Right Inferior Frontal Gyrus Theta-burst Stimulation Reduces Smoking Behaviors and Strengthens Fronto-striatal-limbic Resting-state Functional Connectivity: a Randomized Crossover Trial

Overview

Journal Front Psychiatry

Specialty Psychiatry

Date 2023 Jul 17

PMID 37457779

Authors

Spencer Upton

Alexander A Brown

Mojgan Golzy

Eric L Garland

Brett Froeliger

Affiliations

Soon will be listed here.

Abstract

Introduction: Functional and anatomical irregularities in the right inferior frontal gyrus (rIFG), a ventrolateral prefrontal region that mediates top-down inhibitory control over prepotent behavioral responding, are implicated in the ongoing maintenance of nicotine dependence (ND). However, there is little research on the effects of neuromodulation of the rIFG on smoking behavior, inhibitory control, and resting-state functional connectivity (rsFC) among individuals with ND.

Methods: In this double-blind, crossover, theta-burst stimulation (TBS) study, adults with ND ( = 31; female: = 15) completed a baseline session and were then randomized to two counterbalanced sessions of functionally neuronavigated TBS to the rIFG: continuous TBS (cTBS) on 1 day and intermittent TBS (iTBS) on another. Differences in cigarette cravings, smoking, and fronto-striatal-limbic rsFC were assessed.

Results: Relative to baseline, cTBS significantly reduced appetitive and withdrawal cravings immediately after treatment. The effects of cTBS on withdrawal craving persisted for 24 h, as well as produced a reduction in smoking. Furthermore, cTBS significantly strengthened rsFC between the rIFG pars opercularis and subcallosal cingulate (fronto-striatal circuit), and between the rIFG pars opercularis and the right posterior parahippocampal gyrus (fronto-limbic circuit). At post-24 h, cTBS-induced increase in fronto-striatal rsFC was significantly associated with less appetitive craving, while the increase in fronto-limbic rsFC was significantly associated with less withdrawal craving and smoking.

Discussion: These findings warrant further investigation into the potential value of rIFG cTBS to attenuate smoking behavior among individuals with ND.

Citing Articles

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References

Gu H, Salmeron B, Ross T, Geng X, Zhan W, Stein E . Mesocorticolimbic circuits are impaired in chronic cocaine users as demonstrated by resting-state functional connectivity. Neuroimage. 2010; 53(2):593-601. PMC: 2930044. DOI: 10.1016/j.neuroimage.2010.06.066. View

Kozink R, Kollins S, McClernon F . Smoking withdrawal modulates right inferior frontal cortex but not presupplementary motor area activation during inhibitory control. Neuropsychopharmacology. 2010; 35(13):2600-6. PMC: 2978758. DOI: 10.1038/npp.2010.154. View

Froeliger B, McConnell P, Stankeviciute N, McClure E, Kalivas P, Gray K . The effects of N-Acetylcysteine on frontostriatal resting-state functional connectivity, withdrawal symptoms and smoking abstinence: A double-blind, placebo-controlled fMRI pilot study. Drug Alcohol Depend. 2015; 156:234-242. PMC: 4633320. DOI: 10.1016/j.drugalcdep.2015.09.021. View

Zhang Y, Gong J, Xie C, Ye E, Jin X, Song H . Alterations in brain connectivity in three sub-regions of the anterior cingulate cortex in heroin-dependent individuals: Evidence from resting state fMRI. Neuroscience. 2014; 284:998-1010. DOI: 10.1016/j.neuroscience.2014.11.007. View

Zilverstand A, Huang A, Alia-Klein N, Goldstein R . Neuroimaging Impaired Response Inhibition and Salience Attribution in Human Drug Addiction: A Systematic Review. Neuron. 2018; 98(5):886-903. PMC: 5995133. DOI: 10.1016/j.neuron.2018.03.048. View

Kunas S, Stuke H, Plank I, Laing E, Bermpohl F, Strohle A . Neurofunctional alterations of cognitive down-regulation of craving in quitting motivated smokers. Psychol Addict Behav. 2022; 36(8):1012-1022. DOI: 10.1037/adb0000820. View

Kirkovski M, Donaldson P, Do M, Speranza B, Albein-Urios N, Oberman L . A systematic review of the neurobiological effects of theta-burst stimulation (TBS) as measured using functional magnetic resonance imaging (fMRI). Brain Struct Funct. 2023; 228(3-4):717-749. PMC: 10113132. DOI: 10.1007/s00429-023-02634-x. View

McCalley D, Lench D, Doolittle J, Imperatore J, Hoffman M, Hanlon C . Determining the optimal pulse number for theta burst induced change in cortical excitability. Sci Rep. 2021; 11(1):8726. PMC: 8062542. DOI: 10.1038/s41598-021-87916-2. View

Amiaz R, Levy D, Vainiger D, Grunhaus L, Zangen A . Repeated high-frequency transcranial magnetic stimulation over the dorsolateral prefrontal cortex reduces cigarette craving and consumption. Addiction. 2009; 104(4):653-60. DOI: 10.1111/j.1360-0443.2008.02448.x. View

10.

Cox L, Tiffany S, Christen A . Evaluation of the brief questionnaire of smoking urges (QSU-brief) in laboratory and clinical settings. Nicotine Tob Res. 2001; 3(1):7-16. DOI: 10.1080/14622200020032051. View

11.

Germeroth L, Carpenter M, Baker N, Froeliger B, LaRowe S, Saladin M . Effect of a Brief Memory Updating Intervention on Smoking Behavior: A Randomized Clinical Trial. JAMA Psychiatry. 2017; 74(3):214-223. PMC: 5930385. DOI: 10.1001/jamapsychiatry.2016.3148. View

12.

Chaarani B, Spechler P, Ivanciu A, Snowe M, Nickerson J, Higgins S . Multimodal Neuroimaging Differences in Nicotine Abstinent Smokers Versus Satiated Smokers. Nicotine Tob Res. 2018; 21(6):755-763. PMC: 7182689. DOI: 10.1093/ntr/nty070. View

13.

Kober H, Mende-Siedlecki P, Kross E, Weber J, Mischel W, Hart C . Prefrontal-striatal pathway underlies cognitive regulation of craving. Proc Natl Acad Sci U S A. 2010; 107(33):14811-6. PMC: 2930456. DOI: 10.1073/pnas.1007779107. View

14.

Hong Y, Wu S, Pedapati E, Horn P, Huddleston D, Laue C . Safety and tolerability of theta burst stimulation vs. single and paired pulse transcranial magnetic stimulation: a comparative study of 165 pediatric subjects. Front Hum Neurosci. 2015; 9:29. PMC: 4316715. DOI: 10.3389/fnhum.2015.00029. View

15.

Froeliger B, McConnell P, Bell S, Sweitzer M, Kozink R, Eichberg C . Association Between Baseline Corticothalamic-Mediated Inhibitory Control and Smoking Relapse Vulnerability. JAMA Psychiatry. 2017; 74(4):379-386. PMC: 5562280. DOI: 10.1001/jamapsychiatry.2017.0017. View

16.

Fedota J, Stein E . Resting-state functional connectivity and nicotine addiction: prospects for biomarker development. Ann N Y Acad Sci. 2015; 1349:64-82. PMC: 4563817. DOI: 10.1111/nyas.12882. View

17.

Weafer J, Crane N, Gorka S, Phan K, de Wit H . Neural correlates of inhibition and reward are negatively associated. Neuroimage. 2019; 196:188-194. PMC: 6559844. DOI: 10.1016/j.neuroimage.2019.04.021. View

18.

Nestor L, McCabe E, Jones J, Clancy L, Garavan H . Differences in "bottom-up" and "top-down" neural activity in current and former cigarette smokers: Evidence for neural substrates which may promote nicotine abstinence through increased cognitive control. Neuroimage. 2011; 56(4):2258-75. DOI: 10.1016/j.neuroimage.2011.03.054. View

19.

Garland E, Froeliger B, Howard M . Mindfulness training targets neurocognitive mechanisms of addiction at the attention-appraisal-emotion interface. Front Psychiatry. 2014; 4:173. PMC: 3887509. DOI: 10.3389/fpsyt.2013.00173. View

20.

Stoeckel L, Chai X, Zhang J, Whitfield-Gabrieli S, Evins A . Lower gray matter density and functional connectivity in the anterior insula in smokers compared with never smokers. Addict Biol. 2015; 21(4):972-81. PMC: 4654721. DOI: 10.1111/adb.12262. View