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Review
. 2019 Nov 22;11(12):2864.
doi: 10.3390/nu11122864.

Thirst and Drinking Paradigms: Evolution from Single Factor Effects to Brainwide Dynamic Networks

Lawrence E Armstrong  1 , Stavros A Kavouras  2
Affiliations
Review

Thirst and Drinking Paradigms: Evolution from Single Factor Effects to Brainwide Dynamic Networks

Lawrence E Armstrong et al. Nutrients. .

Abstract

The motivation to seek and consume water is an essential component of human fluid-electrolyte homeostasis, optimal function, and health. This review describes the evolution of concepts regarding thirst and drinking behavior, made possible by magnetic resonance imaging, animal models, and novel laboratory techniques. The earliest thirst paradigms focused on single factors such as dry mouth and loss of water from tissues. By the end of the 19th century, physiologists proposed a thirst center in the brain that was verified in animals 60 years later. During the early- and mid-1900s, the influences of gastric distention, neuroendocrine responses, circulatory properties (i.e., blood pressure, volume, concentration), and the distinct effects of intracellular dehydration and extracellular hypovolemia were recognized. The majority of these studies relied on animal models and laboratory methods such as microinjection or lesioning/oblation of specific brain loci. Following a quarter century (1994-2019) of human brain imaging, current research focuses on networks of networks, with thirst and satiety conceived as hemispheric waves of neuronal activations that traverse the brain in milliseconds. Novel technologies such as chemogenetics, optogenetics, and neuropixel microelectrode arrays reveal the dynamic complexity of human thirst, as well as the roles of motivation and learning in drinking behavior.

Keywords: dehydration; magnetic resonance imaging; motivation; neural network; vasopressin.

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Conflict of interest statement

L.E.A. is a Board of Trustees member and occasional consultant for the Drinking Water Research Foundation, Alexandria, VA, USA, and serves as an occasional consultant to Danone Research, France. L.E.A. is the Managing Member of Hydration & Nutrition, LLC, Newport News, VA, USA. S.A.K. is a scientific consultant and has active research grants with Standard Process, Inc., Kannapolis, NC, USA and Danone Research, France.

Figures

Figure 1
Figure 1
The thirst drive and motivation to seek/consume water are vital aspects of the homeostatic regulation of total body water volume and tonicity, in response to intracellular dehydration, increased plasma osmolality, decreased plasma volume, decreased blood pressure, and extracellular hypovolemia. Abbreviation: Na+, sodium.
Figure 2
Figure 2
Homeostatic normalization of intracellular hydration, plasma osmolality, blood pressure, and extracellular volume (i.e., due to water and food intake), which result from a persistent, strong motivation to drink. These responses result in reduced thirst and decreased motivation to seek/consume water.
Figure 3
Figure 3
Factors that influence thirst are categorized as either homeostatic (i.e., volume, pressure, concentration) or relatively rapid non-homeostatic (anticipatory) inputs. Solid and dashed arrows represent, respectively, factors that increase and decrease thirst. Abbreviations: NaCl, sodium chloride; Posm, plasma osmolality; Ang II, angiotensin II.
Figure 4
Figure 4
Idealistic drawing of human brain loci (dark shading) which have been associated with thirst, tongue movement, touching the tongue, swallowing, and taste (Table 2, Table 4 and Table 5). Three ridges (gyri) on the cerebral cortex surface are shaded lightly. The dashed region represents the insular cortex (IC) which lies deep within the lateral surface of the brain. Brain loci abbreviations are defined in the Table 2 footnote.
Figure 5
Figure 5
Rodent brain loci that have been associated (2016–2019) with dehydration-induced drinking [82,90,91,92,94,113,151]. In this idealistic illustration, arrows denote evidence-based neural circuits that integrate intracellular or extracellular signals and modulate thirst, drinking, rapid satiety, overdrinking, and aversive motivational drives. Abbreviations: IC, insular cortex (insula); SFO, subfornical organ; PVT, paraventricular thalamic nucleus; PP, posterior pituitary; additional brain loci are defined in the text and Table 2 footnote.
Figure 6
Figure 6
(A) Tracks of neuropixel electrode activations, recorded in mouse forebrain and midbrain regions during head-fixed, thirst-motivated choice behavior. (B) Brainwide activity dynamics of individual neurons from 31 brain loci, in response to an olfactory cue, while a mouse was both thirsty and sated. Reproduced with the permission of the publisher [94].
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