Cannabinoid CB1 receptor antagonist AM251 inhibits cocaine-primed relapse in rats: role of glutamate in the nucleus accumbens - PubMed (original) (raw)
Cannabinoid CB1 receptor antagonist AM251 inhibits cocaine-primed relapse in rats: role of glutamate in the nucleus accumbens
Zheng-Xiong Xi et al. J Neurosci. 2006.
Abstract
Blockade of cannabinoid CB1 receptors has been reported to inhibit cocaine- or cocaine cue-induced reinstatement of drug seeking. However, the mechanisms underlying this action are poorly understood. Given the importance of dopamine, glutamate, and GABA in cocaine reward and relapse, we studied the effects of AM251 [N-(piperidin-1-yl)-5-(4-iodophonyl)-1-(2,4-dichlorophenyl)-4-methyl-1H-pyrazole-3-carboxamide], a novel highly selective CB1 receptor antagonist, on cocaine-primed reinstatement of drug-seeking behavior and on cocaine-induced changes in extracellular DA, glutamate, and GABA in the nucleus accumbens (NAc) under reinstatement conditions. We found that systemic administration of AM251 selectively inhibited cocaine-induced, but not sucrose plus sucrose cue-induced, reinstatement of reward-seeking behavior. AM251 alone did not trigger reinstatement. Local perfusion of AM251 into the NAc or the dorsal striatum also inhibited cocaine-triggered reinstatement. AM251 alone dose dependently elevated NAc glutamate in a voltage-dependent Na+ channel-dependent manner. AM251 did not affect NAc DA or GABA. Pretreatment with AM251 dose dependently inhibited cocaine-induced increases in NAc glutamate but not in DA. Blockade of NAc metabotropic glutamate mGluR2/3 receptors by LY341495 [(2S)-2-amino-2-[(1S,2S)-2-carboxycycloprop-1-yl]-3-(xanth-9-yl) propanoic acid] slightly facilitated cocaine-enhanced glutamate release but blocked the antagonism of cocaine-induced reinstatement by AM251. These data suggest the following: (1) CB1 receptors exert tonic inhibition over NAc glutamate release under cocaine-extinction conditions; (2) blockade of CB1 receptors by AM251 inhibits cocaine-enhanced NAc glutamate release and cocaine-triggered reinstatement; and (3) these effects appear to be mediated by activation of presynaptic mGluR2/3 autoreceptors secondary to AM251-induced increase (disinhibition) of NAc glutamate release.
Figures
Figure 1.
Effects of AM251 on cocaine-primed reinstatement. Systemic administration of AM251 (1, 3, and 10 mg/kg, i.p.) dose-dependently inhibited cocaine-primed relapse (a) but not sucrose plus cue-induced relapse to sucrose-seeking behavior (b). AM251 alone failed to reinstate cocaine-seeking behavior (c). Microinjection of AM251 (5 and 10 μg/1 μl) into the NAc (d) or the dorsal striatum (D. Str.; e) inhibited cocaine-primed relapse. Microinjection of LY341495 (LY) (0.2 μg/1 μl) into the NAc failed to inhibit cocaine-primed relapse but attenuated the antagonism of cocaine-triggered relapse by AM251 (f). *p < 0.05, **p < 0.01 compared with the vehicle group.
Figure 2.
Effect of AM251 pretreatment on cocaine-induced increase in extracellular NAc DA. a, b, AM251 alone had no effect on NAc DA. c, d, AM251 (1–10 mg/kg, i.p.) did not alter cocaine priming-induced increases in NAc DA. ***p < 0.001 compared with pre-cocaine baseline. NS, Not statistically significant.
Figure 3.
Effect of AM251 pretreatment on cocaine-induced increase in extracellular NAc glutamate. a, b, AM251 alone significantly augmented NAc glutamate. Intra-NAc perfusion of TTX prevented 10 mg/kg AM251-induced increases in NAc glutamate. c, d, AM251 (1–10 mg/kg, i.p.) dose-dependently blocked cocaine-induced increases in NAc glutamate. e, f, Intra-NAc microinjection of LY341495 (mGluR2/3 antagonist) slightly facilitated or prolonged cocaine-enhanced NAc extracellular glutamate. *p < 0.01 compared with pre-cocaine baseline.
Figure 4.
Effect of AM251 pretreatment on the effects of cocaine on extracellular NAc GABA. a, b, AM251 alone failed to alter extracellular NAc GABA. c, d, Neither cocaine priming nor cocaine in combination with AM251 significantly altered NAc GABA. e, AM251 microinjection loci in the NAc and the dorsal striatum. f, Microdialysis probe placement in the NAc. NS, Not statistically significant.
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References
- Anderson SM, Bari AA, Pierce RC (2003). Administration of the D1-like dopamine receptor antagonist SCH-23390 into the medial nucleus accumbens shell attenuates cocaine priming-induced reinstatement of drug-seeking behavior in rats. Psychopharmacology 168:132–138. - PubMed
- Anderson SM, Schmidt HD, Pierce RC (2006). Administration of the D2 dopamine receptor antagonist sulpiride into the shell, but not the core, of the nucleus accumbens attenuates cocaine priming-induced reinstatement of drug-seeking. Neuropsychopharmacology 31:1452–1461. - PubMed
- Anggadiredja K, Nakamichi M, Hiranita T, Tanaka H, Shoyama Y, Watanabe S, Yamamoto T (2004). Endocannabinoid system modulates relapse to methamphetamine seeking: possible mediation by the arachidonic acid cascade. Neuropsychopharmacology 29:1470–1478. - PubMed
- Bachtell RK, Whisler K, Karanian D, Self DW (2005). Effects of intra-nucleus accumbens shell administration of dopamine agonists and antagonists on cocaine-taking and cocaine-seeking behaviors in the rat. Psychopharmacology 183:41–53. - PubMed
- Baker DA, McFarland K, Lake RW, Shen H, Tang XC, Toda S, Kalivas PW (2003). Neuroadaptations in cystine-glutamate exchange underlie cocaine relapse. Nat Neurosci 6:743–749. - PubMed
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