Short- and long-term functional plasticity of white matter induced by oligodendrocyte depolarization in the hippocampus

Yoshihiko Yamazaki, Hiroki Fujiwara, Kenya Kaneko, Yasukazu Hozumi, Ming Xu, Kazuhiro Ikenaka, Satoshi Fujii, Kenji Tanaka

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

Plastic changes in white matter have received considerable attention in relation to normal cognitive function and learning. Oligodendrocytes and myelin, which constitute the white matter in the central nervous system, can respond to neuronal activity with prolonged depolarization of membrane potential and/or an increase in the intracellular Ca2+ concentration. Depolarization of oligodendrocytes increases the conduction velocity of an action potential along axons myelinated by the depolarized oligodendrocytes, indicating that white matter shows functional plasticity, as well as structural plasticity. However, the properties and mechanism of oligodendrocyte depolarization-induced functional plastic changes in white matter are largely unknown. Here, we investigated the functional plasticity of white matter in the hippocampus using mice with oligodendrocytes expressing channelrhodopsin-2. Using extracellular recordings of compound action potentials at the alveus of the hippocampus, we demonstrated that light-evoked depolarization of oligodendrocytes induced early- and late-onset facilitation of axonal conduction that was dependent on the magnitude of oligodendrocyte depolarization; the former lasted for approximately 10 min, whereas the latter continued for up to 3 h. Using whole-cell recordings from CA1 pyramidal cells and recordings of antidromic action potentials, we found that the early-onset short-lasting component included the synchronization of action potentials. Moreover, pharmacological analysis demonstrated that the activation of Ba2+-sensitive K+ channels was involved in early- and late-onset facilitation, whereas 4-aminopyridine-sensitive K+ channels were only involved in the early-onset component. These results demonstrate that oligodendrocyte depolarization induces short- and long-term functional plastic changes in the white matter of the hippocampus and plays active roles in brain functions. GLIA 2014;62:1299-1312 Main Points: Transcription factor Fosb gene products regulate C5ar1 and C5ar2 gene expression in microglia. In the neurodegenerative state, microglial activation was attenuated in Fosb-null microglia with decreased expression of C5aR1.

Original languageEnglish
Pages (from-to)1299-1312
Number of pages14
JournalGLIA
Volume62
Issue number8
DOIs
Publication statusPublished - 2014

Fingerprint

Oligodendroglia
Hippocampus
Action Potentials
Microglia
Activation Analysis
4-Aminopyridine
White Matter
Pyramidal Cells
Patch-Clamp Techniques
Myelin Sheath
Membrane Potentials
Cognition
Axons
Transcription Factors
Central Nervous System
Learning
Pharmacology
Gene Expression
Light
Brain

Keywords

  • Action potential
  • Axonal conduction
  • Channelrhodopsin-2
  • Myelin

ASJC Scopus subject areas

  • Cellular and Molecular Neuroscience
  • Neurology
  • Medicine(all)

Cite this

Short- and long-term functional plasticity of white matter induced by oligodendrocyte depolarization in the hippocampus. / Yamazaki, Yoshihiko; Fujiwara, Hiroki; Kaneko, Kenya; Hozumi, Yasukazu; Xu, Ming; Ikenaka, Kazuhiro; Fujii, Satoshi; Tanaka, Kenji.

In: GLIA, Vol. 62, No. 8, 2014, p. 1299-1312.

Research output: Contribution to journalArticle

Yamazaki, Y, Fujiwara, H, Kaneko, K, Hozumi, Y, Xu, M, Ikenaka, K, Fujii, S & Tanaka, K 2014, 'Short- and long-term functional plasticity of white matter induced by oligodendrocyte depolarization in the hippocampus', GLIA, vol. 62, no. 8, pp. 1299-1312. https://doi.org/10.1002/glia.22681
Yamazaki, Yoshihiko ; Fujiwara, Hiroki ; Kaneko, Kenya ; Hozumi, Yasukazu ; Xu, Ming ; Ikenaka, Kazuhiro ; Fujii, Satoshi ; Tanaka, Kenji. / Short- and long-term functional plasticity of white matter induced by oligodendrocyte depolarization in the hippocampus. In: GLIA. 2014 ; Vol. 62, No. 8. pp. 1299-1312.
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