Shared and divergent neural reactivity to non-drug operant response outcomes in current smokers and ex-smokers

Abstract

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.

Subjective reward processing and catechol-O- methyltransferase Val158Met polymorphism as potential research domain criteria in addiction: A pilot study

“…For cannabis-dependent inpatients, gain expectancy correlated negatively with the activation of the right anterior cingulate cortex during the anticipation of gain vs. loss. The anterior cingulate cortex is involved in error monitoring and is affected by nicotine and cannabis (59,60). For error monitoring, the expectation about an action is compared with the outcome and a deviation elicits the correction of behavioral responses (61).…”

Neurobiological Considerations for Tobacco Use Disorder

“…Many comparative studies of past smokers suggest factors that may facilitate prolonged abstinence. For example, when studying reward outcomes on the monetary incentive delay task, one fMRI study identified reduced BOLD signal in both current and past smokers in the left amygdala during monetary gain and in the ACC during monetary gain/loss, and past smokers showed increased BOLD signal in the right amygdala during monetary loss; the latter suggesting alterations in negative valence processing in past smokers that may facilitate abstinence [68]. Another study compared past smokers to current smokers and nonsmokers in two fMRI experiments on an attention bias task, measuring cue-reactivity, and a go/no-go task, measuring error monitoring and response inhibition [69].…”