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The Journal of Neuroscience, October 1, 1998, 18(19):8074-8085

Dopamine Depletion Reorganizes Projections from the Nucleus Accumbens and Ventral Pallidum That Mediate Opioid-Induced Motor Activity

Lynn Churchill¹, Mark A. Klitenick², and Peter W. Kalivas³

¹ Alcohol and Drug Abuse Program, Department of Veterinary and Comparative Anatomy, Pharmacology, and Physiology, Washington State University, Pullman, Washington 99164, ² Department of Behavioral Neuropharmacology, Allelix Neuroscience, South Plainfield, New Jersey 07080, and ³ Department of Physiology and Neuroscience, Medical University of South Carolina, Charleston, South Carolina 29425

Motor activity elicited pharmacologically from the nucleus accumbens by the µ-opioid receptor agonist D-Ala-Tyr-Gly-NMePhe-Gly-OH (DAMGO) is augmented in rats sustaining dopamine depletions. GABAergic projections from the nucleus accumbens to ventral pallidum and ventral tegmental area (VTA) are involved because stimulation of GABA_B receptors in the VTA (by baclofen) or GABA_A receptors in the ventral pallidum (by muscimol) inhibit the motor response induced by the microinjection of DAMGO into the nucleus accumbens. The present study was done to determine which of these projections is mediating the augmented DAMGO-induced motor activity that follows 6-hydroxydopamine lesions of the nucleus accumbens. The inhibition of DAMGO-induced activation by pallidal injections of muscimol was markedly attenuated in lesioned animals, whereas the inhibition by VTA injections with baclofen was greatly enhanced. A similar switch in emphasis from pallidal to mesencephalic efferents was not observed for dopamine-induced motor activity, because muscimol microinjections inhibited the response elicited by dopamine microinjection into the nucleus accumbens in all subjects. The stimulation of µ-opioid receptors in the ventral pallidum also elicits motor activation, and this is blocked by baclofen microinjection into the VTA. However, after dopamine depletion in the nucleus accumbens, baclofen in the VTA was ineffective in blocking the motor response by DAMGO in the ventral pallidum. These data reveal that dopamine depletion in the nucleus accumbens produces a lesion-induced plasticity that alters the effect of µ-opioid receptor stimulation on efferent projections from the nucleus accumbens and ventral pallidum.

Key words: dopamine lesion; opioid receptor; nucleus accumbens; ventral pallidum; ventral mesencephalon; locomotion

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Copyright © 1998 Society for Neuroscience  0270-6474/98/18198074-12$05.00/0

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