Cue-evoked cocaine "craving": Role of dopamine in the accumbens core

Journal of Neuroscience

Volumn 33, Issue 35, 2013, Pages 13989-14000

  Saunders, Benjamin T ^a,b   Yager, Lindsay M ^a   Robinson, Terry E ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHETAMINE; ANTIBIOTIC AGENT; CARPROFEN; COCAINE; DOPAMINE; FLUPENTIXOL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; CONTROLLED STUDY; DRUG SEEKING BEHAVIOR; DRUG SELF ADMINISTRATION; HISTOLOGY; MALE; MICROINJECTION; NONHUMAN; NUCLEUS ACCUMBENS; PAIN; PRIORITY JOURNAL; RAT; TRAINING; WITHDRAWAL SYNDROME;

AMPHETAMINE; ANIMALS; COCAINE; COCAINE-RELATED DISORDERS; CUES; DOPAMINE; DOPAMINE ANTAGONISTS; DRUG-SEEKING BEHAVIOR; MALE; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY; REWARD;

EID: 84883024809     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0450-13.2013     Document Type: Article

References (98)

1. Aragona BJ, Day JJ, Roitman MF, Cleaveland NA, Wightman RM, Carelli RM (2009) Regional specificity in the real-time development of phasic dopamine transmission patterns during acquisition of a cue-cocaine association in rats. Eur J Neurosci 30:1889-1899. CrossRef Medline
2. Barker JM, Torregrossa MM, Taylor JR (2012) Low prefrontal PSA-NCAM confers risk for alcoholism-related behavior. Nat Neurosci 15:1356-1358. CrossRef Medline
3. Barnea-Ygael N, Yadid G, Yaka R, Ben-Shahar O, Zangen A (2012) Cueinduced reinstatement of cocaine seeking in the rat "conflict model": effect of prolonged home-cage confinement. Psychopharmacology 219: 875-883. CrossRef Medline
4. Berridge KC (2007) The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berl) 191:391-431. CrossRef Medline
5. Berridge KC (2012) From prediction error to incentive salience: mesolimbic computation of reward motivation. Eur J Neurosci 35:1124-1143. CrossRef Medline
6. Bertz J, Woods J (2013) Acquisition of responding with a remifentanilassociated conditioned reinforcer in the rat. Psychopharmacology. Advance online publication. doi:10.1007/s00213-013-3102-0. CrossRef Medline
7. Bindra D (1978) How adaptive behavior is produced: a perceptualmotivation alternative to response reinforcement. Behav Brain Sci 1:41-91. Cross Ref
8. Boileau I, Dagher A, Leyton M, Welfeld K, Booij L, Diksic M, Benkelfat C (2007) Conditioned dopamine release in humans: a positron emission tomography [11C]raclopride study with amphetamine. J Neurosci 27: 3998-4003. CrossRef Medline
9. Bossert J, Marchant N, Calu D, Shaham Y (2013) The reinstatement model of drug relapse: recent neurobiological findings, emerging research topics, and translational research. Psychopharmacology. Advance online publication. doi:10.1007/s00213-013-3120-y. CrossRef Medline
10. Cardinal RN, Parkinson JA, Hall J, Everitt BJ (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26:321-352. CrossRef Medline
11. Carter BL, Tiffany ST (1999) Meta-analysis of cue-reactivity in addiction research. Addiction 94:327-340. CrossRef Medline
12. Childress AR, Mozley PD, McElgin W, Fitzgerald J, Reivich M, O'Brien CP (1999) Limbic activation during cue-induced cocaine craving. Am J Psychiatry 156:11-18. Medline
13. Childress AR, Ehrman RN, Wang Z, Li Y, Sciortino N, Hakun J, Jens W, Suh J, Listerud J, Marquez K, Franklin T, Langleben D, Detre J, O'Brien CP (2008) Prelude to passion: limbic activation by "unseen" drug and sexual cues. PLo S One 3:e1506. CrossRef Medline
14. Clark JJ, Collins AL, Sanford CA, Phillips PE (2013) Dopamine encoding of pavlovian incentive stimuli diminishes with extended training. J Neurosci 33:3526-3532. CrossRef Medline
15. Collins GT, Cunningham AR, Chen J, Wang S, Newman AH, Woods JH (2012) Effects of pramipexole on the reinforcing effectiveness of stimuli that were previously paired with cocaine reinforcement in rats. Psychopharmacology (Berl) 219:123-135. CrossRef Medline
16. Cooper A, Barnea-Ygael N, Levy D, Shaham Y, Zangen A (2007) A conflict rat model of cue-induced relapse to cocaine seeking. Psychopharmacology 194:117-125. CrossRef Medline
17. Corbit LH, Janak PH (2007) Ethanol-associated cues produce general pavlovian-instrumental transfer. Alcohol Clin Exp Res 31:766-774. CrossRef Medline
18. Crombag HS, Badiani A, Maren S, Robinson TE (2000) The role of contextual versus discrete drug-associated cues in promoting the induction of psychomotor sensitization to intravenous amphetamine. Behav Brain Res 116:1-22. CrossRef Medline
19. Deroche-Gamonet V, Piat F, Le Moal M, Piazza PV (2002) Influence of cue-conditioning on acquisition, maintenance and relapse of cocaine intravenous self-administration. Eur J Neurosci 15:1363-1370. CrossRef Medline
20. de Wit H, Stewart J (1981) Reinstatement of cocaine-reinforced responding in the rat. Psychopharmacology 75:134-143. CrossRef Medline
21. Di Ciano P, Cardinal RN, Cowell RA, Little SJ, Everitt BJ (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. Medline
22. Dickinson A, Smith J, Mirenowicz J (2000) Dissociation of pavlovian and instrumental incentive learning under dopamine antagonists. Behav Neurosci 114:468-483. CrossRef Medline
23. Ehrman RN, Robbins SJ, Childress AR, O'Brien CP (1992) Conditionedresponses to cocaine-related stimuli in cocaine abuse patients. Psychopharmacology 107:523-529. CrossRef Medline
24. Epstein DH, Preston KL (2003) The reinstatement model and relapse prevention: a clinical perspective. Psychopharmacology 168:31-41. CrossRef Medline
25. Epstein DH, Preston KL, Stewart J, Shaham Y (2006) Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure. Psychopharmacology 189:1-16. CrossRef Medline
26. Ersche KD, Bullmore ET, Craig KJ, Shabbir SS, Abbott S, Mü ller U, Ooi C, Suckling J, Barnes A, Sahakian BJ, Merlo-Pich EV, Robbins TW (2010) Influence of compulsivity of drug abuse on dopaminergic modulation of attentional bias in stimulant dependence. Arch Gen Psychiatry 67:632-644. CrossRef Medline
27. Estes WK (1943) Discriminative conditioning. I. A discriminative property of conditioned anticipation. J Exp Psychol 32:150-155. Cross Ref
28. Estes WK (1948) Discriminative conditioning. II. Effects of a Pavlovian conditioned stimulus upon a subsequently established operant response. J Exp Psychol 38:173-177. CrossRef Medline
29. Fischman MW (1989) Relationship between self-reported drug effects and their reinforcing effects: studies with stimulant drugs. NIDA Res Monogr 92:211-230. Medline
30. Fischman MW, Foltin RW (1992) Self-administration of cocaine by humans: a laboratory perspective. Ciba Found Symp 166:165-173. Medline
31. Flagel SB, Watson SJ, Robinson TE, Akil H (2007) Individual differences in the propensity to approach signals vs goals promote different adaptations in the dopamine system of rats. Psychopharmacology (Berl) 191:599-607. CrossRef Medline
32. Flagel SB, Akil H, Robinson TE (2009) Individual differences in the attribution of incentive salience to reward-related cues: implications for addiction. Neuropharmacology 56:139-148. CrossRef Medline
33. Flagel SB, Robinson TE, Clark JJ, Clinton SM, Watson SJ, Seeman P, Phillips PE, Akil H (2010) An animal model of genetic vulnerability to behavioral disinhibition and responsiveness to reward-related cues: implications for addiction. Neuropsychopharmacology 35:388-400. CrossRef Medline
34. Flagel SB, Cameron CM, Pickup KN, Watson SJ, Akil H, Robinson TE (2011a) A food predictive cue must be attributed with incentive salience for it to induce c-fos m RNA expression in cortico-striatal-thalamic brain regions. Neuroscience 196:80-96. CrossRef Medline
35. Flagel SB, Clark JJ, Robinson TE, Mayo L, Czuj A, Willuhn I, Akers CA, Clinton SM, Phillips PE, Akil H (2011b) A selective role for dopamine in stimulus-reward learning. Nature 469:53-57. CrossRef Medline
36. Franken IH, Hendriks VM, Stam CJ, Van den Brink W (2004) A role for dopamine in the processing of drug cues in heroin dependent patients. Eur Neuropsychopharmacol 14:503-508. CrossRef Medline
37. Franklin TR, Lohoff FW, Wang Z, Sciortino N, Harper D, Li Y, Jens W, Cruz J, Kampman K, Ehrman R, Berrettini W, Detre JA, O'Brien CP, Childress AR (2009) DAT genotype modulates brain and behavioral responses elicited by cigarette cues. Neuropsychopharmacology 34:717-728. CrossRef Medline
38. Fuchs RA, Branham RK, See RE (2006) Different neural substrates mediate cocaine seeking after abstinence versus extinction training: a critical role for the dorsolateral caudate-putamen. J Neurosci 26:3584-3588. CrossRef Medline
39. Grimm JW, Kruzich PJ, See RE (2000) Contingent access to stimuli associated with cocaine self-administration is required for reinstatement of drug-seeking behavior. Psychobiology 28:383-386.
40. Grimm JW, Hope BT, Wise RA, Shaham Y (2001) Neuroadaptation-incubation of cocaine craving after withdrawal. Nature 412:141-142. CrossRef Medline
41. Hall J, Parkinson JA, Connor TM, Dickinson A, Everitt BJ (2001) Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour. Eur J Neurosci 13:1984-1992. CrossRef Medline
42. Hester R, Garavan H (2004) Executive dysfunction in cocaine addiction: evidence for discordant frontal, cingulate, and cerebellar activity. J Neurosci 24:11017-11022. CrossRef Medline
43. Hill RT (1970) Facilitation of conditioned reinforcement as a mechanism of psychomotor stimulation. In: Amphetamine and related compounds (Costa E, Garattini S, eds), pp 781-795. New York: Raven.
44. Hitchcott PK, Harmer CJ, Phillips GD (1997) Enhanced acquisition of discriminative approach following intra-amygdala d-amphetamine. Psychopharmacology 132:237-246. CrossRef Medline
45. Hitsman B, MacKillop J, Lingford-Hughes A, Williams TM, Ahmad F, Adams S, Nutt DJ, Munafo MR (2008) Effects of acute tyrosine/phenylalanine depletion on the selective processing of smoking-related cues and the relative value of cigarettes in smokers. Psychopharmacology (Berl) 196: 611-621. CrossRef Medline
46. Holden JM, Peoples LL (2010) Effects of acute amphetamine exposure on two kinds of Pavlovian approach behavior. Behav Brain Res 208:270-273. CrossRef Medline
47. Hutchison KE, La Chance H, Niaura R, Bryan A, Smolen A (2002) The DRD4 VNTR polymorphism influences reactivity to smoking cues. J Abnorm Psychol 111:134-143. CrossRef Medline
48. 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. CrossRef Medline
49. Ito R, Hayen A (2011) Opposing roles of nucleus accumbens core and shell dopamine in the modulation of limbic information processing. J Neurosci 31:6001-6007. CrossRef Medline
50. Jaffe JH, Cascella NG, Kumor KM, Sherer MA (1989) Cocaine-induced cocaine craving. Psychopharmacology 97:59-64. CrossRef Medline
51. Katz JL, Higgins ST (2003) The validity of the reinstatement model of craving and relapse to drug use. Psychopharmacology 168:21-30. CrossRef Medline
52. Knackstedt LA, Moussawi K, Lalumiere R, Schwendt M, Klugmann M, Kalivas PW (2010) Extinction training after cocaine self-administration induces glutamatergic plasticity to inhibit cocaine seeking. J Neurosci 30: 7984-7992. CrossRef Medline
53. Kruzich PJ, Congleton KM, See RE (2001) Conditioned reinstatement of drug-seeking behavior with a discrete compound stimulus classically conditioned with intravenous cocaine. Behav Neurosci 115:1086-1092. CrossRef Medline
54. Le Blanc KH, Ostlund SB, Maidment NT (2012) Pavlovian-to-instrumental transfer in cocaine seeking rats. Behav Neurosci 126:681-689. CrossRef Medline
55. Lex A, Hauber W (2008) Dopamine D1 and D2 receptors in the nucleus accumbens core and shell mediate Pavlovian-instrumental transfer. Learn Mem 15:483-491. CrossRef Medline
56. Lovibond PF (1983) Facilitation of instrumental behavior by a Pavlovian appetitive conditioned stimulus. J Exp Psychol Anim Behav Process 9:225-247. CrossRef Medline
57. Lovic V, Saunders BT, Yager LM, Robinson TE (2011) Rats prone to attribute incentive salience to reward cues are also prone to impulsive action. Behav Brain Res 223:255-261. CrossRef Medline
58. Marchant NJ, Li X, Shaham Y (2013) Recent developments in animal models of drug relapse. Curr Opin Neurobiol. Advance online publication. doi:10.1016/j.conb.2013.01.003. CrossRef Medline
59. McClernon FJ, Hutchison KE, Rose JE, Kozink RV (2007) DRD4 VNTR polymorphism is associated with transient f MRI-BOLD responses to smoking cues. Psychopharmacology 194:433-441. CrossRef Medline
60. Meyer PJ, Lovic V, Saunders BT, Yager LM, Flagel SB, Morrow JD, Robinson TE (2012) Quantifying individual variation in the propensity to attribute incentive salience to reward cues. PLo S One 7:e38987. CrossRef Medline
61. Milton AL, Everitt BJ (2010) The psychological and neurochemical mechanisms of drug memory reconsolidation: implications for the treatment of addiction. Eur J Neurosci 31:2308-2319. CrossRef Medline
62. Munafò MR, Mannie ZN, Cowen PJ, Harmer CJ, McTavish SB (2007) Effects of acute tyrosine depletion on subjective craving and selective processing of smoking-related cues in abstinent cigarette smokers. J Psychopharmacol 21:805-814. CrossRef Medline
63. 2 dopamine receptor gene: a review. Eur Psychiatry 15:79-89. CrossRef Medline
64. Ostlund SB, Maidment NT (2012) Dopamine receptor blockade attenuates the general incentive motivational effects of noncontingently delivered rewards and reward-paired cues without affecting their ability to bias action selection. Neuropsychopharmacology 37:508-519. CrossRef Medline
65. Paolone G, Angelakos CC, Meyer PJ, Robinson TE, Sarter M (2013) Cholinergic control over attention in rats prone to attribute incentive salience to reward cues. J Neurosci 33:8321-8335. CrossRef Medline
66. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, Ed 6. New York: Academic.
67. Peck JA, Wercberger R, Kariyeva E, Ranaldi R (2013) Cue-induced resumption of heroin and cocaine seeking in rats using a conflict model of abstinence and relapse. Psychopharmacology (Berl). Advance online publication. doi:10.1007/s00213-013-3069-x. CrossRef Medline
68. Pelloux Y, Everitt BJ, Dickinson A (2007) Compulsive drug seeking by rats under punishment: effects of drug taking history. Psychopharmacology 194:127-137. CrossRef Medline
69. Phillips GD, Setzu E, Hitchcott PK (2003) Facilitation of appetitive Pavlovian conditioning by d-amphetamine in the shell, but not the core, of the nucleus accumbens. Behav Neurosci 117:675-684. CrossRef Medline
70. Preston KL, Vahabzadeh M, Schmittner J, Lin JL, Gorelick DA, Epstein DH (2009) Cocaine craving and use during daily life. Psychopharmacology (Berl) 207:291-301. CrossRef Medline
71. Rescorla RA (1967) Pavlovian conditioning and its proper control procedures. Psychol Rev 74:71-80. CrossRef Medline
72. Robbins TW (1976) Relationship between reward-enhancing and stereotypical effects of psychomotor stimulant drugs. Nature 264:57-59. CrossRef Medline
73. Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Rev 18:247-291. CrossRef Medline
74. Robinson TE, Yager LM, Cogan ES, Saunders BT (2013) Onthemotivationalproperties of reward cues: individual differences. Neuropharmacology. Advance online publication. doi:10.1016/j.neuropharm.2013.05.040. CrossRef Medline
75. Saddoris MP, Stamatakis A, Carelli RM (2011) Neural correlates of Pavlovian-to-instrumental transfer in the nucleus accumbens shell are selectively potentiated following cocaine self-administration. Eur J Neurosci 33:2274-2287. CrossRef Medline
76. Saunders BT, Robinson TE (2010) A cocaine cue acts as an incentive stimulus in some but not others: implications for addiction. Biol Psychiatry 67:730-736. CrossRef Medline
77. Saunders BT, Robinson TE (2011) Individual variation in the motivational properties of cocaine. Neuropsychopharmacology 36:1668-1676. CrossRef Medline
78. Saunders BT, Robinson TE (2012) The role of dopamine in the accumbens core in the expression of Pavlovian-conditioned responses. Eur J Neurosci 36:2521-2532. CrossRef Medline
79. Saunders BT, Robinson TE (2013) Individual variation in resisting temptation: implications for addiction. Neurosci Biobehav Rev. Advance online publication. doi:10.1016/j.neubiorev.2013.02.008. CrossRef Medline
80. Schroeder JP, Alisha Epps S, Grice TW, Weinshenker D (2013) The selective dopamine β-hydroxylase inhibitor nepicastat attenuates multiple aspects of cocaine-seeking behavior. Neuropsychopharmacology. Advance online publication. doi:10.1038/npp.2012.267. CrossRef Medline
81. Seiden LS, Sabol KE, Ricaurte GA (1993) Amphetamine: effects on catecholamine systems and behavior. Annu Rev Pharmacol Toxicol 33:639-677. CrossRef Medline
82. Shaham Y, Shalev U, Lu L, De Wit H, Stewart J (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology 168:3-20. CrossRef Medline
83. Shiffman S, Gwaltney CJ, Balabanis MH, Liu KS, Paty JA, Kassel JD, Hickcox M, Gnys M (2002) Immediate antecedents of cigarette smoking: an analysis from ecological momentary assessment. J Abnorm Psychol 111: 531-545. CrossRef Medline
84. Simon NW, Mendez IA, Setlow B (2009) Effects of prior amphetamine exposure on approach strategy in appetitive Pavlovian conditioning in rats. Psychopharmacology (Berl) 202:699-709. CrossRef Medline
85. Sinha R (2013) The clinical neurobiology of drug craving. Curr Opin Neurobiol. Advance online publication. doi:10.1016/j.conb.2013. 05.001. CrossRef Medline
86. Stewart J, de Wit H, Eikelboom R (1984) Role of unconditioned and conditioned drug effects in the self-administration of opiates and stimulants. Psychol Rev 91:251-268. CrossRef Medline
87. Stone AA, Shiffman S (1994) Ecological momentary assessment (EMA) in behavorial medicine. Ann Behav Med 16:199-202.
88. Taylor JR, Robbins TW (1984) Enhanced behavioural control by conditioned reinforcers following microinjections of d-amphetamine into the nucleus accumbens. Psychopharmacology (Berl) 84:405-412. CrossRef Medline
89. 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 (Berl) 90:390-397. Medline
90. Tomie A (1996) Locating reward cue at response manipulandum (CAM) induces symptoms of drug abuse. Neurosci Biobehav Rev 20:505-535. CrossRef Medline
91. Verbeke G (2009) Linear mixed models for longitudinal data. New York: Springer.
92. Volkow ND, Wang GJ, Telang F, Fowler JS, Logan J, Childress AR, Jayne M, Ma Y, Wong C (2006) Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. J Neurosci 26:6583-6588. CrossRef Medline
93. Wassum KM, Ostlund SB, Balleine BW, Maidment NT (2011) Differential dependence of Pavlovian incentive motivation and instrumental incentive learning processes on dopamine signaling. Learn Mem 18:475-483. CrossRef Medline
94. Wassum KM, Ostlund SB, Loewinger GC, Maidment NT (2013) Phasic mesolimbic dopamine release tracks reward seeking during expression of pavlovian-to-instrumental transfer. Biol Psychiatry 73:747-755. CrossRef Medline
95. Wong DF, Kuwabara H, Schretlen DJ, Bonson KR, Zhou Y, Nandi A, Brasić JR, Kimes AS, Maris MA, Kumar A, Contoreggi C, Links J, Ernst M, Rousset O, Zukin S, Grace AA, Lee JS, Rohde C, Jasinski DR, Gjedde A, et al. (2006) Increased occupancy of dopamine receptors in human striatum during cue-elicited cocaine craving. Neuropsychopharmacology 31: 2716-2727. CrossRef Medline
96. Wyvell CL, Berridge KC (2000) Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward "wanting" without enhanced "liking" or response reinforcement. J Neurosci 20:8122-8130. Medline
97. Wyvell CL, Berridge KC (2001) Incentive sensitization by previous amphetamine exposure: increased cue-triggered "wanting" for sucrose reward. J Neurosci 21:7831-7840. Medline
98. Yager LM, Robinson TE (2013) A classically conditioned cocaine cue acquires greater control over behavior in rats prone to attribute incentive salience to a food cue. Psychopharmacology 226:217-228. CrossRef Medline