Presentation of Smoking-Associated Cues Does Not Elicit Dopamine Release after One-Hour Smoking Abstinence: A [11C]-(+)-PHNO PET Study

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Abstract

The presentation of drug-associated cues has been shown to elicit craving and dopamine release in the striatum of drug-dependent individuals. Similarly, exposure to tobacco-associated cues induces craving and increases the propensity to relapse in tobacco- dependent smokers. However, whether exposure to tobacco-associated cues elicits dopamine release in the striatum of smokers remains to be investigated. We hypothesized that presentation of smoking-related cues compared to neutral cues would induce craving and elevation of intrasynaptic dopamine levels in subregions of the striatum and that the magnitude of dopamine release would be correlated with subjective levels of craving in briefly abstinent tobacco smokers. Eighteen participants underwent two [11C]-(+)-PHNO positron emission tomography (PET) scans after one-hour abstinence period: one during presentation of smoking-associated images and one during presentation of neutral images. Smoking cues significantly increased craving compared to neutral cues on one, but not all, craving measures; however, this increase in craving was not associated with overall significant differences in [11C]-(+)-PHNO binding potential (BPND) (an indirect measure of dopamine release) between the two experimental conditions in any of the brain regions of interest sampled. Our findings suggest that presentation of smoking cues does not elicit detectable (by PET) overall increases in dopamine in humans after one-hour nicotine abstinence. Future research should consider studying smoking cue-induced dopamine release at a longer abstinence period, since recent findings suggest the ability of smoking-related cues to induce craving is associated with a longer duration of smoking abstinence. © 2013 Chiuccariello et al.

Figures

  • Table 1. Descriptive characteristics for participants.
  • Figure 1. Craving measures assessed comparing smoking and neutral cue conditions. (a) Visual analog scale measurements of craving for a cigarette assessed every fifteen minutes during cue-presentation (Blocks 1–4) and every 15 minutes following the completion of the paradigm (Blocks 5–6). There was a main effect of cue type (Repeated Measures Analysis of Variance (RM-ANOVA, F(1,17) = 6.935, p,0.05) and time (RM-ANOVA, F(7,119) = 18.098, p,0.005) on craving for a cigarette. (b) Withdrawal symptoms as rated by the Minnesota Nicotine Withdrawal Scale at baseline (prior to cue presentation) and at the end of the scan. There was a main effect of time on withdrawal symptoms (RM-ANOVA, F(1,17) = 23.996, p,0.001) (c) Cigarette craving as measured by the Questionnaire of Smoking Urges Factor 1 (urge to smoke for pleasure effects of smoking) and Factor 2 (urge to smoke for relief of negative effect of withdrawal) at baseline and at the end of the scan. There was a main effect of time on the urge to smoke for pleasurable effects (RM-ANOVA, QSU Factor 1 F(1,17) = 53.866, p,0.001) and on the urge to smoke for relief of negative symptoms (RM-ANOVA, QSU Factor 2, F(1,17) = 27.591, p ,0.001) (d) Cigarette craving measured by the Tobacco Craving Questionnaire factors 1 (Emotionality), 2 (Expectancy), 3 (Compulsivity) and 4 (Purposefulness) at baseline and at the end of the scan. There was a main effect of time on the urge to smoke for relief of negative withdrawal effects (RM-ANOVA, TCQ 1/emotionality F(1,17) = 11.907, p,0.005), urge to smoke for pleasurable effects (RM-ANOVA, TCQ 2/ expectancy F(1,17) = 25.510, p,0.001) and intention to smoke (RM-ANOVA, TCQ 4/purposefulness F(1,17) = 14.336, p,0.005). * p,0.05, ** p,0.01, *** p,0.005 doi:10.1371/journal.pone.0060382.g001
  • Figure 2. [11C]-(+)-PHNO BPND in brain regions of interest. [11C]-(+)-PHNO BPND in the associative striatum (AST), limbic striatum (LST), sensorimotor striatum (SMST), globus pallidus (GP) and substantia nigra (SN) in the neutral and smoking cue conditions. There were no overall significant differences between the cue conditions in [11C]-(+)-PHNO BPND in any of the apriori selected regions of interest. doi:10.1371/journal.pone.0060382.g002
  • Figure 3. High cravers versus low cravers area under the visual analog scale curve and percent change in [11C]-(+)-PHNO BPND in regions of interest. (a) Area under the Visual Analog Scale curve in high cravers and low cravers. (b) Percent change in [11C]-(+)-PHNO BPND in the associative striatum (AST), limbic striatum (LST), sensorimotor striatum (SMST), globus pallidus (GP) and substantia nigra (SN) in high cravers versus low cravers. There were no significant differences in percent change in [11C]-(+)-PHNO BPND in any of the aprior regions of interest when comparing high cravers to low cravers (multivariate analysis of variance (MANOVA) F(5,10) = 0.759, p = 0.731). doi:10.1371/journal.pone.0060382.g003

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Chiuccariello, L., Boileau, I., Guranda, M., Rusjan, P. M., Wilson, A. A., Zawertailo, L., … Le Foll, B. (2013). Presentation of Smoking-Associated Cues Does Not Elicit Dopamine Release after One-Hour Smoking Abstinence: A [11C]-(+)-PHNO PET Study. PLoS ONE, 8(3). https://doi.org/10.1371/journal.pone.0060382

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