Do brain responses to emotional images and cigarette cues differ? An fMRI study in smokers

Abstract

Chronic smoking is thought to cause changes in brain reward systems that result in overvaluation of cigarette-related stimuli and undervaluation of natural rewards. We tested the hypotheses that, in smokers, brain circuits involved in emotional processing: (i) would be more active during exposure to cigarette-related than neutral pictures; and (ii) would be less active to pleasant compared with cigarette-related pictures, suggesting a devaluation of intrinsically pleasant stimuli. We obtained whole-brain blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging data from 35 smokers during the presentation of pleasant (erotica and romance), unpleasant (mutilations and sad), neutral, and cigarette-related pictures. Whole-brain analyses showed significantly larger BOLD responses during presentation of cigarette-related pictures relative to neutral ones within the secondary visual areas, the cingulate gyrus, the frontal gyrus, the dorsal striatum, and the left insula. BOLD responses to erotic pictures exceeded responses to cigarette-related pictures in all clusters except the insula. Within the left insula we observed larger BOLD responses to cigarette-related pictures than to all other picture categories. By including intrinsically pleasant and unpleasant pictures in addition to neutral ones, we were able to conclude that the presentation of cigarette-related pictures activates brain areas supporting emotional processes, but we did not find evidence of overall reduced activation of the brain reward systems in the presence of intrinsically pleasant stimuli.

Trial registration: ClinicalTrials.gov NCT00507728.

Figure 1

(A) Clusters of significantly higher functional activity during cigarette-related picture processing relative to neutral pictures in the visual association cortex. (B) Event-related time courses of the percent blood oxygenation level-dependent (BOLD) signal change from baseline averaged across cuneus, inferior parietal lobule, and middle temporal gyrus in response to the different categories of pictures. (C) Percent signal change relative to the baseline from 6 to 12 s post stimulus onset averaged across cuneus, inferior parietal lobule, and middle temporal gyrus in response to the different categories of pictures. # indicates that BOLD responses to neutral pictures were significantly smaller than those to all other picture categories (ps < 0.05). ^ indicates that BOLD responses to erotic pictures were significantly larger than those to all other picture categories (ps < 0.001). MUT = mutilations, SAD = sad contents, NEU = neutral people, ROM = romantic couples, ERO = erotic couples, CIG = cigarette-related pictures.

Figure 2

(A) Cluster of significantly higher functional activity during cigarette-related picture processing relative to neutral pictures in the head of the right caudate nucleus (NC, Talairach coordinates: 9, 3, 4; yellow circle), and the left anterior cingulate gyrus (ACG, Talairach coordinates: 0, 38, 2; red circle). (B) Percent signal change relative to the baseline from 6 to 12 s post stimulus onset in the head of the right caudate nucleus in response to the different categories of pictures. ^ BOLD responses to erotic pictures were significantly larger than those to all other picture categories (ps < 0.05). (C) Percent signal change relative to the baseline from 6 to 12 s post stimulus onset averaged across the anterior and the posterior cingulate gyri in response to the different categories of pictures. NC = Caudate Nucleus, ACG = Anterior Cingulate Gyrus, INS = Insula, MUT = mutilations, SAD = sad contents, NEU = neutral people, ROM = romantic couples, ERO = erotic couples, CIG = cigarette-related pictures.

Figure 3

(A) Cluster of significantly higher functional activity during cigarette-related picture processing relative to neutral pictures in the left insula (Talairach coordinates: −37, −8, 9) (B) Percent signal change relative to the baseline from 6 to 12 s post stimulus onset in the left insula in response to the different categories of pictures. Unlike what observed in other all other areas of activation, cigarette-related pictures elicited a larger BOLD response than the other categories of pictures. ◆ = BOLD responses to cigarette-related pictures vs. the mean of all other picture categories p < 0.01; MUT = mutilations, SAD = sad contents, NEU = neutral people, ROM = romantic couples, ERO = erotic couples, CIG = cigarette-related pictures.

Figure 4

(A) Percent signal change relative to the baseline from 6 to 12 s after stimulus onset in the ROIs covering left and right amygdala (Talairach coordinates: ±20, −4, −11; see inset). (B) Percent signal change relative to the baseline from 6 to 12 s after stimulus onset in the two ROIs covering left and right ventral striatum (Talairach coordinates: ±9, 9, −4; see inset). MUT = mutilations, SAD = sad contents, NEU = neutral people, ROM = romantic couples, ERO = erotic couples, CIG = cigarette-related pictures.