The cerebellum and addiction: Insights gained from neuroimaging research

Addiction Biology

Volumn 19, Issue 3, 2014, Pages 317-331

  Moulton, Eric A ^a   Elman, Igor ^b,c   Becerra, Lino R ^a   Goldstein, Rita Z ^d   Borsook, David ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b PROVIDENCE VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c CAMBRIDGE HEALTH ALLIANCE   (United States)

^d BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

Alcohol; cocaine; craving; marijuana; MRI; opioids; PET.

Indexed keywords

CANNABIS; METHYLPHENIDATE; NICOTINE;

ADDICTION; ALCOHOLISM; ARTICLE; BRAIN SIZE; CANNABIS ADDICTION; CEREBELLUM; COCAINE DEPENDENCE; DIFFUSION TENSOR IMAGING; DRUG EXPOSURE; EXECUTIVE FUNCTION; EYE MOVEMENT; FRACTIONAL ANISOTROPY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; MOTIVATION; MOTOR COORDINATION; OPIATE ADDICTION; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REWARD; TOBACCO DEPENDENCE; VOXEL BASED MORPHOMETRY; WITHDRAWAL SYNDROME; BIOLOGICAL MODEL; CEREBELLUM DISEASE; FEMALE; MALE; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES;

BEHAVIOR, ADDICTIVE; CEREBELLAR DISEASES; CEREBELLUM; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MODELS, BIOLOGICAL; NEUROIMAGING; POSITRON-EMISSION TOMOGRAPHY; SUBSTANCE-RELATED DISORDERS;

EID: 84899465796     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/adb.12101     Document Type: Article

References (109)

1. Anderson CM, Maas LC, Frederick BD, Bendor JT, Spencer TJ, Livni E, Lukas ES, Fischman AJ, Madras BK, Renshaw PF, Kaufman MJ, (2006) Cerebellar vermis involvement in cocaine-related behaviors. Neuropsychopharmacology 31: 1318-1326.
2. Ashton JC, Appleton I, Darlington CL, Smith PF, (2004) Immunohistochemical localization of cannabinoid CB1 receptor in inhibitory interneurons in the cerebellum. Cerebellum 3: 222-226.
3. Barrós-Loscertales A, Garavan H, Bustamante JC, Ventura-Campos N, Llopis JJ, Belloch V, Parcet MA, Avila C, (2011) Reduced striatal volume in cocaine-dependent patients. Neuroimage 56: 1021-1026.
4. Bauer DJ, Kerr AL, Swain RA, (2011) Cerebellar dentate nuclei lesions reduce motivation in appetitive operant conditioning and open field exploration. Neurobiol Learn Mem 95: 166-175.
5. Benegal V, Antony G, Venkatasubramanian G, Jayakumar PN, (2007) Gray matter volume abnormalities and externalizing symptoms in subjects at high risk for alcohol dependence. Addict Biol 12: 122-132.
6. Berridge KC, Robinson TE, (2003) Parsing reward. Trends Neurosci 26: 507-513.
7. Block RI, O'Leary DS, Ehrhardt JC, Augustinack JC, Ghoneim MM, Arndt S, Hall JA, (2000a) Effects of frequent marijuana use on brain tissue volume and composition. Neuroreport 11: 491-496.
8. Block RI, O'Leary DS, Hichwa RD, Augustinack JC, Ponto LL, Ghoneim MM, Arndt S, Ehrhardt JC, Hurtig RR, Watkins GL, Hall JA, Nathan PE, Andreasen NC, (2000b) Cerebellar hypoactivity in frequent marijuana users. Neuroreport 11: 749-753.
9. Bonson KR, Grant SJ, Contoreggi CS, Links JM, Metcalfe J, Weyl HL, Kurian V, Ernst M, London ED, (2002) Neural systems and cue-induced cocaine craving. Neuropsychopharmacology 26: 376-386.
10. Bora E, Yücel M, Fornito A, Pantelis C, Harrison BJ, Cocchi L, Pell G, Lubman DI, (2012) White matter microstructure in opiate addiction. Addict Biol 17: 141-148.
11. Bostan AC, Strick PL, (2010) The cerebellum and basal ganglia are interconnected. Neuropsychol Rev 20: 261-270.
12. Brody AL, Mandelkern MA, Jarvik ME, Lee GS, Smith EC, Huang JC, Bota RG, Batzokis G, London ED, (2004) Differences between smokers and nonsmokers in regional gray matter volumes and densities. Biol Psychiatry 55: 77-84.
13. Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BTT, (2011) The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol 106: 2322-2345.
14. Chanraud S, Martelli C, Delain F, Kostogianni N, Douaud G, Aubin H-J, Reynaud M, Martinot J-L, (2007) Brain morphometry and cognitive performance in detoxified alcohol-dependents with preserved psychosocial functioning. Neuropsychopharmacology 32: 429-438.
15. Chanraud S, Pitel A-L, Rohlfing T, Pfefferbaum A, Sullivan EV, (2010) Dual tasking and working memory in alcoholism: relation to frontocerebellar circuitry. Neuropsychopharmacology 35: 1868-1878.
16. Courchesne E, Allen G, (1997) Prediction and preparation, fundamental functions of the cerebellum. Learn Mem 4: 1-35.
17. Cousijn J, Wiers RW, Ridderinkhof KR, van den Brink W, Veltman DJ, Goudriaan AE, (2012) Grey matter alterations associated with cannabis use: results of a VBM study in heavy cannabis users and healthy controls. Neuroimage 59: 3845-3851.
18. Craig AD, (2009) How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10: 59-70.
19. D'Angelo E, Casali S, (2012) Seeking a unified framework for cerebellar function and dysfunction: from circuit operations to cognition. Front Neural Circuits 6: 116.
20. De Bellis MD, Narasimhan A, Thatcher DL, Keshavan MS, Soloff P, Clark DB, (2005) Prefrontal cortex, thalamus, and cerebellar volumes in adolescents and young adults with adolescent-onset alcohol use disorders and comorbid mental disorders. Alcohol Clin Exp Res 29: 1590-1600.
21. Diedrichsen J, (2006) A spatially unbiased atlas template of the human cerebellum. Neuroimage 33: 127-138.
22. Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N, (2009) A probabilistic MR atlas of the human cerebellum. Neuroimage 46: 39-46.
23. Diedrichsen J, Maderwald S, Küper M, Thürling M, Rabe K, Gizewski ER, Ladd ME, Timmann D, (2011) Imaging the deep cerebellar nuclei: a probabilistic atlas and normalization procedure. Neuroimage 54: 1786-1794.
24. Diedrichsen J, Verstynen T, Schlerf J, Wiestler T, (2010) Advances in functional imaging of the human cerebellum. Curr Opin Neurol 23: 382-387.
25. Domino EF, Minoshima S, Guthrie S, Ohl L, Ni L, Koeppe RA, Zubieta JK, (2000) Nicotine effects on regional cerebral blood flow in awake, resting tobacco smokers. Synapse 38: 313-321.
26. Doyon J, Penhune V, Ungerleider LG, (2003) Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 41: 252-262.
27. Ersche KD, Jones PS, Williams GB, Turton AJ, Robbins TW, Bullmore ET, (2012) Abnormal brain structure implicated in stimulant drug addiction. Science 335: 601-604.
28. Ferrucci M, Busceti CL, Falleni A, Giorgi FS, Ruggieri S, Fornai F, (2006) Effects of methamphetamine on the cerebellar cortex: a preliminary study. Ann N Y Acad Sci 1074: 149-153.
29. Gallinat J, Meisenzahl E, Jacobsen LK, Kalus P, Bierbrauer J, Kienast T, Witthaus H, Leopold K, Seifert F, Schubert F, Staedtgen M, (2006) Smoking and structural brain deficits: a volumetric MR investigation. Eur J Neurosci 24: 1744-1750.
30. Gallucci M, Amicarelli I, Rossi A, Stratta P, Masciocchi C, Zobel BB, Casacchia M, Passariello R, (1989) MR imaging of white matter lesions in uncomplicated chronic alcoholism. J Comput Assist Tomogr 13: 395-398.
31. Geller T, Loftis L, Brink DS, (2004) Cerebellar infarction in adolescent males associated with acute marijuana use. Pediatrics 113: e365-e370.
32. Goldstein RZ, Volkow ND, (2002) Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am J Psychiatry 159: 1642-1652.
33. Goldstein RZ, Volkow ND, (2011) Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 12: 652-669.
34. Grant S, London ED, Newlin DB, Villemagne VL, Liu X, Contoreggi C, Phillips RL, Kimes AS, Margolin A, (1996) Activation of memory circuits during cue-elicited cocaine craving. PNAS 93: 12040-12045.
35. Habas C, Kamdar N, Nguyen D, Prater K, Beckmann CF, Menon V, Greicius MD, (2009) Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci 29: 8586-8594.
36. Haubek A, Lee K, (1979) Computed tomography in alcoholic cerebellar atrophy. Neuroradiology 18: 77-79.
37. Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR, Rice KC, (1990) Cannabinoid receptor localization in brain. PNAS 87: 1932-1936.
38. Hill SY, Wang S, Carter H, Tessner K, Holmes B, McDermott M, Zezza N, Stiffler S, (2011) Cerebellum volume in high-risk offspring from multiplex alcohol dependence families: association with allelic variation in GABRA2 and BDNF. Psychiatry Res 194: 304-313.
39. Hillbom M, Muuronen A, Holm L, Hindmarsh T, (1986) The clinical versus radiological diagnosis of alcoholic cerebellar degeneration. J Neurol Sci 73: 45-53.
40. Hyman SE, Malenka RC, Nestler EJ, (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29: 565-598.
41. Ito M, (2006) Cerebellar circuitry as a neuronal machine. Prog Neurobiol 78: 272-303.
42. Ivry R, (1997) Cerebellar timing systems. Int Rev Neurobiol 41: 555-573.
43. Kelly RM, Strick PL, (2003) Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci 23: 8432-8444.
44. Kilts CD, Schweitzer JB, Quinn CK, Gross RE, Faber TL, Muhammad F, Ely TD, Hoffman JM, Drexler KP, (2001) Neural activity related to drug craving in cocaine addiction. Arch Gen Psychiatry 58: 334-341.
45. Kohlmeyer K, Stober B, Jennen C, (1986) Computed tomography in chronic alcoholism. Acta Radiol Suppl 369: 393-395.
46. Koob GF, (1996) Drug addiction: the yin and yang of hedonic homeostasis. Neuron 16: 893-896.
47. Krienen FM, Buckner RL, (2009) Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb Cortex 19: 2485-2497.
48. Kühn S, Romanowski A, Schilling C, Mobascher A, Warbrick T, Winterer G, Gallinat J, (2012) Brain grey matter deficits in smokers: focus on the cerebellum. Brain Struct Funct 217: 517-522.
49. Lin W-C, Chou K-H, Chen H-L, Huang C-C, Lu C-H, Li S-H, Wang Y-L, Cheng Y-F, Lin C-C, Chen C-C, (2012) Structural deficits in the emotion circuit and cerebellum are associated with depression, anxiety and cognitive dysfunction in methadone maintenance patients: a voxel-based morphometric study. Psychiatry Res 201: 89-97.
50. Lou M, Wang E, Shen Y, Wang J, (2012) Cue-elicited craving in heroin addicts at different abstinent time: an fMRI pilot study. Subst Use Misuse 47: 631-639.
51. Manto M, (2012) Toxic agents causing cerebellar ataxias. Handb Clin Neurol 103: 201-213. edited by P.J. Vinken and G.W. Bruyn.
52. Martin PR, Singleton CK, Hiller-Sturmhöfel S, (2003) The role of thiamine deficiency in alcoholic brain disease. Alcohol Res Health 27: 134-142.
53. Mathew RJ, Wilson WH, Turkington TG, Coleman RE, (1998) Cerebellar activity and disturbed time sense after THC. Brain Res 797: 183-189.
54. Mathew RJ, Wilson WH, Turkington TG, Hawk TC, Coleman RE, DeGrado TR, Provenzale J, (2002) Time course of tetrahydrocannabinol-induced changes in regional cerebral blood flow measured with positron emission tomography. Psychiatry Res 116: 173-185.
55. Matochik JA, Eldreth DA, Cadet J-L, Bolla KI, (2005) Altered brain tissue composition in heavy marijuana users. Drug Alcohol Depend 77: 23-30.
56. Mechtcheriakov S, Brenneis C, Egger K, Koppelstaetter F, Schocke M, Marksteiner J, (2007) A widespread distinct pattern of cerebral atrophy in patients with alcohol addiction revealed by voxel-based morphometry. J Neurol Neurosurg Psychiatry 78: 610-614.
57. Medina KL, Nagel BJ, Tapert SF, (2010) Abnormal cerebellar morphometry in abstinent adolescent marijuana users. Psychiatry Res 182: 152-159.
58. Middleton FA, Strick PL, (1994) Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science 266: 458-461.
59. Middleton FA, Strick PL, (2000) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Brain Res Rev 31: 236-250.
60. Middleton FA, Strick PL, (2001) Cerebellar projections to the prefrontal cortex of the primate. J Neurosci 21: 700-712.
61. Miquel M, Toledo R, García LI, Coria-Avila GA, Manzo J, (2009) Why should we keep the cerebellum in mind when thinking about addiction? Curr Drug Abuse Rev 2: 26-40.
62. Moulton EA, Elman I, Pendse G, Schmahmann J, Becerra L, Borsook D, (2011) Aversion-related circuitry in the cerebellum: responses to noxious heat and unpleasant images. J Neurosci 31: 3795-3804.
63. Mouraux A, Diukova A, Lee MC, Wise RG, Iannetti GD, (2011) A multisensory investigation of the functional significance of the 'pain matrix'. Neuroimage 54: 2237-2249.
64. Mulholland PJ, (2006) Susceptibility of the cerebellum to thiamine deficiency. Cerebellum 5: 55-63.
65. O'Reilly JX, Beckmann CF, Tomassini V, Ramnani N, Johansen-Berg H, (2010) Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cereb cortex 20: 953-965.
66. Phillips SC, Harper CG, Kril J, (1987) A quantitative histological study of the cerebellar vermis in alcoholic patients. Brain 110 (Pt 2): 301-314.
67. Ramnani N, (2012) Frontal lobe and posterior parietal contributions to the cortico-cerebellar system. Cerebellum 11: 366-383.
68. Ramos A, Quintana F, Díez C, Leno C, Berciano J, (1987) CT findings in spinocerebellar degeneration. AJNR Am J Neuroradiol 8: 635-640.
69. Risinger RC, Salmeron BJ, Ross TJ, Amen SL, Sanfilipo M, Hoffmann RG, Bloom AS, Garavan H, Stein EA, (2005) Neural correlates of high and craving during cocaine self-administration using BOLD fMRI. Neuroimage 26: 1097-1108.
70. Sang L, Qin W, Liu Y, Han W, Zhang Y, Jiang T, Yu C, (2012) Resting-state functional connectivity of the vermal and hemispheric subregions of the cerebellum with both the cerebral cortical networks and subcortical structures. Neuroimage 61: 1213-1225.
71. Schadrack J, Willoch F, Platzer S, Bartenstein P, Mahal B, Dworzak D, Wester HJ, Zieglgansberger W, Tölle TR, (1999) Opioid receptors in the human cerebellum: evidence from [11C]diprenorphine PET, mRNA expression and autoradiography. Neuroreport 10: 619-624.
72. Schmahmann JD, (1991) An emerging concept. The cerebellar contribution to higher function. Arch Neurol 48: 1178-1187.
73. Schmahmann JD, (1996) From movement to thought: anatomic substrates of the cerebellar contribution to cognitive processing. Hum Brain Mapp 4: 174-198.
74. Schmahmann JD, Doyon J, Toga AW, Petrides M, Evans AC, (2000) MRI Atlas of the Human Cerebellum, p. 167. San Diego, CA: Academic Press.
75. Schmahmann JD, (2004) Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci 16: 367-378.
76. Schmahmann JD, Sherman JC, (1998) The cerebellar cognitive affective syndrome. Brain 121 (Pt 4): 561-579.
77. Schneider F, Habel U, Wagner M, Franke P, Salloum JB, Shah NJ, Toni I, Sulzbach C, Honig K, Maier W, Gaebel W, Zilles K, (2001) Subcortical correlates of craving in recently abstinent alcoholic patients. Am J Psychiatry 158: 1075-1083.
78. Seidman LJ, Biederman J, Liang L, Valera EM, Monuteaux MC, Brown A, Kaiser J, Spencer T, Faraone SV, Makris N, (2011) Gray matter alterations in adults with attention-deficit/hyperactivity disorder identified by voxel based morphometry. Biol Psychiatry 69: 857-866.
79. Sell LA, Morris JS, Bearn J, Frackowiak RSJ, Friston KJ, Dolan RJ, (2000) Neural responses associated with cue evoked emotional states and heroin in opiate addicts. Drug Alcohol Depend 60: 207-216.
80. Shear PK, Sullivan EV, Lane B, Pfefferbaum A, (1996) Mammillary body and cerebellar shrinkage in chronic alcoholics with and without amnesia. Alcohol Clin Exp Res 20: 1489-1495.
81. Sim ME, Lyoo IK, Streeter CC, Covell J, Sarid-Segal O, Ciraulo DA, Kim MJ, Kaufman MJ, Yurgelun-Todd DA, Renshaw PF, (2007) Cerebellar gray matter volume correlates with duration of cocaine use in cocaine-dependent subjects. Neuropsychopharmacology 32: 2229-2237.
82. Sneider JT, Pope HG, Jr, Silveri MM, Simpson NS, Gruber SA, Yurgelun-Todd DA, (2008) Differences in regional blood volume during a 28-day period of abstinence in chronic cannabis smokers. Eur Neuropsychopharmacol 18: 612-619.
83. Solowij N, Yücel M, Respondek C, Whittle S, Lindsay E, Pantelis C, Lubman DI, (2011) Cerebellar white-matter changes in cannabis users with and without schizophrenia. Psychol Med 41: 2349-2359.
84. Sorensen SM, Johnson SW, Freedman R, (1982) Persistent effects of amphetamine on cerebellar Purkinje neurons following chronic administration. Brain Res 247: 365-371.
85. Stoodley CJ, (2012) The cerebellum and cognition: evidence from functional imaging studies. Cerebellum 11: 352-365.
86. Stoodley CJ, Schmahmann JD, (2009) Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage 44: 489-501.
87. Strick PL, Dum RP, Fiez JA, (2009) Cerebellum and nonmotor function. Annu Rev Neurosci 32: 413-434.
88. Sullivan EV, Deshmukh A, Desmond JE, Mathalon DH, Rosenbloom MJ, Lim KO, Pfefferbaum A, (2000) Contribution of alcohol abuse to cerebellar volume deficits in men with schizophrenia. Arch Gen Psychiatry 57: 894-902.
89. Sullivan EV, Rohlfing T, Pfefferbaum A, (2010) Pontocerebellar volume deficits and ataxia in alcoholic men and women: no evidence for 'telescoping'. Psychopharmacology (Berl) 208: 279-290.
90. Swain RA, Kerr AL, Thompson RF, (2011) The cerebellum: a neural system for the study of reinforcement learning. Front Behav Neurosci 5: 8.
91. Tessner KD, Hill SY, (2010) Neural circuitry associated with risk for alcohol use disorders. Neuropsychol Rev 20: 1-20.
92. Thoma P, Bellebaum C, Koch B, Schwarz M, Daum I, (2008) The cerebellum is involved in reward-based reversal learning. Cerebellum 7: 433-443.
93. Tzilos GK, Cintron CB, Wood JBR, Simpson NS, Young AD, Pope HG, Jr, Yurgelun-Todd DA, (2005) Lack of hippocampal volume change in long-term heavy cannabis users. Am J Addict 14: 64-72.
94. Uǧurbil K, Xu J, Auerbach EJ, Moeller S, Vu AT, Duarte-Carvajalino JM, Lenglet C, Wu X, Schmitter S, Van de Moortele PF, Strup J, Sapiro G, Martino FD, Wang D, Harel N, Garwood M, Chen L, Feinberge DA, Smith SM, Miller KL, Sotiropoulos SN, Jbabh S, Andersson JLR, Behrens TEJ, Glasser MF, Van Essen DC, Yacoud E, (2013) Pushing spatial and temporal resolution for functional and diffusion MRI in the Human Connectome Project. Neuroimage 80: 80-104.
95. Upadhyay J, Maleki N, Potter J, Elman I, Rudrauf D, Knudsen J, Wallin D, Pendse G, McDonald L, Griffin M, Anderson J, Nutile L, Renshaw P, Weiss R, Becerra L, Borsook D, (2010) Alterations in brain structure and functional connectivity in prescription opioid-dependent patients. Brain 133 (Pt 7): 2098-2114.
96. Volkow ND, Fowler JS, Wang G-J, (2003) The addicted human brain: insights from imaging studies. J Clin Invest 111: 1444-1451.
97. Volkow ND, Gillespie H, Mullani N, Tancredi L, Grant C, Ivanovic M, Hollister L, (1991) Cerebellar metabolic activation by delta-9-tetrahydro- cannabinol in human brain: a study with positron emission tomography and 18F-2-fluoro-2-deoxyglucose. Psychiatry Res 40: 69-78.
98. Volkow ND, Gillespie H, Mullani N, Tancredi L, Grant C, Valentine A, Hollister L, (1996) Brain glucose metabolism in chronic marijuana users at baseline and during marijuana intoxication. Psychiatry Res 67: 29-38.
99. Volkow ND, Wang GJ, Fowler JS, Hitzemann R, Angrist B, Gatley SJ, Logan J, Ding YS, Pappas N, (1999) Association of methylphenidate-induced craving with changes in right striato-orbitofrontal metabolism in cocaine abusers: implications in addiction. Am J Psychiatry 156: 19-26.
100. Volkow ND, Wang GJ, Fowler JS, Logan J, Angrist B, Hitzemann R, Lieberman J, Pappas N, (1997) Effects of methylphenidate on regional brain glucose metabolism in humans: relationship to dopamine D2 receptors. Am J Psychiatry 154: 50-55.
101. Volkow ND, Wang G-J, Fowler JS, 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.
102. Volkow ND, Wang G-J, Ma Y, Fowler JS, Wong C, Jayne M, Telang F, Swanson JM, (2006) Effects of expectation on the brain metabolic responses to methylphenidate and to its placebo in non-drug abusing subjects. Neuroimage 32: 1782-1792.
103. Volkow ND, Wang G-J, Ma Y, Fowler JS, Zhu W, Maynard L, Telang F, Vaska P, Ding YS, Wong C, Swanson JM, (2003) Expectation enhances the regional brain metabolic and the reinforcing effects of stimulants in cocaine abusers. J Neurosci 23: 11461-11468.
104. Walhovd KB, Moe V, Slinning K, Due-Tønnessen P, Bjørnerud A, Dale AM, van der Kouwe A, Quinn BT, Kosofsky B, Greve D, Fischl B, (2007) Volumetric cerebral characteristics of children exposed to opiates and other substances in utero. Neuroimage 36: 1331-1344.
105. Wang GJ, Volkow ND, Fowler JS, Cervany P, Hitzemann RJ, Pappas NR, Wong CT, Felder C, (1999) Regional brain metabolic activation during craving elicited by recall of previous drug experiences. Life Sci 64: 775-784.
106. Wilson W, Mathew R, Turkington T, Hawk T, Coleman RE, Provenzale J, (2000) Brain morphological changes and early marijuana use: a magnetic resonance and positron emission tomography study. J Addict Dis 19: 1-22.
107. Yokota O, Tsuchiya K, Terada S, Oshima K, Ishizu H, Matsushita M, Kuroda S, Akiyama H, (2006) Frequency and clinicopathological characteristics of alcoholic cerebellar degeneration in Japan: a cross-sectional study of 1509 postmortems. Acta Neuropathol (Berl) 112: 43-51.
108. Zarei M, Mataix-Cols D, Heyman I, Hough M, Doherty J, Burge L, Winmill L, Nijhawan S, Matthews P, James A, (2011) Changes in gray matter volume and white matter microstructure in adolescents with obsessive-compulsive disorder. Biol Psychiatry 70: 1083-1090.
109. Zubieta J-K, Heitzeg MM, Xu Y, Koeppe RA, Ni L, Guthrie S, Domino EF, (2005) Regional cerebral blood flow responses to smoking in tobacco smokers after overnight abstinence. Am J Psychiatry 162: 567-577.