From Thirst to Satiety: The Anterior Mid-Cingulate Cortex and Right Posterior Insula Indicate Dynamic Changes in Incentive Value

Abstract

The cingulate cortex and insula are among the neural structures whose activations have been modulated in functional imaging studies examining discrete states of thirst and drinking to satiation. Building upon these findings, the present study aimed to identify neural structures that change their pattern of activation elicited by water held in the mouth in relation to the internal body state, i.e., proportional to continuous water consumption. Accordingly, participants in a thirsty state were scanned while receiving increments of water until satiety was reached. As expected, fluid ingestion led to a clear decrease in self-reported thirst and the pleasantness ratings of the water ingested. Furthermore, linear decreases in the blood oxygenation level dependent (BOLD) response to water ingestion were observed in the anterior mid-cingulate cortex (aMCC) and right posterior insula as participants shifted towards the non-thirsty state. In addition, regions in the superior temporal gyrus (STG), supplementary motor area (SMA), superior parietal lobule (SPL), precuneus and calcarine sulcus also showed a linear decrease with increasing fluid consumption. Further analyses related single trial BOLD responses of associated regions to trial-by-trial ratings of thirst and pleasantness. Overall, the aMCC and posterior insula may be key sites of a neural network representing the motivation for drinking based on the dynamic integration of internal state and external stimuli.

Keywords: deprivation; drinking; fMRI; moment-to-moment; motivation.

Figure 1

Schematic representation and timing of a trial. Each trial lasted for 23 s and was followed by a variable inter-trial interval (ITI) of 2–5 s. Abbreviations: S, signal cue; T, thirst rating; P, stimulus pleasantness rating.

Figure 2

Illustration of the intra-task thirst ratings (mean ± SEM). Each time bin represents an interval of 10 trials, i.e., the ingestion of 100 ml of water.

Figure 3

Brain sections and extracted percent signal changes (PSC; mean ± SEM) illustrating the modulation in blood oxygenation level dependent (BOLD) activity in (A) the anterior mid-cingulate cortex (aMCC) and (B) posterior insula proportional to the amount of water ingested. Statistical maps are thresholded with a cluster-defining voxel-level threshold of p < 0.001 (uncorrected) and a cluster-level threshold of p < 0.05 (FWE-corrected). Abbreviations: aMCC, anterior mid-cingulate cortex; pInsula, posterior insula.

Figure 4

Brain sections and extracted PSC (mean ± SEM) illustrating the modulation in BOLD activity in (A) the supplementary motor cortex (SMA)/PreCG, (B) superior parietal lobule/intra-parietal sulcus (SPL/IPS) and (C) the Precun/Paracentr proportional to the amount of water ingested. Statistical maps are thresholded with a cluster-defining voxel-level threshold of p < 0.001 (uncorrected) and a cluster-level threshold of p < 0.05 (FWE-corrected). Abbreviations: SMA, supplementary motor cortex; PreCG, pre-central gyrus; SPL, superior parietal lobule; IPS, intra-parietal sulcus; Precun, precuneus; Paracentr, paracentral lobule.

Figure 5

Scatterplots showing the relationship between single trial PSC and corresponding thirst ratings in (A) the aMCC and (B) posterior insula. Abbreviations: aMCC, anterior mid-cingulate cortex; pInsula, posterior insula.

Figure 6

Bar graphs showing the PSC in (A) the aMCC and (B) posterior insula during the pleasantness rating period as a function of time bins. Abbreviations: aMCC, anterior mid-cingulate cortex; pInsula, posterior insula.