FMRI response in the medial prefrontal cortex predicts cocaine but not sucrose self-administration history

NeuroImage

Volumn 62, Issue 3, 2012, Pages 1857-1866

  Lu, Hanbing ^a   Chefer, Svetlana ^a   Kurup, Pradeep K ^a   Guillem, Karine ^b,d,e   Vaupel, D Bruce ^a   Ross, Thomas J ^a   Moore, Anna ^c   Yang, Yihong ^a   Peoples, Laura L ^b,f   Stein, Elliot A ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITÉ DE BORDEAUX   (France)

^e INSTITUT DES MALADIES NEURODÉGÉNÉRATIVES   (France)

^f DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Abstinence; Neuroadaptation; Pharmacological MRI; Self administration

Indexed keywords

COCAINE; SUCROSE;

ABSTINENCE; ADAPTATION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTERIOR CINGULATE; ARTICLE; BRAIN BLOOD VOLUME; BRAIN FUNCTION; COCAINE DEPENDENCE; CONTROLLED STUDY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; LIMBIC CORTEX; MEDIAL PREFRONTAL CORTEX; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; REINFORCEMENT; REWARD;

ANIMALS; BRAIN MAPPING; COCAINE; COCAINE-RELATED DISORDERS; DISEASE MODELS, ANIMAL; DOPAMINE UPTAKE INHIBITORS; MAGNETIC RESONANCE IMAGING; NEURONAL PLASTICITY; PREFRONTAL CORTEX; RATS; RATS, LONG-EVANS; SELF ADMINISTRATION; SUCROSE;

EID: 84863508906     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.05.076     Document Type: Article

References (70)

1. Ahmed S.H., Cador M. Dissociation of psychomotor sensitization from compulsive cocaine consumption. Neuropsychopharmacology 2006, 31:563-571.
2. Avena N., Rada P., Hoebel B. Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci. Biobehav. Rev. 2008, 32:20-39.
3. Baker D.A., McFarland K., Lake R.W., Shen H., Tang X.C., Toda S., Kalivas P.W. Neuroadaptations in cystine-glutamate exchange underlie cocaine relapse. Nat. Neurosci. 2003, 6:743-749.
4. Barr A.M., Markou A. Psychostimulant withdrawal as an inducing condition in animal models of depression. Neurosci. Biobehav. Rev. 2005, 29:675-706.
5. Beveridge T.J., Smith H.R., Daunais J.B., Nader M.A., Porrino L.J. Chronic cocaine self-administration is associated with altered functional activity in the temporal lobes of non human primates. Eur. J. Neurosci. 2006, 23:3109-3118.
6. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34:537-541.
7. Bossert J.M., Ghitza U.E., Lu L., Epstein D.H., Shaham Y. Neurobiology of relapse to heroin and cocaine seeking: an update and clinical implications. Eur. J. Pharmacol. 2005, 526:36-50.
8. Bowers M.S., McFarland K., Lake R.W., Peterson Y.K., Lapish C.C., Gregory M.L., Lanier S.M., Kalivas P.W. Activator of G protein signaling 3: a gatekeeper of cocaine sensitization and drug seeking. Neuron 2004, 42:269-281.
9. Capriles N., Rodaros D., Sorge R.E., Stewart J. A role for the prefrontal cortex in stress- and cocaine-induced reinstatement of cocaine seeking in rats. Psychopharmacology (Berl.) 2003, 168:66-74.
10. Chen Y.C., Choi J.K., Andersen S.L., Rosen B.R., Jenkins B.G. Mapping dopamine D2/D3 receptor function using pharmacological magnetic resonance imaging. Psychopharmacology (Berl.) 2005, 180:705-715.
11. Chen B., Bowers M., Martin M., Hopf F., Guillory A., Carelli R., Chou J., Bonci A. Cocaine but not natural reward self-administration nor passive cocaine infusion produces persistent LTP in the VTA. Neuron 2008, 59:288-297.
12. Choi J.K., Chen Y.I., Hamel E., Jenkins B.G. Brain hemodynamic changes mediated by dopamine receptors: role of the cerebral microvasculature in dopamine-mediated neurovascular coupling. Neuroimage 2006, 30:700-712.
13. Churchill L., Zahm D.S., Duffy P., Kalivas P.W. The mediodorsal nucleus of the thalamus in rats .2. Behavioral and neurochemical effects of GABA agonists. Neuroscience 1996, 70:103-112.
14. Clow D.W., Hammer R.P. Cocaine abstinence following chronic treatment alters cerebral metabolism in dopaminergic reward regions. Bromocriptine enhances recovery. Neuropsychopharmacology 1991, 4:71-75.
15. Cox R. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996, 29:162-173.
16. Epstein D.H., Preston K.L., Stewart J., Shaham Y. Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure. Psychopharmacology (Berl.) 2006, 189:1-16.
17. Febo M., Segarra A.C., Tenney J.R., Brevard M.E., Duong T.Q., Ferris C.F. Imaging cocaine-induced changes in the mesocorticolimbic dopaminergic system of conscious rats. J. Neurosci. Methods 2004, 139:167-176.
18. Febo M., Segarra A.C., Nair G., Schmidt K., Duong T.Q., Ferris C.F. The neural consequences of repeated cocaine exposure revealed by functional MRI in awake rats. Neuropsychopharmacology 2005, 30:936-943.
19. Gaffan D., Murray E.A. Amygdalar interaction with the mediodorsal nucleus of the thalamus and the ventromedial prefrontal cortex in stimulus reward associative learning in the monkey. J. Neurosci. 1990, 10:3479-3493.
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. Goldstein R.Z., Volkow N.D. Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am. J. Psychiatry 2002, 159:1642-1652.
22. Gu H., Salmeron B.J., Ross T.J., Geng X., Zhan W., Stein E.A., Yang Y. Mesocorticolimbic circuits are impaired in chronic cocaine users as demonstrated by resting-state functional connectivity. Neuroimage 2010, 53:593-601.
23. Hammer R.P., Pires W.S., Markou A., Koob G.F. Withdrawal following cocaine self-administration decreases regional cerebral metabolic rate in critical brain reward regions. Synapse 1993, 14:73-80.
24. 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.
25. Hong L.E., Gu H., Yang Y., Ross T.J., Salmeron B.J., Buchholz B., Thaker G.K., Stein E.A. Association of nicotine addiction and nicotine's actions with separate cingulate cortex functional circuits. Arch. Gen. Psychiatry 2009, 66:431-441.
26. Jentsch J.D., Taylor J.R. Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Psychopharmacology (Berl.) 1999, 146:373-390.
27. Jones J.L., Wheeler R.A., Carelli R.M. Behavioral responding and nucleus accumbens cell firing are unaltered following periods of abstinence from sucrose. Synapse 2008, 62:219-228.
28. Kalivas P.W. Glutamate systems in cocaine addiction. Curr. Opin. Pharmacol. 2004, 4:23-29.
29. Kalivas P., Volkow N., Seamans J. Unmanageable motivation in addiction: a pathology in prefrontal-accumbens glutamate transmission. Neuron 2005, 647-650.
30. Kelley A.E., Berridge K.C. The neuroscience of natural rewards: relevance to addictive drugs. J. Neurosci. 2002, 22:3306-3311.
31. Kiyatkin E.A., Lenoir M. Intravenous saline injection as an interoceptive signal in rats. Psychopharmacology (Berl.) 2011, 217:387-396.
32. Leventhal A.M., Brightman M., Ameringer K.J., Greenberg J., Mickens L., Ray L.A., Sun P., Sussman S. Anhedonia associated with stimulant use and dependence in a population-based sample of American adults. Exp. Clin. Psychopharmacol. 2010, 18:562-569.
33. Levy D., Shabat-Simon M., Shalev U., Barnea-Ygael N., Cooper A., Zangen A. Repeated electrical stimulation of reward-related brain regions affects cocaine but not "Natural" reinforcement. J. Neurosci. 2007, 27:14179-14189.
34. Lu L., Grimm J.W., Dempsey J., 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 6months. Psychopharmacology (Berl.) 2004, 176:101-108.
35. Lu H., Scholl C.A., Zuo Y., Stein E.A., Yang Y. Quantifying the blood oxygenation level dependent effect in cerebral blood volume-weighted functional MRI at 9.4T. Magn. Reson. Med. 2007, 58:616-621.
36. Lu H., Xi Z.X., Gitajn L., Rea W., Yang Y., Stein E.A. Cocaine-induced brain activation detected by dynamic manganese-enhanced magnetic resonance imaging (MEMRI). Proc. Natl. Acad. Sci. U. S. A. 2007, 104:2489-2494.
37. Lu H., Yang S., Zuo Y., Demny S., Stein E.A., Yang Y. Real-time animal functional magnetic resonance imaging and its application to neuropharmacological studies. Magn. Reson. Imaging 2008, 26:1266-1272.
38. Lu H., Scholl C.A., Zuo Y., Demny S., Rea W., Stein E.A., Yang Y. Registering and analyzing rat fMRI data in the stereotaxic framework by exploiting intrinsic anatomical features. Magn. Reson. Imaging 2010, 28:146-152.
39. Luo F., Wu G., Li Z., Li S.J. Characterization of effects of mean arterial blood pressure induced by cocaine and cocaine methiodide on BOLD signals in rat brain. Magn. Reson. Med. 2003, 49:264-270.
40. Mandeville J.B., Marota J.J., Kosofsky B.E., Keltner J.R., Weissleder R., Rosen B.R., Weisskoff R.M. Dynamic functional imaging of relative cerebral blood volume during rat forepaw stimulation. Magn. Reson. Med. 1998, 39:615-624.
41. Markou A., Koob G.F. Postcocaine anhedonia-an animal-model of cocaine withdrawal. Neuropsychopharmacology 1991, 4:17-26.
42. Marota J.J., Mandeville J.B., Weisskoff R.M., Moskowitz M.A., Rosen B.R., Kosofsky B.E. Cocaine activation discriminates dopaminergic projections by temporal response: an fMRI study in rat. Neuroimage 2000, 11:13-23.
43. Martinez D., Narendran R., Foltin R.W., Slifstein M., Hwang D.R., Broft A., Huang Y., Cooper T.B., Fischman M.W., Kleber H.D., Laruelle M. Amphetamine-induced dopamine release: markedly blunted in cocaine dependence and predictive of the choice to self-administer cocaine. Am. J. Psychiatry 2007, 164:622-629.
44. McFarland K., Lapish C.C., Kalivas P.W. Prefrontal glutamate release into the core of the nucleus accumbens mediates cocaine-induced reinstatement of drug-seeking behavior. J. Neurosci. 2003, 23:3531-3537.
45. Mogenson G.J., Jones D.L., Yim C.Y. From motivation to action: functional interface between the limbic system and the motor system. Prog. Neurobiol. 1980, 14:69-97.
46. Nestler E.J. Molecular basis of long-term plasticity underlying addiction. Nat. Rev. Neurosci. 2001, 2:119-128.
47. O'Brien C.P. Progress in the science of addiction. Am. J. Psychiatry 1997, 154:1195-1197.
48. Park W.K., Bari A.A., Jey A.R., Anderson S.M., Spealman R.D., Rowlett J.K., Pierce R.C. Cocaine administered into the medial prefrontal cortex reinstates cocaine-seeking behavior by increasing AMPA receptor-mediated glutamate transmission in the nucleus accumbens. J. Neurosci. 2002, 22:2916-2925.
49. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2005, Elsevier Inc. 6th ed.
50. Peoples L.L., Kravitz A.V., Guillem K. The role of accumbal hypoactivity in cocaine addiction. ScientificWorldJournal 2007, 7:22-45.
51. Peoples L.L., Kravitz A.V., Lynch K.G., Cavanaugh D.J. Accumbal neurons that are activated during cocaine self-administration are spared from inhibitory effects of repeated cocaine self-administration. Neuropsychopharmacology 2007, 32:1141-1158.
52. Pierce R.C., Bell K., Duffy P., Kalivas P.W. Repeated cocaine augments excitatory amino acid transmission in the nucleus accumbens only in rats having developed behavioral sensitization. J. Neurosci. 1996, 16:1550-1560.
53. Porrino L., Lyons D., Smith H., Daunais J., Nader M. Cocaine self-administration produces a progressive involvement of limbic, association, and sensorimotor striatal domains. J. Neurosci. 2004, 24:3554-3562.
54. Price J.L. Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Ann. N. Y. Acad. Sci. 2007, 1121:54-71.
55. Ritz M., Cone E., Kuhar M. Cocaine inhibition of ligand binding at dopamine, norepinephrine and serotonin transporters: a structure-activity study. Life Sci. 1990, 46:635-645.
56. Sinha R., Shaham Y., Heilig M. Translational and reverse translational research on the role of stress in drug craving and relapse. Psychopharmacology (Berl.) 2011, 218:69-82.
57. Stewart J., Dewit H., Eikelboom R. Role of unconditioned and conditioned drug effects in the self-administration of opiates and stimulants. Psychol. Rev. 1984, 91:251-268.
58. Sun W., Rebec G.V. Repeated cocaine self-administration alters processing of cocaine-related information in rat prefrontal cortex. J. Neurosci. 2006, 26:8004-8008.
59. Trantham H., Szumlinski K.K., McFarland K., Kalivas P.W., Lavin A. Repeated cocaine administration alters the electrophysiological properties of prefrontal cortical neurons. Neuroscience 2002, 113:749-753.
60. Ungless M., Whistler J., Malenka R., Bonci A. Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 2001, 411:583-587.
61. Vanderschuren L.J., Everitt B.J. Drug seeking becomes compulsive after prolonged cocaine self-administration. Science 2004, 305:1017-1019.
62. Vanderschuren L.J., Everitt B.J. Behavioral and neural mechanisms of compulsive drug seeking. Eur. J. Pharmacol. 2005, 526:77-88.
63. Volkow N., Wise R. How can drug addiction help us understand obesity?. Nat. Neurosci. 2005, 8:555-560.
64. Volkow N., Mullani N., Gould K., Adler S., Krajewski K. Cerebral blood-flow in chronic cocaine users-a study with positron emission tomography. Br. J. Psychiatry 1988, 641-648.
65. Volkow N., Hitzemann R., Wang G., Fowler J., Wolf A., Dewey S., Handlesman L. Long-term frontal brain metabolic changes in cocaine abusers. Synapse 1992, 184-190.
66. Volkow N., Wang G., Fowler J., Logan J., Gatley S., Hitzemann R., Chen A., Dewey S., Pappas N. Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects. Nature 1997, 830-833.
67. Weissenborn R., Whitelaw R.B., Robbins T.W., Everitt B.J. Excitotoxic lesions of the mediodorsal thalamic nucleus attenuate intravenous cocaine self administration. Psychopharmacology 1998, 140:225-232.
68. Wise R.A., Wang B., You Z.B. Cocaine serves as a peripheral interoceptive conditioned stimulus for central glutamate and dopamine release. PLoS One 2008, 3.
69. You Z.B., Wang B., Zitzman D., Azari S., Wise R.A. A role for conditioned ventral tegmental glutamate release in cocaine seeking. J. Neurosci. 2007, 27:10546-10555.
70. Yuan Z., Luo Z., Volkow N.D., Pan Y., Du C. Imaging separation of neuronal from vascular effects of cocaine on rat cortical brain in vivo. Neuroimage 2011, 54:1130-1139.