Multimodal Neuroimaging Differences in Nicotine Abstinent Smokers Versus Satiated Smokers

Bader Chaarani, Philip A. Spechler, Alexandra Ivanciu, Mitchell Snowe, Joshua Nickerson, Stephen T. Higgins, Hugh Garavan

Research output: Contribution to journalArticle

Abstract

INTRODUCTION: Research on cigarette smokers suggests cognitive and behavioral impairments. However, much remains unclear how the functional neurobiology of smokers is influenced by nicotine state. Therefore, we sought to determine which state, be it acute nicotine abstinence or satiety, would yield the most robust differences compared with nonsmokers when assessing neurobiological markers of nicotine dependence. METHODS: Smokers (N = 15) and sociodemographically matched nonsmokers (N = 15) were scanned twice using a repeated-measures design. Smokers were scanned after a 24-hour nicotine abstinence and immediately after smoking their usual brand cigarette. The neuroimaging battery included a stop-signal task of response inhibition and pseudocontinuous arterial spin labeling to measure cerebral blood flow (CBF). Whole-brain voxel-wise analyses of covariance were carried out on stop success and stop fail Stop-Signal Task contrasts and CBF maps to assess differences among nonsmokers, abstinent smokers, and satiated smokers. Cluster correction was performed using AFNI's 3dClustSim to achieve a significance of p < .05. RESULTS: Smokers exhibited higher brain activation in bilateral inferior frontal gyrus, a brain region known to be involved in inhibitory control, during successful response inhibitions relative to nonsmokers. This effect was significantly higher during nicotine abstinence relative to satiety. Smokers also exhibited lower CBF in the bilateral inferior frontal gyrus than nonsmokers. These hypoperfusions were not different between abstinence and satiety. CONCLUSIONS: These findings converge on alterations in smokers in prefrontal circuits known to be critical for inhibitory control. These effects are present, even when smokers are satiated, but the neural activity required to achieve performance equal to controls is increased when smokers are in acute abstinence. IMPLICATIONS: Our multimodal neuroimaging study gives neurobiological insights into the cognitive demands of maintaining abstinence and suggests targets for assessing the efficacy of therapeutic interventions.

Original languageEnglish (US)
Pages (from-to)755-763
Number of pages9
JournalNicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco
Volume21
Issue number6
DOIs
StatePublished - May 21 2019
Externally publishedYes

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Cerebrovascular Circulation
Nicotine
Neuroimaging
Prefrontal Cortex
Tobacco Products
Brain
Tobacco Use Disorder
Neurobiology
Smoking
Research
Inhibition (Psychology)
Therapeutics

ASJC Scopus subject areas

  • Public Health, Environmental and Occupational Health

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Multimodal Neuroimaging Differences in Nicotine Abstinent Smokers Versus Satiated Smokers. / Chaarani, Bader; Spechler, Philip A.; Ivanciu, Alexandra; Snowe, Mitchell; Nickerson, Joshua; Higgins, Stephen T.; Garavan, Hugh.

In: Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco, Vol. 21, No. 6, 21.05.2019, p. 755-763.

Research output: Contribution to journalArticle

Chaarani, Bader ; Spechler, Philip A. ; Ivanciu, Alexandra ; Snowe, Mitchell ; Nickerson, Joshua ; Higgins, Stephen T. ; Garavan, Hugh. / Multimodal Neuroimaging Differences in Nicotine Abstinent Smokers Versus Satiated Smokers. In: Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco. 2019 ; Vol. 21, No. 6. pp. 755-763.
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abstract = "INTRODUCTION: Research on cigarette smokers suggests cognitive and behavioral impairments. However, much remains unclear how the functional neurobiology of smokers is influenced by nicotine state. Therefore, we sought to determine which state, be it acute nicotine abstinence or satiety, would yield the most robust differences compared with nonsmokers when assessing neurobiological markers of nicotine dependence. METHODS: Smokers (N = 15) and sociodemographically matched nonsmokers (N = 15) were scanned twice using a repeated-measures design. Smokers were scanned after a 24-hour nicotine abstinence and immediately after smoking their usual brand cigarette. The neuroimaging battery included a stop-signal task of response inhibition and pseudocontinuous arterial spin labeling to measure cerebral blood flow (CBF). Whole-brain voxel-wise analyses of covariance were carried out on stop success and stop fail Stop-Signal Task contrasts and CBF maps to assess differences among nonsmokers, abstinent smokers, and satiated smokers. Cluster correction was performed using AFNI's 3dClustSim to achieve a significance of p < .05. RESULTS: Smokers exhibited higher brain activation in bilateral inferior frontal gyrus, a brain region known to be involved in inhibitory control, during successful response inhibitions relative to nonsmokers. This effect was significantly higher during nicotine abstinence relative to satiety. Smokers also exhibited lower CBF in the bilateral inferior frontal gyrus than nonsmokers. These hypoperfusions were not different between abstinence and satiety. CONCLUSIONS: These findings converge on alterations in smokers in prefrontal circuits known to be critical for inhibitory control. These effects are present, even when smokers are satiated, but the neural activity required to achieve performance equal to controls is increased when smokers are in acute abstinence. IMPLICATIONS: Our multimodal neuroimaging study gives neurobiological insights into the cognitive demands of maintaining abstinence and suggests targets for assessing the efficacy of therapeutic interventions.",
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AB - INTRODUCTION: Research on cigarette smokers suggests cognitive and behavioral impairments. However, much remains unclear how the functional neurobiology of smokers is influenced by nicotine state. Therefore, we sought to determine which state, be it acute nicotine abstinence or satiety, would yield the most robust differences compared with nonsmokers when assessing neurobiological markers of nicotine dependence. METHODS: Smokers (N = 15) and sociodemographically matched nonsmokers (N = 15) were scanned twice using a repeated-measures design. Smokers were scanned after a 24-hour nicotine abstinence and immediately after smoking their usual brand cigarette. The neuroimaging battery included a stop-signal task of response inhibition and pseudocontinuous arterial spin labeling to measure cerebral blood flow (CBF). Whole-brain voxel-wise analyses of covariance were carried out on stop success and stop fail Stop-Signal Task contrasts and CBF maps to assess differences among nonsmokers, abstinent smokers, and satiated smokers. Cluster correction was performed using AFNI's 3dClustSim to achieve a significance of p < .05. RESULTS: Smokers exhibited higher brain activation in bilateral inferior frontal gyrus, a brain region known to be involved in inhibitory control, during successful response inhibitions relative to nonsmokers. This effect was significantly higher during nicotine abstinence relative to satiety. Smokers also exhibited lower CBF in the bilateral inferior frontal gyrus than nonsmokers. These hypoperfusions were not different between abstinence and satiety. CONCLUSIONS: These findings converge on alterations in smokers in prefrontal circuits known to be critical for inhibitory control. These effects are present, even when smokers are satiated, but the neural activity required to achieve performance equal to controls is increased when smokers are in acute abstinence. IMPLICATIONS: Our multimodal neuroimaging study gives neurobiological insights into the cognitive demands of maintaining abstinence and suggests targets for assessing the efficacy of therapeutic interventions.

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