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Contributed by Derek A. Denton, February 24, 2014 (sent for review November 15, 2013)
Significance
Drinking water in response to thirst following fluid loss is a pleasant experience, whereas drinking water after thirst has been satiated is unpleasant. The pleasantness of drinking when thirsty is associated with activation in the anterior cingulate cortex and orbitofrontal region. The unpleasantness and aversion of overdrinking is associated with activations in the midcingulate cortex, insula, amygdala, and periaqueductal grey. Activations in the putamen and cerebellum, and also in the motor cortex, possibly reflect volitional effort to conduct compliant drinking in the face of mechanisms inhibiting intake. These regions may contribute to the termination of drinking. Overdrinking with hyponatraemia and cerebral edema can occur in schizophrenia, reflecting that this brain disorder can derange physiological mechanisms regulating water balance.
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.
Footnotes
- ↵1To whom correspondence may be addressed. E-mail: michael.farrell{at}florey.edu.au or ddenton{at}unimelb.edu.au.
Author contributions: P.S., M.J.F., G.F.E., M.J.M., and D.A.D. designed research; P.S., M.J.F., and F.R.M.A. performed research; P.S., M.J.F., and F.R.M.A. analyzed data; and P.S., M.J.F., G.F.E., M.J.M., and D.A.D. wrote the paper.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1403382111/-/DCSupplemental.
Freely available online through the PNAS open access option.
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