Maternal experience unmasks temporal integration for vocalization processing

Abstract

New parents become highly responsive to infant cries in parallel with auditory cortical plasticity enhancing representations of these calls. To promote caretaking behavior, increased cortical activity must be appropriately routed to downstream areas in combination with suppression of circuits that could promote aversive responses to infant cries. We investigated responses to multi syllable mouse pup calls in cortical output neurons projecting to either the auditory striatum or auditory midbrain (inferior colliculus) using longitudinal 2-photon imaging and in vivo optically tagged whole-cell recordings. In mice with maternal experience, corticocollicular but not corticostriatal projections responded to pup calls over extended durations and were required for pup retrieval behavior, indicating that corticocollicular output neurons integrated multiple call syllables. The two populations diverged with parental experience, enhancing sustained responses in corticocollicular projections and reducing responses in corticostriatal projections. We performed simultaneous Neuropixels recordings from auditory cortex, thalamus, and midbrain to examine the temporal structure of call responses across areas, and to determine the influences of feedforward and feedback processing. Facilitation of later syllables increased in midbrain of maternally experienced animals, together with reduced firing rates in a subset of units that were weakly coupled to cortical and midbrain activity. Overall, maternal experience leads to broad suppression of subcortical excitation in response to pup calls while selectively unmasking a subset of midbrain neurons that integrate over multiple syllables.