Hierarchical neural architecture underlying thirst regulation

Vineet Augustine, Sertan Kutal Gokce, Sangjun Lee, Bo Wang, Thomas J. Davidson, Frank Reimann, Fiona Gribble, Karl Deisseroth, Carlos Lois and Yuki Oka ()
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Vineet Augustine: Computation and Neural Systems, California Institute of Technology
Sertan Kutal Gokce: California Institute of Technology
Sangjun Lee: California Institute of Technology
Bo Wang: California Institute of Technology
Thomas J. Davidson: University of California
Frank Reimann: University of Cambridge
Fiona Gribble: University of Cambridge
Karl Deisseroth: Howard Hughes Medical Institute, Stanford University
Carlos Lois: California Institute of Technology
Yuki Oka: Computation and Neural Systems, California Institute of Technology

Nature, 2018, vol. 555, issue 7695, 204-209

Abstract: Abstract Neural circuits for appetites are regulated by both homeostatic perturbations and ingestive behaviour. However, the circuit organization that integrates these internal and external stimuli is unclear. Here we show in mice that excitatory neural populations in the lamina terminalis form a hierarchical circuit architecture to regulate thirst. Among them, nitric oxide synthase-expressing neurons in the median preoptic nucleus (MnPO) are essential for the integration of signals from the thirst-driving neurons of the subfornical organ (SFO). Conversely, a distinct inhibitory circuit, involving MnPO GABAergic neurons that express glucagon-like peptide 1 receptor (GLP1R), is activated immediately upon drinking and monosynaptically inhibits SFO thirst neurons. These responses are induced by the ingestion of fluids but not solids, and are time-locked to the onset and offset of drinking. Furthermore, loss-of-function manipulations of GLP1R-expressing MnPO neurons lead to a polydipsic, overdrinking phenotype. These neurons therefore facilitate rapid satiety of thirst by monitoring real-time fluid ingestion. Our study reveals dynamic thirst circuits that integrate the homeostatic-instinctive requirement for fluids and the consequent drinking behaviour to maintain internal water balance.

Date: 2018
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DOI: 10.1038/nature25488

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