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Abstract:Despite an increased understanding of nicotine addiction, there is a scarcity of research comparing the neural correlates of non-drug reward between smokers and ex-smokers. Long-term changes in reward-related brain functioning for non-drug incentives may elucidate patterns of functioning that potentially contribute to ongoing smoking behaviour in current smokers. Similarly, examining the effects of previous chronic nicotine exposure during a period of extended abstinence may reveal whether there are neural correlates responsible for non-drug reward processing that are different from current smokers. The current study, therefore, set out to examine the neural correlates of reward and loss anticipation, and their respective outcomes, in smokers, ex-smokers and matched controls using a monetary incentive delay task during functional MRI. Here we report that in the absence of any significant behavioural group differences, both smokers and ex-smokers showed a significantly greater activation change in the lateral orbitofrontal/anterior insular cortex compared to smokers when anticipating both potential monetary gains and losses. We further report that ex-smokers showed a significantly greater activation change in the ventral putamen compared to both controls and smokers, and in the caudate compared to controls during the anticipation of potential monetary losses only. The results suggest that smoking may sensitize striato-orbitofrontal circuitry subserving motivational processes for loss avoidance and reward gain in nicotine addiction. Comments to the Author This is a revision of an article detailing brain response differences between smokers, ex-smokers and non-smokers using the monetary incentive delay task. The authors did a great job addressing previous concerns and clarifying the analysis methods.A major limitation of the study is the sample size which could only be addressed by recruiting more subjects, despite this limitation the study is the first step towards dissociating theoretical models of reward processing in smokers.The inclusion of the mask in the supplemental materials is helpful, however, the inclusion of the whole-brain analysis in the supplemental materials would be helpful (although not necessary). The exploratory whole brain analysis demonstrates that the ROI approach did not miss any key reward processing regions. New Author Response: We have now included the ROI mask as a supplementary figure.Reviewer: 1 Comments to the Author SummaryThis report titled 'Smokers and ex-smokers have shared differences in the neural substrates for potential monetary gains and losses' tests the neural correlates of reward and loss anticipation and outcomes via the Monetary Incentive Delay task during fMRI in current cigarette smokers, exsmokers, and non-smoking young adults. This reviewer continues to have no major concerns, but there were some responses that may require further thought and elaboration (outlined below) before this paper is accepted for publication. Materials and MethodsfMRI Data Analysis ...

Addiction to cigarettes presents with considerable health risks and induces high costs on healthcare resources. While the majority of cigarette smokers endorse the desire to quit, only a small percentage of quit attempts lead to full abstinence. Failure to achieve abstinence may arise from maladaptive reactivity in fronto-striatal regions that track positive and negative valence outcomes, thus biasing the choice to smoke in the presence of alternative, non-drug reinforcement. Alternatively, long-term nicotine abstinence may reveal neural substrates of adaptive valence outcome processing that promote and maintain smoking cessation. The present study set out to examine the neural correlates of operant response outcomes in current smokers, ex-smokers and matched controls using a monetary incentive delay task during functional MRI. Here we report that compared to controls, both current smokers and ex-smokers showed significantly less activation change in the left amygdala during positive response outcomes, and in the anterior cingulate cortex, during both positive and negative response outcomes. Ex-smokers, however, demonstrated significantly greater activation change compared to smokers and controls in the right amygdala during negative response outcomes. Activation change in the anterior cingulate cortex and middle frontal gyrus of smokers was significantly negatively correlated with nicotine dependence and cigarette pack-years. These results suggest a pattern of shared and divergent reactivity in current smokers and ex-smokers within corticolimbic regions that track both positive and negative operant response outcomes. Exaggerated adaptive processing in ex-smokers may promote long-term smoking cessation through amplified negative valence outcome monitoring.

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