Principles of nociceptive coding in the anterior cingulate cortex

Autores
Acuña, Mario A.; Kasanetz, Fernando; De Luna, Paolo; Falkowska, Marta; Nevian, Thomas
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The perception of pain is a multidimensional sensory and emotional/affective experience arising from distributed brain activity. However, the involved brain regions are not specific for pain. Thus, how the cortex distinguishes nociception from other aversive and salient sensory stimuli remains elusive. Additionally, the resulting consequences of chronic neuropathic pain on sensory processing have not been characterized. Using in vivo miniscope calcium imaging with cellular resolution in freely moving mice, we elucidated the principles of nociceptive and sensory coding in the anterior cingulate cortex, a region essential for pain processing. We found that population activity, not single-cell responses, allowed discriminating noxious from other sensory stimuli, ruling out the existence of nociception-specific neurons. Additionally, single-cell stimulus selectivity was highly dynamic over time, but stimulus representation at the population level remained stable. Peripheral nerve injury-induced chronic neuropathic pain led to dysfunctional encoding of sensory events by exacerbation of responses to innocuous stimuli and impairment of pattern separation and stimulus classification, which were restored by analgesic treatment. These findings provide a novel interpretation for altered cortical sensory processing in chronic neuropathic pain and give insights into the effects of systemic analgesic treatment in the cortex.
Fil: Acuña, Mario A.. University of Bern; Suiza
Fil: Kasanetz, Fernando. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina. University of Bern; Suiza
Fil: De Luna, Paolo. University of Bern; Suiza
Fil: Falkowska, Marta. University of Bern; Suiza
Fil: Nevian, Thomas. University of Bern; Suiza
Materia
ANTERIOR CINGULATE CORTEX
IN VIVO CALCIUM IMAGING
NEUROPATHIC PAIN
NOCICEPTION
SENSORY REPRESENTATION
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:11336/227888
Acceder
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network_name_str CONICET Digital (CONICET)
spelling Principles of nociceptive coding in the anterior cingulate cortexAcuña, Mario A.Kasanetz, FernandoDe Luna, PaoloFalkowska, MartaNevian, ThomasANTERIOR CINGULATE CORTEXIN VIVO CALCIUM IMAGINGNEUROPATHIC PAINNOCICEPTIONSENSORY REPRESENTATIONhttps://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3The perception of pain is a multidimensional sensory and emotional/affective experience arising from distributed brain activity. However, the involved brain regions are not specific for pain. Thus, how the cortex distinguishes nociception from other aversive and salient sensory stimuli remains elusive. Additionally, the resulting consequences of chronic neuropathic pain on sensory processing have not been characterized. Using in vivo miniscope calcium imaging with cellular resolution in freely moving mice, we elucidated the principles of nociceptive and sensory coding in the anterior cingulate cortex, a region essential for pain processing. We found that population activity, not single-cell responses, allowed discriminating noxious from other sensory stimuli, ruling out the existence of nociception-specific neurons. Additionally, single-cell stimulus selectivity was highly dynamic over time, but stimulus representation at the population level remained stable. Peripheral nerve injury-induced chronic neuropathic pain led to dysfunctional encoding of sensory events by exacerbation of responses to innocuous stimuli and impairment of pattern separation and stimulus classification, which were restored by analgesic treatment. These findings provide a novel interpretation for altered cortical sensory processing in chronic neuropathic pain and give insights into the effects of systemic analgesic treatment in the cortex.Fil: Acuña, Mario A.. University of Bern; SuizaFil: Kasanetz, Fernando. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina. University of Bern; SuizaFil: De Luna, Paolo. University of Bern; SuizaFil: Falkowska, Marta. University of Bern; SuizaFil: Nevian, Thomas. University of Bern; SuizaNational Academy of Sciences2023-06info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/zipapplication/pdfhttp://hdl.handle.net/11336/227888Acuña, Mario A.; Kasanetz, Fernando; De Luna, Paolo; Falkowska, Marta; Nevian, Thomas; Principles of nociceptive coding in the anterior cingulate cortex; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 120; 23; 6-2023; 1-90027-8424CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.pnas.org/doi/10.1073/pnas.2212394120info:eu-repo/semantics/altIdentifier/doi/10.1073/pnas.2212394120info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-nd/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-22T12:16:09Zoai:ri.conicet.gov.ar:11336/227888instacron: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:34982025-10-22 12:16:10.066CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Principles of nociceptive coding in the anterior cingulate cortex
title Principles of nociceptive coding in the anterior cingulate cortex
spellingShingle Principles of nociceptive coding in the anterior cingulate cortex
Acuña, Mario A.
ANTERIOR CINGULATE CORTEX
IN VIVO CALCIUM IMAGING
NEUROPATHIC PAIN
NOCICEPTION
SENSORY REPRESENTATION
title_short Principles of nociceptive coding in the anterior cingulate cortex
title_full Principles of nociceptive coding in the anterior cingulate cortex
title_fullStr Principles of nociceptive coding in the anterior cingulate cortex
title_full_unstemmed Principles of nociceptive coding in the anterior cingulate cortex
title_sort Principles of nociceptive coding in the anterior cingulate cortex
dc.creator.none.fl_str_mv Acuña, Mario A.
Kasanetz, Fernando
De Luna, Paolo
Falkowska, Marta
Nevian, Thomas
author Acuña, Mario A.
author_facet Acuña, Mario A.
Kasanetz, Fernando
De Luna, Paolo
Falkowska, Marta
Nevian, Thomas
author_role author
author2 Kasanetz, Fernando
De Luna, Paolo
Falkowska, Marta
Nevian, Thomas
author2_role author
author
author
author
dc.subject.none.fl_str_mv ANTERIOR CINGULATE CORTEX
IN VIVO CALCIUM IMAGING
NEUROPATHIC PAIN
NOCICEPTION
SENSORY REPRESENTATION
topic ANTERIOR CINGULATE CORTEX
IN VIVO CALCIUM IMAGING
NEUROPATHIC PAIN
NOCICEPTION
SENSORY REPRESENTATION
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv The perception of pain is a multidimensional sensory and emotional/affective experience arising from distributed brain activity. However, the involved brain regions are not specific for pain. Thus, how the cortex distinguishes nociception from other aversive and salient sensory stimuli remains elusive. Additionally, the resulting consequences of chronic neuropathic pain on sensory processing have not been characterized. Using in vivo miniscope calcium imaging with cellular resolution in freely moving mice, we elucidated the principles of nociceptive and sensory coding in the anterior cingulate cortex, a region essential for pain processing. We found that population activity, not single-cell responses, allowed discriminating noxious from other sensory stimuli, ruling out the existence of nociception-specific neurons. Additionally, single-cell stimulus selectivity was highly dynamic over time, but stimulus representation at the population level remained stable. Peripheral nerve injury-induced chronic neuropathic pain led to dysfunctional encoding of sensory events by exacerbation of responses to innocuous stimuli and impairment of pattern separation and stimulus classification, which were restored by analgesic treatment. These findings provide a novel interpretation for altered cortical sensory processing in chronic neuropathic pain and give insights into the effects of systemic analgesic treatment in the cortex.
Fil: Acuña, Mario A.. University of Bern; Suiza
Fil: Kasanetz, Fernando. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina. University of Bern; Suiza
Fil: De Luna, Paolo. University of Bern; Suiza
Fil: Falkowska, Marta. University of Bern; Suiza
Fil: Nevian, Thomas. University of Bern; Suiza
description The perception of pain is a multidimensional sensory and emotional/affective experience arising from distributed brain activity. However, the involved brain regions are not specific for pain. Thus, how the cortex distinguishes nociception from other aversive and salient sensory stimuli remains elusive. Additionally, the resulting consequences of chronic neuropathic pain on sensory processing have not been characterized. Using in vivo miniscope calcium imaging with cellular resolution in freely moving mice, we elucidated the principles of nociceptive and sensory coding in the anterior cingulate cortex, a region essential for pain processing. We found that population activity, not single-cell responses, allowed discriminating noxious from other sensory stimuli, ruling out the existence of nociception-specific neurons. Additionally, single-cell stimulus selectivity was highly dynamic over time, but stimulus representation at the population level remained stable. Peripheral nerve injury-induced chronic neuropathic pain led to dysfunctional encoding of sensory events by exacerbation of responses to innocuous stimuli and impairment of pattern separation and stimulus classification, which were restored by analgesic treatment. These findings provide a novel interpretation for altered cortical sensory processing in chronic neuropathic pain and give insights into the effects of systemic analgesic treatment in the cortex.
publishDate 2023
dc.date.none.fl_str_mv 2023-06
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/11336/227888
Acuña, Mario A.; Kasanetz, Fernando; De Luna, Paolo; Falkowska, Marta; Nevian, Thomas; Principles of nociceptive coding in the anterior cingulate cortex; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 120; 23; 6-2023; 1-9
0027-8424
CONICET Digital
CONICET
url http://hdl.handle.net/11336/227888
identifier_str_mv Acuña, Mario A.; Kasanetz, Fernando; De Luna, Paolo; Falkowska, Marta; Nevian, Thomas; Principles of nociceptive coding in the anterior cingulate cortex; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 120; 23; 6-2023; 1-9
0027-8424
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://www.pnas.org/doi/10.1073/pnas.2212394120
info:eu-repo/semantics/altIdentifier/doi/10.1073/pnas.2212394120
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/zip
application/pdf
dc.publisher.none.fl_str_mv National Academy of Sciences
publisher.none.fl_str_mv National Academy of Sciences
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 12.982451

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