Drug addiction and its underlying neurobiological basis: Neuroimaging evidence for the involvement of the frontal cortex

American Journal of Psychiatry

Volumn 159, Issue 10, 2002, Pages 1642-1652

  Goldstein, Rita Z ^a   Volkow, Nora D ^a  

^a BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

(3 CHLOROPHENYL)PIPERAZINE; 4 AMINOBUTYRIC ACID; ALCOHOL; AMPHETAMINE; CANNABIS; COCAINE; CORTICOTROPIN RELEASING FACTOR; DIAMORPHINE; DOPAMINE; DOPAMINE 2 RECEPTOR; GLUCOSE; LORAZEPAM; METHYLPHENIDATE; NEUROTRANSMITTER; NICOTINE; SEROTONIN;

AMYGDALOID NUCLEUS; BRAIN BLOOD FLOW; CINGULATE GYRUS; COGNITION; DENDRITE; DRUG DEPENDENCE; DRUG INTOXICATION; DYSTHYMIA; EXPECTATION; FRONTAL CORTEX; GLUCOSE METABOLISM; HIPPOCAMPUS; HUMAN; LIMBIC SYSTEM; MODEL; MOTIVATION; NEUROANATOMY; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEUS ACCUMBENS; ORBITAL CORTEX; POSITRON EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; PRIORITY JOURNAL; REINFORCEMENT; REVIEW; REWARD; WITHDRAWAL SYNDROME;

BEHAVIOR, ADDICTIVE; CEREBRAL CORTEX; COCAINE-RELATED DISORDERS; COMPULSIVE BEHAVIOR; DOPAMINE; FLUORODEOXYGLUCOSE F18; FRONTAL LOBE; HUMANS; LIMBIC SYSTEM; MODELS, THEORETICAL; REINFORCEMENT (PSYCHOLOGY); SUBSTANCE WITHDRAWAL SYNDROME; SUBSTANCE-RELATED DISORDERS; SYNDROME; TERMINOLOGY; TOMOGRAPHY, EMISSION-COMPUTED;

EID: 0036787356     PISSN: 0002953X     EISSN: None     Source Type: Journal    
DOI: 10.1176/appi.ajp.159.10.1642     Document Type: Review

References (103)

1. Blum K, Braverman ER, Holder JM, Lubar JF, Monastra VJ, Miller D, Lubar JO, Chen TJ, Comings DE: Reward deficiency syndrome: a biogenetic model for the diagnosis and treatment of impulsive, addictive, and compulsive behaviors. J Psychoactive Drugs 2000; 32(suppl i-iv):1-112
2. Koob GF, Caine B, Markou A, Pulvirenti L, Weiss F: Role for the mesocortical dopamine system in the motivating effects of cocaine. NIDA Res Monogr 1994; 145:1-18
3. Di Chiara G: Drug addiction as dopamine-dependent associative learning disorder. Eur J Pharmacol 1999; 375:13-30
4. Volkow ND, Wang G-J, Fowler JS, Logan J, Gatley SJ, Hitzemann R, Chen AD, Dewey SL, Pappas N: Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects. Nature 1997; 386:830-833
5. Liu X, Matochik JA, Cadet JL, London ED: Smaller volume of prefrontal lobe in polysubstance abusers: a magnetic resonance imaging study. Neuropsychopharmacology 1998; 18:243-252
6. Franklin TR, Acton PD, Maldjian JA, Gray JD, Croft JR, Dackis CA, O'Brien CP, Childress AR: Decreased gray matter concentration in the insular, orbitofrontal, cingulate, and temporal cortices of cocaine patients. Biol Psychiatry 2002; 51:134-142
7. Jernigan TL, Butters N, DiTraglia G, Schafer K, Smith T, Irwin M, Grant I, Schuckit M, Cermak LS: Reduced cerebral grey matter observed in alcoholics using magnetic resonance imaging. Alcohol Clin Exp Res 1991; 15:418-427
8. Jernigan TL, Schafer K, Butters N, Cermak LS: Magnetic resonance imaging of alcoholic Korsakoff patients. Neuropsychopharmacology 1991; 4:175-186
9. Pfefferbaum A, Sullivan EV, Mathalon DH, Lim KO: Frontal lobe volume loss observed with magnetic resonance imaging in older chronic alcoholics. Alcohol Clin Exp Res 1997; 21:521-529
10. Robinson TE, Gorny G, Mitton E, Kolb B: Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex. Synapse 2001; 39:257-266
11. Rosenkranz JA, Grace AA: Dopamine attenuates prefrontal cortical suppression of sensory inputs to the basolateral amygdala of rats. J Neurosci 2001; 21:4090-4103
12. Miller EK, Cohen JD: An integrative theory of prefrontal cortex function. Annu Rev Neurosci 2001; 24:167-202
13. Ritz MC, Lamb RJ, Goldberg SR, Kuhar MJ: Cocaine receptors on dopamine transporters are related to self-administration of cocaine. Science 1987; 237:1219-1223
14. Hurd YL, Ungerstedt U: Cocaine: an in vivo microdialysis evaluation of its acute action on dopamine transmission in rat striatum. Synapse 1989; 3:48-54
15. Goeders NE, Smith JE: Reinforcing properties of cocaine in the medial prefrontal cortex: primary action on presynaptic dopaminergic terminals. Pharmacol Biochem Behav 1986; 25:191-199
16. Brown EE, Fibiger HC: Differential effects of excitotoxic lesions of the amygdala on cocaine-induced conditioned locomotion and conditioned place preference. Psychopharmacology (Berl) 1993; 113:123-130
17. Meil WM, See RE: Lesions of the basolateral amygdala abolish the ability of drug associated cues to reinstate responding during withdrawal from self-administered cocaine. Behav Brain Res 1997; 87:139-148
18. Franklin TR, Druhan JP: Expression of Fos-related antigens in the nucleus accumbens and associated regions following exposure to a cocaine-paired environment. Eur J Neurosci 2000; 12: 2097-2106
19. Volkow ND, Wang G-J, Fowler JS, Hitzemann R, Angrist B, Gatley SJ, Logan J, Ding Y-S, Pappas N: Association of methylphenidate-induced craving with changes in right striato-orbitofrontal metabolism in cocaine abusers: implications in addiction. Am J Psychiatry 1999; 156:19-26
20. Fischman MW, Schuster CR, Javaid J, Hatano Y, Davis J: Acute tolerance development to the cardiovascular and subjective effects of cocaine. J Pharmacol Exp Ther 1985; 235:677-682
21. Loh EA, Roberts DC: Break-points on a progressive ratio schedule reinforced by intravenous cocaine increase following depletion of forebrain serotonin. Psychopharmacology (Berl) 1990; 101:262-266
22. Cornish JL, Duffy P, Kalivas PW: A role for nucleus accumbens glutamate transmission in the relapse to cocaine-seeking behavior. Neuroscience 1999; 93:1359-1367
23. Willner P, Muscat R, Papp M: Chronic mild stress-induced anhedonia: a realistic animal model of depression. Neurosci Biobehav Rev 1992; 16:525-534
24. Hodgins DC, el-Guebaly N, Armstrong S: Prospective and retrospective reports of mood states before relapse to substance use. J Consult Clin Psychol 1995; 63:400-407
25. Johanson CE, Fischman MW: The pharmacology of cocaine related to its abuse. Pharmacol Rev 1989; 41:3-52
26. Koob GF, Le Moal M: Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 2001; 24:97-129
27. Volkow ND, Hitzemann R, Wolf AP, Logan J, Fowler JS, Christman D, Dewey SL, Schlyer D, Burr G, Vitkun S, Hirschowitz J: Acute effects of ethanol on regional brain glucose metabolism and transport. Psychiatry Res 1990; 35:39-48
28. London ED, Broussolle EPM, Links JM, Wong DF, Cascella NG, Dannals RF, Sano M, Herning R, Snyder FR, Rippetoe LR, Toung TJK, Jaffe JH, Wagner HN Jr: Morphine-induced metabolic changes in human brain: studies with positron emission tomography and [fluorine 18]fluorodeoxyglucose. Arch Gen Psychiatry 1990; 47:73-81
29. London ED, Cascella NG, Wong DF, Phillips RL, Dannals RF, Links JM, Herning R, Grayson R, Jaffe JH, Wagner HN Jr: Cocaine-induced reduction of glucose utilization in human brain: a study using positron emission tomography and [fluorine 18]-fluorodeoxyglucose. Arch Gen Psychiatry 1990; 47:567-574
30. de Wit H, Metz J, Wagner N, Cooper M: Behavioral and subjective effects of ethanol: relationship to cerebral metabolism using PET. Alcohol Clin Exp Res 1990; 14:482-489
31. Volkow ND, Gillespie H, Mullani N, Tancredi L, Grant C, Valentine A, Hollister L: Brain glucose metabolism in chronic marijuana users at baseline and during marijuana intoxication. Psychiatry Res 1996; 67:29-38
32. Nakamura H, Tanaka A, Nomoto Y Ueno Y, Nakayama Y: Activation of fronto-limbic system in the human brain by cigarette smoking: evaluated by a CBF measurement. Keio J Med 2000; 49(suppl 1):A122-A124
33. Mathew RJ, Wilson WH, Humphreys DF, Lowe JV, Wiethe KE: Regional cerebral blood flow after marijuana smoking. J Cereb Blood Flow Metab 1992; 12:750-758
34. Volkow ND, Mullani N, Gould L, Adler SS, Guynn RW, Overall JE, Dewey S: Effects of acute alcohol intoxication on cerebral blood flow measured with PET. Psychiatry Res 1988; 24:201-209
35. Tiihonen J, Kuikka J, Hakola P, Paanila J, Airaksinen J, Eronen M, Hallikainen T: Acute ethanol-induced changes in cerebral blood flow. Am J Psychiatry 1994; 151:1505-1508
36. Ingvar M, Ghatan PH, Wirsen-Meurling A, Risberg J, Von Heijne G, Stone-Elander S, Ingvar DH: Alcohol activates the cerebral reward system in man. J Stud Alcohol 1998; 59:258-269
37. Wallace EA, Wisniewski G, Zubal G, vanDyck CH, Pfau SE, Smith EO, Rosen MI, Sullivan MC, Woods SW, Kosten TR: Acute cocaine effects on absolute cerebral blood flow. Psychopharmacology (Berl) 1996; 128:17-20
38. Breiter HC, Gollub RL, Weisskoff RM, Kennedy DN, Makris N, Berke JD, Goodman JM, Kantor HL, Gastfriend DR, Riorden JP, Mathew RT, Rosen BR, Hyman SE: Acute effects of cocaine on human brain activity and emotion. Neuron 1997; 19:591-611
39. Stein EA, Pankiewicz J, Harsch HH, Cho J-K, Fuller SA, Hoffmann RG, Hawkins M, Rao SM, Bandettini PA, Bloom AS: Nicotine-induced limbic cortical activation in the human brain: a functional MRI study. Am J Psychiatry 1998; 155:1009-1015
40. Childress AR, Mozley PD, McElgin W, Fitzgerald J, Reivich M, O'Brien CP: Limbic activation during cue-induced cocaine craving. Am J Psychiatry 1999; 156:11-18
41. Garavan H, Pankiewicz J, Bloom A, Cho J-K, Sperry L, Ross TJ, Salmeron BJ, Risinger R, Kelley D, Stein EA: Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli. Am J Psychiatry 2000; 157:1789-1798
42. Grant S, London ED, Newlin DB, Villemagne VL, Liu X, Contoreggi C, Phillips RL, Kimes AS, Margolin A: Activation of memory circuits during cue-elicited cocaine craving. Proc Natl Acad Sci USA 1996; 93:12040-12045
43. Maas LC, Lukas SE, Kaufman MJ, Weiss RD, Daniels SL, Rogers VW, Kukes TJ, Renshaw PF: Functional magnetic resonance imaging of human brain activation during cue-induced cocaine craving. Am J Psychiatry 1998; 155:124-126
44. Wexler BE, Gottschalk CH, Fulbright RK, Prohovnik I, Lacadie CM, Rounsaville BJ, Gore JC: Functional magnetic resonance imaging of cocaine craving. Am J Psychiatry 2001; 158:86-95
45. Wang G-J, Volkow ND, Fowler JS, Cervany P, Hitzemann RJ, Pappas NR, Wong CT, Felder C: Regional brain metabolic activation during craving elicited by recall of previous drug experiences. Life Sci 1999; 64:775-784
46. Ploghaus A, Tracey I, Gati JS, Clare S, Menon RS, Matthews PM, Rawlins JN: Dissociating pain from its anticipation in the human brain. Science 1999; 284:1979-1981
47. Volkow ND, Fowler JS, Wolf AP, Hitzemann R, Dewey S, Bendriem B, Alpert R, Hoff A: Changes in brain glucose metabolism in cocaine dependence and withdrawal. Am J Psychiatry 1991; 148:621-626
48. Tiffany ST: A cognitive model of drug urges and drug-use behavior: role of automatic and nonautomatic processes. Psychol Rev 1990; 97:147-168
49. Volkow ND, Mullani N, Gould KL, Adler S, Krajewski K: Cerebral blood flow in chronic cocaine users: a study with positron emission tomography. Br J Psychiatry 1988; 152:641-648
50. Volkow ND, Hitzemann R, Wang G-J, Fowler JS, Wolf AP, Dewey SL, Handlesman L: Long-term frontal brain metabolic changes in cocaine abusers. Synapse 1992; 11:184-190
51. Volkow ND, Hitzemann R, Wang G-J, Fowler JS, Burr G, Pascani K, Dewey SL, Wolf AP: Decreased brain metabolism in neurologically intact healthy alcoholics. Am J Psychiatry 1992; 149:1016-1022
52. Volkow ND, Wang G-J, Hitzemann R, Fowler JS, Overall JE, Burr G, Wolf AP: Recovery of brain glucose metabolism in detoxified alcoholics. Am J Psychiatry 1994; 151:178-183
53. Volkow ND, Wang G-J, Hitzemann R, Fowler JS, Wolf AP, Pappas N, Biegon A, Dewey SL: Decreased cerebral response to inhibitory neurotransmission in alcoholics. Am J Psychiatry 1993; 150:417-422
54. Volkow ND, Wang G-J, Overall JE, Hitzemann R, Fowler JS, Pappas N, Frecska E, Piscani K: Regional brain metabolic response to lorazepam in alcoholics during early and late alcohol detoxification. Alcohol Clin Exp Res 1997; 21:1278-1284
55. Catafau AM, Etcheberrigaray A, Perez de los Cobos J, Estorch M, Guardia J, Flotats A, Berna L, Mari C, Casas M, Carrio I: Regional cerebral blood flow changes in chronic alcoholic patients induced by naltrexone challenge during detoxification. J Nucl Med 1999; 40:19-24
56. Hommer D, Andreasen P, Rio D, Williams W, Ruttimann U, Momenan R, Zametkin A, Rawlings R, Linnoila M: Effects of m-chlorophenylpiperazine on regional brain glucose utilization: a positron emission tomographic comparison of alcoholic and control subjects. J Neurosci 1997; 17:2796-2806
57. Volkow ND, Fowler JS, Wolf AP, Schlyer D, Shiue C-Y, Alpert R, Dewey SL, Logan J, Bendriem B, Christman D, Hitzemann R, Henn F: Effects of chronic cocaine abuse on postsynaptic dopamine receptors. Am J Psychiatry 1990; 147:719-724
58. Volkow ND, Fowler JS, Wang G-J, Hitzemann R, Logan J, Schlyer D, Dewey S, Wolf AP: Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse 1993; 14:169-177
59. 2 receptor availability in opiate-dependent subjects before and after naloxone-precipitated withdrawal. Neuropsychopharmacology 1997; 16:174-182
60. Volkow ND, Chang L, Wang G-J, Fowler JS, Leonido-Yee M, Franceschi D, Sedler MJ, Gatley SJ, Hitzemann R, Ding Y-S, Logan J, Wong C, Miller EN: Association of dopamine transporter reduction with psychomotor impairment in methamphetamine abusers. Am J Psychiatry 2001; 158:377-382
61. Volkow ND, Wang G-J, Fowler JS, Logan J, Hitzemann R, Ding Y-S, Pappas N, Shea C, Piscani K: Decreases in dopamine receptors but not in dopamine transporters in alcoholics. Alcohol Clin Exp Res 1996; 20:1594-1598
62. 2 receptors in methamphetamine abusers: association with metabolism in the orbitofrontal cortex. Am J Psychiatry 2001; 158:2015-2021
63. Jentsch JD, Taylor JR: Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Psychopharmacology (Berl) 1999; 146:373-390
64. Karreman M, Moghaddam B: The prefrontal cortex regulates the basal release of dopamine in the limbic striatum: an effect mediated by ventral tegmental area. J Neurochem 1996; 66: 589-598
65. Schultz W, Tremblay L, Hollerman JR: Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb Cortex 2000; 10:272-284
66. Kiyatkin EA, Rebec GV: Dopaminergic modulation of glutamate-induced excitations of neurons in the neostriatum and nucleus accumbens of awake, unrestrained rats. J Neurophysiol 1996; 75:142-153
67. 2 receptor levels. Am J Psychiatry 1999; 156:1440-1443
68. 2 receptors reduces alcohol self-administration. J Neurochem 2001; 78:1094-1103
69. Volkow ND, Fowler JS: Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. Cereb Cortex 2000; 10:318-325
70. Cassens G, Actor C, Kling M, Schildkraut JJ: Amphetamine withdrawal: effects on threshold of intracranial reinforcement. Psychopharmacology (Berl) 1981; 73:318-322
71. Barr AM, Phillips AG: Withdrawal following repeated exposure to d-amphetamine decreases responding for a sucrose solution as measured by a progressive ratio schedule of reinforcement. Psychopharmacology (Berl) 1999; 141:99-106
72. Barr AM, Fiorino DF, Phillips AG: Effects of withdrawal from an escalating dose schedule of d-amphetamine on sexual behavior in the male rat. Pharmacol Biochem Behav 1999; 64:597-604
73. Breiter HC, Aharon I, Kahneman D, Dale A, Shizgal P: Functional imaging of neural responses to expectancy and experience of monetary gains and losses. Neuron 2001; 30:619-639
74. Elliott R, Rees G, Dolan RJ: Ventromedial prefrontal cortex mediates guessing. Neuropsychologia 1999; 37:403-411
75. Berns GS, McClure SM, Pagnoni G, Montague PR: Predictability modulates human brain response to reward. J Neurosci 2001; 21:2793-2798
76. Grant SJ, Bonson KR, Contoreggi CC, London ED: Activation of the ventromedial prefrontal cortex correlates with gambling task performance: a FDG-PET study. Abstracts of the Society for Neuroscience 1999; 25(part 2):1551
77. Rogers RD, Owen AM, Middleton HC, Williams EJ, Pickard JD, Sahakian BJ, Robbins TW: Choosing between small, likely rewards and large, unlikely rewards activates inferior and orbital prefrontal cortex. J Neurosci 1999; 19:9029-9038
78. Elliott R, Frith CD, Dolan RJ: Differential neural response to positive and negative feedback in planning and guessing tasks. Neuropsychologia 1997; 35:1395-1404
79. Thut G, Schultz W, Roelcke U, Nienhusmeier M, Missimer J, Maguire RP, Leenders KL: Activation of the human brain by monetary reward. Neuroreport 1997; 8:1225-1228
80. George MS, Ketter TA, Gill DS, Haxby JV, Ungerleider LG, Herscovitch P, Post RM: Brain regions involved in recognizing facial emotion or identity: an oxygen-15 PET study. J Neuropsychiatry Clin Neurosci 1993; 5:384-394
81. Lane RD, Fink GR, Chau PM, Dolan RJ: Neural activation during selective attention to subjective emotional responses. Neuroreport 1997; 8:3969-3972
82. Pardo JV, Pardo PJ, Raichle ME: Neural correlates of self-induced dysphoria. Am J Psychiatry 1993; 150:713-719
83. Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC: Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 1997; 277:968-971
84. Elliott R, Rubinsztein JS, Sahakian BJ, Dolan RJ: Selective attention to emotional stimuli in a verbal go/no-go task: an fMRI study. Neuroreport 2000; 11:1739-1744
85. Francis S, Rolls ET, Bowtell R, McGlone F, O'Doherty J, Browning A, Clare S, Smith E: The representation of pleasant touch in the brain and its relationship with taste and olfactory areas. Neuroreport 1999; 10:453-459
86. Sprengelmeyer R, Rausch M, Eysel UT, Przuntek H: Neural structures associated with recognition of facial expressions of basic emotions. Proc R Soc Lond B Biol Sci 1998; 265:1927-1931
87. Blair RJR, Morris JS, Frith CD, Perrett DI, Dolan RJ: Dissociable neural responses to facial expressions of sadness and anger. Brain 1999; 122:883-893
88. Casey BJ, Trainor RJ, Orendi JL, Schubert AB, Nystrom LE, Giedd JN, Castellanos FX, Haxby JV, Noll DC, Cohen JD, Forman SD, Dahl RE, Rapoport JL: A developmental functional MRI study of prefrontal activation during performance of a go-no-go task. J Cogn Neurosci 1997; 9:835-847
89. Vaidya CJ, Austin G, Kirkorian G, Ridlehuber HW, Desmond JE, Glover GH, Gabrieli JDE: Selective effects of methylphenidate in attention deficit hyperactivity disorder: a functional magnetic resonance study. Proc Natl Acad Sci USA 1998; 95:14494-14499
90. Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD: Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 1998; 280:747-749
91. Kiehl KA, Liddle PF, Hopfinger JB: Error processing and the rostral anterior cingulate: an event-related fMRI study. Psychophysiology 2000; 37:216-223
92. Rubia K, Overmeyer S, Taylor E, Brammer M, Williams SCR, Simmons A, Andrew C, Bullmore ET: Functional frontalisation with age: mapping neurodevelopmental trajectories with fMRI. Neurosci Biobehav Rev 2000; 24:13-19
93. Krams M, Rushworth MFS, Deiber MP, Frackowiak RSJ, Passingham RE: The preparation, execution and suppression of copied movements in the human brain. Exp Brain Res 1998; 120:386-398.
94. Carter CS, Macdonald AM, Botvinickk M, Ross LL, Stenger VA, Noll D, Cohen JD: Parsing executive processes: strategic vs evaluative functions of the anterior cingulate cortex. Proc Natl Acad Sci USA 2000; 97:1944-1948
95. Goldstein RZ, Volkow ND, Wang G-J, Fowler JS, Rajaram S: Addiction changes orbitofrontal gyrus function: involvement in response inhibition. Neuroreport 2001; 12:2595-2599
96. Nobre AC, Coull JT, Frith CD, Mesulam MM: Orbitofrontal cortex is activated during breaches of expectation in tasks of visual attention. Nat Neurosci 1999; 2:11-12
97. Hugdahl K, Berardi A, Thompson WL, Kosslyn SM, Macy R, Baker DP, Alpert NM, Ledoux JE: Brain mechanisms in human classical conditioning: a PET blood flow study. Neuroreport 1995; 6:1723-1728
98. Chua P, Krams M, Toni I, Passingham R, Dolan R: A functional anatomy of anticipatory anxiety. Neuroimage 1999; 9:563-571
99. Robbins TW, Joyce EM, Sahakian BJ: Neuropsychology and neuroimaging of affective disorders, in Handbook of Affective Disorders. Edited by Paykel ES. London, Churchill Livingston, 1992, pp 289-310
100. Mayberg HS, Liotti M, Brannan SK, McGinnis S, Mahurin RK, Jerabek PA, Silva JA, Tekell JL, Martin CC, Lancaster JL, Fox PT: Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry 1999; 156:675-682
101. Elliott R, Sahakian BJ, Michael A, Paykel ES, Dolan RJ: Abnormal neural response to feedback on planning and guessing tasks in patients with unipolar depression. Psychol Med 1998; 28:559-571
102. Teneback CC, Nahas Z, Speer AM, Molloy M, Stallings LE, Spicer KM, Risch SC, George MS: Changes in prefrontal cortex and paralimbic activity in depression following two weeks of daily left prefrontal TMS. J Neuropsychiatry Clin Neurosci 1999; 11: 426-435
103. Hickie I, Ward P, Scott E, Haindl W, Walker B, Dixon J, Turner K: Neo-striatal rCBF correlates of psychomotor slowing in patients with major depression. Psychiatry Res 1999; 92:75-81