Greater ventral striatal functional connectivity in cigarette smokers relative to non-smokers across a spectrum of alcohol consumption.
| Title: | Greater ventral striatal functional connectivity in cigarette smokers relative to non-smokers across a spectrum of alcohol consumption. |
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| Authors: | Halcomb ME; Department of Radiology and Imaging Sciences, Indiana University School of Medicine, 355 W. 16th St., GH 4100, Indianapolis, IN, 46202, USA.; Center for Neuroimaging, Department of Radiology and Imaging Sciences, Indiana University School of Medicine, 355 W. 16th St., GH 4100, Indianapolis, IN, 46202, USA.; Dzemidzic M; Center for Neuroimaging, Department of Radiology and Imaging Sciences, Indiana University School of Medicine, 355 W. 16th St., GH 4100, Indianapolis, IN, 46202, USA.; Department of Neurology, Indiana University School of Medicine, 355 W. 16th St., GH 4700, Indianapolis, IN, 46202, USA.; Avena-Koenigsberger A; Department of Radiology and Imaging Sciences, Indiana University School of Medicine, 355 W. 16th St., GH 4100, Indianapolis, IN, 46202, USA.; Center for Neuroimaging, Department of Radiology and Imaging Sciences, Indiana University School of Medicine, 355 W. 16th St., GH 4100, Indianapolis, IN, 46202, USA.; Hile KL; Department of Radiology and Imaging Sciences, Indiana University School of Medicine, 355 W. 16th St., GH 4100, Indianapolis, IN, 46202, USA.; Center for Neuroimaging, Department of Radiology and Imaging Sciences, Indiana University School of Medicine, 355 W. 16th St., GH 4100, Indianapolis, IN, 46202, USA.; Durazzo TC; Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, 401 Quarry Road, Stanford, CA, 94305, USA.; Yoder KK; Department of Radiology and Imaging Sciences, Indiana University School of Medicine, 355 W. 16th St., GH 4100, Indianapolis, IN, 46202, USA. kkyoder@iu.edu.; Center for Neuroimaging, Department of Radiology and Imaging Sciences, Indiana University School of Medicine, 355 W. 16th St., GH 4100, Indianapolis, IN, 46202, USA. kkyoder@iu.edu.; Department of Psychology, Indiana University Purdue University Indianapolis, 402 N. Blackford St, Indianapolis, IN, 46202, USA. kkyoder@iu.edu.; Stark Neurosciences Research Institute, 320 W. 15th St., NB 414, Indianapolis, IN, 46202, USA. kkyoder@iu.edu. |
| Source: | Brain imaging and behavior [Brain Imaging Behav] 2024 Oct; Vol. 18 (5), pp. 1121-1130. Date of Electronic Publication: 2024 Aug 06. |
| Publication Type: | Journal Article |
| Language: | English |
| Journal Info: | Publisher: Springer Country of Publication: United States NLM ID: 101300405 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1931-7565 (Electronic) Linking ISSN: 19317557 NLM ISO Abbreviation: Brain Imaging Behav Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: Secaucus, NJ : Springer |
| MeSH Terms: | Magnetic Resonance Imaging*/methods ; Ventral Striatum*/physiopathology ; Ventral Striatum*/diagnostic imaging ; Alcohol Drinking*/physiopathology ; Neural Pathways*/physiopathology ; Non-Smokers* ; Smokers*; Cigarette Smoking/physiopathology ; Brain Mapping/methods ; Nucleus Accumbens/physiopathology ; Nucleus Accumbens/diagnostic imaging ; Gyrus Cinguli/physiopathology ; Gyrus Cinguli/diagnostic imaging ; Smoking/physiopathology ; Humans ; Male ; Female ; Adult ; Middle Aged ; Young Adult ; Reward |
| Abstract: | Cigarette smoking is associated with elevated risk of disease and mortality and contributes to heavy healthcare-related economic burdens. The nucleus accumbens is implicated in numerous reward-related behaviors, including reinforcement learning and incentive salience. The established functional connectivity of the accumbens includes regions associated with motivation, valuation, and affective processing. Although the high comorbidity of cigarette smoking with drinking behaviors may collectively affect brain activity, there could be independent effects of smoking in alcohol use disorder that impact brain function and behavior. We hypothesized that smoking status, independent of alcohol use, would be associated with aberrations of nucleus accumbens functional connectivity to brain regions that facilitate reward processing, salience attribution, and inhibitory control. Resting state functional magnetic resonance imaging data from thirty-one nonsmokers and nineteen smoking individuals were analyzed using seed-based correlations of the bilateral accumbens with all other brain voxels. Statistical models accounted for drinks consumed per week. The smoking group demonstrated significantly higher functional connectivity between the left accumbens and the bilateral insula and anterior cingulate cortex, as well as hyperconnectivity between the right accumbens and the insula. Confirmatory analyses using the insula and cingulate clusters generated from the original analysis as seed regions reproduced the hyperconnectivity in smokers between the bilateral insular regions and the accumbens. In conclusion, smoking status had distinct effects on neural activity; hyperconnectivity between the accumbens and insula in smokers may reflect enhanced encoding of the reinforcing effects of smoking and greater orientation toward smoking-associated stimuli.; (© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.) |
| Competing Interests: | Declarations. Ethics approval: This study was approved by the Indiana University Institutional Review Board. Consent to participate: All participants provided written informed consent. Consent for publication: All authors consented to submit this work for publication. Competing interests: The authors declare no competing interests. |
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| Grant Information: | R01 AA026014 United States AA NIAAA NIH HHS; T32 AA00746532 United States AA NIAAA NIH HHS; T32 AA007462 United States AA NIAAA NIH HHS; R01 AA01835402 United States AA NIAAA NIH HHS; R01 AA018354 United States AA NIAAA NIH HHS; R21 AA022650 United States AA NIAAA NIH HHS |
| Contributed Indexing: | Keywords: Alcohol use disorder; Cigarette smoking; Functional connectivity; Insula; Nucleus accumbens |
| Entry Date(s): | Date Created: 20240806 Date Completed: 20241121 Latest Revision: 20251221 |
| Update Code: | 20260130 |
| PubMed Central ID: | PMC12716434 |
| DOI: | 10.1007/s11682-024-00903-9 |
| PMID: | 39106000 |
| Database: | MEDLINE |
Journal Article