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Greater ventral striatal functional connectivity in cigarette smokers relative to non-smokers across a spectrum of alcohol consumption

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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.

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Acknowledgements

We would like to thank the Indiana Institute of Biomedical Imaging Sciences (IIBIS) In-Vivo Imaging Core, Dr. Yu-Chien Wu and Dr. Qiuting Wen for assistance with sequence development and testing. We also greatly appreciate MRI technologists Robert Bryant, Traci Day, and Will Korst for their help during imaging sessions. In addition, we would like to acknowledge Dr. Jenya Chumin’s excellent work in establishing the image processing protocol and assistance in study day activities.

Funding

This work was supported by the National Institute of Alcohol Abuse and Alcoholism grants R01 AA01835402 (KKY), R21 AA02265002 (KKY), and T32 AA00746532 (MEH).

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Authors and Affiliations

  1. Department of Radiology and Imaging Sciences, Indiana University School of Medicine, 355 W. 16th St., GH 4100, Indianapolis, IN, 46202, USA

    Meredith E. Halcomb, Andrea Avena-Koenigsberger, Karen L. Hile & Karmen K. Yoder

  2. Center for Neuroimaging, Department of Radiology and Imaging Sciences, Indiana University School of Medicine, 355 W. 16th St., GH 4100, Indianapolis, IN, 46202, USA

    Meredith E. Halcomb, Mario Dzemidzic, Andrea Avena-Koenigsberger, Karen L. Hile & Karmen K. Yoder

  3. Department of Neurology, Indiana University School of Medicine, 355 W. 16th St., GH 4700, Indianapolis, IN, 46202, USA

    Mario Dzemidzic

  4. Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, 401 Quarry Road, Stanford, CA, 94305, USA

    Timothy C. Durazzo

  5. Department of Psychology, Indiana University Purdue University Indianapolis, 402 N. Blackford St, Indianapolis, IN, 46202, USA

    Karmen K. Yoder

  6. Stark Neurosciences Research Institute, 320 W. 15th St., NB 414, Indianapolis, IN, 46202, USA

    Karmen K. Yoder

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Contributions

Author contributions included conception and study design (TCD, KKY), data collection, acquisition, and/or processing (MD, MEH, KLH, AAK), statistical analysis (MD, MEH, KKY), interpretation of results (TCD, MD, MEH, KKY), drafting the manuscript work or revising it critically for important intellectual content (MD, TCD, MEH, KKY) and approval of final version to be published and agreement to be accountable for the integrity and accuracy of all aspects of the work (All authors).

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Correspondence to Karmen K. Yoder.

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Halcomb, M.E., Dzemidzic, M., Avena-Koenigsberger, A. et al. Greater ventral striatal functional connectivity in cigarette smokers relative to non-smokers across a spectrum of alcohol consumption. Brain Imaging and Behavior 18, 1121–1130 (2024). https://doi.org/10.1007/s11682-024-00903-9

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  • DOI: https://doi.org/10.1007/s11682-024-00903-9

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