Chronic cigarette smoking is linked with structural alterations in brain regions showing acute nicotinic drug-induced functional modulations
Open accessAbstract
BACKGROUND: Whereas acute nicotine administration alters brain function which may, in turn, contribute to enhanced attention and performance, chronic cigarette smoking is linked with regional brain atrophy and poorer cognition. However, results from structural magnetic resonance imaging (MRI) studies comparing smokers versus nonsmokers have been inconsistent and measures of gray matter possess limited ability to inform functional relations or behavioral implications. The purpose of this study was to address these interpretational challenges through meta-analytic techniques in the service of clarifying the impact of chronic smoking on gray matter integrity and more fully contextualizing such structural alterations. METHODS: We first conducted a coordinate-based meta-analysis of structural MRI studies to identify consistent structural alterations associated with chronic smoking. Subsequently, we conducted two additional meta-analytic assessments to enhance insight into potential functional and behavioral relations. Specifically, we performed a multimodal meta-analytic assessment to test the structural-functional hypothesis that smoking-related structural alterations overlapped those same regions showing acute nicotinic drug-induced functional modulations. Finally, we employed database driven tools to identify pairs of structurally impacted regions that were also functionally related via meta-analytic connectivity modeling, and then delineated behavioral phenomena associated with such functional interactions via behavioral decoding. RESULTS: Across studies, smoking was associated with convergent structural decreases in the left insula, right cerebellum, parahippocampus, multiple prefrontal cortex (PFC) regions, and the thalamus. Indicating a structural-functional relation, we observed that smoking-related gray matter decreases overlapped with the acute functional effects of nicotinic agonist administration in the left insula, ventromedial PFC, and mediodorsal thalamus. Suggesting structural-behavioral implications, we observed that the left insula's task-based, functional interactions with multiple other structurally impacted regions were linked with pain perception, the right cerebellum's interactions with other regions were associated with overt body movements, interactions between the parahippocampus and thalamus were linked with memory processes, and interactions between medial PFC regions were associated with face processing. CONCLUSIONS: Collectively, these findings emphasize brain regions (e.g., ventromedial PFC, insula, thalamus) critically linked with cigarette smoking, suggest neuroimaging paradigms warranting additional consideration among smokers (e.g., pain processing), and highlight regions in need of further elucidation in addiction (e.g., cerebellum).
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A meta-analysis of 15 papers found that smoking was associated with decreased gray matter in the insula, specifically the left insular cortex.
“Furthermore, a meta-analysis of 15 papers (761 smokers and 1,182 non-smokers) found that smoking was associated with decreased gray matter in the insula, specifically the left insular cortex (Sutherland et al., 2016).”
From The Insula: A Brain Stimulation Target for the Treatment of Addiction (2019) · cites this paper as Sutherland et al., 2016
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The Insula: A Brain Stimulation Target for the Treatment of Addiction
Ibrahim, C., Rubin-Kahana, D. S., Pushparaj, A., Musiol, M., Blumberger, D. M., Daskalakis, Z. J., Zangen, A., & Le Foll, B. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00720 · Cited by 133 · see citing works
- Authors
- Sutherland, M. T., Riedel, M. C., Flannery, J. S., Yanes, J. A., Fox, P. T., Stein, E. A., & Laird, A. R.
- Affiliations
- Florida International University (US)
- Auburn University (US)
- The University of Texas at San Antonio Health Science Center (US)
- National Institutes of Health (US)
- Corresponding author
- Sutherland, Matthew T.
- ORCID
- Venue
- Behavioral and Brain Functions
- Published
- 2016-06-02
- Volume
- 12
- Issue
- 1
- Pages
- 16-16
- ISSN
- 1744-9081 (ISSN-L)
- PMC
- PMC4890474
- OpenAlex
- W2414069252
- Cited by
- 114
- References
- 112
- Citations by year
- 2026: 8 · 2025: 6 · 2024: 10 · 2023: 15 · 2022: 17 · 2021: 16 · 2020: 9 · 2019: 8 · 2018: 13 · 2017: 11 · 2016: 1
- FWCI
- 1.29
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Behavioral and Brain Functions (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Florida International University Digital Commons (Florida International University) (submittedVersion, cc-by)
- Funders
- National Institute on Drug Abuse (K01-DA037819)
- National Institute of Mental Health (R01-MH074457, R56-MH097870)
- Topics
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- chronic cigarette smoking, gray matter atrophy, acute nicotine administration, nicotinic agonists, insula, cerebellum, parahippocampal cortex, prefrontal cortex, thalamus, meta-analytic connectivity modeling, pain perception, memory, face processing, addiction, brain-behavior relationship
- MeSH terms
- Brain, Cerebral Cortex, Chronic Disease, Female, Humans, Magnetic Resonance Imaging, Male, Smoking, Tobacco Use Disorder, Prefrontal Cortex, Neuroimaging, Gray Matter
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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