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Cerebral Cortex Advance Access originally published online on November 22, 2006
Cerebral Cortex 2007 17(9):2094-2107; doi:10.1093/cercor/bhl117
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© The Author 2006. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Immunoreactivity for the GABAA Receptor {alpha}1 Subunit, Somatostatin and Connexin36 Distinguishes Axoaxonic, Basket, and Bistratified Interneurons of the Rat Hippocampus

Agnès Baude1,2, Catherine Bleasdale1, Yannis Dalezios1,3,4, Peter Somogyi1 and Thomas Klausberger1,5

1 MRC Anatomical Neuropharmacology Unit, Department of Pharmacology, Oxford University, Oxford OX1 3TH, UK, 2 CNRS UMR 6150, IFR Jean Roche, Faculty of Medicine Nord, University Aix-Marseille II, France, 3 Department of Basic Sciences, Faculty of Medicine, University of Crete, Heraklion, Greece, 4 Institute of Applied and Computational Mathematics, Foundation of Research and Technology, Hellas, Heraklion, Greece, 5 Center for Brain Research, Medical University Vienna, 1090 Vienna, Austria

Address correspondence to Thomas Klausberger, MRC Anatomical Neuropharmacology Unit, Oxford University, Mansfield Road, Oxford OX1 3TH, UK. Email: thomas.klausberger{at}pharm.ox.ac.uk.

Parvalbumin (PV)-expressing interneurons synchronize cortical neurons through {gamma}-aminobutyric acidergic (GABAergic) synapses. Three types of PV-containing interneurons populate stratum pyramidale of the hippocampal CA1 area: basket cells targeting somata and proximal dendrites, axoaxonic cells innervating axon initial segments, and bistratified cells targeting the dendrites of pyramidal cells. We tested whether this axonal specialization is accompanied by a differential expression of molecules involved in neuronal signaling. Immunofluorescence evaluation of interneurons labeled by neurobiotin in vivo shows that axoaxonic cells express significantly less GABAA receptor {alpha}1 subunit in the plasma membrane than basket and bistratified cells. Electron microscopic immunogold labeling reveals that this subunit contributes heavily to extrasynaptic receptors providing a substrate for tonic inhibition. Results from additional immunofluorescence experiments were consistent with the finding that only bistratified cells express the neuropeptide somatostatin. From the molecular profiles, we estimate that basket, bistratified, and axoaxonic cells represent about 60%, 25%, and 15%, respectively, of PV-containing cells in CA1 stratum pyramidale. In addition, all 3 interneuron classes form connexin36-immunopositive dendrodendritic gap junctions. The differential expression of signaling molecules and the relative frequency of cells reflect the specialized temporal contribution of the 3 types of PV-positive interneurons to GABA release in the network.

Key Words: extrasynaptic receptor • firing pattern • gap junction • immunofluorescence • parvalbumin • tonic inhibition


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