Nucleus accumbens shell and core involvement in drug context-induced reinstatement of cocaine seeking in rats

Psychopharmacology

Volumn 200, Issue 4, 2008, Pages 545-556

  Fuchs, Rita A ^a   Ramirez, Donna R ^a   Bell, Guinevere H ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Baclofen; Cocaine; Context; Extinction; Muscimol; Nucleus accumbens; Reinstatement; Self administration

Indexed keywords

BACLOFEN; COCAINE; MUSCIMOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONDITIONING; CONTROLLED STUDY; DRUG SELF ADMINISTRATION; MOTIVATION; NONHUMAN; NUCLEUS ACCUMBENS; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; RAT; REINFORCEMENT; RELAPSE;

ANIMALS; BACLOFEN; BEHAVIOR, ANIMAL; COCAINE; EXTINCTION, PSYCHOLOGICAL; GABA AGONISTS; INFUSIONS, INTRAVENOUS; MALE; MUSCIMOL; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY; REINFORCEMENT SCHEDULE; SELF ADMINISTRATION;

EID: 52649130863     PISSN: 00333158     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00213-008-1234-4     Document Type: Article

References (78)

1. Amaral DG, Witter MP (1995) Hippocampal formation. In: Paxinos, G (eds) The rat nervous system. Academic, Los Angeles, CA, pp 443-493
2. SM Anderson AA Bari RC Pierce 2003 Administration of the D1-like dopamine receptor antagonist SCH-23390 into the medial nucleus accumbens shell attenuates cocaine priming-induced reinstatement of drug-seeking behavior in rats Psychopharmacology (Berl) 168 132 138
3. SM Anderson KR Famous G Sadri-Vakili V Kumaresan HD Schmidt CE Bass EF Terwilliger J-HJ Cha RC Pierce 2008 CaMKII: a biochemical bridge linking accumbens dopamine and glutamate systems in cocaine seeking Nat Neurosci 11 344 353
4. R Arikan NM Blake JP Erinjeri TA Woolsey L Giraud SM Highstein 2002 A method to measure the effective spread of focally injected muscimol into the central nervous system with electrophysiology and light microscopy J Neurosci Methods 118 51 57
5. P Bäckström P Hyytiä 2007 Involvement of AMPA/kainate, NMDA, and mGlu5 receptors in the nucleus accumbens core in cue-induced reinstatement of cocaine seeking in rats Psychopharmacology 192 4 571 580
6. D Belin BJ Everitt 2008 Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum Neuron 57 432 441
7. JM Bossert UE Ghitza L Lu DH Epstein Y Shaham 2005 Neurobiology of relapse to heroin and cocaine seeking: an update and clinical implications Eur J Pharmacol 526 36 50
8. JM Bossert SM Gray L Lu Y Shaham 2006 Activation of group II metabotropic glutamate receptors in the nucleus accumbens shell attenuates context-induced relapse to heroin seeking Neuropsychopharmacology 31 2197 2209
9. JM Bossert GC Poles KA Wihbey E Koya Y Shaham 2007 Differential effects of blockade of dopamine D1-family receptors in nucleus accumbens core or shell on reinstatement of heroin seeking induced by contextual and discrete cues J Neurosci 27 12655 12663
10. ME Carroll SD Comer 1996 Animal models of relapse Exp Clin Psychopharmacol 4 11 18
11. AR Childress AV Hole RN Ehrman SJ Robbins AT McLellan CP O'Brien 1993 Cue reactivity and cue reactivity interventions in drug dependence NIDA Res Monogr 137 73 95
12. R Ciccocioppo PP Sanna F Weiss 2001 Cocaine-predictive stimulus induces drug-seeking behavior and neural activation in limbic brain regions after multiple months of abstinence: reversal by D(1) antagonists Proc Natl Acad Sci USA 98 1976 1981
13. HS Crombag Y Shaham 2002 Renewal of drug seeking by contextual cues after prolonged extinction in rats Behav Neurosci 116 169 173
14. HS Crombag JW Grimm Y Shaham 2002 Effect of dopamine receptor antagonists on renewal of cocaine seeking by reexposure to drug-associated contextual cues Neuropsychopharmacology 27 1006 1015
15. CV Dayas TM McGranahan R Martin-Fardon F Weiss 2008 Stimuli linked to ethanol availability activate hypothalamic CART and orexin neurons in a reinstatement model of relapse Biol Psychiatry 63 152 157
16. H de Wit J Stewart 1981 Reinstatement of cocaine-reinforced responding in the rat Psychopharmacology 75 134 143
17. P Di Ciano BJ Everitt 2004 Direct interactions between the basolateral amygdala and nucleus accumbens core underlie cocaine-seeking behavior by rats J Neurosci 24 7167 7173
18. P Di Ciano RN Cardinal RA Cowell SJ Little BJ Everitt 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
19. P Di Ciano TW Robbins BJ Everitt 2008 Differential effects of nucleus accumbens core, shell, or dorsal striatal inactivations on the persistence, reacquisition, or reinstatement of responding for a drug-paired conditioned reinforcer Neuropsychopharmacology 33 1413 25
20. DH Epstein KL Preston J Stewart Y Shaham 2006 Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure Psychopharmacology (Berl) 189 1 16
21. BJ Everitt TW Robbins 2005 Neural systems of reinforcement for drug addiction: from actions to habits to compulsion Nat Neurosci 8 1481 1489
22. BJ Everitt KA Morris A O'Brien TW Robbins 1991 The basolateral amygdale-ventral striatal system and conditioned place preference: further evidence of limbic-striatal interactions underlying reward-related processes Neuroscience 42 1 18
23. J Fadel AY Deutch 2002 Anatomical substrates of orexin-dopamine interactions: lateral hypothalamic projections to the ventral tegmental area Neuroscience 111 379 387
24. J Ferbinteanu RJ McDonald 2001 Dorsal/ventral hippocampus, fornix, and conditioned place preference Hippocampus 11 187 200
25. HC Fibiger FG LePaine A Jakubovic AG Phillips 1987 The role of dopamine in intracranial self-stimulation of the ventral tegmental area J Neurosci 7 3888 3896
26. RA Fuchs RE See 2002 Basolateral amygdala inactivation abolishes conditioned stimulus- and heroin-induced reinstatement of extinguished heroin-seeking behavior in rats Psychopharmacology (Berl) 160 425 433
27. RA Fuchs LT Tran-Nguyen SE Specio RS Groff JL Neisewander 1998 Predictive validity of the extinction/reinstatement model of drug craving Psychopharmacology (Berl) 135 151 160
28. RA Fuchs KA Evans MC Parker RE See 2004 Differential involvement of the core and shell subregions of the nucleus accumbens in conditioned cue-induced reinstatement of cocaine seeking in rats Psychopharmacology (Berl) 176 459 65
29. RA Fuchs KA Evans CC Ledford MP Parker JM Case RH Mehta RE See 2005 The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats Neuropsychopharmacology 30 296 309
30. RA Fuchs RK Branham RE See 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
31. RA Fuchs JL Eaddy ZI Su GH Bell 2007 Interactions of the basolateral amygdala with the dorsal hippocampus and dorsomedial prefrontal cortex regulate drug context-induced reinstatement of cocaine-seeking in rats Eur J Neurosci 26 487 498
32. Gordon WC, Klein RL (1994) In: Animal memory. The effects of context change on retention performance. 2nd edn. Academic, San Diego, CA
33. Y Goto P O'Donnell 2002 Timing-dependent limbic-motor synaptic integration in the nucleus accumbens Proc Natl Acad Sci USA 99 13189 13193
34. JW Grimm RE See 2000 Dissociation of primary and secondary reward-relevant limbic nuclei in an animal model of relapse Neuropsychopharmacology 22 473 479
35. AS Hamlin KJ Clemens GP McNally 2008 Renewal of extinguished cocaine-seeking Neuroscience 151 659 670
36. CA Heidbreder HJ Groenewegen 2003 The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics Neurosci Biobehav Rev 27 555 579
37. L Heimer DS Zahm L Churchill PW Kalivas C Wohltmann 1991 Specificity in the projection patterns of accumbal core and shell in the rat Neuroscience 41 89 125
38. S Ikemoto 2003 Involvement of the olfactory tubercle in cocaine reward: intracranial self-administration studies J Neurosci 23 9305 11
39. S Ikemoto 2007 Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex Brain Res Rev 56 27 78
40. Institute of Laboratory Animal Resources, Commission on Life Sciences (1996) Guide for the Care and Use of Laboratory Animals. National Academy Press, Washington D.C.
41. JH Jaffe NG Cascella KM Kumor MA Sherer 1989 Cocaine-induced cocaine craving Psychopharmacology 97 59 64
42. PW Kalivas K McFarland 2003 Brain circuitry and the reinstatement of cocaine-seeking behavior Psychopharmacology (Berl) 168 44 56
43. C Kornetsky D Huston-Lyons LJ Porrino 1991 The role of the olfactory tubercle in the effects of cocaine, morphine and brain-stimulation reward Brain Res 541 75 81
44. PJ Kruzich JW Grimm NR Rustay CD Parks RE See 1999 Predicting relapse to cocaine-seeking behavior: a multiple regression approach Behav Pharmacol 10 513 521
45. C Leisen P Langguth B Herbert C Dressler A Koggel H Spahn-Langguth 2003 Lipophilicities of baclofen ester prodrugs correlate with affinities to the ATP-dependent efflux pump P-glycoprotein: relevance for their permeation across the blood-brain barrier? Pharm Res 20 772 778
46. I Léna H Dh tel C Garbay V Dauqé 2001 Involvement of D2 dopamine receptors in the opposing effects of two CCK-B agonists in a spatial recognition memory task: role of the anterior nucleus accumbens Psychopharmacology (Berl) 153 170 179
47. L Levita JW Dalley TW Robbins 2002 Disruption of Pavlovian contextual conditioning by excitotoxic lesions of the nucleus accumbens core Behav Neurosci 116 539 552
48. JH Martin 1991 Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat Neurosci Lett 127 160 164
49. JH Martin C Ghez 1999 Pharmacological inactivation in the analysis of the central control of movement J Neurosci Methods 86 145 159
50. AJ McDonald 1991 Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain Neuroscience 44 15 33
51. K McFarland PW Kalivas 2001 The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior J Neurosci 21 8655 8663
52. K McFarland SB Davidge CC Lapish PW Kalivas 2004 Limbic and motor circuitry underlying footshock-induced reinstatement of cocaine-seeking behavior J Neurosci 24 1551 1560
53. J McLaughlin RE See 2003 Selective inactivation of the dorsomedial prefrontal cortex and the basolateral amygdala attenuates conditioned-cued reinstatement of extinguished cocaine-seeking behavior in rats Psychopharmacology (Berl) 168 57 65
54. CA Miller JF Marshall 2005 Molecular substrates for retrieval and reconsolidation of cocaine-associated contextual memory Neuron 47 873 884
55. M Narita Y Nagumo S Hashimoto M Narita J Khotib M Miyatake T Sakurai M Yanagisawa T Nakamachi S Shioda T Suzuki 2006 Direct involvement of orexinergic systems in the activation of the mesolimbic dopamine pathway and related behaviors induced by morphine J Neurosci 26 398 405
56. JL Neisewander DA Baker RA Fuchs LT Tran-Nguyen A Palmer JF Marshall 2000 Fos protein expression and cocaine-seeking behavior in rats after exposure to a cocaine self-administration environment J Neurosci 20 798 805
57. JL Neisewander RA Fuchs LT Tran-Nguyen SM Webber GP Coffee JN Joyce 2004 Increases in dopamine D3 receptor binding in rats receiving a cocaine challenge at various time points after cocaine self-administration: implications for cocaine-seeking behavior Neuropsychopharmacology 29 1479 1487
58. CP O'Brien AR Childress R Ehrman SJ Robbins 1998 Conditioning factors in drug abuse: can they explain compulsion? J Psychopharmacol 12 15 22
59. P O'Donnell AA Grace 1995 Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input J Neurosci 15 3622 3639
60. JA Parkinson JW Dalley RN Cardinal A Bamford B Fehnert G Lachenal N Rudarakanchana KM Halkerston TW Robbins BJ Everitt 2002 Nucleus accumbens dopamine depletion impairs both acquisition and performance of appetitive Pavlovian approach behaviour: implications for mesoaccumbens dopamine function Behav Brain Res 137 149 163
61. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates, 3rd edn. Academic, Los Angeles, CA
62. J Peters PW Kalivas 2006 The group II metabotropic glutamate receptor agonist, LY379268, inhibits both cocaine- and food-seeking behavior in rats Psychopharmacology 186 143 149
63. J Peters J Vallone K Laurendi PW Kalivas 2007 Opposing roles for the ventral prefrontal cortex and the basolateral amygdala on the spontaneous recovery of cocaine-seeking in rats Psychopharmacology (Berl) 197 319 326
64. J Peters RT LaLumiere PW Kalivas 2008 Infralimbic prefrontal cortex is responsible for inhibiting cocaine seeking in extinguished rats J Neurosci 28 6046 6053
65. JL Rogers RE See 2007 Selective inactivation of the ventral hippocampus attenuates cue-induced and cocaine-primed reinstatement of drug-seeking in rats Neurobiol Learn Mem 87 688 692
66. F Sargolini P Roullet A Oliverio A Mele 2003 Effects of intra-accumbens focal administration of glutamate antagonists on object recognition memory in mice Behav Brain Res 138 153 63
67. HD Schmidt RC Pierce 2006 Cooperative activation of D1-like and D2-like dopamine receptors in the nucleus accumbens shell is required for the reinstatement of cocaine-seeking behavior in the rat Neuroscience 142 451 461
68. HD Schmidt SM Anderson RC Pierce 2006 Stimulation of D1-like or D2 dopamine receptors in the shell, but not the core, of the nucleus accumbens reinstates cocaine-seeking behaviour in the rat Eur J Neurosci 23 219 228
69. G Schoenbaum B Setlow 2003 Lesions of nucleus accumbens disrupt learning about aversive outcomes J Neurosci 23 9833 9841
70. RE See 2005 Neural substrates of cocaine-cue associations that trigger relapse Eur J Pharmacol 526 140 146
71. RE See JC Elliott MW Feltenstein 2007 The role of dorsal vs ventral striatal pathways in cocaine-seeking behavior after prolonged abstinence in rats Psychopharmacology (Berl) 194 321 31
72. LH Sellings LE McQuade PB Clarke 2006 Evidence for multiple sites within rat ventral striatum mediating cocaine-conditioned place preference and locomotor activation J Pharmacol Exp Ther 317 1178 87
73. SR Sesack AY Deutch RH Roth BS Bunney 1989 Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin J Comp Neurol 290 213 242
74. U Shalev JW Grimm Y Shaham 2002 Neurobiology of relapse to heroin and cocaine seeking: a review Pharmacol Rev 54 1 42
75. R Sinha 2001 How does stress increase risk of drug abuse and relapse? Psychopharmacology (Berl) 158 343 359
76. YC van Dongen JM Deniau CM Pennartz Y Galis-de Graaf P Voorn AM Thierry HJ Groenewegen 2005 Anatomical evidence for direct connections between the shell and core subregions of the rat nucleus accumbens Neuroscience 136 1049 71
77. T van Groen JM Wyss 1990 Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections J Comp Neurol 302 515 528
78. IA Yun SM Nicola HL Fields 2004 Contrasting effects of dopamine and glutamate receptor antagonist injection in the nucleus accumbens suggest a neural mechanism underlying cue-evoked goal-directed behavior Eur J Neurosci 20 249 263