Behavioral Relevance Helps Untangle Natural Vocal Categories in a Specific Subset of Core Auditory Cortical Pyramidal Neurons

TLDR

Sound categorization is essential for auditory behaviors, yet the neural basis for learned natural categories such as vocalizations remains poorly understood. The study uses electrophysiological mapping and single‑unit recordings in mice to examine how core auditory cortex representations of natural vocal categories change when one category gains behavioral relevance. Maternal experience does not expand cortical maps for pup vocalizations but instead improves discrimination between pup and adult calls in a subset of late‑onset pyramidal neurons, with more of these neurons responding to pup‑specific acoustic features, indicating that higher‑order category representations arise from a biased pyramidal neuron subset.

Abstract

Sound categorization is essential for auditory behaviors like acoustic communication, but its genesis within the auditory pathway is not well understood—especially for learned natural categories like vocalizations, which often share overlapping acoustic features that must be distinguished (e.g., speech). We use electrophysiological mapping and single-unit recordings in mice to investigate how representations of natural vocal categories within core auditory cortex are modulated when one category acquires enhanced behavioral relevance. Taking advantage of a maternal mouse model of acoustic communication, we found no long-term auditory cortical map expansion to represent a behaviorally relevant pup vocalization category—contrary to expectations from the cortical plasticity literature on conditioning with pure tones. Instead, we observed plasticity that improved the separation between acoustically similar pup and adult vocalization categories among a physiologically defined subset of late-onset, putative pyramidal neurons, but not among putative interneurons. Additionally, a larger proportion of these putative pyramidal neurons in maternal animals compared with nonmaternal animals responded to the individual pup call exemplars having combinations of acoustic features most typical of that category. Together, these data suggest that higher-order representations of acoustic categories arise from a subset of core auditory cortical pyramidal neurons that become biased toward the combination of acoustic features statistically predictive of membership to a behaviorally relevant sound category.