Negative urgency and ventromedial prefrontal cortex responses to alcohol cues: FMRI evidence of emotion-based impulsivity.
- Authors
- Cyders, Melissa A; Dzemidzic, Mario; Eiler, William J; Coskunpinar, Ayca; Karyadi, Kenny; Kareken, David A
- Year
- 2014
- Journal
- Alcoholism, clinical and experimental research
- PMID
- 24164291
- DOI
- 10.1111/acer.12266
- PMCID
- PMC3946804
BACKGROUND: Recent research has highlighted the role of emotion-based impulsivity (negative and positive urgency personality traits) for alcohol use and abuse, but has yet to examine how these personality traits interact with the brain's motivational systems. Using functional magnetic resonance imaging (fMRI), we tested whether urgency traits and mood induction affected medial prefrontal responses to alcohol odors (AcO). METHODS: Twenty-seven social drinkers (mean age = 25.2, 14 males) had 6 fMRI scans while viewing negative, neutral, or positive mood images (3 mood conditions) during intermittent exposure to AcO and appetitive control (AppCo) aromas. RESULTS: Voxel-wise analyses (p < 0.001) confirmed [AcO > AppCo] activation throughout medial prefrontal cortex (mPFC) and ventromedial PFC (vmPFC) regions. Extracted from a priori mPFC and vmPFC regions and analyzed in Odor (AcO, AppCo) × Mood factorial models, AcO activation was greater than AppCo in left vmPFC (p < 0.001), left mPFC (p = 0.002), and right vmPFC (p = 0.01) regions. Mood did not interact significantly with activation, but the covariate of trait negative urgency accounted for significant variance in left vmPFC (p = 0.01) and right vmPFC (p = 0.01) [AcO > AppCo] activation. Negative urgency also mediated the relationship between vmPFC activation and both (i) subjective craving and (ii) problematic drinking. CONCLUSIONS: The trait of negative urgency is associated with neural responses to alcohol cues in the vmPFC, a region involved in reward value and emotion-guided decision-making. This suggests that negative urgency might alter subjective craving and brain regions involved in coding reward value.
Outline of the imaging session. A total of six functional imaging scans of combined olfactory/visual stimulation were performed (24 2-second odor events in each of the 3 stimulus classes of AcO, AppCo, and SO were intermixed with 32 2-second IAPS image presentations), with two scans completed for each mood (2 positive image scans, 2 negative image scans, and 2 neutral image scans). Scan order was randomly assigned, with a break after the first three scans, although randomization was restricted so that all three moods were experienced prior to and again following the break.
Significant interaction between drink type (AcO = alcohol, AppCo = grape juice) for self-reported craving levels (p = 0.028), such that the difference in craving between alcohol and grape juice was accentuated in the negative and positive mood conditions.
Main Effect of olfactory cues. Brain regions showing [AcO > SO; left panel] and [AcO > AppCo; right panel] BOLD activation pooling over Mood Condition, cluster-level significance, pfdr < 0.05, display height p = 0.001. Four ROIs were identified: left ventromedial prefrontal cortex (red box), right ventromedial prefrontal cortex (blue box), left medial prefrontal cortex (green box) and right medial prefrontal cortex (not shown). The dashed line indicates the boundaries between the medial and prefrontal ROIs (z = −6 on sagittal views; top panel), and between the right and left vmPFC boundaries (x = 0 on axial views; bottom panel). For more details see Table 2. Color bar represents the t-statistic value.
Mood (3: Negative, Neutral, Positive) × Odor (2: [AcO > SO] and [AppCo > SO]) Linear Mixed-Effects Model Results in four medial frontal regions of interest.
Positive correlation between negative urgency and [AcO>SO] BOLD activation in Left and Right vmPFC. Positive correlation between mean [AcO > SO] BOLD activity as extracted (height threshiold p < 0.001) from the left vmPFC (red box) and right vmPFC (blue box) with negative urgency (NUR). For reference, the inset shows a voxel-wise map of the correlation between [AcO > SO] and NUR in voxel-wise analysis (display threshold, p < 0.05; masked for [AcO > SO] activation).
Interaction between Negative Urgency and Craving Type (Alcohol, Grape) for self-reported craving levels.
Negative Urgency (NUR) as a mediator between mean [AcO > SO] BOLD activation in the left and right ventromedial prefrontal cortex mean BOLD activation and (a) Subjective Alcohol Craving (ACQ; left panel) and (b) Problematic Alcohol Use (AUDIT; right panel).
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