Overdrinking, swallowing inhibition, and regional brain responses prior to swallowing

Abstract

In humans, drinking replenishes fluid loss and satiates the sensation of thirst that accompanies dehydration. Typically, the volume of water drunk in response to thirst matches the deficit. Exactly how this accurate metering is achieved is unknown; recent evidence implicates swallowing inhibition as a potential factor. Using fMRI, this study investigated whether swallowing inhibition is present after more water has been drunk than is necessary to restore fluid balance within the body. This proposal was tested using ratings of swallowing effort and measuring regional brain responses as participants prepared to swallow small volumes of liquid while they were thirsty and after they had overdrunk. Effort ratings provided unequivocal support for swallowing inhibition, with a threefold increase in effort after overdrinking, whereas addition of 8% (wt/vol) sucrose to water had minimal effect on effort before or after overdrinking. Regional brain responses when participants prepared to swallow showed increases in the motor cortex, prefrontal cortices, posterior parietal cortex, striatum, and thalamus after overdrinking, relative to thirst. Ratings of swallowing effort were correlated with activity in the right prefrontal cortex and pontine regions in the brainstem; no brain regions showed correlated activity with pleasantness ratings. These findings are all consistent with the presence of swallowing inhibition after excess water has been drunk. We conclude that swallowing inhibition is an important mechanism in the overall regulation of fluid intake in humans.thirst | drinking | swallowing | inhibition | fMRI F luid depletion leads to drinking, an important evolutionary behavior that satisfies the physiological need to replenish lost fluid. The motivation to begin drinking is normally provided, in humans at least, by the presence of a subjective state of thirst. At some point after drinking has commenced, the sensation of thirst disappears and is replaced by the experience of satiation, along with the cessation of drinking. Studies performed in humans and animals indicate the regulatory mechanisms that have evolved to govern the cessation of drinking appear to be tightly calibrated, with the amount of fluid ingested commensurate with the degree of fluid depletion, even though some variation occurs between species regarding the time taken to conclude drinking (1-3).Several factors have been implicated in the regulation of fluid intake, with the majority relating to thirst and the initiation of drinking. These include signals produced by osmoreceptors in the lamina terminalis (4-6), which respond to cellular dehydration and the resulting increase in sodium concentration within the cerebral spinal fluid (2), and signals produced in response to extracellular dehydration, such as those associated with the renin-angiotensin system, which is activated as a result of changes in vascular pressure and volume (7,8). In comparison, the mechanisms responsible for terminating drinking are less well understood. Oropharyngeal metering ...

Influence of anterior midcingulate cortex on drinking behavior during thirst and following satiation

“…In these studies, decreases in aMCC activity due to progressive intake of water during a state of thirst have been shown to correlate with decreases in ratings of thirst ( 26 ) and pleasantness ( 26 , 27 ). In addition, swallowing is experienced as unpleasant ( 27 , 28 ) and becomes more difficult ( 28 ) if drinking continues after satiation. These findings are consistent with the human aMCC processing dynamic changes in incentive value relating to fluid ingestion ( 26 ).…”

“…To explicitly investigate whether activity in the aMCC is associated with drinking responses during a state of thirst, we analyzed data from one of our earlier fMRI studies ( 28 ) in which participants were scanned while drinking during a thirsty condition and during an “oversated” condition produced by excess compliant drinking. In each condition, participants held 5-mL volumes of liquid in their mouths before swallowing and subsequently rating how pleasant the liquid tasted, along with the effort required to swallow it.…”

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

“…In contrast to homeostatic thirst, non-homeostatic thirst ( Figure 3) is influenced by the taste and temperature of a fluid (i.e., alliesthesia [102,103]), mouth dryness, gastric distention, meal contents, meal timing [105], idiosyncratic learned, preferences, occupational schedules, social interactions, and cultural norms [75,98]. Both physiologists and cognitive neuroscientists have recognized that dehydrated humans drink to satiation rapidly across 3-10 min [74,106], causing decreased thirst and motivation to drink, well before elevated plasma osmolality and sodium return to normal concentrations (i.e., a process that may require 15-50 min [107][108][109], and before the consumed fluid is absorbed from the gut [110][111][112]. Thus, human homeostatic thirst is modulated by non-homeostatic oropharyngeal neural signals which rapidly reduce and limit total fluid intake in the presence of a persistent, strong motivation to drink [107]; these signals modulate satiety and oppose over-drinking [113].…”

“…Previous research has implicated these regions in discomfort and aversion [75]. Subsequently, this research group conducted experiments involving ratings of swallowing effort and regional brain imaging [109], as participants prepared to swallow small volumes of liquid while they were thirsty and after they had overdrunk. After overdrinking, regional brain activations occurred in the motor cortex, prefrontal cortices, posterior parietal cortex, striatum, and thalamus when participants prepared to swallow.…”

“…Effort ratings provided unequivocal support for swallowing inhibition, with a threefold increase in effort after overdrinking; these effort ratings were correlated with activations in the right prefrontal cortex and pontine regions of the brainstem. The authors concluded that swallowing inhibition in humans likely is a "hard-wired" process which helps the body to avoid the detrimental effects of overdrinking that could result in water intoxication and/or death [109]. Although not widely appreciated, both the aversive motivational drive and swallowing inhibition are part of the complex, dynamic regulation of fluid-electrolyte balance.…”