Limits...
Thirst driving and suppressing signals encoded by distinct neural populations in the brain.

Oka Y, Ye M, Zuker CS - Nature (2015)

Bottom Line: The light-induced response is highly specific for water, immediate and strictly locked to the laser stimulus.In contrast, activation of a second population of subfornical organ neurons, marked by expression of the vesicular GABA transporter VGAT, drastically suppresses drinking, even in water-craving thirsty animals.These results reveal an innate brain circuit that can turn an animal's water-drinking behaviour on and off, and probably functions as a centre for thirst control in the mammalian brain.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Biochemistry and Molecular Biophysics, Columbia College of Physicians and Surgeons, Howard Hughes Medical Institute, Columbia University, New York, New York 10032, USA [2] Department of Neuroscience, Columbia College of Physicians and Surgeons, Howard Hughes Medical Institute, Columbia University, New York, New York 10032, USA.

ABSTRACT
Thirst is the basic instinct to drink water. Previously, it was shown that neurons in several circumventricular organs of the hypothalamus are activated by thirst-inducing conditions. Here we identify two distinct, genetically separable neural populations in the subfornical organ that trigger or suppress thirst. We show that optogenetic activation of subfornical organ excitatory neurons, marked by the expression of the transcription factor ETV-1, evokes intense drinking behaviour, and does so even in fully water-satiated animals. The light-induced response is highly specific for water, immediate and strictly locked to the laser stimulus. In contrast, activation of a second population of subfornical organ neurons, marked by expression of the vesicular GABA transporter VGAT, drastically suppresses drinking, even in water-craving thirsty animals. These results reveal an innate brain circuit that can turn an animal's water-drinking behaviour on and off, and probably functions as a centre for thirst control in the mammalian brain.

Show MeSH

Related in: MedlinePlus

CamKII-positive SFO neurons mediate thirstActivation of CamKII-positive neurons in the SFO drives selective drinking of water. (a) Representative raster plots illustrating licking events during a 5 s window in the presence of photostimulation; the open arrowhead indicates the first lick in each trial. The right panel shows quantification of similar data for multiple animals (n=6 for honey, and 7 for others; Mann Whitney P < 0.002); all animals were water-satiated. (b) Photostimulated animals did not drink water in the presence of a bitter compound (3 μM cycloheximide; paired t test, P < 0.0001), or high concentration of salt (300 mM; paired t test, P < 0.001), but did so in the presence of a sweet compound (30 mM sucrose), or low salt (60 mM); data were normalized to the number of licks to water alone. Values are means ± s.e.m (n=5 animals)
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4401619&req=5

Figure 2: CamKII-positive SFO neurons mediate thirstActivation of CamKII-positive neurons in the SFO drives selective drinking of water. (a) Representative raster plots illustrating licking events during a 5 s window in the presence of photostimulation; the open arrowhead indicates the first lick in each trial. The right panel shows quantification of similar data for multiple animals (n=6 for honey, and 7 for others; Mann Whitney P < 0.002); all animals were water-satiated. (b) Photostimulated animals did not drink water in the presence of a bitter compound (3 μM cycloheximide; paired t test, P < 0.0001), or high concentration of salt (300 mM; paired t test, P < 0.001), but did so in the presence of a sweet compound (30 mM sucrose), or low salt (60 mM); data were normalized to the number of licks to water alone. Values are means ± s.e.m (n=5 animals)

Mentions: Next, we asked whether the light-induced “thirst” is selective for water. Therefore, we assessed light-dependent fluid intake using a range of test solutions. Our results (Figures 2a) show that the effect is highly specific for water, with no responses to other fluids such as mineral oil, glycerol, PEG, or even honey. Notably, light-stimulated animals refused to drink water if it contained either a bitter compound or high concentrations of salt, demonstrating that photoactivation of these SFO neurons does not bypass the natural taste-mediated functions that prevent ingestion of toxic, noxious chemicals 17,18 (Figure 2b).


Thirst driving and suppressing signals encoded by distinct neural populations in the brain.

Oka Y, Ye M, Zuker CS - Nature (2015)

CamKII-positive SFO neurons mediate thirstActivation of CamKII-positive neurons in the SFO drives selective drinking of water. (a) Representative raster plots illustrating licking events during a 5 s window in the presence of photostimulation; the open arrowhead indicates the first lick in each trial. The right panel shows quantification of similar data for multiple animals (n=6 for honey, and 7 for others; Mann Whitney P < 0.002); all animals were water-satiated. (b) Photostimulated animals did not drink water in the presence of a bitter compound (3 μM cycloheximide; paired t test, P < 0.0001), or high concentration of salt (300 mM; paired t test, P < 0.001), but did so in the presence of a sweet compound (30 mM sucrose), or low salt (60 mM); data were normalized to the number of licks to water alone. Values are means ± s.e.m (n=5 animals)
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4401619&req=5

Figure 2: CamKII-positive SFO neurons mediate thirstActivation of CamKII-positive neurons in the SFO drives selective drinking of water. (a) Representative raster plots illustrating licking events during a 5 s window in the presence of photostimulation; the open arrowhead indicates the first lick in each trial. The right panel shows quantification of similar data for multiple animals (n=6 for honey, and 7 for others; Mann Whitney P < 0.002); all animals were water-satiated. (b) Photostimulated animals did not drink water in the presence of a bitter compound (3 μM cycloheximide; paired t test, P < 0.0001), or high concentration of salt (300 mM; paired t test, P < 0.001), but did so in the presence of a sweet compound (30 mM sucrose), or low salt (60 mM); data were normalized to the number of licks to water alone. Values are means ± s.e.m (n=5 animals)
Mentions: Next, we asked whether the light-induced “thirst” is selective for water. Therefore, we assessed light-dependent fluid intake using a range of test solutions. Our results (Figures 2a) show that the effect is highly specific for water, with no responses to other fluids such as mineral oil, glycerol, PEG, or even honey. Notably, light-stimulated animals refused to drink water if it contained either a bitter compound or high concentrations of salt, demonstrating that photoactivation of these SFO neurons does not bypass the natural taste-mediated functions that prevent ingestion of toxic, noxious chemicals 17,18 (Figure 2b).

Bottom Line: The light-induced response is highly specific for water, immediate and strictly locked to the laser stimulus.In contrast, activation of a second population of subfornical organ neurons, marked by expression of the vesicular GABA transporter VGAT, drastically suppresses drinking, even in water-craving thirsty animals.These results reveal an innate brain circuit that can turn an animal's water-drinking behaviour on and off, and probably functions as a centre for thirst control in the mammalian brain.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Biochemistry and Molecular Biophysics, Columbia College of Physicians and Surgeons, Howard Hughes Medical Institute, Columbia University, New York, New York 10032, USA [2] Department of Neuroscience, Columbia College of Physicians and Surgeons, Howard Hughes Medical Institute, Columbia University, New York, New York 10032, USA.

ABSTRACT
Thirst is the basic instinct to drink water. Previously, it was shown that neurons in several circumventricular organs of the hypothalamus are activated by thirst-inducing conditions. Here we identify two distinct, genetically separable neural populations in the subfornical organ that trigger or suppress thirst. We show that optogenetic activation of subfornical organ excitatory neurons, marked by the expression of the transcription factor ETV-1, evokes intense drinking behaviour, and does so even in fully water-satiated animals. The light-induced response is highly specific for water, immediate and strictly locked to the laser stimulus. In contrast, activation of a second population of subfornical organ neurons, marked by expression of the vesicular GABA transporter VGAT, drastically suppresses drinking, even in water-craving thirsty animals. These results reveal an innate brain circuit that can turn an animal's water-drinking behaviour on and off, and probably functions as a centre for thirst control in the mammalian brain.

Show MeSH
Related in: MedlinePlus