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The Journal of Neuroscience, March 1, 1998, 18(5):1693-1703

Segregation of Different GABAA Receptors to Synaptic and Extrasynaptic Membranes of Cerebellar Granule Cells

Zoltan Nusser1, Werner Sieghart2, and Peter Somogyi1

1 Medical Research Council, Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford; Oxford OX1 3TH, United Kingdom, and 2 Section of Biochemical Psychiatry, University Clinic for Psychiatry, A-1090 Vienna, Austria

Two types of GABAA receptor-mediated inhibition (phasic and tonic) have been described in cerebellar granule cells, although these cells receive GABAergic input only from a single cell type, the Golgi cell. In adult rats, granule cells express six GABAA receptor subunits abundantly (alpha 1, alpha 6, beta 2, beta 3, gamma 2, and delta ), which are coassembled into at least four to six distinct GABAA receptor subtypes. We tested whether a differential distribution of GABAA receptors on the surface of granule cells could play a role in the different forms of inhibition, assuming that phasic inhibition originates from the activation of synaptic receptors, whereas tonic inhibition is provided mainly by extrasynaptic receptors. The alpha 1, alpha 6, beta 2/3, and gamma 2 subunits have been found by immunogold localizations to be concentrated in GABAergic Golgi synapses and also are present in the extrasynaptic membrane at a lower concentration. In contrast, immunoparticles for the delta  subunit could not be detected in synaptic junctions, although they were abundantly present in the extrasynaptic dendritic and somatic membranes. Gold particles for the alpha 6, gamma 2, and beta 2/3, but not the alpha 1 and delta , subunits also were concentrated in some glutamatergic mossy fiber synapses, where their colocalization with AMPA-type glutamate receptors was demonstrated. The exclusive extrasynaptic presence of the delta  subunit-containing receptors, together with their kinetic properties, suggests that tonic inhibition could be mediated mainly by extrasynaptic alpha 6beta 2/3delta receptors, whereas phasic inhibition is attributable to the activation of synaptic alpha 1beta 2/3gamma 2, alpha 6beta 2/3gamma 2, and alpha 1alpha 6beta 2/3gamma 2 receptors.

Key words: neurotransmission; cerebellum; inhibition; synapse; ion channel; immunocytochemistry

Copyright © 1998 Society for Neuroscience  0270-6474/98/1851693-11$05.00/0


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