Psychopharmacology

, Volume 110, Issue 4, pp 460–466 | Cite as

Potentiation by low doses of selected neuroleptics of food-induced conditioned place preference in rats

  • Alice Guyon
  • Françoise Assouly-Besse
  • Grazyna Biala
  • Alain J. Puech
  • Marie-Hélène Thiébot
Original Investigations

Abstract

Numerous data support the hypothesis that dopamine (DA) plays a crucial role in reward-related processes and in incentive learning in animals and man. The possibility that various neuroleptics exhibiting a high affinity for the dopaminergic D2 (and D3) receptors could reinforce DA transmission was studied using the conditioned place preference paradigm (CPP) in rats. This was done by examining the ability of these compounds to potentiate the reinforcing properties of food in hungry rats subjected to a version of the CPP paradigm which consisted of repeated pairings of food with a single environmental cue, the floor texture of an open field. During the test session when food was no longer available in the open field, the increase in the time spent by drug-free rats on the food-paired texture was assumed to indicate the perceived rewarding value of the food. This time was significantly lengthened when the specific D2 (D3)-receptor antagonists sulpiride (4 mg/kg), amisulpride (0.5, 1 mg/kg) or pimozide (0.03, 0.06 mg/kg) were administered before the food conditioning sessions. Larger doses of these compounds as well as haloperidol, metoclopramide and the non-specific D1-D2 antagonist, chlorpromazine, regardless of the doses tested, did not exhibit this effect, but rather reduced the food-induced CPP, an action usually associated with neuroleptics. The positive effects of amisulpride was reversed by a D1 receptor antagonist, SCH 23390 (0.01 mg/kg). These results suggest that, as with amphetamine (0.5 mg/kg), some D2-specific neuroleptics enhance the incentive value of food in a narrow range of low doses, an effect proposed to reflect a “prohedonic” property. The potentiation of the release of DA unconditionally evoked by food, through a selective blockade of the release-modulating D2-autoreceptors, could constitute the neurobiological substratum of this effect. A concomitant blockade of either D2 or D1 postsynaptic receptors, however, appeared to be sufficient to counteract such activity.

Key words

Conditioned place preference Hedonia Food Dopamine Neuroleptics Autoreceptors Incentive learning Rat 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Acquas E, Carboni E, Leone P, Di Chiara G (1989) SCH 23390 blocks drug-conditioned place-preference and place-aversion: anhedonia (lack of reward) or apathy (lack of motivation) after dopamine-receptor blockade? Psychopharmacology 99:151–155Google Scholar
  2. Ahlenius S (1992) Effects of the local application of 3-PPP and sulpiride enantiomers into the nucleus accumbens or into the ventral tegmental area on rat locomotor activity: evidence for the functional importance of somato-dendritic autoreceptors. Naunyn Schmiedebergs Arch Pharmacol 345:516–522Google Scholar
  3. Beninger RJ (1991) Receptor subtype-specific dopamine agonists and antagonists and conditioned behaviour. In: Willner P, Scheel Krüger J (eds) The mesolimbic dopamine system: from motivation to action, Wiley, Chichester, pp 273–299Google Scholar
  4. Beninger RJ, Freedman NL (1982) The use of two operants to examine the nature of pimozide-induced decreases in responding for brain stimulation. Physiol Psychol 10:409–412Google Scholar
  5. Brown F, Campbell W, Mitchell PJ, Randall K (1985) Dopamine autoreceptors and the effects of drugs on locomotion and dopamine synthesis. Br J Pharmacol 84:853–860Google Scholar
  6. Bull DR, Sheehan MJ (1991) Presynaptic regulation of electrically evoked dopamine overflow in the nucleus accumbens: a pharmacological study using fast cyclic voltametry in vivo. Naunyn Schmiedebergs Arch Pharmacol 343:260–265Google Scholar
  7. Cabib S, Castellano C, Cestari V, Filibeck U, Puglisi-Allegra S (1991) D1 and D2 receptor antagonists differently affect cocaine-induced locomotor hyperactivity in the mouse. Psychopharmacology 105:335–339Google Scholar
  8. Cador M, Robbins TW, Everitt BJ (1989) Involvement of the amygdala in stimulus-reward associations: interaction with the ventral striatum. Neuroscience 30:77–86Google Scholar
  9. Carr GD, Phillips AG, Fibiger HC (1988) Independence of amphetamine reward from locomotor stimulation demonstrated by conditioned place preference. Psychopharmacology 94:221–226Google Scholar
  10. 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. Oxford University Press, Oxford, pp 264–319Google Scholar
  11. Carnoy P, Ravard S, Hervé D. Tassin JP, Soubrié P (1987) Apomorphine induced operant deficits: a neuroleptic-sensitive but drug and dose-dependent animal model of behavior. Psychiatrie & Psychobiologie II [4]:266–273Google Scholar
  12. Clark D, White FJ (1987) Review: D1 dopamine receptor-the search for a function: a critical evaluation of the D1-D2 dopamine receptor classification and its functional implications. Synapse 1:347–388Google Scholar
  13. Costall B, Lim SK, Naylor RJ (1981) Characterisation of the mechanism by which purported dopamine agonists reduce spontaneous locomotor activity of mice. Eur J Pharmacol 73:175–188Google Scholar
  14. Di Scala G, Sandner G (1989) Conditioned place aversion produced by FG 7142 is attenuated by haloperidol. Psychopharmacology 99:176–180Google Scholar
  15. Hernandez L, Hœbel BG (1988) Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sci 42:1705–1712Google Scholar
  16. Hill RT (1970) Facilitation of conditioned reinforcement as a mechanism of psychomotor stimulation. In: Costa E, Garattini S (eds) Amphetamines and related compounds. Raven Press, New York, pp 781–795Google Scholar
  17. Hiroi N, White NM (1991) The amphetamine conditioned place preference: differential involvement of dopamine receptor subtypes and two dopaminergic terminal areas. Brain Res 552:141–152Google Scholar
  18. Hoffman DC, Beninger RJ (1989) The effects of selective dopamine D1 or D2 receptor antagonists on the establishment of agonist-induced place conditioning in rats. Pharmacol Biochem Behav 33:273–279Google Scholar
  19. Imperato A, Di Chiara G (1988) Effects of locally applied D-1 and D-2 receptor agonists and antagonists studied with brain dialysis. Eur J Pharmacol 156:385–393Google Scholar
  20. Jenner P, Marsden CD (1982) The mode of action of sulpiride as an atypical antidepressant agent. In: Costa E, Racagni G (eds) Typical and atypical antidepressants: clinical practice. Raven Press, New York, pp 85–103Google Scholar
  21. Katz JL (1989) Drugs as reinforcers: pharmacological and behavioral factors. In: Liebman JM, Cooper SJ (eds) The neuropharmacological basis of reward. Oxford University Press, Oxford, pp 164–213Google Scholar
  22. Koob GF, Goeders NE (1989) Neuroanatomical substrates of drug self administration. In: Liebman JM, Cooper SJ (eds) The neuropharmacological basis of reward. Oxford University Press, Oxford, pp 214–263Google Scholar
  23. Kullingsjö H, Carlsson A, Svenson K (1991) Effects of repeated administration of the preferential dopamine autoreceptor antagonist, (+)-AJ76, on locomotor activity and brain DA metabolism in the rat. Eur J Pharmacol 205:241–246Google Scholar
  24. Lecrubier Y, Puech AJ, Aubin F, Boyer P, Deyrieux B (1988) Improvement by amisulpride of the negative symptoms in nonpsychotic subjects: a preliminary study. Psychiatrie & Psychobiologie 3:341–350Google Scholar
  25. Lynch MR (1991) Dissociation of autoreceptor activation and behavioural consequences of low dose apomorphine treatment. Prog Neuropsychopharmacol Biol Psychiatry 15:689–698Google Scholar
  26. Mackey WB, van der Kooy D (1985) Neuroleptics block the positive reinforcing effects of amphetamine but not of morphine as measured by place conditioning. Pharmacol Biochem Behav 22:101–105Google Scholar
  27. Maubrey MC, Jacquot C, Godinec J, Guez M, Idée JM, Margarit J (1989) Amisulpride: pharmacological profiles. In: Borenstein P, Boyer P, Braconnier P et al (eds) Amisulpride. Expansion Scientifique Française, Paris, pp 3–24Google Scholar
  28. Mindham RHS, Jerram TC, Cole HL, Oswald AG, Khan S (1991) A comparison of sulpiride, dothiepin, diazepam and placebo in the treatment of depressed out-patients. J Psychopharmacol 5:259–262Google Scholar
  29. Moghaddam B, Bunney BS (1990) Acute effects of typical and atypical antipsychotic drugs on the release of dopamine from prefrontal cortex, nucleus accumbens, and striatum of the rat: an in vivo microdialysis study. J Neurochem 54:1755–1760Google Scholar
  30. Petit M, Zann M, Colonna L (1984) Etude contrôlée de l'effet désinhibiteur de faibles doses de sulpiride dans les psychoses schizophréniques déficitaires. Encéphale X:25–28Google Scholar
  31. Phillips AG, Pfaus JG, Blaha CD (1991) Dopamine and motivated behavior: insights provided by in vivo analyses. In: Willner P, Scheel-Krüger J (eds) The mesolimbic dopamine system: from motivation to action. Wiley, Chichester, pp 199–224Google Scholar
  32. Puech AJ, Rioux P, Poncelet M, Brochet D, Chermat R, Simon P (1981) Pharmacological properties of new antipsychotic agents: use of animal models. Neuropharmacology 20:1279–1284Google Scholar
  33. Puglisi-Allegra S, Cabib S (1988) The dopamine D2 agonists induces catalepsy in the mouse. Pharmacol Biochem Behav 30:765–768Google Scholar
  34. Robbins TW (1978) The acquisition of responding with conditioned reinforcement: effects of pipradrol, methylphenidate,d-amphetamine, and nomifensine. Psychopharmacology 58:79–87Google Scholar
  35. Robertson A, McDonald C (1985) Opposite effects of sulpiride and metoclopramide on amphetamine-induced stereotypy. Eur J Pharmacol 109:81–89Google Scholar
  36. Sallers CF, Salama AI (1985) Dopamine receptor subtypes: in vivo biochemical evidence for functional interaction. Eur J Pharmacol 109:297–300Google Scholar
  37. Santiago M, Westerink BHC (1991) Characterisation and pharmacological responsiveness of dopamine release recorded by microdialysis in the substantia nigra of conscious rats. J Neurochem 57:738–747Google Scholar
  38. Sokoloff P, Martres MP, Redouane K, Schwartz JC, Protais P, Vasse M, Dubuc I, Costentin J, Hamdi P, Mann A, Wermuth CG (1987) Behavioral and neurochemical profiles of discriminant benzamine derivatives. Psychiatrie & Psychobiologie II [4]:253–264Google Scholar
  39. Sokoloff P, Giros B, Martres MP, Bouthenet M, Schwartz JC (1990) Molecular cloning and characterization of a novel dopamine receptor (D3) as a target for neuroleptics. Nature 347:146–151Google Scholar
  40. Spyraki C, Fibiger HC, Phillips AG (1982) Attenuation by haloperidol of place preference conditioning using food reinforcement. Psychopharmacology 77:379–382Google Scholar
  41. Spyraki C, Fibiger HC, Phillips AG (1983) Attenuation of heroin reward in rats by disruption of the mesolimbic dopamine system Psychopharmacology 79:278–283Google Scholar
  42. Ståhle L (1992) Do autoreceptors mediate dopamine agonist-induced yawning and suppression of exploration? A critical review. Psychopharmacology 106:1–13Google Scholar
  43. Ståhle L, Ungerstedt U (1990) Yawning and suppression of exploration induced by dopamine agonists: no relation to extracellular striatal levels of dopamine. Pharmacol Biochem Behav 35:201–209Google Scholar
  44. Stellar JR, Rice MB (1989) Pharmacological basis of intracranial self-stimulation reward. In: Liebman JM, Cooper SJ (eds) The neuropharmacological basis of reward. Oxford University Press, Oxford, pp 14–65Google Scholar
  45. Svenson K, Kling-Petersen T, Waters N, Ekman A, Carlsson A (1991) The preferential dopamine autoreceptor antagonist (+)-AJ76 increases motor activity in habituated rats and antagonizesd-amphetamine-induced hyperactivity. Posters Neurosci 1:75–79Google Scholar
  46. Talmaciu RK, Hoffman IS, Cubeddu LX (1986) Dopamine autoreceptors modulate dopamine release from the prefrontal cortex. J Neurochem 47:865–870Google Scholar
  47. Taylor JR, Robbins TW (1986) 6-Hydroxydopamine lesions of the nucleus accumbens, but not of the caudate nucleus, attenuate enhanced responding with reward-related stimuli produced by intra-accumbensd-amphetamine. Psychopharmacology 90:390–397Google Scholar
  48. Triet D (1990) A comparison of benzodiazepine, serotonin, and dopamine agents in the taste-reactivity paradigm. Pharmacol Biochem Behav 37:451–456Google Scholar
  49. Vezina P, Stewart J (1987) Conditioned locomotion and place preference elicited by tactile cues paired exclusively with morphine in an openfield. Psychopharmacology 91:375–380Google Scholar
  50. Walters JR, Bergstrom DA, Carlson JH, Chase TN, Braun, AR (1987) D1 dopamine receptor activation required for postsynaptic expression of D2 agonist effects. Science 236:719–722Google Scholar
  51. Westerink BHC, de Vries JB (1989) On the mechanism of neuroleptic induced increase in striatal dopamine release: brain dialysis provides direct evidence for mediation by autoreceptors localized on nerve terminals. Neurosci Lett 99:197–202Google Scholar
  52. White NM, Carr GD (1985) The conditioned place preference is affected by two independent reinforcement processes. Pharmacol Biochem Behav 23:37–42Google Scholar
  53. Willner P, Phillips G, Muscat R (1991) Suppression of rewarded behaviour by neuroleptic drugs: can't or won't and why? In: Willner P, Scheel-Krüger J (eds) The mesolimbic dopamine system: from motivation to action. Wiley, Chichester, pp 251–271Google Scholar
  54. Wise RA (1982) Neuroleptics: the anhedonia hypothesis. Behav Brain Sci 5:39–87Google Scholar
  55. Wise RA, Bozarth MA (1981) Brain substrates for reinforcement and drug self administration. Progr Neuropsychopharmacol Biol Psychiatry 5:467–474Google Scholar
  56. Wolf ME, Roth RH (1987) Dopamine neurons projecting to the medial prefrontal cortex possess release-modulating autoreceptors. Neuropharmacology 26:1053–1059Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • Alice Guyon
    • 1
  • Françoise Assouly-Besse
    • 1
  • Grazyna Biala
    • 1
  • Alain J. Puech
    • 1
  • Marie-Hélène Thiébot
    • 2
  1. 1.Département de Pharmacologie, Faculté de Médecine Pitié-SalpêtriéreINSERM U-302Paris Cedex 13France
  2. 2.Département de Pharmacologie, Faculté de Médecine Pitié-SalpêtriéreINSERM U-288Paris Cedex 13France

Personalised recommendations