Hedonic Impact, Reward Learning, Or Incentive Salience?
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Brain Research Reviews 28Ž. 1998 309±369 Full-length review What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Kent C. Berridge ), Terry E. Robinson 1 Department of Psychology, UniÕersity of Michigan, Ann Arbor, MI 48109-1109, USA Accepted 23 June 1998 Abstract What roles do mesolimbic and neostriatal dopamine systems play in reward? Do they mediate the hedonic impact of rewarding stimuli? Do they mediate hedonic reward learning and associatiÕe prediction? Our review of the literature, together with results of a new study of residual reward capacity after dopamine depletion, indicates the answer to both questions is `no'. Rather, dopamine systems may mediate the incentiÕe salience of rewards, modulating their motivational value in a manner separable from hedonia and reward learning. In a study of the consequences of dopamine loss, rats were depleted of dopamine in the nucleus accumbens and neostriatum by up to 99% using 6-hydroxydopamine. In a series of experiments, we applied the `taste reactivity' measure of affective reactionsŽ gapes, etc...Ž.. to assess the capacity of dopamine-depleted rats for: 1 normal affect hedonic and aversive reactions , 2 modulation of hedonic affect by associative learningŽ.. taste aversion conditioning , and 3 hedonic enhancement of affect by non-dopaminergic pharmacological manipulation of palatabilityŽ. benzodiazepine administration . We found normal hedonic reaction patterns to sucrose vs. quinine, normal learning of new hedonic stimulus valuesŽ. a change in palatability based on predictive relations , and normal pharmacological hedonic enhancement of palatability. We discuss these results in the context of hypotheses and data concerning the role of dopamine in reward. We review neurochemical, electrophysiological, and other behavioral evidence. We conclude that dopamine systems are not needed either to mediate the hedonic pleasure of reinforcers or to mediate predictive associations involved in hedonic reward learning. We conclude instead that dopamine may be more important to incentiÕe salience attributions to the neural representations of reward-related stimuli. Incentive salience, we suggest, is a distinct component of motivation and reward. In other words, dopamine systems are necessary for `wanting' incentiÕes, but not for `liking' them or for learning new `likes' and `dislikes'. q 1998 Elsevier Science B.V. All rights reserved. Keywords: Neostriatum; Nucleus accumbens; Substantia nigra; Tegmentum; Mesolimbic; Nigrostriatal; Mesotelencephalic mesostriatal; Dopamine; 6-hydroxydopamine; Lateral hypothalamus; Brain; Reinforcement; Motivation; Self-administration; Conditioning; Reward; Emotion; Palatability; Pleasure; Feeding; Food intake appetitive behavior; Consummatory behavior; Affect; Anhedonia; Hedonic; Diazepam; Conditioned taste aversion; Taste; Taste reactivity; Aphagia; Aversion; Appetite; Ingestion; Neurotransmitters; Substance-related disorders; Addiction Contents 1. Introduction ....................................................................... 311 2. Evidence for a role of dopamine in reward ....................................................... 311 2.1. Nature of dopamine's role in reward: hedonia, incentive salience or reward learning? ............................. 312 3. Brain manipulations of behavior for revealing dopamine's function in reward .................................... 315 3.1. Traditional measures of reward: instrumental behavior and choiceŽ. `wanting' ................................. 316 ) Corresponding author. Fax: q1-734-763-7480; E-mail: berridge@umich.edu 1 E-mail: ter@umich.edu. 0165-0173r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved. PII: S0165-0173Ž. 98 00019-8 310 K.C. Berridge, T.E. RobinsonrBrain Research ReÕiews 28() 1998 309±369 3.2. Measures of reward based on affective reactionsŽ. `liking' ............................................ 316 3.3. Dopamine manipulations dissociate `wanting' vs. `liking' ............................................ 317 4. Effects of mesolimbic and neostriatal dopamine depletion on subcomponents of reward ............................... 317 4.1. General experimental approach .......................................................... 318 5. Experiment 1: Unconditioned affective reactions to sucrose or quinine ........................................ 318 5.1. Methods ...................................................................... 318 5.2. Results ....................................................................... 320 5.3. Discussion of Experiment 1 ............................................................ 321 6. Experiment 2: Modulation of affective reactions by taste aversion conditioning ................................... 323 6.1. Methods ...................................................................... 323 6.2. Results ....................................................................... 324 6.3. Discussion of Experiment 2 ............................................................ 324 7. Experiment 3: enhancement of hedonic reaction patterns by diazepam ........................................ 324 7.1. Methods ...................................................................... 326 7.2. Results ....................................................................... 326 7.3. Discussion of Experiment 3 ............................................................ 327 8. General discussion.................................................................... 328 8.1. Unconditioned hedonic reactivity ......................................................... 328 8.2. Palatability modulation............................................................... 328 9. Dopamine and reward: choosing among competing explanations ........................................... 328 9.1. Not motor deficits ................................................................. 328 9.2. Not anhedonia ................................................................... 328 9.3. Not reward learning? ................................................................ 330 9.4. Loss of incentive salience?............................................................. 332 10. Conditioned dopamine activity: re-examination of implications for incentive salience and reward learning hypotheses ............... 335 10.1. Predictions of `reward learning' vs. `incentive salience' hypotheses of dopamine function .......................... 335 11. Effects of dopamine antagonists: a re-examination of anhedonia, incentive salience or anergia explanations .................... 338 11.1. Comparing dopamine antagonist effects on hedonic activation ......................................... 338 11.2. Affective taste reactivity and dopamine antagonists: sensorimotor anergia but not anhedonia ......................... 339 11.3. Subjective hedonic ratings by humans and dopamine antagonists: conscious pleasure persists ........................ 339 12. Phenomena that don't fit: problems for the incentive salience model?......................................... 340 12.1. Euphorigenic dopaminergic drugs ........................................................ 340 12.2. Paradoxical effects of dopamine antagonists ................................................... 341 12.3. The `Two Motivational Systems' hypothesisŽ. Bechara et al. .......................................... 345 13. Caveats to the `Incentive Salience' hypothesis ..................................................... 348 13.1. Beyond reward to aversion ............................................................ 348 13.2. Beyond the dopamine synapse .......................................................... 349 14. General conclusion ................................................................... 350 15. Addendum 1: Taste reactivity patterns as a measure of `liking' ............................................ 350 15.1. Insufficiency of alternative interpretations of affective taste reactivity ..................................... 351 15.2. Conclusion: Affective reaction patterns reflect hedonic impact of `liked' stimulus............................... 354 16. Addendum 2: Measuring cognitive expectations of reward in animalsŽ. studies of incentive learning by Dickinson and Balleine ......... 355 17. Note added in proof ................................................................... 356 Acknowledgements...................................................................... 356 References .......................................................................... 356 K.C. Berridge, T.E. RobinsonrBrain Research ReÕiews 28() 1998 309±369 311 Appearances to the mind are of four kinds. Things quantified by electrophysiological, microdialysis, or either are what they appear to be; or they neither are, voltammetric measures, is triggered in animals by encoun- nor appear to be; or they are, and do not appear to be; ters with food, sex, drugs of abuse, electrical stimulation at or they are not, and yet appear to be. Rightly to aim in brain sites that support self-stimulation, and by secondary all these cases is the wise man's task. reinforcers for these incentivesw 5,52,159,233,259,260,263, 283,300,301,344±346,359,401,403±405,425,478x . In hu- Epictetus Ž60 A.D. Translation: Elizabeth Carterwx 142 mans, presentation of rewards such as cocaine, drug-asso- Ð Thomas Higginsonwx 143 . ciated stimuli, and even a video gameŽ. `tank combat' , has similarly been reported in PET and fMRI imaging studies to modulate activity in