Cigarette smoking leads to persistent and dose-dependent alterations of brain activity and connectivity in anterior insula and anterior cingulate

Zanchi, Davide; Brody, Arthur L.; Montandon, Marie‐Louise; Kopel, Rotem; Emmert, Kirsten; Preti, Maria Giulia; Ville, Dimitri Van De; Haller, Sven

doi:10.1111/adb.12292

Cited by 16 publications

(14 citation statements)

References 48 publications

(53 reference statements)

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“…Our findings add to mounting evidence that the insula plays a central role in addictive behavior (Cisler et al, 2013; Goldstein et al, 2009; McHugh et al, 2013; Naqvi et al, 2014; Noel et al, 2013a; Sutherland, McHugh, Pariyadath, & Stein, 2012; Viswanath et al, 2015; Volkow & Baler, 2015; Wisner, Patzelt, Lim, & MacDonald, 2013; Zhang et al, 2015), including cigarette addiction (Addicott et al, 2015; Clewett et al, 2014; Dinur-Klein et al, 2014; Forget, Pushparaj, & Le Foll, 2010; Gaznick, Tranel, McNutt, & Bechara, 2014; Janes et al, 2010; Naqvi et al, 2007; Suner-Soler et al, 2012; Zanchi et al, 2015). The link between the insula and addiction has largely been conceptualized as one that relates to the interoceptive functions commonly attributed to the region.…”

Section: Discussionsupporting

confidence: 75%

The first day is always the hardest: Functional connectivity during cue exposure and the ability to resist smoking in the initial hours of a quit attempt

et al. 2017

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Quitting smoking is the single best change in behavior that smokers can make to improve their health and extend their lives. Although most smokers express a strong desire to stop using cigarettes, the vast majority of quit attempts end in relapse. Relapse is particularly likely when smokers encounter cigarette cues. A striking number of relapses occur very quickly, with many occurring within as little as 24 hrs. Characterizing what distinguishes successful quit attempts from unsuccessful ones, particularly just after cessation is initiated, is a research priority. We addressed this significant issue by examining the association between functional connectivity during cigarette cue exposure and smoking behavior during the first 24 hrs of a quit attempt. Functional MRI was used to measure brain activity during cue exposure in nicotine-deprived daily smokers during the first day of a quit attempt. Participants were then given the opportunity to smoke. Using data collected in two parent studies, we identified a subset of participants who chose to smoke and a matched subset who declined (n = 38). Smokers who were able to resist smoking displayed significant functional connectivity between the left anterior insula and the dorsolateral prefrontal cortex, whereas there was no such connectivity for those who chose to smoke. Notably, there were no differences in mean levels of activation in brain regions of interest, underscoring the importance of assessing interregional connectivity when investigating the links between cue-related neural responses and overt behavior. To our knowledge, this is the first study to link patterns of functional connectivity and actual cigarette use during the pivotal first hours of attempt to change smoking behavior.

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Section: Discussionsupporting

confidence: 75%

The first day is always the hardest: Functional connectivity during cue exposure and the ability to resist smoking in the initial hours of a quit attempt

et al. 2017

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“…In adults, alterations in functional connectivity between the insula and Acc persisted even following prolonged abstinence in adult smokers (Zanchi et al, 2015), and increased functional connectivity between the insula and sensorimotor areas has been associated with favorable outcomes following a quit-attempt (Addicott et al, 2015). Thus, an important future direction will be to employ network-based analyses to identify network-level factors potentially related to smoking-cessation outcomes among youth.…”

Section: Discussionmentioning

confidence: 99%

Intra-individual changes in Stroop-related activations linked to cigarette abstinence in adolescent tobacco smokers: Preliminary findings

Yip

Balodis²,

Carroll

et al. 2016

Drug and Alcohol Dependence

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Background Adolescence is a crucial time for initiation of tobacco-smoking. Developing more effective treatment interventions for tobacco-smoking in youth is therefore critical to reduce smoking rates in both adolescent and adult populations. Elucidation of the neural mechanisms of successful behavioral change (abstinence) will allow for improvement of therapies based on known brain mechanisms. Methods Twenty-one adolescent tobacco-smokers (14–19 years) participated in functional magnetic resonance imaging (fMRI) during performance of a cognitive control (Stroop) task prior to randomization to smoking cessation treatment (trial of combined nicotine replacement therapy/placebo and contingency management for attendance/abstinence; NCT01145001). Fourteen adolescents also participated in fMRI scanning following completion of the six-week trial. fMRI data were analyzed using random-effects models in SPM12. Paired t-tests were used to identify group-level changes (main effect of treatment exposure) in neural functional responses. Regression models were used to identify individual-level changes associated with treatment-outcomes (percent days abstinent, maximum days of consecutive abstinence). Results Main effects of Stroop task performance (contrast of incongruent versus congruent trials) were seen across a priori ROIs at both pre- and post-treatment (pFWE<.05). At the group-level, no changes in neural responses were found following treatment. However, intra-individual reductions in Stroop-related activity (within the insula and anterior cingulate) were positively associated with measures of smoking abstinence during treatment (pFWE<.05). Conclusions Abstinence from tobacco during smoking cessation treatment among adolescents is associated with cognitive-control related reductions in neural activity within specific regions (anterior cingulate, insula), suggesting that increases in cognitive efficiency may underlie optimal treatment responses in this population.

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“…The presented work is an extension of an fMRI dataset previously published by Zanchi et al (14). Details of the study population, fMRI acquisition protocol, task, and fMRI group analyses and results are defined in the abovementioned publication.…”

Section: Methodsmentioning

confidence: 99%

“…For technical details regarding the fMRI parameters, please see Ref. (14). During the functional run, an on–off block-design with two active conditions (smoking and control cue videos) and a neutral condition (cross displayed) developed by Brody et al (15) were shown as in the previous work (14).…”

Section: Methodsmentioning

confidence: 99%

“…(14). During the functional run, an on–off block-design with two active conditions (smoking and control cue videos) and a neutral condition (cross displayed) developed by Brody et al (15) were shown as in the previous work (14). After each video, a visual analog scale was presented in which the subjects rated the craving perceived during the video cues (0 = no craving, 100 = maximum craving).…”

Section: Methodsmentioning

confidence: 99%

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Sex Effects on Smoking Cue Perception in Non-Smokers, Smokers, and Ex-Smokers: A Pilot Study

et al. 2016

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IntroductionRecent neuroimaging research suggests sex-related brain differences in smoking addiction. In the present pilot study, we assessed gender-related differences in brain activation in response to cigarette-related video cues, investigating non-smokers, smokers, and ex-smokers.MethodsFirst, we compared 29 females (28.6 ± 5.3) vs. 23 males (31.5 ± 6.4), regardless of current smoking status to assess global gender-related effects. Second, we performed a post hoc analysis of non-smokers (9 females and 8 males), smokers (10 females and 8 males), and ex-smokers (10 females and 7 males). Participants performed a block-design functional magnetic resonance imaging paradigm contrasting smoking with control cue video exposures. Data analyses included task-related general linear model, voxel-based morphometry of gray matter (GM), and tract-based spatial statistics of white matter (WM).ResultsFirst, the global effect regardless of current smoking status revealed higher activation in the bilateral superior frontal gyrus and anterior cingulate cortex (ACC) for females compared to males. Second, the analysis according to current smoking status demonstrated higher activation in female vs. male smokers vs. non-smokers in the superior frontal gyrus, anterior and posterior cingulate cortex, and precuneus, and higher activation in female vs. male ex-smokers vs. non-smokers in the right precentral gyrus, in the right insula and ACC. No structural differences were found in GM or WM.ConclusionThe current study identifies gender-related brain functional differences in smokers and ex-smokers compared to non-smokers. The current work can be considered as a starting point for future investigations into gender differences in brain responses to cigarette-related cues.

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Cigarette smoking leads to persistent and dose-dependent alterations of brain activity and connectivity in anterior insula and anterior cingulate

Cited by 16 publications

References 48 publications

The first day is always the hardest: Functional connectivity during cue exposure and the ability to resist smoking in the initial hours of a quit attempt

The first day is always the hardest: Functional connectivity during cue exposure and the ability to resist smoking in the initial hours of a quit attempt

Intra-individual changes in Stroop-related activations linked to cigarette abstinence in adolescent tobacco smokers: Preliminary findings

Sex Effects on Smoking Cue Perception in Non-Smokers, Smokers, and Ex-Smokers: A Pilot Study

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