Tonotopic map plasticity in the adult auditory cortex (AC) is a well-established and oft-cited measure of auditory associative learning in classical conditioning paradigms. However, its necessity as an enduring memory trace has been debated, especially given a recent finding that the areal expansion of core AC tuned to a newly relevant frequency range may arise only transiently to support auditory learning. This has been reinforced by an ethological paradigm showing that map expansion is not observed for ultrasonic vocalizations (USV) nor ultrasound frequencies in post-weaning dams for whom USVs emitted by pups acquire behavioral relevance. Whether transient expansion occurs during maternal experience is not known though, but could help reveal the generality of cortical map expansion as a correlate for auditory learning. We thus mapped the auditory cortices of maternal mice at postnatal time points surrounding the peak in pup USV emission, but found no evidence of frequency map expansion for the behaviorally relevant high ultrasound range in AC. Instead, regions tuned to low frequencies outside of the ultrasound range show progressively greater suppression of activity in response to playback of ultrasounds or pup USVs for maternally experienced animals assessed at their pups’ postnatal day P9-10, or post-weaning. This provides new evidence for a lateral-band suppression mechanism elicited by behaviorally meaningful USVs, likely enhancing their population level signal-to-noise ratio. These results demonstrate that tonotopic map enlargement has limits as a construct for conceptualizing how experience leaves neural memory traces within sensory cortex in the context of ethological auditory learning.
Significance Statement: A commonly held impression in neuroscience is that learning the behavioral meaning of a stimulus expands the sensory cortical territory representing it, at least transiently if not persistently. Here we investigated whether such expansion occurs in a natural sound learning paradigm wherein mouse mothers come to recognize the importance of pup ultrasonic vocalizations over the course of pup care. Contrary to expectation, we found no evidence for transient or sustained expansion in the representational area of these calls, but instead observed an enhancement in the contrast between how neurons tuned to and away from ultrasonic frequencies respond to those calls. This work has relevance for understanding the neural correlates of learning in evolved species-specific communication systems.
- auditory learning
- lateral inhibition
- map plasticity
- maternal behavior
- tonotopic map
- ultrasonic vocalization
The authors declare no competing financial interests.
HHS | NIH | National Institute on Deafness and Other Communication Disorders (NIDCD) [F31 DC011987] [R01 DC008343]; HHS | NIH | Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) [T32 HD-071845]; NSF | EHR | Division of Graduate Education (DGE) [DGE0536941].