Developmental deprivation-induced perceptual and cortical processing deficits in awake-behaving animals
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.
Data availability
MATLAB files and code are available at the New York University Box (https://nyu.box.com/v/Yao-Sanes-eLife-2018).
Article and author information
Author details
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.
Reviewing Editor
- Eve Marder, Brandeis University, United States
Version history
- Received: November 28, 2017
- Accepted: June 4, 2018
- Accepted Manuscript published: June 6, 2018 (version 1)
- Accepted Manuscript updated: June 7, 2018 (version 2)
- Version of Record published: June 18, 2018 (version 3)
Copyright
© 2018, Yao & Sanes
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.
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Further reading
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- Neuroscience
Complex behaviors depend on the coordinated activity of neural ensembles in interconnected brain areas. The behavioral function of such coordination, often measured as co-fluctuations in neural activity across areas, is poorly understood. One hypothesis is that rapidly varying co-fluctuations may be a signature of moment-by-moment task-relevant influences of one area on another. We tested this possibility for error-corrective adaptation of birdsong, a form of motor learning which has been hypothesized to depend on the top-down influence of a higher-order area, LMAN (lateral magnocellular nucleus of the anterior nidopallium), in shaping moment-by-moment output from a primary motor area, RA (robust nucleus of the arcopallium). In paired recordings of LMAN and RA in singing birds, we discovered a neural signature of a top-down influence of LMAN on RA, quantified as an LMAN-leading co-fluctuation in activity between these areas. During learning, this co-fluctuation strengthened in a premotor temporal window linked to the specific movement, sequential context, and acoustic modification associated with learning. Moreover, transient perturbation of LMAN activity specifically within this premotor window caused rapid occlusion of pitch modifications, consistent with LMAN conveying a temporally localized motor-biasing signal. Combined, our results reveal a dynamic top-down influence of LMAN on RA that varies on the rapid timescale of individual movements and is flexibly linked to contexts associated with learning. This finding indicates that inter-area co-fluctuations can be a signature of dynamic top-down influences that support complex behavior and its adaptation.
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