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Author Notes:

Correspondence should be addressed to Robert C. Liu, Rollins Research Building, Room 2006, 1510 Clifton Road NE, Atlanta, GA 30322. E-mail: robert.liu@emory.edu

Author contributions: K.N.S. and R.C.L. designed research; K.N.S. performed research; K.N.S. and K.K.C. analyzed data; K.N.S., K.K.C., and R.C.L. wrote the paper.

The authors declare no competing financial interests.

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Research Funding:

This work was supported by Department of Health and Human Services (HHS)/National Institutes of Health (NIH)/National Institute on Deafness and Other Communication Disorders Grants F31-DC-011987 (to K.N.S.) and R01-DC-008343 (to R.C.L.); HHS/NIH /Eunice Kennedy Shriver National Institute of Child Health and Human Development Grant T32-HD-071845 (to K.K.C.); and Emory University PRISM fellowship DGE0536941 (to K.N.S.), a GK-12 program of the National Science Foundation.

Keywords:

  • auditory learning
  • lateral inhibition
  • map plasticity
  • maternal behavior
  • tonotopic map
  • ultrasonic vocalization

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

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Journal Title:

eNeuro

Volume:

Volume 3, Number 6

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Type of Work:

Article | Final Publisher PDF

Abstract:

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 (USVs) or for ultrasound frequencies in postweaning dams for whom USVs emitted by pups acquire behavioral relevance. However, whether transient expansion occurs during maternal experience is not known, and could help to 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 the playback of ultrasounds or pup USVs for maternally experienced animals assessed at their pups’ postnatal day 9 (P9) to P10, or postweaning. 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.

Copyright information:

© 2016 Shepard et al.

This is an Open Access work distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/).
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