Ventral Striatal Activation During Reward Anticipation Correlates with Impulsivity in Alcoholics

doi:10.1016/j.biopsych.2009.04.035

Biological Psychiatry

Volume 66, Issue 8, 15 October 2009, Pages 734-742

https://doi.org/10.1016/j.biopsych.2009.04.035 Get rights and content

Background

Alcohol dependence is often associated with impulsivity, which may be correlated with dysfunction of the brain reward system. We explored whether functional brain activation during anticipation of incentive stimuli is associated with impulsiveness in detoxified alcoholics and healthy control subjects.

Methods

Nineteen detoxified male alcoholics and 19 age-matched healthy men participated in a functional magnetic resonance imaging (fMRI) study using a monetary incentive delay (MID) task, in which visual cues predicted that a rapid response to a subsequent target stimulus would either result in monetary gain, avoidance of monetary loss, or no consequence. Impulsivity was assessed with the Barratt Impulsiveness Scale-Version 10 (BIS-10).

Results

Detoxified alcoholics showed reduced activation of the ventral striatum during anticipation of monetary gain relative to healthy control subjects. Low activation of the ventral striatum and anterior cingulate during gain anticipation was correlated with high impulsivity only in alcoholics, not in control subjects.

Conclusions

This study suggests that reduced ventral striatal recruitment during anticipation of conventional rewards in alcoholics may be related to their increased impulsivity and indicate possibilities for enhanced treatment approaches in alcohol dependence.

Section snippets

Subjects

Nineteen alcohol-dependent right-handed male patients and 19 age-matched healthy subjects were included in the study. Written informed consent was obtained from all participants. The study was approved by the Ethics Committee of the Charité Universitätsmedizin Berlin. All patients were diagnosed as alcohol-dependent according to ICD-10 and DSM-IV criteria and had no other neurological and psychiatric Axis I disorders and no past history of dependency or current abuse of other drugs than alcohol

Behavioral Data

Healthy subjects succeeded (i.e., responded during target presentation) on 65.98% (SEM = 2.84) of gain trials, on 67.25% (SEM = 1.99) of loss trials, and on 45.47% (SEM = 3.04) of neutral trials and earned €18.82 ± €6.82, on average. Alcohol-dependent patients succeeded on 67.84% (SEM = 2.41) of gain trials, on 62.28% (SEM = 2.75) of loss trials, and on 49.71% (SEM = 4.70) of neutral trials and earned €17.75 ± €5.69, on average. Total average earnings did not differ between the two groups (t =

Discussion

The current findings suggest that reduced ventral striatal activation during reward expectation correlates with impulsivity in alcohol-dependent patients.

Alcoholics showed a significantly reduced activation of the ventral striatum during gain anticipation, as well as a trendwise decrease in ventral striatal activation during loss anticipation. These findings support the hypotheses that the ventral striatum is involved in processing of reward-related cues and that the reward system of alcoholics

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Research suggests that disproportionate exposure to risk factors places American Indian (AI) peoples at higher risk for substance use disorders (SUD). Although SUD is linked to striatal prioritization of drug rewards over other appetitive stimuli, there are gaps in the literature related to the investigation of aversive valuation processing, and inclusion of AI samples. To address these gaps, this study compared striatal anticipatory gain and loss processing between AI-identified with SUD (SUD+; n = 52) and without SUD (SUD-; n = 35) groups from the Tulsa 1000 study who completed a monetary incentive delay (MID) task during functional magnetic resonance imaging. Results indicated that striatal activations in the nucleus accumbens (NAcc), caudate, and putamen were greatest for anticipating gains (ps < 0.001) but showed no group differences. In contrast to gains, the SUD+ exhibited lower NAcc (p = .01, d =0.53) and putamen (p = .04, d =0.40) activation to anticipating large losses than the comparison group. Within SUD+ , lower striatal responses during loss anticipations were associated with slower MID reaction times (NAcc: r = −0.43; putamen: r = −0.35) during loss trials. This is among the first imaging studies to examine underlying neural mechanisms associated with SUD within AIs. Attenuated loss processing provides initial evidence of a potential mechanism wherein blunted prediction of aversive consequences may be a defining feature of SUD that can inform future prevention and intervention targets.
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: Authors AB and FS contributed equally to this work.

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Archival ReportVentral Striatal Activation During Reward Anticipation Correlates with Impulsivity in Alcoholics

Background

Methods

Results

Conclusions

Section snippets

Subjects

Behavioral Data

Discussion

Eur Psychiatry

Neuron

Biol Psychol

Neuron

Neuroimage

Biol Psychiatry

Psychiatry Res

Drug Alcohol Depend

Neuropsychologia

Addict Behav

Biol Psychiatry

Neuroimage

Biol Psychiatry

Addict Behav

Neuropsychologia

Pain

Neural Netw

Neuroimage

Neurosci Biobehav Rev

World Health Statistics

Neurobiologic processes in drug reward and addiction

Harv Rev Psychiatry

Alcohol and dopamine

Alcohol Health Res World

Alcohol-associated stimuli activate the ventral striatum in abstinent alcoholics

J Neural Transm

Differential brain activity in alcoholics and social drinkers to alcohol cues: Relationship to craving

Neuropsychopharmacology

Anticipation of increasing monetary reward selectively recruits nucleus accumbens

J Neurosci

Psychoactive drug use in evolutionary perspective

Science

The neural basis of addiction: A pathology of motivation and choice

Am J Psychiatry

Immediate reward bias in humans: Fronto-parietal networks and a role for the catechol-O-methyltransferase 158(Val/Val) genotype

J Neurosci

The role of cognitive control in cocaine dependence

Neuropsychol Rev

Is decreased prefrontal cortical sensitivity to monetary reward associated with impaired motivation and self-control in cocaine addiction?

Am J Psychiatry

Decision making, impulse control and loss of willpower to resist drugs: A neurocognitive perspective

Nat Neurosci

Neurogenetic adaptive-mechanisms in alcoholism

Science

Serotonergic dysfunction, negative mood states, and response to alcohol

Alcohol Clin Exp Res

The role of behavioral impulsivity in the development of alcohol dependence: A 4-year follow-up study

Alcohol Clin Exp Res

Impulsivity: A link between bipolar disorder and substance abuse

Bipolar Disord

Personality profiles and state aggressiveness in Finnish alcoholic, violent offenders, fire setters, and healthy-volunteers

Arch Gen Psychiatry

Impulsivity in abstinent early- and late-onset alcoholics: Differences in self-report measures and a discounting task

Addiction

Increased sensitivity to the disinhibiting effects of alcohol in binge drinkers

Psychol Addict Behav

Archival Report
Ventral Striatal Activation During Reward Anticipation Correlates with Impulsivity in Alcoholics