Skip to main content
SpringerLink
Log in

Cannabinoid CB1 receptors are involved in motivational effects of nicotine in rats

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

The endocannabinoid system plays a role in mediating the appetitive value of a variety of reinforcing compounds, either natural rewards or drugs of abuse, but little is known about its involvement in the incentive properties of nicotine.

Objectives

The objective of the study is to evaluate whether activation of CB1 cannabinoid receptors is necessary for the establishment and the short- and long-term expression of nicotine-induced conditioned place preference (CPP). This was studied in rats subjected to an unbiased, one-compartment place conditioning procedure, using the selective CB1 receptor antagonist, rimonabant, as a pharmacological tool.

Methods

Wistar rats, given previous experience with nicotine in their home cage, were subjected to eight alternating nicotine (0.006–0.6 mg/kg s.c.) and saline pairings with distinct floor textures in an open field and given a test session, with no nicotine injection, in the open field whose floor was covered by two quadrants of the saline-paired texture and two quadrants of the nicotine-paired texture. Rimonabant (0.3–3 mg/kg i.p.) was administered 30 min before each nicotine (0.06 mg/kg) pairing to assess its effect on the establishment of nicotine-CPP. To study the effects of CB1 receptor blockade on short- and long-term expression of nicotine-CPP, rimonabant was administered as a single injection 30 min before the test session, conducted either 24 h, 3 weeks or 12 weeks after the last conditioning session.

Results

Rats developed reliable and robust CPP to the 0.06- and 0.125-mg/kg doses of nicotine. Once established, CPP persisted for at least 12 weeks without additional exposure to nicotine and the test apparatus. Pre-pairing injections of rimonabant (3 mg/kg, but not lower doses) prevented the acquisition of nicotine-CPP, and a single pretest administration of rimonabant (3 mg/kg) abolished the expression of nicotine-CPP when the test session took place 24 h after the last conditioning session. However, rimonabant (3 mg/kg) did not antagonize the expression of nicotine-CPP when the test session was conducted 3 or 12 weeks after the acquisition phase.

Conclusions

The endocannabinoids are a necessary component in both the perception by rats of the motivational value of nicotine and the short-term capacity of nicotine-paired conditioned stimuli to elicit approach behaviour. In contrast, the acute blockade of CB1 receptors no longer impairs the long-term control of behaviour by nicotine-associated environmental cues. These data provide support to the notion that the blockade of CB1 receptors can oppose tobacco dependence, withdrawal and even relapse, though the time window of efficacy and/or the schedule of administration remain to be established.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alger BE (2002) Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol 68:247–286

    Article  PubMed  CAS  Google Scholar 

  • Arnold JC, Hunt GE, McGregor IS (2001) Effects of the cannabinoid receptor agonist CP 55,940 and the cannabinoid receptor antagonist SR 141716 on intracranial self-stimulation in Lewis rats. Life Sci 70:97–108

    Article  PubMed  CAS  Google Scholar 

  • Arnone M, Maruani J, Chaperon F, Thiébot MH, Poncelet M, Soubrié P, Le Fur G (1997) Selective inhibition of sucrose and ethanol intake by SR 141716, an antagonist of central cannabinoid (CB1) receptors. Psychopharmacology (Berl) 132:104–106

    Article  CAS  Google Scholar 

  • Balerio GN, Aso E, Berrendero F, Murtra P, Maldonado R (2004) Δ9-tetrahydrocannabinol decreases somatic and motivational manifestations of nicotine withdrawal in mice. Eur J Neurosci 20:2737–2748

    Article  PubMed  Google Scholar 

  • Balfour DJ (2002) Neuroplasticity within the mesoaccumbens dopamine system and its role in tobacco dependence. Curr Drug Targets CNS Neurol Disord 1:413–421

    Article  PubMed  CAS  Google Scholar 

  • Balfour DJ, Wright AE, Benwell ME, Birrell CE (2000) The putative role of extra-synaptic mesolimbic dopamine in the neurobiology of nicotine dependence. Behav Brain Res 113:73–83

    Article  PubMed  CAS  Google Scholar 

  • Barrett RJ, Caul WF, Stadler JR, Smith RL (2001) Long-lasting rebound cue effects following single doses of nicotine and amphetamine: implications for understanding tolerance. Psychopharmacology (Berl) 157:349–357

    Article  CAS  Google Scholar 

  • Bell SM, Stewart RB, Thompson SC, Meisch RA (1997) Food-deprivation increases cocaine-induced conditioned place preference and locomotor activity in rats. Psychopharmacology (Berl) 131:1–8

    Article  CAS  Google Scholar 

  • Belluzzi JD, Lee AG, Oliff HS, Leslie FM (2004) Age-dependent effects of nicotine on locomotor activity and conditioned place preference in rats. Psychopharmacology (Berl) 174:389–395

    Article  CAS  Google Scholar 

  • Braida D, Pozzi M, Parolaro D, Sala M (2001) Intracerebral self-administration of the cannabinoid receptor agonist CP 55,940 in the rat: interaction with the opioid system. Eur J Pharmacol 413:227–234

    Article  PubMed  CAS  Google Scholar 

  • Braida D, Iosuè S, Pegorini S, Sala M (2004) Δ9-Tetrahydrocannabinol-induced conditioned place preference and intracerebroventricular self-administration in rats. Eur J Pharmacol 506:63–69

    Article  PubMed  CAS  Google Scholar 

  • Caillé S, Parsons LH (2003) SR141716A reduces the reinforcing properties of heroin but not heroin-induced increases in nucleus accumbens dopamine in rats. Eur J Neurosci 18:3145–3149

    Article  PubMed  Google Scholar 

  • Carr KD (2002) Augmentation of drug reward by chronic food restriction: behavioral evidence and underlying mechanisms. Physiol Behav 76:353–364

    Article  PubMed  CAS  Google Scholar 

  • Carr GD, Fibiger HC, Phillips AG (1989) Conditioned place preference as a measure of drug reward. In: Liebman JM, Cooper SJ (eds) The neuropharmacological basis of reward. Clarendon Press, Oxford, pp 264–319

    Google Scholar 

  • Castañé A, Valjent E, Ledent C, Parmentier M, Maldonado R, Valverde O (2002) Lack of CB1 cannabinoid receptors modifies nicotine behavioural responses, but not nicotine abstinence. Neuropharmacology 43:857–867

    Article  PubMed  Google Scholar 

  • Chaperon F (1997) Etude du rôle des récepteurs dopaminergiques D3, neurotensinergiques NT1 et cannabinoïdes CB1 dans le contrôle des processus motivationnels chez le rat. Thèse de l'Université Pierre et Marie Curie (Paris VI): spécialité Neurosciences

  • Chaperon F, Thiébot MH (1999) Behavioral effects of cannabinoid agents in animals. Crit Rev Neurobiol 13:243–281

    PubMed  CAS  Google Scholar 

  • Chaperon F, Soubrié P, Puech AJ, Thiébot MH (1998) Involvement of central cannabinoid (CB1) receptors in the establishment of place conditioning in rats. Psychopharmacology (Berl) 135:324–332

    Article  CAS  Google Scholar 

  • Cheer JF, Kendall DA, Marsden CA (2000) Cannabinoid receptor and reward in the rat: a conditioned place preference study. Psychopharmacology (Berl) 151:25–30

    Article  CAS  Google Scholar 

  • Clarke PB, Fibiger HC (1987) Apparent absence of nicotine-induced conditioned place preference in rats. Psychopharmacology (Berl) 92:84–88

    Article  CAS  Google Scholar 

  • Cohen C, Perrault G, Voltz C, Steinberg R, Soubrié P (2002) SR141716, a central cannabinoid (CB1) receptor antagonist, blocks the motivational and dopamine-releasing effects of nicotine in rats. Behav Pharmacol 13:451–463

    PubMed  CAS  Google Scholar 

  • Cohen C, Perrault G, Griebel G, Soubrié P (2005) Nicotine-associated cues maintain nicotine-seeking behavior in rats several weeks after nicotine withdrawal: reversal by the cannabinoid (CB1) receptor antagonist, rimonabant (SR141716). Neuropsychopharmacology 30:145–155

    Article  PubMed  CAS  Google Scholar 

  • Colombo G, Vacca G, Serra S, Carai M, Gessa G (2004) Suppressing effects of the CB1 receptor antagonist, SR 141716, on alcohol's motivational properties in alcohol-preferring rats. Eur J Pharmacol 498:119–123

    Article  PubMed  CAS  Google Scholar 

  • Cossu G, Ledent C, Fattore L, Imperato A, Böhme GA, Parmentier M, Fratta W (2001) Cannabinoid CB1 receptor knockout mice fail to self-administer morphine but not other drugs of abuse. Behav Brain Res 118:61–65

    Article  PubMed  CAS  Google Scholar 

  • Dale L, Anthenelli R, Despres JP, Golay A, Sjostrom L (2004) Effects of rimonabant in the reduction of major cardiovascular risk factors: results from the STRATUS-US trial (smoking cessation in smokers motivated to quit) and the RIO-LIPIDS trial (weight reducing and metabolic effects in overweight/obese patients with dyslipidemia) American College of Cardiology, New Orleans; Presentation 409-1 <http://en.sanofi-synthelabo.com/press/ppc_23312.asp?ComponentID=23312&SourcePageID=23126>

  • Dewey SL, Brodie JD, Gerasimov M, Horan B, Gardner EL, Ashby CR Jr (1999) A pharmacologic strategy for the treatment of nicotine addiction. Synapse 31:76–86

    Article  PubMed  CAS  Google Scholar 

  • De Vries TJ, Shaham Y, Homberg JR, Crombag H, Schuurman K, Dieben J, Vanderschuren LJ, Schoffelmeer AN (2001) A cannabinoid mechanism in relapse to cocaine seeking. Nat Med 7:1151–1154

    Article  PubMed  CAS  Google Scholar 

  • Di Chiara G (1999) Drug addiction as dopamine-dependent associative learning disorder. Eur J Pharmacol 375:13–30

    Article  PubMed  Google Scholar 

  • Di Chiara G (2000) Role of dopamine in the behavioural actions of nicotine related to addiction. Eur J Pharmacol 393:295–314

    Article  PubMed  Google Scholar 

  • Di Chiara G, Tanda G, Bassareo V, Pontieri F, Acquas E, Fenu S, Cadoni C, Carboni E (1999) Drug addiction as a disorder of associative learning. Role of nucleus accumbens shell/extended amygdala dopamine. Ann N Y Acad Sci 877:461–485

    Article  PubMed  Google Scholar 

  • Domino EF (2001) Nicotine induced behavioral locomotor sensitization. Prog Neuropsychopharmacol Biol Psychiatry 25:59–71

    Article  PubMed  CAS  Google Scholar 

  • Duarte C, Lefebvre C, Chaperon F, Hamon M, Thiébot MH (2003) Effects of a dopamine D3 receptor ligand, BP 897, on acquisition and expression of food-, morphine-, and cocaine-induced conditioned place preference, and food-seeking behavior in rats. Neuropsychopharmacology 28:1903–1915

    PubMed  CAS  Google Scholar 

  • Fattore L, Martellotta MC, Cossu G, Mascia MS, Fratta W (1999) CB1 cannabinoid receptor agonist WIN 55,212-2 decreases intravenous cocaine self-administration in rats. Behav Brain Res 104:141–146

    Article  PubMed  CAS  Google Scholar 

  • Fattore L, Spano MS, Cossu G, Deiana S, Fratta W (2003) Cannabinoid mechanism in reinstatement of heroin-seeking after a long period of abstinence in rats. Eur J Neurosci 17:1723–1726

    Article  PubMed  CAS  Google Scholar 

  • Fratta W, Martellotta MC, Cossu G, Fattore L (1998) Self-administration of the cannabinoid agonist WIN 55212-2 and morphine in mice: evidence for a common neurobiological mechanism. Eur Neuropsychopharmacol 8(Suppl 1):S41–S42

    Google Scholar 

  • Freedland CS, Sharpe AL, Samson HH, Porrino LJ (2001) Effects of SR141716A on ethanol and sucrose self-administration. Alcohol Clin Exp Res 25:277–282

    Article  PubMed  CAS  Google Scholar 

  • Fudala PJ, Iwamoto ET (1986) Further studies on nicotine-induced conditioned place preference in the rat. Pharmacol Biochem Behav 25:1041–1049

    Article  PubMed  CAS  Google Scholar 

  • Fudala PJ, Teoh KW, Iwamoto ET (1985) Pharmacologic characterization of nicotine-induced conditioned place preference. Pharmacol Biochem Behav 22:237–241

    Article  PubMed  CAS  Google Scholar 

  • Gallate JE, McGregor IS (1999) The motivation for beer in rats: effects of ritanserin, naloxone and SR 141716. Psychopharmacology (Berl) 142:302–308

    Article  CAS  Google Scholar 

  • Gallate JE, Saharov T, Mallet PE, McGregor IS (1999) Increased motivation for beer in rats following administration of a cannabinoid CB1 receptor agonist. Eur J Pharmacol 370:233–240

    Article  PubMed  CAS  Google Scholar 

  • Guyon A, Assouly-Besse F, Biala G, Puech AJ, Thiébot MH (1993) Potentiation by low doses of selected neuroleptics of food-induced conditioned place preference in rats. Psychopharmacology (Berl) 110:460–466

    Article  CAS  Google Scholar 

  • Herberg LJ, Montgomery AM, Rose IC (1993) Tolerance and sensitization to stimulant and depressant effects of nicotine in intracranial self-stimulation in the rat. Behav Pharmacol 4:419–427

    Article  PubMed  CAS  Google Scholar 

  • Higgs S, Williams CM, Kirkham TC (2003) Cannabinoid influences on palatability: microstructural analysis of sucrose drinking after delta9-tetrahydrocannabinol, anandamide, 2-arachidonoyl glycerol and SR141716. Psychopharmacology (Berl) 165:370–377

    CAS  Google Scholar 

  • Horan B, Smith M, Gardner EL, Lepore M, Ashby CR Jr (1997) (−)-Nicotine produces conditioned place preference in Lewis, but not Fischer 344 rats. Synapse 26:93–94

    Article  PubMed  CAS  Google Scholar 

  • Hungund BL, Szakall I, Adam A, Basavarajappa BS, Vadasz C (2003) Cannabinoid CB1 receptor knockout mice exhibit markedly reduced voluntary alcohol consumption and lack alcohol-induced dopamine release in the nucleus accumbens. J Neurochem 84:698–704

    Article  PubMed  CAS  Google Scholar 

  • Hyland BI, Reynolds JN, Hay J, Perk CG, Miller R (2002) Firing modes of midbrain dopamine cells in the freely moving rat. Neuroscience 114:475–492

    Article  PubMed  CAS  Google Scholar 

  • Ito R, Dalley JW, Howes SR, Robbins TW, Everitt BJ (2000) Dissociation in conditioned dopamine release in the nucleus accumbens core and shell in response to cocaine cues and during cocaine-seeking behavior in rats. J Neurosci 20:7489–7495

    PubMed  CAS  Google Scholar 

  • Iyaniwura TT, Wright AE, Balfour DJ (2001) Evidence that mesoaccumbens dopamine and locomotor responses to nicotine in the rat are influenced by pretreatment dose and strain. Psychopharmacology (Berl) 158:73–79

    Article  CAS  Google Scholar 

  • Jorenby DE, Steinpreis RE, Sherman JE, Baker TB (1990) Aversion instead of preference learning indicated by nicotine place conditioning in rats. Psychopharmacology (Berl) 101:533–538

    Article  CAS  Google Scholar 

  • Kirkham TC, Williams CM (2001) Endogenous cannabinoids and appetite. Nutr Res Rev 14:65–86

    Article  CAS  PubMed  Google Scholar 

  • Ksir C (1994) Acute and chronic nicotine effects on measures of activity in rats: a multivariate analysis. Psychopharmacology (Berl) 115:105–109

    Article  CAS  Google Scholar 

  • Laviolette SR, van der Kooy D (2004) The neurobiology of nicotine addiction: bridging the gap from molecules to behaviour. Nat Rev Neurosci 5:55–65

    Article  PubMed  CAS  Google Scholar 

  • Ledent C, Valverde O, Cossu G, Petitet F, Aubert JF, Beslot F, Böhme GA, Imperato A, Fratta W, Parmentier M (1999) Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 283:401–404

    Article  PubMed  CAS  Google Scholar 

  • Lepore M, Liu X, Savage V, Matalon D, Gardner EL (1996) Genetic differences in delta 9-tetrahydrocannabinol-induced facilitation of brain stimulation reward as measured by a rate-frequency curve-shift electrical brain stimulation paradigm in three different rat strains. Life Sci 58:PL365–PL372

    Article  PubMed  CAS  Google Scholar 

  • Le Foll B, Goldberg S (2004) Rimonabant, a CB1 antagonist, blocks nicotine-conditioned place preferences. NeuroReport 15:2139–2143

    Article  PubMed  Google Scholar 

  • Lichtman AH (2000) SR141716A enhances spatial memory as assessed in a radial-maze task in rats. Eur J Pharmacol 404:175–179

    Article  PubMed  CAS  Google Scholar 

  • Mansvelder HD, McGehee DS (2002) Cellular and synaptic mechanisms of nicotine addiction. J Neurobiol 53:606–617

    Article  PubMed  CAS  Google Scholar 

  • Martin M, Ledent C, Parmentier M, Maldonado R, Valverde O (2000) Cocaine, but not morphine, induces conditioned place preference and sensitization to locomotor responses in CB1 knockout mice. Eur J Neurosci 12:4038–4046

    Article  PubMed  CAS  Google Scholar 

  • Mas-Nieto M, Pommier B, Tzavara ET, Caneparo A, Da Nascimento S, Le Fur G, Roques BP, Noble F (2001) Reduction of opioid dependence by the CB1 antagonist SR141716A in mice: evaluation of the interest in pharmacotherapy of opioid addiction. Br J Pharmacol 132:1809–1816

    Article  PubMed  CAS  Google Scholar 

  • Mueller D, Stewart J (2000) Cocaine-induced conditioned place preference: reinstatement by priming injections of cocaine after extinction. Behav Brain Res 115:39–47

    Article  PubMed  CAS  Google Scholar 

  • Mueller D, Perdikaris D, Stewart J (2002) Persistence and drug-induced reinstatement of a morphine-induced conditioned place preference. Behav Brain Res 136:389–397

    Article  PubMed  CAS  Google Scholar 

  • Navarro M, Carrera MR, Fratta W, Valverde O, Cossu G, Fattore L, Chowen JA, Gomez R, del Arco I, Villanua MA, Maldonado R, Koob GF, Rodríguez de Fonseca F (2001) Functional interaction between opioid and cannabinoid receptors in drug self-administration. J Neurosci 21:5344–5350

    PubMed  CAS  Google Scholar 

  • Olausson P, Jentsch JD, Taylor JR (2003) Repeated nicotine exposure enhances reward-related learning in the rat. Neuropsychopharmacology 28:1264–1271

    Article  PubMed  CAS  Google Scholar 

  • Parker LA (1992) Place conditioning in a three- or four-choice apparatus: role of stimulus novelty in drug-induced place conditioning. Behav Neurosci 106:294–306

    Article  PubMed  CAS  Google Scholar 

  • Pertwee RG (1999) Pharmacology of cannabinoid receptor ligands. Curr Med Chem 6:635–664

    PubMed  CAS  Google Scholar 

  • Philibin SD, Vann RE, Varvel SA, Covington HE 3rd, Rosecrans JA, James JR, Robinson SE (2005) Differential behavioral responses to nicotine in Lewis and Fischer-344 rats. Pharmacol Biochem Behav 80:87–92

    Article  PubMed  CAS  Google Scholar 

  • Phillips PE, Stuber GD, Heien ML, Wightman RM, Carelli RM (2003) Subsecond dopamine release promotes cocaine seeking. Nature 422:614–618

    Article  PubMed  CAS  Google Scholar 

  • Poncelet M, Maruani J, Calassi R, Soubrié P (2003) Overeating, alcohol and sucrose consumption decrease in CB1 receptor deleted mice. Neurosci Lett 343:216–218

    PubMed  CAS  Google Scholar 

  • Pontieri FE, Tanda G, Orzi F, Di Chiara G (1996) Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature 382:255–257

    Article  PubMed  CAS  Google Scholar 

  • Pothos EN, Creese I, Hoebel BG (1995) Restricted eating with weight loss selectively decreases extracellular dopamine in the nucleus accumbens and alters dopamine response to amphetamine, morphine, and food intake. J Neurosci 15:6640–6650

    PubMed  CAS  Google Scholar 

  • Rice ME, Cragg SJ (2004) Nicotine amplifies reward-related dopamine signals in striatum. Nat Neurosci 7:583–584

    Article  PubMed  CAS  Google Scholar 

  • Rinaldi-Carmona M, Barth F, Héaulme M, Alonso R, Shire D, Congy C, Soubrié P, Brelière JC, Le Fur G (1995) Biochemical and pharmacological characterization of SR 141716A, the first potent and selective brain cannabinoid receptor antagonist. Life Sci 56:1941–1947

    Article  PubMed  CAS  Google Scholar 

  • Risinger FO, Oakes RA (1995) Nicotine-induced conditioned place preference and conditioned place aversion in mice. Pharmacol Biochem Behav 51:457–461

    Article  PubMed  CAS  Google Scholar 

  • Rogers DT, Barron S, Littleton JM (2004) Neonatal ethanol exposure produces a hyperalgesia that extends into adolescence, and is associated with increased analgesic and rewarding properties of nicotine in rats. Psychopharmacology (Berl) 171:204–211

    Article  CAS  Google Scholar 

  • Sanchis-Segura C, Cline BH, Marsicano G, Lutz B, Spanagel R (2004) Reduced sensitivity to reward in CB1 knockout mice. Psychopharmacology (Berl) 176:223–232

    Article  CAS  Google Scholar 

  • Sañudo-Peña MC, Tsou K, Delay ER, Hohman AG, Force M, Walker JM (1997) Endogenous cannabinoids as an aversive or counter-rewarding system in the rat. Neurosci Lett 223:125–128

    Article  PubMed  Google Scholar 

  • Schaefer GJ, Michael RP (1986) Task-specific effects of nicotine in rats. Intracranial self-stimulation and locomotor activity. Neuropharmacology 25:125–131

    Article  PubMed  CAS  Google Scholar 

  • Schultz W (2002) Getting formal with dopamine and reward. Neuron 36:241–263

    Article  PubMed  CAS  Google Scholar 

  • Serra S, Carai MA, Brunetti G, Gomez R, Melis S, Vacca G, Colombo G, Gessa GL (2001) The cannabinoid receptor antagonist SR 141716 prevents acquisition of drinking behavior in alcohol-preferring rats. Eur J Pharmacol 430:369–371

    Article  PubMed  CAS  Google Scholar 

  • Serra S, Brunetti G, Pani M, Vacca G, Carai MA, Gessa GL, Colombo G (2002) Blockade by the cannabinoid CB1 receptor antagonist, SR 141716, of alcohol deprivation effect in alcohol-preferring rats. Eur J Pharmacol 443:95–97

    Article  PubMed  CAS  Google Scholar 

  • Shaham Y, Adamson LK, Grocki S, Corrigall WA (1997) Reinstatement and spontaneous recovery of nicotine seeking in rats. Psychopharmacology (Berl) 130:396–403

    Article  CAS  Google Scholar 

  • Shoaib M, Stolerman IP, Kumar RC (1994) Nicotine-induced place preferences following prior nicotine exposure in rats. Psychopharmacology (Berl) 113:445–452

    Article  CAS  Google Scholar 

  • Shoaib M, Gommans J, Morley A, Stolerman IP, Grailhe R, Changeux JP (2002) The role of nicotinic receptor beta-2 subunits in nicotine discrimination and conditioned taste aversion. Neuropharmacology 42:530–539

    Article  PubMed  CAS  Google Scholar 

  • Solinas M, Panlilio LV, Antoniou K, Pappas LA, Goldberg SR (2003) The cannabinoid CB1 antagonist N-piperidinyl-5-(4-chlorophenyl)-1-(2,4-dichlorophenyl)-4-methylpyrazole-3-carboxamide (SR-141716A) differentially alters the reinforcing effects of heroin under continuous reinforcement, fixed ratio, and progressive ratio schedules of drug self-administration in rats. J Pharmacol Exp Ther 306:93–102

    Article  PubMed  CAS  Google Scholar 

  • Spanagel R, Weiss F (1999) The dopamine hypothesis of reward: past and current status. Trends Neurosci 22:521–527

    Article  PubMed  CAS  Google Scholar 

  • Stolerman IP (1999) Inter-species consistency in the behavioural pharmacology of nicotine dependence. Behav Pharmacol 10:559–580

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Ise Y, Tsuda M, Maeda J, Misawa M (1996) Mecamylamine-precipitated nicotine-withdrawal aversion in rats. Eur J Pharmacol 314:281–284

    Article  PubMed  CAS  Google Scholar 

  • Tanda G, Goldberg SR (2003) Cannabinoids: reward, dependence, and underlying neurochemical mechanisms—a review of recent preclinical data. Psychopharmacology (Berl) 169: 115–134

    Article  CAS  Google Scholar 

  • Tanda G, Pontieri FE, Di Chiara G (1997) Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common μ1 opioid receptor mechanism. Science 276:2048–2050

    Article  PubMed  CAS  Google Scholar 

  • Tanda G, Munzar P, Goldberg SR (2000) Self-administration behavior is maintained by the psychoactive ingredient of marijuana in squirrel monkeys. Nat Neurosci 3:1073–1074

    Article  PubMed  CAS  Google Scholar 

  • Terranova J-P, Storme J-J, Lafon N, Pério A, Rinaldi-Carmona M, Le Fur G, Soubrié P (1996) Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716. Psychopharmacology (Berl) 126:165–172

    Article  CAS  Google Scholar 

  • Vastola BJ, Douglas LA, Varlinskaya EI, Spear LP (2002) Nicotine-induced conditioned place preference in adolescent and adult rats. Physiol Behav 77:107–114

    Article  PubMed  CAS  Google Scholar 

  • Verty AN, McGregor IS, Mallet PE (2004) Consumption of high carbohydrate, high fat, and normal chow is equally suppressed by a cannabinoid receptor antagonist in non-deprived rats. Neurosci Lett 354:217–220

    Article  PubMed  CAS  Google Scholar 

  • Villégier AS, Blanc G, Glowinski J, Tassin JP (2003) Transient behavioral sensitization to nicotine becomes long-lasting with monoamine oxidases inhibitors. Pharmacol Biochem Behav 76:267–274

    Article  PubMed  CAS  Google Scholar 

  • Vinklerová J, Nováková J, Sulcová A (2002) Inhibition of methamphetamine self-administration in rats by cannabinoid receptor antagonist AM 251. J Psychopharmacol 16:139–143

    Article  PubMed  Google Scholar 

  • Vlachou S, Nomikos GG, Panagis G (2003) WIN 55,212-2 decreases the reinforcing actions of cocaine through CB1 cannabinoid receptor stimulation. Behav Brain Res 141:215–222

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Liu J, Harvey-White J, Zimmer A, Kunos G (2003) Endocannabinoid signaling via cannabinoid receptor 1 is involved in ethanol preference and its age-dependent decline in mice. Proc Natl Acad Sci U S A 100:1393–1398

    Article  PubMed  CAS  Google Scholar 

  • Zarrindast MR, Faraji N, Rostami P, Sahraei H, Ghoshouni H (2003) Cross-tolerance between morphine- and nicotine-induced conditioned place preference in mice. Pharmacol Biochem Behav 74:363–369

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Sulzer D (2004) Frequency-dependent modulation of dopamine release by nicotine. Nat Neurosci 7:581–582

    Article  PubMed  CAS  Google Scholar 

  • Zimmer A, Zimmer AM, Hohmann AG, Herkenham M, Bonner TI (1999) Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc Natl Acad Sci U S A 96:5780–5785

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This study has been supported by grants from INSERM, MILDT (AO MILDT-Inserm 2001), LSHM-CT-2003-503474 CEE contract "New Mood" and Sanofi-Aventis. Benoît Forget was the recipient of a grant from the “Société de Tabacologie.” We are grateful to Sanofi-Aventis for the gift of rimonabant. The authors would like to thank warmly Dr. Hans C. Neijt (Novartis Pharma, Basel, Switzerland) for the generous gift of the SuperG Software for image analysis. We gratefully acknowledge Dr. Philippe Soubrié for helpful comments on the manuscript.

Author information

Authors and Affiliations

  1. INSERM U.677 (ex. U.288), Faculté de Médecine Pitié-Salpêtrière, 91 Boulevard de l'Hôpital, 75634, Paris Cedex 13, France

    Benoît Forget, Michel Hamon & Marie-Hélène Thiébot

Authors
  1. Benoît Forget
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michel Hamon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marie-Hélène Thiébot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marie-Hélène Thiébot.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Forget, B., Hamon, M. & Thiébot, MH. Cannabinoid CB1 receptors are involved in motivational effects of nicotine in rats. Psychopharmacology 181, 722–734 (2005). https://doi.org/10.1007/s00213-005-0015-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-005-0015-6

Keywords

Search

Navigation