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Dark Rearing in the Visual Critical Period Causes Structural Changes in Myelinated Axons in the Adult Mouse Visual Pathway

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Abstract

An appropriate sensory experience during the early developmental period is important for brain maturation. Dark rearing during the visual critical period delays the maturation of neuronal circuits in the visual cortex. Although the formation and structural plasticity of the myelin sheaths on retinal ganglion cell axons modulate the visual function, the effects of dark rearing during the visual critical period on the structure of the retinal ganglion cell axons and their myelin sheaths are still unclear. To address this question, mice were reared in a dark box during the visual critical period and then normally reared to adulthood. We found that myelin sheaths on the retinal ganglion cell axons of dark-reared mice were thicker than those of normally reared mice in both the optic chiasm and optic nerve. Furthermore, whole-mount immunostaining with fluorescent axonal labeling and tissue clearing revealed that the myelin internodal length in dark-reared mice was shorter than that in normally reared mice in both the optic chiasm and optic nerve. These findings demonstrate that dark rearing during the visual critical period affects the morphology of myelin sheaths, shortens and thickens myelin sheaths in the visual pathway, despite the mice being reared in normal light/dark conditions after the dark rearing.

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Data availability

Raw data were generated at the Jichi Medical University. Datasets supporting the findings of this study are available from the corresponding authors on request.

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Acknowledgements

This work was supported by Jichi Medical University Young Investigator Award 2021 to Y.O., Kawano Masanori Memorial Public Interest Incorporated Foundation for Promotion of Pediatric The 33rd research grants for young scientists to Y.O., Japan Society for the Promotion of Science (JSPS) KAKENHI Grant Number 20K22691 and 21K15197 to Y.O., and 20K21506, 21H05241, 21H04786 and 20KK0170 to N.O., and a research grant from the National Center of Neurology and Psychiatry (No. 30-5, 3-5) to N.O. We thank the Jichi Medical University craft center for manufacturing the dark boxes.

Funding

Funding was provided by Japan Society for the Promotion of Science (Grant Nos.: 20K22691 and 21K15197 to Y.O., and 20K21506, 21H05241, 21H04786 and 20KK0170 to N.O.), by the National Center of Neurology and Psychiatry (Grant No.: 30-5, 3-5 to N.O.), by Kawano Masanori Memorial Public Interest Incorporated Foundation (The 33rd research grants for young scientists to Y.O.), and also by Jichi Medical University (Young Investigator Award 2021 to Y.O.)

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Authors and Affiliations

  1. Division of Histology and Cell Biology, Department of Anatomy, School of Medicine, Jichi Medical University, Shimotsuke, Japan

    Yasuyuki Osanai, Batpurev Battulga, Reiji Yamazaki, Tom Kouki, Megumi Yatabe, Yoshiaki Shinohara & Nobuhiko Ohno

  2. Australian Regenerative Medicine Institute, Monash University, 15 Innovation Walk, Clayton, VIC, 3800, Australia

    Yasuyuki Osanai

  3. Division of Genetic Therapeutics, Center for Molecular Medicine, Jichi Medical University, Shimotsuke, Japan

    Hiroaki Mizukami

  4. Section of Viral Vector Development, National Institute for Physiological Sciences, Okazaki, Japan

    Kenta Kobayashi

  5. SOKENDAI (The Graduate University for Advanced Studies), Okazaki, Japan

    Kenta Kobayashi & Yumiko Yoshimura

  6. Division of Visual Information Processing, National Institute for Physiological Sciences, Okazaki, 444-8585, Japan

    Yumiko Yoshimura

  7. Division of Ultrastructural Research, National Institute for Physiological Sciences, Okazaki, Japan

    Nobuhiko Ohno

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  1. Yasuyuki Osanai
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Contributions

YO, YY, and NO contributed to the experimental design. YO, BB, RY, TK, and MY conducted the experiments. HM and KK prepared the viral vectors. YO and YS performed image processing. YO and NO wrote the paper.

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Correspondence to Yasuyuki Osanai or Nobuhiko Ohno.

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The authors declare no competing financial interests.

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All animal study designs and recombinant DNA experiment designs were approved by the Ethics Review Board of the Jichi Medical University.

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Osanai, Y., Battulga, B., Yamazaki, R. et al. Dark Rearing in the Visual Critical Period Causes Structural Changes in Myelinated Axons in the Adult Mouse Visual Pathway. Neurochem Res 47, 2815–2825 (2022). https://doi.org/10.1007/s11064-022-03689-8

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