Hunger- and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestion

Autores
González Segarra, Amanda J.; Barcelos Pontes, Gina; Jourjine, Nicholas; Del Toro, Alexander; Scott, Kristin
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Consumption of food and water is tightly regulated by the nervous system to maintain internal nutrient homeostasis. Although generally considered independently, interactions between hunger and thirst drives are important to coordinate competing needs. In Drosophila, four neurons called the interoceptive subesophageal zone neurons (ISNs) respond to intrinsic hunger and thirst signals to oppositely regulate sucrose and water ingestion. Here, we investigate the neural circuit downstream of the ISNs to examine how ingestion is regulated based on internal needs. Utilizing the recently available fly brain connectome, we find that the ISNs synapse with a novel cell-type bilateral T-shaped neuron (BiT) that projects to neuroendocrine centers. In vivo neural manipulations revealed that BiT oppositely regulates sugar and water ingestion. Neuroendocrine cells downstream of ISNs include several peptide-releasing and peptide-sensing neurons, including insulin producing cells (IPCs), crustacean cardioactive peptide (CCAP) neurons, and CCHamide-2 receptor isoform RA (CCHa2R-RA) neurons. These neurons contribute differentially to ingestion of sugar and water, with IPCs and CCAP neurons oppositely regulating sugar and water ingestion, and CCHa2R-RA neurons modulating only water ingestion. Thus, the decision to consume sugar or water occurs via regulation of a broad peptidergic network that integrates internal signals of nutritional state to generate nutrient-specific ingestion.
Fil: González Segarra, Amanda J.. University of California at Berkeley; Estados Unidos
Fil: Barcelos Pontes, Gina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Biodiversidad y Biología Experimental y Aplicada. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biodiversidad y Biología Experimental y Aplicada; Argentina
Fil: Jourjine, Nicholas. University of California at Berkeley; Estados Unidos
Fil: Del Toro, Alexander. University of California at Berkeley; Estados Unidos
Fil: Scott, Kristin. University of California at Berkeley; Estados Unidos
Materia
DROSOPHILA
TASTE
NEURAL CIRCUIT
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/228175

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spelling Hunger- and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestionGonzález Segarra, Amanda J.Barcelos Pontes, GinaJourjine, NicholasDel Toro, AlexanderScott, KristinDROSOPHILATASTENEURAL CIRCUIThttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Consumption of food and water is tightly regulated by the nervous system to maintain internal nutrient homeostasis. Although generally considered independently, interactions between hunger and thirst drives are important to coordinate competing needs. In Drosophila, four neurons called the interoceptive subesophageal zone neurons (ISNs) respond to intrinsic hunger and thirst signals to oppositely regulate sucrose and water ingestion. Here, we investigate the neural circuit downstream of the ISNs to examine how ingestion is regulated based on internal needs. Utilizing the recently available fly brain connectome, we find that the ISNs synapse with a novel cell-type bilateral T-shaped neuron (BiT) that projects to neuroendocrine centers. In vivo neural manipulations revealed that BiT oppositely regulates sugar and water ingestion. Neuroendocrine cells downstream of ISNs include several peptide-releasing and peptide-sensing neurons, including insulin producing cells (IPCs), crustacean cardioactive peptide (CCAP) neurons, and CCHamide-2 receptor isoform RA (CCHa2R-RA) neurons. These neurons contribute differentially to ingestion of sugar and water, with IPCs and CCAP neurons oppositely regulating sugar and water ingestion, and CCHa2R-RA neurons modulating only water ingestion. Thus, the decision to consume sugar or water occurs via regulation of a broad peptidergic network that integrates internal signals of nutritional state to generate nutrient-specific ingestion.Fil: González Segarra, Amanda J.. University of California at Berkeley; Estados UnidosFil: Barcelos Pontes, Gina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Biodiversidad y Biología Experimental y Aplicada. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biodiversidad y Biología Experimental y Aplicada; ArgentinaFil: Jourjine, Nicholas. University of California at Berkeley; Estados UnidosFil: Del Toro, Alexander. University of California at Berkeley; Estados UnidosFil: Scott, Kristin. University of California at Berkeley; Estados UnidoseLife Sciences Publications2023-09info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/228175González Segarra, Amanda J.; Barcelos Pontes, Gina; Jourjine, Nicholas; Del Toro, Alexander; Scott, Kristin; Hunger- and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestion; eLife Sciences Publications; eLife; 12; 9-2023; 1-242050-084XCONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://elifesciences.org/articles/88143info:eu-repo/semantics/altIdentifier/doi/10.7554/eLife.88143.3info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:49:53Zoai:ri.conicet.gov.ar:11336/228175instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 09:49:54.574CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Hunger- and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestion
title Hunger- and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestion
spellingShingle Hunger- and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestion
González Segarra, Amanda J.
DROSOPHILA
TASTE
NEURAL CIRCUIT
title_short Hunger- and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestion
title_full Hunger- and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestion
title_fullStr Hunger- and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestion
title_full_unstemmed Hunger- and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestion
title_sort Hunger- and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestion
dc.creator.none.fl_str_mv González Segarra, Amanda J.
Barcelos Pontes, Gina
Jourjine, Nicholas
Del Toro, Alexander
Scott, Kristin
author González Segarra, Amanda J.
author_facet González Segarra, Amanda J.
Barcelos Pontes, Gina
Jourjine, Nicholas
Del Toro, Alexander
Scott, Kristin
author_role author
author2 Barcelos Pontes, Gina
Jourjine, Nicholas
Del Toro, Alexander
Scott, Kristin
author2_role author
author
author
author
dc.subject.none.fl_str_mv DROSOPHILA
TASTE
NEURAL CIRCUIT
topic DROSOPHILA
TASTE
NEURAL CIRCUIT
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Consumption of food and water is tightly regulated by the nervous system to maintain internal nutrient homeostasis. Although generally considered independently, interactions between hunger and thirst drives are important to coordinate competing needs. In Drosophila, four neurons called the interoceptive subesophageal zone neurons (ISNs) respond to intrinsic hunger and thirst signals to oppositely regulate sucrose and water ingestion. Here, we investigate the neural circuit downstream of the ISNs to examine how ingestion is regulated based on internal needs. Utilizing the recently available fly brain connectome, we find that the ISNs synapse with a novel cell-type bilateral T-shaped neuron (BiT) that projects to neuroendocrine centers. In vivo neural manipulations revealed that BiT oppositely regulates sugar and water ingestion. Neuroendocrine cells downstream of ISNs include several peptide-releasing and peptide-sensing neurons, including insulin producing cells (IPCs), crustacean cardioactive peptide (CCAP) neurons, and CCHamide-2 receptor isoform RA (CCHa2R-RA) neurons. These neurons contribute differentially to ingestion of sugar and water, with IPCs and CCAP neurons oppositely regulating sugar and water ingestion, and CCHa2R-RA neurons modulating only water ingestion. Thus, the decision to consume sugar or water occurs via regulation of a broad peptidergic network that integrates internal signals of nutritional state to generate nutrient-specific ingestion.
Fil: González Segarra, Amanda J.. University of California at Berkeley; Estados Unidos
Fil: Barcelos Pontes, Gina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Biodiversidad y Biología Experimental y Aplicada. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biodiversidad y Biología Experimental y Aplicada; Argentina
Fil: Jourjine, Nicholas. University of California at Berkeley; Estados Unidos
Fil: Del Toro, Alexander. University of California at Berkeley; Estados Unidos
Fil: Scott, Kristin. University of California at Berkeley; Estados Unidos
description Consumption of food and water is tightly regulated by the nervous system to maintain internal nutrient homeostasis. Although generally considered independently, interactions between hunger and thirst drives are important to coordinate competing needs. In Drosophila, four neurons called the interoceptive subesophageal zone neurons (ISNs) respond to intrinsic hunger and thirst signals to oppositely regulate sucrose and water ingestion. Here, we investigate the neural circuit downstream of the ISNs to examine how ingestion is regulated based on internal needs. Utilizing the recently available fly brain connectome, we find that the ISNs synapse with a novel cell-type bilateral T-shaped neuron (BiT) that projects to neuroendocrine centers. In vivo neural manipulations revealed that BiT oppositely regulates sugar and water ingestion. Neuroendocrine cells downstream of ISNs include several peptide-releasing and peptide-sensing neurons, including insulin producing cells (IPCs), crustacean cardioactive peptide (CCAP) neurons, and CCHamide-2 receptor isoform RA (CCHa2R-RA) neurons. These neurons contribute differentially to ingestion of sugar and water, with IPCs and CCAP neurons oppositely regulating sugar and water ingestion, and CCHa2R-RA neurons modulating only water ingestion. Thus, the decision to consume sugar or water occurs via regulation of a broad peptidergic network that integrates internal signals of nutritional state to generate nutrient-specific ingestion.
publishDate 2023
dc.date.none.fl_str_mv 2023-09
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/228175
González Segarra, Amanda J.; Barcelos Pontes, Gina; Jourjine, Nicholas; Del Toro, Alexander; Scott, Kristin; Hunger- and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestion; eLife Sciences Publications; eLife; 12; 9-2023; 1-24
2050-084X
CONICET Digital
CONICET
url http://hdl.handle.net/11336/228175
identifier_str_mv González Segarra, Amanda J.; Barcelos Pontes, Gina; Jourjine, Nicholas; Del Toro, Alexander; Scott, Kristin; Hunger- and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestion; eLife Sciences Publications; eLife; 12; 9-2023; 1-24
2050-084X
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://elifesciences.org/articles/88143
info:eu-repo/semantics/altIdentifier/doi/10.7554/eLife.88143.3
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv eLife Sciences Publications
publisher.none.fl_str_mv eLife Sciences Publications
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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