Acute nicotine differentially impacts anticipatory valence- and magnitude-related striatal activity

Emma Jane Rose, Thomas J. Ross, Betty Jo Salmeron, Mary Lee, Diaa M. Shakleya, Marilyn A. Huestis, Elliot A. Stein

Research output: Contribution to journalArticle

31 Citations (Scopus)

Abstract

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.

Original languageEnglish (US)
Pages (from-to)280-288
Number of pages9
JournalBiological Psychiatry
Volume73
Issue number3
DOIs
StatePublished - Feb 1 2013

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Corpus Striatum
Nicotine
Reward
Motivation
Placebos
Tobacco Use Cessation Products
Punishment
Prefrontal Cortex
Smoke
Tobacco Products
Smoking

All Science Journal Classification (ASJC) codes

  • Biological Psychiatry

Cite this

Rose, Emma Jane ; Ross, Thomas J. ; Salmeron, Betty Jo ; Lee, Mary ; Shakleya, Diaa M. ; Huestis, Marilyn A. ; Stein, Elliot A. / Acute nicotine differentially impacts anticipatory valence- and magnitude-related striatal activity. In: Biological Psychiatry. 2013 ; Vol. 73, No. 3. pp. 280-288.
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abstract = "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.",
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Acute nicotine differentially impacts anticipatory valence- and magnitude-related striatal activity. / Rose, Emma Jane; Ross, Thomas J.; Salmeron, Betty Jo; Lee, Mary; Shakleya, Diaa M.; Huestis, Marilyn A.; Stein, Elliot A.

In: Biological Psychiatry, Vol. 73, No. 3, 01.02.2013, p. 280-288.

Research output: Contribution to journalArticle

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AU - Salmeron, Betty Jo

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