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J Neurophysiol 88: 3150-3166, 2002; doi:10.1152/jn.00335.2002
0022-3077/02 $5.00
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J Neurophysiol (December 1, 2002). 10.1152/jn.00335.2002
Submitted on 6 May 2002
Accepted on 8 August 2002

Mechanisms of Dopamine Activation of Fast-Spiking Interneurons That Exert Inhibition in Rat Prefrontal Cortex

Natalia Gorelova,1 Jeremy K. Seamans,2 and Charles R. Yang3

 1Department of Psychiatry, University of British Columbia, Vancouver, British Columbia V6T 2A1, Canada;  2Department of Physiology and Neuroscience, Medical University of South Carolina, Charleston, South Carolina 29425; and  3Neuroscience Discovery, Eli Lilly and Company, Indianapolis, Indiana 46238-0510

Gorelova, Natalia, Jeremy K. Seamans, and Charles R. Yang. Mechanisms of Dopamine Activation of Fast-Spiking Interneurons That Exert Inhibition in Rat Prefrontal Cortex. J. Neurophysiol. 88: 3150-3166, 2002. Prefrontal cortical dopamine (DA) modulates pyramidal cell excitability directly and indirectly by way of its actions on local circuit GABAergic interneurons. DA modulation of interneuronal functions is implicated in the computational properties of prefrontal networks during cognitive processes and in schizophrenia. Morphologically and electrophysiologically distinct classes of putative GABAergic interneurons are found in layers II-V of rat prefrontal cortex. Our whole cell patch-clamp study shows that DA induced a direct, TTX-insensitive, reversible membrane depolarization, and increased the excitability of fast-spiking (FS) interneurons. The DA-induced membrane depolarization was reduced significantly by D1/D5 receptor antagonist SCH 23390, but not by the D2 receptor antagonist (-)sulpiride, D4 receptor antagonists U101958 or L-745870, alpha 1-adrenoreceptor antagonist prazosin, or serotoninergic receptor antagonist mianserin. The D1/5 agonists SKF81297 or dihydrexidine, but not D2 agonist quinpirole, also induced a prolonged membrane depolarization. Voltage-clamp analyses of the voltage-dependence of DA-sensitive currents, and the effects of changing [K+]O on reversal potentials of DA responses, revealed that DA suppressed a Cs+-sensitive inward rectifier K+ current and a resting leak K+ current. D1/D5, but not D2 agonists mimicked the suppressive effects of DA on the leak current, but the DA effects on the inward rectifier K+ current were not mimicked by either agonist. In a subgroup of FS interneurons, the slowly inactivating membrane outward rectification evoked by depolarizing voltage steps was also attenuated by DA. Collectively, these data showed that DA depolarizes FS interneurons by suppressing a voltage-independent `leak' K+ current (via D1/D5 receptor mechanism) and an inwardly rectifying K+ current (via unknown DA mechanisms). Additional suppression of a slowly inactivating K+ current led to increase in repetitive firing in response to depolarizing inputs. This D1-induced increase in interneuron excitability enhances GABAergic transmission to PFC pyramidal neurons and could represent a mechanism via which DA suppresses persistent firing of pyramidal neurons in vivo.




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