24-h smoking abstinence potentiates fMRI-BOLD activation to smoking cues in cerebral cortex and dorsal striatum

Abstract

Rationale: Exposure to smoking-related cues can trigger relapse in smokers attempting to maintain abstinence.

Objectives: In the present study, we evaluated the effect of 24-h smoking abstinence on brain responses to smoking-related cues using functional magnetic resonance imaging (fMRI).

Materials and methods: Eighteen adult smokers underwent fMRI scanning following smoking as usual (satiated condition) and following 24-h abstinence (abstinent condition). During scanning, they viewed blocks of photographic smoking and control cues.

Results: Following abstinence, greater activation was found in response to smoking cues compared to control cues in parietal (BA 7/31), frontal (BA 8/9), occipital (BA 19), and central (BA 4) cortical regions and in dorsal striatum (putamen) and thalamus. In contrast, no smoking cue greater than control cue activations were observed following smoking as usual. Direct comparisons between conditions (satiated vs. abstinent) showed greater brain reactivity in response to smoking cues following abstinence. In addition, positive correlations between pre-scan craving in the abstinent condition and smoking cue activation were observed in right dorsomedial prefrontal cortex (dmPFC) including superior frontal gyrus (BA 6/10), anterior cingulate gyrus (BA 32), and supplementary motor area (BA 6).

Conclusions: The present findings indicate that smoking abstinence significantly potentiates neural responses to smoking-related cues in brain regions subserving visual sensory processing, attention, and action planning. Moreover, greater abstinence-induced craving was significantly correlated with increased smoking cue activation in dmPFC areas involved in action planning and decision making. These findings suggest that drug abstinence can increase the salience of conditioned cues, which is consistent with incentive-motivation models of addiction.

Figure 1

Cue-Viewing Task

Figure 2

Pre-scan measures of withdrawal symptoms as reported on the Shiffman-Jarvik Withdrawal Questionnaire (SJWQ). Compared to the satiated condition, abstinence increased pre-scan craving [F(1,17) = 102.67, p < .001], negative affect [F(1,17) = 11.65, p = .003], hunger [F(1,17) = 11.56, p = .003], somatic symptoms [F(1,17) = 6.42, p = .021], and habit withdrawal [F(1,17) = 27.86, < .001]; but decreased arousal [F(1,17) = 13.54, p = .002]. *p<0.05; **p<0.01; ***p<0.001.

Figure 3

BOLD response to smoking cues versus control cues was greater following 24-hr abstinence in right paracentral lobule (PcL; BA 4), right posterior cingulate gyrus (PCG; BA 31), bilateral precuneus (Precun; BA 7), left superior frontal gyrus (SFG; BA 8), left medial inferior occipital gyrus (mIOG; BA 19), right superior parietal lobule (SPL; BA 7), and bilateral putamen (Put). There were no significant areas of activation for smoking cues > control cues in the satiated condition. Greater cue-reactivity to smoking cues in the abstinent condition when compared to the satiated condition was observed in the right PCG (BA 31), left SFG (BA 6), bilateral mIOG (BA 19/30), right SPL (BA 7) and right caudate/internal capsule (Cd/iC).

Figure 4

A significant positive correlation between pre-scan craving and smoking cue > control cue activation was observed in right superior frontal gyrus (SFG; BA 6) during the abstinent condition (R²=0.59), but not in the satiated condition (R²=0.08). Similar correlations in the abstinent and satiated conditions were also observed in right anterior cingulated gyrus (ACG; BA 32), right lingual gyrus (LG; BA 18), and right cerebellum. A test of difference between dependent correlations (Steiger 1980) indicated that correlations in the abstinent and satiated conditions were significantly different.