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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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Mol. Cell. Biol., September 15, 2003; 23(18): 6419 - 6434.
[Abstract] [Full Text] [PDF]

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G. B. Richerson and Y. Wu
Dynamic Equilibrium of Neurotransmitter Transporters: Not Just for Reuptake Anymore
J Neurophysiol, September 1, 2003; 90(3): 1363 - 1374.
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I. Spigelman, Z. Li, J. Liang, E. Cagetti, S. Samzadeh, R. M. Mihalek, G. E. Homanics, and R. W. Olsen
Reduced Inhibition and Sensitivity to Neurosteroids in Hippocampus of Mice Lacking the GABAA Receptor {delta} Subunit
J Neurophysiol, August 1, 2003; 90(2): 903 - 910.
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Y. Iwai, M. Fagiolini, K. Obata, and T. K. Hensch
Rapid Critical Period Induction by Tonic Inhibition in Visual Cortex
J. Neurosci., July 30, 2003; 23(17): 6695 - 6702.
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F.-C. Hsu, R. Waldeck, D. S. Faber, and S. S. Smith
Neurosteroid Effects on GABAergic Synaptic Plasticity in Hippocampus
J Neurophysiol, April 1, 2003; 89(4): 1929 - 1940.
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D. J Rossi, M. Hamann, and D. Attwell
Multiple modes of GABAergic inhibition of rat cerebellar granule cells
J. Physiol., April 1, 2003; 548(1): 97 - 110.
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F.-C. Hsu and S. S. Smith
Progesterone Withdrawal Reduces Paired-Pulse Inhibition in Rat Hippocampus: Dependence on GABAA Receptor alpha 4 Subunit Upregulation
J Neurophysiol, January 1, 2003; 89(1): 186 - 198.
[Abstract] [Full Text] [PDF]

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J. Y. T. Yeung, K. J. Canning, G. Zhu, P. Pennefather, J. F. MacDonald, and B. A. Orser
Tonically Activated GABAA Receptors in Hippocampal Neurons Are High-Affinity, Low-Conductance Sensors for Extracellular GABA
Mol. Pharmacol., January 1, 2003; 63(1): 2 - 8.
[Abstract] [Full Text] [PDF]

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E. Cagetti, J. Liang, I. Spigelman, and R. W. Olsen
Withdrawal from Chronic Intermittent Ethanol Treatment Changes Subunit Composition, Reduces Synaptic Function, and Decreases Behavioral Responses to Positive Allosteric Modulators of GABAA Receptors
Mol. Pharmacol., January 1, 2003; 63(1): 53 - 64.
[Abstract] [Full Text] [PDF]

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R. Riquelme, C. P. Miralles, and A. L. De Blas
Bergmann Glia GABAA Receptors Concentrate on the Glial Processes That Wrap Inhibitory Synapses
J. Neurosci., December 15, 2002; 22(24): 10720 - 10730.
[Abstract] [Full Text] [PDF]

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L. W J Bosman, T. W Rosahl, and A. B Brussaard
Neonatal development of the rat visual cortex: synaptic function of GABAa receptor {alpha} subunits
J. Physiol., November 15, 2002; 545(1): 169 - 181.
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M. T Bianchi and R. L Macdonald
Slow phases of GABAA receptor desensitization: structural determinants and possible relevance for synaptic function
J. Physiol., October 1, 2002; 544(1): 3 - 18.
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I. Sarto, T. Klausberger, N. Ehya, B. Mayer, K. Fuchs, and W. Sieghart
A Novel Site on gamma 3 Subunits Important for Assembly of GABAA Receptors
J. Biol. Chem., August 16, 2002; 277(34): 30656 - 30664.
[Abstract] [Full Text] [PDF]

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M. Beck, K. Brickley, H. L. Wilkinson, S. Sharma, M. Smith, P. L. Chazot, S. Pollard, and F. A. Stephenson
Identification, Molecular Cloning, and Characterization of a Novel GABAA Receptor-associated Protein, GRIF-1
J. Biol. Chem., August 9, 2002; 277(33): 30079 - 30090.
[Abstract] [Full Text] [PDF]

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Z. Nusser and I. Mody
Selective Modulation of Tonic and Phasic Inhibitions in Dentate Gyrus Granule Cells
J Neurophysiol, May 1, 2002; 87(5): 2624 - 2628.
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T. Klausberger, J. D. B. Roberts, and P. Somogyi
Cell Type- and Input-Specific Differences in the Number and Subtypes of Synaptic GABAA Receptors in the Hippocampus
J. Neurosci., April 1, 2002; 22(7): 2513 - 2521.
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K. M. Wohlfarth, M. T. Bianchi, and R. L. Macdonald
Enhanced Neurosteroid Potentiation of Ternary GABAA Receptors Containing the delta Subunit
J. Neurosci., March 1, 2002; 22(5): 1541 - 1549.
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S. B. Christie, C. P. Miralles, and A. L. De Blas
GABAergic Innervation Organizes Synaptic and Extrasynaptic GABAA Receptor Clustering in Cultured Hippocampal Neurons
J. Neurosci., February 1, 2002; 22(3): 684 - 697.
[Abstract] [Full Text] [PDF]

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H. Mohler, J. M. Fritschy, and U. Rudolph
A New Benzodiazepine Pharmacology
J. Pharmacol. Exp. Ther., January 1, 2002; 300(1): 2 - 8.
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Z. Mtchedlishvili, E. H Bertram, and J. Kapur
Diminished allopregnanolone enhancement of GABAA receptor currents in a rat model of chronic temporal lobe epilepsy
J. Physiol., December 1, 2001; 537(2): 453 - 465.
[Abstract] [Full Text] [PDF]

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P. A Davies, E. F Kirkness, and T. G Hales
Evidence for the formation of functionally distinct {alpha}{beta}{gamma}{varepsilon} GABAA receptors
J. Physiol., November 15, 2001; 537(1): 101 - 113.
[Abstract] [Full Text] [PDF]

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S. H. Browne, J. Kang, G. Akk, L. W. Chiang, H. Schulman, J. R. Huguenard, and D. A. Prince
Kinetic and Pharmacological Properties of GABAA Receptors in Single Thalamic Neurons and GABAA Subunit Expression
J Neurophysiol, November 1, 2001; 86(5): 2312 - 2322.
[Abstract] [Full Text] [PDF]

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A. F. Keller, J. A. M. Coull, N. Chery, P. Poisbeau, and Y. De Koninck
Region-Specific Developmental Specialization of GABA-Glycine Cosynapses in Laminas I-II of the Rat Spinal Dorsal Horn
J. Neurosci., October 15, 2001; 21(20): 7871 - 7880.
[Abstract] [Full Text] [PDF]

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C. E. Adkins, G. V. Pillai, J. Kerby, T. P. Bonnert, C. Haldon, R. M. McKernan, J. E. Gonzalez, K. Oades, P. J. Whiting, and P. B. Simpson
alpha 4beta 3delta GABAA Receptors Characterized by Fluorescence Resonance Energy Transfer-derived Measurements of Membrane Potential
J. Biol. Chem., October 12, 2001; 276(42): 38934 - 38939.
[Abstract] [Full Text] [PDF]

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A. J. Delaney and P. Sah
Pathway-Specific Targeting of GABAA Receptor Subtypes to Somatic and Dendritic Synapses in the Central Amygdala
J Neurophysiol, August 1, 2001; 86(2): 717 - 723.
[Abstract] [Full Text] [PDF]

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C. Sur, K. A. Wafford, D. S. Reynolds, K. L. Hadingham, F. Bromidge, A. Macaulay, N. Collinson, G. O'Meara, O. Howell, R. Newman, et al.
Loss of the Major GABAA Receptor Subtype in the Brain Is Not Lethal in Mice
J. Neurosci., May 15, 2001; 21(10): 3409 - 3418.
[Abstract] [Full Text] [PDF]

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S. Vicini, C. Ferguson, K. Prybylowski, J. Kralic, A. L. Morrow, and G. E. Homanics
GABAA Receptor {alpha}1 Subunit Deletion Prevents Developmental Changes of Inhibitory Synaptic Currents in Cerebellar Neurons
J. Neurosci., May 1, 2001; 21(9): 3009 - 3016.
[Abstract] [Full Text] [PDF]

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A. Devor, J.-M. Fritschy, and Y. Yarom
Spatial Distribution and Subunit Composition of GABAA Receptors in the Inferior Olivary Nucleus
J Neurophysiol, April 1, 2001; 85(4): 1686 - 1696.
[Abstract] [Full Text] [PDF]

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G. W. Hubert, M. Paquet, and Y. Smith
Differential Subcellular Localization of mGluR1a and mGluR5 in the Rat and Monkey Substantia Nigra
J. Neurosci., March 15, 2001; 21(6): 1838 - 1847.
[Abstract] [Full Text] [PDF]

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A. L. Scotti and H. Reuter
Synaptic and extrasynaptic gamma -aminobutyric acid type A receptor clusters in rat hippocampal cultures during development
PNAS, March 1, 2001; (2001) 61028798.
[Abstract] [Full Text]

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S. J. Mitchell and R. A. Silver
GABA Spillover from Single Inhibitory Axons Suppresses Low-Frequency Excitatory Transmission at the Cerebellar Glomerulus
J. Neurosci., December 1, 2000; 20(23): 8651 - 8658.
[Abstract] [Full Text] [PDF]

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A. Rao, E. M. Cha, and A. M. Craig
Mismatched Appositions of Presynaptic and Postsynaptic Components in Isolated Hippocampal Neurons
J. Neurosci., November 15, 2000; 20(22): 8344 - 8353.
[Abstract] [Full Text] [PDF]


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