Neural Signatures of Cognitive Flexibility and Reward Sensitivity Following Nicotinic Receptor Stimulation in Dependent Smokers

Lesage, Elise; Aronson, Sarah E.; Ross, Thomas J.; Salmeron, Betty Jo; Stein, Elliot A.

doi:10.1001/jamapsychiatry.2017.0400

Cited by 38 publications

(52 citation statements)

References 60 publications

(129 reference statements)

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“…However, consistent with previous observations [22] and an effect of chronic nicotine dependence, larger reductions in ventral striatal responsivity to positive feedback among smokers correlated with higher FTND scores, a trait-level measure of addiction severity ( Fig. 4C; left: r [21] = 0.52, p = 0.036; right: r [21] = 0.43, p = 0.13).…”

Section: Imaging Measuressupporting

confidence: 91%

“…within the striatum that manifest as both hypersensitivity to drug-related reward (e.g., cues) [23] and hyposensitivity to monetary rewards [15,17,22,26,32]. Another noteworthy aspect of this study is that the current task utilized non-monetary feedback (i.e., emojis) to inform participants about trial outcomes, thereby speaking to the generalizability of striatal dysfunction beyond the anticipation and receipt of monetary rewards.…”

Section: Discussionmentioning

confidence: 99%

“…Reward processing alterations frequently observed among dependent smokers manifest as both striatal hypo-responsivity to nondrug rewards [15][16][17][18][19][20][21][22] and striatal hyper-responsivity to drug-related stimuli [23,24].…”

Section: Introductionmentioning

confidence: 99%

“…Nicotine delivery via smoking ameliorates acute abstinence-induced dysregulation of affective [28], cognitive [29], and reward processes [30], thereby perpetuating smoking via negative reinforcement [31]. However, emerging evidence suggests a distinction in the neural responses contributing to smoker's dysregulated reward processing such that nicotine administration may normalize blunted striatal activity linked with reward anticipation [15,26], but not with reward receipt [22]. As opposed to being modulated by acute nicotine administration, blunted striatal responsivity to reward receipt has been linked with measures of chronic nicotine exposure including scores on the Fagerström Test of Nicotine Dependence (FTND) [22] and years of daily smoking [16].…”

Section: Introductionmentioning

confidence: 99%

“…However, emerging evidence suggests a distinction in the neural responses contributing to smoker's dysregulated reward processing such that nicotine administration may normalize blunted striatal activity linked with reward anticipation [15,26], but not with reward receipt [22]. As opposed to being modulated by acute nicotine administration, blunted striatal responsivity to reward receipt has been linked with measures of chronic nicotine exposure including scores on the Fagerström Test of Nicotine Dependence (FTND) [22] and years of daily smoking [16]. Accordingly, we have previously proposed that blunted striatal responsivity is linked with trait-level addiction severity whereas other neurobiological circuits (e.g., those centered on the insula) are linked with state-level nicotine withdrawal [32].…”

Section: Introductionmentioning

confidence: 99%

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Habenular and striatal activity during performance feedback are differentially linked with state-like and trait-like aspects of tobacco use disorder

Flannery

Riedel

Poudel

et al. 2019

Preprint

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248 words Manuscript body: 8,724 words Figures: 5 Tables: 0 References: 110 Supplemental Information: 1 file ABSTRACTAlthough tobacco use disorder is linked with functional alterations in the striatum, anterior cingulate cortex (ACC), and insula, preclinical evidence also implicates the habenula as a contributor to negative reinforcement mechanisms maintaining nicotine use. The habenula is a small and understudied epithalamic nucleus involved in reward and aversive processing that is hypothesized to be hyperactive during nicotine withdrawal thereby contributing to anhedonia. In a pharmacologic fMRI study involving administration of nicotine and varenicline, two relatively efficacious cessation aids, we utilized a positive and negative performance feedback task previously shown to differentially activate the striatum and habenula. By administering these nicotinic drugs (vs. placebos) to both overnight abstinent smokers (n=24) and nonsmokers (n=20), we delineated feedbackrelated functional alterations both as a function of a chronic smoking history (trait: smokers vs. nonsmokers) and as a function of drug administration (state: nicotine, varenicline). We observed that smokers showed less ventral striatal responsivity to positive feedback, an alteration not mitigated by drug administration, but rather correlated with higher trait-level addiction severity among smokers and elevated self-reported negative affect across all participants. Conversely, nicotine administration reduced habenula activity following both positive and negative feedback among abstinent smokers, but not nonsmokers; greater habenula activity correlated with elevated abstinence-induced, state-level tobacco craving among smokers and elevated social anhedonia across all participants. These outcomes highlight a dissociation between neurobiological processes linked with the trait of dependence severity and with the state of acute nicotine withdrawal. Interventions simultaneously targeting both aspects may improve currently poor cessation outcomes.One-sentence teaser: In a pharmacological fMRI study, e dissociate brain alterations in the habenula linked with nicotine withdrawal and striatal alterations linked with addiction.

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Section: Imaging Measuressupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Habenular and striatal activity during performance feedback are differentially linked with state-like and trait-like aspects of tobacco use disorder

Flannery

Riedel

Poudel

et al. 2019

Preprint

Self Cite

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Common and separable neural alterations in substance use disorders: A coordinate‐based meta‐analyses of functional neuroimaging studies in humans

Klugah‐Brown

Zweerings

et al. 2020

Human Brain Mapping

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Delineating common and separable neural alterations in substance use disorders (SUD) is imperative to understand the neurobiological basis of the addictive process and to inform substance-specific treatment strategies. Given numerous functional MRI (fMRI) studies in different SUDs, a meta-analysis could provide an opportunity to determine robust shared and substance-specific alterations. The present study employed a coordinate-based meta-analysis covering fMRI studies in individuals with addictive cocaine, cannabis, alcohol, and nicotine use. The primary meta-analysis

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Changes in distinct brain systems identified with fMRI during smoking cessation treatment with varenicline: a review

Panagopoulos,

Bailey,

Kostopoulos

et al. 2024

Psychopharmacology

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Background Varenicline is considered one of the most effective treatment options for smoking cessation. Nonetheless, it is only modestly effective. A deeper comprehension of the effects of varenicline by means of the in-depth review of relevant fMRI studies may assist in paving the development of more targeted and effective treatments. Methodology A search of PubMed and Google Scholar databases was conducted with the keywords “functional magnetic resonance imaging” or “fMRI”, and “varenicline”. All peer-reviewed articles regarding the assessment of smokers with fMRI while undergoing treatment with varenicline and meeting the predefined criteria were included. Results Several studies utilizing different methodologies and targeting different aspects of brain function were identified. During nicotine withdrawal, decreased mesocorticolimbic activity and increased amygdala activity, as well as elevated amygdala-insula and insula-default-mode-network functional connectivity are alleviated by varenicline under specific testing conditions. However, other nicotine withdrawal-induced changes, including the decreased reward responsivity of the ventral striatum, the bilateral dorsal striatum and the anterior cingulate cortex are not influenced by varenicline suggesting a task-dependent divergence in neurocircuitry activation. Under satiety, varenicline treatment is associated with diminished cue-induced activation of the ventral striatum and medial orbitofrontal cortex concomitant with reduced cravings; during the resting state, varenicline induces activation of the lateral orbitofrontal cortex and suppression of the right amygdala. Conclusions The current review provides important clues with regard to the neurobiological mechanism of action of varenicline and highlights promising research opportunities regarding the development of more selective and effective treatments and predictive biomarkers for treatment efficacy.

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Neural Signatures of Cognitive Flexibility and Reward Sensitivity Following Nicotinic Receptor Stimulation in Dependent Smokers

Abstract: clinicaltrials.gov Identifier: NCT00830739.

Cited by 38 publications

References 60 publications

Habenular and striatal activity during performance feedback are differentially linked with state-like and trait-like aspects of tobacco use disorder

Habenular and striatal activity during performance feedback are differentially linked with state-like and trait-like aspects of tobacco use disorder

Common and separable neural alterations in substance use disorders: A coordinate‐based meta‐analyses of functional neuroimaging studies in humans

Changes in distinct brain systems identified with fMRI during smoking cessation treatment with varenicline: a review

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