Prelimbic and infralimbic cortical regions differentially encode cocaine-associated stimuli and cocaine-seeking before and following abstinence

European Journal of Neuroscience

Volumn 39, Issue 11, 2014, Pages 1891-1902

  West, Elizabeth A ^a   Saddoris, Michael P ^a   Kerfoot, Erin C ^a   Carelli, Regina M ^a,b  

^a University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Behavior; Craving; Electrophysiology; Relapse; Self administration

Indexed keywords

ABSTINENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; CELL POPULATION; CELLULAR DISTRIBUTION; COCAINE DEPENDENCE; CONTROLLED STUDY; DRUG SEEKING BEHAVIOR; DRUG SELF ADMINISTRATION; INFRALIMBIC CORTEX; MALE; NEUROPATHOLOGY; NONHUMAN; PREFRONTAL CORTEX; PRELIMBIC CORTEX; PRIORITY JOURNAL; RAT; STATE DEPENDENT LEARNING; ACTION POTENTIAL; ANIMAL; ANTIBODY SPECIFICITY; ASSOCIATION; CONDITIONED REFLEX; CYTOLOGY; DRUG EFFECTS; LEARNING; LIMBIC SYSTEM; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; REINFORCEMENT; SPRAGUE DAWLEY RAT; TIME FACTOR;

COCAINE;

ACTION POTENTIALS; ANIMALS; COCAINE; COCAINE-RELATED DISORDERS; CONDITIONING, CLASSICAL; CUES; DRUG-SEEKING BEHAVIOR; EXTINCTION, PSYCHOLOGICAL; GENERALIZATION (PSYCHOLOGY); LIMBIC SYSTEM; MALE; NEURONS; ORGAN SPECIFICITY; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; SELF ADMINISTRATION; TIME FACTORS;

EID: 84901689588     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12578     Document Type: Article

References (68)

1. Ahmed, S.H., Lenoir, M. & Guillem, K. (2013) Neurobiology of addiction versus drug use driven by lack of choice. Curr. Opin. Neurobiol., 23, 581-587.
2. Ball, K.T. & Slane, M. (2012) Differential involvement of prelimbic and infralimbic medial prefrontal cortex in discrete cue-induced reinstatement of 3, 4-methylenedioxymethamphetamine (MDMA; ecstasy) seeking in rats. Psychopharmacology, 224, 377-385.
3. Berglind, W.J., Whitfield, T.W. Jr., LaLumiere, R.T., Kalivas, P.W. & McGinty, J.F. (2009) A single intra-PFC infusion of BDNF prevents cocaine-induced alterations in extracellular glutamate within the nucleus accumbens. J. Neurosci., 29, 3715-3719.
4. Bonson, K.R., Grant, S.J., Contoreggi, C.S., Links, J.M., Metcalfe, J., Weyl, H.L., Kurian, V., Ernst, M. & London, E.D. (2002) Neural systems and cue-induced cocaine craving. Neuropsychopharmacology, 26, 376-386.
5. Cameron, C.M. & Carelli, R.M. (2012) Cocaine abstinence alters nucleus accumbens firing dynamics during goal-directed behaviors for cocaine and sucrose. Eur. J. Neurosci., 35, 940-951.
6. Carelli, R.M. (2000) Activation of accumbens cell firing by stimuli associated with cocaine delivery during self-administration. Synapse, 35, 238-242.
7. Carelli, R.M. & Ijames, S.G. (2001) Selective activation of accumbens neurons by cocaine-associated stimuli during a water/cocaine multiple schedule. Brain Res., 907, 156-161.
8. Carelli, R.M. & Wondolowski, J. (2003) Selective encoding of cocaine versus natural rewards by nucleus accumbens neurons is not related to chronic drug exposure. J. Neurosci., 23, 11214-11223.
9. Carelli, R.M., Ijames, S.G. & Crumling, A.J. (2000) Evidence that separate neural circuits in the nucleus accumbens encode cocaine versus "natural" (water and food) reward. J. Neurosci., 20, 4255-4266.
10. Chang, J.Y., Janak, P.H. & Woodward, D.J. (2000) Neuronal and behavioral correlations in the medial prefrontal cortex and nucleus accumbens during cocaine self-administration by rats. Neuroscience, 99, 433-443.
11. Chen, B.T., Yau, H.J., Hatch, C., Kusumoto-Yoshida, I., Cho, S.L., Hopf, F.W. & Bonci, A. (2013) Rescuing cocaine-induced prefrontal cortex hypoactivity prevents compulsive cocaine seeking. Nature, 496, 359-362.
12. Conrad, K.L., Tseng, K.Y., Uejima, J.L., Reimers, J.M., Heng, L.J., Shaham, Y., Marinelli, M. & Wolf, M.E. (2008) Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature, 454, 118-121.
13. Day, J.J., Jones, J.L. & Carelli, R.M. (2011) Nucleus accumbens neurons encode predicted and ongoing reward costs in rats. Eur. J. Neurosci., 33, 308-321.
14. Franklin, T.R., Acton, P.D., Maldjian, J.A., Gray, J.D., Croft, J.R., Dackis, C.A., O'Brien, C.P. & Childress, A.R. (2002) Decreased gray matter concentration in the insular, orbitofrontal, cingulate, and temporal cortices of cocaine patients. Biol. Psychiat., 51, 134-142.
15. Fuchs, R.A., Evans, K.A., Parker, M.C. & See, R.E. (2004) Differential involvement of the core and shell subregions of the nucleus accumbens in conditioned cue-induced reinstatement of cocaine seeking in rats. Psychopharmacology, 176, 459-465.
16. Gawin, F.H. (1991) Cocaine addiction: psychology and neurophysiology. Science, 251, 1580-1586.
17. George, O., Mandyam, C.D., Wee, S. & Koob, G.F. (2008) Extended access to cocaine self-administration produces long-lasting prefrontal cortex-dependent working memory impairments. Neuropsychopharmacology, 33, 2474-2482.
18. Ghitza, U.E., Fabbricatore, A.T., Prokopenko, V., Pawlak, A.P. & West, M.O. (2003) Persistent cue-evoked activity of accumbens neurons after prolonged abstinence from self-administered cocaine. J. Neurosci., 23, 7239-7245.
19. Gipson, C.D., Kupchik, Y.M., Shen, H., Reissner, K.J., Thomas, C.A. & Kalivas, P.W. (2013) Relapse induced by cues predicting cocaine depends on rapid, transient synaptic potentiation. Neuron, 77, 867-872.
20. Goldstein, R.Z. & Volkow, N.D. (2002) Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am. J. Psychiat., 159, 1642-1652.
21. Goldstein, R.Z. & Volkow, N.D. (2011) Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat. Rev. Neurosci., 12, 652-669.
22. Grimm, J.W., Hope, B.T., Wise, R.A. & Shaham, Y. (2001) Neuroadaptation. Incubation of cocaine craving after withdrawal. Nature, 412, 141-142.
23. Guillem, K., Ahmed, S.H. & Peoples, L.L. (2013) Escalation of cocaine intake and incubation of cocaine seeking are correlated with dissociable neuronal processes in different accumbens subregions. Biol. Psychiat., doi: 10.1016/j.biopsych.2013.08.032. [Epub ahead of print].
24. Heidbreder, C.A. & Groenewegen, H.J. (2003) The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci. Biobehav. R., 27, 555-579.
25. Hollander, J.A. & Carelli, R.M. (2005) Abstinence from cocaine self-administration heightens neural encoding of goal-directed behaviors in the accumbens. Neuropsychopharmacology, 30, 1464-1474.
26. Hollander, J.A. & Carelli, R.M. (2007) Cocaine-associated stimuli increase cocaine seeking and activate accumbens core neurons after abstinence. J. Neurosci., 27, 3535-3539.
27. Kalivas, P.W. (2007) Cocaine and amphetamine-like psychostimulants: neurocircuitry and glutamate neuroplasticity. Dialogues Clin. Neurosci., 9, 389-397.
28. Kalivas, P.W. (2008) Addiction as a pathology in prefrontal cortical regulation of corticostriatal habit circuitry. Neurotox. Res., 14, 185-189.
29. Koob, G.F. & Le Moal, M. (2008) Addiction and the brain antireward system. Annu. Rev. Psychol., 59, 29-53.
30. Koob, G.F. & Volkow, N.D. (2010) Neurocircuitry of addiction. Neuropsychopharmacology, 35, 217-238.
31. Koya, E., Uejima, J.L., Wihbey, K.A., Bossert, J.M., Hope, B.T. & Shaham, Y. (2009) Role of ventral medial prefrontal cortex in incubation of cocaine craving. Neuropharmacology, 56(Suppl 1), 177-185.
32. LaLumiere, R.T. & Kalivas, P.W. (2008) Glutamate release in the nucleus accumbens core is necessary for heroin seeking. J. Neurosci., 28, 3170-3177.
33. LaLumiere, R.T., Smith, K.C. & Kalivas, P.W. (2012) Neural circuit competition in cocaine-seeking: roles of the infralimbic cortex and nucleus accumbens shell. Eur. J. Neurosci., 35, 614-622.
34. Lasseter, H.C., Ramirez, D.R., Xie, X. & Fuchs, R.A. (2009) Involvement of the lateral orbitofrontal cortex in drug context-induced reinstatement of cocaine-seeking behavior in rats. Eur. J. Neurosci., 30, 1370-1381.
35. Lasseter, H.C., Xie, X., Ramirez, D.R. & Fuchs, R.A. (2010) Prefrontal cortical regulation of drug seeking in animal models of drug relapse. Curr. Top. Behav. Neurosci., 3, 101-117.
36. Lenoir, M., Augier, E., Vouillac, C. & Ahmed, S.H. (2013) A choice-based screening method for compulsive drug users in rats. Curr. Protoc. Neurosci., 64, 9.44.1-9.44.17.
37. Maas, L.C., Lukas, S.E., Kaufman, M.J., Weiss, R.D., Daniels, S.L., Rogers, V.W., Kukes, T.J. & Renshaw, P.F. (1998) Functional magnetic resonance imaging of human brain activation during cue-induced cocaine craving. Am. J. Psychiat., 155, 124-126.
38. Matochik, J.A., London, E.D., Eldreth, D.A., Cadet, J.L. & Bolla, K.I. (2003) Frontal cortical tissue composition in abstinent cocaine abusers: a magnetic resonance imaging study. NeuroImage, 19, 1095-1102.
39. McFarland, K., Lapish, C.C. & Kalivas, P.W. (2003) Prefrontal glutamate release into the core of the nucleus accumbens mediates cocaine-induced reinstatement of drug-seeking behavior. J. Neurosci., 23, 3531-3537.
40. McGeorge, A.J. & Faull, R.L. (1989) The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience, 29, 503-537.
41. McGinty, J.F., Whitfield, T.W. Jr. & Berglind, W.J. (2010) Brain-derived neurotrophic factor and cocaine addiction. Brain Res., 1314, 183-193.
42. McLaughlin, J. & See, R.E. (2003) Selective inactivation of the dorsomedial prefrontal cortex and the basolateral amygdala attenuates conditioned-cued reinstatement of extinguished cocaine-seeking behavior in rats. Psychopharmacology, 168, 57-65.
43. Moussawi, K., Zhou, W., Shen, H., Reichel, C.M., See, R.E., Carr, D.B. & Kalivas, P.W. (2010) Reversing cocaine-induced synaptic potentiation provides enduring protection from relapse. Proc. Natl. Acad. Sci. USA, 108, 385-390.
44. Moussawi, K., Zhou, W., Shen, H., Reichel, C.M., See, R.E., Carr, D.B. & Kalivas, P.W. (2011) Reversing cocaine-induced synaptic potentiation provides enduring protection from relapse. Proc. Natl. Acad. Sci. USA, 108, 385-390.
45. O'Brien, C.P. (1997) A range of research-based pharmacotherapies for addiction. Science, 278, 66-70.
46. Ongur, D. & Price, J.L. (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb. Cortex, 10, 206-219.
47. Owesson-White, C.A., Ariansen, J., Stuber, G.D., Cleaveland, N.A., Cheer, J.F., Wightman, R.M. & Carelli, R.M. (2009) Neural encoding of cocaine-seeking behavior is coincident with phasic dopamine release in the accumbens core and shell. Eur. J. Neurosci., 30, 1117-1127.
48. Paxinos, G. & Watson, C. (2005) The Rat Brain in Stereotaxic Coordinates. Elsevier, New York.
49. Pelloux, Y., Everitt, B.J. & Dickinson, A. (2007) Compulsive drug seeking by rats under punishment: effects of drug taking history. Psychopharmacology, 194, 127-137.
50. Pelloux, Y., Murray, J.E. & Everitt, B.J. (2013) Differential roles of the prefrontal cortical subregions and basolateral amygdala in compulsive cocaine seeking and relapse after voluntary abstinence in rats. Eur. J. Neurosci., 38, 3018-3026.
51. Pennartz, C.M., Groenewegen, H.J. & Lopes da Silva, F.H. (1994) The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog. Neurobiol., 42, 719-761.
52. Peoples, L.L., Uzwiak, A.J., Gee, F. & West, M.O. (1997) Operant behavior during sessions of intravenous cocaine infusion is necessary and sufficient for phasic firing of single nucleus accumbens neurons. Brain Res., 757, 280-284.
53. Peters, J., LaLumiere, R.T. & Kalivas, P.W. (2008) Infralimbic prefrontal cortex is responsible for inhibiting cocaine seeking in extinguished rats. J. Neurosci., 28, 6046-6053.
54. Pettit, H.O. & Justice, J.B. Jr. (1989) Dopamine in the nucleus accumbens during cocaine self-administration as studied by in vivo microdialysis. Pharmacol. Biochem. Be., 34, 899-904.
55. Pickens, C.L., Airavaara, M., Theberge, F., Fanous, S., Hope, B.T. & Shaham, Y. (2011) Neurobiology of the incubation of drug craving. Trends Neurosci., 34, 411-420.
56. Risinger, R.C., Salmeron, B.J., Ross, T.J., Amen, S.L., Sanfilipo, M., Hoffmann, R.G., Bloom, A.S., Garavan, H. & Stein, E.A. (2005) Neural correlates of high and craving during cocaine self-administration using BOLD fMRI. NeuroImage, 26, 1097-1108.
57. Robinson, T.E., Gorny, G., Mitton, E. & Kolb, B. (2001) Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex. Synapse, 39, 257-266.
58. Schwendt, M., Hearing, M.C., See, R.E. & McGinty, J.F. (2007) Chronic cocaine reduces RGS4 mRNA in rat prefrontal cortex and dorsal striatum. NeuroReport, 18, 1261-1265.
59. Sesack, S.R. & Pickel, V.M. (1992) Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J. Comp. Neurol., 320, 145-160.
60. Stefanik, M.T., Kupchik, Y.M., Brown, R.M. & Kalivas, P.W. (2013) Optogenetic evidence that pallidal projections, not nigral projections, from the nucleus accumbens core are necessary for reinstating cocaine seeking. J. Neurosci., 33, 13654-13662.
61. Tanabe, J., Tregellas, J.R., Dalwani, M., Thompson, L., Owens, E., Crowley, T. & Banich, M. (2009) Medial orbitofrontal cortex gray matter is reduced in abstinent substance-dependent individuals. Biol. Psychiat., 65, 160-164.
62. Thomas, M.J., Kalivas, P.W. & Shaham, Y. (2008) Neuroplasticity in the mesolimbic dopamine system and cocaine addiction. Brit. J. Pharmacol., 154, 327-342.
63. Trantham, H., Szumlinski, K.K., McFarland, K., Kalivas, P.W. & Lavin, A. (2002) Repeated cocaine administration alters the electrophysiological properties of prefrontal cortical neurons. Neuroscience, 113, 749-753.
64. Volkow, N.D., Wang, G.J., Fowler, J.S., Tomasi, D., Telang, F. & Baler, R. (2010) Addiction: decreased reward sensitivity and increased expectation sensitivity conspire to overwhelm the brain's control circuit. BioEssays, 32, 748-755.
65. Wee, S., Specio, S.E. & Koob, G.F. (2007) Effects of dose and session duration on cocaine self-administration in rats. J. Pharmacol. Exp. Ther., 320, 1134-1143.
66. Wheeler, R.A., Twining, R.C., Jones, J.L., Slater, J.M., Grigson, P.S. & Carelli, R.M. (2008) Behavioral and electrophysiological indices of negative affect predict cocaine self-administration. Neuron, 57, 774-785.
67. Wolf, M.E. & Ferrario, C.R. (2010) AMPA receptor plasticity in the nucleus accumbens after repeated exposure to cocaine. Neurosci. Biobehav. R., 35, 185-211.
68. Zavala, A.R., Osredkar, T., Joyce, J.N. & Neisewander, J.L. (2008) Upregulation of Arc mRNA expression in the prefrontal cortex following cue-induced reinstatement of extinguished cocaine-seeking Behavior. Synapse, 62, 421-431.