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Modulatory Effects of Perineuronal Oligodendrocytes on Neuronal Activity in the Rat Hippocampus

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Abstract

Action potentials are fundamental to relaying information from region to region in the nervous system. Changes in action potential firing patterns in neural circuits influence how the brain processes information. In our previous study, we focused on interneuron/perineuronal astrocyte pairs in the hippocampal CA1 region and reported that direct depolarization of perineuronal astrocytes modulated the firing pattern of interneurons. In the current study, we investigated the morphological and electrophysiological properties of perineuronal oligodendrocytes, and examined their modulatory effects on interneuronal firing in the CA1 region. Perineuronal oligodendrocytes only had a few processes, which were crooked, intricately twisted, and twined around the soma and proximal region of the main processes of adjacent interneurons. Whole-cell current patterns of perineuronal oligodendrocytes were homogenous and the current–voltage relationship showed remarkable outward rectification. Although the K+ channel blockers, tetraethylammonium and 4-aminopyridine, clearly blocked outward currents, Ba2+ did not significantly alter whole-cell currents. Unlike perineuronal astrocytes, the depolarization of perineuronal oligodendrocytes had no effect on interneuronal firing; however, when the interneurons were firing at a higher frequency, the hyperpolarization of perineuronal oligodendrocytes suppressed their action potentials. The suppressive effects of perineuronal oligodendrocytes were inhibited in the presence of a low concentration of tetraethylammonium, which selectively blocked deep and fast afterhyperpolarization. These results suggest that perineuronal oligodendrocytes suppress interneuronal firing through their influence on K+ channels, which are responsible for deep and fast afterhyperpolarization.

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Acknowledgements

This research was supported by JSPS KAKENHI [Grant-in-Aid for Scientific Research on Innovation Areas “Glial assembly: a new regulatory machinery of brain function and disorders” (Grant Number 25117005) and Grant-in-Aid for Scientific Research (C) (Grant Number 16K01943)].

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Authors and Affiliations

  1. Department of Physiology, Yamagata University School of Medicine, 2-2-2 Iida-Nishi, Yamagata, 990-9585, Japan

    Yoshihiko Yamazaki, Kenya Kaneko & Satoshi Fujii

  2. Department of Anatomy & Cell Biology, Yamagata University School of Medicine, Yamagata, 990-9585, Japan

    Yasukazu Hozumi

  3. Department of Cell Biology and Morphology, Akita University Graduate School of Medicine, Akita, 010-8543, Japan

    Yasukazu Hozumi

Authors
  1. Yoshihiko Yamazaki
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  2. Yasukazu Hozumi
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  3. Kenya Kaneko
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  4. Satoshi Fujii
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Correspondence to Yoshihiko Yamazaki.

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The authors declare that they have no conflict of interest.

Ethical Approval

All animal procedures were conducted in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals and were approved by the Committee for Animal Experimentation of Yamagata University.

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Yamazaki, Y., Hozumi, Y., Kaneko, K. et al. Modulatory Effects of Perineuronal Oligodendrocytes on Neuronal Activity in the Rat Hippocampus. Neurochem Res 43, 27–40 (2018). https://doi.org/10.1007/s11064-017-2278-9

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  • DOI: https://doi.org/10.1007/s11064-017-2278-9

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