Modulatory Effects of Perineuronal Oligodendrocytes on Neuronal Activity in the Rat Hippocampus
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ORIGINAL PAPER
Modulatory Effects of Perineuronal Oligodendrocytes on Neuronal Activity in the Rat Hippocampus Yoshihiko Yamazaki1 · Yasukazu Hozumi2,3 · Kenya Kaneko1 · Satoshi Fujii1
Received: 9 March 2017 / Revised: 17 April 2017 / Accepted: 20 April 2017 © Springer Science+Business Media New York 2017
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 * Yoshihiko Yamazaki [email protected]‑u.ac.jp 1
Department of Physiology, Yamagata University School of Medicine, 2‑2‑2 Iida‑Nishi, Yamagata 990‑9585, Japan
2
Department of Anatomy & Cell Biology, Yamagata University School of Medicine, Yamagata 990‑9585, Japan
3
Department of Cell Biology and Morphology, Akita University Graduate School of Medicine, Akita 010‑8543, Japan
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. Keywords Oligodendrocyte · Perineuronal glial cell · Hippocampus · Afterhyperpolarization
Introduction Glial cells, in addition to their supportive roles in the nervous system, make up functional units with neurons, e.g., the tripartite synapse by astrocytes [1] or oligodendrocyte bound axonal bale [2], which play novel roles in neuronal activity and information processing. The best-known function of oligodendrocytes in the central nervous system is the myelination of axons, along with K + buffering along axons [3, 4]. More
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