Role of ventral medial prefrontal cortex in incubation of cocaine craving

Neuropharmacology

Volumn 56, Issue SUPPL. 1, 2009, Pages 177-185

  Koya, Eisuke ^a   Uejima, Jamie L ^a   Wihbey, Kristina A ^a   Bossert, Jennifer M ^a   Hope, Bruce T ^a   Shaham, Yavin ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

Cocaine self administration; Craving; Drug cues; ERK; Extinction; Prefrontal cortex; Reinstatement; Relapse

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; COCAINE; MITOGEN ACTIVATED PROTEIN KINASE; MUSCIMOL; SACLOFEN;

ARTICLE; ASSOCIATION; COCAINE DEPENDENCE; DRUG SELF ADMINISTRATION; ENZYME PHOSPHORYLATION; HUMAN; NERVE CELL EXCITABILITY; NEUROMODULATION; NONHUMAN; PATHOPHYSIOLOGY; PREFRONTAL CORTEX; PRIORITY JOURNAL; REINFORCEMENT; WITHDRAWAL SYNDROME;

ANIMALS; BACLOFEN; BEHAVIOR, ADDICTIVE; BEHAVIOR, ANIMAL; BICUCULLINE; COCAINE; CONDITIONING, OPERANT; CUES; DOPAMINE UPTAKE INHIBITORS; EXTINCTION, PSYCHOLOGICAL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GABA AGONISTS; GABA ANTAGONISTS; MALE; MUSCIMOL; PREFRONTAL CORTEX; RATS; RATS, LONG-EVANS; SELF ADMINISTRATION; SUCROSE; SWEETENING AGENTS; TIME FACTORS;

EID: 58149083606     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2008.04.022     Document Type: Article

References (83)

1. Ahmed S.H., and Koob G.F. Transition to drug addiction: a negative reinforcement model based on an allostatic decrease in reward function. Psychopharmacology 180 (2005) 473-490
2. Ahmed S.H., Lutjens R., van der Stap L.D., Lekic D., Romano-Spica V., Morales M., Koob G.F., Repunte-Canonigo V., and Sanna P.P. Gene expression evidence for remodeling of lateral hypothalamic circuitry in cocaine addiction. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 11533-11538
3. Akirav I., Raizel H., and Maroun M. Enhancement of conditioned fear extinction by infusion of the GABA agonist muscimol into the rat prefrontal cortex and amygdala. Eur. J. Neurosci. 23 (2006) 758-764
4. Berendse H.W., Galis-de Graaf Y., and Groenewegen H.J. Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J. Comp. Neurol. 316 (1992) 314-347
5. Bienkowski P., Rogowski A., Korkosz A., Mierzejewski P., Radwanska K., Kaczmarek L., Bogucka-Bonikowska A., and Kostowski W. Time-dependent changes in alcohol-seeking behaviour during abstinence. Eur. Neuropsychopharmacol 14 (2004) 355-360
6. Blaschke M., Keller B.U., Rivosecchi R., Hollmann M., Heinemann S., and Konnerth A. A single amino acid determines the subunit-specific spider toxin block of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate/kainate receptor channels. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 6528-6532
7. Bouton M.E., and Swartzentruber D. Sources of relapse after extinction in Pavlovian and instrumental learning. Clin. Psychol. Rev. 11 (1991) 123-140
8. Capriles N., Rodaros D., Sorge R.E., and Stewart J. A role for the prefrontal cortex in stress- and cocaine-induced reinstatement of cocaine seeking in rats. Psychopharmacology 168 (2003) 66-74
9. Childress A.R., Mozley P.D., McElgin W., Fitzgerald J., Reivich M., and O'Brien C.P. Limbic activation during cue-induced cocaine craving. Am. J. Psychiatry 156 (1999) 11-18
10. Ciccocioppo R., Sanna P.P., and Weiss F. 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. U.S.A. 98 (2001) 1976-1981
11. Conrad K.L., Tseng K.Y., Uejima J.L., Reimers J.R., Heng L.J., Shaham Y., Marinelli M., and Wolf M.E. Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature (2008) in press, doi:10.1038\nature.06995
12. Corcoran K.A., and Quirk G.J. Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J. Neurosci. 27 (2007) 840-844
13. Crombag, H., Bossert, J.M., Koya, E., Shaham, Y., in press. Context-induced relapse to drug seeking: a review. Trans. R. Soc. Lond. B: Biol. Sci. (in press).
14. Crombag H., Grimm J.W., and Shaham Y. Effect of dopamine receptor antagonists on renewal of cocaine seeking by reexposure to drug-associated contextual cues. Neuropsychopharmacology 27 (2002) 1007-1016
15. 2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr. Opin. Neurobiol. 16 (2006) 288-297
16. Di Ciano P., and Everitt B.J. Conditioned reinforcing properties of stimuli paired with self-administered cocaine, heroin or sucrose: implications for the persistence of addictive behaviour. Neuropharmacology 47 Suppl 1 (2004) 202-213
17. Epstein D.H., Preston K.L., Stewart J., and Shaham Y. Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure. Psychopharmacology 189 (2006) 1-16
18. Ferrario C.R., Gorny G., Crombag H.S., Li Y., Kolb B., and Robinson T.E. Neural and behavioral plasticity associated with the transition from controlled to escalated cocaine use. Biol. Psychiatry 58 (2005) 751-759
19. Fuchs R.A., Branham R.K., and See R.E. Different neural substrates mediate cocaine seeking after abstinence versus extinction training: a critical role for the dorsolateral caudate-putamen. J. Neurosci. 26 (2006) 3584-3588
20. Fuchs R.A., Evans K.A., Ledford C.C., Parker M.P., Case J.M., Mehta R.H., and See R.E. The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats. Neuropsychopharmacology 30 (2005) 296-309
21. Gawin F.H., and Kleber H.D. Abstinence symptomatology and psychiatric diagnosis in cocaine abusers. Clinical observations. Arch. Gen. Psychiatry 43 (1986) 107-113
22. Girault J.A., Valjent E., Caboche J., and Herve D. ERK2: a logical AND gate critical for drug-induced plasticity?. Curr. Opin. Pharmacol. 7 (2007) 77-85
23. Grimm J.W., Fyall A.M., and Osincup D.P. Incubation of sucrose craving: effects of reduced training and sucrose pre-loading. Physiol. Behav. 84 (2005) 73-79
24. Grimm J.W., Hope B.T., Wise R.A., and Shaham Y. Incubation of cocaine craving after withdrawal. Nature 412 (2001) 141-142
25. Grimm J.W., Lu L., Hayashi T., Hope B.T., Su T.P., and Shaham Y. Time-dependent increases in brain-derived neurotrophic factor protein levels within the mesolimbic dopamine system after withdrawal from cocaine: implications for incubation of cocaine craving. J. Neurosci. 23 (2003) 742-747
26. Grimm J.W., Shaham Y., and Hope B.T. Effect of the cocaine and sucrose withdrawal period on extinction behavior, cue-induced reinstatement and protein levels of the dopamine transporter and tyrosine hydroxylase in limbic and cortical areas in rats. Behav. Pharmacol. 13 (2002) 379-388
27. Herremans A.H., Hijzen T.H., Welborn P.F., Olivier B., and Slangen J.L. Effects of infusion of cholinergic drugs into the prefrontal cortex area on delayed matching to position performance in the rat. Brain Res. 711 (1996) 102-111
28. Hollander J.A., and Carelli R.M. Cocaine-associated stimuli increase cocaine seeking and activate accumbens core neurons after abstinence. J. Neurosci. 27 (2007) 3535-3539
29. Jasmin L., Rabkin S.D., Granato A., Boudah A., and Ohara P.T. Analgesia and hyperalgesia from GABA-mediated modulation of the cerebral cortex. Nature 424 (2003) 316-320
30. Jentsch J.D., and Taylor J.R. Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Psychopharmacology 146 (1999) 373-390
31. Kalivas P.W., Peters J., and Knackstedt L. Animal models and brain circuits in drug addiction. Mol. Interv. 6 (2006) 339-344
32. Kalivas P.W., Volkow N., and Seamans J. Unmanageable motivation in addiction: a pathology in prefrontal-accumbens glutamate transmission. Neuron 45 (2005) 647-650
33. Kippin T.E., Fuchs R.A., and See R.E. Contributions of prolonged contingent and noncontingent cocaine exposure to enhanced reinstatement of cocaine seeking in rats. Psychopharmacology 187 (2006) 60-67
34. Kiyatkin E.A. Chemoreactive properties of neurons of the medial thalamus in rats during urethane narcosis, wakefulness and restraint stress. J. Higher Nerv. Activity 35 (1985) 146-154
35. Kiyatkin E.A., and Rebec G.V. Impulse activity of ventral tegmental area neurons during heroin self-administration in rats. Neuroscience 102 (2001) 565-580
36. Kosten, T.R., Kosten, T.A., Poling, J., Oliveto, A., 2005. "Incubation" of cocaine relapse during a disulfiram clinical trial. CPDD, Annual Meeting Abstracts, p. 90.
37. Kreuter J.D., Mattson B.J., Wang B., You Z.B., and Hope B.T. Cocaine-induced Fos expression in rat striatum is blocked by chloral hydrate or urethane. Neuroscience 127 (2004) 233-242
38. Lee J.L., Milton A.L., and Everitt B.J. Cue-induced cocaine seeking and relapse are reduced by disruption of drug memory reconsolidation. J. Neurosci. 26 (2006) 5881-5887
39. Lu L., Dempsey J., Liu S.Y., Bossert J.M., and Shaham Y. A single infusion of brain-derived neurotrophic factor into the ventral tegmental area induces long-lasting potentiation of cocaine seeking after withdrawal. J. Neurosci. 24 (2004) 1604-1611
40. Lu L., Grimm J.W., Dempsey J., and Shaham Y. Cocaine seeking over extended withdrawal periods in rats: different time courses of responding induced by cocaine cues versus cocaine priming over the first 6 months. Psychopharmacology 176 (2004) 101-108
41. Lu L., Grimm J.W., Hope B.T., and Shaham Y. Incubation of cocaine craving after withdrawal: a review of preclinical data. Neuropharmacology 47 Suppl 1 (2004) 214-226
42. Lu L., Hope B.T., Dempsey J., Liu S.Y., Bossert J.M., and Shaham Y. Central amygdala ERK signaling pathway is critical to incubation of cocaine craving. Nat. Neurosci. 8 (2005) 212-219
43. Lu L., Koya E., Zhai H., Hope B.T., and Shaham Y. Role of ERK in cocaine addiction. Trends Neurosci. 29 (2006) 695-703
44. Lu L., Uejima J.L., Gray S.M., Bossert J.M., and Shaham Y. Systemic and central amygdala injections of the mGluR(2/3) agonist LY379268 attenuate the expression of incubation of cocaine craving. Biol. Psychiatry 61 (2007) 591-598
45. Maas L.C., Lukas S.E., Kaufman M.J., Weiss R.D., Daniels S.L., Rogers V.W., Kukes T.J., and Renshaw P.F. Functional magnetic resonance imaging of human brain activation during cue-induced cocaine craving. Am. J. Psychiatry 155 (1998) 124-126
46. Mattson B.J., Bossert J.M., Simmons D.E., Nozaki N., Nagarkar D., Kreuter J.D., and Hope B.T. Cocaine-induced CREB phosphorylation in nucleus accumbens of cocaine-sensitized rats is enabled by enhanced activation of extracellular signal-related kinase, but not protein kinase. A.J. Neurochem. 95 (2005) 1481-1494
47. McDonald A.J., Mascagni F., and Guo L. Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 71 (1996) 55-75
48. McFarland K., and Kalivas P.W. The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior. J. Neurosci. 21 (2001) 8655-8663
49. McLaughlin J., and See R.E. Selective inactivation of the dorsomedial prefrontal cortex and the basolateral amygdala attenuates conditioned-cued reinstatement of extinguished cocaine-seeking behavior in rats. Psychopharmacology 168 (2003) 57-65
50. Mead A.N., Zamanillo D., Becker N., and Stephens D.N. AMPA-receptor GluR1 subunits are involved in the control over behavior by cocaine-paired cues. Neuropsychopharmacology 32 (2007) 343-353
51. Milad M.R., and Quirk G.J. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420 (2002) 70-74
52. Miller C.A., and Marshall J.F. Molecular substrates for retrieval and reconsolidation of cocaine-associated contextual memory. Neuron 47 (2005) 873-884
53. Mueller D., Porter J.T., and Quirk G.J. Noradrenergic signaling in infralimbic cortex increases cell excitability and strengthens memory for fear extinction. J. Neurosci. 28 (2008) 369-375
54. Neisewander J.L., Baker D.A., Fuchs R.A., Tran-Nguyen L.T., Palmer A., and Marshall J.F. Fos protein expression and cocaine-seeking behavior in rats after exposure to a cocaine self-administration environment. J. Neurosci. 20 (2000) 798-805
55. O'Brien C.P. Anticraving medications for relapse prevention: a possible new class of psychoactive medications. Am. J. Psychiatry. 162 (2005) 1423-1431
56. Peters J., Vallone J., Laurendi K., and Kalivas P.W. Opposing roles for the ventral prefrontal cortex and the basolateral amygdala on the spontaneous recovery of cocaine-seeking in rats. Psychopharmacology 197 (2008) 319-326
57. Petrovich G.D., and Gallagher M. Control of food consumption by learned cues: a forebrain-hypothalamic network. Physiol.Behav. 91 (2007) 397-403
58. Petrovich G.D., Ross C.A., Holland P.C., and Gallagher M. Medial prefrontal cortex is necessary for an appetitive contextual conditioned stimulus to promote eating in sated rats. J. Neurosci. 27 (2007) 6436-6441
59. Quirk G.J., Likhtik E., Pelletier J.G., and Pare D. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J. Neurosci. 23 (2003) 8800-8807
60. Quirk G.J., and Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33 (2008) 56-72
61. Rhodes S.E., and Killcross S. Lesions of rat infralimbic cortex enhance recovery and reinstatement of an appetitive Pavlovian response. Learn. Mem. 11 (2004) 611-616
62. Rogers J.L., Ghee S., and See R.E. The neural circuitry underlying reinstatement of heroin-seeking behavior in an animal model of relapse. Neuroscience 151 (2008) 579-588
63. Schmidt E.F., Sutton M.A., Schad C.A., Karanian D.A., Brodkin E.S., and Self D.W. Extinction training regulates tyrosine hydroxylase during withdrawal from cocaine self-administration. J. Neurosci. 21 (2001) RC137
64. See R.E. Neural substrates of conditioned-cued relapse to drug-seeking behavior. Pharmacol. Biochem. Behav. 71 (2002) 517-529
65. See R.E., Elliott J.C., and Feltenstein M.W. The role of dorsal vs ventral striatal pathways in cocaine-seeking behavior after prolonged abstinence in rats. Psychopharmacology 194 (2007) 321-331
66. Self D.W., Choi K.H., Simmons D., Walker J.R., and Smagula C.S. Extinction training regulates neuroadaptive responses to withdrawal from chronic cocaine self-administration. Learn. Mem. 11 (2004) 648-657
67. Shaham Y., Rajabi H., and Stewart J. Relapse to heroin-seeking under opioid maintenance: the effects of opioid withdrawal, heroin priming and stress. J. Neurosci. 16 (1996) 1957-1963
68. Shaham Y., Shalev U., Lu L., De Wit H., and Stewart J. The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology 168 (2003) 3-20
69. Shalev U., Grimm J.W., and Shaham Y. Neurobiology of relapse to heroin and cocaine seeking: a review. Pharmacol. Rev. 54 (2002) 1-42
70. Shalev U., Morales M., Hope B., Yap J., and Shaham Y. Time-dependent changes in extinction behavior and stress-induced reinstatement of drug seeking following withdrawal from heroin in rats. Psychopharmacology 156 (2001) 98-107
71. Shepard J.D., Bossert J.M., Liu S.Y., and Shaham Y. The anxiogenic drug yohimbine reinstates methamphetamine seeking in a rat model of drug relapse. Biol. Psychiatry 55 (2004) 1082-1089
72. Sierra-Mercado Jr. D., Corcoran K.A., Lebron-Milad K., and Quirk G.J. Inactivation of the ventromedial prefrontal cortex reduces expression of conditioned fear and impairs subsequent recall of extinction. Eur. J. Neurosci. 24 (2006) 1751-1758
73. Sorge R.E., and Stewart J. The contribution of drug history and time since termination of drug taking to footshock stress-induced cocaine seeking in rats. Psychopharmacology 183 (2005) 210-217
74. Stewart J., and de Wit H. Reinstatement of drug-taking behavior as a method of assessing incentive motivational properties of drugs. In: Bozarth M.A. (Ed). Methods of Assessing the Reinforcing Properties of Abused Drugs (1987), Springer-Verlag, New York 211-227
75. Sutton M.A., Schmidt E.F., Choi K.H., Schad C.A., Whisler K., Simmons D., Karanian D.A., Monteggia L.M., Neve R.L., and Self D.W. Extinction-induced upregulation in AMPA receptors reduces cocaine-seeking behaviour. Nature 421 (2003) 70-75
76. Swanson L.W. Brain Maps: Structure of the Rat Brain (1998), Elsevier, Amsterdam
77. Thomas G.M., and Huganir R.L. MAPK cascade signalling and synaptic plasticity. Nat. Rev. Neurosci. 5 (2004) 173-183
78. Valjent E., Corvol J.C., Pages C., Besson M.J., Maldonado R., and Caboche J. Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties. J. Neurosci. 20 (2000) 8701-8709
79. Van den Oever, M.C., Gouriounova, M., Li, K.W., Van der Schors, R.C., Binnekade, R., Schoffelmeer, A.N.M., Mansvelder, H.D., Smit, A.B., Spijker, S., De Vries, T.J., in press. Prefrontal cortex AMPA receptor plasticity is critical for cue-induced relapse to heroin seeking. Nat. Neurosci.
80. Van Eden C.G., and Uylings H.B. Cytoarchitectonic development of the prefrontal cortex in the rat. J. Comp. Neurol. 241 (1985) 253-267
81. Voorn P., Vanderschuren L.J., Groenewegen H.J., Robbins T.W., and Pennartz C.M. Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci. 27 (2004) 468-474
82. Windels F., and Kiyatkin E.A. Dopamine action in the substantia nigra pars reticulata: iontophoretic studies in awake, unrestrained rats. Eur. J. Neurosci. 24 (2006) 1385-1394
83. Youtz R.E.P. The change with time of a Thorndikian response in the rat. J. Exp. Psychol. 23 (1938) 128-140