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, Matthew P Gunn, M.A Department of Psychology, Southern Illinois University, Carbondale , IL, USA Corresponding author: Matthew P. Gunn, M.A., matthewpgunn@gmail.com, Phone: 217-652-7701, Southern Illinois University, Mail Code 6502, Carbondale, Illinois, 62901-6502. United States, Sydney, NSW, Australia Search for other works by this author on: Oxford Academic Gregory M Rose, Ph.D Department of Anatomy, Southern Illinois University School of Medicine, Carbondale , IL, 62901-4306 USA Search for other works by this author on: Oxford Academic Alexis E Whitton, Ph.D McLean Hospital & Harvard Medical School, Boston , MA, USA Black Dog Institute, University of New South Wales, Sydney , NSW, Australia Search for other works by this author on: Oxford Academic Diego A Pizzagalli, Ph.D McLean Hospital & Harvard Medical School, Boston , MA, USA Search for other works by this author on: Oxford Academic David G Gilbert, Ph.D Department of Psychology, Southern Illinois University, Carbondale , IL, USA Search for other works by this author on: Oxford Academic
https://orcid.org/0000-0003-1017-8577 Nicotine & Tobacco Research, ntae084, https://doi.org/10.1093/ntr/ntae084
Published:
16 April 2024
Article history
Received:
28 August 2023
Published:
16 April 2024
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Matthew P Gunn, Gregory M Rose, Alexis E Whitton, Diego A Pizzagalli, David G Gilbert, Smoking Progression and Nicotine-Enhanced Reward Sensitivity Predicted by Resting-State Functional Connectivity in Salience and Executive Control Networks, Nicotine & Tobacco Research, 2024;, ntae084, https://doi.org/10.1093/ntr/ntae084
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Abstract
Introduction
The neural underpinnings underlying individual differences in nicotine-enhanced reward sensitivity and smoking progression are poorly understood. Thus, we investigated whether brain resting-state functional connectivity (rsFC) during smoking abstinence predicts nicotine-enhanced reward sensitivity and smoking progression in young light smokers. We hypothesized that high rsFC between brain areas with high densities of nicotinic receptors (insula, anterior cingulate cortex [ACC], hippocampus, thalamus) and areas involved in reward-seeking (nucleus accumbens [NAcc], prefrontal cortex [PFC]) would predict nicotine-enhanced reward sensitivity and smoking progression.
Methods
Young light smokers (N=64, age 18-24, M = 1.89 cigarettes/day) participated in the study. These individuals smoked between 5 to 35 cigarettes per week and lifetime use never exceeded 35 cigarettes per week. Their rsFC was assessed using functional magnetic resonance imaging after 14-hour nicotine-deprivation. Subjects also completed a probabilistic reward task after smoking a placebo on one day and a regular cigarette on another day.
Results
The probabilistic-reward-task assessed greater nicotine-enhanced reward sensitivity was associated with greater rsFC between the right anterior PFC and right NAcc, but with reduced rsFC between the ACC and left inferior prefrontal gyrus and the insula and ACC. Decreased rsFC within the salience network (ACC and insula) predicted increased smoking progression across 18 months and greater nicotine-enhanced reward sensitivity.
Conclusions
These findings provide the first evidence that differences in rsFCs in young light smokers are associated with nicotine-enhanced reward sensitivity and smoking progression.
Implications
Weaker rsFC within the salience network predicted greater nicotine-enhanced reward sensitivity and smoking progression. These findings suggest that salience network rsFC and drug-enhanced reward sensitivity may be useful tools and potential endophenotypes for reward sensitivity and drug-dependence research.
Accepted manuscripts
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© The Author(s) 2024. Published by Oxford University Press on behalf of the Society for Research on Nicotine and Tobacco. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.
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