Skip to main content
SpringerLink
Log in

Mesoaccumbens dopamine-opiate interactions in the control over behaviour by a conditioned reinforcer

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

Abstract

These experiments examined the role of dopamine-opiate interactions in the ventral tegmental area (VTA) and nucleus accumbens in the mediation of reinforcement-related behaviour. It has been shown previously that opiates induce a dopamine-dependent increase in locomotor activity in rats when infused into the VTA, and a dopamine-independent hyperactivity when infused into the nucleus accumbens. The present study investigated the generality and significance of these two findings, by examining dopamine-opiate interactions in the control over behaviour exerted by a conditioned reinforcer (CR), an arbitrary stimulus which gains control by association with primary reinforcement. Rats were trained to associate a light/noise stimulus with sucrose reinforcement, and the efficacy of the CR in controlling behaviour was assessed by measuring its ability to support a new lever pressing response. Responding on one lever (CR lever) produced the CR, responding on the other lever had no programmed consequences. In experiment 1, intra-accumbens infusions ofd-amphetamine (10 µg), the D1 dopamine receptor agonist SKF-38393 (0.1 µg), the D2 dopamine receptor agonist LY-171555 (quinpirole; 0.1 µg) or the opiate receptor agonist [d-Ala2]-methionine enkephalinamide (DALA; 1 µg) selectively increased responding on the CR lever. Infusion with DALA intra-VTA had no effect. However, pretreatment with DALA intra-VTA (10 × 1 µg/day) subsequently reduced the selectivity of the response to infusions intra-accumbens withd-amphetamine or SKF-38393, and blocked the response to LY-171555 or DALA. Pretreatment also shifted to the right the dose-response function for DALA intra-accumbens. In experiment 2, intra-accumbens infusions ofd-amphetamine, SKF-38393, LY-171555 or DALA again increased responding on the CR lever only. Pretreatment with intra-accumbensd-amphetamine (5 × 1 µg/day) reduced the selectivity of the response subsequently tod-amphetamine, and blocked the response to SKF-38393, LY-171555 or DALA. In experiment 3, intra-accumbens infusions of the μ-opiate receptor agonist [d-Ala2,N-Me-Phe4,Gly5-ol]-enkephalin (0.003–0.1 µg), or the δ-opiate receptor agonist [d-Pen2, 5]-enkephalin (0.03–1 µg) enhanced selectively responding on the CR lever. Thus, the dopamine-dependent locomotor-stimulant properties of intra-VTA infusions of opiates are associated with impaired conditioned reinforcer efficacy. Finally, repeated stimulation of the mesoaccumbens dopamine pathway may compromise the dopamine-independence of the opiate system within the nucleus accumbens.

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

Similar content being viewed by others

References

  • Anisman H, Zacharko RM (1986) Behavioural and neurochemical consequences associated with stressors. Ann N Y Acad Sci 467:205–225

    Google Scholar 

  • Anisman H, Hamilton ME, Zacharko RM (1979) Effects of inescapable shock on subsequent escape performance: catecholaminergic and cholinergic mediation of response initiation and maintenance. Psychopharmacology 61:107–124

    Google Scholar 

  • Bannon MJ, Kelland M, Chiodo LA (1989a) Medial forebrain bundle stimulation or D2 dopamine receptor activation increases preproenkephalin mRNA in rat striatum. J Neurochem 52:859–862

    Google Scholar 

  • Beninger RJ, Hanson DR, Phillips AG (1980) The effects of pipradrol on responding with conditioned reinforcement: a role for sensory pre-conditioning. Psychopharmacology 69:235–242

    Google Scholar 

  • Bolam JP, Izzo PN (1988) The postsynaptic targets of substance P-immunoreactive terminals in the rat neostriatum with particular reference to identified spiny striatonigral neurons. Exp Brain Res 70:361–377

    Google Scholar 

  • Broekkamp CLE, Phillips AG, Cools AR (1979) Stimulant effects of enkephalin microinjection into the DAergic A10 area. Nature 278:560–562

    Google Scholar 

  • Cador M, Taylor JR, Robbins TW (1991) Potentiation of the effects of reward-related stimuli by dopaminergic-dependent mechanisms in the nucleus accumbens. Psychopharmacology 104:377–385

    Google Scholar 

  • Cador M, Rivet J-M, Kelley AE, Le Moal M, Stinus L (1989) Substance P, neurotensin and enkephalin injections into the ventral tegmental area: comparative study on dopamine turnover in several forebrain structures. Brain Res 486:357–363

    Google Scholar 

  • Churchill L, Kalivas PW (1992) Dopamine depletion produces augmented behavioural responses to a μ-, but not δ-opioid receptor agonist in the nucleus accumbens: lack of a role for receptor upregulation. Synapse 11:47–57

    Google Scholar 

  • Clark JA, Houghten R, Pasternak GW (1988) Opiate binding in calf thalamic membranes: a selective mu1 binding assay. Mol Pharmacol 34:308–317

    Google Scholar 

  • Cunningham ST, Kelley AE (1992a) Evidence for opiate-dopamine cross-sensitization in nucleus accumbens: studies of conditioned reward. Brain Res Bull 29:675–680

    Google Scholar 

  • Cunningham ST, Kelley AE (1992b) Opiate infusion into nucleus accumbens: contrasting effects on motor activity and responding for conditioned reward. Brain Res 588:104–114

    Google Scholar 

  • De Montis MG, Devoto P, Gessa GL, Porcella A, Serra G, Tagliomonte A (1990) Possible role of dopamine receptors in the mechanism of action of antidepressants. In: Gessa GL, Serra G (eds) Dopamine and mental depression. (Advances in the Biosciences) Pergamon, New York, pp 147–157

    Google Scholar 

  • Deutsch AY, Tam S-Y, Roth RH (1985) Footshock and conditioned stress increase 3,4-dihydroxyphenylacetic acid (DOPAC) in the ventral tegmental area but not the substantia nigra. Brain Res 333:143–146

    Google Scholar 

  • Dilts RP, Kalivas PW (1988) Localization of mu opioid and neurotensin receptors within the A10 region of the rat. Ann N Y Acad Sci 537:472–474

    Google Scholar 

  • Dilts RP, Kalivas PW (1989) Autoradiographic localization of muopioid and neurotensin receptors within the mesolimbic dopamine system. Brain Res 488:311–327

    Google Scholar 

  • Everitt BJ, Robbins TW (1992) Amygdala-ventral striatal interactions and reward-related processes. In: Aggleton JP (ed) The amygdala: neurobiological aspects of emotion, memory and mental dysfunction. Wiley, New York, pp 401–430

    Google Scholar 

  • Fadda F, Argiolas A, Melis M, Tissari A, Onali P, Gessa G (1978) Stress induced increase in 3,4-dihydroxyphenylacetic acid (DOPAC) levels in the cerebral cortex but not in the nucleus accumbens: reversal by diazepam. Life Sci 23:2219–2224

    Google Scholar 

  • Gerfen CR (1992) D1 and D2 dopamine receptor regulation of striatonigral and striatopallidal neurons. Semin Neurosci 4:109–118

    Google Scholar 

  • Gysling K, Wang RY (1983) Morphine-induced activation of A10 dopamine neurons in the rat brain. Brain Res 277:119–127

    Google Scholar 

  • Handa BK, Lane A, Lord JAH, Morgan BA, Rance JJ, Smith CFC (1981) Analogs of beta-LPH61–64 possessing selective agonist activity of mu-opiate receptors. Eur J Pharmacol 70:531–540

    Google Scholar 

  • Heijna MH, Padt M, Hogenboom F, Portoghese PS, Mulder AH, Schoffelmeer AN (1990) Opioid receptor-mediated inhibition of dopamine and acetylcholine release from slices of rat nucleus accumbens, olfactory tubercle and frontal cortex. Eur J Pharmacol 181:267–278

    Google Scholar 

  • Henry DJ, White FJ (1991) Repeated cocaine administration causes persistent enhancement of D1 dopamine receptor sensitivity within the rat nucleus accumbens. J Pharmacol Exp Ther 258:882–890

    Google Scholar 

  • Herkenham M, Moon Edley S, Stuart J (1984) Cell clusters in the nucleus accumbens of the rat, and the mosaic relationship of opiate receptors, acetylcholinesterase and subcortical afferent terminations. Neuroscience 11:561–593

    Google Scholar 

  • Higashi H, Inanaga K, Nishi S, Uchimura N (1989) Enhancement of dopamine actions on rat nucleus accumbens neurones in vitro after methamphetamine pre-treatment. J Physiol (Lond) 408:587–603

    Google Scholar 

  • Hill RT (1970) Facilitation of conditioned reinforcement as a mechanism of psychomotor stimulation. In: Costa E, Garattini S (eds) Amphetamine and related compounds. Raven, New York, pp 781–795

    Google Scholar 

  • Hong JS, Yang M-Y, Fratta W, Costa E (1978) Rat striatal metenkephalin content after chronic treatment with cataleptogenic and non-cataleptogenic antischizophrenia drugs. J Pharmacol Exp Ther 205:141–147

    Google Scholar 

  • Hong JS, Yang M-Y, Gillin JC, Di Guilio AM, Fratta W, Costa E (1979) Chronic treatment with haloperidol accelerates the biosynthesis of enkephalins in rat striatum. Brain Res 160:192–195

    Google Scholar 

  • Johnson SW, North RA (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12:483–488

    Google Scholar 

  • Kalivas PW, Abhold R (1987) Enkephalin release into the ventral tegmental area in response to stress: modulation of mesocorticolimbic dopamine. Brain Res 414:339–348

    Google Scholar 

  • Kalivas PW, Bronson M (1985) Mesolimbic dopamine lesions produce an augmented behavioural response to enkephalin. Neuropharmacology 24:931–936

    Google Scholar 

  • Kalivas PW, Duffy P (1987) Sensitization to repeated morphine injection in the rat: possible involvement of A10 dopamine neurons. J Parmacol Exp Ther 241:201–212

    Google Scholar 

  • Kalivas PW, Duffy P (1990) Effect of acute and daily neurotensin and enkephalin treatments on extracellular dopamine in the nucleus accumbens. J Neurosci 10:2940–2949

    Google Scholar 

  • Kalivas PW, Duffy P (1993a) Time course of extracellular dopamine and behavioural sensitization to cocaine. I. Dopamine axon terminals. J Neurosci 13:266–275

    Google Scholar 

  • Kalivas PW, Duffy P (1993b) Time course of extracellular dopamine and behavioural sensitization to cocaine. II. Dopamine perikarya. J Neurosci 13:276–284

    Google Scholar 

  • Kalivas PW, Richardson-Carlson R (1986) Endogenous enkephalin modulation of dopamine neurons in the ventral tegmental area. Am J Physiol 251: R243-R249

    Google Scholar 

  • Kalivas PW, Widerlov E, Stanley D, Breese GR, Prange A (1983) Enkephalin action on the mesolimbic system: a dopamine-dependent and a dopamine-independent increase in locomotor activity. J Pharmacol Exp Ther 227:229–237

    Google Scholar 

  • Kalivas PW, Taylor S, Miller JS (1985) Sensitization to repeated enkephalin administration into the ventral tegmental area of the rat. I. Behavioral characterization. J Pharmacol Exp Ther 235:537–543

    Google Scholar 

  • Kalivas PW, Richardson Carlson R, Van Orden G (1986) Cross-sensitization between foot shock stress and enkephalin-induced motor activity. Biol Psychiatry 21:939–950

    Google Scholar 

  • Kalivas PW, Duffy P, Dilts R, Abhold R (1988) Enkephalin modulation of A10 dopamine neurons: a role in dopamine sensitization. Ann N Y Acad Sci 537:405–414

    Google Scholar 

  • Katz RJ (1982) Animal model of depression: pharmacological sensitivity of a hedonic deficit. Pharmacol Biochem Behav 16:965–968

    Google Scholar 

  • Katz JL, Griffiths JW, Sharpe LG, De Souza EB, Witkin JM (1993) Cocaine tolerance and cross-tolerance. J Pharmacol Exp Ther 264:183–192

    Google Scholar 

  • Kelley AE, Delfs JM (1991) Dopamine and conditioned reinforcement. II. Contrasting effects of amphetamine microinjection into the nucleus accumbens with peptide microinjection into the ventral tegmental area. Psychopharmacology 103:197–203

    Google Scholar 

  • Khatchaturian H, Lewis ME, Watson SJ (1983) Enkephalin systems in the diencephalon and brainstem of the rat. J Comp Neurol 220:310–320

    Google Scholar 

  • Klimek V, Maj J (1990) The effect of antidepressant drugs given repeatedly on the binding of3H-SCH-23390 and3H-spiperone to dopaminergic receptors. In: Gessa GL, Serra G (eds) Dopamine and mental depression. (Advances in the Biosciences) Pergamon, New York, pp 159–166

    Google Scholar 

  • Klimek V, Nielsen EB (1987) Chronic treatment with anti-depressants decreases the number of [3H]SCH 23390 binding sites in the rat striatum and limbic system. Eur J Pharmacol 139:163–169

    Google Scholar 

  • Latimer LG, Duffy P, Kalivas PW (1987)Mu opioid receptor involvement in enkephalin activation of dopamine neurons in the ventral tegmental area. J Pharmacol Exp Ther 241:328–337

    Google Scholar 

  • Lutz RA, Cruciani RA, Munson PJ, Rodbard D (1985) Mu1: a very high affinity subtype of enkephalin binding sites in the rat brain. Life Sci 36:2233–2238

    Google Scholar 

  • Mackintosh, NJ (1974) The psychology of animal learning. Academic, London

    Google Scholar 

  • Maier SF, Seligman MEP (1976) Learned helplessness: theory and evidence. J Exp Psychol Gen 105:3–46

    Google Scholar 

  • Maj J (1990) Behavioural effects of antidepressant drugs given repeatedly on the dopaminergic system. In: Gessa GL, Serra G (eds) Dopamine and mental depression. (Advances in the Biosciences) Pergamon, New York, pp 139–146

    Google Scholar 

  • Maldonado R, Dauge V, Feger J, Roques BP (1990) Chronic blockade of D2 but not D1 dopamine receptors facilitates behavioural responses to endogenous enkephalins, protected by kelatorphan, administered in the accumbens in rats. Neuropharmacology 29:215–223

    Google Scholar 

  • Matthews RT, German DC (1984) Electrophysiological evidence for excitation of rat ventral tegmental area dopamine neurons by morphine. Neuroscience 11:617–625

    Google Scholar 

  • Mocchetti I, Naranjo JR, Costa E (1987) Regulation of striatal enkephalin turnover in rats receiving antagonists of specific dopamine receptor subtypes. J Pharmacol Exp Ther 241:1120–1124

    Google Scholar 

  • Morris BJ, Herz A, Hollt V (1989) Localization of striatal opioid gene expression, and its modulation by the mesostriatal dopamine pathway: an in situ hybridization study. J Mol Neurosci 1:9–18

    Google Scholar 

  • Mosberg HI, Hurst R, Hruby VJ, Gee K, Yamamura HI, Galligan JJ, Burks TF (1983) Bis-penicillamine enkephalins possess highly improved specificity toward δ-opioid receptors. Proc Natl Acad Sci USA 80:5871–5874

    Google Scholar 

  • Mugnaini E, Oertel WH (1985) An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunohistochemistry. In: Bjorklund A, Hokfelt T (eds) Handbook of chemical neuroanatomy, vol 4. GABA and neuropeptides in the CNS. Elsevier, Amsterdam, pp 436–608

    Google Scholar 

  • O'Connell ML, Canipari R, Strickland S (1987) Hormonal regulation of tissue plasminogen activator secretion and mRNA levels in rat granulosa cells. J Biol Chem 262:2339–2344

    Google Scholar 

  • Pasternak GW (1986) Multiple mu opiate receptors: biochemical and pharmacological evidence for multiplicity. Biochem Pharmacol 35:361–364

    Google Scholar 

  • Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates sydney. Academic Press

  • Pellegrino LJ, Pellegrino AS, Cushman AJ (1979) A stereotaxic atlas of the rat brain. 2nd ed. Plenum, New York

    Google Scholar 

  • Pendleton RG, Samler L, Kaiser C, Ridley PT (1978) Studies on renal dopamine receptors with SK&F 38393, a new agonist. Eur J Pharmacol 51:19–28

    Google Scholar 

  • Pentney RJW, Gratton A (1991) Effects of local delta and mu opioid receptor activation on basal and stimulated dopamine release in striatum and nucleus accumbens of rat: an in vivo electrochemical study. Neuroscience 45:95–102

    Google Scholar 

  • Pert A, Sivit C (1977) Neuroanatomical focus for morphine and enkephalin-induced hypermotility. Nature 265:645–647

    Google Scholar 

  • Petit F, Hamon M, Fournie Zaluski MC, Roques BP, Glowinski J (1986) Further evidence for a role of delta-opiate receptors in the presynaptic regulation of newly synthesized dopamine release. Eur J Pharmacol 126:1–9

    Google Scholar 

  • Petrusz P, Merchenthaler I, Maderdrut JL (1985) Distribution of enkephalin-containing neurons in the central nervous system. In: Bjorklund A, Hokfelt T (eds) Handbook of chemical neuroanatomy, vol 4. GABA and neuropeptides in the CNS. Elsevier, Amsterdam, pp 273–334

    Google Scholar 

  • Pettit HO, Ettenberg A, Bloom FE, Koob GF (1984) Destruction of dopamine in the nucleus accumbens selectively attenuates cocaine but not heroin self-administration in rats. Psychopharmacology 84:167–173

    Google Scholar 

  • Robbins TW (1978) The acquisition of responding with conditioned reinforcement: effects of pipradrol, methylphenidate,d-amphetamine and nomifensine. Psychopharmacology 58:79–87

    Google Scholar 

  • Robbins TW, Watson BA, Gaskin M, Ennis C (1983) Contrasting interactions of pipradrol,d-amphetamine, cocaine, cocaine analogues, apomorphine and other drugs with conditioned reinforcement. Psychopharmacology 80:113–119

    Google Scholar 

  • Robbins TW, Cador M, Taylor JR, Everitt BJ (1989) Limbic-striatal interactions in reward-related processes. Neurosci Biobehav Rev 13:155–162

    Google Scholar 

  • Rosellini RA, De Cola JP, Shapiro NR (1982) Cross-motivational effects of inescapable shock are associative in nature. J Exp Psychol [Anim Behav Proc] 8:376–388

    Google Scholar 

  • Rothman RB, Mahboubi A, Bykov V, Kim C-H, de Costa BR, Jacobson AE, Rice K (1992) Probing the opioid receptor complex with (+)-Trans-SUPERFIT. II. evidence that m ligands are noncompetitive inhibitors of the δcx opioid peptide binding site. Peptides 13:1137–1143

    Google Scholar 

  • Sabol SL, Yoshikawa K, Hong JS (1983) Regulation of methionine-enkephalin precursor messenger RNA in rat striatum by haloperidol and lithium. Biochem Biophys Res Commun 113:391–399

    Google Scholar 

  • Setler PE, Sarau HM, Zirkle CL, Saunders HL (1978) The central effects of a novel dopamine agonist. Eur J Pharmacol 50:419–430

    Google Scholar 

  • Somogyi P, Bolam JP, Smith AD (1981) Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons. A light and electron microscopic study using the golgi-peroxidase transport-degeneration procedure. J Comp Neurol 195:567–584

    Google Scholar 

  • Stamford JA, Muscat R, O'Connor JJ, Patel J, Trout SJ, Wieczorek WJ, Kruk ZL, Willner P (1991) Voltammetric evidence that subsensitivity to reward following chronic mild stress is associated with increased release of mesolimbic dopamine. Psychopharmacology 105:275–282

    Google Scholar 

  • Stinus L, Winnock MR, Kelley AE (1985) Chronic neuroleptic treatment and mesolimbic dopamine denervation induce behavioral supersensitivity to opiates. Psychopharmacology 85:323–328

    Google Scholar 

  • Stinus L, Nadaud D, Jauregui J, Kelley AE (1986) Chronic treatment with five different neuroleptics elicits behavioral supersensitivity to opiate infusion into the nucleus accumbens. Biol Psychiatry 21:34–48

    Google Scholar 

  • Stinus L, Nadaud D, Deminiere JM, Jauregui J, Hand TT, Le Moal M (1989) Chronic flupentixol treatment potentiates the reinforcing properties of systemic heroin administration. Biol Psychiatry 26:363–371

    Google Scholar 

  • Taylor JR, Robbins TW (1984) Enhanced behavioural control by conditioned reinforcers following microinjections of d-amphetamine into the nucleus accumbens. Psychopharmacology 84:405–412

    Google Scholar 

  • 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-accumbens d-amphetamine. Psychopharmacology 90:390–397

    Google Scholar 

  • Thierry A, Tassin J-P, Blanc G, Glowinski J (1979) Selective activation of the mesocortical dopamine system by stress. Nature 263:242–244

    Google Scholar 

  • Titus RD, Kornfeld EC, Jones ND, Clemens JA, Smalstig EB, Fuller RW, Hahn RA (1983) Resolution and absolute confirmation of an ergoline-related dopamine agonist, trans-4,4a,5,6,7,8a,9-Octahydro-5-propyl-1H(or 2H)-pyrazolo (3,4-9)quinolino. J Med Chem 26:1112–1116

    Google Scholar 

  • Trovero F, Herve D, Desban M, Glowinski J, Tassin J-P (1990) Striatal opiate mu-receptors are not located on dopamine nerve endings in the rat. Neuroscience 39:313–322

    Google Scholar 

  • Unterwald EM, Tempel A, Koob GF, Zukin RS (1989) Characterization of opioid receptors in rat nucleus accumbens following mesolimbic dopaminergic lesions. Brain Res 505:111–118

    Google Scholar 

  • Vezina P, Kalivas PW, Stewart J (1987) Sensitization occurs to the locomotor effects of morphine and the specific mu opioid receptor agonist, DAGO, administered repeatedly to the ventral tegmental area but not to the nucleus accumbens. Brain Res 417:51–58

    Google Scholar 

  • Vezina P, Blanc G, Glowinski J, Tassin JP (1992) Nicotine and morphine differentially activate brain dopamine in prefrontocortical and subcortical terminal fields: effects of acute and repeated injections. J Pharmacol Exp Ther 261:484–490

    Google Scholar 

  • Voorn P, Roest G, Groenewegen HJ (1987) Increase of enkephalin and decrease of substance P immunoreactivity in the dorsal and ventral striatum of the rat after midbrain 6-hydroxydopamine lesions. Brain Res 412:391–396

    Google Scholar 

  • Voorn P, Gerfen CR, Groenewegen HJ (1989) Compartmental organization of the ventral striatum of the rat: immunohistochemical distribution of enkephalin, substance P, dopamine, and calcium-binding protein. J Comp Neurol 289:189–201

    Google Scholar 

  • Weiss JM, Goodman PA, Losito BG, Corrigan S, Charry JM, Bailey WH (1981) Behavioural depression produced by an uncontrollable stressor: relationship to norepinephrine, dopamine and serotonin levels in various regions of rat brain. Brain Res Rev 3:157–205

    Google Scholar 

  • Willner P, Muscat R, Papp M, Sampson D (1991) Dopamine, depression and anti-depressant drugs. In: Willner P, Scheel-Kruger J (eds) The mesolimbic dopamine system: from motivation to action. Wiley, Chichester, pp 387–410

    Google Scholar 

  • Wilson CJ, Groves PM (1980) Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intracellular injection of horseradish peroxidase. J Comp Neurol 194:599–615

    Google Scholar 

  • Winer BJ (1971) Statistical principles in experimental design. McGraw-Hill, New York

    Google Scholar 

  • Wolf ME, White FJ, Nassar R, Brooderson RJ, Khansa MR (1993) Differential development of autoreceptor subsensitivity and enhanced dopamine release during amphetamine sensitization. J Pharmacol Exp Ther 264:249–255

    Google Scholar 

  • Wolterink G, Phillips G, Cador M, Donselaar-Wolterink I, Robbins TW, Everitt BJ (1993) Relative roles of ventral striatal D1 and D2 dopamine receptors in responding with conditioned reinforcement. Psychopharmacology 110:355–364

    Google Scholar 

  • Xu H, Partilla JS, de Costa BR, Rice KC, Rothman RB (1992) Interaction of opioid peptides and other drugs with multiple δcx binding sites in rat brain: further evidence for heterogeneity. Peptides 13:1207–1213

    Google Scholar 

  • Young WS, Bonner TI, Brann MR (1986) Mesencephalic dopamine neurons regulate the expression of neuropeptide mRNAs in the rat forebrain. Proc Natl Acad Sci USA 83:9827–9831

    Google Scholar 

  • Zacharko RM, Anisman H (1991) Stressor-induced anhedonia in the mesocorticolimbic system. Neurosci Biobehav Rev 15:391–405

    Google Scholar 

  • Zacharko RM, Bowers WJ, Kokkindis L, Anisman H (1983) Region specific reductions of intracranial self-stimulation after uncontrollable stress: possible effects on reward processes. Behav Brain Res 9:129–141

    Google Scholar 

  • Zacharko RM, Bowers WJ, Kelley MS, Anisman H (1984) Prevention of stressor-induced disturbances of self-stimulation by desmethylimipramine. Brain Res 321:175–179

    Google Scholar 

  • Zacharko RM, Kasain M, MacNeil G, Anisman H (1990) Stressor induced behavioural alterations in intracranial self-stimulation from the ventral tegmental area: evidence for regional variations. Brain Res Bull 25:241–246

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, University of Cambridge, Downing Street, CB2 3DY, Cambridge, United Kingdom

    Gavin D. Phillips & Barry J. Everitt

  2. Department of Experimental Psychology, University of Cambridge, Downing Street, CB2 3DY, Cambridge, United Kingdom

    Trevor W. Robbins

Authors
  1. Gavin D. Phillips
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Trevor W. Robbins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Barry J. Everitt
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Phillips, G.D., Robbins, T.W. & Everitt, B.J. Mesoaccumbens dopamine-opiate interactions in the control over behaviour by a conditioned reinforcer. Psychopharmacology 114, 345–359 (1994). https://doi.org/10.1007/BF02244858

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02244858

Key words

Search

Navigation