Short- and long-term functional plasticity of white matter induced by oligodendrocyte depolarization in the hippocampus.
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 Ca(2+) 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 Ba(2+) -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.
Department of Physiology, Yamagata University School of Medicine, Yamagata, Japan.
Yoshihiko
Y
Yamazaki
Hiroki
H
Fujiwara
Kenya
K
Kaneko
Yasukazu
Y
Hozumi
Ming
M
Xu
Kazuhiro
K
Ikenaka
Satoshi
S
Fujii
Kenji F
KF
Tanaka
D000200:Action Potentials / Q000187:drug effects; D000818:Animals; D001369:Axons / Q000187:drug effects / Q000502:physiology; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D000075402:Channelrhodopsins; D005260:Female; D006624:Hippocampus / Q000187:drug effects / Q000502:physiology*; D008164:Luminescent Proteins / Q000235:genetics / Q000378:metabolism; D008297:Male; D008564:Membrane Potentials / Q000187:drug effects / Q000502:physiology*; D008822:Mice, Transgenic; D008839:Microelectrodes; D009473:Neuronal Plasticity / Q000187:drug effects / Q000502:physiology*; D009836:Oligodendroglia / Q000187:drug effects / Q000502:physiology*; D018408:Patch-Clamp Techniques; D010775:Photic Stimulation; D015221:Potassium Channels / Q000378:metabolism; D017966:Pyramidal Cells / Q000187:drug effects / Q000502:physiology; D013997:Time Factors; D046509:Tissue Culture Techniques; D066127:White Matter / Q000187:drug effects / Q000502:physiology*
D001426:Bacterial Proteins; D000075402:Channelrhodopsins; D008164:Luminescent Proteins; D015221:Potassium Channels; C054562:yellow fluorescent protein, Bacteria
action potential; axonal conduction; channelrhodopsin-2; myelin