Region- and Cell Type-Specific Facilitation of Synaptic Function at Destination Synapses Induced by Oligodendrocyte Depolarization

Yoshihiko Yamazaki, Yoshifumi Abe, Shinsuke Shibata, Tomoko Shindo, Satoshi Fujii, Kazuhiro Ikenaka, Kenji F. Tanaka

Research output: Contribution to journalArticle

Abstract

The axonal conduction of action potentials affects the absolute time it takes to transmit nerve impulses as well as temporal summation at destination synapses. At the physiological level, oligodendrocyte depolarization facilitates axonal conduction along myelinated fibers in the hippocampus; however, the functional significance of this facilitation is largely unknown. In this study, we examined the physiology of the facilitation of axonal conduction by investigating the changes in synaptic responses at destination synapses using male and female mice in which channelrhodopsin-2 expression was restricted to oligodendrocytes. The subiculum, one of the projection areas of the examined axons at the alveus of the hippocampus, is divided into three regions (proximal, mid, and distal) and contains two types of principal neurons: regular firing and bursting pyramidal cells. We found a significant increase in excitatory synaptic responses following optogenetic oligodendrocyte depolarization in bursting neurons at two of the three regions, but not in regular firing neurons at any region. The long-term potentiation (LTP) induced by theta burst stimulation at the synapses showing a significant increase was also enhanced after oligodendrocyte depolarization. Conversely, the reduction of oligodendrocyte depolarization during theta burst stimulation, which was achieved by photostimulation of archaerhodopsin-T expressed selectively on oligodendrocytes, reduced the magnitude of LTP. These results show that oligodendrocyte depolarization contributes to the fine control of synaptic activity between the axons they myelinate and targets subicular cells in a region- and cell type-specific manner, and suggest that oligodendrocyte depolarization during conditioning of stimuli is involved in the induction of LTP.SIGNIFICANCE STATEMENT All activity in the nervous system depends on the propagation of action potentials. Changes in the axonal conduction of action potentials influence the timing of synaptic transmission and information processing in neural circuits. At the physiological level, oligodendrocyte depolarization facilitates axonal conduction along myelinated fibers. In this study, we investigated the functional significance of the facilitation of axonal conduction induced by physiological oligodendrocyte depolarization. Using optogenetics and electrophysiological recordings, we demonstrated that oligodendrocyte depolarization in mice expressing channelrhodopsin-2 on oligodendrocytes increased excitatory synaptic responses and enhanced the induction of long-term potentiation at destination synapses in a region- and cell type-specific manner. This facilitation may have a hitherto unappreciated influence on the transfer of information between regions in the nervous system.

Original languageEnglish
Pages (from-to)4036-4050
Number of pages15
JournalThe Journal of neuroscience : the official journal of the Society for Neuroscience
Volume39
Issue number21
DOIs
Publication statusPublished - 2019 May 22

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Oligodendroglia
Synapses
Long-Term Potentiation
Action Potentials
Optogenetics
Hippocampus
Neurons
Nervous System
Axons
Pyramidal Cells
Automatic Data Processing
Synaptic Transmission

Keywords

  • channelrhodopsin-2
  • hippocampus
  • long-term potentiation
  • subiculum

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Region- and Cell Type-Specific Facilitation of Synaptic Function at Destination Synapses Induced by Oligodendrocyte Depolarization. / Yamazaki, Yoshihiko; Abe, Yoshifumi; Shibata, Shinsuke; Shindo, Tomoko; Fujii, Satoshi; Ikenaka, Kazuhiro; Tanaka, Kenji F.

In: The Journal of neuroscience : the official journal of the Society for Neuroscience, Vol. 39, No. 21, 22.05.2019, p. 4036-4050.

Research output: Contribution to journalArticle

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