Modulatory effects of oligodendrocytes on the conduction velocity of action potentials along axons in the alveus of the rat hippocampal CA1 region

Abstract

Like neurons and astrocytes, oligodendrocytes have a variety of neurotransmitter receptors and ion channels. However, except for facilitating the rapid conduction of action potentials by forming myelin and buffering extracellular K(+), little is known about the direct involvement of oligodendrocytes in neuronal activities. To investigate their physiological roles, we focused on oligodendrocytes in the alveus of the rat hippocampal CA1 region. These cells were found to respond to exogenously applied glutamate by depolarization through N-methyl-D-aspartate (NMDA) receptors and non-NMDA receptors. Electrical stimulation of the border between the alveus and stratum oriens evoked inward currents through several routes involving glutamate receptors and inward rectifier K(+) channels. Moreover, electrical stimulation resembling in vivo activity evoked long-lasting depolarization. To examine the modulatory effects of oligodendrocytes on neuronal activities, we performed dual, whole-cell recording on CA1 pyramidal neurons and oligodendrocytes. Direct depolarization of oligodendrocytes shortened the latencies of action potentials evoked by antidromic stimulation. These results indicate that oligodendrocytes increase the conduction velocity of action potentials by a mechanism additional to saltatory conduction, and that they have active roles in information processing in the brain.

Axon Physiology

“…Conduction velocity along myelinated axons has been shown to depend also on neuron-glia interactions (123,190,526,570). Importantly, depolarization of a single oligodendrocyte was found to increase the action potential conduction velocity of the axons it myelinates by ϳ10% (570).…”

“…Importantly, depolarization of a single oligodendrocyte was found to increase the action potential conduction velocity of the axons it myelinates by ϳ10% (570). Although the precise mechanism has not been yet fully elucidated, it may result from ephaptic interaction between the myelin depolarization and the axon (280; see also sect.…”

“…Mature oligodendrocytes in the rat hippocampus are depolarized by theta burst stimulation of axons. Thus myelin may also dynamically regulate impulse transmission through axons and promote synchrony among the multiple axons under the domain of an individual oligodendrocyte (570). In a recent study, the conduction velocity in small myelinated axons was found to depend on tight junctions between myelin lamellae (153).…”

Chemoarchitecture of glial fibrillary acidic protein (GFAP) and glutamine synthetase in the rat optic nerve: An immunohistochemical study

“…Each oligodendrocyte envelops between one and 30 axonal segments (called internodes), depending on the axon diameter 18) . From a molecular biological standpoint, oligodendrocytes possess various neurotransmitter receptors and ion channels [53][54] . Electrophysiologically, oligodendrocytes facilitate the rapid conduction of action potentials by forming myelin and buffering extracellular K + .…”

Mice with Altered Myelin Proteolipid Protein Gene Expression Display Cognitive Deficits Accompanied by Abnormal Neuron-Glia Interactions and Decreased Conduction Velocities

“…The CV and localization of axonal membrane proteins are known to be altered under certain pathological conditions, including demyelinating diseases, but they have not been shown to vary under nondemyelinating conditions. Recently Yamazaki et al (2007) showed that activation of oligodendrocytes could alter the CV of the axons it myelinates. Thus, the relationship between myelin and axon may not be stationary, but may in fact be dynamic.…”