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

RationaleAnimal experiments have provided evidence that the striatum and medial prefrontal cortex play a predominant role in the acquisition and maintenance of drug-seeking behavior.ObjectivesAlcohol-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.MethodsWe 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.ResultsAlcohol-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.ConclusionsThis 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.

[1]  M. Hamilton.  A RATING SCALE FOR DEPRESSION , 1960, Journal of neurology, neurosurgery, and psychiatry.

[2]  J. Fuster.  Prefrontal Cortex , 2018 .

[3]  O. Andy.  The prefrontal cortex: Anatomy, physiology and neuropsychology of the frontal lobe , 1981 .

[4]  H A Skinner,et al.  Reliability of alcohol use indices. The Lifetime Drinking History and the MAST. , 1982, Journal of studies on alcohol.

[5]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[6]  K. Berridge,et al.  The neural basis of drug craving: An incentive-sensitization theory of addiction , 1993, Brain Research Reviews.

[7]  F. D. Del Boca,et al.  Measurement of drinking behavior using the Form 90 family of instruments. , 1994, Journal of studies on alcohol. Supplement.

[8]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.

[9]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[10]  J. Mountz,et al.  Focal cerebral blood flow change during craving for alcohol measured by SPECT. , 1995, The Journal of neuropsychiatry and clinical neurosciences.

[11]  A. Heinz,et al.  Psychopathological and behavioral correlates of dopaminergic sensitivity in alcohol-dependent patients. , 1996, Archives of general psychiatry.

[12]  V L Villemagne,et al.  Activation of memory circuits during cue-elicited cocaine craving. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[13]  W. Schultz,et al.  Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli , 1996, Nature.

[14]  K. Mann,et al.  Relapse prevention by acamprosate. Results from a placebo-controlled study on alcohol dependence. , 1996, Archives of general psychiatry.

[15]  M. Heilig,et al.  Decreased experimental anxiety and voluntary ethanol consumption in rats following central but not basolateral amygdala lesions , 1997, Brain Research.

[16]  G F Koob,et al.  Drug abuse: hedonic homeostatic dysregulation. , 1997, Science.

[17]  M. First,et al.  Structured clinical interview for DSM-IV axis II personality disorders : SCID-II , 1997 .

[18]  S. J. Gatley,et al.  Relationship between subjective effects of cocaine and dopamine transporter occupancy , 1997, Nature.

[19]  M. Bradley,et al.  Emotional arousal and activation of the visual cortex: an fMRI analysis. , 1998, Psychophysiology.

[20]  P F Renshaw,et al.  Functional magnetic resonance imaging of human brain activation during cue-induced cocaine craving. , 1998, The American journal of psychiatry.

[21]  B. Carter,et al.  Is craving the source of compulsive drug use? , 1998, Journal of psychopharmacology.

[22]  D. Brooks,et al.  Evidence for striatal dopamine release during a video game , 1998, Nature.

[23]  T. Tzschentke,et al.  Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues , 1998, Progress in Neurobiology.

[24]  M. Reivich,et al.  Limbic activation during cue-induced cocaine craving. , 1999, The American journal of psychiatry.

[25]  H. Breiter,et al.  Functional Magnetic Resonance Imaging of Brain Reward Circuitry in the Human , 1999, Annals of the New York Academy of Sciences.

[26]  Karl J. Friston,et al.  Amygdala–Hippocampal Involvement in Human Aversive Trace Conditioning Revealed through Event-Related Functional Magnetic Resonance Imaging , 1999, The Journal of Neuroscience.

[27]  E. Stein,et al.  Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli. , 2000, The American journal of psychiatry.

[28]  Endel Tulving,et al.  Prefrontal cortex and episodic memory retrieval mode. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[29]  R. Mucha,et al.  Appetitive effects of drug cues modelled by pictures of the intake ritual: generality of cue-modulated startle examined with inpatient alcoholics , 2000, Psychopharmacology.

[30]  H. Flor,et al.  Standardized stimuli to assess drug craving and drug memory in addicts , 2000, Journal of Neural Transmission.

[31]  Nikolaus R. McFarland,et al.  Striatonigrostriatal Pathways in Primates Form an Ascending Spiral from the Shell to the Dorsolateral Striatum , 2000, The Journal of Neuroscience.

[32]  L. Nystrom,et al.  Tracking the hemodynamic responses to reward and punishment in the striatum. , 2000, Journal of neurophysiology.

[33]  J. Lorberbaum,et al.  From the Departments Of , 2022 .

[34]  D. Kahneman,et al.  Functional Imaging of Neural Responses to Expectancy and Experience of Monetary Gains and Losses tasks with monetary payoffs , 2001 .

[35]  D. F. Braus,et al.  Alcohol-associated stimuli activate the ventral striatum in abstinent alcoholics , 2001, Journal of Neural Transmission.

[36]  Brian Knutson,et al.  Dissociation of reward anticipation and outcome with event-related fMRI , 2001, Neuroreport.

[37]  R. Dolan,et al.  Psychology: Reward value of attractiveness and gaze , 2001, Nature.

[38]  K. Zilles,et al.  Subcortical correlates of craving in recently abstinent alcoholic patients. , 2001, The American journal of psychiatry.

[39]  R. Zatorre,et al.  Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[40]  J C Gore,et al.  Functional magnetic resonance imaging of cocaine craving. , 2001, The American journal of psychiatry.

[41]  Barry J. Everitt,et al.  Psychomotor Stimulant Addiction: A Neural Systems Perspective , 2002, The Journal of Neuroscience.

[42]  H. Flor,et al.  Stimulus-induced craving and startle potentiation in abstinent alcoholics and controls , 2002, European Psychiatry.

[43]  J. O'Doherty,et al.  Neural Responses during Anticipation of a Primary Taste Reward , 2002, Neuron.

[44]  G. Di Chiara.  Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. , 2002, Behavioural brain research.

[45]  T. Robbins,et al.  Dopamine Release in the Dorsal Striatum during Cocaine-Seeking Behavior under the Control of a Drug-Associated Cue , 2002, The Journal of Neuroscience.

[46]  J. Desmond,et al.  Brain activation and sexual arousal in healthy, heterosexual males. , 2002, Brain : a journal of neurology.

[47]  H. Flor,et al.  Development of alcohol-associated cues and cue-induced brain activation in alcoholics , 2002, European Psychiatry.

[48]  Arnoud Arntz,et al.  Short-interval test-retest interrater reliability of the Dutch version of the Structured Clinical Interview for DSM-IV personality disorders (SCID-II). , 2003, Journal of personality disorders.