The role of dopamine in the accumbens core in the expression of pavlovian-conditioned responses

European Journal of Neuroscience

Volumn 36, Issue 4, 2012, Pages 2521-2532

  Saunders, Benjamin T ^a   Robinson, Terry E ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Goal tracking; Learning; Motivation; Rat; Sign tracking

Indexed keywords

DOPAMINE; FLUPENTIXOL;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; CONDITIONED REFLEX; CONTROLLED STUDY; DRUG MEGADOSE; HISTOPATHOLOGY; HUMAN; LATENT PERIOD; LEARNING; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROBABILITY; PROTEIN EXPRESSION; RAT; REINFORCEMENT; REWARD; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; TOPOGRAPHY;

ANIMALS; CONDITIONING, CLASSICAL; DOPAMINE; DOPAMINE ANTAGONISTS; FLUPENTHIXOL; MALE; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84865314101     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08217.x     Document Type: Article

References (73)

1. Balleine, B.W. & Dickinson, A. (1998) Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology, 37, 407-419.
2. Bayer, H.M. & Glimcher, P.W. (2005) Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron, 47, 129-141.
3. Berridge, K.C. (2001) Reward learning: reinforcement, incentives, and expectations. In Medin, D.L. (Eds), Psychology of Learning and Motivation: Advances in Research and Theory. Academic Press, San Diego, CA, pp. 223-278.
4. Berridge, K.C. (2007) The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology, 191, 391-431.
5. Berridge, K.C. (2012) From prediction error to incentive salience: mesolimbic computation of reward motivation. Eur. J. Neurosci., 35, 1124-1143.
6. Berridge, K.C. & Robinson, T.E. (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Rev., 28, 309-369.
7. Berridge, K.C. & Robinson, T.E. (2003) Parsing reward. Trends Neurosci., 26, 507-513.
8. Bindra, D. (1978) How adaptive behavior is produced: a perceptual-motivation alternative to response reinforcement. Behav. Brain Sci., 1, 41-91.
9. Blaiss, C.A. & Janak, P.H. (2009) The nucleus accumbens core and shell are critical for the expression, but not the consolidation, of Pavlovian conditioned approach. Behav. Brain Res., 200, 22-32.
10. Boakes, R.A. (1977) Performance on learning to associate a stimulus with positive reinforcement. In Davis, H. & Hurwitz, H. (Eds), Operant-Pavlovian Interactions. Earlbaum, Hillsdale, NJ, pp. 67-97.
11. Bromberg-Martin, E.S., Matsumoto, M. & Hikosaka, O. (2010) Dopamine in motivational control: rewarding, aversive, and alerting. Neuron, 68, 815-834.
12. Cardinal, R.N., Parkinson, J.A., Hall, J. & Everitt, B.J. (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci. Biobehav. Rev., 26, 321-352.
13. Chang, S.E., Wheeler, D.S. & Holland, P.C. (2012) Roles of nucleus accumbens and basolateral amygdala in autoshaped lever pressing. Neurobiol. Learn. Mem., 97, 441-451.
14. Cleland, G.G. & Davey, G.C. (1983) Autoshaping in the rat: the effects of localizable visual and auditory signals for food. J. Exp. Anal. Behav., 40, 47-56.
15. Cohen, J.Y., Haesler, S., Vong, L., Lowell, B.B. & Uchida, N. (2012) Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature, 482, 85-88.
16. Danna, C.L. & Elmer, G.I. (2010) Disruption of conditioned reward association by typical and atypical antipsychotics. Pharmacol. Biochem. Behav., 96, 40-47.
17. Daw, N.D., Niv, Y. & Dayan, P. (2005) Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nat. Neurosci., 8, 1704-1711.
18. Day, J.J., Roitman, M.F., Wightman, R.M. & Carelli, R.M. (2007) Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens. Nat. Neurosci., 10, 1020-1028.
19. Dayan, P. & Balleine, B.W. (2002) Reward, motivation, and reinforcement learning. Neuron, 36, 285-298.
20. Di Ciano, P., Cardinal, R.N., Cowell, R.A., Little, S.J. & Everitt, B.J. (2001) Differential involvement of NMDA, AMPA/kainate, and dopamine receptors in the nucleus accumbens core in the acquisition and performance of Pavlovian approach behavior. J. Neurosci., 21, 9471-9477.
21. Dickinson, A. & Balleine, B. (1994) Motivational control of goal-directed action. Anim. Learn. Behav., 22, 1-18.
22. Dickinson, A. & Balleine, B. (2002) The role of learning in the operation of motivational systems. In Pashler, H. & Gallistel, R. (Eds), Steven's Handbook of Experimental Psychology: Learning, Motivation, and Emotion. Wiley, New York, pp. 497-533.
23. Dickinson, A., Smith, J. & Mirenowicz, J. (2000) Dissociation of pavlovian and instrumental incentive learning under dopamine antagonists. Behav. Neurosci., 114, 468-483.
24. Difeliceantonio, A.G. & Berridge, K.C. (2012) Which cue to 'want'? Opioid stimulation of central amygdala makes goal-trackers show stronger goal-tracking, just as sign-trackers show stronger sign-tracking Behav. Brain Res., 230, 399-408.
25. Fields, H.L., Hjelmstad, G.O., Margolis, E.B. & Nicola, S.M. (2007) Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu. Rev. Neurosci., 30, 289-316.
26. Flagel, S.B., Watson, S.J., Robinson, T.E. & Akil, H. (2007) Individual differences in the propensity to approach signals vs goals promote different adaptations in the dopamine system of rats. Psychopharmacology, 191, 599-607.
27. Flagel, S.B., Akil, H. & Robinson, T.E. (2009) Individual differences in the attribution of incentive salience to reward-related cues: implications for addiction. Neuropharmacology, 56, 139-148.
28. Flagel, S.B., Cameron, C.M., Pickup, K.N., Watson, S.J., Akil, H. & Robinson, T.E. (2011a) A food predictive cue must be attributed with incentive salience for it to induce c-fos mRNA expression in cortico-striatal-thalamic brain regions. Neuroscience, 196, 80-96.
29. Flagel, S.B., Clark, J.J., Robinson, T.E., Mayo, L., Czuj, A., Willuhn, I., Akers, C.A., Clinton, S.M., Phillips, P.E. & Akil, H. (2011b) A selective role for dopamine in stimulus-reward learning. Nature, 469, 53-57.
30. Glascher, J., Daw, N., Dayan, P. & O'Doherty, J.P. (2010) States versus rewards: dissociable neural prediction error signals underlying model-based and model-free reinforcement learning. Neuron, 66, 585-595.
31. Han, J.S., McMahan, R.W., Holland, P. & Gallagher, M. (1997) The role of an amygdalo-nigrostriatal pathway in associative learning. J. Neurosci., 17, 3913-3919.
32. Hearst, E. & Jenkins, H. (1974) Sign-tracking: The Stimulus-Reinforcer Relation and Directed Action. Monograph of the Psychonomic Society, Austin.
33. Holland, P.C. (1977) Conditioned stimulus as a determinant of the form of the Pavlovian conditioned response. J. Exp. Psychol. Anim. Behav. Process., 3, 77-104.
34. Ikemoto, S. & Panksepp, J. (1999) The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res. Brain Res. Rev., 31, 6-41.
35. Konorski, J. (1967) Integrative Activity of the Brain: an Interdisciplinary Approach. University of Chicago Press, Chicago, IL.
36. Lammel, S., Ion, D.I., Roeper, J. & Malenka, R.C. (2011) Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron, 70, 855-862.
37. Lex, B. & Hauber, W. (2010) The role of nucleus accumbens dopamine in outcome encoding in instrumental and Pavlovian conditioning. Neurobiol. Learn. Mem., 93, 283-290.
38. Lomanowska, A.M., Lovic, V., Rankine, M.J., Mooney, S.J., Robinson, T.E. & Kraemer, G.W. (2011) Inadequate early social experience increases the incentive salience of reward-related cues in adulthood. Behav. Brain Res., 220, 91-99.
39. Lovic, V., Saunders, B.T., Yager, L.M. & Robinson, T.E. (2011) Rats prone to attribute incentive salience to reward cues are also prone to impulsive action. Behav. Brain Res., 223, 255-261.
40. Mahler, S.V. & Berridge, K.C. (2009) Which cue to "want?" Central amygdala opioid activation enhances and focuses incentive salience on a prepotent reward cue. J. Neurosci., 29, 6500-6513.
41. McClure, S.M., Daw, N.D. & Montague, P.R. (2003) A computational substrate for incentive salience. Trends Neurosci., 26, 423-428.
42. Meyer, P.J., Ma, S.T. & Robinson, T.E. (2012a) A cocaine cue is more preferred and evokes more frequency-modulated 50-kHz ultrasonic vocalizations in rats prone to attribute incentive salience to a food cue. Psychopharmacology, 219, 999-1009.
43. Meyer, P.J., Lovic, V., Saunders, B.T., Yager, L.M., Flagel, S.B., Morrow, J.D. & Robinson, T.E. (2012b) Quantifying individual variation in the propensity to attribute incentive salience to reward cues. PLoS ONE, 7, e38987.
44. Montague, P.R., Dayan, P. & Sejnowski, T.J. (1996) A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J. Neurosci., 16, 1936-1947.
45. Pan, W.X., Schmidt, R., Wickens, J.R. & Hyland, B.I. (2005) Dopamine cells respond to predicted events during classical conditioning: evidence for eligibility traces in the reward-learning network. J. Neurosci., 25, 6235-6242.
46. Paxinos, G. & Watson, C. (2007) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York.
47. Phillips, A.G., McDonald, A.C. & Wilkie, D.M. (1981) Disruption of autoshaped responding to a signal of brain-stimulation reward by neuroleptic drugs. Pharmacol. Biochem. Behav., 14, 543-548.
48. Robbins, T.W. & Everitt, B.J. (1992) Functions of dopamine in the dorsal and ventral striatum. Sem. Neurosci, 4, 119-127.
49. Robinson, T.E. & Berridge, K.C. (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Rev., 18, 247-291.
50. Robinson, T.E. & Flagel, S.B. (2009) Dissociating the predictive and incentive motivational properties of reward-related cues through the study of individual differences. Biol. Psychiatry, 65, 869-873.
51. Salamone, J.D., Correa, M., Farrar, A. & Mingote, S.M. (2007) Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology, 191, 461-482.
52. Salamone, J.D., Correa, M., Nunes, E.J., Randall, P.A. & Pardo, M. (2012) The behavioral pharmacology of effort-related choice behavior: dopamine, adenosine and beyond. J. Exp. Anal. Behav., 97, 125-146.
53. Saunders, B.T. & Robinson, T.E. (2010) A cocaine cue acts as an incentive stimulus in some but not others: implications for addiction. Biol. Psychiatry, 67, 730-736.
54. Saunders, B.T. & Robinson, T.E. (2011) Individual variation in the motivational properties of cocaine. Neuropsychopharmacol., 36, 1668-1676.
55. Schultz, W., Dayan, P. & Montague, P.R. (1997) A neural substrate of prediction and reward. Science, 275, 1593-1599.
56. Shiner, T., Seymour, B., Wunderlich, K., Hill, C., Bhatia, K.P., Dayan, P. & Dolan, R.J. (2012) Dopamine and performance in a reinforcement learning task: evidence from Parkinson's disease. Brain, doi:10.1093/brain/aws1083 [Epub ahead of print].
57. Smith, K.S., Berridge, K.C. & Aldridge, J.W. (2011) Disentangling pleasure from incentive salience and learning signals in brain reward circuitry. Proc. Natl. Acad. Sci. USA, 108, E255-E264.
58. Sutton, R.S. (1988) Learning to predict by the methods of temporal differences. Machine Learn., 3, 9-44.
59. Sutton, R.S. & Barto, A.G. (1998) Reinforcement Learning: An Introduction. MIT Press, Cambridge, MA.
60. Tindell, A.J., Berridge, K.C., Zhang, J., Pecina, S. & Aldridge, J.W. (2005) Ventral pallidal neurons code incentive motivation: amplification by mesolimbic sensitization and amphetamine. Eur. J. Neurosci., 22, 2617-2634.
61. Tindell, A.J., Smith, K.S., Berridge, K.C. & Aldridge, J.W. (2009) Dynamic computation of incentive salience: "wanting" what was never "liked". J. Neurosci., 29, 12220-12228.
62. Toates, F. (1986) Motivational Systems. Cambridge University Press, Cambridge, UK.
63. Tolman, E.C. (1948) Cognitive maps in rats and men. Psychol. Rev., 55, 189-208.
64. Verbeke, G. (2009) Linear Mixed Models for Longitudinal Data. Springer, New York.
65. Wassum, K., Ostlund, S., Maidment, N. & Balleine, B. (2009) Distinct opioid circuits determine the palatability and the desirability of rewarding events. Proc. Natl. Acad. Sci. USA, 106, 12512-12517.
66. Wassum, K.M., Ostlund, S.B., Balleine, B.W. & Maidment, N.T. (2011) Differential dependence of Pavlovian incentive motivation and instrumental incentive learning processes on dopamine signaling. Learn. Mem., 18, 475-483.
67. Wise, R.A., Spindler, J., deWit, H. & Gerberg, G.J. (1978) Neuroleptic-induced "anhedonia" in rats: pimozide blocks reward quality of food. Science, 201, 262-264.
68. Witten, I.B., Steinberg, E.E., Lee, S.Y., Davidson, T.J., Zalocusky, K.A., Brodsky, M., Yizhar, O., Cho, S.L., Gong, S., Ramakrishnan, C., Stuber, G.D., Tye, K.M., Janak, P.H. & Deisseroth, K. (2011) Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron, 72, 721-733.
69. Wyvell, C.L. & Berridge, K.C. (2001) Incentive sensitization by previous amphetamine exposure: Increased cue-triggered "wanting" for sucrose reward. J. Neurosci., 21, 7831-7840.
70. Yager, L.M. & Robinson, T.E. (2010) Cue-induced reinstatement of food seeking in rats that differ in their propensity to attribute incentive salience to food cues. Behav. Brain Res., 214, 30-34.
71. Yin, H., Zhuang, X. & Balleine, B. (2006) Instrumental learning in hyperdopaminergic mice. Neurobiol. Learn. Mem., 85, 283-288.
72. Zhang, J., Berridge, K.C., Tindell, A.J., Smith, K.S. & Aldridge, J.W. (2009) A neural computational model of incentive salience. PLoS Comput. Biol., 5, e1000437.
73. Zhang, J., Berridge, K.C. & Aldridge, J.W. (2012) Computational models of incentive-sensitization in addiction: dynamic limbic transformation of learning into motivation. In Gutkin, B. & Ahmed, S.H. (Eds), Computational Neuroscience of Drug Addiction. Springer, New York, pp. 189-203.