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The Journal of Neuroscience, August 4, 2004, 24(31):6939-6945; doi:10.1523/JNEUROSCI.0671-04.2004

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Behavioral/Systems/Cognitive
A Single In Vivo Exposure to Cocaine Abolishes Endocannabinoid-Mediated Long-Term Depression in the Nucleus Accumbens

Lawrence Fourgeaud,^1 * Susana Mato,^1 * Delphine Bouchet,² Agnès Hémar,² Paul F. Worley,³ and Olivier J. Manzoni¹

¹Equipe Institut National de la Santé et de la Recherche Médicale Avenir (Plasticité Synaptique: Maturation et Addiction), and ²Unité Mixte de Recherche, Centre National de la Recherche Scientifique 5091, Institut Magendie des Neurosciences, 33077 Bordeaux Cedex, France, and ³Department of Neuroscience, The Johns Hopkins School of Medicine, Baltimore, Maryland 21287

In the nucleus accumbens (NAc), a key structure to the effects of all addictive drugs, presynaptic cannabinoid CB1 receptors (CB1Rs) and postsynaptic metabotropic glutamate 5 receptors (mGluR5s) are the principal effectors of endocannabinoid (eCB)-mediated retrograde long-term depression (LTD) (eCB-LTD) at the prefrontal cortex-NAc synapses. Both CB1R and mGluR5 are involved in cocaine-related behaviors; however, the impact of in vivo cocaine exposure on eCB-mediated retrograde synaptic plasticity remains unknown. Electrophysiological and biochemical approaches were used, and we report that a single in vivo cocaine administration abolishes eCB-LTD. This effect of cocaine was not present in D₁ dopamine receptor (D₁R) -/- mice and was prevented when cocaine was coadministered with the selective D₁R antagonist 8-chloro-2,3,4,5-tetrahydro-3-5-1h-3-benzazepin-7-ol (0.5 mg/kg) or with the NMDA receptor (NMDAR) blocker (+)-5-methyl-10,11-dihydro-5H-dibenzo [a,d] cyclohepten-5,10-imine maleate (1 mg/kg), suggesting the involvement of D₁R and NMDAR. We found that the cocaine-induced blockade of retrograde signaling was correlated with enhanced expression levels of Homer scaffolding proteins containing the coiled-coil domain and accompanied by a strong reduction of mGluR5 surface expression. The results suggest that cocaine-induced loss of eCB retrograde signaling is caused by a reduction in the ability of mGluR5 to translate anterograde glutamate transmission into retrograde eCB signaling.

Key words: endocannabinoid; synaptic plasticity; long-term depression; drug abuse; accumbens; mGluR; CB1; D₁; NMDA; cocaine

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Received Feb 24, 2004; revised June 15, 2004; accepted June 15, 2004.

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