Internal neural states influence the short-term effect of monocular deprivation in human adults.
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
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
- 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
- Received: September 29, 2022
- Preprint posted: October 28, 2022 (view preprint)
- Accepted: January 26, 2023
- Accepted Manuscript published: January 27, 2023 (version 1)
- 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
-
- 730
- Page views
-
- 158
- Downloads
-
- 4
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Download links
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)
Further reading
-
- Medicine
- Neuroscience
Background:
Ketamine has emerged as one of the most promising therapies for treatment-resistant depression. However, inter-individual variability in response to ketamine is still not well understood and it is unclear how ketamine’s molecular mechanisms connect to its neural and behavioral effects.
Methods:
We conducted a single-blind placebo-controlled study, with participants blinded to their treatment condition. 40 healthy participants received acute ketamine (initial bolus 0.23 mg/kg, continuous infusion 0.58 mg/kg/hr). We quantified resting-state functional connectivity via data-driven global brain connectivity and related it to individual ketamine-induced symptom variation and cortical gene expression targets.
Results:
We found that: (i) both the neural and behavioral effects of acute ketamine are multi-dimensional, reflecting robust inter-individual variability; (ii) ketamine’s data-driven principal neural gradient effect matched somatostatin (SST) and parvalbumin (PVALB) cortical gene expression patterns in humans, while the mean effect did not; and (iii) behavioral data-driven individual symptom variation mapped onto distinct neural gradients of ketamine, which were resolvable at the single-subject level.
Conclusions:
These results highlight the importance of considering individual behavioral and neural variation in response to ketamine. They also have implications for the development of individually precise pharmacological biomarkers for treatment selection in psychiatry.
Funding:
This study was supported by NIH grants DP5OD012109-01 (A.A.), 1U01MH121766 (A.A.), R01MH112746 (J.D.M.), 5R01MH112189 (A.A.), 5R01MH108590 (A.A.), NIAAA grant 2P50AA012870-11 (A.A.); NSF NeuroNex grant 2015276 (J.D.M.); Brain and Behavior Research Foundation Young Investigator Award (A.A.); SFARI Pilot Award (J.D.M., A.A.); Heffter Research Institute (Grant No. 1–190420) (FXV, KHP); Swiss Neuromatrix Foundation (Grant No. 2016–0111) (FXV, KHP); Swiss National Science Foundation under the framework of Neuron Cofund (Grant No. 01EW1908) (KHP); Usona Institute (2015 – 2056) (FXV).
Clinical trial number:
-
- Neuroscience
Storing and accessing memories is required to successfully perform day-to-day tasks, for example for engaging in a meaningful conversation. Previous studies in both rodents and primates have correlated hippocampal cellular activity with behavioral expression of memory. A key role has been attributed to awake hippocampal replay – a sequential reactivation of neurons representing a trajectory through space. However, it is unclear if awake replay impacts immediate future behavior, gradually creates and stabilizes long-term memories over a long period of time (hours and longer), or enables the temporary memorization of relevant events at an intermediate time scale (seconds to minutes). In this study, we aimed to address the uncertainty around the timeframe of impact of awake replay by collecting causal evidence from behaving rats. We detected and disrupted sharp wave ripples (SWRs) - signatures of putative replay events - using electrical stimulation of the ventral hippocampal commissure in rats that were trained on three different spatial memory tasks. In each task, rats were required to memorize a new set of locations in each trial or each daily session. Interestingly, the rats performed equally well with or without SWR disruptions. These data suggest that awake SWRs - and potentially replay - does not affect the immediate behavior nor the temporary memorization of relevant events at a short timescale that are required to successfully perform the spatial tasks. Based on these results, we hypothesize that the impact of awake replay on memory and behavior is long-term and cumulative over time.