Neural substrates of smoking and reward cue reactivity in smokers: a meta-analysis of fMRI studies

Abstract

Smoking is partly attributed to alterations of reward processing. However, findings on the neurobiological mechanisms that underlie smoking-related and smoking-unrelated reward processing in smokers have been inconsistent. Neuroimaging experiments that used functional magnetic resonance imaging (fMRI) and reported brain responses to smoking-related cues and nonsmoking reward-related cues in smokers and healthy controls as coordinates in a standard anatomic reference space were identified by searching the PubMed, Embase, and Web of Science databases up to December 2018. Three meta-analyses were performed using random-effect nonparametric statistics with Seed-based d Mapping software, with brain activity contrast from individual studies as the input. The striatum showed higher activation in response to smoking-related cues compared with neutral cues in 816 smokers from 28 studies and lower activation in response to nonsmoking reward-related cues in 275 smokers compared with 271 healthy control individuals from 13 studies. The relative reactivity of the putamen to smoking-related cues increased in 108 smokers compared with 107 healthy controls from seven studies. Meta-regression showed that smokers with a greater severity of nicotine dependence exhibited less engagement of the striatum in response to both smoking-related cues and nonsmoking reward-related cues. The present results reveal the disruption of reward system function in smokers and provide new insights into diverging theories of addiction. With the escalation of nicotine dependence, nicotine appears to exert dynamic effects on reward processing, based on incentive sensitization theory and reward deficiency syndrome theory.

Nicotine dependence and functional connectivity of insular cortex subregions

“…Our functional connectivity finding is also supported by a structural connectivity study that mapped insular subregions to subcortical regions, indicating that of the subcortical regions tested (thalamus, amygdala, hippocampus, putamen, globus pallidus, caudate nucleus, and nucleus accumbens), the putamen had the most connections with the posterior insula 74 . Association of weaker posterior insula-left putamen functional connectivity with greater nicotine dependence is in line with meta-analytic findings of less engagement of striatal regions in response to smoking-related and non-smoking reward-related cues with greater nicotine dependence 75 . The latter findings suggest that weak posterior insula-putamen connectivity may also be related to disrupted reward-related responses in the striatum.…”

Sexual incentive delay in the scanner: Sexual cue and reward processing, and links to problematic porn consumption and sexual motivation

“…Interestingly, also in substance-related addictions the results concerning the Incentive Sensitization Theory are inconsistent. Several meta-analyses showed an increased cue reactivity in the reward system (Chase, Eickhoff, Laird, & Hogarth, 2011;K€ uhn & Gallinat, 2011b;Schacht, Anton, & Myrick, 2012), but some studies could not confirm these findings (Engelmann et al, 2012;Lin et al, 2020;Zilberman, Lavidor, Yadid, & Rassovsky, 2019). Also for behavioral addictions a higher cue reactivity in the reward network of addictive subjects in comparison to healthy subjects was only found in a minority of the studies as summarized in a most recent review by Antons et al (2020).…”

The cue-reactivity paradigm: An ensemble of networks driving attention and cognition when viewing drug and natural reward-related stimuli

“…In the first iteration, we searched multiple databases, including Google Scholar (https://scholar.google.com) and PubMed (https://www.ncbi.nlm.nih.gov/pubmed), for peer-reviewed articles indexed by a combination of keywords: (“cue-reactivity” OR “drug cue” OR “natural cue”) AND (“fMRI” OR “meta-analysis” OR “GingerALE”) AND/OR (“nicotine” OR “smoking” OR “cocaine” OR “cannabis” OR “heroin” OR “alcohol” OR “sexual” OR “sex” OR “food”). In the second iteration, candidate studies were identified by reviewing the bibliographies of existing meta-analyses [3, 19, 20, 26, 40–42]. Finally, we examined the reference lists of relevant articles for potential studies not located via database searches or existing meta-analyses.…”