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The Journal of Neuroscience, August 27, 2008, 28(35):8682-8690; doi:10.1523/JNEUROSCI.2411-08.2008

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Cellular/Molecular
Recurrent Inhibitory Network among Striatal Cholinergic Interneurons

Matthew A. Sullivan, Huanmian Chen, and Hitoshi Morikawa

Waggoner Center for Alcohol and Addiction Research, Section of Neurobiology and Institute for Cellular and Molecular Biology, The University of Texas at Austin, Austin, Texas 78712

Correspondence should be addressed to Hitoshi Morikawa, Section of Neurobiology, The University of Texas at Austin, 2415 Speedway, PAT 402, Austin, TX 78712. Email: morikawa{at}mail.utexas.edu

The striatum plays a central role in sensorimotor learning and action selection. Tonically active cholinergic interneurons in the striatum give rise to dense axonal arborizations and significantly shape striatal output. However, it is not clear how the activity of these neurons is regulated within the striatal microcircuitry. In this study, using rat brain slices, we find that stimulation of intrastriatal cholinergic fibers evokes polysynaptic GABA_A IPSCs in cholinergic interneurons. These polysynaptic GABA_A IPSCs were abolished by general nicotinic acetylcholine receptor antagonists and also by a specific antagonist of nicotinic receptors containing β2 subunits. Dopamine receptor antagonists or dopamine depletion failed to block polysynaptic IPSCs, indicating that phasic dopamine release does not directly mediate the polysynaptic transmission. Dual recording from pairs of cholinergic interneurons revealed that activation of a single cholinergic interneuron is capable of eliciting polysynaptic GABA_A IPSCs both in itself and in nearby cholinergic interneurons. Although polysynaptic transmission arising from a single cholinergic interneuron was depressed during repetitive 2 Hz firing, intrastriatal stimulation reliably evoked large polysynaptic IPSCs by recruiting many cholinergic fibers. We also show that polysynaptic GABAergic inhibition leads to a transient suppression of tonic cholinergic interneuron firing. We propose a novel microcircuit in the striatum, in which cholinergic interneurons are connected to one another through GABAergic interneurons. This may provide a mechanism to convert activation of cholinergic interneurons into widespread recurrent inhibition of these neurons via nicotinic excitation of striatal GABAergic neurons.

Key words: striatum; microcircuit; cholinergic neuron; acetylcholine; ACh; nicotinic receptor; patch clamp

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Received May 15, 2008; revised July 9, 2008; accepted July 21, 2008.

Correspondence should be addressed to Hitoshi Morikawa, Section of Neurobiology, The University of Texas at Austin, 2415 Speedway, PAT 402, Austin, TX 78712. Email: morikawa{at}mail.utexas.edu

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