Exposure to the taste of alcohol elicits activation of the mesocorticolimbic neurocircuitry

Abstract

A growing number of imaging studies suggest that alcohol cues, mainly visual, elicit activation in mesocorticolimbic structures. Such findings are consistent with the growing recognition that these structures play an important role in the attribution of incentive salience and the pathophysiology of addiction. The present study investigated whether the presentation of alcohol taste cues can activate brain regions putatively involved in the acquisition and expression of incentive salience. Using functional magnetic resonance imaging, we recorded BOLD activity while delivering alcoholic tastes to 37 heavy drinking but otherwise healthy volunteers. The results yielded a pattern of BOLD activity in mesocorticolimbic structures (ie prefrontal cortex, striatum, ventral tegmental area/substantia nigra) relative to an appetitive control. Further analyses suggested strong connectivity between these structures during cue-elicited urge and demonstrated significant positive correlations with a measure of alcohol use problems (ie the Alcohol Use Disorders Identification Test). Thus, repeated exposure to the taste alcohol in the scanner elicits activation in mesocorticolimbic structures, and this activation is related to measures of urge and severity of alcohol problems.

Conflict of interest statement

DISCLOSURE/CONFLICT OF INTEREST

Dr Kent Hutchison was paid consulting fee by TransOral Pharmaceuticals for an unrelated project. Dr Marie Banich has been part of a MacArthur Foundation network on Adolescent Development and Juvenile Justice and was paid a consultation fee. She also receives royalties from her textbook Cognitive Neuroscience and Neuropsychology, 2nd edition, published by Houghton-Mifflin.

Figures

Figure 1

Schematic of a single taste cue trial. To control for taste detection and head movement, participants were asked, via visual instructions, to perform two cycles of ‘taste’ for 10 s with intervening ‘swallow’ prompts for 2 s during the 24-s taste delivery period. The taste delivery period is always immediately followed by a washout period wherein ‘REST’ was visually presented for 16 s. A single urge question was presented for a duration of 2 s at the end of the washout period, followed by ‘Ready?’ for 2 s as a prompt for the preceding the next trial. The taste and rest period of each taste cue (ie alcohol, control) are illustrated in addition to the explanatory variables (EVs) of no interest (ie urge question).

Figure 2

Regions of interest. The demarcation for the (a) right and left striatum ranged from x: + 30 to −30, y: + 28 to −18, z: 14 to −24; for the (b) right and left VTA/SN ranged from x: + 20 to −20, y−10 to −24, z: −6 to −22; for the (c) right and left OFC ranged from x: + 4 to + 40, −40 to −4, y: + 58 to + 14, z: +8 to −24; for the (d) right and left VMPFC ranged from x: −16 to + 16, y: + 10 to +54, z: +24 to −24. VS/DS = ventral striatum/dorsal striatum, VTA/SN = ventral tegmental area/substantia nigra, MPFC = medial prefrontal cortex, OFC = orbitofrontal cortex.

Figure 3

Greater ROI activity during alcohol vs control contrasts. All of the a priori ROIs showed significantly greater activity during alcohol taste cues compared with the control taste cues. Significance was determined at voxel-corrected p<0.05, z = 1.64; Colorscale represents Z-scores; The right side of the images represent right hemispheric activations; The maximum z-values for each ROI are given; The ROIs are: VS/DS = ventral striatum/dorsal striatum; VTA/SN = ventral tegmental area/substantia nigra; ACG/MPFC = anterior cingulate gyrus/medial prefrontal cortex; OFC = orbitofrontal cortex.

Figure 4

Areas of increased BOLD activity in response to alcohol cues as revealed by exploratory analyses. These figures illustrate widespread areas with significantly greater activity during alcohol cues compared with (a) alcohol rest and (b) control (ie litchi juice) cues during whole brain analyses. Significance was determined at FDR-corrected p < 0.05; Colorscale represents Z-scores.

Figure 5

Correlations between ROI maximum percent signal change and drinking behavior. These plots illustrate the significant associations between brain signal in response to alcohol cues (over control cues) and drinking behavior as assessed by the total AUDIT score.