EXPRESSION OF VOLTAGE-ACTIVATED ION CHANNELS BY ASTROCYTES AND OLIGODENDROCYTES IN THE HIPPOCAMPAL SLICE

1. Using patch-clamp recordings, expression of voltage-activated ion channels by identified glial cells in situ was studied in hippocampal slices derived from 5- to 24-day-old rats. Glial cells were filled with Lucifer yellow during recording, and were identified by staining for glial fibrillary acidic protein (GFAP). Of 105 cells presumed to be glial cells from which recordings were obtained, 40 were identified as astrocytes and 22 as oligodendrocytes. 2. Astrocytes in the hippocampal slice express three types of K+ current, singly or in combination: delayed rectifying currents (K(d)), transient ''A''-type currents (K(a)) and inward-rectifying currents (K(ir)). K(d)-like currents were observed in 88% of astrocytes recorded; these currents activated rapidly with a threshold of -40 mV and did not inactivate during a 10- to 30-ms pulse. A-type transient K+ currents were identified in 43% of astrocytes and required a negative holding potential (-110 mV) for activation. These activated at about -50 mV, and their time constant of inactivation was close to 10 ms. In 20% of astrocytes recorded in slices from animals >7 days old, inwardly rectifying K+ currents were observed in addition to K(d) or K(a). 3. Voltage-activated Na+ currents were observed in 11 of the 105 cells, and 5 of these were identified as astrocytes by GFAP staining. These were located in either stratum oriens or close to the granule cell layer in CA3. Na+ current densities ranged from 1.5 to 90 pA/pF. Voltage steps more positive than -40 mV were required for activation, peaks were close to -10 mV, and time to peak was between 300 and 800 mus. Extrapolated current reversal potentials were close to the theoretical Na+ equilibrium potential. 4. Spontaneous action potentials were never observed in any of the hippocampal astrocytes recorded, including those astrocytes that expressed Na+ currents. Additionally, action potentials could not be induced by current injections. By contrast, 26 hippocampal neurons recorded in the same slices showed both spontaneous and elicited action potentials as well as synaptic currents. 5. Oligodendrocytes, identified by lack of GFAP staining and cell morphology, had resting potentials ranging between -25 and -82 mV in 5 mM KCl. In approximately 50% of oligodendrocytes, time-dependent currents were not observed and only time-independent currents with linear current-voltage curves were recorded. In the remaining 50% of oligodendrocytes, time- and voltage-dependent K+ currents characterized by inward rectification were present. In all oligodendrocytes recorded, tail current analysis identified time-dependent as well as time-independent currents as K+ currents with the reversal potential being close to the equilibrium potential for potassium. 6. These observations demonstrate the ability of glial cells in situ to express voltage-activated ion channels and show that those channels are not an artifact of cell culture. Astrocytes in the hippocampal slice express Na+ as well as K+ channels. Because Na+ channels are expressed in low densities in these cells and regenerative responses are not present, it is likely that these channels subserve functions other than action potential generation.