Bidirectional flow of action potentials in axons drives activity dynamics in neuronal cultures

Detalhes bibliográficos
Autor(a) principal: Mateus, J. C.
Data de Publicação: 2021
Outros Autores: Lopes, C. D. F., Aroso, M., Costa, A. R., Gerós, A., Meneses, J., Faria, P., Neto, E., Lamghari, M., Sousa, M. M., Aguiar, P
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10400.8/8382
Resumo: Objective. Recent technological advances are revealing the complex physiology of the axon and challenging long-standing assumptions. Namely, while most action potential (AP) initiation occurs at the axon initial segment in central nervous system neurons, initiation in distal parts of the axon has been reported to occur in both physiological and pathological conditions. The functional role of these ectopic APs, if exists, is still not clear, nor its impact on network activity dynamics. Approach. Using an electrophysiology platform specifically designed for assessing axonal conduction we show here for the first time regular and effective bidirectional axonal conduction in hippocampal and dorsal root ganglia cultures. We investigate and characterize this bidirectional propagation both in physiological conditions and after distal axotomy. Main results. A significant fraction of APs are not coming from the canonical synapse-dendrite-soma signal flow, but instead from signals originating at the distal axon. Importantly, antidromic APs may carry information and can have a functional impact on the neuron, as they consistently depolarize the soma. Thus, plasticity or gene transduction mechanisms triggered by soma depolarization can also be affected by these antidromic APs. Conduction velocity is asymmetrical, with antidromic conduction being slower than orthodromic. Significance. Altogether these findings have important implications for the study of neuronal function in vitro, reshaping our understanding on how information flows in neuronal cultures.
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spelling Bidirectional flow of action potentials in axons drives activity dynamics in neuronal culturesMicrofluidicsMicroelectrode arrayDorsal root gangliaHippocampal neuronsEctopic action potentialBidirectional axonal conductionAxonal electrophysiologyObjective. Recent technological advances are revealing the complex physiology of the axon and challenging long-standing assumptions. Namely, while most action potential (AP) initiation occurs at the axon initial segment in central nervous system neurons, initiation in distal parts of the axon has been reported to occur in both physiological and pathological conditions. The functional role of these ectopic APs, if exists, is still not clear, nor its impact on network activity dynamics. Approach. Using an electrophysiology platform specifically designed for assessing axonal conduction we show here for the first time regular and effective bidirectional axonal conduction in hippocampal and dorsal root ganglia cultures. We investigate and characterize this bidirectional propagation both in physiological conditions and after distal axotomy. Main results. A significant fraction of APs are not coming from the canonical synapse-dendrite-soma signal flow, but instead from signals originating at the distal axon. Importantly, antidromic APs may carry information and can have a functional impact on the neuron, as they consistently depolarize the soma. Thus, plasticity or gene transduction mechanisms triggered by soma depolarization can also be affected by these antidromic APs. Conduction velocity is asymmetrical, with antidromic conduction being slower than orthodromic. Significance. Altogether these findings have important implications for the study of neuronal function in vitro, reshaping our understanding on how information flows in neuronal cultures.IOPIC-OnlineMateus, J. C.Lopes, C. D. F.Aroso, M.Costa, A. R.Gerós, A.Meneses, J.Faria, P.Neto, E.Lamghari, M.Sousa, M. M.Aguiar, P2023-04-13T15:40:44Z2021-12-292021-12-29T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.8/8382engMateus JC, Lopes C, Aroso M, Costa AR, Gerós A, Meneses J, Faria P, Neto E, Lamghari M, Sousa MM, Aguiar P. Bidirectional flow of action potentials in axons drives activity dynamics in neuronal cultures. J Neural Eng. 2021 Dec 29;18(6). doi: 10.1088/1741-2552/ac41db. PMID: 3489114910.1088/1741-2552/ac41dbinfo:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2024-01-17T15:57:12Zoai:iconline.ipleiria.pt:10400.8/8382Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-20T01:51:06.941698Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv Bidirectional flow of action potentials in axons drives activity dynamics in neuronal cultures
title Bidirectional flow of action potentials in axons drives activity dynamics in neuronal cultures
spellingShingle Bidirectional flow of action potentials in axons drives activity dynamics in neuronal cultures
Mateus, J. C.
Microfluidics
Microelectrode array
Dorsal root ganglia
Hippocampal neurons
Ectopic action potential
Bidirectional axonal conduction
Axonal electrophysiology
title_short Bidirectional flow of action potentials in axons drives activity dynamics in neuronal cultures
title_full Bidirectional flow of action potentials in axons drives activity dynamics in neuronal cultures
title_fullStr Bidirectional flow of action potentials in axons drives activity dynamics in neuronal cultures
title_full_unstemmed Bidirectional flow of action potentials in axons drives activity dynamics in neuronal cultures
title_sort Bidirectional flow of action potentials in axons drives activity dynamics in neuronal cultures
author Mateus, J. C.
author_facet Mateus, J. C.
Lopes, C. D. F.
Aroso, M.
Costa, A. R.
Gerós, A.
Meneses, J.
Faria, P.
Neto, E.
Lamghari, M.
Sousa, M. M.
Aguiar, P
author_role author
author2 Lopes, C. D. F.
Aroso, M.
Costa, A. R.
Gerós, A.
Meneses, J.
Faria, P.
Neto, E.
Lamghari, M.
Sousa, M. M.
Aguiar, P
author2_role author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv IC-Online
dc.contributor.author.fl_str_mv Mateus, J. C.
Lopes, C. D. F.
Aroso, M.
Costa, A. R.
Gerós, A.
Meneses, J.
Faria, P.
Neto, E.
Lamghari, M.
Sousa, M. M.
Aguiar, P
dc.subject.por.fl_str_mv Microfluidics
Microelectrode array
Dorsal root ganglia
Hippocampal neurons
Ectopic action potential
Bidirectional axonal conduction
Axonal electrophysiology
topic Microfluidics
Microelectrode array
Dorsal root ganglia
Hippocampal neurons
Ectopic action potential
Bidirectional axonal conduction
Axonal electrophysiology
description Objective. Recent technological advances are revealing the complex physiology of the axon and challenging long-standing assumptions. Namely, while most action potential (AP) initiation occurs at the axon initial segment in central nervous system neurons, initiation in distal parts of the axon has been reported to occur in both physiological and pathological conditions. The functional role of these ectopic APs, if exists, is still not clear, nor its impact on network activity dynamics. Approach. Using an electrophysiology platform specifically designed for assessing axonal conduction we show here for the first time regular and effective bidirectional axonal conduction in hippocampal and dorsal root ganglia cultures. We investigate and characterize this bidirectional propagation both in physiological conditions and after distal axotomy. Main results. A significant fraction of APs are not coming from the canonical synapse-dendrite-soma signal flow, but instead from signals originating at the distal axon. Importantly, antidromic APs may carry information and can have a functional impact on the neuron, as they consistently depolarize the soma. Thus, plasticity or gene transduction mechanisms triggered by soma depolarization can also be affected by these antidromic APs. Conduction velocity is asymmetrical, with antidromic conduction being slower than orthodromic. Significance. Altogether these findings have important implications for the study of neuronal function in vitro, reshaping our understanding on how information flows in neuronal cultures.
publishDate 2021
dc.date.none.fl_str_mv 2021-12-29
2021-12-29T00:00:00Z
2023-04-13T15:40:44Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10400.8/8382
url http://hdl.handle.net/10400.8/8382
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Mateus JC, Lopes C, Aroso M, Costa AR, Gerós A, Meneses J, Faria P, Neto E, Lamghari M, Sousa MM, Aguiar P. Bidirectional flow of action potentials in axons drives activity dynamics in neuronal cultures. J Neural Eng. 2021 Dec 29;18(6). doi: 10.1088/1741-2552/ac41db. PMID: 34891149
10.1088/1741-2552/ac41db
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv IOP
publisher.none.fl_str_mv IOP
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
instacron:RCAAP
instname_str Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
instacron_str RCAAP
institution RCAAP
reponame_str Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
collection Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository.name.fl_str_mv Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
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