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The Journal of Neuroscience, November 9, 2005, 25(45):10520-10536; doi:10.1523/JNEUROSCI.2547-05.2005
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Cellular/Molecular
Metabotropic Glutamate Receptor 8-Expressing Nerve Terminals Target Subsets of GABAergic Neurons in the Hippocampus
Francesco Ferraguti,1,2 Thomas Klausberger,1,3 Philip Cobden,1 Agnes Baude,1,4 J. David B. Roberts,1 Peter Szucs,5 Ayae Kinoshita,6 Ryuichi Shigemoto,7 Peter Somogyi,1 andYannis Dalezios1,8 1Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, Oxford University, Oxford OX1 3TH, United Kingdom, 2Department of Pharmacology, Innsbruck Medical University, A-6020 Innsbruck, Austria, 3Centre for Brain Research, Medical University Vienna, A-1090 Vienna, Austria, 4Laboratoire de NeuroPhysiologie Cellulaire, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 6150, 13402 Cedex 20 Marseille, France, 5Department of Anatomy, Histology, and Embryology, Faculty of Medicine, Medical and Health Centre, University of Debrecen, H-4012 Debrecen, Hungary, 6Horizontal Medical Research Organization, Kyoto University Graduate School of Medicine, Kyoto 606-8501, Japan, 7Division of Cerebral Structure, National Institute for Physiological Sciences, Okazaki 444-8787, Japan, and 8Department of Basic Sciences, Faculty of Medicine, University of Crete, GR-71003 Heraklion, Greece
Presynaptic metabotropic glutamate receptors (mGluRs) show a highly selective expression and subcellular location in nerve terminals modulating neurotransmitter release. We have demonstrated that alternatively spliced variants of mGluR8, mGluR8a and mGluR8b, have an overlapping distribution in the hippocampus, and besides perforant path terminals, they are expressed in the presynaptic active zone of boutons making synapses selectively with several types of GABAergic interneurons, primarily in the stratum oriens. Boutons labeled for mGluR8 formed either type I or type II synapses, and the latter were GABAergic. Some mGluR8-positive boutons also expressed mGluR7 or vasoactive intestinal polypeptide. Interneurons strongly immunopositive for the muscarinic M2 or the mGlu1 receptors were the primary targets of mGluR8-containing terminals in the stratum oriens, but only neurochemically distinct subsets were innervated by mGluR8-enriched terminals. The majority of M2-positive neurons were mGluR8 innervated, but a minority, which expresses somatostatin, was not. Rare neurons coexpressing calretinin and M2 were consistently targeted by mGluR8-positive boutons. In vivo recording and labeling of an mGluR8-decorated and strongly M2-positive interneuron revealed a trilaminar cell with complex spike bursts during theta oscillations and strong discharge during sharp wave/ripple events. The trilaminar cell had a large projection from the CA1 area to the subiculum and a preferential innervation of interneurons in the CA1 area in addition to pyramidal cell somata and dendrites. The postsynaptic interneuron type-specific expression of the high-efficacy presynaptic mGluR8 in both putative glutamatergic and in identified GABAergic terminals predicts a role in adjusting the activity of interneurons depending on the level of network activity.
Key words: presynaptic; immunogold labeling; muscarinic receptors; inhibition; network oscillation; hippocampus
Received June 21, 2005; revised September 9, 2005; accepted October 2, 2005.
This article has been cited by other articles:
S. Jinno, T. Klausberger, L. F. Marton, Y. Dalezios, J. D. B. Roberts, P. Fuentealba, E. A. Bushong, D. Henze, G. Buzsaki, and P. Somogyi
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[Abstract] [Full Text] [PDF]
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Differential Changes of Group II and Group III mGluR Function in Central Amygdala Neurons in a Model of Arthritic Pain
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[Abstract] [Full Text] [PDF]
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