Controversy surrounding the existence of discrete functional classes of astrocytes in adult gray matter

Abstract

Since 1992, it has been possible to record ionic currents from identified astrocytes in situ, using brain slice technology. Brain slice recordings confirm previous in vitro findings that expression of voltage-gated K(+) and Na(+) channels are a feature of this cell type. In contrast to cultured astrocytes, most investigators found that astrocytes in situ did not contain detectable, or at very best only low, levels of glial fibrillary acidic protein (GFAP). Structural and immunocytochemical investigations determined that these cells are different from oligodendrocyte precursors. In addition to cells with this current pattern, many but not all investigators found a second pool of astrocytes with no voltage-gated ion channels and high GFAP content. These two subpopulations of cells were termed complex and passive astrocytes. The existence of passive astrocytes has been questioned because of possible problems with space clamp conditions and spillage of EGTA-buffered pipette solution around the cells before recordings. Another problem is the fact there is a discrepancy regarding the GFAP content of complex astrocytes. It is of interest that recent immunocytochemical studies suggest the existence of two pools of astrocytes, one with a high GFAP content and one with nondetectable GFAP. Given this, it is tempting to correlate the two (controversial) electrophysiological patterns with immunochemical differences (GFAP) in order to demonstrate two functionally discrete classes of astrocytes in adult gray matter. However, despite evidence that some of the K(+) channels may be involved in proliferation, the role of voltage-gated ion channels in this nonexcitable cell type remains unknown. This is despite the fact that astrocytic Na(+) channels show dramatic changes after pathological events, re-enforcing the notion that the expression of this channel is under tight neuronal control. Several studies suggest that there is a great degree of flexibility and that astrocytes can undergo rapid changes in expression of both membrane ion currents and GFAP. Although it is likely that astrocytes exhibit different structural and membrane properties, this heterogeneity might be a reflection of the flexible plasticity of one astrocyte type under influence of environmental factors rather than of the existence of two distinct and permanent subtypes.