Internal neural states influence the short-term effect of monocular deprivation in human adults.

  1. Yiya Chen
  2. Yige Gao
  3. Zhifen He
  4. Zhouyuan Sun
  5. Yu Mao
  6. Robert F Hess  Is a corresponding author
  7. Peng Zhang  Is a corresponding author
  8. Jiawei Zhou  Is a corresponding author
  1. Wenzhou Medical University, China
  2. Chinese Academy of Sciences, China
  3. McGill University, Canada

Abstract

The adult human visual system maintains the ability to be altered by sensory deprivation. What has not been considered is whether the internal neural states modulate visual sensitivity to short-term monocular deprivation. In this study we manipulated the internal neural state and reported changes in intrinsic neural oscillations with a patched eye open or closed. We investigated the influence of eye open/eye closure on the unpatched eye's contrast sensitivity and ocular dominance (OD) shifts induced by short-term monocular deprivation. The results demonstrate that internal neural states influence not only baseline contrast sensitivity but also the extent to which the adult visual system can undergo changes in ocular dominance.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file.

Article and author information

Author details

  1. Yiya Chen

    State Key Laboratory of Ophthalmology, Optometry and Visual Science, Wenzhou Medical University, Wenzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Yige Gao

    Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Zhifen He

    State Key Laboratory of Ophthalmology, Optometry and Visual Science, Wenzhou Medical University, Wenzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Zhouyuan Sun

    Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Yu Mao

    State Key Laboratory of Ophthalmology, Optometry and Visual Science, Wenzhou Medical University, Wenzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Robert F Hess

    Department of Ophthalmology and Visual Sciences, McGill University, Montreal, Canada
    For correspondence
    robert.hess@mcgill.ca
    Competing interests
    The authors declare that no competing interests exist.
  7. Peng Zhang

    Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    For correspondence
    zhangpeng@ibp.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9603-8454
  8. Jiawei Zhou

    State Key Laboratory of Ophthalmology, Optometry and Visual Science, Wenzhou Medical University, Wenzhou, China
    For correspondence
    zhoujw@mail.eye.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4220-344X

Funding

National Natural Science Foundation of China (31970975)

  • Jiawei Zhou

National Science and Technology Major Project (2022ZD0211900)

  • Peng Zhang

National Science and Technology Major Project (2021ZD0204200)

  • Peng Zhang

Natural Science Foundation for Distinguished Young scholars of zhejiang Province (LR22H120001)

  • Jiawei Zhou

Project of State Key Laboratory of Ophthalmology, Optometry and Vision Science, Wenzhou Medical University (J02-20210203)

  • Jiawei Zhou

Canadian Institutes of Health Research (CCI-125686)

  • Robert F Hess

Natural Sciences and Engineering Research Council of Canada (228103)

  • Robert F Hess

ERA-NET Neuron (JTC2015)

  • Robert F Hess

National Natural Science Foundation of China (31871107)

  • Peng Zhang

National Natural Science Foundation of China (31930053)

  • Peng Zhang

Project of State Key Laboratory of Ophthalmology, Optometry and Vision Science, Wenzhou Medical University (K03-20220102)

  • Peng Zhang

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

Reviewing Editor

  1. Eric D Gaier, Boston Children's Hospital, United States

Ethics

Human subjects: This study complied with the Declaration of Helsinki and was approved by the Institutional Review Boards of Wenzhou Medical University. The methods were carried out in accordance with the approved guidelines under the protocol 'Adult amblyopia: binocular visual deficits and rehabilitation' version #1 dated 5/29/2019. All subjects were naive to the purpose of the study, and provided written informed consent which included consent to process and preserve the data and publish them in anonymous form.

Version history

  1. Received: September 29, 2022
  2. Preprint posted: October 28, 2022 (view preprint)
  3. Accepted: January 26, 2023
  4. Accepted Manuscript published: January 27, 2023 (version 1)
  5. Version of Record published: February 9, 2023 (version 2)

Copyright

© 2023, Chen et al.

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

  • 773
    views
  • 165
    downloads
  • 4
    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. Yiya Chen
  2. Yige Gao
  3. Zhifen He
  4. Zhouyuan Sun
  5. Yu Mao
  6. Robert F Hess
  7. Peng Zhang
  8. Jiawei Zhou
(2023)
Internal neural states influence the short-term effect of monocular deprivation in human adults.
eLife 12:e83815.
https://doi.org/10.7554/eLife.83815

Share this article

https://doi.org/10.7554/eLife.83815

Further reading

    1. Neuroscience
    Ya-Hui Lin, Li-Wen Wang ... Li-An Chu
    Research Article

    Tissue-clearing and labeling techniques have revolutionized brain-wide imaging and analysis, yet their application to clinical formalin-fixed paraffin-embedded (FFPE) blocks remains challenging. We introduce HIF-Clear, a novel method for efficiently clearing and labeling centimeter-thick FFPE specimens using elevated temperature and concentrated detergents. HIF-Clear with multi-round immunolabeling reveals neuron circuitry regulating multiple neurotransmitter systems in a whole FFPE mouse brain and is able to be used as the evaluation of disease treatment efficiency. HIF-Clear also supports expansion microscopy and can be performed on a non-sectioned 15-year-old FFPE specimen, as well as a 3-month formalin-fixed mouse brain. Thus, HIF-Clear represents a feasible approach for researching archived FFPE specimens for future neuroscientific and 3D neuropathological analyses.

    1. Neuroscience
    Amanda Chu, Nicholas T Gordon ... Michael A McDannald
    Research Article

    Pavlovian fear conditioning has been extensively used to study the behavioral and neural basis of defensive systems. In a typical procedure, a cue is paired with foot shock, and subsequent cue presentation elicits freezing, a behavior theoretically linked to predator detection. Studies have since shown a fear conditioned cue can elicit locomotion, a behavior that - in addition to jumping, and rearing - is theoretically linked to imminent or occurring predation. A criticism of studies observing fear conditioned cue-elicited locomotion is that responding is non-associative. We gave rats Pavlovian fear discrimination over a baseline of reward seeking. TTL-triggered cameras captured 5 behavior frames/s around cue presentation. Experiment 1 examined the emergence of danger-specific behaviors over fear acquisition. Experiment 2 examined the expression of danger-specific behaviors in fear extinction. In total, we scored 112,000 frames for nine discrete behavior categories. Temporal ethograms show that during acquisition, a fear conditioned cue suppresses reward seeking and elicits freezing, but also elicits locomotion, jumping, and rearing - all of which are maximal when foot shock is imminent. During extinction, a fear conditioned cue most prominently suppresses reward seeking, and elicits locomotion that is timed to shock delivery. The independent expression of these behaviors in both experiments reveal a fear conditioned cue to orchestrate a temporally organized suite of behaviors.