Abstinent smokers show reduced brain responses to positive feedback and enhanced responses to negative feedback

Flannery JS, Sutherland MT, Riedel MC, Laird AR, Salmeron BJ, Ross TJ, Stein EA, SfN (2017).


Cigarette smokers attempting to quit will often fail due to nicotine withdrawal symptoms. These symptoms include anxiety, irritability (enhanced sensitivity to negative outcomes), and anhedonia (reduced sensitivity to positive outcomes). To characterize brain activity associated with positive and negative outcomes, as well as differences between smokers and nonsmokers, we utilized a performance feedback fMRI task called the motion prediction (MP) task and collected data from abstinent smokers (n=24) and nonsmoking controls (n=20). We first assessed task effects by characterizing brain activity associated with performance feedback across both smoking and nonsmoking groups and then assessed group effects by identifying differences in brain activity between smokers and nonsmokers. In the MP task participants were presented with positive and negative performance feedback (correct vs. error) that did, or did not, provide information about trial outcomes (informative vs. non-informative). Differential activations on error-trials vs. correct-trials followed by informative, but not non-informative, feedback (response x feedback interaction) were anticipated in task-related regions. Regarding task effects, we found that negative feedback increased activity in the insula, rostral motor cingulate area/supplementary motor area (rCMA) and a habenular/thalamic region, whereas positive feedback increased activity in the ventral striatum (VS; pcorrected < 0.001; Fig.1). These results replicate previously reported task effects and extend the body of literature on human habenula (Hb) activity. Regarding group effects, abstinent smokers vs. nonsmokers displayed elevated insula activity following negative feedback and decreased VS activity following positive feedback (pcorrected < 0.05; Fig.2). These group differences are consistent with a hypodopaminergic view of drug withdrawal and speak to the effect of nicotine withdrawal on performance feedback processing brain activity.