A preliminary study of the human brain response to oral sucrose and its association with recent drinking

Abstract

Background: A preference for sweet tastes has been repeatedly shown to be associated with alcohol preference in both animals and humans. In this study, we tested the extent to which recent drinking is related to blood oxygen level-dependent (BOLD) activation from an intensely sweet solution in orbitofrontal areas known to respond to primary rewards.

Methods: Sixteen right-handed, non-treatment-seeking, healthy volunteers (mean age: 26 years; 75% male) were recruited from the community. All underwent a taste test using a range of sucrose concentrations, as well as functional magnetic resonance imaging (fMRI) during pseudorandom, event-driven stimulation with water and a 0.83 M concentration of sucrose in water.

Results: [Sucrose > water] provoked a significant BOLD activation in primary gustatory cortex and amygdala, as well as in the right ventral striatum and in bilateral orbitofrontal cortex. Drinks/drinking day correlated significantly with the activation as extracted from the left orbital area (r = 0.52, p = 0.04 after correcting for a bilateral comparison). Using stepwise multiple regression, the addition of rated sucrose liking accounted for significantly more variance in drinks/drinking day than did left orbital activation alone (multiple R = 0.79, p = 0.002).

Conclusions: Both the orbitofrontal response to an intensely sweet taste and rated liking of that taste accounted for significant variance in drinking behavior. The brain response to sweet tastes may be an important phenotype of alcoholism risk.

Keywords: Alcoholism; Ethanol; Flavor; Gustation; Neuroimaging; Sucrose; Taste.

Figure 1

Diagram of events (not to temporal scale), with text prompts in quotation marks indicating visual cues shown to subjects. A 3 sec visually displayed “Ready” text prompt alerted subjects to the impending 1 sec liquid spray, which was also accompanied by a text prompt (“Spray”). A subsequent 1 sec water purge followed immediately and contiguously to purge the volume of the spray nozzle. A variable 1–3 sec blank interval ensued (hatched area), followed by a 1 sec “Swallow” prompt. A variable 4–8 sec interval (during which a fixation cross appeared) separated the trials. Total trial length was 11 – 17 sec.

Figure 2

Perceived intensity and liking of the sweet solutions as a function of sucrose molar concentration. Error bars = standard errors.

Figure 3

BOLD activation from the [Sucrose > Water] contrast. (1) Coronal slice (y=−4 mm) showing activation in the bilateral insula/“area G” (green circles), dorsal amygdala (blue box), and peri-Rolandic cortex (green ovals, in this slice corresponding to the prefrontal gyrus). (b) Bilateral orbitofrontal (y = 30 mm) activation (blue circles). (c) Axial view (z=−20 mm) of activation in the orbital and amygdala areas. Display, p < 0.005, k > 10. Color bar indicates t-statistic.

Figure 4

(Top) Brain image shows responding cluster, as extracted from each subject, at a voxel-wise threshold of p < 0.01, uncorrected. (Bottom) Scatter plot of the correlation between [Sucrose > Water] BOLD contrast in the extracted left orbital area (as depicted in top image) and drinks/drinking day from the Timeline Followback interview (r = 0.52, p= 0.02; p = 0.04 corrected for the bilateral comparison).