Correlation of regional cerebral blood flow and change of plasma sodium concentration during genesis and satiation of thirst

Denton, Derek A.; Shade, Robert E.; Zamarippa, Frank; Egan, Gary F.; Blair‐West, J. R.; Fox, Peter T.

doi:10.1073/pnas.96.5.2532

Cited by 95 publications

(80 citation statements)

References 31 publications

(26 reference statements)

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“…Previous reports from this group have identified activations associated with thirst (13,14,26) and plasma Na (27) in two regions of the cingulate cortex: the pACC and the aMCC (summarized graphically in ref. 28).…”

Section: Discussionmentioning

confidence: 99%

Effect of aging on regional cerebral blood flow responses associated with osmotic thirst and its satiation by water drinking: A PET study

Farrell

Zamarripa

Shade

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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Levels of thirst and ad libitum drinking decrease with advancing age, making older people vulnerable to dehydration. This study investigated age-related changes in brain responses to thirst and drinking in healthy men. Thirst was induced with hypertonic infusions (3.1 ml/kg 0.51M NaCl) in young (Y) and older (O) subjects. Regional cerebral blood flow (rCBF) was measured with positron emission tomography (PET). Thirst activations were identified by correlating rCBF with thirst ratings. Average rCBF was measured from regions of interest (ROI) corresponding to activation clusters in each group. The effects of drinking were examined by correlating volume of water drunk with changes in ROI rCBF from maximum thirst to postdrinking. There were increases in blood osmolality (Y, 2.8 ؎ 1.8%; O, 2.2 ؎ 1.4%) and thirst ratings (Y, 3.1 ؎ 2.1; O, 3.7 ؎ 2.8) from baseline to the end of the hypertonic infusion. Older subjects drank less water (1.9 ؎ 1.6 ml/kg) than younger subjects (3.9 ؎ 1.9 ml/kg). Thirst-related activation was evident in S1/M1, prefrontal cortex, anterior midcingulate cortex (aMCC), premotor cortex, and superior temporal gyrus in both groups. Postdrinking changes of rCBF in the aMCC correlated with drinking volumes in both groups. There was a greater reduction in aMCC rCBF relative to water drunk in the older group. Aging is associated with changes in satiation that militate against adequate hydration in response to hyperosmolarity, although it is unclear whether these alterations are due to changes in primary afferent inflow or higher cortical functioning.cingulate cortex ͉ positron emission tomography U nder usual ambient conditions, volumes of water sufficient to maintain fluid balance are consumed in the routine of regular meals (1, 2). Heat or vigorous activity may cause dehydration, resulting in thirst and the desire to drink. Aging alters thirst and drinking responses, making older people vulnerable to body fluid imbalance (3). This study compared the pattern of brain responses in younger and older men during the development and the satiation of thirst. The aim of the study was to assess the role of cortical and subcortical processes in agerelated changes of thirst and drinking.There are two major physiological changes that cause the onset of thirst; increased blood/CSF osmolality and decreased volume of extracellular fluid. Studies differ on the effects of aging on the relations among blood tonicity, blood volume, and thirst. Increase of blood osmolality through the systemic infusion of hypertonic solutions has been reported to demonstrate either no age-related change in thirst ratings (4, 5) or decreased thirst responses in older men (6). Head-out water immersion drives water into the intrathoracic cavity, leads to increased blood volume and cardiac filling pressure in both young and older subjects, and has been used to assess the effects of blood volume changes on thirst ratings. Head-out immersion leads to a decrease in thirst in young subjects, but does not change thirst ratings in older subjects...

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Section: Discussionmentioning

confidence: 99%

Effect of aging on regional cerebral blood flow responses associated with osmotic thirst and its satiation by water drinking: A PET study

Farrell

Zamarripa

Shade

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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“…24 We ,5,6 and others 25,26 have observed activation of the insula in response to hunger and the sight of food in hungry people. Thus, analogous to the activation of this region in response to a variety of other cravings, [27][28][29] the increase in neural activity in the middle The change in regional cerebral blood flow (rCBF) is expressed in counts per voxel per minute (mean7s.e.m. and [range]).…”

Section: Discussionmentioning

confidence: 99%

Persistence of abnormal neural responses to a meal in postobese individuals

DelParigi¹,

Chen

Salbe³

et al. 2003

Int J Obes

165

131

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OBJECTIVE:To determine whether abnormal obese-like neural responses to a meal persist in postobese individuals, who achieved and maintained a normal body weight despite a past history of severe obesity. DESIGN AND SUBJECTS: Cross-sectional study of the brain's response to tasting and consuming a satiating meal in 11 postobese (age: 4076 y, body mass index (BMI): 23.671.9 kg/m 2 ), 23 obese (age: 2976 y, BMI: 39.673.8 kg/m 2 ) and 21 lean (age: 3379 y, BMI: 22.872.1 kg/m 2 ) subjects. MEASUREMENTS: Regional cerebral blood flow (rCBF, a marker of neural activity) at baseline (after a 36-h fast), after tasting and after consuming a satiating liquid meal was assessed using positron emission tomography and state-dependent changes (taste-baseline; satiation-baseline), and compared across groups. Subjective ratings of hunger and fullness were measured by a visual analogue scale and body fatness by dual-energy X-ray absorptiometry. RESULTS: In response to tasting the liquid meal, changes in rCBF were different in the obese as compared to the lean individuals (Po0.05, corrected for multiple comparisons) in the middle insula (peak voxel, x ¼ À41, y ¼ 1, z ¼ 8; Montreal Neurological Institute coordinates) and posterior cingulate cortex (peak voxel, x ¼ 17, y ¼ À47, z ¼ 40). The middle insular cortex exhibited a similar increase of neural activity in the obese and postobese subjects, whereas in the lean subjects the regional activity did not change. In the posterior cingulate cortex, the changes in rCBF in the postobese subjects were not different from those in the other groups. In response to a satiating amount of the same liquid meal, changes in rCBF were different in the obese as compared to the lean individuals (Po0.05, corrected for multiple comparisons) in the posterior hippocampus (peak voxel, x ¼ 21, y ¼ À45, x ¼ 4), posterior cingulate cortex (peak voxel, x ¼ 17, y ¼ À47, z ¼ 40), and amygdala (peak voxel, x ¼ 27, y ¼ 1, z ¼ À24). The posterior hippocampus exhibited a similar decrease of neural activity in the obese and postobese subjects, whereas in the lean subjects the regional activity increased. In the posterior cingulate cortex and amygdala, the changes in rCBF were not different between the postobese and lean individuals. None of the changes in neural activity were correlated with the age of the individuals, the subjective ratings of hunger and fullness, or the meal induced-changes in plasma glucose, insulin, or serum free fatty acids. CONCLUSION: Persistence of abnormal neural responses to a meal in the postobese individuals, a group at high risk for relapse, indicates that a predisposition to obesity may involve areas of the brain that control complex aspects of eating behavior including anticipation and reward, chemosensory perception, and autonomic control of digestion (insular cortex), as well as enteroception and learning/memory (hippocampus).

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“…A statistical parametric map of the pain response was generated by contrasting noxious pressure (scans 2, 4, 9, and 10) with no pressure (scans 1, 3, 8, and 11). A maximum thirst statistical parametric map was generated by contrasting the baseline (scans 1-4) with maximum thirst (scans [8][9][10][11]. Interactions between pain and maximum thirst were tested by contrasting concurrent pain and thirst (scans 9 and 10) with maximum thirst (scans 8 and 11) and pain (scans 2 and 4) in isolation.…”

Section: Discussionmentioning

confidence: 99%

“…Studies of thirst-related brain activity have identified a network including the hypothalamus, thalamus, insula, parahippocampus, somatosensory cortex, anterior cingulate, posterior cingulate, and cerebellum (1,(10)(11)(12). A metaanalysis of pain imaging studies revealed a consistent network incorporating activity in the diencephalon and posterior parietal, insula, and limbic cortices and cerebellum (13).…”

mentioning

confidence: 99%

Unique, common, and interacting cortical correlates of thirst and pain

Farrell

Egan

Zamarripa

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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This study used positron-emission tomography to establish the patterns of brain activity involved in the isolated and concurrent experiences of thirst and pain. Ten subjects were scanned while experiencing pain evoked with noxious pressure, while experiencing thirst after the infusion of hypertonic saline, and while experiencing pain when thirsty. After the onset of thirst, noxious pressure evoked more intense sensations of pain. Noxious pressure did not change subjective ratings of thirst. Thirst caused activation in the anterior cingulate (Brodmann area 32) and the insula. Enhanced pain responses were associated with increased activity in cortical regions that are known to correlate with pain intensity, and also with unique activity in the pregenual anterior cingulate and ventral orbitofrontal cortex. These findings suggest a role for limbic and prefrontal cortices in the modulation of pain during the experience of thirst.interoception ͉ neuroimaging S ensations determined by interoceptors guide behaviors that maintain homeostasis. Experiences such as thirst, hunger, pain, and temperature sensation reflect imbalances of the internal state and have important implications for survival (1, 2). Interoceptive sensations can occur in tandem and create conflicts that are not resolved by a single behavior. Prevailing circumstances determine which internal imbalance requires the most urgent attention. Interoception would be more consistent with survival if competing sensations were modified to reflect relative priorities. To investigate competing interoceptive sensations, we measured brain activity during painful pressure and thirst, both in isolation and occurring concurrently.Changes in sensations determined by interoceptors in response to changing environmental circumstances can be described as context-dependent responses (3). Both appetitive and aversive drives shape the state of an organism, and these drives must be reconciled to make the most adaptive behavioral choice. The juxtaposition of pain and thirst is particularly suited to the investigation of human brain activity associated with contextdependent changes in responses to competing drives. Both pain and thirst can be manipulated in a time frame compatible with imaging protocols, the former being particularly amenable to rapid onset and offset. There is evidence that the respective sensations are modified by contextual factors, although pain and thirst have yet to be examined contemporaneously. Finally, the concurrence of conditions likely to stimulate osmoreceptors and nociceptors would conceivably be associated with conflicting implications for behavioral responses. Drinking can be deferred without detrimental effect, but ultimately thirst must be sated to avoid desiccation. The acute onset of pain has more immediate implications for tissue integrity than the early experience of thirst. For example, during mild to moderate thirst, withdrawal from noxious stimuli would be more likely if thirst is decreased and͞or pain is increased. Furthermore, the opposit...

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Correlation of regional cerebral blood flow and change of plasma sodium concentration during genesis and satiation of thirst

Cited by 95 publications

References 31 publications

Effect of aging on regional cerebral blood flow responses associated with osmotic thirst and its satiation by water drinking: A PET study

Effect of aging on regional cerebral blood flow responses associated with osmotic thirst and its satiation by water drinking: A PET study

Persistence of abnormal neural responses to a meal in postobese individuals

Unique, common, and interacting cortical correlates of thirst and pain

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