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Nicotine-related beliefs induce dose-dependent responses in the human brain

Nature Mental Health volume 2, pages 177–188 (2024)Cite this article

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Abstract

Beliefs have a powerful influence on our behavior, yet their neural mechanisms remain elusive. Here we investigate whether beliefs could impact brain activities in a way akin to pharmacological dose-dependent effects. Nicotine-dependent humans were told that nicotine strength in an electronic cigarette was either ‘low’, ‘medium’ or ‘high’, while nicotine content was held constant. After vaping, participants underwent functional neuroimaging and performed a decision-making task known to engage neural circuits affected by nicotine. Beliefs about nicotine strength induced dose-dependent responses in the thalamus, a key binding site for nicotine, but not in other brain regions such as the striatum. Nicotine-related beliefs also parametrically modulated the connectivity between the thalamus and ventromedial prefrontal cortex, a region important for decision-making. These findings reveal a high level of precision in the way beliefs influence the brain, offering mechanistic insights into humans’ heterogeneous responses to drugs and a pivotal role of beliefs in addiction.

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Fig. 1: Experimental paradigm and sanity check measures.
Fig. 2: Belief about nicotine strength induced dose-dependent responses in the thalamus.
Fig. 3: Belief about nicotine strength did not modulate striatal reward-related responses.
Fig. 4: Belief about nicotine strength modulated thalamus–vmPFC functional connectivity in a dose-dependent fashion.

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Data availability

Data supporting the findings of this study are deposited at https://osf.io/3hq6s/.

Code availability

The scripts used for data acquisition and analysis are available at https://osf.io/3hq6s/. Analyses were conducted using open software and toolboxes available online as described in Methods (SPM: www.fil.ion.ucl.ac.uk/spm/software/spm12; R Studio: https://www.rstudio.com/products/rstudio/download/#download; Lead-DBS: https://www.lead-dbs.org/download/; MRIcroGL: https://www.nitrc.org/projects/mricrogl/).

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Acknowledgements

This work was supported by National Institute on Drug Abuse grant R01DA043695 (X.G.), National Institute on Drug Abuse grant R21DA049243 (X.G.) and University of Texas, Dallas internal funding (X.G.). The funders had no role in study design, data collection, data analysis or manuscript preparation. We thank staff members at the University of Texas Southwestern Imaging Center for their assistance with scanning, J. Jung and M. Labinski for their help with developing the fMRI task and J. Maclin for her help with participant recruitment. We also thank L. Berner for her advice on the statistical analysis, and D. Schiller and P. Kenny for their helpful discussions and comments on an earlier version of this manuscript.

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Authors and Affiliations

  1. Center for Computational Psychiatry, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Ofer Perl, Anastasia Shuster, Matthew Heflin, Soojung Na, Vincenzo G. Fiore & Xiaosi Gu

  2. Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Ofer Perl, Anastasia Shuster, Matthew Heflin, Soojung Na, Vincenzo G. Fiore & Xiaosi Gu

  3. Nash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Ofer Perl & Xiaosi Gu

  4. School of Behavioral and Brain Sciences, University of Texas at Dallas, Dallas, TX, USA

    Ambereen Kidwai

  5. Department of Pharmacy Practice, Jerry H. Hodge School of Pharmacy, Texas Tech University Health Sciences Center, Dallas, TX, USA

    Natalie Booker & William C. Putnam

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Contributions

Conceptualization: X.G. Methodology: O.P, A.S., N.B., W.C.P. and X.G. Investigation: M.H., S.N. and A.K. Visualization: O.P. Funding acquisition: X.G. Project administration: M.H. and X.G. Supervision: X.G. Writing—original draft: O.P., W.C.P., V.G.F. and X.G. Writing—review and editing: O.P., V.G.F. and X.G.

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Correspondence to Xiaosi Gu.

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Perl, O., Shuster, A., Heflin, M. et al. Nicotine-related beliefs induce dose-dependent responses in the human brain. Nat. Mental Health 2, 177–188 (2024). https://doi.org/10.1038/s44220-023-00188-9

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