Elsevier

Biological Psychiatry

Volume 71, Issue 8, 15 April 2012, Pages 749-757
Biological Psychiatry

Archival Report
Diminished Frontostriatal Activity During Processing of Monetary Rewards and Losses in Pathological Gambling

https://doi.org/10.1016/j.biopsych.2012.01.006Get rights and content

Background

Mesocorticolimbic neurocircuitry and impulsivity have both been implicated in pathological gambling (PG) and in reward processing. However, the neural underpinnings of specific phases of reward and loss processing in PG and their relationships to impulsivity remain only partially understood. The present functional magnetic resonance imaging study examined brain activity associated with different phases of reward and loss processing in PG. Given an inverse relationship between ventral striatal recruitment during anticipation of monetary rewards and impulsivity in alcohol dependence, the current study explored whether a similar association might also be present in PG.

Methods

Fourteen adults with PG and 14 control comparison participants performed the Monetary Incentive Delay Task to identify brain activation changes associated with reward/loss prospect, reward/loss anticipation, and reward/loss notification. Impulsivity was assessed separately using the Barratt Impulsiveness Scale.

Results

Relative to the control comparison group, the PG group exhibited significantly reduced activity in the ventromedial prefrontal cortex, insula, and ventral striatum during several phases, including the prospect and anticipation phases of both gains and losses. Activity in the ventral striatum correlated inversely with levels of impulsivity in PG participants, consistent with prior findings in alcohol dependence.

Conclusions

Relatively decreased activity in corticostriatal neurocircuitry during multiple phases of reward processing suggests consistent alterations in neurocircuitry underlying incentive valuation and loss prediction. Together with findings in alcohol dependence, these results suggest that impulsive tendencies in addictions may be reflected in diminished ventral striatal activations to reward anticipation and may represent targets for treatment development in addictions.

Section snippets

Participants

Participants were 14 individuals who met criteria for PG and 14 control comparison (CC) participants (demographic and self-reported measures are displayed in Table 1). Sample characteristics are more fully described in Supplement 1. All participants except one CC individual completed the Barratt Impulsivity Scale version 11 (BIS-11) (31). The BIS-11 is a valid and reliable measure of impulsivity that factors into motor, attention, and nonplanning subscales (31). Urine toxicology at the time of

In-Scanner Behavior

Multiple one-way ANOVAs examining behavioral responses in scanner showed no significant between-groups differences in earnings, reaction times, or hit rates on the different incentive conditions (all p > .05; see Supplement 1).

A1Win

Between-group contrasts of neural activity during the A1Win phase revealed significantly decreased activity in PG relative to CC in the medial prefrontal cortex (mPFC) extending through the vmPFC and anterior cingulate into the left VS (Table 2, Figure 2A) and another

Discussion

Consistent with our hypotheses, PG as compared with CC participants showed diminished VS activation during reward anticipation, diminished vmPFC activation during reward outcome, and diminished insula activation during loss outcome. However, these patterns extended to wins and losses, were less phase-specific than hypothesized, and involved additional brain regions. As hypothesized, VS activity during the A2Win phase inversely correlated with impulsivity measures in the PG group. The biological

References (77)

  • D.K. Campbell-Meiklejohn et al.

    Knowing when to stop: The brain mechanisms of chasing losses

    Biol Psychiatry

    (2008)
  • L. Clark et al.

    Gambling near-misses enhance motivation to gamble and recruit win-related brain circuitry

    Neuron

    (2009)
  • J. Hewig et al.

    Hypersensitivity to reward in problem gamblers

    Biol Psychiatry

    (2010)
  • J. Wrase et al.

    Dysfunction of reward processing correlates with alcohol craving in detoxified alcoholics

    Neuroimage

    (2007)
  • T.D. Wager et al.

    Increased sensitivity in neuroimaging analyses using robust regression

    Neuroimage

    (2005)
  • H.C. Breiter et al.

    Acute effects of cocaine on human brain activity and emotion

    Neuron

    (1997)
  • B. Knutson et al.

    Neural predictors of purchases

    Neuron

    (2007)
  • A. Verdejo-Garcia et al.

    A somatic marker theory of addiction

    Neuropharmacology

    (2009)
  • P. Cavedini et al.

    Frontal lobe dysfunction in pathological gambling patients

    Biol Psychiatry

    (2002)
  • A.E. Goudriaan et al.

    Decision making in pathological gambling: A comparison between pathological gamblers, alcohol dependents, persons with Tourette syndrome, and normal controls

    Brain Res Cogn Brain Res

    (2005)
  • H.D. Critchley et al.

    Neural activity in the human brain relating to uncertainty and arousal during anticipation

    Neuron

    (2001)
  • M.P. Paulus et al.

    Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism

    Neuroimage

    (2003)
  • T.D. Wager et al.

    Valence, gender, and lateralization of functional brain anatomy in emotion: A meta-analysis of findings from neuroimaging

    Neuroimage

    (2003)
  • G. Xue et al.

    The impact of prior risk experiences on subsequent risky decision-making: The role of the insula

    Neuroimage

    (2010)
  • N.H. Naqvi et al.

    The hidden island of addiction: The insula

    Trends Neurosci

    (2009)
  • K. Ballard et al.

    Dissociable neural representations of future reward magnitude and delay during temporal discounting

    Neuroimage

    (2009)
  • C. Blanco et al.

    A pilot study of impulsivity and compulsivity in pathological gambling

    Psychiatry Res

    (2009)
  • J.E. Grant et al.

    N-acetyl cysteine, a glutamate-modulating agent, in the treatment of pathological gambling: A pilot study

    Biol Psychiatry

    (2007)
  • S. Krishnan-Sarin et al.

    Behavioral impulsivity predicts treatment outcome in a smoking cessation program for adolescent smokers

    Drug Alcohol Depend

    (2007)
  • C. Holden

    PsychiatryBehavioral addictions debut in proposed DSM-V

    Science

    (2010)
  • M.N. Potenza et al.

    Gambling urges in pathological gambling: A functional magnetic resonance imaging study

    Arch Gen Psychiatry

    (2003)
  • J. Reuter et al.

    Pathological gambling is linked to reduced activation of the mesolimbic reward system

    Nat Neurosci

    (2005)
  • J. Tanabe et al.

    Prefrontal cortex activity is reduced in gambling and nongambling substance users during decision-making

    Hum Brain Mapp

    (2007)
  • N.D. Volkow et al.

    The addicted human brain: Insights from imaging studies

    J Clin Invest

    (2003)
  • M.N. Potenza

    ReviewThe neurobiology of pathological gambling and drug addiction: An overview and new findings

    Philos Trans R Soc Lond B Biol Sci

    (2008)
  • J. Frascella et al.

    Shared brain vulnerabilities open the way for nonsubstance addictions: Carving addiction at a new joint?

    Ann N Y Acad Sci

    (2010)
  • B. Knutson et al.

    Anticipation of increasing monetary reward selectively recruits nucleus accumbens

    J Neurosci

    (2001)
  • S.M. McClure et al.

    The neural substrates of reward processing in humans: The modern role of FMRI

    Neuroscientist

    (2004)
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