Differential brain response to alcohol cue distractors across stages of alcohol dependence

Abstract

Altered attention to alcohol-related cues is implicated in the craving and relapse cycle characteristic of alcohol dependence (ALC). Prior cue reactivity studies typically invoke explicit attention to alcohol cues, so the neural response underlying incidental cue exposure remains unclear. Here, we embed infrequent, task-irrelevant alcohol and non-alcohol cues in an attention-demanding task, enabling evaluation of brain responses to distracting alcohol cues. Alcohol dependent individuals, across illness phase (n=44), and controls (n=20) performed a cue-reactivity fMRI target detection task. Significant Group-by-Distractor effects were observed in dorsal anterior cingulate cortex (ACC), inferior parietal lobule, and amygdala. Controls and long-term abstainers increased recruitment of attention and cognitive control regions, while recent and long-term abstainers decreased limbic recruitment to alcohol distractors. Across phases of ALC, self-reported craving positively correlated with cue-related activations in ventral ACC, medial prefrontal cortex, and cerebellum. Results indicate that brain responses elicited by incidental alcohol cues differentiate phases of ALC.

Copyright © 2012 Elsevier B.V. All rights reserved.

Figures

Figure 1

Mean (± standard error) post-scanner craving ratings by Group (healthy controls = HC; long-term abstainers = LTA; recent abstainers = RA; current drinkers = CD), for alcohol and non-alcohol pictures. For each beverage distractor stimulus, subjects responded to the 4 following statements on a 7-point Likert scale (1= strongly disagree; 7 = strongly agree): 1) I liked looking at this picture, 2) This picture was unpleasant, 3) If I were to drink this, I would enjoy it, 4) I have no desire for this drink. Responses to statements 2 and 4 were inverted, so that for all questions, higher picture rating scores reflect greater endorsement of craving for the beverage stimulus. Results for analyses with craving ratings were as follows (*p< .05): Main effects of Group by Picture Type *Alcohol Picture Ratings, Main effect of Group: (F (3, 60) = 6.94, p<.001); pairwise Tukey HSD corrected follow-ups (CD>HC, p = .03; CD>LTA, p = .001; CD>RA, p = .002) Non-alcohol Picture Ratings, Main effect of Group: non-significant, p > .7

Figure 2

Conjunction of activations to the Alcohol Distractors – Frequents and Non-alcohol Distractors – Frequents contrasts, averaged across group, revealed activations in ventral stream regions (e.g., extrastriate cortex/Brodmann Areas (BA) 18, 19, fusiform gyri), medial temporal regions (hippocampi, parahippocampal gyri), amygdala, thalamus, inferior and superior parietal lobules (BA 7, 40), dorsal cingulate/medial superior frontal cortex (including BA 6, 8, 24, 32), dorsolateral prefrontal cortex (BA 9, 46), and inferior frontal cortex (BA 45, 47) (p < .01, FDR-corrected).

Figure 3

Group-by-Distractor (Alcohol Distractor (AD), Non-alcohol Distractor (NAD)) interaction effects were observed in two regions: A) a left-hemispheric inferior parietal lobule (IPL) cluster (p<.01 height threshold p fwe-corrected and b a right-hemispheric dorsal anterior cingulate cortex cluster bar graphs display each region mean fmri contrast value standard error by group controls="HC;" long-term abstainers="LTA;" recent current drinkers="CD)," with showing significant group-by-distractor effect depicted in figure left.>

Figure 4

Group-by-Distractor (Alcohol Distractor (AD), Non-alcohol Distractor (NAD)) interaction effects in the amygdala region-of-interest (ROI) analysis (p<.003 bar graphs display mean fmri contrast value standard error within the amygdala roi by group controls="HC;" long-term abstainers="LTA;" recent current drinkers="CD)." voxels surviving group-by-distractor f-map intersection are shown in figure left.>

Figure 5

Alcohol beverage craving ratings were positively correlated with Alcohol Distractor – Non-alcohol Distractor (AD-NAD) fMRI mean cluster contrast values within the combined alcohol dependence (ALC) group. Higher craving scores reflect greater self-reported craving to beverage stimuli. Ventral anterior cingulate cortex is depicted in Figure, Top; bilateral cerebellum is depicted in Figure, Bottom (p<.005, height threshold; p<.05, FWE-corrected).