A neural basis for tonic suppression of sodium appetite.
Amygdala
/ cytology
Animals
Appetite
/ physiology
Brachial Plexus
/ physiology
Feeding Behavior
Glutamates
/ physiology
Homeostasis
Hypovolemia
/ psychology
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
Patch-Clamp Techniques
Receptor, Serotonin, 5-HT2C
/ genetics
Serotonergic Neurons
/ physiology
Sodium
/ metabolism
Sodium, Dietary
Journal
Nature neuroscience
ISSN: 1546-1726
Titre abrégé: Nat Neurosci
Pays: United States
ID NLM: 9809671
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
16
03
2018
accepted:
09
12
2019
pubmed:
22
1
2020
medline:
14
4
2020
entrez:
22
1
2020
Statut:
ppublish
Résumé
Sodium appetite is a powerful form of motivation that can drive ingestion of high, yet aversive concentrations of sodium in animals that are depleted of sodium. However, in normal conditions, sodium appetite is suppressed to prevent homeostatic deviations. Although molecular and neural mechanisms underlying the stimulation of sodium appetite have received much attention recently, mechanisms that inhibit sodium appetite remain largely obscure. Here we report that serotonin 2c receptor (Htr2c)-expressing neurons in the lateral parabrachial nucleus (LPBN
Identifiants
pubmed: 31959933
doi: 10.1038/s41593-019-0573-2
pii: 10.1038/s41593-019-0573-2
pmc: PMC7065971
mid: NIHMS1546061
doi:
Substances chimiques
5-hydroxytryptamine2C receptor, mouse
0
Glutamates
0
Receptor, Serotonin, 5-HT2C
0
Sodium, Dietary
0
Sodium
9NEZ333N27
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
423-432Subventions
Organisme : American Heart Association-American Stroke Association
ID : 16SDG27260001
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK100699
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK114036
Pays : United States
Références
Wagman, W. Sodium chloride deprivation: development of sodium chloride as a reinforcement. Science 140, 1403–1404 (1963).
doi: 10.1126/science.140.3574.1403
Matsuda, T.et al. Distinct neural mechanisms for the control of thirst and salt appetite in the subfornical organ. Nat. Neurosci. 20, 230–241 (2017).
pubmed: 27991901
Jarvie, B. C. & Palmiter, R. D. HSD2 neurons in the hindbrain drive sodium appetite. Nat. Neurosci. 20, 167–169 (2017).
doi: 10.1038/nn.4451
Resch, J. M. et al. Aldosterone-sensing neurons in the NTS exhibit state-dependent pacemaker activity and drive sodium appetite via synergy with angiotensin II signaling. Neuron 96, 190–206 (2017).
doi: 10.1016/j.neuron.2017.09.014
Oka, Y., Butnaru, M., von Buchholtz, L., Ryba, N. J. & Zuker, C. S. High salt recruits aversive taste pathways. Nature 494, 472–475 (2013).
doi: 10.1038/nature11905
de Oliveira, L. B., Callera, J. C., De Luca, L. A. Jr, Colombari, D. S. & Menani, J. V. GABAergic mechanisms of the lateral parabrachial nucleus on sodium appetite. Brain Res. Bull. 73, 238–247 (2007).
doi: 10.1016/j.brainresbull.2007.03.006
De Gobbi, J. I. et al. Non-NMDA receptors in the lateral parabrachial nucleus modulate sodium appetite. Brain Res. 1301, 44–51 (2009).
doi: 10.1016/j.brainres.2009.08.094
Johnson, A. K. & Thunhorst, R. L. The neuroendocrinology of thirst and salt appetite: visceral sensory signals and mechanisms of central integration. Front. Neuroendocrinol. 18, 292–353 (1997).
doi: 10.1006/frne.1997.0153
Scalera, G., Spector, A. C. & Norgren, R. Excitotoxic lesions of the parabrachial nuclei prevent conditioned taste aversions and sodium appetite in rats. Behav. Neurosci. 109, 997–1008 (1995).
doi: 10.1037/0735-7044.109.5.997
Geerling, J. C. et al. FoxP2 expression defines dorsolateral pontine neurons activated by sodium deprivation. Brain Res. 1375, 19–27 (2011).
doi: 10.1016/j.brainres.2010.11.028
Castro, L. et al. Central 5-HT
doi: 10.1016/S0006-8993(03)03015-4
Gentili, L., Saija, A., Luchetti, G. & Massi, M. Effect of the 5-HT
doi: 10.1016/0091-3057(91)90417-Z
Menani, J. V., Thunhorst, R. L. & Johnson, A. K. Lateral parabrachial nucleus and serotonergic mechanisms in the control of salt appetite in rats. Am. J. Physiol. 270, R162–R168 (1996).
pubmed: 8769798
De Gobbi, J. I. et al. 5-HT
Yamamoto, T. et al. c-Fos expression in the parabrachial nucleus after ingestion of sodium chloride in the rat. Neuroreport 4, 1223–1226 (1993).
doi: 10.1097/00001756-199309000-00003
Geerling, J. C. & Loewy, A. D. Sodium deprivation and salt intake activate separate neuronal subpopulations in the nucleus of the solitary tract and the parabrachial complex. J. Comp. Neurol. 504, 379–403 (2007).
doi: 10.1002/cne.21452
Ryan, P. J., Ross, S. I., Campos, C. A., Derkach, V. A. & Palmiter, R. D. Oxytocin-receptor-expressing neurons in the parabrachial nucleus regulate fluid intake. Nat. Neurosci. 20, 1722–1733 (2017).
doi: 10.1038/s41593-017-0014-z
Donnelly, M. L. et al. Analysis of the aphthovirus 2A/2B polyprotein ‘cleavage’ mechanism indicates not a proteolytic reaction, but a novel translational effect: a putative ribosomal ‘skip’. J. Gen. Virol. 82, 1013–1025 (2001).
doi: 10.1099/0022-1317-82-5-1013
Carter, M. E., Soden, M. E., Zweifel, L. S. & Palmiter, R. D. Genetic identification of a neural circuit that suppresses appetite. Nature 503, 111–114 (2013).
doi: 10.1038/nature12596
Campos, C. A. et al. Cancer-induced anorexia and malaise are mediated by CGRP neurons in the parabrachial nucleus. Nat. Neurosci. 20, 934–942 (2017).
doi: 10.1038/nn.4574
Campos, C. A., Bowen, A. J., Schwartz, M. W. & Palmiter, R. D. Parabrachial CGRP neurons control meal termination. Cell Metab. 23, 811–820 (2016).
doi: 10.1016/j.cmet.2016.04.006
Garfield, A. S. et al. A neural basis for melanocortin-4 receptor-regulated appetite. Nat. Neurosci. 18, 863–871 (2015).
doi: 10.1038/nn.4011
Stricker, E. M. & Verbalis, J. G. Central inhibitory control of sodium appetite in rats: correlation with pituitary oxytocin secretion. Behav. Neurosci. 101, 560 (1987).
doi: 10.1037/0735-7044.101.4.560
Geerling, J. C., Chimenti, P. C. & Loewy, A. D. Phox2b expression in the aldosterone-sensitive HSD2 neurons of the NTS. Brain Res. 1226, 82–88 (2008).
doi: 10.1016/j.brainres.2008.05.072
Kang, B. J. et al. Central nervous system distribution of the transcription factor Phox2b in the adult rat. J. Comp. Neurol. 503, 627–641 (2007).
doi: 10.1002/cne.21409
Hashimoto, K., Obata, K. & Ogawa, H. Characterization of parabrachial subnuclei in mice with regard to salt tastants: possible independence of taste relay from visceral processing. Chem. Senses 34, 253–267 (2009).
doi: 10.1093/chemse/bjn085
Biondolillo, J. W., Williams, L. A. & King, M. S. Blocking glutamate receptors in the waist area of the parabrachial nucleus decreases taste reactivity behaviors in conscious rats. Chem. Senses 34, 221–230 (2009).
doi: 10.1093/chemse/bjn081
Chandrashekar, J. et al. The cells and peripheral representation of sodium taste in mice. Nature 464, 297–301 (2010).
doi: 10.1038/nature08783
Zardetto-Smith, A. M., Beltz, T. G. & Johnson, A. K. Role of the central nucleus of the amygdala and bed nucleus of the stria terminalis in experimentally-induced salt appetite. Brain Res. 645, 123–134 (1994).
doi: 10.1016/0006-8993(94)91645-4
Galaverna, O., De Luca, L. A. Jr, Schulkin, J., Yao, S. Z. & Epstein, A. N. Deficits in NaCl ingestion after damage to the central nucleus of the amygdala in the rat. Brain Res. Bull. 28, 89–98 (1992).
doi: 10.1016/0361-9230(92)90234-O
Dong, H. W., Petrovich, G. D. & Swanson, L. W. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res. Rev. 38, 192–246 (2001).
doi: 10.1016/S0165-0173(01)00079-0
Dong, H. W., Petrovich, G. D., Watts, A. G. & Swanson, L. W. Basic organization of projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis in adult rat brain. J. Comp. Neurol. 436, 430–455 (2001).
doi: 10.1002/cne.1079
Lee, S. et al. Chemosensory modulation of neural circuits for sodium appetite. Nature 568, 93–97 (2019).
doi: 10.1038/s41586-019-1053-2
Chen, Y., Baez, M. & Yu, L. Functional coupling of the 5-HT
doi: 10.1016/0304-3940(94)90944-X
Lucaites, V. L., Nelson, D. L., Wainscott, D. B. & Baez, M. Receptor subtype and density determine the coupling repertoire of the 5-HT
doi: 10.1016/0024-3205(96)00423-7
Kurachi, Y., Tung, R. T., Ito, H. & Nakajima, T. G protein activation of cardiac muscarinic K
doi: 10.1016/0301-0082(92)90017-9
Petrov, T., Krukoff, T. L. & Jhamandas, J. H. The hypothalamic paraventricular and lateral parabrachial nuclei receive collaterals from raphe nucleus neurons: a combined double retrograde and immunocytochemical study. J. Comp. Neurol. 318, 18–26 (1992).
doi: 10.1002/cne.903180103
Bang, S. J., Jensen, P., Dymecki, S. M. & Commons, K. G. Projections and interconnections of genetically defined serotonin neurons in mice. Eur. J. Neurosci. 35, 85–96 (2012).
doi: 10.1111/j.1460-9568.2011.07936.x
Smits, J. F., van Essen, H. & Struyker-Boudier, H. A. Serotonin-mediated cardiovascular responses to electrical stimulation of the raphe nuclei in the rat. Life Sci. 23, 173–178 (1978).
doi: 10.1016/0024-3205(78)90267-9
Berglund, E. D. et al. Serotonin 2C receptors in pro-opiomelanocortin neurons regulate energy and glucose homeostasis. J. Clin. Invest. 123, 5061–5070 (2013).
doi: 10.1172/JCI70338