Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation

Autores
Lowet, Eric; Sheehan, Daniel J.; Chialva, Ulises; De Oliveira Pena, Rodrigo; Mount, Rebecca A.; Xiao, Sheng; Zhou, Samuel L.; Tseng, Hua-an; Gritton, Howard; Shroff, Sanaya; Kondabolu, Krishnakanth; Cheung, Cyrus; Wang, Yangyang; Piatkevich, Kiryl D.; Boyden, Edward S.; Mertz, Jerome; Hasselmo, Michael E.; Rotstein, Horacio; Han, Xue
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Hippocampal CA1 neurons generate single spikes and stereotyped bursts of spikes. However, it is unclear how individual neurons dynamically switch between these output modes and whether these two spiking outputs relay distinct information. We performed extracellular recordings in spatially navigating rats and cellular voltage imaging and optogenetics in awake mice. We found that spike bursts are preferentially linked to cellular and network theta rhythms (3–12 Hz) and encode an animal's position via theta phase precession, particularly as animals are entering a place field. In contrast, single spikes exhibit additional coupling to gamma rhythms (30–100 Hz), particularly as animals leave a place field. Biophysical modeling suggests that intracellular properties alone are sufficient to explain the observed input frequency-dependent spike coding. Thus, hippocampal neurons regulate the generation of bursts and single spikes according to frequency-specific network and intracellular dynamics, suggesting that these spiking modes perform distinct computations to support spatial behavior.
Fil: Lowet, Eric. Boston University; Estados Unidos
Fil: Sheehan, Daniel J.. Boston University; Estados Unidos
Fil: Chialva, Ulises. Universidad Nacional del Sur. Departamento de Matemática; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Bahía Blanca; Argentina
Fil: De Oliveira Pena, Rodrigo. New Jersey Institute of Technology; Estados Unidos
Fil: Mount, Rebecca A.. Boston University; Estados Unidos
Fil: Xiao, Sheng. Boston University; Estados Unidos
Fil: Zhou, Samuel L.. Boston University; Estados Unidos
Fil: Tseng, Hua-an. Boston University; Estados Unidos
Fil: Gritton, Howard. University of Illinois. Urbana - Champaign; Estados Unidos
Fil: Shroff, Sanaya. Boston University; Estados Unidos
Fil: Kondabolu, Krishnakanth. Boston University; Estados Unidos
Fil: Cheung, Cyrus. Boston University; Estados Unidos
Fil: Wang, Yangyang. Boston University; Estados Unidos
Fil: Piatkevich, Kiryl D.. Westlake University; China
Fil: Boyden, Edward S.. McGovern Institute for Brain Research; Estados Unidos. Massachusetts Institute of Technology; Estados Unidos
Fil: Mertz, Jerome. Boston University; Estados Unidos
Fil: Hasselmo, Michael E.. Boston University; Estados Unidos
Fil: Rotstein, Horacio. New Jersey Institute of Technology; Estados Unidos
Fil: Han, Xue. Boston University; Estados Unidos
Materia
COMPLEX SPIKES
CP: NEUROSCIENCE
NEURAL OSCILLATIONS
OPTOGENETICS, BURSTS
PLACE FIELDS
PLATEAU POTENTIALS
SOMARCHON
SPATIAL NAVIGATION
SUBTHRESHOLD VOLTAGE
VOLTAGE IMAGING
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/223080
Acceder
id CONICETDig_950359fedb2c929f40667d03818cbd5c
oai_identifier_str oai:ri.conicet.gov.ar:11336/223080
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigationLowet, EricSheehan, Daniel J.Chialva, UlisesDe Oliveira Pena, RodrigoMount, Rebecca A.Xiao, ShengZhou, Samuel L.Tseng, Hua-anGritton, HowardShroff, SanayaKondabolu, KrishnakanthCheung, CyrusWang, YangyangPiatkevich, Kiryl D.Boyden, Edward S.Mertz, JeromeHasselmo, Michael E.Rotstein, HoracioHan, XueCOMPLEX SPIKESCP: NEUROSCIENCENEURAL OSCILLATIONSOPTOGENETICS, BURSTSPLACE FIELDSPLATEAU POTENTIALSSOMARCHONSPATIAL NAVIGATIONSUBTHRESHOLD VOLTAGEVOLTAGE IMAGINGhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Hippocampal CA1 neurons generate single spikes and stereotyped bursts of spikes. However, it is unclear how individual neurons dynamically switch between these output modes and whether these two spiking outputs relay distinct information. We performed extracellular recordings in spatially navigating rats and cellular voltage imaging and optogenetics in awake mice. We found that spike bursts are preferentially linked to cellular and network theta rhythms (3–12 Hz) and encode an animal's position via theta phase precession, particularly as animals are entering a place field. In contrast, single spikes exhibit additional coupling to gamma rhythms (30–100 Hz), particularly as animals leave a place field. Biophysical modeling suggests that intracellular properties alone are sufficient to explain the observed input frequency-dependent spike coding. Thus, hippocampal neurons regulate the generation of bursts and single spikes according to frequency-specific network and intracellular dynamics, suggesting that these spiking modes perform distinct computations to support spatial behavior.Fil: Lowet, Eric. Boston University; Estados UnidosFil: Sheehan, Daniel J.. Boston University; Estados UnidosFil: Chialva, Ulises. Universidad Nacional del Sur. Departamento de Matemática; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Bahía Blanca; ArgentinaFil: De Oliveira Pena, Rodrigo. New Jersey Institute of Technology; Estados UnidosFil: Mount, Rebecca A.. Boston University; Estados UnidosFil: Xiao, Sheng. Boston University; Estados UnidosFil: Zhou, Samuel L.. Boston University; Estados UnidosFil: Tseng, Hua-an. Boston University; Estados UnidosFil: Gritton, Howard. University of Illinois. Urbana - Champaign; Estados UnidosFil: Shroff, Sanaya. Boston University; Estados UnidosFil: Kondabolu, Krishnakanth. Boston University; Estados UnidosFil: Cheung, Cyrus. Boston University; Estados UnidosFil: Wang, Yangyang. Boston University; Estados UnidosFil: Piatkevich, Kiryl D.. Westlake University; ChinaFil: Boyden, Edward S.. McGovern Institute for Brain Research; Estados Unidos. Massachusetts Institute of Technology; Estados UnidosFil: Mertz, Jerome. Boston University; Estados UnidosFil: Hasselmo, Michael E.. Boston University; Estados UnidosFil: Rotstein, Horacio. New Jersey Institute of Technology; Estados UnidosFil: Han, Xue. Boston University; Estados UnidosCell Press2023-08info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/223080Lowet, Eric; Sheehan, Daniel J.; Chialva, Ulises; De Oliveira Pena, Rodrigo; Mount, Rebecca A.; et al.; Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation; Cell Press; Cell Reports; 42; 8; 8-2023; 1-242211-1247CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1016/j.celrep.2023.112906info:eu-repo/semantics/altIdentifier/url/https://www.sciencedirect.com/science/article/pii/S2211124723009178info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-nd/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:25:00Zoai:ri.conicet.gov.ar:11336/223080instacron: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:34982025-09-29 10:25:01.157CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation
title Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation
spellingShingle Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation
Lowet, Eric
COMPLEX SPIKES
CP: NEUROSCIENCE
NEURAL OSCILLATIONS
OPTOGENETICS, BURSTS
PLACE FIELDS
PLATEAU POTENTIALS
SOMARCHON
SPATIAL NAVIGATION
SUBTHRESHOLD VOLTAGE
VOLTAGE IMAGING
title_short Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation
title_full Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation
title_fullStr Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation
title_full_unstemmed Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation
title_sort Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation
dc.creator.none.fl_str_mv Lowet, Eric
Sheehan, Daniel J.
Chialva, Ulises
De Oliveira Pena, Rodrigo
Mount, Rebecca A.
Xiao, Sheng
Zhou, Samuel L.
Tseng, Hua-an
Gritton, Howard
Shroff, Sanaya
Kondabolu, Krishnakanth
Cheung, Cyrus
Wang, Yangyang
Piatkevich, Kiryl D.
Boyden, Edward S.
Mertz, Jerome
Hasselmo, Michael E.
Rotstein, Horacio
Han, Xue
author Lowet, Eric
author_facet Lowet, Eric
Sheehan, Daniel J.
Chialva, Ulises
De Oliveira Pena, Rodrigo
Mount, Rebecca A.
Xiao, Sheng
Zhou, Samuel L.
Tseng, Hua-an
Gritton, Howard
Shroff, Sanaya
Kondabolu, Krishnakanth
Cheung, Cyrus
Wang, Yangyang
Piatkevich, Kiryl D.
Boyden, Edward S.
Mertz, Jerome
Hasselmo, Michael E.
Rotstein, Horacio
Han, Xue
author_role author
author2 Sheehan, Daniel J.
Chialva, Ulises
De Oliveira Pena, Rodrigo
Mount, Rebecca A.
Xiao, Sheng
Zhou, Samuel L.
Tseng, Hua-an
Gritton, Howard
Shroff, Sanaya
Kondabolu, Krishnakanth
Cheung, Cyrus
Wang, Yangyang
Piatkevich, Kiryl D.
Boyden, Edward S.
Mertz, Jerome
Hasselmo, Michael E.
Rotstein, Horacio
Han, Xue
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv COMPLEX SPIKES
CP: NEUROSCIENCE
NEURAL OSCILLATIONS
OPTOGENETICS, BURSTS
PLACE FIELDS
PLATEAU POTENTIALS
SOMARCHON
SPATIAL NAVIGATION
SUBTHRESHOLD VOLTAGE
VOLTAGE IMAGING
topic COMPLEX SPIKES
CP: NEUROSCIENCE
NEURAL OSCILLATIONS
OPTOGENETICS, BURSTS
PLACE FIELDS
PLATEAU POTENTIALS
SOMARCHON
SPATIAL NAVIGATION
SUBTHRESHOLD VOLTAGE
VOLTAGE IMAGING
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Hippocampal CA1 neurons generate single spikes and stereotyped bursts of spikes. However, it is unclear how individual neurons dynamically switch between these output modes and whether these two spiking outputs relay distinct information. We performed extracellular recordings in spatially navigating rats and cellular voltage imaging and optogenetics in awake mice. We found that spike bursts are preferentially linked to cellular and network theta rhythms (3–12 Hz) and encode an animal's position via theta phase precession, particularly as animals are entering a place field. In contrast, single spikes exhibit additional coupling to gamma rhythms (30–100 Hz), particularly as animals leave a place field. Biophysical modeling suggests that intracellular properties alone are sufficient to explain the observed input frequency-dependent spike coding. Thus, hippocampal neurons regulate the generation of bursts and single spikes according to frequency-specific network and intracellular dynamics, suggesting that these spiking modes perform distinct computations to support spatial behavior.
Fil: Lowet, Eric. Boston University; Estados Unidos
Fil: Sheehan, Daniel J.. Boston University; Estados Unidos
Fil: Chialva, Ulises. Universidad Nacional del Sur. Departamento de Matemática; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Bahía Blanca; Argentina
Fil: De Oliveira Pena, Rodrigo. New Jersey Institute of Technology; Estados Unidos
Fil: Mount, Rebecca A.. Boston University; Estados Unidos
Fil: Xiao, Sheng. Boston University; Estados Unidos
Fil: Zhou, Samuel L.. Boston University; Estados Unidos
Fil: Tseng, Hua-an. Boston University; Estados Unidos
Fil: Gritton, Howard. University of Illinois. Urbana - Champaign; Estados Unidos
Fil: Shroff, Sanaya. Boston University; Estados Unidos
Fil: Kondabolu, Krishnakanth. Boston University; Estados Unidos
Fil: Cheung, Cyrus. Boston University; Estados Unidos
Fil: Wang, Yangyang. Boston University; Estados Unidos
Fil: Piatkevich, Kiryl D.. Westlake University; China
Fil: Boyden, Edward S.. McGovern Institute for Brain Research; Estados Unidos. Massachusetts Institute of Technology; Estados Unidos
Fil: Mertz, Jerome. Boston University; Estados Unidos
Fil: Hasselmo, Michael E.. Boston University; Estados Unidos
Fil: Rotstein, Horacio. New Jersey Institute of Technology; Estados Unidos
Fil: Han, Xue. Boston University; Estados Unidos
description Hippocampal CA1 neurons generate single spikes and stereotyped bursts of spikes. However, it is unclear how individual neurons dynamically switch between these output modes and whether these two spiking outputs relay distinct information. We performed extracellular recordings in spatially navigating rats and cellular voltage imaging and optogenetics in awake mice. We found that spike bursts are preferentially linked to cellular and network theta rhythms (3–12 Hz) and encode an animal's position via theta phase precession, particularly as animals are entering a place field. In contrast, single spikes exhibit additional coupling to gamma rhythms (30–100 Hz), particularly as animals leave a place field. Biophysical modeling suggests that intracellular properties alone are sufficient to explain the observed input frequency-dependent spike coding. Thus, hippocampal neurons regulate the generation of bursts and single spikes according to frequency-specific network and intracellular dynamics, suggesting that these spiking modes perform distinct computations to support spatial behavior.
publishDate 2023
dc.date.none.fl_str_mv 2023-08
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/11336/223080
Lowet, Eric; Sheehan, Daniel J.; Chialva, Ulises; De Oliveira Pena, Rodrigo; Mount, Rebecca A.; et al.; Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation; Cell Press; Cell Reports; 42; 8; 8-2023; 1-24
2211-1247
CONICET Digital
CONICET
url http://hdl.handle.net/11336/223080
identifier_str_mv Lowet, Eric; Sheehan, Daniel J.; Chialva, Ulises; De Oliveira Pena, Rodrigo; Mount, Rebecca A.; et al.; Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation; Cell Press; Cell Reports; 42; 8; 8-2023; 1-24
2211-1247
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.celrep.2023.112906
info:eu-repo/semantics/altIdentifier/url/https://www.sciencedirect.com/science/article/pii/S2211124723009178
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-nd/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 13.070432

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