditory corticofugal circuits drive vocalization-guided maternal behavior

Perception of vocalizations is crucial for social behavior. A conserved example of this is mothers responding to distress calls from infants. In mice, experienced mothers (dams) find and retrieve isolated pups into the nest when pups emit ultrasonic vocalizations (USVs). Virgin females generally do not retrieve pups until they gain experience, for example by co-housing with a dam and litter. The onset of retrieval behavior is correlated with heightened sensitivity to USVs in left auditory cortex (AC). This plasticity may support learning via projections from cortex to early structures in the auditory pathway. To test whether projections from left AC are required for retrieval, we chemogenetically silenced activity in layer 5 during retrieval. In expert retrievers, silencing only neurons projecting to inferior colliculus (corticocollicular) led to impairment in retrieval. However, silencing neurons projecting to striatum had no effect. We used optically-tagged in vivo whole-cell recordings and 2-photon Ca2+ imaging in awake mice to compare encoding of USVs in corticostriatal and corticollicular neurons. Corticocollicular neurons in expert retrievers exhibited sustained increases in activity during USV playback compared to presentation of pure tones, while activity was equivalent during USV and pure tone presentation in corticostriatal neurons. The sustained activity we observed in corticollicular neurons may reflect increased excitability in a dedicated network of recurrently-linked cortical and subcortical areas. We tracked activity in corticocollicular and corticostriatal neurons over several days before and during co-housing as retrieval performance improved. This revealed robust population responses to USVs on each day in both groups. In both groups, delayed responses to USVs were larger in magnitude on days in which mice had reached expert performance, which may reflect network-level plasticity upregulating activity in recurrent auditory circuits to support perception of USVs.