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The Journal of Neuroscience, December 27, 2006, 26(52):13443-13453; doi:10.1523/JNEUROSCI.3578-06.2006

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Behavioral/Systems/Cognitive
Metabotropic Glutamate Receptors Differentially Regulate GABAergic Inhibition in Thalamus

G. Govindaiah and Charles L. Cox

Department of Molecular and Integrative Physiology, Department of Pharmacology, Beckman Institute for Advanced Science and Technology, University of Illinois, Urbana, Illinois 61801

Correspondence should be addressed to Dr. Charles L. Cox, Department of Molecular and Integrative Physiology, University of Illinois, 2357 Beckman Institute, 405 North Mathews Avenue, Urbana, IL 61801. Email: cox2{at}uiuc.edu

Thalamic interneurons and thalamic reticular nucleus (TRN) neurons provide inhibitory innervation of thalamocortical cells that significantly influence thalamic gating. The local interneurons in the dorsal lateral geniculate nucleus (dLGN) give rise to two distinct synaptic outputs: classical axonal and dendrodendritic. Activation of metabotropic glutamate receptors (mGluRs) by agonists or optic tract stimulation increases the output of these presynaptic dendrites leading to increased inhibition of thalamocortical neurons. The present study was aimed to evaluate the actions of specific mGluRs on inhibitory GABA-mediated signaling. We found that the group I mGluR (mGluR_1,5) agonist (RS)-3,5-dihydroxyphenylglycine (DHPG) or optic tract stimulation produced a robust increase in spontaneous IPSCs (sIPSCs) in thalamocortical neurons that was attenuated by the selective mGluR₅ antagonist 2-methyl-6-(phenylethynyl)pyridine hydrochloride (MPEP). In contrast, the group II mGluR (mGluR_2,3) agonists (2R, 4R)-4-aminopyrrolidine-2,4-dicarboxylate (APDC) or (2S,2'R,3'R)-2-(2'3'-dicarboxycyclopropyl)glycine (DCG-IV) suppressed the frequency of sIPSCs. In addition, mGluR_1,5 agonist DHPG produced depolarizations and mGluR_2/3 agonists APDC or L-CCG-I [(2S,1'S,2'S)-2-(carboxycyclopropyl)glycine] produced hyperpolarizations in dLGN interneurons. Furthermore, the enhanced sIPSC activity by optic tract stimulation was reduced when paired with corticothalamic fiber stimulation. The present data indicate that activation of specific mGluR subtypes differentially regulates inhibitory activity via different synaptic pathways. Our results suggest that activation of specific mGluR subtypes can upregulate or downregulate inhibitory activity in thalamic relay neurons, and these actions likely shape excitatory synaptic integration and thus regulate information transfer through thalamocortical circuits.

Key words: inhibition; interneuron; lateral geniculate; LGN; metabotropic glutamate receptor; presynaptic; thalamus

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Received Aug. 17, 2006; revised Nov. 20, 2006; accepted Nov. 21, 2006.

Correspondence should be addressed to Dr. Charles L. Cox, Department of Molecular and Integrative Physiology, University of Illinois, 2357 Beckman Institute, 405 North Mathews Avenue, Urbana, IL 61801. Email: cox2{at}uiuc.edu

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