Dopamine and reward: The anhedonia hypothesis 30 years on

Abstract

The anhedonia hypothesis — that brain dopamine plays a critical role in the subjective pleasure associated with positive rewards — was intended to draw the attention of psychiatrists to the growing evidence that dopamine plays a critical role in the objective reinforcement and incentive motivation associated with food and water, brain stimulation reward, and psychomotor stimulant and opiate reward. The hypothesis called to attention the apparent paradox that neuroleptics, drugs used to treat a condition involving anhedonia (schizophrenia), attenuated in laboratory animals the positive reinforcement that we normally associate with pleasure. The hypothesis held only brief interest for psychiatrists, who pointed out that the animal studies reflected acute actions of neuroleptics whereas the treatment of schizophrenia appears to result from neuroadaptations to chronic neuroleptic administration, and that it is the positive symptoms of schizophrenia that neuroleptics alleviate, rather than the negative symptoms that include anhedonia. Perhaps for these reasons, the hypothesis has had minimal impact in the psychiatric literature. Despite its limited heuristic value for the understanding of schizophrenia, however, the anhedonia hypothesis has had major impact on biological theories of reinforcement, motivation, and addiction. Brain dopamine plays a very important role in reinforcement of response habits, conditioned preferences, and synaptic plasticity in cellular models of learning and memory. The notion that dopamine plays a dominant role in reinforcement is fundamental to the psychomotor stimulant theory of addiction, to most neuroadaptation theories of addiction, and to current theories of conditioned reinforcement and reward prediction. Properly understood, it is also fundamental to recent theories of incentive motivation.

This is a preview of subscription content, access via your institution.

References

  1. Ahlenius S (1985) A functional consideration of anatomical connections between the basal ganglia and the thalamus suggests that antipsychotic drugs inhibit the initiation of movement.Behav. Brain Sci. 8, 173–174.

    Google Scholar 

  2. Axelrod J (1970) Amphetamine: metabolism, physiological disposition, and its effects on catecholamine storage, In:Amphetamines and Related Compounds (Costa E and S Garattini, Eds.) (Raven Press:New York), pp 207–216.

    Google Scholar 

  3. Baldo BA and AE Kelley (2007) Discrete neurochemical coding of distinguishable motivational processes: insights from nucleus accumbens control of feeding.Psychopharmacol. 191, 439–459.

    CAS  Article  Google Scholar 

  4. Bellmaker RH and D Wald (1977) Haloperidol in normalsBr. J. Psychiatry 131, 222–223.

    Article  Google Scholar 

  5. Berridge KC (2000) Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns.Neurosci. Biobehav. Rev. 24, 173–198.

    PubMed  CAS  Article  Google Scholar 

  6. Berridge KC and HJ Grill (1984) Isohedonic tastes support a two-dimensional hypothesis of palatability.Appetite 5, 221–231.

    PubMed  CAS  Google Scholar 

  7. Berridge KC and TE Robinson (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?Brain Res. Rev. 28, 309–369.

    PubMed  CAS  Article  Google Scholar 

  8. Bielajew C and P Shizgal (1986) Evidence implicating descending fibers in self-stimulation of the medial forebrain bundle.J. Neurosci. 6, 919–929.

    PubMed  CAS  Google Scholar 

  9. Bijerot N (1980) Addiction to pleasure: a biological and social-psychological theory of addiction, In:Theories on Drug Abuse:Selected Contemporary Perspectives (Lettieri DJ, M Sayersand & HW Pearson, Eds.) (National Institute on Drug Abuse, Rockville, MD), pp 246–255.

    Google Scholar 

  10. Bloom FE and ELF Battenberg (1976) A rapid, simple and sensitive method for the demonstration of central catecholamine-containing neurons and axons by glyoxylic acid-induced fluorescence. II. A detailed description of methodology.J. Histochem. Cytochem. 24, 561–571.

    PubMed  CAS  Google Scholar 

  11. Bozarth MA and RA Wise (1981) Intracranial self-administration of morphine into the ventral tegmental area in rats.Life Sci. 28, 551–555.

    PubMed  CAS  Article  Google Scholar 

  12. Brauer LH and H de Wit (1996) Subjective responses to d-amphet-amine alone and after pimozide pretreatment in normal, healthy volunteers.Biol. Psychiatry 39, 26–32.

    PubMed  CAS  Article  Google Scholar 

  13. Brauer LH and H de Wit (1997) High dose pimozide does not block amphetamine-inducedeuphoria innormal volunteers.Pharmacol. Biochem. Behav. 56, 265–272.

    PubMed  CAS  Article  Google Scholar 

  14. Broekkamp CLE, JH Van den Bogaard, HJ Heijnen, RH Rops, AR Cools and JM Van Rossum (1976) Separation of inhibiting and stimulating effects of morphine on self-stimulation behavior by intracerebral microinjections.Eur. J. Pharmacol. 36, 443–446.

    PubMed  CAS  Article  Google Scholar 

  15. Carlezon WA Jr, DP Devine and RA Wise (1995) Habit-forming actions of nomifensine in nucleus accumbens.Psychopharmacol. 122, 194–197.

    CAS  Article  Google Scholar 

  16. Carlsson A (1959) The occurrence, distribution and physiological role of catecholamines in the nervous system.Pharmacol. Rev. 11, 90–493.

    Google Scholar 

  17. Carlsson A (1970) Amphetamine and brain catecholamines, In:Amphetamines and Related Compounds (Costa E & S Garattini, Eds.) (Raven Press:New York), pp 289–300.

    Google Scholar 

  18. Carlsson A, M Lindqvist, T Magnusson and B Waldeck (1958) On the presence of 3-hydroxytyramine in brain.Science 127, 471.

    PubMed  CAS  Article  Google Scholar 

  19. Carlsson A, B Falck and N Hillarp (1962) Cellular localization of brain monoamines.Acta Physiol. Scand. Suppl.56, 1–28.

    Google Scholar 

  20. Centonze D, B Picconi, P Gubellini, G Bernard and P Calabresi (2001) Dopaminergic control of synaptic plasticity in the dorsal striatum.Eur. J. Neurosci. 13, 1071–1077.

    PubMed  CAS  Article  Google Scholar 

  21. Colpaert F, W Koek, M Kleven and J Besnard (2007) Induction by antipsychotics of “win-shift” in the drug discrimination paradigm.J. Pharmacol. Exp. Ther. 322, 288–298.

    PubMed  CAS  Article  Google Scholar 

  22. Corbett D and RA Wise (1979) Intracranial self-stimulation in relation to the ascending noradrenergic fiber systems of the pontine tegmentum and caudal midbrain: a moveable electrode mapping study.Brain Res. 177, 423–436.

    PubMed  CAS  Article  Google Scholar 

  23. Corbett D and RA Wise (1980) Intracranial self-stimulation in relation to the ascending dopaminergic systems of the midbrain: a moveable electrode mapping study.Brain Res. 185, 1–15.

    PubMed  CAS  Article  Google Scholar 

  24. Corbett D, RW Skelton and RA Wise (1977) Dorsal noradrenergic bundle lesions fail to disrupt self-stimulation from the region of locus coeruleus.Brain Res. 133, 37–44.

    PubMed  CAS  Article  Google Scholar 

  25. Crow TJ (1972) A map of the rat mesencephalon for electrical self-stimulation.Brain Res. 36, 265–273.

    PubMed  CAS  Article  Google Scholar 

  26. Crow TJ, PJ Spear and GW Arbuthnott (1972) Intracranial self-stimulation with electrodes in the region of the locus coeruleus.Brain Res. 36, 275–287.

    PubMed  CAS  Article  Google Scholar 

  27. de Wit H and J Stewart (1983) Drug reinstatement of heroin-reinforced responding in the rat.Psychopharmacol. 79, 29–31.

    Article  Google Scholar 

  28. de Wit H and RA Wise (1977) Blockade of cocaine reinforcement in rats with the dopamine receptor blocker pimozide, but not with the noradrenergic blockers phentolamine or phenoxybenzamine.Can. J. Psychol. 31, 195–203.

    PubMed  Google Scholar 

  29. Edmonds DE and CR Gallistel (1974) Parametric analysis of brain stimulation reward in the rat: III. Effect of performance variables on the reward summation function.J. Comp. Physiol. Psychol. 87, 876–883.

    PubMed  CAS  Article  Google Scholar 

  30. Ettenberg A and CH Camp (1986a) A partial reinforcement extinction effect in water-reinforced rats intermittently treated with haloperidol.Pharmacol. Biochem. Behav. 25, 1231–1235.

    PubMed  CAS  Article  Google Scholar 

  31. Ettenberg A and CH Camp (1986b) Haloperidol induces a partial reinforcement extinction effect in rats: implications for dopamine involvement in food reward.Pharmacol. Biochem. Behav. 25, 813–821.

    PubMed  CAS  Article  Google Scholar 

  32. Ferre S, BB Fredholm, M Morelli, P Popoli and K Fuxe (1997) Adenosine-dopamine receptor-receptor interactions as an integrative mechanism in the basal ganglia.Trends Neurosci. 20, 482–487.

    PubMed  CAS  Article  Google Scholar 

  33. Fibiger HC (1978) Drugs and reinforcement mechanisms: a critical review of the catecholamine theory.Annu. Rev. Pharmacol. Toxicol. 18, 37–56.

    PubMed  CAS  Article  Google Scholar 

  34. Fibiger HC, DA Carter and AG Phillips (1976) Decreased intracranial self-stimulation after neuroleptics or 6-hydroxydopamine: evidence for mediation by motor deficits rather than by reduced reward.Psychopharmacol. 47, 21–27.

    CAS  Article  Google Scholar 

  35. Fouriezos G (1985) Sedation-induced jumping?Behav. Brain Sci. 8, 174–175.

    Google Scholar 

  36. Fouriezos G and RA Wise (1976) Pimozide-induced extinction of intracranial self-stimulation: response patterns rule out motor or performance deficits.Brain Res. 103, 377–380.

    PubMed  CAS  Article  Google Scholar 

  37. Fouriezos G, P Hansson and RA Wise (1978) Neuroleptic-induced attenuation of brain stimulation reward in rats.J. Comp. Physiol. Psychol. 92, 661–671.

    PubMed  CAS  Article  Google Scholar 

  38. Franklin KBJ (1978) Catecholamines and self-stimulation: reward and performance effects dissociated.Pharmacol. Biochem. Behav. 9, 813–820.

    PubMed  CAS  Article  Google Scholar 

  39. Franklin KBJ and SN McCoy (1979) Pimozide-induced extinction in rats: stimulus control of responding rules out motor deficit.Pharmacol. Biochem. Behav. 11, 71–75.

    PubMed  CAS  Article  Google Scholar 

  40. Freed WJ and RF Zec (1982) Criteria for ruling out sedation as an interpretation of neuroleptic effects.Behav. Brain Sci. 5, 57–59.

    Google Scholar 

  41. Gallistel CR and D Karras (1984) Pimozide and amphetamine have opposing effects on the reward summation function.Pharmacol. Biochem. Behav. 20, 73–77.

    PubMed  CAS  Article  Google Scholar 

  42. Gallistel CR, P Shizgal and J Yeomans (1981) A portrait of the substrate for self-stimulation.Psychol. Rev. 88, 228–273.

    PubMed  CAS  Article  Google Scholar 

  43. Gallistel CR, M Boytim, Y Gomita and L Klebanoff (1982) Does pimozide block the reinforcing effect of brain stimulation?Pharmacol. Biochem. Behav. 17, 769–781.

    PubMed  CAS  Article  Google Scholar 

  44. German DC and DM Bowden (1974) Catecholamine systems as the neural substrate for intracranial self-stimulation: a hypothesis.Brain Res. 73, 381–419.

    PubMed  CAS  Article  Google Scholar 

  45. Goeders NE and JE Smith (1983) Cortical dopaminergic involvement in cocaine reinforcement.Science 221, 773–775.

    PubMed  CAS  Article  Google Scholar 

  46. Goeders NE, SIDworkinand JE Smith(1986)Neuropharmacological assessment of cocaine self-administration into the medial pre-frontal cortex.Pharmacol. Biochem. Behav. 24, 1429–1440.

    PubMed  CAS  Article  Google Scholar 

  47. Grace AA (2000) The tonic/phasic model of dopamine system regulation and its implications for understanding alcohol and stimulant craving.Addiction 95, S119-S128.

    PubMed  Google Scholar 

  48. Gramling SE, SC Fowler and KR Collins (1984) Some effects of pimozide on nondeprived rats licking sucrose solutions in an anhedonia paradigm.Pharmacol. Biochem. Behav. 21, 617–624.

    PubMed  CAS  Article  Google Scholar 

  49. Greengard P (1976) Possible role for cyclic nucleotides and phosphorylated membrane proteins in postsynaptic actions of neurotransmitters.Nature 260, 101–108.

    PubMed  CAS  Article  Google Scholar 

  50. Grill HJ and R Norgren (1978) The taste reactivity test. II. Mimetic responses to gustatory stimuli in chronic thalamic and chronic decerebrate rats.Brain Res. 143, 281–297.

    PubMed  CAS  Article  Google Scholar 

  51. Gunne LM, E Änggard E and LE Jönsson (1972) Clinical trials with amphetamine-blocking drugs.Psychiatr. Neurol. Neurochirurg. 75, 225–226.

    CAS  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  53. Healy D (1989) Neuroleptics and psychic indifference: a review.J. Royal Soc. Med. 82, 615–619.

    CAS  Google Scholar 

  54. Heath RG (1963) Intracranial self-stimulation in man.Science 140, 394–396.

    PubMed  Article  Google Scholar 

  55. Heath RG (1972) Pleasure and brain activity in man.J. Nerv. Ment. Disord. 154, 3–18.

    CAS  Article  Google Scholar 

  56. Hollister LE, DT Eikenberry and S Raffel (1960) Chlorprom-azine in nonpsychotic patients with pulmonary tuberculosis.Am. Rev. Resp. Dis. 82, 562–566.

    Google Scholar 

  57. Hornykiewicz O (1979) Brain dopamine in Parkinson’s disease and other neurological disturbances, In:The Neurobiology of Dopamine (Horn AS, J Korf & BHC Westerink, Eds.) (Academic Press:New York), pp 633–653.

    Google Scholar 

  58. Howarth CI and JA Deutsch (1962) Drive decay: the cause of fast “extinction” of habits learned for brain stimulation.Science 137, 35–36.

    PubMed  CAS  Article  Google Scholar 

  59. Hyman SE, RC Malenka and EJ Nestler (2006) Neural mechanisms of addiction: the role of reward-related learning and memory.Annu. Rev. Neurosci. 29, 565–598.

    PubMed  CAS  Article  Google Scholar 

  60. Ikemoto S (2003) Involvement of the olfactory tubercle in cocaine reward: intracranial self-administration studies.J. Neurosci. 23, 9305–9511.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  62. Jönsson L, E Änggard and L Gunne L (1971) Blockade of intravenous amphetamine euphoria in man.Clin. Pharmacol. Ther. 12, 889–896.

    PubMed  Google Scholar 

  63. Katz LD (1982) Hedonic arousal, memory, and motivation.Behav. Brain Sci. 5, 60.

    Google Scholar 

  64. Kelleher RT and WH Morse (1968) Schedules using noxious stimuli. 3. Responding maintained with response produced electric shocks.J. Exp. Anal. Behav. 11, 819–838.

    PubMed  Article  Google Scholar 

  65. Koob GF (1982) The dopamine anhedonia hypothesis: a pharmacological phrenology.Behav. Brain Sci. 5, 63–64.

    Google Scholar 

  66. Kornetsky C (1985) Neuroleptic drugs may attenuate pleasure in the operant chamber, but in the schizophrenic’s head they may simply reduce motivational arousal.Behav. Brain Sci. 8, 176–177.

    Article  Google Scholar 

  67. Landauer TK (1969) Reinforcement as consolidation.Psychol. Rev. 76, 82–96.

    PubMed  CAS  Article  Google Scholar 

  68. Lepore M and KBJ Franklin (1992) Modelling drug kinetics with brain stimulation: dopamine antagonists increase self-stimulation.Pharmacol. Biochem. Behav. 41, 489–496.

    PubMed  CAS  Article  Google Scholar 

  69. Liebman J (1982) Understanding neuroleptics: From “anhedonia” to “neuroleptothesia”.Behav. Brain Sci. 5, 64–65.

    Google Scholar 

  70. Ljungberg T, P Apicella and W Schultz (1992) Responses of monkey dopamine neurons during learning of behavioral reactions.J. Neurophysiol. 67, 145–163.

    PubMed  CAS  Google Scholar 

  71. Mason ST, RJ Beninger, HC Fibiger and AG Phillips (1980) Pimozide-induced suppression of responding: evidence against a block of food reward.Pharmacol. Biochem. Behav. 12, 917–923.

    PubMed  CAS  Article  Google Scholar 

  72. Matthews RT and DC German (1984) Electrophysiological evidence for excitation of rat ventral tegmental area dopaminergic neurons by morphine.Neurosci. 11, 617–626.

    CAS  Article  Google Scholar 

  73. McFarland K and A Ettenberg (1995) Haloperidol differentially affects reinforcement and motivational processes in rats running an alley for intravenous heroin.Psychopharmacol. 122, 346–350.

    CAS  Article  Google Scholar 

  74. McFarland K and A Ettenberg (1998) Haloperidol does not affect motivational processes in an operant runway model of food-seeking behavior.Behav. Neurosci. 112, 630–635.

    PubMed  CAS  Article  Google Scholar 

  75. Mogenson GJ, DL Jones and A Ettenberg CY Yim (1980) From motivation to action: functional interface between the limbic system and the motor system.Prog. Neurobiol. 14, 69–97.

    PubMed  CAS  Article  Google Scholar 

  76. Morgan MJ (1974) Resistance to satiation.Animal Behav. 22, 449–466.

    Article  Google Scholar 

  77. Nauta WJH, A Ettenberg and VB Domesick (1978a) Crossroads of limbic and striatal circuitry: hypothalamo-nigral connections, In:Limbic Mechanisms (Livingston KE & O Hornykiewicz, Eds.) (Plenum Press:New York), pp 75–93.

    Google Scholar 

  78. Nauta WJH, GP Smith, RLM Faull and VB Domesick (1978b) Efferent connections and nigral afferents of the nucleus accumbens septi in the rat.Neurosci. 3, 385–401.

    CAS  Article  Google Scholar 

  79. Olds J (1956) Pleasure centers in the brain.Sci. Am. 195, 105–116.

    Google Scholar 

  80. Olds J (1959) Self-stimulation experiments and differentiated reward systems, In:Reticular Formation of the Brain (Jasper H, LD Proctor, RS Knighton, WC Noshay & RT Costello, Eds.) (Little, Brown and Company:Boston), pp 671–687.

    Google Scholar 

  81. Olds J and PM Milner (1954) Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain.J. Comp. Physiol. Psychol. 47, 419–427.

    PubMed  CAS  Article  Google Scholar 

  82. Olds ME and J Olds (1963) Approach-avoidance analysis of rat diencephalon.J. Comp. Neurol. 120, 259–295.

    PubMed  CAS  Article  Google Scholar 

  83. Olds J and ME Olds (1965) Drives, rewards, and the brain, In:New Directions in Psychology (TM Newcombe, Ed.) (Holt, Rinehart and Winston:New York), pp 327–410.

    Google Scholar 

  84. Olds J and RP Travis (1960) Effects of chlorpromazine, meprobamate, pentobarbital andmorphine on self-stimulation.J. Pharmacol. Exp. Ther. 128, 397–404.

    PubMed  CAS  Google Scholar 

  85. Pavlov IP (1928)Lectures on Conditioned Reflexes (International Publishers:New York).

    Google Scholar 

  86. Pecina S, KC Berridge and LA Parker (1997) Pimozide does not shift palatability: separation of anhedonia from sensorimotor suppression by taste reactivity.Pharmacol. Biochem. Behav. 58, 801–811.

    PubMed  CAS  Article  Google Scholar 

  87. Phillips AG and HC Fibiger (1973) Dopaminergic and noradrenergic substrates of positive reinforcement: differential effects of d- and l-amphetamine.Science 179, 575–577.

    PubMed  CAS  Article  Google Scholar 

  88. Phillips AG and FG LePiane (1980) Reinforcing effects of morphine microinjection into the ventral tegmental area.Pharmacol. Biochem. Behav. 12, 965–968.

    PubMed  CAS  Article  Google Scholar 

  89. Pickens R and WC Harris (1968) Self-administration of d-amphetamine by rats. Psychopharmacologia12, 158–163.

    PubMed  CAS  Article  Google Scholar 

  90. Quinlan MG, R Sharf, DY Lee, RA Wise and R Ranaldi (2004) Blockade of substantia nigra dopamine D1 receptors reduces intravenous cocaine reward in rats.Psychopharmacol. 175, 53–59.

    CAS  Google Scholar 

  91. Ranaldi R and RA Wise (2001) Blockade of D1 dopamine receptors in the ventral tegmental area decreases cocaine reward: possible role for dendritically released dopamine.J. Neurosci. 21, 5841–5846.

    PubMed  CAS  Google Scholar 

  92. Rech R (1982) Neurolepsis: anhedonia or blunting of emotional reactivity.Behav. Brain Sci. 5, 72–73.

    Google Scholar 

  93. Reynolds JN, BI Hyland and JR Wickens (2001) A cellular mechanism of reward-related learning. Nature413, 67–70.

    PubMed  CAS  Article  Google Scholar 

  94. Risner ME and BE Jones (1976) Role of noradrenergic and dopaminergic processes in amphetamine self-administration.Pharmacol. Biochem. Behav. 5, 477–482.

    PubMed  CAS  Article  Google Scholar 

  95. Risner ME and BE Jones (1980) Intravenous self-administration of cocaine and norcocaine by dogs.Psychopharmacol. 71, 83–89.

    CAS  Article  Google Scholar 

  96. Robbins D (1971) Partial reinforcement: a selective review of the alleyway literature since 1960.Psychol. Bull. 76, 415–431.

    Article  Google Scholar 

  97. Roberts DCS, ME Corcoran and HC Fibiger (1977) On the role of ascending catecholaminergic systems in intravenous self-administration of cocaine.Pharmacol. Biochem. Behav. 6, 615–620.

    PubMed  CAS  Article  Google Scholar 

  98. Robinson S, SM Sandstrom, VH Denenberg and RD Palmiter (2005) Distinguishing whether dopamine regulates liking, wanting, and/or learning about rewards.Behav. Neurosci. 119, 5–15.

    PubMed  CAS  Article  Google Scholar 

  99. Roll SK (1970) Intracranial self-stimulation and wakefulness: effect of manipulating ambient brain catecholamines.Science 168, 1370–1372.

    PubMed  CAS  Article  Google Scholar 

  100. 7Romo R and W Schultz (1990) Dopamine neurons of the monkey midbrain: contingencies of responses to active touch during self-initiated arm movements.J. Neurophysiol. 63, 592–606.

    PubMed  CAS  Google Scholar 

  101. Salamone JD and M Correa (2002) Motivational views of reinforcement: implications for understanding the behavioral functions of nucleus accumbens dopamine.Behav. Brain Res. 137, 3–25.

    PubMed  CAS  Article  Google Scholar 

  102. Salamone JD, MS Cousins and S Bucher (1994) Anhedonia or anergia? Effects of haloperidol and nucleus accumbens dopamine depletion on instrumental response selection in a T-maze cost/benefit procedure.Behav. Brain Res. 65, 221–229.

    PubMed  CAS  Article  Google Scholar 

  103. Salamone JD, MS Cousins and BJ Snyder (1997) Behavioral functions of nucleus accumbens dopamine: empirical and conceptual problems with the anhedonia hypothesis.Neurosci. Biobehav. Rev. 21, 341–359.

    PubMed  CAS  Article  Google Scholar 

  104. Salamone JD, M Correa, S Mingote and SM Weber (2003) Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: implications for studies of natural motivation, psychiatry, and drug abuse.J. Pharmacol. Exp. Ther. 305, 1–8.

    PubMed  CAS  Article  Google Scholar 

  105. Salamone JD, M Correa, SM Mingote and SM Weber (2005) Beyond the reward hypothesis: alternative functions of nucleus accumbens dopamine.Curr. Opin. Pharmacol. 5, 34–41.

    PubMed  CAS  Article  Google Scholar 

  106. Schiffmann SN, G Fisone, R Moresco, RA Cunha and S Ferré (2007) Adenosine A2A receptors and basal ganglia physiology. Prog. Neurobiol. 83(5) 277–292. Epub 2007 June 26.

    PubMed  CAS  Article  Google Scholar 

  107. Schultz W (1998) Predictive reward signal of dopamine neurons.J. Neurophysiol. 80, 1–27.

    PubMed  CAS  Google Scholar 

  108. Sclafani A and K Ackroff (1994) Glucose-and fructose-conditioned flavor preferences in rats: taste versus postingestive conditioning.Physiol. Behav. 56, 399–405.

    PubMed  CAS  Article  Google Scholar 

  109. Sem-Jacobsen CW (1959) Depth-electrographic observations in psychotic patients: a system related to emotion and behavior.Acta Psychiatr. Scand. Suppl.34, 412–416.

    Google Scholar 

  110. Skinner BF (1937) Two types of conditioned reflex: a reply to Konorski and Miller.J. Gen. Psychol. 16, 272–279.

    Google Scholar 

  111. Snyder SH, JJ Katims, Z Annau, RF Bruns and JW Daly (1981) Adenosine receptors and behavioral actions of methylxanthines.Proc. Natl. Acad. Sci. USA 78, 3260–3264.

    PubMed  CAS  Article  Google Scholar 

  112. Stein L (1962) Effects and interactions of imipramine, chlorpromazine, reserpine and amphetamine on self-stimulation: possible neurophysiological basis of depression, InRecent Advances in Biological Psychiaty (Wortis J, Ed.) (Plenum:New York), pp 288–308.

    Google Scholar 

  113. Stein L (1968) Chemistry of reward and punishment, In:Proceedings of the American College of NeuroPsychophar-macology (Efron DH, Ed.) (U.S. Government Printing Office:Washington, DC), pp 105–123.

    Google Scholar 

  114. Steiner JE (1973) The gustofacial response: observation on normal and anencephalic newborn infants.Symp. Oral Sensat. Percept. 4, 254–278.

    Google Scholar 

  115. Steiner JE (1974) Innate, discriminative human facial expressions to taste and smell stimulation.Ann. NY Acad. Sci. 237, 229–233.

    PubMed  CAS  Article  Google Scholar 

  116. Stretch R and GJ Gerber (1973) Drug-induced reinstatement of amphetamine self-administation behaviour in monkeys.Can. J. Psychol. 27, 168–177.

    PubMed  CAS  Google Scholar 

  117. Stricker EM and MJ Zigmond (1974) Effects on homeostasis of intraventricular injections of 6-hydroxydopamine in rats.J. Comp. Physiol. Psychol. 86, 973–994.

    PubMed  CAS  Article  Google Scholar 

  118. Stricker EM, MB Zimmerman, MI Friedman and MJ Zigmond (1977) Caffeine restores feeding response to 2-deoxy-D-glucose in 6-hydroxydopamine-treated rats.Nature 267, 174–175.

    PubMed  CAS  Article  Google Scholar 

  119. Teitelbaum P and AN Epstein (1962) The lateral hypothalamic syndrome: recovery of feeding and drinking after lateral hypothalamic lesions.Psychol. Rev. 69, 74–90.

    PubMed  CAS  Article  Google Scholar 

  120. Thorndike EL (1898) Animal intelligence: an experimental study of the associative processes in animals.Psychol. Monogr. 8, 1–109.

    Google Scholar 

  121. Thorndike EL (1911)Animal Intelligence (Macmillan:New York).

    Google Scholar 

  122. Tombaugh TN, J Tombaugh and H Anisman (1979) Effects of dopamine receptor blockade on alimentary behaviors: home cage food consumption, magazine training, operant acquisition, and performance.Psychopharmacol. 66, 219–225.

    CAS  Article  Google Scholar 

  123. Treit D and KC Berridge (1990) A comparison of benzodiazepine, serotonin, and dopamine agents in the taste-reactivity paradigm.Pharmacol. Biochem. Behav. 37, 451–456.

    PubMed  CAS  Article  Google Scholar 

  124. Ungerstedt U (1971) Adipsia and aphagia after 6-hydroxydopamine induced degeneration of the nigro-striatal dopamine system.Acta Physiol. Scand. Suppl.367, 95–122.

    Google Scholar 

  125. vanRossum JM, JB van der Schoot JB and JA Hurkmans (1962) Mechanism of action of cocaine and amphetamine in the brain.Experientia 18, 229–230.

    PubMed  CAS  Article  Google Scholar 

  126. Volkow ND and JM Swanson (2003) Variables that affect the clinical use and abuse of methylphenidate in the treatment of ADHD.Am. J. Psychiatry 160, 1909–1918.

    PubMed  Article  Google Scholar 

  127. White NM (1989) Reward or reinforcement: what’s the difference?Neurosci. Biobehav. Rev. 13, 181–186.

    PubMed  CAS  Article  Google Scholar 

  128. White NM and PM Milner (1992) The psychobiology of reinforcers.Annu. Rev. Psychol. 43, 443–471.

    PubMed  CAS  Article  Google Scholar 

  129. White NM and M Viaud (1991) Localized intracaudate dopamine D2 receptor activation during the post-training period improves memory for visual or olfactory conditioned emotional responses in rats.Behav. Neural Biol. 55, 255–269.

    PubMed  CAS  Article  Google Scholar 

  130. Wickens JR, JC Horvitz, RM Costa and S Killcross (2007) Dopaminergic mechanisms in actions and habits.J. Neurosci. 27, 8181–8183.

    PubMed  CAS  Article  Google Scholar 

  131. Wise CD and L Stein (1969) Facilitation of brain self-stimulation by central administration of norepinephrine.Science 163, 299–301.

    PubMed  CAS  Article  Google Scholar 

  132. Wise CD and L Stein (1970) Amphetamine: facilitation of behavior by augmented release of norepinephrine from the medial forebrain bundle,. In:Amphetamines and Related Compounds (Costa E and S Garattini, Eds.) (Raven Press:New York), pp 463–485.

    Google Scholar 

  133. Wise RA (1976) Moveable electrode for chronic brain stimulation in the rat.Physiol. Behav. 16, 105–106.

    PubMed  CAS  Article  Google Scholar 

  134. Wise RA (1978) Catecholamine theories of reward: a critical review.Brain Res. 152, 215–247.

    PubMed  CAS  Article  Google Scholar 

  135. Wise RA (1981) Intracranial self-stimulation: mapping against the lateral boundaries of the dopaminergic cells of the substantia nigra.Brain Res. 213, 190–194.

    PubMed  CAS  Article  Google Scholar 

  136. Wise RA (1982) Neuroleptics and operant behavior: the anhedonia hypothesis.Behav. Brain Sci. 5, 39–87.

    Google Scholar 

  137. Wise RA (1985) The anhedonia hypothesis: Mark III.Behav. Brain Sci. 8, 178–186.

    Google Scholar 

  138. Wise RA (1989) The brain and reward, In:The Neuropharmacological Basis of Reward (Liebmanand JM & SJ Cooper, Eds) (Oxford University Press:Oxford), pp 377–424.

    Google Scholar 

  139. Wise RA (1990) Drugs against pleasure.Curr. Contents 22, 20.

    Google Scholar 

  140. Wise RA (2002) Brain reward circuitry: insights from unsensed incentives.Neuron 36, 229–240.

    PubMed  CAS  Article  Google Scholar 

  141. Wise RA (2004) Dopamine, learning and motivation.Nat. Rev. Neurosci. 5, 483–494.

    PubMed  CAS  Article  Google Scholar 

  142. Wise RA and LM Colle (1984) Pimozide attenuates free feeding: best scores analysis reveals a motivational deficit.Psychopharmacol. 84, 446–451.

    CAS  Article  Google Scholar 

  143. Wise RA and L Raptis (1986) Effects of naloxone and pimozide on initiation and maintenance measures of free feeding.Brain Res. 368, 62–68.

    PubMed  CAS  Article  Google Scholar 

  144. Wise RA and HV Schwartz (1981) Pimozide attenuates acquisition of lever pressing for food in rats.Pharmacol. Biochem. Behav. 15, 655–656.

    PubMed  CAS  Article  Google Scholar 

  145. Wise RA, J Spindler, H de Wit and GJ Gerber (1978) Neuroleptic-induced “anhedonia” in rats: pimozide blocks reward quality of food.Science 201, 262–264.

    PubMed  CAS  Article  Google Scholar 

  146. Wise RA, A Murray and MA Bozarth (1990) Bromocriptine self-administration and bromocriptine-reinstatement of cocaine-trained and heroin-trained lever pressing in rats.Psychopharmacol. 100, 355–360.

    CAS  Article  Google Scholar 

  147. Yeomans JS, NT Maidment and BS Bunney (1988) Excitability properties of medial forebrain bundle axons of A9 and A10 dopamine cells.Brain Res. 450, 86–93.

    PubMed  CAS  Article  Google Scholar 

  148. Yokel RA and RA Wise (1975) Increased lever pressing for amphetamine after pimozide in rats: implications for a dopamine theory of reward.Science 187, 547–549.

    PubMed  CAS  Article  Google Scholar 

  149. Yokel RA and RA Wise (1976) Attenuation of intravenous amphetamine reinforcement by central dopamine blockade in rats.Psychopharmacol. 48, 311–318.

    CAS  Article  Google Scholar 

  150. Zigmond MJ and EM Stricker (1989) Animal models of parkinsonism using selective neurotoxins: clinical and basic implications.Int. Rev. Neurobiol. 31, 1–79.

    PubMed  CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Roy A. Wise.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Wise, R.A. Dopamine and reward: The anhedonia hypothesis 30 years on. neurotox res 14, 169–183 (2008). https://doi.org/10.1007/BF03033808

Download citation

Keywords

  • Dopamine
  • Reward
  • Reinforcement
  • Motivation
  • Anhedondia