Gustatory responses in macaque monkeys revealed with fMRI: Comments on taste, taste preference, and internal state

Abstract

Studies of the neural mechanisms underlying value-based decision making typically employ food or fluid rewards to motivate subjects to perform cognitive tasks. Rewards are often treated as interchangeable, but it is well known that the specific tastes of foods and fluids and the values associated with their taste sensations influence choices and contribute to overall levels of food consumption. Accordingly, we characterized the gustatory system in three macaque monkeys (Macaca mulatta) and examined whether gustatory responses were modulated by preferences and hydration status. To identify taste-responsive cortex, we delivered small quantities (0.1 ml) of sucrose (sweet), citric acid (sour), or distilled water in random order without any predictive cues while scanning monkeys using event-related fMRI. Neural effects were evaluated by using each session in each monkey as a data point in a second-level analysis. By contrasting BOLD responses to sweet and sour tastes with those from distilled water in a group level analysis, we identified taste responses in primary gustatory cortex area G, an adjacent portion of the anterior insular cortex, and prefrontal cortex area 12o. Choice tests administered outside the scanner revealed that all three monkeys strongly preferred sucrose to citric acid or water. BOLD responses in the ventral striatum, ventral pallidum, and amygdala reflected monkeys' preferences, with greater BOLD responses to sucrose than citric acid. Finally, we examined the influence of hydration level by contrasting BOLD responses to receipt of fluids when monkeys were thirsty and after ad libitum water consumption. BOLD responses in area G and area 12o in the left hemisphere were greater following full hydration. By contrast, BOLD responses in portions of medial frontal cortex were reduced after ad libitum water consumption. These findings highlight brain regions involved in representing taste, taste preference and internal state.

Keywords: Amygdala; Motivation; Orbitofrontal cortex; Prelimbic cortex; Reward; Ventral striatum.

Figure 1.. Taste responsive areas.

A-H. Areas exhibiting greater BOLD responses to sucrose and citric acid relative to water included area 12o, area G, and an adjacent portion of the anterior insula. t-maps range from 4.3 (p = 0.001) to 7.0 (p < 1.43 × 10⁻⁵) and above (red color scale), and −4.3 (p = 0.001) to −7.0 (p < 1.43 × 10⁻⁵) and below (blue color scale); corrected FWE = 0.01. t-maps are masked with licking prior to fluid delivery. Sections A-H are taken at 1.5 mm intervals. Two distinct clusters were identified in the left insula, indicated as “Cluster 1” in panels A-D, and “Cluster 2” in panels E-H. The center of Cluster 1 is ~8 mm rostral to the anterior commissure, and is about 13 mm from the midline. The center of Cluster 2 is ~2 mm rostral to the anterior commissure, and is about 16 mm from the midline. The cluster in the insula in the right hemisphere spans 7.5 mm (Sections C-G) and is centered ~4 mm rostral to the anterior commissure; it is about 19 mm from the midline. Note the anterior commissure in Section H for reference. Area 25 exhibited greater BOLD responses to water relative to sucrose and citric acid (blue voxels). I. Time course for a cluster in the right insula and operculum, including area G, shows greater BOLD responses to sucrose and citric acid than to water. J. Time course for a cluster in MFC area 25, encroaching on the ventral striatum, shows greater BOLD responses for water than sucrose or citric acid. Time-course plots show average percent signal change for all voxels in the cluster. Error bars in I and J show +/− SEM across sessions.

Figure 2.. Ventral striatum, ventral pallidum, and amygdala encode preferred taste.

t-maps at three different thresholds are shown for the sucrose vs. citric acid contrast, revealing greater BOLD responses in the ventral striatum, ventral pallidum, and left anterior amygdala for sucrose relative to citric acid. t-maps thresholded at p = 0.01, p = 0.005 and p = 0.001, each corrected at FWE 0.01. t-maps are masked with licking prior to fluid delivery.

Figure 3.. Choice preferences and anticipatory licking.

A. Monkeys’ choice preferences from the Choice and View task for all completed choice trials. Each bar represents the percent chosen across three days for each possible pairing of fluid types: sucrose vs. water, sucrose vs. citric acid, and citric acid vs. water (see legend in B). For each bar, the fraction of color segment indicates the percent chosen. All three monkeys chose cues signaling delivery of sucrose over those signaling water (all ps < 0.001). All three monkeys also chose cues signaling delivery of sucrose over those signaling delivery of citric acid (all ps < 0.001). Monkey 1 preferred water over citric acid (p = 0.015) and Monkey 2 preferred citric acid to water (p = 3.02 ×10⁻⁶), while Monkey 3 showed no preference (p = 0.457). B. Monkeys’ anticipatory licking from the Choice and View task for all completed View trials. Licking was evaluated between cue onset (t = 0) and the earliest fluid delivery time. Bars depict the mean (+/− 1 SEM) lick area under the curve (AUC) for each fluid type, for each day. Monkey 1 exhibited no significantly different licking cues associated with delivery of sucrose, citric acid, or water. Monkey 2 showed significantly greater licking in anticipation of sucrose over water on day one (p = 0. 026). Monkey 3 licked more in anticipation of sucrose than water (p = 0.024) or citric acid (p = 0.018) on day three. Asterisks denote significance as follows: p < 0.001 sig = ***, p < 0.01, sig = **; p < 0.05, sig = *. The legend shown in panel B applies to the entire figure.

Figure 4.. Taste responsive areas affected by hydration.

A-F. Of identified taste responsive areas, only area 12o and area G in the left hemisphere show responses modulated by hydration level. These regions exhibited greater BOLD responses following full hydration (pre minus post hydration contrast maps shown). There was no interaction between fluid type and hydration (not shown). z-maps range from −3.29 (p = 0.001) to −7.0 (p < × 2.56 × 10⁻¹²); corrected FWE = 0.01. Sections A-F are taken at 1.5 mm intervals. G-H. Mean BOLD time courses for all fluid types before and after monkeys were given ad libitum water. G. Time course for a cluster in area G, area 12o and anterior insula shows BOLD responses significantly modulated by the hydration manipulation (hydrated > thirsty). H. Time course for a cluster of taste-responsive voxels in the right hemisphere does not show significant effects of hydration. Error bars in G and H show +/− SEM across sessions. Compare and contrast with Figure 1.

Figure 5.. Brain areas affected by hydration: regions outside taste-responsive areas.

Additional areas exhibiting BOLD responses modulated by changes in hydration level included area 32/10m, a small region of cortex near the rostral extent of the ventral bank of the cingulate sulcus, area 46v, anterodorsal striatum, and 12r in the right hemisphere. These regions exhibited greater BOLD responses prior to full hydration (thirsty > hydrated). z-maps range from 3.29 (p = 0.001) to 7.0 (p < × 2.56 × 10⁻¹²) and above; corrected FWE = 0.01.