Environmental living conditions introduced during forced abstinence alter cocaine-seeking behavior and Fos protein expression

Neuroscience

Volumn 171, Issue 4, 2010, Pages 1187-1196

  Thiel, K J ^a   Pentkowski, N S ^a,b   Peartree, N A ^a   Painter, M R ^a   Neisewander, J L ^b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Cocaine cues; Craving; Environmental enrichment; Immediate early gene; Incentive motivation; Neurocircuitry

Indexed keywords

COCAINE; PROTEIN FOS;

ABSTINENCE; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; CAUDATE NUCLEUS; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; HELP SEEKING BEHAVIOR; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LIMBIC SYSTEM; MALE; MOTIVATION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; ORBITAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REINFORCEMENT; STRIA TERMINALIS; SUBSTANTIA NIGRA;

ANALYSIS OF VARIANCE; ANESTHETICS, LOCAL; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; COCAINE; COCAINE-RELATED DISORDERS; CONDITIONING, OPERANT; CUES; DISEASE MODELS, ANIMAL; ENVIRONMENT; MALE; ONCOGENE PROTEINS V-FOS; RATS; RATS, SPRAGUE-DAWLEY; REINFORCEMENT (PSYCHOLOGY); REINFORCEMENT SCHEDULE; SELF ADMINISTRATION;

EID: 78650172959     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.10.001     Document Type: Article

References (80)

1. Acosta J.I., Thiel K.J., Sanabria F., Browning J.R., Neisewander J.L. Effects of schedule of reinforcement on cue-elicited reinstatement of cocaine-seeking behavior. Behav Pharmacol 2008, 19:129-136.
2. Bardo M.T., Klebaur J.E., Valone J.M., Deaton C. Environmental enrichment decreases intravenous self-administration of amphetamine in female and male rats. Psychopharmacology (Berl) 2001, 155:278-284.
3. Brown E.E., Robertson G.S., Fibiger H.C. Evidence for conditional neuronal activation following exposure to a cocaine-paired environment: role of forebrain limbic structures. J Neurosci 1992, 12:4112-4121.
4. Buffalari D.M., See R.E. Footshock stress potentiates cue-induced cocaine-seeking in an animal model of relapse. Physiol Behav 2009, 98:614-617.
5. Canales J.J. Stimulant-induced adaptations in neostriatal matrix and striosome systems: transiting from instrumental responding to habitual behavior in drug addiction. Neurobiol Learn Mem 2005, 83:93-103.
6. Carroll M.E., Anker J.J., Perry J.L. Modeling risk factors for nicotine and other drug abuse in the preclinical laboratory. Drug Alcohol Depend 2009, 104(Suppl 1):S70-S78.
7. Cavada C., Company T., Tejedor J., Cruz-Rizzolo R.J., Reinoso-Suarez F. The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb Cortex 2000, 10:220-242.
8. Chauvet C., Lardeux V., Goldberg S.R., Jaber M., Solinas M. Environmental enrichment reduces cocaine seeking and reinstatement induced by cues and stress but not by cocaine. Neuropsychopharmacology 2009, 34:2767-2778.
9. Ciccocioppo R., Sanna P.P., 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 2001, 98:1976-1981.
10. Crawford C.A., McDougall S.A., Bolanos C.A., Hall S., Berger S.P. The effects of the kappa agonist U-50,488 on cocaine-induced conditioned and unconditioned behaviors and Fos immunoreactivity. Psychopharmacology (Berl) 1995, 120:392-399.
11. Dackis C.A., O'Brien C.P. Cocaine dependence: a disease of the brain's reward centers. J Subst Abuse Treat 2001, 21:111-117.
12. de Lima M.S., de Oliveira Soares B.G., Reisser A.A., Farrell M. Pharmacological treatment of cocaine dependence: a systematic review. Addiction 2002, 97:931-949.
13. de Wit H., Stewart J. Reinstatement of cocaine-reinforced responding in the rat. Psychopharmacology (Berl) 1981, 75:134-143.
14. Dielenberg R.A., Hunt G.E., McGregor I.S. "When a rat smells a cat": the distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience 2001, 104:1085-1097.
15. Erb S. Evaluation of the relationship between anxiety during withdrawal and stress-induced reinstatement of cocaine seeking. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:798-807.
16. Everitt B.J., Belin D., Economidou D., Pelloux Y., Dalley J.W., Robbins T.W. Review. Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Philos Trans R Soc Lond B Biol Sci 2008, 363:3125-3135.
17. Everitt B.J., Robbins T.W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 2005, 8:1481-1489.
18. Feltenstein M.W., See R.E. The neurocircuitry of addiction: an overview. Br J Pharmacol 2008, 154:261-274.
19. Fuchs R.A., Branham R.K., See R.E. Different neural substrates mediate cocaine seeking after abstinence versus extinction training: a critical role for the dorsolateral caudate-putamen. J Neurosci 2006, 26:3584-3588.
20. Gawin F.H., Kleber H.D. Abstinence symptomatology and psychiatric diagnosis in cocaine abusers. Clinical observations. Arch Gen Psychiatry 1986, 43:107-113.
21. Georges F., Aston-Jones G. Potent regulation of midbrain dopamine neurons by the bed nucleus of the stria terminalis. J Neurosci 2001, 21:RC160.
22. Georges F., Aston-Jones G. Activation of ventral tegmental area cells by the bed nucleus of the stria terminalis: a novel excitatory amino acid input to midbrain dopamine neurons. J Neurosci 2002, 22:5173-5187.
23. Ghitza U.E., Fabbricatore A.T., Prokopenko V., Pawlak A.P., West M.O. Persistent cue-evoked activity of accumbens neurons after prolonged abstinence from self-administered cocaine. J Neurosci 2003, 23:7239-7245.
24. Green T.A., Alibhai I.N., Roybal C.N., Winstanley C.A., Theobald D.E., Birnbaum S.G., Graham A.R., Unterberg S., Graham D.L., Vialou V., Bass C.E., Terwilliger E.F., Bardo M.T., Nestler E.J. Environmental enrichment produces a behavioral phenotype mediated by low cyclic adenosine monophosphate response element binding (CREB) activity in the nucleus accumbens. Biol Psychiatry 2010, 67:28-35.
25. Green T.A., Gehrke B.J., Bardo M.T. Environmental enrichment decreases intravenous amphetamine self-administration in rats: dose-response functions for fixed- and progressive-ratio schedules. Psychopharmacology (Berl) 2002, 162:373-378.
26. Grimm J.W., Osincup D., Wells B., Manaois M., Fyall A., Buse C., Harkness J.H. Environmental enrichment attenuates cue-induced reinstatement of sucrose seeking in rats. Behav Pharmacol 2008, 19:777-785.
27. Hall F.S. Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Crit Rev Neurobiol 1998, 12:129-162.
28. Hamlin A.S., Clemens K.J., McNally G.P. Renewal of extinguished cocaine-seeking. Neuroscience 2008, 151:659-670.
29. Harlan R.E., Garcia M.M. Drugs of abuse and immediate-early genes in the forebrain. Mol Neurobiol 1998, 16:221-267.
30. Herrera D.G., Robertson H.A. Activation of c-fos in the brain. Prog Neurobiol 1996, 50:83-107.
31. Hollander J.A., Carelli R.M. Cocaine-associated stimuli increase cocaine seeking and activate accumbens core neurons after abstinence. J Neurosci 2007, 27:3535-3539.
32. Hotsenpiller G., Horak B.T., Wolf M.E. Dissociation of conditioned locomotion and Fos induction in response to stimuli formerly paired with cocaine. Behav Neurosci 2002, 116:634-645.
33. Howes S.R., Dalley J.W., Morrison C.H., Robbins T.W., Everitt B.J. Leftward shift in the acquisition of cocaine self-administration in isolation-reared rats: relationship to extracellular levels of dopamine, serotonin and glutamate in the nucleus accumbens and amygdala-striatal FOS expression. Psychopharmacology (Berl) 2000, 151:55-63.
34. Jog M.S., Kubota Y., Connolly C.I., Hillegaart V., Graybiel A.M. Building neural representations of habits. Science 1999, 286:1745-1749.
35. Kalivas P.W. Addiction as a pathology in prefrontal cortical regulation of corticostriatal habit circuitry. Neurotox Res 2008, 14:185-189.
36. Kalivas P.W., Volkow N.D. The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 2005, 162:1403-1413.
37. Kearns D.N., Weiss S.J. Contextual renewal of cocaine seeking in rats and its attenuation by the conditioned effects of an alternative reinforcer. Drug Alcohol Depend 2007, 90:193-202.
38. Kennerley S.W., Walton M.E., Behrens T.E., Buckley M.J., Rushworth M.F. Optimal decision making and the anterior cingulate cortex. Nat Neurosci 2006, 9:940-947.
39. Koob G.F. Brain stress systems in the amygdala and addiction. Brain Res 2009, 1293:61-75.
40. Koob G.F., Le Moal M. Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 2001, 24:97-129.
41. Krawczyk D.C. Contributions of the prefrontal cortex to the neural basis of human decision making. Neurosci Biobehav Rev 2002, 26:631-664.
42. Kufahl P.R., Zavala A.R., Singh A., Thiel K.J., Dickey E.D., Joyce J.N., Neisewander J.L. c-Fos expression associated with reinstatement of cocaine-seeking behavior by response-contingent conditioned cues. Synapse 2009, 63:823-835.
43. Laviolette S.R., Lipski W.J., Grace A.A. A subpopulation of neurons in the medial prefrontal cortex encodes emotional learning with burst and frequency codes through a dopamine D4 receptor-dependent basolateral amygdala input. J Neurosci 2005, 25:6066-6075.
44. Lu L., Grimm J.W., Hope B.T., Shaham Y. Incubation of cocaine craving after withdrawal: a review of preclinical data. Neuropharmacology 2004, 47(Suppl 1):214-226.
45. Markham J.A., Greenough W.T. Experience-driven brain plasticity: beyond the synapse. Neuron Glia Biol 2004, 1:351-363.
46. Markou A., Weiss F., Gold L.H., Caine S.B., Schulteis G., Koob G.F. Animal models of drug craving. Psychopharmacology (Berl) 1993, 112:163-182.
47. McFarland K., Davidge S.B., Lapish C.C., Kalivas P.W. Limbic and motor circuitry underlying footshock-induced reinstatement of cocaine-seeking behavior. J Neurosci 2004, 24:1551-1560.
48. McGinty J.F., Whitfield T.W., Berglind W.J. Brain-derived neurotrophic factor and cocaine addiction. Brain Res 2010, 1314:183-193.
49. McLellan A.T., Lewis D.C., O'Brien C.P., Kleber H.D. Drug dependence, a chronic medical illness: implications for treatment, insurance, and outcomes evaluation. JAMA 2000, 284:1689-1695.
50. Neisewander J.L., Baker D.A., Fuchs R.A., Tran-Nguyen L.T., Palmer A., Marshall J.F. Fos protein expression and cocaine-seeking behavior in rats after exposure to a cocaine self-administration environment. J Neurosci 2000, 20:798-805.
51. O'Brien C.P. Anticraving medications for relapse prevention: a possible new class of psychoactive medications. Am J Psychiatry 2005, 162:1423-1431.
52. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, San Diego, CA.
53. Rushworth M.F., Walton M.E., Kennerley S.W., Bannerman D.M. Action sets and decisions in the medial frontal cortex. Trends Cogn Sci 2004, 8:410-417.
54. Schoenbaum G., Setlow B. Cocaine makes actions insensitive to outcomes but not extinction: implications for altered orbitofrontal-amygdalar function. Cereb Cortex 2005, 15:1162-1169.
55. Schoenbaum G., Setlow B., Saddoris M.P., Gallagher M. Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron 2003, 39:855-867.
56. See R.E., Elliott J.C., Feltenstein M.W. The role of dorsal vs ventral striatal pathways in cocaine-seeking behavior after prolonged abstinence in rats. Psychopharmacology (Berl) 2007, 194:321-331.
57. Sesack S.R., Grace A.A. Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 2010, 35:27-47.
58. Shaham Y., Erb S., Stewart J. Stress-induced relapse to heroin and cocaine seeking in rats: a review. Brain Res Brain Res Rev 2000, 33:13-33.
59. Shalev U., Grimm J.W., Shaham Y. Neurobiology of relapse to heroin and cocaine seeking: a review. Pharmacol Rev 2002, 54:1-42.
60. Smith M.A., Schmidt K.T., Iordanou J.C., Mustroph M.L. Aerobic exercise decreases the positive-reinforcing effects of cocaine. Drug Alcohol Depend 2008, 98:129-135.
61. Sofuoglu M., Kosten T.R. Pharmacologic management of relapse prevention in addictive disorders. Psychiatr Clin North Am 2004, 27:627-648.
62. Solinas M., Chauvet C., Thiriet N., El Rawas R., Jaber M. Reversal of cocaine addiction by environmental enrichment. Proc Natl Acad Sci U S A 2008, 105:17145-17150.
63. Solinas M., Thiriet N., El Rawas R., Lardeux V., Jaber M. Environmental enrichment during early stages of life reduces the behavioral, neurochemical, and molecular effects of cocaine. Neuropsychopharmacology 2009, 34:1102-1111.
64. Stairs D.J., Bardo M.T. Neurobehavioral effects of environmental enrichment and drug abuse vulnerability. Pharmacol Biochem Behav 2009, 92:377-382.
65. Stairs D.J., Klein E.D., Bardo M.T. Effects of environmental enrichment on extinction and reinstatement of amphetamine self-administration and sucrose-maintained responding. Behav Pharmacol 2006, 17:597-604.
66. Stalnaker T.A., Franz T.M., Singh T., Schoenbaum G. Basolateral amygdala lesions abolish orbitofrontal-dependent reversal impairments. Neuron 2007, 54:51-58.
67. Thiel KJ, Engelhardt B, Hood LE, Peartree NA, Neisewander JL (in press) The interactive effects of environmental enrichment and extinction interventions in attenuating cue-elicited cocaine-seeking behavior in rats. Pharmacol Biochem Behav; doi:10.1016/j.pbb.2010.09.014.
68. Thiel K.J., Sanabria F., Pentkowski N.S., Neisewander J.L. Anti-craving effects of environmental enrichment. Int J Neuropsychopharmacol 2009, 12:1151-1156.
69. Thomas M.J., Kalivas P.W., Shaham Y. Neuroplasticity in the mesolimbic dopamine system and cocaine addiction. Br J Pharmacol 2008, 154:327-342.
70. Tiffany S.T., Carter B.L. Is craving the source of compulsive drug use?. J Psychopharmacol 1998, 12:23-30.
71. van Praag H., Kempermann G., Gage F.H. Neural consequences of environmental enrichment. Nat Rev Neurosci 2000, 1:191-198.
72. Vanderschuren L.J., Di Ciano P., Everitt B.J. Involvement of the dorsal striatum in cue-controlled cocaine seeking. J Neurosci 2005, 25:8665-8670.
73. Volkow N.D., Fowler J.S. Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. Cereb Cortex 2000, 10:318-325.
74. Volkow N.D., Wang G.J., Telang F., Fowler J.S., Logan J., Childress A.R., Jayne M., Ma Y., Wong C. Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. J Neurosci 2006, 26:6583-6588.
75. Winstanley C.A. The orbitofrontal cortex, impulsivity, and addiction: probing orbitofrontal dysfunction at the neural, neurochemical, and molecular level. Ann N Y Acad Sci 2007, 1121:639-655.
76. Wise R.A. Ventral tegmental glutamate: a role in stress-, cue-, and cocaine-induced reinstatement of cocaine-seeking. Neuropharmacology 2009, 56(Suppl 1):174-176.
77. Zahm D.S. The evolving theory of basal forebrain functional-anatomical "macrosystems". Neurosci Biobehav Rev 2006, 30:148-172.
78. Zavala A.R., Biswas S., Harlan R.E., Neisewander J.L. Fos and glutamate AMPA receptor subunit coexpression associated with cue-elicited cocaine-seeking behavior in abstinent rats. Neuroscience 2007, 145:438-452.
79. Zavala A.R., Browning J.R., Dickey E.D., Biswas S., Neisewander J.L. Region specific involvement of AMPA/Kainate receptors in Fos protein expression induced by cocaine-conditioned cues. Eur Neuropsychopharmacol 2008, 18:600-611.
80. Zlebnik N.E., Anker J.J., Gliddon L.A., Carroll M.E. Reduction of extinction and reinstatement of cocaine seeking by wheel running in female rats. Psychopharmacology (Berl) 2010, 209:113-125.