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Volume 16, Number 9, Issue of May 1, 1996 pp. 2912-2923
Copyright ©1996 Society for Neuroscience

Upregulation of GABA_A Current by Astrocytes in Cultured Embryonic Rat Hippocampal Neurons

Received Dec. 15, 1995; revised Feb. 12, 1996; accepted Feb. 14, 1996.

Qi-Ying Liu, Anne E. Schaffner, Yong-Xin Li, Veronica Dunlap, and Jeffery L. Barker

Laboratory of Neurophysiology, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892

Embryonic rat hippocampal neurons were cultured on poly-D-lysine (PDL) or a monolayer of postnatal cortical astrocytes to reveal putative changes in neuronal physiology that involve astrocyte-derived signals during the first 4 d of culture. GABA-induced Cl current (I_GABA) was quantified using outside-out and whole-cell patch-clamp recordings beginning at 30 min, when cells had become adherent. The amplitude and density (current normalized to membrane capacitance) of I_GABA in neurons grown on astrocytes became statistically greater than that recorded in neurons grown on PDL after 2 hr in culture (HIC). Although the current density remained unchanged in neurons on astrocytes, that in neurons on PDL decreased and became statistically lower beginning after 2 HIC. The differences in amplitude and density of I_GABA in the two groups of neurons were maintained during the 4 d experiment. The upregulation effect of astrocytes on neuronal I_GABA required intimate contact between the neuronal cell body and underlying astrocytes. Suppression of spontaneous Ca_c²⁺ elevations in astrocytes by bis(2-aminophenoxy)ethane-N,N,N,N-tetra-acetic acid that was loaded intracellularly decreased their modulatory effects on I_GABA. I_GABA in all cells was blocked completely by bicuculline and exhibited virtually identical affinity constants, Hill coefficients, and potentiation by diazepam in the two groups. Outside-out patch recordings revealed identical unitary properties of I_GABA in the two groups. More channels per unit of membrane area could explain the astrocyte enhancement of I_GABA. The results reveal that cortical astrocytes potentiate I_GABA in hippocampal neurons in a contact-dependent manner via a mechanism involving astrocyte Ca_c²⁺ elevation.

Key words: GABA_A receptor; ion channels; neuronal development; astrocyte; intracellular calcium; hippocampus; rat

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