Developmental changes in the membrane current pattern, K+ buffer capacity, and morphology of glial cells in the corpus callosum slice

Abstract

Recent studies indicated that glial cells in tissue culture can express a variety of different voltage-gated channels, while little is known about the presence of such channels in glial cells in vivo. We used a mouse corpus callosum slice preparation, in which after postnatal day 5 (P5) more than 99% of all perikarya belong to glial cells (Sturrock, 1976), to study the current patterns of glial cells during their development in situ. We combined the patch-clamp technique with intracellular labeling using Lucifer yellow (LY) and subsequent ultrastructural characterization. In slices of mice from P6 to P8, we predominantly found cells expressing delayed-rectifier K+ currents. They were similar to those described for cultured glial precursor cells (Sontheimer et al., 1989). A-type K+ currents or Na+ currents were not or only rarely observed, in contrast to cultured glial precursors. LY labeling revealed that numerous thin processes extended radially from the perikaryon of these cells, and ultrastructural observations suggested that they resemble immature glial cells. In slices of older mice (P10-13), when myelination of the corpus callosum has already commenced, many cells were characterized by an almost linear current-voltage relationship. This current pattern was similar to cultured oligodendrocytes (Sontheimer et al., 1989). Most processes of LY-filled cells with such a current profile extended parallel to each other. Electron microscopy showed that these processes surround thick, unmyelinated axons. We suggest that cells with oligodendrocyte-type electrophysiology are promyelinating oligodendrocytes. In contrast to cultured oligodendrocytes, membrane currents of promyelinating oligodendrocytes in the slice decayed during the voltage command. This decay was due not to inactivation, but to a marked change in the potassium equilibrium potential within the voltage jump. This implies that, in the more mature corpus callosum, small membrane polarizations in a physiological range can lead to extensive changes in the K+ gradient across the glial membrane within a few milliseconds.

Glial potassium channels activated by neuronal firing or intracellular cyclic AMP in Helix.

“…This raises the question as to whether channel and receptor expression may be epiphenomenal to cell culture. Several attempts have therefore been made to record the activity of glial cells in intact (Marrero, Astion, Coles & Orkand, 1989;Erxleben, 1991;Gola, Niel, Delmas & Jacquet, 1993) or semi-intact tissues (brain slices: Walz & MacVicar, 1988;Berger, Schnitzer & Kettenmann, 1991;Steinhauiser, Berger, Frotscher & Kettenmann, 1992;Dani, Chernjavsky & Smith, 1992) and in glial cell-neurone cocultures (Murphy, Blatter, Weir & Baraban, 1993;Mennerick & Zorumski, 1994;Parpura, Basarsky, Liu, Jeftinija, Jeftinija & Haydon, 1994). The results of these studies support the idea put forward by Bevan, Chiu, Gray & Ritchie (1985) that glial cell membrane properties may be regulated by active neurones.…”

Axon-to-Glia Interaction Regulates GABAAReceptor Expression in Oligodendrocytes

“…1989; Berger et al, 1991;Attali et al, 1997). To assess this property, OLGs were cocultured with DRG neurons and monitored electrically by applying voltage steps from 2140 to 140 mV.…”

The Fate of Synaptic Input to NG2 Glial Cells: Neurons Specifically Downregulate Transmitter Release onto Differentiating Oligodendroglial Cells

“…It is known that also OPCs in brain slices express prominent amounts of voltage-gated sodium and potassium channels (Berger et al, 1991(Berger et al, , 1992Chvátal et al, 1995;Ge et al, 2006) (Fig. 6; supplemental Figs.…”