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Acute Nicotine Differentially Impacts Anticipatory Valence- and Magnitude-Related Striatal Activity

  • Emma Jane Rose
    Correspondence
    Address correspondence to Emma Jane Rose, Ph.D., Transdisciplinary Science and Translational Prevention Program, Molecular Epidemiology, Genomics, Environment and Health, RTI International, 5520 Research Park Drive, Suite 210, UMBC Main Campus, Baltimore, MD 21228
    Affiliations
    Neuroimaging Research Branch, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, Maryland
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  • Thomas J. Ross
    Affiliations
    Neuroimaging Research Branch, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, Maryland
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  • Betty Jo Salmeron
    Affiliations
    Neuroimaging Research Branch, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, Maryland
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  • Mary Lee
    Affiliations
    Neuroimaging Research Branch, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, Maryland
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  • Diaa M. Shakleya
    Affiliations
    Chemistry and Drug Metabolism, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, Maryland
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  • Marilyn A. Huestis
    Affiliations
    Chemistry and Drug Metabolism, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, Maryland
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  • Elliot A. Stein
    Affiliations
    Neuroimaging Research Branch, National Institute on Drug Abuse, Intramural Research Program, National Institutes of Health, Baltimore, Maryland
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      Background

      Dopaminergic activity plays a role in mediating the rewarding aspects of abused drugs, including nicotine. Nicotine modulates the reinforcing properties of other motivational stimuli, yet the mechanisms of this interaction are poorly understood. This study aimed to ascertain the impact of nicotine exposure on neuronal activity associated with reinforcing outcomes in dependent smokers.

      Methods

      Smokers (n = 28) and control subjects (n = 28) underwent functional imaging during performance of a monetary incentive delay task. Using a randomized, counterbalanced design, smokers completed scanning after placement of a nicotine or placebo patch; nonsmokers were scanned twice without nicotine manipulation. In regions along dopaminergic pathway trajectories, we considered event-related activity for valence (reward/gain vs. punishment/loss), magnitude (small, medium, large), and outcome (successful vs. unsuccessful).

      Results

      Both nicotine and placebo patch conditions were associated with reduced activity in regions supporting anticipatory valence, including ventral striatum. In contrast, relative to controls, acute nicotine increased activity in dorsal striatum for anticipated magnitude. Across conditions, anticipatory valence-related activity in the striatum was negatively associated with plasma nicotine concentration, whereas the number of cigarettes daily correlated negatively with loss anticipation activity in the medial prefrontal cortex only during abstinence.

      Conclusions

      These data suggest a partial dissociation in the state- and trait-specific effects of smoking and nicotine exposure on magnitude- and valence-dependent anticipatory activity within discrete reward processing brain regions. Such variability may help explain, in part, nicotine's impact on the reinforcing properties of nondrug stimuli and speak to the continued motivation to smoke and cessation difficulty.

      Key Words

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      Linked Article

      • Nicotine, Striatum, and Reward
        Biological PsychiatryVol. 73Issue 3
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          The ability to resist an immediate, smaller reward to get a larger, delayed reward is impaired in current smokers (1) and is thought to reflect greater impulsivity that leads to relapse to cigarette smoking. Although studies have shown that this type of delay discounting is greater in abstinent smokers than in those who have smoked just before the test (2), it is not clear what role smoking status and acute effects of nicotine play on the brain circuits that are important for this reward processing.
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