Mesocorticolimbic circuits are impaired in chronic cocaine users as demonstrated by resting-state functional connectivity

NeuroImage

Volumn 53, Issue 2, 2010, Pages 593-601

  Gu, Hong ^a   Salmeron, Betty Jo ^a   Ross, Thomas J ^a   Geng, Xiujuan ^a   Zhan, Wang ^a   Stein, Elliot A ^a   Yang, Yihong ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COCAINE;

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BEHAVIOR DISORDER; CLINICAL ARTICLE; COCAINE DEPENDENCE; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; IMAGE ANALYSIS; LIMBIC SYSTEM; MALE; MESOCORTICOLIMBIC SYSTEM; NERVE CELL NETWORK; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; THALAMUS; VENTRAL TEGMENTUM;

ADULT; BRAIN MAPPING; CEREBRAL CORTEX; CHRONIC DISEASE; COCAINE-RELATED DISORDERS; CUES; DATA INTERPRETATION, STATISTICAL; FEMALE; HUMANS; LIMBIC SYSTEM; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURAL PATHWAYS; REST; SOCIOECONOMIC FACTORS; SUBSTANCE-RELATED DISORDERS;

EID: 77956061301     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.06.066     Document Type: Article

References (68)

1. American Psychiatric Association Diagnostic and statistical manual of mental disorders 1994, American Psychiatric Association, Washington, DC. Fourth Edition.
2. 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.
3. Behzadi Y., Restom K., Liau J., Liu T.T. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 2007, 37:90-101.
4. 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.
5. Buckner R.L., Andrews-Hanna J.R., Schacter D.L. The brain's default network: anatomy, function, and relevance to disease. Ann.N.Y.Acad.Sci. 2008, 1124:1-38.
6. Cao X., Cao Q., Long X., Sun L., Sui M., Zhu C., Zuo X., Zang Y., Wang Y. Abnormal resting-state functional connectivity patterns of the putamen in medication-naive children with attention deficit hyperactivity disorder. Brain Res. 2009, 1303:195-206.
7. Chachich M., Powell D.A. Both medial prefrontal and amygdala central nucleus lesions abolish heart rate classical conditioning, but only prefrontal lesions impair reversal of eyeblink differential conditioning. Neurosci. Lett. 1998, 257:151-154.
8. Chen B.T., Bowers M.S., Martin M., Hopf F.W., Guillory A.M., Carelli R.M., Chou J.K., Bonci A. Cocaine but not natural reward self-administration nor passive cocaine infusion produces persistent LTP in the VTA. Neuron 2008, 59:288-297.
9. Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996, 29:162-173.
10. Curran H.V., Bolton J., Wanigaratne S., Smyth C. Additional methadone increases craving for heroin: a double-blind, placebo-controlled study of chronic opiate users receiving methadone substitution treatment. Addiction 1999, 94:665-674.
11. Di Chiara G. Drug addiction as dopamine-dependent associative learning disorder. Eur. J. Pharmacol. 1999, 375:13-30.
12. Ersche K.D., Roiser J.P., Robbins T.W., Sahakian B.J. Chronic cocaine but not chronic amphetamine use is associated with perseverative responding in humans. Psychopharmacology (Berl) 2008, 197:421-431.
13. 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.
14. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van E., Raichle M.E. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:9673-9678.
15. 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. Decreased gray matter concentration in the insular, orbitofrontal, cingulate, and temporal cortices of cocaine patients. Biol. Psychiatry 2002, 51:134-142.
16. Friston K.J., Holmes A.P., Worsley K.J., Poline J.-P., Frith R.S., Frackowiak S.J. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 1995, 2:189-210.
17. Geng X., Christensen G.E., Gu H., Ross T.J., Yang Y. Implicit reference-based group-wise image registration and its application to structural and functional MRI. Neuroimage 2009, 47:1341-1351.
18. 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.
19. Gray A.C., Coupar I.M., White P.J. Comparison of opioid receptor distributions in the rat central nervous system. Life Sci. 2006, 79:674-685.
20. Greicius M.D., Krasnow B., Reiss A.L., Menon V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:253-258.
21. Greicius M.D., Flores B.H., Menon V., Glover G.H., Solvason H.B., Kenna H., Reiss A.L., Schatzberg A.F. Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol. Psychiatry 2007, 62:429-437.
22. Grigson P.S., Twining R.C. Cocaine-induced suppression of saccharin intake: a model of drug-induced devaluation of natural rewards. Behav. Neurosci. 2002, 116:321-333.
23. Haber S., McFarland N.R. The place of the thalamus in frontal cortical-basal ganglia circuits. Neuroscientist 2001, 7:315-324.
24. Hampson M., Driesen N.R., Skudlarski P., Gore J.C., Constable R.T. Brain connectivity related to working memory performance. J. Neurosci. 2006, 26:13338-13343.
25. Hampson M., Tokoglu F., Sun Z., Schafer R.J., Skudlarski P., Gore J.C., Constable R.T. Connectivity-behavior analysis reveals that functional connectivity between left BA39 and Broca's area varies with reading ability. Neuroimage 2006, 31:513-519.
26. 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.
27. 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.
28. 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.
29. Kalivas P.W., Volkow N.D. The neural basis of addiction: a pathology of motivation and choice. Am. J. Psychiatry 2005, 162:1403-1413.
30. Kaufman J.N., Ross T.J., Stein E.A., Garavan H. Cingulate hypoactivity in cocaine users during a GO-NOGO task as revealed by event-related functional magnetic resonance imaging. J. Neurosci. 2003, 23:7839-7843.
31. Kelly A.M., Uddin L.Q., Biswal B.B., Castellanos F.X., Milham M.P. Competition between functional brain networks mediates behavioral variability. Neuroimage 2008, 39:527-537.
32. Koob G.F., Le Moal M. Drug abuse: hedonic homeostatic dysregulation. Science 1997, 278:52-58.
33. Koob G.F., Le Moal M. Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 2001, 24:97-129.
34. Kosten T.R., Scanley B.E., Tucker K.A., Oliveto A., Prince C., Sinha R., Potenza M.N., Skudlarski P., Wexler B.E. Cue-induced brain activity changes and relapse in cocaine-dependent patients. Neuropsychopharmacology 2006, 31:644-650.
35. Kreek M.J., Bart G., Lilly C., LaForge K.S., Nielsen D.A. Pharmacogenetics and human molecular genetics of opiate and cocaine addictions and their treatments. Pharmacol. Rev. 2005, 57:1-26.
36. Krienen F.M., Buckner R.L. Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb. Cortex 2009, 19:2485-2497.
37. Lancaster J.L., Woldorff M.G., Parsons L.M., Liotti M., Freitas C.S., Rainey L., Kochunov P.V., Nickerson D., Mikiten S.A., Fox P.T. Automated Talairach atlas labels for functional brain mapping. Hum. Brain Mapp. 2000, 10:120-131.
38. Langleben D.D., Ruparel K., Elman I., Busch-Winokur S., Pratiwadi R., Loughead J., O'Brien C.P., Childress A.R. Acute effect of methadone maintenance dose on brain FMRI response to heroin-related cues. Am. J. Psychiatry 2008, 165:390-394.
39. Li S.J., Wang Y., Pankiewicz J., Stein E.A. Neurochemical adaptation to cocaine abuse: reduction of N-acetyl aspartate in thalamus of human cocaine abusers. Biol. Psychiatry 1999, 45:1481-1487.
40. Li S.J., Li Z., Wu G., Zhang M.J., Franczak M., Antuono P.G. Alzheimer Disease: evaluation of a functional MR imaging index as a marker. Radiology 2002, 225:253-259.
41. Liang M., Zhou Y., Jiang T., Liu Z., Tian L., Liu H., Hao Y. Widespread functional disconnectivity in schizophrenia with resting-state functional magnetic resonance imaging. NeuroReport 2006, 17:209-213.
42. Lim K.O., Wozniak J.R., Mueller B.A., Franc D.T., Specker S.M., Rodriguez C.P., Silverman A.B., Rotrosen J.P. Brain macrostructural and microstructural abnormalities in cocaine dependence. Drug Alcohol Depend. 2008, 92:164-172.
43. Lowe M.J., Mock B.J., Sorenson J.A. Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 1998, 7:119-132.
44. Lu H., Zuo Y., Gu H., Waltz J.A., Zhan W., Scholl C.A., Rea W., Yang Y., Stein E.A. Synchronized delta oscillations correlate with the resting-state functional MRI signal. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:18265-18269.
45. Ma N., Liu Y., Li N., Wang C.X., Zhang H., Jiang X.F., Xu H.S., Fu X.M., Hu X., Zhang D.R. Addiction related alteration in resting-state brain connectivity. Neuroimage 2010, 49:738-744.
46. Matochik J.A., London E.D., Eldreth D.A., Cadet J.L., Bolla K.I. Frontal cortical tissue composition in abstinent cocaine abusers: a magnetic resonance imaging study. Neuroimage 2003, 19:1095-1102.
47. Oades R.D., Halliday G.M. Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res. 1987, 434:117-165.
48. Parent A. Carpenter's human neuroanatomy, 9th ed 1996, Williams & Wilkins, Baltimore.
49. Peoples L.L., Cavanaugh D. Differential changes in signal and background firing of accumbal neurons during cocaine self-administration. J. Neurophysiol. 2003, 90:993-1010.
50. Poling J., Kosten T.R., Sofuoglu M. Treatment outcome predictors for cocaine dependence. Am. J. Drug Alcohol Abuse 2007, 33:191-206.
51. Porrino L.J., Smith H.R., Nader M.A., Beveridge T.J. The effects of cocaine: a shifting target over the course of addiction. Prog. Neuropsychopharmacol. Biol. Psychiatry 2007, 31:1593-1600.
52. Robinson T.E., Berridge K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Brain Res. Rev. 1993, 18:247-291.
53. Saxon A.J., Oreskovich M.R., Brkanac Z. Genetic determinants of addiction to opioids and cocaine. Harv. Rev. Psychiatry 2005, 13:218-232.
54. Schultz W. Getting formal with dopamine and reward. Neuron 2002, 36:241-263.
55. Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., Reiss A.L., Greicius M.D. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007, 27:2349-2356.
56. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., Filippini N., Watkins K.E., Toro R., Laird A.R., Beckmann C.F. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:13040-13045.
57. Stein M.B., Simmons A.N., Feinstein J.S., Paulus M.P. Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. Am. J. Psychiatry 2007, 164:318-327.
58. Talairach J., Tournoux P., Missir O. Referentially oriented cerebral MRI anatomy an atlas of sterotaxic anatomical correlations for gray and white matter 1993, G. Thieme Verlag, Stuttgart.
59. Tomasi D., Goldstein R.Z., Telang F., Maloney T., ia-Klein N., Caparelli E.C., Volkow N.D. Thalamo-cortical dysfunction in cocaine abusers: implications in attention and perception. Psychiatry Res. 2007, 155:189-201.
60. Verdejo-Garcia A.J., Perales J.C., Perez-Garcia M. Cognitive impulsivity in cocaine and heroin polysubstance abusers. Addict. Behav. 2007, 32:950-966.
61. Vincent J.L., Patel G.H., Fox M.D., Snyder A.Z., Baker J.T., Van E., Zempel J.M., Snyder L.H., Corbetta M., Raichle M.E. Intrinsic functional architecture in the anaesthetized monkey brain. Nature 2007, 447:83-86.
62. Volkow N.D., Li T.K. The neuroscience of addiction. Nat. Neurosci. 2005, 8:1429-1430.
63. Volkow N.D., Fowler J.S., Wang G.J., Hitzemann R., Logan J., Schlyer D.J., Dewey S.L., Wolf A.P. Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse 1993, 14:169-177.
64. Waites A.B., Briellmann R.S., Saling M.M., Abbott D.F., Jackson G.D. Functional connectivity networks are disrupted in left temporal lobe epilepsy. Ann. Neurol. 2006, 59:335-343.
65. Washton A.M. Structured outpatient treatment of cocaine abuse. Adv. Alcohol Subst. Abuse 1986, 6:143-157.
66. Weissenborn R., Whitelaw R.B., Robbins T.W., Everitt B.J. Excitotoxic lesions of the mediodorsal thalamic nucleus attenuate intravenous cocaine self-administration. Psychopharmacology (Berl) 1998, 140:225-232.
67. Xiong J., Parsons L.M., Gao J.H., Fox P.T. Interregional connectivity to primary motor cortex revealed using MRI resting state images. Hum. Brain Mapp. 1999, 8:151-156.
68. Yang S., Salmeron B.J., Ross T.J., Xi Z.X., Stein E.A., Yang Y. Lower glutamate levels in rostral anterior cingulate of chronic cocaine users - A (1)H-MRS study using TE-averaged PRESS at 3T with an optimized quantification strategy. Psychiatry Res. 2009, 174:171-176.