Developmental deprivation-induced perceptual and cortical processing deficits in awake-behaving animals

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Abstract

Sensory deprivation during development induces lifelong changes to central nervous system function that are associated with perceptual impairments. However, the relationship between neural and behavioral deficits is uncertain due to a lack of simultaneous measurements during task performance. Therefore, we telemetrically recorded from auditory cortex neurons in gerbils reared with developmental conductive hearing loss as they performed an auditory task in which rapid fluctuations in amplitude are detected. These data were compared to a measure of auditory brainstem temporal processing from each animal. We found that developmental HL diminished behavioral performance, but did not alter brainstem temporal processing. However, the simultaneous assessment of neural and behavioral processing revealed that perceptual deficits were associated with a degraded cortical population code that could be explained by greater trial-to-trial response variability. Our findings suggest that the perceptual limitations that attend early hearing loss are best explained by an encoding deficit in auditory cortex.

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Justin D Yao

Center for Neural Science, New York University, New York, United States

For correspondence
jdyao@nyu.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-8762-9044
Dan H Sanes

Center for Neural Science, New York University, New York, United States

For correspondence
dhs1@nyu.edu

Competing interests
The authors declare that no competing interests exist.

Funding

National Institute on Deafness and Other Communication Disorders (F32 DC016508)

Justin D Yao

National Institute on Deafness and Other Communication Disorders (R01 DC014656)

Dan H Sanes

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All procedures of this study were approved by the Institutional Animal Care and Use Committee at New York University and followed guidelines established by the National Institutes of Health for the care and use of laboratory animals. All conductive hearing loss surgeries were performed under a surgical level of anesthesia induced with methoxyflurane. All auditory brainstem response recordings were performed under ketamine and pentobarbital. All electrode implant surgeries were performed under isoflurane/O2. Every effort was made to minimize suffering.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.