Cue-induced activation of the striatum and medial prefrontal cortex is associated with subsequent relapse in abstinent alcoholics

Psychopharmacology - Tập 175 - Trang 296-302 - 2004
Sabine M. Grüsser1, Jana Wrase2, Sabine Klein3, Derik Hermann3, Michael N. Smolka3, Matthias Ruf4, Wolfgang Weber-Fahr5, Herta Flor6, Karl Mann3, Dieter F. Braus5, Andreas Heinz2
1Department of Medical Psychology, Campus Charité Mitte, Charité—University Medicine Berlin, Berlin, Germany
2Department of Psychiatry, Charité Campus Mitte, Charité—University Medicine Berlin, Berlin, Germany
3Department of Addictive Behavior and Addiction Medicine, Central Institute of Mental Health, University of Heidelberg, Mannheim, Germany
4Department of NMR-Research in Psychiatry, Central Institute of Mental Health, University of Heidelberg, Mannheim, Germany
5Neuroimage Nord, Department of Psychiatry, University of Hamburg, Hamburg, Germany
6Department of Neuropsychology, Central Institute of Mental Health, University of Heidelberg, Mannheim, Germany

Tóm tắt

Animal experiments have provided evidence that the striatum and medial prefrontal cortex play a predominant role in the acquisition and maintenance of drug-seeking behavior. Alcohol-associated stimuli that were regularly paired with alcohol intake may become conditioned cues and elicit a motivational response that triggers relapse in alcohol-dependent patients. We used functional magnetic resonance imaging and visual alcohol-associated and control cues to assess brain activation in ten abstinent alcoholics and control subjects. Patients were followed for 3 months, and alcohol intake was recorded. Alcohol-related versus neutral visual stimuli activated the putamen, anterior cingulate and adjacent medial prefrontal cortex in alcoholics compared with healthy controls. Cue-induced activation of these brain areas was pronounced in the five alcoholics who subsequently relapsed during the observation period. A multiple regression analysis showed that, in alcoholics, the amount of subsequent alcohol intake was associated with the intensity of cue-induced brain activation but not the severity of alcohol craving, amount of previous alcohol intake or duration of abstinence before scanning. This pilot study showed that cue-induced activation of the anterior cingulate, medial prefrontal cortex and striatum may play a role in the attribution of incentive salience to alcohol-associated stimuli, thus increasing the motivational value and attentional processing of alcohol cues. Functional brain imaging may help to identify a group of alcoholics with an otherwise undetected high risk of relapse.

Tài liệu tham khảo

Arnow BA, Desmond JE, Banner LL, Glover GH, Solomon A, Polan ML, Lue TF, Atlas SW (2002) Brain activation and sexual arousal in healthy, heterosexual males. Brain 125:1014–1023 Blood AJ, Zatorre RJ (2001) Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc Natl Acad Sci U S A 98:11818–11823 Bradley MM, Lang PJ (1994) Measuring emotion: the self-assessment manikin and the semantic differential. J Behav Ther Exp Psychiatry 25:49–59 Braus DF, Wrase J, Grusser S, Hermann D, Ruf M, Flor H, Mann K, Heinz A (2001) Alcohol-associated stimuli activate the ventral striatum in abstinent alcoholics. J Neural Transm 108:887–894 Breiter HC, Rosen BR (1999) Functional magnetic resonance imaging of brain reward circuitry in the human. Ann NY Acad Sci 877:523–547 Breiter HC, Aharon I, Kahneman D, Dale A, Shizgal P (2001) Functional imaging of neural responses to expectancy and experience of monetary gains and losses. Neuron 30:619–639 Buechel C, Dolan RJ, Armony JL, Friston KJ (1999) Amygdala-hippocampal involvement in human aversive trace conditioning revealed through event-related functional magnetic resonance imaging. J Neurosci 19:10869–10876 Childress AR, Mozley PD, McElgin W, Fitzgerald J, Reivich M, O’Brien CP (1999) Limbic activation during cue-induced cocaine craving. Am J Psychiatry 156:11–18 Delgado MR, Nystrom LE, Fissell C, Noll DC, Fiez JA (2000) Tracking the hemodynamic responses to reward and punishment in the striatum. J Neurophysiol 84:3072–3077 Di Chiara G (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 7:75–114 Everitt BJ, Wolf ME (2002) Psychomotor stimulant addiction: a neural systems perspective. J Neurosci 22:3312–3320 First MB, Spitzer RL, Gibbon M, Williams J (1997) Structured clinical interview for DSM-IV personality disorders, (SCID-II). American Psychiatric Press, Inc., Washington, DC First MB, Spitzer RL, Gibbon M, Williams J (2001) Structured clinical interview for DSM-IV-TR axis I disorders, research version, patient edition with psychotic screen (SCID-I/P W/PSY SCREEN). Biometrics Research, New York State Psychiatric Institute, New York Friston KJ, Holmes AP, Worsley K, Poline JB, Frith CD, Frackowiak RSJ (1995) Statistical parametric maps in functional brain imaging: a general linear approach. Hum Brain Mapp 2:189–210 Fuster JM (1997) The prefrontal cortex. Anatomy, physiology, and neuropsychology of the frontal lobe. Lippincott-Raven, Philadelphia Garavan H, Pankiewicz J, Bloom A, Cho JK, Sperry L, Ross TJ, Salmeron BJ, Risinger R, Kelley D, Stein EA (2000) Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli. Am J Psychiatry 157:1789–1798 George MS, Anton RF, Bloomer C, Teneback C, Drobes DJ, Lorberbaum JP, Nahas Z, Vincent DJ (2001) Activation of prefrontal cortex and anterior thalamus in alcoholic subjects on exposure to alcohol-specific cues. Arch Gen Psychiatry 58:345–352 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. Proc Natl Acad Sci U S A 93:12040–12045 Grüsser SM, Heinz A, Flor H (2000) Standardized stimuli to assess drug craving and drug memory in addicts. J Neural Transm 107:715–720 Grüsser SM, Heinz A, Raabe A, Wessa M, Podschus J, Flor H (2002) Stimulus-induced craving and startle potentiation in abstinent alcoholics and controls. Eur Psychiatry 17:188–193 Haber SN, Fudge JL, McFarland NR (2000) Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 20:2369–2382 Hamilton MA (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56–62 Heinz A, Dufeu P, Kuhn S, Dettling M, Graf K, Kurten I, Rommelspacher H, Schmidt LG (1996) Psychopathological and behavioral correlates of dopaminergic sensitivity in alcohol-dependent patients. Arch Gen Psychiatry 53:1123–1128 Ito R, Dalley JW, Robbins TW, Everitt BJ (2002) Dopamine release in the dorsal striatum during cocaine seeking behavior under the control of a drug-associated cue. J Neurosci 22:6247–6253 Kampe KK, Frith CD, Dolan RJ, Frith U (2001) Reward value of attractiveness and gaze. Nature 413:589 Knutson B, Fong GW, Adams CM, Varner JL, Hommer D (2001) Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport 12:3683–3687 Koepp MJ, Gunn RN, Lawrence AD, Cunningham VJ, Dagher A, Jones T, Brooks DJ, Bench CJ, Grasby PM (1998) Evidence for striatal dopamine release during a video game. Nature 393:266–268 Koob GF, Le Moal M (1997) Drug abuse: hedonic homeostatic dysregulation. Science 278:52–58 Lang PJ, Oehman A, Vaitl D (1988) The International affective picture system (photographic slides). Center for Research in Psychophysiology, University of Florida, Gainsville, FL Lang PJ, Bradley MM, Fitzsimmons JR, Cuthbert BN, Scott JD, Moulder B, Nangia V (1998) Emotional arousal and activation of the visual cortex: an fMRI analysis. Psychophysiology 35:199–210 Lepage M, Ghaffar O, Nyberg L, Tulving E (2000) Prefrontal cortex and episodic memory retrieval mode. Proc Natl Acad Sci U S A 97:506–511 Maas LC, Lukas SE, Kaufman MJ, Weiss RD, Daniels SL, Rogers VW, Kukes TJ, Renshaw PF (1998) Functional magnetic resonance imaging of human brain activation during cue-induced cocaine craving. Am J Psychiatry 155:124–126 Miller WR, Del Boca FK (1994) Measurement of drinking behavior using the Form 90 family of instruments. J Stud Alcohol 12[Suppl]:112–118 Mirenowicz J, Schultz W (1996) Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 379:449–451 Modell JG, Mountz JM (1995) Focal cerebral blood flow change during craving for alcohol measured by SPECT. J Neuropsychiatry Clin Neurosci 7:15–22 Moeller C, Wiklund L, Sommer W, Thorsell A, Heilig M (1997) Decreased experimental anxiety and voluntary ethanol consumption in rats following central but not basolateral amygdala lesions. Brain Res 760:94–101 Mucha RF, Geier A, Stuhlinger M, Mundle G (2000) Appetitive effects of drug cues modelled by pictures of the intake ritual: generality of cue-modulated startle examined with inpatient alcoholics. Psychopharmacology 151:428–432 O’Doherty JP, Deichmann R, Critchley HD, Dolan RJ (2002) Neural responses during anticipation of a primary taste reward. Neuron 33:815–826 Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18:247–291 Sass H, Soyka M, Mann K, Zieglgansberger W (1996) Relapse prevention by acamprosate. Results from a placebo-controlled study on alcohol dependence. Arch Gen Psychiatry 53:673–680 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 Singleton EG, Henningfield JE, Tiffany ST (1994) Alcohol craving questionnaire: ACQ-Now: background and administration manual. NIDA Addiction Research Center, Baltimore Skinner HA, Horn JL (1984) Alcohol dependence scale: users guide. Addiction Research Foundation, Toronto Skinner HA, Sheu WJ (1982) Reliability of alcohol use indices. The lifetime drinking history and the MAST. J Stud Alcohol 43:1157–1170 Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, New York Tiffany ST, Carter BL (1998) Is craving the source of compulsive drug use? Psychopharmacology 12:23–30 Tzschentke TM (1998) Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog Neurobiol 56:613–672 Volkow ND, Wang GJ, Fischman MW, Foltin RW, Fowler JS, Abumrad NN, Vitkun S, Logan J, Gatley SJ, Pappas N, Hitzemann R, Shea CE (1997) Relationship between subjective effects of cocaine and dopamine transporter occupancy. Nature 386:827–830 Wexler BE, Gottschalk CH, Fulbright RK, Prohovnik I, Lacadie CM, Rounsaville BJ, Gore JC (2001) Functional magnetic resonance imaging of cocaine craving. Am J Psychiatry 158:86–95 Wrase J, Grüsser SM, Klein S, Diener C, Hermann D, Flor H, Mann K, Braus DF, Heinz A (2002) Development of alcohol-associated cues and cue-induced brain activation in alcoholics. Eur Psychiatry 17:287–291