Peripherally driven low-threshold inhibitory inputs to lamina I local-circuit and projection neurones: a new circuit for gating pain responses

Detalhes bibliográficos
Autor(a) principal: Luz, LL
Data de Publicação: 2014
Outros Autores: Szucs, P, Safronov, BV
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10216/114496
Resumo: Spinal lamina I is a key element of the pain processing system which relays primary afferent input to supraspinal areas. However, little is known about how the signal is modulated by its intrinsic network including local-circuit neurones (LCNs) and much less numerous anterolateral tract projection neurones (PNs). Here, we used whole-cell patch clamp recordings in an isolated spinal cord preparation to examine properties of identified LCNs (n = 85) and PNs (n = 73) in their functionally preserved local networks. Forty LCNs showed spontaneous rhythmic firing (2-7 Hz) at zero current injection, which persisted in the presence of blockers of fast synaptic transmission. In the remaining cases, most LCNs and PNs fired tonically in response to depolarizing current injections. We identified LCNs and PNs receiving low-threshold primary afferent-driven inhibitory inputs, which in many cases were disynaptic and temporally preceded classical high-threshold excitatory inputs. This direct inhibitory link between low-threshold afferents and PNs can function as a postsynaptic gate controlling the nociceptive information flow in the spinal cord. The LCNs were found to be integrated into the superficial dorsal horn network by their receipt of monosynaptic and disynaptic inputs from other lamina I and II neurones. One-third of LCNs and two-thirds of PNs tested responded to substance P application. Thus, substance P released by a noxious afferent stimulation may excite PNs in two ways: directly, and via the activation of presynaptic LCN circuitries. In conclusion, we have described important properties of identified lamina I neurones and their roles in a new circuit for gating pain responses.
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spelling Peripherally driven low-threshold inhibitory inputs to lamina I local-circuit and projection neurones: a new circuit for gating pain responsesAnimalsElectric StimulationExcitatory Postsynaptic PotentialsGlycine/metabolismIn Vitro TechniquesInhibitory Postsynaptic PotentialsNeural Inhibition/drug effectsNeural Pathways/physiopathologyPain/metabolismPain/physiopathologyPain PerceptionPeriodicityRats, WistarReaction TimeSignal Transduction/drug effectsSpinal Cord Dorsal Horn/drug effectsSpinal Cord Dorsal Horn/metabolismSpinal Cord Dorsal Horn/physiopathologySubstance P/pharmacologySynaptic TransmissionTime Factorsgamma-Aminobutyric Acid/metabolismSpinal lamina I is a key element of the pain processing system which relays primary afferent input to supraspinal areas. However, little is known about how the signal is modulated by its intrinsic network including local-circuit neurones (LCNs) and much less numerous anterolateral tract projection neurones (PNs). Here, we used whole-cell patch clamp recordings in an isolated spinal cord preparation to examine properties of identified LCNs (n = 85) and PNs (n = 73) in their functionally preserved local networks. Forty LCNs showed spontaneous rhythmic firing (2-7 Hz) at zero current injection, which persisted in the presence of blockers of fast synaptic transmission. In the remaining cases, most LCNs and PNs fired tonically in response to depolarizing current injections. We identified LCNs and PNs receiving low-threshold primary afferent-driven inhibitory inputs, which in many cases were disynaptic and temporally preceded classical high-threshold excitatory inputs. This direct inhibitory link between low-threshold afferents and PNs can function as a postsynaptic gate controlling the nociceptive information flow in the spinal cord. The LCNs were found to be integrated into the superficial dorsal horn network by their receipt of monosynaptic and disynaptic inputs from other lamina I and II neurones. One-third of LCNs and two-thirds of PNs tested responded to substance P application. Thus, substance P released by a noxious afferent stimulation may excite PNs in two ways: directly, and via the activation of presynaptic LCN circuitries. In conclusion, we have described important properties of identified lamina I neurones and their roles in a new circuit for gating pain responses.Wiley20142014-01-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10216/114496eng0022-375110.1113/jphysiol.2013.269472Luz, LLSzucs, PSafronov, BVinfo: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:RCAAP2023-11-29T14:10:37Zoai:repositorio-aberto.up.pt:10216/114496Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T23:56:26.612871Repositório 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 Peripherally driven low-threshold inhibitory inputs to lamina I local-circuit and projection neurones: a new circuit for gating pain responses
title Peripherally driven low-threshold inhibitory inputs to lamina I local-circuit and projection neurones: a new circuit for gating pain responses
spellingShingle Peripherally driven low-threshold inhibitory inputs to lamina I local-circuit and projection neurones: a new circuit for gating pain responses
Luz, LL
Animals
Electric Stimulation
Excitatory Postsynaptic Potentials
Glycine/metabolism
In Vitro Techniques
Inhibitory Postsynaptic Potentials
Neural Inhibition/drug effects
Neural Pathways/physiopathology
Pain/metabolism
Pain/physiopathology
Pain Perception
Periodicity
Rats, Wistar
Reaction Time
Signal Transduction/drug effects
Spinal Cord Dorsal Horn/drug effects
Spinal Cord Dorsal Horn/metabolism
Spinal Cord Dorsal Horn/physiopathology
Substance P/pharmacology
Synaptic Transmission
Time Factors
gamma-Aminobutyric Acid/metabolism
title_short Peripherally driven low-threshold inhibitory inputs to lamina I local-circuit and projection neurones: a new circuit for gating pain responses
title_full Peripherally driven low-threshold inhibitory inputs to lamina I local-circuit and projection neurones: a new circuit for gating pain responses
title_fullStr Peripherally driven low-threshold inhibitory inputs to lamina I local-circuit and projection neurones: a new circuit for gating pain responses
title_full_unstemmed Peripherally driven low-threshold inhibitory inputs to lamina I local-circuit and projection neurones: a new circuit for gating pain responses
title_sort Peripherally driven low-threshold inhibitory inputs to lamina I local-circuit and projection neurones: a new circuit for gating pain responses
author Luz, LL
author_facet Luz, LL
Szucs, P
Safronov, BV
author_role author
author2 Szucs, P
Safronov, BV
author2_role author
author
dc.contributor.author.fl_str_mv Luz, LL
Szucs, P
Safronov, BV
dc.subject.por.fl_str_mv Animals
Electric Stimulation
Excitatory Postsynaptic Potentials
Glycine/metabolism
In Vitro Techniques
Inhibitory Postsynaptic Potentials
Neural Inhibition/drug effects
Neural Pathways/physiopathology
Pain/metabolism
Pain/physiopathology
Pain Perception
Periodicity
Rats, Wistar
Reaction Time
Signal Transduction/drug effects
Spinal Cord Dorsal Horn/drug effects
Spinal Cord Dorsal Horn/metabolism
Spinal Cord Dorsal Horn/physiopathology
Substance P/pharmacology
Synaptic Transmission
Time Factors
gamma-Aminobutyric Acid/metabolism
topic Animals
Electric Stimulation
Excitatory Postsynaptic Potentials
Glycine/metabolism
In Vitro Techniques
Inhibitory Postsynaptic Potentials
Neural Inhibition/drug effects
Neural Pathways/physiopathology
Pain/metabolism
Pain/physiopathology
Pain Perception
Periodicity
Rats, Wistar
Reaction Time
Signal Transduction/drug effects
Spinal Cord Dorsal Horn/drug effects
Spinal Cord Dorsal Horn/metabolism
Spinal Cord Dorsal Horn/physiopathology
Substance P/pharmacology
Synaptic Transmission
Time Factors
gamma-Aminobutyric Acid/metabolism
description Spinal lamina I is a key element of the pain processing system which relays primary afferent input to supraspinal areas. However, little is known about how the signal is modulated by its intrinsic network including local-circuit neurones (LCNs) and much less numerous anterolateral tract projection neurones (PNs). Here, we used whole-cell patch clamp recordings in an isolated spinal cord preparation to examine properties of identified LCNs (n = 85) and PNs (n = 73) in their functionally preserved local networks. Forty LCNs showed spontaneous rhythmic firing (2-7 Hz) at zero current injection, which persisted in the presence of blockers of fast synaptic transmission. In the remaining cases, most LCNs and PNs fired tonically in response to depolarizing current injections. We identified LCNs and PNs receiving low-threshold primary afferent-driven inhibitory inputs, which in many cases were disynaptic and temporally preceded classical high-threshold excitatory inputs. This direct inhibitory link between low-threshold afferents and PNs can function as a postsynaptic gate controlling the nociceptive information flow in the spinal cord. The LCNs were found to be integrated into the superficial dorsal horn network by their receipt of monosynaptic and disynaptic inputs from other lamina I and II neurones. One-third of LCNs and two-thirds of PNs tested responded to substance P application. Thus, substance P released by a noxious afferent stimulation may excite PNs in two ways: directly, and via the activation of presynaptic LCN circuitries. In conclusion, we have described important properties of identified lamina I neurones and their roles in a new circuit for gating pain responses.
publishDate 2014
dc.date.none.fl_str_mv 2014
2014-01-01T00:00:00Z
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/10216/114496
url http://hdl.handle.net/10216/114496
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv 0022-3751
10.1113/jphysiol.2013.269472
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 Wiley
publisher.none.fl_str_mv Wiley
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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