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

  1. Justin D Yao  Is a corresponding author
  2. Dan H Sanes  Is a corresponding author
  1. New York University, United States

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

  1. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8762-9044
  2. 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

© 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.

Metrics

  • 1,805
    views
  • 195
    downloads
  • 28
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Justin D Yao
  2. Dan H Sanes
(2018)
Developmental deprivation-induced perceptual and cortical processing deficits in awake-behaving animals
eLife 7:e33891.
https://doi.org/10.7554/eLife.33891

Share this article

https://doi.org/10.7554/eLife.33891

Further reading

    1. Neuroscience
    Elena Massai, Marco Bonizzato ... Marina Martinez
    Research Article

    Control of voluntary limb movement is predominantly attributed to the contralateral motor cortex. However, increasing evidence suggests the involvement of ipsilateral cortical networks in this process, especially in motor tasks requiring bilateral coordination, such as locomotion. In this study, we combined a unilateral thoracic spinal cord injury (SCI) with a cortical neuroprosthetic approach to investigate the functional role of the ipsilateral motor cortex in rat movement through spared contralesional pathways. Our findings reveal that in all SCI rats, stimulation of the ipsilesional motor cortex promoted a bilateral synergy. This synergy involved the elevation of the contralateral foot along with ipsilateral hindlimb extension. Additionally, in two out of seven animals, stimulation of a sub-region of the hindlimb motor cortex modulated ipsilateral hindlimb flexion. Importantly, ipsilateral cortical stimulation delivered after SCI immediately alleviated multiple locomotor and postural deficits, and this effect persisted after ablation of the homologous motor cortex. These results provide strong evidence of a causal link between cortical activation and precise ipsilateral control of hindlimb movement. This study has significant implications for the development of future neuroprosthetic technology and our understanding of motor control in the context of SCI.

    1. Neuroscience
    Bharath Krishnan, Noah Cowan
    Insight

    Mice can generate a cognitive map of an environment based on self-motion signals when there is a fixed association between their starting point and the location of their goal.