Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamus

Autores
Pérez Gómez, Anabel; Bleymehl, Katherin; Stein, Benjamin; Pyrski, Martina; Birnbaumer, Lutz; Munger, Steven D.; Leinders Zufall, Trese; Zufall, Frank; Chamero, Pablo
Año de publicación
2015
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The existence of innate predator aversion evoked by predator-derived chemostimuli called kairomones offers a strong selective advantage for potential prey animals. However, it is unclear how chemically diverse kairomones can elicit similar avoidance behaviors. Using a combination of behavioral analyses and single-cell Ca2+ imaging in wild-type and gene-targeted mice, we show that innate predator-evoked avoidance is driven by parallel, non-redundant processing of volatile and nonvolatile kairomones through the activation of multiple olfactory subsystems including the Grueneberg ganglion, the vomeronasal organ, and chemosensory neurons within the main olfactory epithelium. Perturbation of chemosensory responses in specific subsystems through disruption of genes encoding key sensory transduction proteins (Cnga3, Gnao1) or by surgical axotomy abolished avoidance behaviors and/or cellular Ca2+ responses to different predator odors. Stimulation of these different subsystems resulted in the activation of widely distributed target regions in the olfactory bulb, as assessed by c-Fos expression. However, in each case, this c-Fos increase was observed within the same subnuclei of the medial amygdala and ventromedial hypothalamus, regions implicated in fear, anxiety, and defensive behaviors. Thus, the mammalian olfactory system has evolved multiple, parallel mechanisms for kairomone detection that converge in the brain to facilitate a common behavioral response. Our findings provide significant insights into the genetic substrates and circuit logic of predator-driven innate aversion and may serve as a valuable model for studying instinctive fear [1] and human emotional and panic disorders [2, 3].
Fil: Pérez Gómez, Anabel. Universitat Saarland; Alemania
Fil: Bleymehl, Katherin. Universitat Saarland; Alemania
Fil: Stein, Benjamin. Universitat Saarland; Alemania
Fil: Pyrski, Martina. Universitat Saarland; Alemania
Fil: Birnbaumer, Lutz. National Institute of Environmental Health Sciences; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Munger, Steven D.. University of Florida; Estados Unidos
Fil: Leinders Zufall, Trese. Universitat Saarland; Alemania
Fil: Zufall, Frank. Universitat Saarland; Alemania
Fil: Chamero, Pablo. Universitat Saarland; Alemania
Materia
Odor Aversion
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:11336/39686
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/39686
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamusPérez Gómez, AnabelBleymehl, KatherinStein, BenjaminPyrski, MartinaBirnbaumer, LutzMunger, Steven D.Leinders Zufall, TreseZufall, FrankChamero, PabloOdor Aversionhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The existence of innate predator aversion evoked by predator-derived chemostimuli called kairomones offers a strong selective advantage for potential prey animals. However, it is unclear how chemically diverse kairomones can elicit similar avoidance behaviors. Using a combination of behavioral analyses and single-cell Ca2+ imaging in wild-type and gene-targeted mice, we show that innate predator-evoked avoidance is driven by parallel, non-redundant processing of volatile and nonvolatile kairomones through the activation of multiple olfactory subsystems including the Grueneberg ganglion, the vomeronasal organ, and chemosensory neurons within the main olfactory epithelium. Perturbation of chemosensory responses in specific subsystems through disruption of genes encoding key sensory transduction proteins (Cnga3, Gnao1) or by surgical axotomy abolished avoidance behaviors and/or cellular Ca2+ responses to different predator odors. Stimulation of these different subsystems resulted in the activation of widely distributed target regions in the olfactory bulb, as assessed by c-Fos expression. However, in each case, this c-Fos increase was observed within the same subnuclei of the medial amygdala and ventromedial hypothalamus, regions implicated in fear, anxiety, and defensive behaviors. Thus, the mammalian olfactory system has evolved multiple, parallel mechanisms for kairomone detection that converge in the brain to facilitate a common behavioral response. Our findings provide significant insights into the genetic substrates and circuit logic of predator-driven innate aversion and may serve as a valuable model for studying instinctive fear [1] and human emotional and panic disorders [2, 3].Fil: Pérez Gómez, Anabel. Universitat Saarland; AlemaniaFil: Bleymehl, Katherin. Universitat Saarland; AlemaniaFil: Stein, Benjamin. Universitat Saarland; AlemaniaFil: Pyrski, Martina. Universitat Saarland; AlemaniaFil: Birnbaumer, Lutz. National Institute of Environmental Health Sciences; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas; ArgentinaFil: Munger, Steven D.. University of Florida; Estados UnidosFil: Leinders Zufall, Trese. Universitat Saarland; AlemaniaFil: Zufall, Frank. Universitat Saarland; AlemaniaFil: Chamero, Pablo. Universitat Saarland; AlemaniaCell Press2015-05info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/39686Pérez Gómez, Anabel; Bleymehl, Katherin; Stein, Benjamin; Pyrski, Martina; Birnbaumer, Lutz; et al.; Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamus; Cell Press; Current Biology; 25; 10; 5-2015; 1340-13460960-9822CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1016/j.cub.2015.03.026info:eu-repo/semantics/altIdentifier/url/http://www.cell.com/current-biology/fulltext/S0960-9822(15)00341-3info:eu-repo/semantics/altIdentifier/url/https://www.sciencedirect.com/science/article/pii/S0960982215003413info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T10:02:47Zoai:ri.conicet.gov.ar:11336/39686instacron: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 10:02:48.001CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamus
title Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamus
spellingShingle Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamus
Pérez Gómez, Anabel
Odor Aversion
title_short Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamus
title_full Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamus
title_fullStr Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamus
title_full_unstemmed Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamus
title_sort Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamus
dc.creator.none.fl_str_mv Pérez Gómez, Anabel
Bleymehl, Katherin
Stein, Benjamin
Pyrski, Martina
Birnbaumer, Lutz
Munger, Steven D.
Leinders Zufall, Trese
Zufall, Frank
Chamero, Pablo
author Pérez Gómez, Anabel
author_facet Pérez Gómez, Anabel
Bleymehl, Katherin
Stein, Benjamin
Pyrski, Martina
Birnbaumer, Lutz
Munger, Steven D.
Leinders Zufall, Trese
Zufall, Frank
Chamero, Pablo
author_role author
author2 Bleymehl, Katherin
Stein, Benjamin
Pyrski, Martina
Birnbaumer, Lutz
Munger, Steven D.
Leinders Zufall, Trese
Zufall, Frank
Chamero, Pablo
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Odor Aversion
topic Odor Aversion
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The existence of innate predator aversion evoked by predator-derived chemostimuli called kairomones offers a strong selective advantage for potential prey animals. However, it is unclear how chemically diverse kairomones can elicit similar avoidance behaviors. Using a combination of behavioral analyses and single-cell Ca2+ imaging in wild-type and gene-targeted mice, we show that innate predator-evoked avoidance is driven by parallel, non-redundant processing of volatile and nonvolatile kairomones through the activation of multiple olfactory subsystems including the Grueneberg ganglion, the vomeronasal organ, and chemosensory neurons within the main olfactory epithelium. Perturbation of chemosensory responses in specific subsystems through disruption of genes encoding key sensory transduction proteins (Cnga3, Gnao1) or by surgical axotomy abolished avoidance behaviors and/or cellular Ca2+ responses to different predator odors. Stimulation of these different subsystems resulted in the activation of widely distributed target regions in the olfactory bulb, as assessed by c-Fos expression. However, in each case, this c-Fos increase was observed within the same subnuclei of the medial amygdala and ventromedial hypothalamus, regions implicated in fear, anxiety, and defensive behaviors. Thus, the mammalian olfactory system has evolved multiple, parallel mechanisms for kairomone detection that converge in the brain to facilitate a common behavioral response. Our findings provide significant insights into the genetic substrates and circuit logic of predator-driven innate aversion and may serve as a valuable model for studying instinctive fear [1] and human emotional and panic disorders [2, 3].
Fil: Pérez Gómez, Anabel. Universitat Saarland; Alemania
Fil: Bleymehl, Katherin. Universitat Saarland; Alemania
Fil: Stein, Benjamin. Universitat Saarland; Alemania
Fil: Pyrski, Martina. Universitat Saarland; Alemania
Fil: Birnbaumer, Lutz. National Institute of Environmental Health Sciences; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Munger, Steven D.. University of Florida; Estados Unidos
Fil: Leinders Zufall, Trese. Universitat Saarland; Alemania
Fil: Zufall, Frank. Universitat Saarland; Alemania
Fil: Chamero, Pablo. Universitat Saarland; Alemania
description The existence of innate predator aversion evoked by predator-derived chemostimuli called kairomones offers a strong selective advantage for potential prey animals. However, it is unclear how chemically diverse kairomones can elicit similar avoidance behaviors. Using a combination of behavioral analyses and single-cell Ca2+ imaging in wild-type and gene-targeted mice, we show that innate predator-evoked avoidance is driven by parallel, non-redundant processing of volatile and nonvolatile kairomones through the activation of multiple olfactory subsystems including the Grueneberg ganglion, the vomeronasal organ, and chemosensory neurons within the main olfactory epithelium. Perturbation of chemosensory responses in specific subsystems through disruption of genes encoding key sensory transduction proteins (Cnga3, Gnao1) or by surgical axotomy abolished avoidance behaviors and/or cellular Ca2+ responses to different predator odors. Stimulation of these different subsystems resulted in the activation of widely distributed target regions in the olfactory bulb, as assessed by c-Fos expression. However, in each case, this c-Fos increase was observed within the same subnuclei of the medial amygdala and ventromedial hypothalamus, regions implicated in fear, anxiety, and defensive behaviors. Thus, the mammalian olfactory system has evolved multiple, parallel mechanisms for kairomone detection that converge in the brain to facilitate a common behavioral response. Our findings provide significant insights into the genetic substrates and circuit logic of predator-driven innate aversion and may serve as a valuable model for studying instinctive fear [1] and human emotional and panic disorders [2, 3].
publishDate 2015
dc.date.none.fl_str_mv 2015-05
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/11336/39686
Pérez Gómez, Anabel; Bleymehl, Katherin; Stein, Benjamin; Pyrski, Martina; Birnbaumer, Lutz; et al.; Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamus; Cell Press; Current Biology; 25; 10; 5-2015; 1340-1346
0960-9822
CONICET Digital
CONICET
url http://hdl.handle.net/11336/39686
identifier_str_mv Pérez Gómez, Anabel; Bleymehl, Katherin; Stein, Benjamin; Pyrski, Martina; Birnbaumer, Lutz; et al.; Innate predator odor aversion driven by parallel olfactory subsystems that converge in the ventromedial hypothalamus; Cell Press; Current Biology; 25; 10; 5-2015; 1340-1346
0960-9822
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1016/j.cub.2015.03.026
info:eu-repo/semantics/altIdentifier/url/http://www.cell.com/current-biology/fulltext/S0960-9822(15)00341-3
info:eu-repo/semantics/altIdentifier/url/https://www.sciencedirect.com/science/article/pii/S0960982215003413
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 Cell Press
publisher.none.fl_str_mv Cell Press
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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score 13.13397

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