Double dissociation of the dorsomedial and dorsolateral striatal control over the acquisition and performance of cocaine seeking

Neuropsychopharmacology

Volumn 37, Issue 11, 2012, Pages 2456-2466

  Murray, Jennifer E ^a,b   Belin, David ^b,c   Everitt, Barry J ^a,b  

^a UK   (United Kingdom)

^b INSERM   (France)

^c UNIVERSITÉ DE POITIERS   (France)

Author keywords

cocaine self administration; conditioned reinforcement; dopamine; dorsolateral striatum; dorsomedial striatum; habit formation

Indexed keywords

COCAINE; DOPAMINE; FLUPENTIXOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTERIOR DORSOLATERAL STRIATUM; ARTICLE; ASSOCIATION; COCAINE SEEKING BEHAVIOR; CONDITIONING; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC TRANSMISSION; DRUG SEEKING BEHAVIOR; DRUG SELF ADMINISTRATION; MALE; NONHUMAN; PERFORMANCE; POSTERIOR DORSOMEDIAL STRIATUM; PRIORITY JOURNAL; RAT; REINFORCEMENT;

ANALYSIS OF VARIANCE; ANIMALS; COCAINE; COCAINE-RELATED DISORDERS; CONDITIONING, OPERANT; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE ANTAGONISTS; DOPAMINE UPTAKE INHIBITORS; FLUPENTHIXOL; MALE; RATS; REINFORCEMENT (PSYCHOLOGY); REINFORCEMENT SCHEDULE; SELF ADMINISTRATION;

EID: 84866413736     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.104     Document Type: Article

References (56)

1. Adams CD, Dickinson A (1981). Instrumental responding following reinforcer devaluation. Q J Exp Psychol B 33: 109-122.
2. Balleine BW, Liljeholm M, Ostlund SB (2009). The integrative function of the basal ganglia in instrumental conditioning. Behav Brain Res 199: 43-52.
3. Belin D, Economidou D, Pelloux Y, Everitt BJ (2011). Habit formation and compulsion. Neuromethods 53: 337-378.
4. Belin D, Everitt BJ (2008). Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 57: 432-441. (Pubitemid 351179162)
5. Belin D, Jonkman S, Dickinson A, Robbins TW, Everitt BJ (2009). Parallel and interactive learning processes within the basal ganglia: relevance for the understanding of addiction. Behav Brain Res 199: 89-102.
6. Cardinal RN, Parkinson JA, Lachenal G, Halkerston KM, Rudarakanchana N, Hall J et al (2002). Effects of selective excitotoxic lesions of the nucleus accumbens core, anterior cingulate cortex, and central nucleus of the amygdala on autoshaping performance in rats. Behav Neurosci 116: 553-567. (Pubitemid 34793377)
7. Cardinal RN, Pennicott DR, Sugathapala CL, Robbins TW, Everitt BJ (2001). Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science 292: 2499-2501. (Pubitemid 32601663)
8. Corbit LH, Nie H, Janak PH (2012). Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol Psychiatry. http://dx.doi.org/10.1016/j.biopsych. 2012.02.02.
9. Di Ciano P, Everitt BJ (2004). Direct interactions between the basolateral amygdala and nucleus accumbens core underlie cocaine-seeking behaviour by rats. J Neurosci 24: 7167-7173. (Pubitemid 39096382)
10. Dickinson A (1985). Actions and habits: the development of behavioural autonomy. Phil Trans R Soc Lond B 308: 67-78.
11. Dickinson A, Wood N, Smith JW (2002). Alcohol seeking by rats: action or habit? Q J Exp Psychol B 55: 331-348.
12. Everitt BJ, Belin D, Economidou D, Pelloux Y, Dalley JW, Robbins TW (2008). Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Phil Trans R Soc B 363: 3125-3135.
13. Everitt BJ, Robbins TW (2000). Second-order schedules of drug reinforcement in rats and monkeys: measurement of reinforcing efficacy and drug-seeking behaviour. Psychopharmacology 153: 17-30. (Pubitemid 32127901)
14. Everitt BJ, Robbins TW (2005). Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8: 1481-1489. (Pubitemid 41573659)
15. Faure A, Haberland U, Condé F, El Massioui N (2005). Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation. J Neurosci 25: 2771-2780. (Pubitemid 40389235)
16. Garavan H, Pankiewicz J, Bloom A, Cho JK, Sperry L, Ross TJ et al (2000). Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli. Am J Psychiatry 157: 1789-1798.
17. Gerfen CR, Herkenham M, Thibault J (1987). The neostriatal mosaic: II. patch-and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J Neurosci 7: 3915-3934. (Pubitemid 18012405)
18. Haber SN (2003). The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 26: 317-330. (Pubitemid 38077155)
19. Hernandez PJ, Sadeghian K, Kelley AE (2002). Early consolidation of instrumental learning requires protein synthesis in the nucleus accumbens. Nat Neurosci 5: 1327-1331. (Pubitemid 35417768)
20. Ikemoto S (2007). Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbensolfactory tubercle complex. Brain Res Rev 56: 27-78. (Pubitemid 350110353)
21. Ito R, Dalley JW, Howes SR, Robbins TW, Everitt BJ (2000). Dissociation in conditioned dopamine release in the nucleus accumbens core and shell in response to cocaine cues and during cocaine-seeking behaviour in rats. J Neurosci 20: 7489-7495.
22. Ito R, Dalley JW, Robbins TW, Everitt BJ (2002). Dopamine release in the dorsal striatum during cocaine-seeking behaviour under the control of a drug-associated cue. J Neurosci 22: 6247-6253. (Pubitemid 35387665)
23. Ito R, Robbins TW, Everitt BJ (2004). Differential control over cocaine-seeking behaviour by nucleus accumbens core and shell. Nat Neurosci 7: 389-397. (Pubitemid 38429179)
24. Jedynak JR, Uslaner JM, Esteban JA, Robinson TE (2007). Methamphetamine-induced structural plasticity in the dorsal striatum. Eur J Neurosci 25: 847-853.
25. Kahnt T, Park SQ, Cohen MX, Beck A, Heinz A, Wrase J (2009). Dorsal striatal-midbrain connectivity in humans predicts how reinforcements are used to guide decisions. J Cogn Neurosci 21: 1332-1345.
26. Kelley AE, Domesick VB, Nauta WJ (1982). The amygdalostriatal projection in the ratFan anatomical study by anterograde and retrograde tracing methods. Neuroscience 7: 615-630. (Pubitemid 12192041)
27. Letchworth SR, Nader MA, Smith HR, Friedman DP, Porrino LJ (2001). Progression of changes in dopamine transporter binding site density as a result of cocaine self-administration in rhesus monkeys. J Neurosci 21: 2799-2807. (Pubitemid 32298221)
28. Lex B, Hauber W (2010). The role of dopamine in the prelimbic cortex and the dorsomedial striatum in instrumental conditioning. Cereb Cortex 20: 873-883.
29. Lex B, Sommer S, Hauber W (2011). The role of dopamine in the dorsomedial striatum in place and response learning. Neuroscience 172: 212-218.
30. Murray JE, Everitt BJ, Belin D (2012). N-Acetylcysteine reduces early-and late-stage cocaine seeking without affecting cocaine taking in rats. Addict Biol 17: 437-440.
31. Nauta WJH, Smith GP, Faull RLM, Domesick VB (1978). Efferent connections and nigral afferents of the nucleus accumbens septi in the rat. Neuroscience 3: 385-401. (Pubitemid 8361179)
32. O'Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ (2004). Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304: 452-454. (Pubitemid 38495943)
33. Olmstead MC, Lafond MV, Everitt BJ, Dickinson A (2001). Cocaine seeking by rats is a goal-directed action. Behav Neurosci 115: 394-402. (Pubitemid 32378168)
34. Packard MG, McGaugh JL (1996). Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65: 65-72. (Pubitemid 26112655)
35. Paxinos G, Watson C (1998). The Rat Brain in Stereotaxic Coordinates, 4th Edn. Academic Press: San Diego, CA.
36. Porrino LJ, Lyons D, Smith HR, Daunais JB, Nader MA (2004). Cocaine self-administration produces a progressive involvement of limbic, association, and sensoriomotor striatal domains. J Neurosci 24: 3554-3562. (Pubitemid 38481112)
37. Porrino LJ, Smith HR, Nader MA, Beveridge TJ (2007). The effects of cocaine: a shifting target over the course of addiction. Prog Neuropsychopharmacol Biol Psychiatry 31: 1593-1600. (Pubitemid 47625705)
38. Roberts DC, Koob GF (1982). Disruption of cocaine self-administration following 6-hydroxydopamine lesions of the ventral tegmental area in rats. Pharmacol Biochem Behav 17: 901-904. (Pubitemid 13208458)
39. Robledo P, Maldonado-Lopez R, Koob GF (1992). Role of dopamine receptors in the nucleus accumbens in the rewarding properties of cocaine. Ann NY Acad Sci 654: 509-512.
40. Schindler CW, Katz JL, Goldberg SR (1988). The use of secondorder schedules to study the influence of environmental stimuli on drug-seeking behaviour. NIDA Res Monogr 84: 180-195.
41. Shiflett MW, Brown RA, Balleine BW (2010). Acquisition and performance of goal-directed instrumental actions depends on ERK signalling in distinct regions of dorsal striatum of rats. J Neurosci 30: 2951-2959.
42. Smith-Roe SL, Kelley AE (2000). Coincident activation of NMDA and dopamine D1 receptors within the nucleus accumbens core is required for appetitive instrumental learning. J Neurosci 20: 7737-7742.
43. Suto N, Ecke LE, Wise RA (2009). Control of within-binge cocaineseeking by dopamine and glutamate in the core of nucleus accumbens. Psychopharmacology 205: 431-439.
44. Suto N, Ecke LE, You ZB, Wise RA (2010). Extracellular fluctuations of dopamine and glutamate in the nucleus accumbens core and shell associated with lever-pressing during cocaine self-administration, extinction, and yoked cocaine administration. Psychopharmacology 211: 267-275.
45. Thorn CA, Atallah H, Howe M, Graybiel AM (2010). Differential dynamics of activity changes in dorsolateral and dorsomedial striatal loops during learning. Neuron 66: 781-795.
46. Vanderschuren LJMJ, Di Ciano P, Everitt BJ (2005). Involvement of the dorsal striatum in cue-controlled cocaine seeking. J Neurosci 25: 8665-8670. (Pubitemid 41362043)
47. Veeneman MM, Broekhoven MH, Damsteegt R, Vanderschuren LJ (2012). Distinct contributions of dopamine in the dorsolateral striatum and nucleus accumbens shell to the reinforcing properties of cocaine. Neuropsychopharmacology 37: 487-498.
48. Volkow ND, Wang G-J, Telang F, Fowler JS, Logan J, Childress A-R et al (2006). Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. J Neurosci 26: 6583-6588. (Pubitemid 44318339)
49. Whitelaw RB, Markou A, Robbins TW, Everitt BJ (1996). Excitotoxic lesions of the basolateral amygdala impair the acquisition of cocaine-seeking behaviour under a second-order schedule of reinforcement. Psychopharmacology 127: 213-224. (Pubitemid 26342853)
50. Wise RA (2004). Dopamine, learning and motivation. Nat Rev Neurosci 5: 483-494. (Pubitemid 38715515)
51. Wong DF, Kuwabara H, Schretlen DJ, Bonson KR, Zhou Y, Nandi A et al (2006). Increased occupancy of dopamine receptors in human striatum during cue-elicited cocaine craving. Neuropsychopharmacology 31: 2716-2727. (Pubitemid 44764168)
52. Wyvell CL, Berridge KC (2000). Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of rewarding "wanting" without enhancing "liking" or response reinforcement. J Neurosci 20: 8122-8130.
53. Yin HH, Knowlton BJ, Balleine BW (2004). Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J Neurosci 19: 181-189. (Pubitemid 38122084)
54. Yin HH, Mulcare SP, Hilário MRF, Clouse E, Holloway T, Davis MI et al (2009). Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat Neurosci 12: 333-341.
55. Yin HH, Ostlund SB, Knowlton BJ, Balleine BW (2005). The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci 22: 513-523. (Pubitemid 41097624)
56. Zapata A, Minney VL, Shippenberg TS (2010). Shift from goaldirected to habitual cocaine seeking after prolonged experience in rats. J Neurosci 30: 15457-15463.