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

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.

Contrast Enhancement without Transient Map Expansion for Species-Specific Vocalizations in Core Auditory Cortex during Learning

“…Indeed, in core AC, ultrasound-evoked inhibition of single units tuned to low frequencies (<40 kHz) is stronger in mothers than in pup-naive females, while the strength of inhibition in neurons with high BFs (>40 kHz) is comparable between groups (Galindo-Leon et al, 2009; Lin et al, 2013). Ultrasound-evoked overall excitation of single units also showed no such modulation by maternal status (although distinct subgroups of neurons do; Shepard et al, 2015b). This observation led to the hypothesis that, upon ultrasound presentation, net population activity (excited–inhibited) in low-frequency-tuned regions of core AC (i.e., A1 and AAF), but not in area UF, would be suppressed to a greater degree in mothers compared with naive females.…”

“…1 D , hashed areas) increases over motherhood. Since a site does not need to have an ultrasonic BF to respond to USVs (Portfors et al, 2009; Shepard et al, 2015b), we next assessed the area of core AC that simply responds to any of the pup USVs we presented, as a fraction of the whole AC. This analysis also provided no evidence for map plasticity, as the pup USV-responsive area does not change across motherhood (Fig.…”

“…Neuronal plasticity that enhances excitatory responses to pup USV features is observed both during motherhood (Cohen et al, 2011; Cohen and Mizrahi, 2015) and afterward (Liu et al, 2006; Liu and Schreiner, 2007; Marlin et al, 2015; Shepard et al, 2015b), but it had been an open question whether such changes in an ethological learning context are accompanied by spatial map expansion. Shepard et al (2015b) reported that postweaning dams do not show relative expansion for ultrasonic sounds within core AC, but it was unclear whether transient expansion could arise to support learning (Kilgard, 2012).…”

“…Shepard et al (2015b) reported that postweaning dams do not show relative expansion for ultrasonic sounds within core AC, but it was unclear whether transient expansion could arise to support learning (Kilgard, 2012). Cohen et al (2011) initially reported a relative increase in USV-responsive single units in the lower BF region of A1 in P5 lactating dams compared with naive mice, feeding the expectation of concomitant areal plasticity.…”

“…In fact, in an earlier study of auditory plasticity for communication sounds, tonotopic plasticity at the map level was not observed after those sounds gained behavioral relevance, despite plasticity on a smaller size scale observed at the single-neuron level (Cohen et al, 2011; Marlin et al, 2015; Shepard et al, 2015b) and local population level (Galindo-Leon et al, 2009; Rothschild et al, 2013). Specifically, mouse pups displaced from their nest emit ultrasonic vocalizations (USVs), which maternal mice, but not pup-naive virgins, preferentially approach in search of lost pups.…”