Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in rats

Autores
Moreira, Carlos G; Baumann, Christian R.; Scandella, Maurizio; Nemirovsky, Sergio Ivan; Leach, Sven; Huber, Reto; Noain, Daniela Maria Clara
Año de publicación
2021
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Slow waves and cognitive output have been modulated in humans by phase-targeted auditory stimulation. However, to advance its technical development and further our understanding, implementation of the method in animal models is indispensable. Here, we report the successful employment of slow waves’ phase-targeted closed-loop auditory stimulation (CLAS) in rats. To validate this new tool both conceptually and functionally, we tested the effects of up- and down-phase CLAS on proportions and spectral characteristics of sleep, and on learning performance in the single-pellet reaching task, respectively. Without affecting 24 hr sleep-wake behavior, CLAS specifically altered delta (slow waves) and sigma (sleep spindles) power persistently over chronic periods of stimulation. While up-phase CLAS does not elicit a significant change in behavioral performance, down-phase CLAS exerted a detrimental effect on overall engagement and success rate in the behavioral test. Overall CLAS-dependent spectral changes were positively correlated with learning performance. Altogether, our results provide proof-of-principle evidence that phase-targeted CLAS of slow waves in rodents is efficient, safe, and stable over chronic experimental periods, enabling the use of this high-specificity tool for basic and preclinical translational sleep research.
Fil: Moreira, Carlos G. Universitat Zurich; Suiza
Fil: Baumann, Christian R.. Universitat Zurich; Suiza. Neuroscience Center Zurich; Suiza
Fil: Scandella, Maurizio. Universitat Zurich; Suiza
Fil: Nemirovsky, Sergio Ivan. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; Argentina
Fil: Leach, Sven. University Children's Hospital Zurich; Suiza
Fil: Huber, Reto. University Children's Hospital Zurich; Suiza. Universitat Zurich; Suiza
Fil: Noain, Daniela Maria Clara. University Hospital Zurich; Suiza. Universitat Zurich; Suiza
Materia
NEUROSCIENCE
RAT
COGNITION
SLOW WAVE SLEEP
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/182332
Acceder
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network_name_str CONICET Digital (CONICET)
spelling Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in ratsMoreira, Carlos GBaumann, Christian R.Scandella, MaurizioNemirovsky, Sergio IvanLeach, SvenHuber, RetoNoain, Daniela Maria ClaraNEUROSCIENCERATCOGNITIONSLOW WAVE SLEEPhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Slow waves and cognitive output have been modulated in humans by phase-targeted auditory stimulation. However, to advance its technical development and further our understanding, implementation of the method in animal models is indispensable. Here, we report the successful employment of slow waves’ phase-targeted closed-loop auditory stimulation (CLAS) in rats. To validate this new tool both conceptually and functionally, we tested the effects of up- and down-phase CLAS on proportions and spectral characteristics of sleep, and on learning performance in the single-pellet reaching task, respectively. Without affecting 24 hr sleep-wake behavior, CLAS specifically altered delta (slow waves) and sigma (sleep spindles) power persistently over chronic periods of stimulation. While up-phase CLAS does not elicit a significant change in behavioral performance, down-phase CLAS exerted a detrimental effect on overall engagement and success rate in the behavioral test. Overall CLAS-dependent spectral changes were positively correlated with learning performance. Altogether, our results provide proof-of-principle evidence that phase-targeted CLAS of slow waves in rodents is efficient, safe, and stable over chronic experimental periods, enabling the use of this high-specificity tool for basic and preclinical translational sleep research.Fil: Moreira, Carlos G. Universitat Zurich; SuizaFil: Baumann, Christian R.. Universitat Zurich; Suiza. Neuroscience Center Zurich; SuizaFil: Scandella, Maurizio. Universitat Zurich; SuizaFil: Nemirovsky, Sergio Ivan. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; ArgentinaFil: Leach, Sven. University Children's Hospital Zurich; SuizaFil: Huber, Reto. University Children's Hospital Zurich; Suiza. Universitat Zurich; SuizaFil: Noain, Daniela Maria Clara. University Hospital Zurich; Suiza. Universitat Zurich; SuizaeLife Sciences Publications Ltd2021-10-06info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/182332Moreira, Carlos G; Baumann, Christian R.; Scandella, Maurizio; Nemirovsky, Sergio Ivan; Leach, Sven; et al.; Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in rats; eLife Sciences Publications Ltd; eLife; 10; 6-10-2021; 1-232050-084X2050-084XCONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://elifesciences.org/articles/68043info:eu-repo/semantics/altIdentifier/doi/10.7554/eLife.68043info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:38:48Zoai:ri.conicet.gov.ar:11336/182332instacron: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 09:38:49.159CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in rats
title Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in rats
spellingShingle Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in rats
Moreira, Carlos G
NEUROSCIENCE
RAT
COGNITION
SLOW WAVE SLEEP
title_short Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in rats
title_full Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in rats
title_fullStr Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in rats
title_full_unstemmed Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in rats
title_sort Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in rats
dc.creator.none.fl_str_mv Moreira, Carlos G
Baumann, Christian R.
Scandella, Maurizio
Nemirovsky, Sergio Ivan
Leach, Sven
Huber, Reto
Noain, Daniela Maria Clara
author Moreira, Carlos G
author_facet Moreira, Carlos G
Baumann, Christian R.
Scandella, Maurizio
Nemirovsky, Sergio Ivan
Leach, Sven
Huber, Reto
Noain, Daniela Maria Clara
author_role author
author2 Baumann, Christian R.
Scandella, Maurizio
Nemirovsky, Sergio Ivan
Leach, Sven
Huber, Reto
Noain, Daniela Maria Clara
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv NEUROSCIENCE
RAT
COGNITION
SLOW WAVE SLEEP
topic NEUROSCIENCE
RAT
COGNITION
SLOW WAVE SLEEP
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Slow waves and cognitive output have been modulated in humans by phase-targeted auditory stimulation. However, to advance its technical development and further our understanding, implementation of the method in animal models is indispensable. Here, we report the successful employment of slow waves’ phase-targeted closed-loop auditory stimulation (CLAS) in rats. To validate this new tool both conceptually and functionally, we tested the effects of up- and down-phase CLAS on proportions and spectral characteristics of sleep, and on learning performance in the single-pellet reaching task, respectively. Without affecting 24 hr sleep-wake behavior, CLAS specifically altered delta (slow waves) and sigma (sleep spindles) power persistently over chronic periods of stimulation. While up-phase CLAS does not elicit a significant change in behavioral performance, down-phase CLAS exerted a detrimental effect on overall engagement and success rate in the behavioral test. Overall CLAS-dependent spectral changes were positively correlated with learning performance. Altogether, our results provide proof-of-principle evidence that phase-targeted CLAS of slow waves in rodents is efficient, safe, and stable over chronic experimental periods, enabling the use of this high-specificity tool for basic and preclinical translational sleep research.
Fil: Moreira, Carlos G. Universitat Zurich; Suiza
Fil: Baumann, Christian R.. Universitat Zurich; Suiza. Neuroscience Center Zurich; Suiza
Fil: Scandella, Maurizio. Universitat Zurich; Suiza
Fil: Nemirovsky, Sergio Ivan. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; Argentina
Fil: Leach, Sven. University Children's Hospital Zurich; Suiza
Fil: Huber, Reto. University Children's Hospital Zurich; Suiza. Universitat Zurich; Suiza
Fil: Noain, Daniela Maria Clara. University Hospital Zurich; Suiza. Universitat Zurich; Suiza
description Slow waves and cognitive output have been modulated in humans by phase-targeted auditory stimulation. However, to advance its technical development and further our understanding, implementation of the method in animal models is indispensable. Here, we report the successful employment of slow waves’ phase-targeted closed-loop auditory stimulation (CLAS) in rats. To validate this new tool both conceptually and functionally, we tested the effects of up- and down-phase CLAS on proportions and spectral characteristics of sleep, and on learning performance in the single-pellet reaching task, respectively. Without affecting 24 hr sleep-wake behavior, CLAS specifically altered delta (slow waves) and sigma (sleep spindles) power persistently over chronic periods of stimulation. While up-phase CLAS does not elicit a significant change in behavioral performance, down-phase CLAS exerted a detrimental effect on overall engagement and success rate in the behavioral test. Overall CLAS-dependent spectral changes were positively correlated with learning performance. Altogether, our results provide proof-of-principle evidence that phase-targeted CLAS of slow waves in rodents is efficient, safe, and stable over chronic experimental periods, enabling the use of this high-specificity tool for basic and preclinical translational sleep research.
publishDate 2021
dc.date.none.fl_str_mv 2021-10-06
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/11336/182332
Moreira, Carlos G; Baumann, Christian R.; Scandella, Maurizio; Nemirovsky, Sergio Ivan; Leach, Sven; et al.; Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in rats; eLife Sciences Publications Ltd; eLife; 10; 6-10-2021; 1-23
2050-084X
2050-084X
CONICET Digital
CONICET
url http://hdl.handle.net/11336/182332
identifier_str_mv Moreira, Carlos G; Baumann, Christian R.; Scandella, Maurizio; Nemirovsky, Sergio Ivan; Leach, Sven; et al.; Closed-loop auditory stimulation method to modulate sleep slow waves and motor learning performance in rats; eLife Sciences Publications Ltd; eLife; 10; 6-10-2021; 1-23
2050-084X
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://elifesciences.org/articles/68043
info:eu-repo/semantics/altIdentifier/doi/10.7554/eLife.68043
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv eLife Sciences Publications Ltd
publisher.none.fl_str_mv eLife Sciences Publications Ltd
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
_version_ 1844613227282956288
score 13.070432

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