Regional brain responses associated with drinking water during thirst and after its satiation

Abstract

The instinct of thirst was a cardinal element in the successful colonization by vertebrates of the dry land of the planet, which began in the Ordovician period about 400 million y ago. It is a commonplace experience in humans that drinking water in response to thirst following fluid loss is a pleasant experience. However, continuing to drink water once thirst has been satiated becomes unpleasant and, eventually, quite aversive. Functional MRI experiments reported here show pleasantness of drinking is associated with activation in the anterior cingulate cortex (Brodmann area 32) and the orbitofrontal cortex. The unpleasantness and aversion of overdrinking is associated with activation in the midcingulate cortex, insula, amygdala, and periaqueductal gray. Drinking activations in the putamen and cerebellum also correlated with the unpleasantness of water, and the motor cortex showed increased activation during overdrinking compared with drinking during thirst. These activations in motor regions may possibly reflect volitional effort to conduct compliant drinking in the face of regulatory mechanisms inhibiting intake. The results suggestive of a specific inhibitory system in the control of drinking are unique.

Keywords: fMRI; swallowing.

Fig. 1.

Participants gave ratings of the pleasantness or unpleasantness of drinking 5-mL volumes of water on 10 occasions during each of four functional brain imaging scans. Drinks were rated as pleasant during the first two scans, when participants were dehydrated and thirsty. The final two scans took place after participants drank in excess of the amount required for satiation. Increasing ratings of unpleasantness were associated with drinking water during this overdrinking condition.

Fig. 2.

(A) Bilateral regions of the primary motor cortex showed increased levels of drinking-related activation during the overdrinking condition compared with the thirst condition. (B) BOLD signals measured from an activated cluster in the right motor cortex (indicated by white arrow in A) show hemodynamic responses associated with drinking during the thirst condition (closed blue squares) and during the overdrinking condition (open red triangles). Drinking events were averaged according to the timing of water placed in the mouth (time = 0 s). The signal increases associated with drinking were larger during the overdrinking condition compared with the thirst condition. *P < 0.05.

Fig. 3.

(A) Drinking-related activation in the right pACC (indicated with arrow) was related to participants’ pleasantness ratings of water during the thirst condition. (B) Data in the scattergram was collected during two functional brain imaging scans when participants were thirsty. The average percentage signal changes in the right pACC during drinking are paired with the corresponding average ratings of pleasantness for the 5-mL drinks of water for each participant to represent the level of correlation between the two parameters. (C) Variance among participants in drinking-related activation in the right OFC (arrowed) also showed an association with pleasantness ratings of drinks of water. (D) The scattergram shows the level of correlation between pleasantness ratings and drinking-related signal changes in the right OFC.

Fig. 4.

Drinking-related activations that correlated with unpleasantness ratings after overdrinking were distributed throughout the cortex and subcortical regions. (A) Variance in drinking-related activation associated with unpleasantness ratings was seen in the right SMA and MCC. (B) Unpleasantness was also associated with drinking-related activation in the left midinsula (MI), bilateral posterior insula (PI), bilateral putamen (Put), and thalamus (Th). (C) The amygdala in the left (inside circle) and right (inside square) hemispheres showed drinking-related activation that was correlated with unpleasantness ratings. (D) Drinking-related BOLD signal changes were extracted from the amygdala in the left (○) and right (■) hemispheres and plotted against participants corresponding mean unpleasantness ratings to illustrate the correlations between the two parameters.

Fig. 5.

(A) A sagittal view of the brainstem shows drinking-related activations that correlated with unpleasantness ratings after overdrinking, and indicates the location of axial slices in the remaining insets in the figure. (B) An axial slice through the rostral midbrain that shows drinking activations correlated with unpleasantness ratings in a cluster incorporating the PAG and ventral tegmental area (VTA). (C) A slice through the caudal midbrain shows a cluster near the dorsal midline likely to include the PAG and dorsal nucleus of the raphe (DNR), where unpleasantness ratings were correlated with drinking-related activation. (D) Dorsal regions of the rostral pons overlying the motor and principal sensory trigeminal nuclei (V) showed drinking-related activation associated with unpleasantness ratings. (E) An axial slice through the caudal pons showed clusters of drinking-related activation associated with unpleasantness ratings in a cluster that was likely to include the facial nuclei (VII) dorsally and pontine nuclei (PN) ventrally.