Repeated Cocaine Exposure Facilitates the Expression of Incentive Motivation and Induces Habitual Control in Rats

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  LeBlanc, Kimberly H ^a,b   Maidment, Nigel T ^a,b   Ostlund, Sean B ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COCAINE;

ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BEHAVIOR CONTROL; COCAINE DEPENDENCE; CONDITIONING; CONTROLLED STUDY; DECISION MAKING; DRUG EXPOSURE; DRUG SENSITIZATION; FEEDBACK SYSTEM; HABITUATION; INCENTIVE MOTIVATION; MALE; MOTIVATION; NONHUMAN; PAVLOVIAN TO INSTRUMENTAL TRANSFER TEST; PAVLOVIAN TRAINING; RAT; REINFORCEMENT; REWARD; REWARD DEVALUATION TEST; TASK PERFORMANCE; ADDICTION; ANIMAL; ANIMAL BEHAVIOR; ASSOCIATION; DRUG EFFECTS;

RATTUS;

ANIMALS; BEHAVIOR, ANIMAL; COCAINE; CONDITIONING (PSYCHOLOGY); CUES; MALE; MOTIVATION; RATS; REWARD; SUBSTANCE-RELATED DISORDERS;

EID: 84876969817     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061355     Document Type: Article

References (84)

1. Robinson TE, Berridge KC, (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18: 247-291.
2. Robinson TE, Berridge KC, (2008) Review. The incentive sensitization theory of addiction: some current issues. Philos Trans R Soc Lond B Biol Sci 363: 3137-3146.
3. Di Chiara G, Imperato A, (1988) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci U S A 85: 5274-5278.
4. Pierce RC, Kalivas PW, (1997) A circuitry model of the expression of behavioral sensitization to amphetamine-like psychostimulants. Brain Res Brain Res Rev 25: 192-216.
5. Berridge KC, Robinson TE, (2003) Parsing reward. Trends Neurosci 26: 507-513.
6. 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.
7. 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.
8. 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.
9. Ostlund SB, Wassum KM, Murphy NP, Balleine BW, Maidment NT, (2011) Extracellular dopamine levels in striatal subregions track shifts in motivation and response cost during instrumental conditioning. Journal of Neuroscience 31: 200-207.
10. 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.
11. Dickinson A, Smith J, Mirenowicz J, (2000) Dissociation of Pavlovian and instrumental incentive learning under dopamine antagonists. Behav Neurosci 114: 468-483.
12. Everitt BJ, Dickinson A, Robbins TW, (2001) The neuropsychological basis of addictive behaviour. Brain Res Brain Res Rev 36: 129-138.
13. Everitt B, Robbins T, (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8: 1481-1489.
14. Tiffany ST, (1990) A cognitive model of drug urges and drug-use behavior: role of automatic and nonautomatic processes. Psychol Rev 97: 147-168.
15. Hyman SE, Malenka RC, Nestler EJ, (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29: 565-598.
16. Berke JD, Hyman SE, (2000) Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25: 515-532.
17. Balleine B, Dickinson A, (1998) Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology 37: 407-419.
18. Dickinson A, Wood N, Smith JW, (2002) Alcohol seeking by rats: action or habit? Q J Exp Psychol B 55: 331-348.
19. Miles F, Everitt B, Dickinson A, (2003) Oral cocaine seeking by rats: action or habit? Behav Neurosci 117: 927-938.
20. Zapata A, Minney VL, Shippenberg TS, (2010) Shift from goal-directed to habitual cocaine seeking after prolonged experience in rats. J Neurosci 30: 15457-15463.
21. Vanderschuren LJ, Everitt BJ, (2004) Drug seeking becomes compulsive after prolonged cocaine self-administration. Science 305: 1017-1019.
22. Shaham Y, Shalev U, Lu L, De Wit H, Stewart J, (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl) 168: 3-20.
23. Mendrek A, Blaha CD, Phillips AG, (1998) Pre-exposure of rats to amphetamine sensitizes self-administration of this drug under a progressive ratio schedule. Psychopharmacology (Berl) 135: 416-422.
24. Horger BA, Giles MK, Schenk S, (1992) Preexposure to amphetamine and nicotine predisposes rats to self-administer a low dose of cocaine. Psychopharmacology 107: 271-276.
25. Suto N, Austin JD, Tanabe LM, Kramer MK, Wright DA, et al. (2002) Previous exposure to VTA amphetamine enhances cocaine self-administration under a progressive ratio schedule in a D1 dopamine receptor dependent manner. Neuropsychopharmacology 27: 970-979.
26. Vezina P, Lorrain DS, Arnold GM, Austin JD, Suto N, (2002) Sensitization of midbrain dopamine neuron reactivity promotes the pursuit of amphetamine. J Neurosci 22: 4654-4662.
27. Ostlund S, Balleine B, (2008) On habits and addiction: An associative analysis of compulsive drug seeking. Drug Discov Today Dis Models 5: 235-245.
28. Wyvell CL, Berridge KC, (2001) Incentive sensitization by previous amphetamine exposure: increased cue-triggered "wanting" for sucrose reward. Journal of Neuroscience 21: 7831-7840.
29. Nelson A, Killcross S, (2006) Amphetamine exposure enhances habit formation. J Neurosci 26: 3805-3812.
30. Nordquist RE, Voorn P, de Mooij-van Malsen JG, Joosten RN, Pennartz CM, et al. (2007) Augmented reinforcer value and accelerated habit formation after repeated amphetamine treatment. Eur Neuropsychopharmacol 17: 532-540.
31. Ostlund SB, Maidment NT, Balleine BW, (2010) Alcohol-Paired Contextual Cues Produce an Immediate and Selective Loss of Goal-directed Action in Rats. Front Integr Neurosci 4.
32. Ranaldi R, Egan J, Kest K, Fein M, Delamater AR, (2009) Repeated heroin in rats produces locomotor sensitization and enhances appetitive Pavlovian and instrumental learning involving food reward. Pharmacol Biochem Behav 91: 351-357.
33. Shiflett MW, (2012) The effects of amphetamine exposure on outcome-selective Pavlovian-instrumental. Psychopharmacology (Berl) 223: 361-370.
34. Nocjar C, Panksepp J, (2002) Chronic intermittent amphetamine pretreatment enhances future appetitive behavior for drug- and natural-reward: interaction with environmental variables. Behav Brain Res 128: 189-203.
35. Mendez IA, Williams MT, Bhavsar A, Lu AP, Bizon JL, et al. (2009) Long-lasting sensitization of reward-directed behavior by amphetamine. Behav Brain Res 201: 74-79.
36. Harmer CJ, Phillips GD, (1998) Enhanced appetitive conditioning following repeated pretreatment with d-amphetamine. Behav Pharmacol 9: 299-308.
37. Klein ED, Gehrke BJ, Green TA, Zentall TR, Bardo MT, (2007) Repeated cocaine experience facilitates sucrose-reinforced operant responding in enriched and isolated rats. Learn Motiv 38: 44-55.
38. Schoenbaum G, Setlow B, (2005) Cocaine makes actions insensitive to outcomes but not extinction: implications for altered orbitofrontal-amygdalar function. Cereb Cortex 15: 1162-1169.
39. White FJ, Kalivas PW, (1998) Neuroadaptations involved in amphetamine and cocaine addiction. Drug Alcohol Depend 51: 141-153.
40. Kuczensk R, Segal D, Aizenstein M, (1991) Amphetamine, cocaine, and fencamfamine: relationship between locomotor and stereotypy response profiles and caudate and accumbens dopamine dynamics. The Journal of Neuroscience 11: 2703-2712.
41. Pontieri FE, Tanda G, Chiara GD, (1995) Intravenous cocaine, morphine, and amphetamine preferentially increase extracellular dopamine in the "shell" as compared with the "core" of the rat nucleus accumbens. Proceedings of the National Academy of Sciences 92: 12304-12308.
42. Holland PC, (2004) Relations between Pavlovian-instrumental transfer and reinforcer devaluation. J Exp Psychol Anim Behav Process 30: 104-117.
43. Kalivas PW, Duffy P, (1993) Time course of extracellular dopamine and behavioral sensitization to cocaine. I. Dopamine axon terminals. J Neurosci 13: 266-275.
44. Sorg BA, Chen SY, Kalivas PW, (1993) Time course of tyrosine hydroxylase expression after behavioral sensitization to cocaine. J Pharmacol Exp Ther 266: 424-430.
45. Mayfield RD, Larson G, Zahniser NR, (1992) Cocaine-induced behavioral sensitization and D1 dopamine receptor function in rat nucleus accumbens and striatum. Brain Res 573: 331-335.
46. Berridge KC, (1991) Modulation of taste affect by hunger, caloric satiety, and sensory-specific satiety in the rat. Appetite 16: 103-120.
47. Young P, (1940) Reversal of food preferences of the white rat through controlled pre-feeding. J Gen Psychol 22: 33-66.
48. Hetherington M, Rolls BJ, Burley VJ, (1989) The time course of sensory-specific satiety. Appetite 12: 57-68.
49. de Wit S, Ostlund SB, Balleine BW, Dickinson A, (2009) Resolution of conflict between goal-directed actions: outcome encoding and neural control processes. J Exp Psychol Anim Behav Process 35: 382-393.
50. Wiltgen BJ, Law M, Ostlund S, Mayford M, Balleine BW, (2007) The influence of Pavlovian cues on instrumental performance is mediated by CaMKII activity in the striatum. Eur J Neurosci 25: 2491-2497.
51. Wyvell C, Berridge K, (2001) Incentive sensitization by previous amphetamine exposure: increased cue-triggered "wanting" for sucrose reward. J Neurosci 21: 7831-7840.
52. De Vries TJ, Schoffelmeer ANM, Binnekade R, Mulder AH, Vanderschuren LJMJ, (1998) Drug-induced reinstatement of heroin- and cocaine-seeking behaviour following long-term extinction is associated with expression of behavioural sensitization. European Journal of Neuroscience 10: 3565-3571.
53. Cador M, Bjijou Y, Stinus L, (1995) Evidence of a complete independence of the neurobiological substrates for the induction and expression of behavioral sensitization to amphetamine. Neuroscience 65: 385-395.
54. de Wit H, Stewart J, (1981) Reinstatement of cocaine-reinforced responding in the rat. Psychopharmacology (Berl) 75: 134-143.
55. 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.
56. Hemby SE, Co C, Koves TR, Smith JE, Dworkin SI, (1997) Differences in extracellular dopamine concentrations in the nucleus accumbens during response-dependent and response-independent cocaine administration in the rat. Psychopharmacology (Berl) 133: 7-16.
57. Wilson JM, Nobrega JN, Corrigall WA, Coen KM, Shannak K, et al. (1994) Amygdala dopamine levels are markedly elevated after self- but not passive-administration of cocaine. Brain Res 668: 39-45.
58. Chen B, Bowers M, Martin M, Hopf F, Guillory A, et al. (2008) Cocaine but not natural reward self-administration nor passive cocaine infusion produces persistent LTP in the VTA. Neuron 59: 288-297.
59. Stefanski R, Ladenheim B, Lee S, Cadet J, Goldberg S, (1999) Neuroadaptations in the dopaminergic system after active self-administration but not after passive administration of methamphetamine. Eur J Pharmacol 371: 123-135.
60. Leblanc KH, Ostlund SB, Maidment NT, (2012) Pavlovian-to-instrumental transfer in cocaine seeking rats. Behav Neurosci 126: 681-689.
61. Fiorino DF, Phillips AG, (1999) Facilitation of sexual behavior in male rats following d-amphetamine-induced behavioral sensitization. Psychopharmacology (Berl) 142: 200-208.
62. Fiorino DF, Phillips AG, (1999) Facilitation of sexual behavior and enhanced dopamine efflux in the nucleus accumbens of male rats after D-amphetamine-induced behavioral sensitization. Journal of Neuroscience 19: 456-463.
63. Clark JJ, Bernstein IL, (2004) Reciprocal cross-sensitization between amphetamine and salt appetite. Pharmacol Biochem Behav 78: 691-698.
64. Taylor JR, Jentsch JD, (2001) Repeated intermittent administration of psychomotor stimulant drugs alters the acquisition of Pavlovian approach behavior in rats: differential effects of cocaine, d-amphetamine and 3,4- methylenedioxymethamphetamine ("Ecstasy"). Biol Psychiatry 50: 137-143.
65. Ranaldi R, Egan J, Kest K, Fein M, Delamater AR, (2009) Repeated heroin in rats produces locomotor sensitization and enhances appetitive Pavlovian and instrumental learning involving food reward. Pharmacol Biochem Behav 91: 351-357.
66. Pierce RC, Kalivas PW, (1995) Amphetamine produces sensitized increases in locomotion and extracellular dopamine preferentially in the nucleus accumbens shell of rats administered repeated cocaine. J Pharmacol Exp Ther 275: 1019-1029.
67. Akimoto K, Hamamura T, Kazahaya Y, Akiyama K, Otsuki S, (1990) Enhanced extracellular dopamine level may be the fundamental neuropharmacological basis of cross-behavioral sensitization between methamphetamine and cocaine-an in vivo dialysis study in freely moving rats. Brain Res 507: 344-346.
68. Vanderschuren LJ, Kalivas PW, (2000) Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacology (Berl) 151: 99-120.
69. Kantor L, Hewlett GH, Gnegy ME, (1999) Enhanced amphetamine- and K+-mediated dopamine release in rat striatum after repeated amphetamine: differential requirements for Ca2+- and calmodulin-dependent phosphorylation and synaptic vesicles. J Neurosci 19: 3801-3808.
70. De Luca MA, Bimpisidis Z, Bassareo V, Di Chiara G, (2011) Influence of morphine sensitization on the responsiveness of mesolimbic and mesocortical dopamine transmission to appetitive and aversive gustatory stimuli. Psychopharmacology (Berl) 216: 345-353.
71. Harmer CJ, Phillips GD, (1999) Enhanced dopamine efflux in the amygdala by a predictive, but not a non-predictive, stimulus: facilitation by prior repeated D-amphetamine. Neuroscience 90: 119-130.
72. Robinson T, Berridge K, (2008) Review. The incentive sensitization theory of addiction: some current issues. Philos Trans R Soc Lond B Biol Sci 363: 3137-3146.
73. Belin D, Everitt B, (2008) Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 57: 432-441.
74. Vanderschuren L, Di Ciano P, Everitt B, (2005) Involvement of the Dorsal Striatum in Cue-Controlled Cocaine Seeking. The Journal of Neuroscience 25: 8665-8670.
75. Ito R, Dalley JW, Robbins TW, Everitt BJ, (2002) Dopamine release in the dorsal striatum during cocaine-seeking behavior under the control of a drug-associated cue. J Neurosci 22: 6247-6253.
76. Robinson TE, Browman KE, Crombag HS, Badiani A, (1998) Modulation of the Induction or Expression of Psychostimulant Sensitization by the Circumstances Surrounding Drug Administration. Neuroscience & Biobehavioral Reviews 22: 347-354.
77. Post RM, Lockfeld A, Squillace KM, Contel NR, (1981) Drug-environment interaction: context dependency of cocaine-induced behavioral sensitization. Life Sci 28: 755-760.
78. Weiss SR, Post RM, Pert A, Woodward R, Murman D, (1989) Context-dependent cocaine sensitization: differential effect of haloperidol on development versus expression. Pharmacol Biochem Behav 34: 655-661.
79. Xie X, Arguello AA, Reittinger AM, Wells AM, Fuchs RA, (2012) Role of nicotinic acetylcholine receptors in the effects of cocaine-paired contextual stimuli on impulsive decision making in rats. Psychopharmacology (Berl) 223: 271-279.
80. Belin D, Balado E, Piazza PV, Deroche-Gamonet V, (2009) Pattern of Intake and Drug Craving Predict the Development of Cocaine Addiction-like Behavior in Rats. Biological Psychiatry 65: 863-868.
81. Deroche-Gamonet V, Belin D, Piazza PV, (2004) Evidence for addiction-like behavior in the rat. Science 305: 1014-1017.
82. Pierce RC, Vanderschuren L, (2010) Kicking the habit: The neural basis of ingrained behaviors in cocaine addiction. Neuroscience & Biobehavioral Reviews 35: 212-219.
83. Holland PC, (2004) Relations between Pavlovian-instrumental transfer and reinforcer devaluation. J Exp Psychol Anim Behav Process 30: 104-117.
84. Rescorla RA, (1994) Transfer of Instrumental Control Mediated by a Devalued Outcome. Animal Learning & Behavior 22: 27-33.