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
  7. Peng Zhang
  8. Jiawei Zhou

  • Curated by eLife

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    eLife assessment

    The authors report the results of three experiments assessing how one or both eyes open under a patch influence resting EEG activity, contrast sensitivity, and binocular balance in normally sighted subjects. Their results suggest that the state of eye opening temporarily, but significantly, influences shifts in ocular dominance with relevance for treatment of binocular visual disorders such as amblyopia that are treated with periodic monocular occlusion. The evidence supporting their conclusions is solid and the findings are important for the field.

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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.

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  1. Version published to 10.7554/elife.83815 on eLife
  2. eLife

    eLife assessment

    The authors report the results of three experiments assessing how one or both eyes open under a patch influence resting EEG activity, contrast sensitivity, and binocular balance in normally sighted subjects. Their results suggest that the state of eye opening temporarily, but significantly, influences shifts in ocular dominance with relevance for treatment of binocular visual disorders such as amblyopia that are treated with periodic monocular occlusion. The evidence supporting their conclusions is solid and the findings are important for the field.

  3. eLife

    Reviewer #1 (Public Review):

    Chen and colleagues report the results of 3 experiments assessing how one or both eyes open under a patch influence resting EEG activity, contrast sensitivity, and binocular balance in normally sighted subjects. They found that keeping an eye open (as opposed to closed) under a patch enhances contrast sensitivity and evoked responses through the unpatched eye as well as interocular shifts in contrast sensitivity and binocular balance in favor of the patched eye once the patch is removed. These results suggest that the state of eye opening temporarily, but significantly, influences shifts in ocular dominance with relevance for treatment of binocular visual disorders such as amblyopia that are treated with periodic monocular occlusion.

    Strengths:
    1. Elegant simplicity in study design.
    2. Well-designed and executed psychophysical assessments of contrast sensitivity and binocular balance. More than one assay for binocular balance is used.
    3. Cross-modality relationships are analyzed and support the underlying hypothesis.

    Weaknesses:
    1. The investigators demonstrate an effect of eye open status under the patch on occipital oscillatory activity, but subsequent results cannot be directly attributed to these changes since occipital oscillation are not directly manipulated. Therefore, the extent to which the oscillatory activity in visual cortex mediates differential open versus closed eye effects on contrast sensitivity and binocular balance cannot be concluded based on these data alone.
    2. Long-term effects produced or enabled through open or closed eye patching are not reported, limiting translational potential for visual disorders such as amblyopia.

  4. eLife

    Reviewer #2 (Public Review):

    There are fundamental differences in resting state with eyes open or eyes closed regardless of visual stimulation. Without visual stimulation, these differences are attributed to the switching of involuntary attention from internal (eyes closed) to external (eyes open). The authors employ a monocular deprivation paradigm by patching one eye (with it either open or closed) to induce differences in alpha amplitude that are similar to differences measured with both eyes open or closed. They then examine how these differences from monocular deprivation impact after-effects in contrast sensitivity and binocular balance.

    The authors pose an interesting and well-supported hypothesis based on prior knowledge that internal oscillations (i.e. alpha waves) can be modulated with eyes open vs eyes closed. The presented experiments build well upon one another and the authors clearly describe how relevant findings from experiment 1 contribute to the design of the following monocular deprivation experiments. The authors also combine several metrics including EEG, SSVEP and contrast sensitivity to assess both neural activity and perception in tandem.

    Despite these strengths, the reported data in the first experiments only shows a modest difference between conditions. In experiment one, the authors make the assumption that differences in alpha measured with binocular eyes open vs closed translates to differences in alpha noted with a patched eye open or closed. Although changes in alpha amplitude appear comparable under monocular and binocular viewing, the differences in perceptual contrast sensitivity between the patched eye open and closed condition are quite modest. The authors do not report differences in contrast sensitivity in the binocular condition, so it is difficult to assess if these are comparable (contrast sensitivity changes in binocular (both eyes open vs closed) and monocular (patched eye open vs closed). The authors also employ their results to make claims about neuroplasticity, however this may be too general a claim. It seems as though the authors are specifically using an adaptation paradigm to elicit short-term changes (within 30 minutes from deprivation). While technically, the visual system is changing, it may be slightly misleading to refer to these neuroplastic changes given there are no measured long-term effects. The authors also fail to explain differences in binocular paradigm, noting recovery of binocularity in their phase combination paradigm, but persistent changes in their rivalry assessment. The authors also may overstate the implications of this in the discussion, as they provide no direct evidence that their reported changes after monocular deprivation are attributed to GABA interactions in primary visual cortex.

    This work is important to our understanding of not only endogenous modulators of visual perception, but may have implications in how this knowledge is applied in clinical practice, specifically the treatment of amblyopia with patching.

  5. Version published to 10.1101/2022.10.27.513994v1 on bioRxiv