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The Journal of Neuroscience, March 15, 1998, 18(6):2009-2016

Dopamine D₁ Receptors Facilitate GABA_A Synaptic Currents in the Rat Substantia Nigra Pars Reticulata

Gabriele Radnikow and Ulrich Misgeld

I. Physiologisches Institut der Universität Heidelberg, D-69120 Heidelberg, Germany

GABA neurons in the substantia nigra pars reticulata receive input from GABAergic fibers originating in the forebrain. The role of dopaminergic D₁ receptors located on these fibers was investigated using tight-seal whole-cell recordings from visually identified pars reticulata neurons of rat substantia nigra slices. Nondopaminergic pars reticulata neurons were characterized by their electrophysiological properties. Postsynaptic currents evoked by minimal stimulation in the presence of ionotropic glutamate receptor antagonists were blocked by bicuculline, indicating that they were GABA_A IPSCs. Evoked GABA_A IPSCs were potentiated by D₁ receptor agonists. After application of D₁ receptor agonists, miniature IPSCs [recorded in the presence of tetrodotoxin (TTX) and the Ca²⁺ channel blocker Cd²⁺] increased in frequency but not in amplitude. Effects of D₁ receptor stimulation were mimicked by forskolin, as expected, if a cAMP-dependent mechanism was involved. The D₁ antagonist SCH23390 blocked the effects of the agonists, and perfusion with SCH23390 resulted in a reduction of evoked IPSCs. In TTX and Cd²⁺, which prevented dopamine release, the D₁ antagonist had no effect on miniature IPSCs. Blocking of monoamine uptake by imipramine increased the amplitude of evoked IPSCs. We conclude that dopamine released from dendrites of dopaminergic neurons enhances GABA release in the pars reticulata of the substantia nigra through D₁ receptors presumably located on striatonigral afferents. These D₁ receptors, thereby, can reinforce D₁ receptor-mediated activation of striatal projection neurons that inhibit the inhibitory output neurons of the basal ganglia in substantia nigra.

Key words: dopamine; D₁ receptors; GABA_A IPSCs; GABA release; miniature IPSCs; forskolin; substantia nigra; direct pathway

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Copyright © 1998 Society for Neuroscience  0270-6474/98/1862009-08$05.00/0

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