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Volume 17, Number 21, Issue of November 1, 1997 pp. 8498-8505
Copyright ©1997 Society for Neuroscience

Substantia Nigra D₁ Receptors and Stimulation of Striatal Cholinergic Interneurons by Dopamine: A Proposed Circuit Mechanism

Received June 10, 1997; revised Aug. 4, 1997; accepted Aug. 13, 1997.

Elizabeth D. Abercrombie and Peter DeBoer

Center for Molecular and Behavioral Neuroscience, Rutgers University, Newark, New Jersey 07102

Dopamine release can regulate striatal acetylcholine efflux in vivo through at least two receptor mechanisms: (1) direct inhibition by dopamine D₂ receptors on the cholinergic neurons, and (2) excitation initiated by dopamine D₁ receptors. The neuroanatomical locus of the latter population of D₁ receptors and the pathway(s) involved in the expression of their influence are controversial issues. We have tested the hypothesis that D₁ receptors in substantia nigra pars reticulata are involved in the excitatory component of dopaminergic actions on striatal acetylcholine output. In vivo microdialysis was used in awake rats. Infusion of the selective D₁ receptor agonist R(+)-1-Phenyl-2,3,4,5-tetrahydro-1H-3-benzazepine-7,8-diol (SKF 38393) hydrochloride into pars reticulata of substantia nigra elicited a significant increase in striatal acetylcholine efflux. Likewise, D-amphetamine applied into pars reticulata of substantia nigra by reverse dialysis produced an elevation in acetylcholine output measured at a second microdialysis probe in the striatum. Application of D-amphetamine in the striatum by reverse dialysis elicited a decrease in striatal acetylcholine efflux that could be reversed subsequently by local application of D-amphetamine in substantia nigra pars reticulata. A 2 mg/kg intraperitoneal dose of D-amphetamine, which has no net effect on striatal acetylcholine output under control conditions, elicited a significant decrease in acetylcholine efflux when the D₁ receptor antagonist R(+)-7-Chloro-8-hydroxy-3-methyl-1-phenyl-2,3,4,5-tetrahydro-1H-3-benzazepine (SCH 23390) hydrochloride was applied simultaneously via a second microdialysis probe in substantia nigra pars reticulata. Thus, an excitatory D₁-mediated influence on striatal acetylcholine output is initiated in substantia nigra pars reticulata, and this influence contributes to the effects of indirect dopaminergic agonists such as D-amphetamine on striatal acetylcholine efflux. These results indicate an important role of somatodendritic dopamine release, in addition to nerve terminal dopamine release, in the regulation of activity in basal ganglia circuits.

Key words: acetylcholine; dopamine; GABA; substantia nigra; striatum; D-amphetamine; dopamine D₁ receptor; in vivo microdialysis

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