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Effects of transcranial magnetic stimulation to the dorsolateral prefrontal cortex on craving and state anxiety in tobacco use disorder

Nature Mental Health volume 1, pages 1001–1012 (2023)Cite this article

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Abstract

Abstinence from cigarettes is associated with withdrawal and anxiety symptoms, which are barriers to smoking cessation, although they may respond to treatment using repetitive transcranial magnetic stimulation (rTMS). We hypothesized that (1) withdrawal symptoms and state anxiety were related and (2) rTMS-related reductions in anxiety would mediate reductions in withdrawal. Participants received one session of rTMS applied to the dorsolateral prefrontal cortex and one session to a control region, and reported their withdrawal and anxiety before and after rTMS. Withdrawal and state anxiety were significantly related (P < 0.001). Stimulation of the dorsolateral prefrontal cortex significantly reduced craving (P < 0.05). However, state anxiety did not mediate this reduction in craving (P > 0.05). Exploratory post-hoc analyses indicated that rTMS had no direct effect on anxiety or affect, and larger amygdala volumes were related to greater craving reductions. This study is a step towards elucidating the psychological mechanisms of rTMS on nicotine withdrawal and craving.

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Fig. 1: CONSORT (consolidated standards of reporting trials) diagram depicting the eligibility screening, attrition and randomization of the treatment arms.
Fig. 2: Individualized rTMS targets.
Fig. 3: Raincloud plot displaying the effects of rTMS on the SJWS craving subscale scores.
Fig. 4: Mediation analysis.

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Data availability

The study design, hypotheses and analysis plan were pre-registered with the Open Science Framework (OSF) data repository, available at https://osf.io/82s6p. The ROIs depicted in Extended Data Fig. 3 and the raw data for the planned and exploratory analyses, including cortical thickness and subcortical volume values, are available for download from the OSF repository at https://osf.io/z3rd5/files/osfstorage. Source data are provided with this paper.

Code availability

The MRI preprocessing and analysis code is available upon request; the tools used to analyse the data are openly available through FSL and Freesurfer.

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Acknowledgements

This work was supported by a National Institute on Drug Abuse grant R00DA045749 to N.P. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. We would like to thank A. Sun, G. Liu, G. Haase, L. Kim, M. Belnap and S. Ewing for their assistance with table/figure creation, data cleaning and proofreading; C. Wells and A. Lin for statistical consulting; J. Gilbert for assistance with MRI data collection; and D. Ngo, N. Vince-Cruz and B. Ramesh for assistance in collecting the TMS data. This work used computational and storage services associated with the Hoffman2 Shared Cluster provided by the UCLA Institute for Digital Research and Education Research Technology Group.

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Authors and Affiliations

  1. Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, CA, USA

    Michael R. Apostol & Andrew F. Leuchter

  2. Department of Psychiatry and Biobehavioral Sciences, UCLA, Los Angeles, CA, USA

    Timothy Jordan & Nicole Petersen

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Contributions

M.R.A. and N.P. conceptualized the research question and analysis plan. M.R.A., T.J., A.F.L. and N.P. collected the data. M.R.A. analysed the behavioral data. T.J. and N.P. performed the neuroimaging data preprocessing. All authors interpreted the results. M.R.A. and N.P. prepared the original draft of the manuscript. A.F.L. contributed to the neuromodulation protocol design, safety and interpretation of the findings. All authors contributed to the critical evaluation of the manuscript. N.P. gave critical supervision and guidance.

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Correspondence to Michael R. Apostol or Nicole Petersen.

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Competing interests

M.R.A., T.J. and N.P. have no conflicts of interest to disclose. A.F.L. has received research support from National Institutes of Health, Department of Defense, and Neuroptics. He serves as a consultant for ElMindA. These organizations were not involved with the conceptualization, design, data collection, analysis, decision to publish or preparation of the manuscript. These organizations will not gain or lose financially through publication of this manuscript.

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Nature Mental Health thanks Abraham Zangen and the other, anonymous reviewers for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Smoking Characteristics.

Smoking behavior and characteristics of participants at baseline (non-abstinent) and pre-rTMS (abstinent).

Source data

Extended Data Fig. 2 Scatterplot.

State anxiety and withdrawal were significantly correlated before (black) and after (gray) rTMS.

Source data

Extended Data Fig. 3 Regions of Interest.

The DLPFC (top panel) and V5 (bottom panel) ROIs were generated by thresholding the left DLPFC and V5, respectively, as defined by neurosynth.org.

Extended Data Fig. 4 Demographics.

Sociodemographic characteristics of participants.

Source data

Supplementary information

Supplementary Information

Supplementary Tables 1–5, Discussion and Figures.

Reporting Summary

Source data

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Apostol, M.R., Jordan, T., Leuchter, A.F. et al. Effects of transcranial magnetic stimulation to the dorsolateral prefrontal cortex on craving and state anxiety in tobacco use disorder. Nat. Mental Health 1, 1001–1012 (2023). https://doi.org/10.1038/s44220-023-00154-5

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