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

Pascal Saker, Michael J. Farrell, Faiz R. M. Adib, Gary F. Egan, Michael J. McKinley, and Derek A. Denton
PNAS published ahead of print March 24, 2014 https://doi.org/10.1073/pnas.1403382111
Pascal Saker
aFlorey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, VIC 3010, Australia;
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Michael J. Farrell
aFlorey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, VIC 3010, Australia;bDepartment of Anatomy and Neuroscience,
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  • For correspondence: michael.farrell@florey.edu.auddenton@unimelb.edu.au
Faiz R. M. Adib
aFlorey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, VIC 3010, Australia;
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Gary F. Egan
bDepartment of Anatomy and Neuroscience,cMonash Biomedical Imaging, Monash University, Clayton, VIC 3800, Australia; and
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Michael J. McKinley
aFlorey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, VIC 3010, Australia;dDepartment of Physiology,
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Derek A. Denton
aFlorey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, VIC 3010, Australia;eOffice of the Dean, Faculty of Medicine, Dentistry, and Health Sciences,fBaker IDI Heart and Diabetes Institute, Melbourne, VIC 3004, Australia
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  • For correspondence: michael.farrell@florey.edu.auddenton@unimelb.edu.au
  1. Contributed by Derek A. Denton, February 24, 2014 (sent for review November 15, 2013)

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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.

  • fMRI
  • swallowing

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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Drinking control
Pascal Saker, Michael J. Farrell, Faiz R. M. Adib, Gary F. Egan, Michael J. McKinley, Derek A. Denton
Proceedings of the National Academy of Sciences Mar 2014, 201403382; DOI: 10.1073/pnas.1403382111

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Drinking control
Pascal Saker, Michael J. Farrell, Faiz R. M. Adib, Gary F. Egan, Michael J. McKinley, Derek A. Denton
Proceedings of the National Academy of Sciences Mar 2014, 201403382; DOI: 10.1073/pnas.1403382111
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