Delay discounting and alcohol consumption correlate with dorsal anterior insula activation during choice in nontreatment-seeking heavy drinkers

Abstract

Background: The anterior insular cortex (AIC), a prominent salience network node, integrates interoceptive information and emotional states into decision making. While AIC activation during delay discounting (DD) in alcohol use disorder (AUD) has been previously reported, the associations between AIC activation, impulsive choice, alcohol consumption, and connectivity remain unknown. We therefore tested AIC brain responses during DD in heavy drinkers and their association with DD performance, alcohol drinking, and task-based connectivity.

Methods: Twenty-nine heavy drinkers (12 females; mean (SD) age=31.5 ± 6.1 years; mean (SD)=40.8 ± 23.4 drinks/week) completed a DD task during functional MRI. Regions activated during DD decision making were tested for correlation with DD behavior and alcohol drinking. Psychophysiological interaction (PPI) models assessed the task-dependent functional connectivity (FC) of activation during choice.

Results: Delay discounting choice activated bilateral anterior insular cortex, anterior cingulate cortex, and left precentral gyrus. Right dorsal (d) AIC activation during choice negatively correlated withdiscounting of delayed rewards and alcohol consumption. PPI analysis revealed FC of the right dAIC to both the anterior and posterior cingulate cortices-key nodes in the midline default mode network.

Conclusions: Greater dAIC involvement in intertemporal choice may confer more adaptive behavior (lower impulsivity and alcohol consumption). Moreover, salience network processes governing discounting may require midline default mode (precuneus/posterior cingulate cortex) recruitment. These findings supporta key adaptive role for right dAIC in decision making involving future rewards and risky drinking.

Keywords: alcohol use disorder; alcoholism; monetary discounting; psychophysiological interaction; task fMRI.

FIGURE 1

Intertemporal choice regions. Choice trials relative to baseline elicited activation in the left and right dorsal anterior insula (panels A, B), the dorsal anterior cingulate cortex (panels B, C), and left precentral gyrus (panel C). Illustrated activation foci contain significant peak voxels (p _FWE < 0.05, corrected for whole‐brain multiple comparisons), displayed as a p‐value heat map, k > 15

FIGURE 2

Dorsal anterior insula activation correlations with behavior. (A) Mean [Choice > Control] contrast values in the right dorsal anterior insula cortex (dAIC) cluster were positively associated with greater delayed reward preference during the pre‐MRI DD and (B, C) negatively with alcohol consumption. Right dAIC cluster (yellow) is depicted in the middle panel inset. p.e., parameter estimate

FIGURE 3

Psychophysiological interaction analysis. Illustration of connectivity clusters including significant peak voxels. (A) The right dorsal anterior insula seed (yellow) showed stimulus‐dependent functional connectivity with precuneus/PCC (green) and pregenual ACC/medial prefrontal (blue) in [Choice > Control], and (B) precuneus/PCC alone in the [Choice > Baseline] comparison. Correction for multiple comparisons within a (C) medial default mode mask (45,074 mm³, red) was performed using a small volume correction. Peak voxel p _FWE < 0.05; display threshold, p < 0.001, uncorrected. FWE, family‐wise error corrected

FIGURE 4

Discounting and drinking. Greater discounting was associated with higher alcohol consumption as illustrated by the negative correlation between DD (pre‐MRI) discounting and (A) drinks consumed per drinking day and (B) per week