Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep

Detalhes bibliográficos
Autor(a) principal: Calais, Julien Braga
Data de Publicação: 2015
Outros Autores: Ojopi, Elida Benquique, Morya, Edgard, Sameshima, Koichi, Ribeiro, Sidarta Tollendal Gomes
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UFRN
Texto Completo: https://repositorio.ufrn.br/jspui/handle/123456789/18982
Resumo: Sleep is beneficial to learning, but the underlying mechanisms remain controversial. The synaptic homeostasis hypothesis (SHY) proposes that the cognitive function of sleep is related to a generalized rescaling of synaptic weights to intermediate levels, due to a passive downregulation of plasticity mechanisms. A competing hypothesis proposes that the active upscaling and downscaling of synaptic weights during sleep embosses memories in circuits respectively activated or deactivated during prior waking experience, leading to memory changes beyond rescaling. Both theories have empirical support but the experimental designs underlying the conflicting studies are not congruent, therefore a consensus is yet to be reached. To advance this issue, we used real-time PCR and electrophysiological recordings to assess gene expression related to synaptic plasticity in the hippocampus and primary somatosensory cortex of rats exposed to novel objects, then kept awake (WK) for 60 min and finally killed after a 30 min period rich in WK, slow-wave sleep (SWS) or rapid-eye-movement sleep (REM). Animals similarly treated but not exposed to novel objects were used as controls. We found that the mRNA levels of Arc, Egr1, Fos, Ppp2ca and Ppp2r2d were significantly increased in the hippocampus of exposed animals allowed to enter REM, in comparison with control animals. Experience-dependent changes during sleep were not significant in the hippocampus for Bdnf, Camk4, Creb1, and Nr4a1, and no differences were detected between exposed and control SWS groups for any of the genes tested. No significant changes in gene expression were detected in the primary somatosensory cortex during sleep, in contrast with previous studies using longer post-stimulation intervals (>180 min). The experience-dependent induction of multiple plasticity-related genes in the hippocampus during early REM adds experimental support to the synaptic embossing theory.
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spelling Calais, Julien BragaOjopi, Elida BenquiqueMorya, EdgardSameshima, KoichiRibeiro, Sidarta Tollendal Gomes2015-03-17T13:40:32Z2015-03-17T13:40:32Z2015CALAIS, Julien Braga; et al. Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep. Neurobiology of Learning and Memory. 2015. Disponível em: .Doi: 10.1016/j.nlm.2015.01.0021074-7427https://repositorio.ufrn.br/jspui/handle/123456789/18982Sleep is beneficial to learning, but the underlying mechanisms remain controversial. The synaptic homeostasis hypothesis (SHY) proposes that the cognitive function of sleep is related to a generalized rescaling of synaptic weights to intermediate levels, due to a passive downregulation of plasticity mechanisms. A competing hypothesis proposes that the active upscaling and downscaling of synaptic weights during sleep embosses memories in circuits respectively activated or deactivated during prior waking experience, leading to memory changes beyond rescaling. Both theories have empirical support but the experimental designs underlying the conflicting studies are not congruent, therefore a consensus is yet to be reached. To advance this issue, we used real-time PCR and electrophysiological recordings to assess gene expression related to synaptic plasticity in the hippocampus and primary somatosensory cortex of rats exposed to novel objects, then kept awake (WK) for 60 min and finally killed after a 30 min period rich in WK, slow-wave sleep (SWS) or rapid-eye-movement sleep (REM). Animals similarly treated but not exposed to novel objects were used as controls. We found that the mRNA levels of Arc, Egr1, Fos, Ppp2ca and Ppp2r2d were significantly increased in the hippocampus of exposed animals allowed to enter REM, in comparison with control animals. Experience-dependent changes during sleep were not significant in the hippocampus for Bdnf, Camk4, Creb1, and Nr4a1, and no differences were detected between exposed and control SWS groups for any of the genes tested. No significant changes in gene expression were detected in the primary somatosensory cortex during sleep, in contrast with previous studies using longer post-stimulation intervals (>180 min). The experience-dependent induction of multiple plasticity-related genes in the hippocampus during early REM adds experimental support to the synaptic embossing theory.m Financiadora de Estudos e Projetos (FINEP) Grant 01.06.1092.00, Ministério da Ciência, Tecnologia e Inovação (MCTI), State of São Paulo Research Foundation (FAPESP) Grant 06/05436-8, Associação Alberto Santos Dumont para Apoio à Pesquisa (AASDAP), FAPERN/CNPq PRONEM 003/ 2011, and National Council for Scientific and Technological Development (CNPq Edital Universal 481506/2007-1 and 481351/2011- 6, PQ 306604/2012-4).ElsevierSleepProtein phosphatase 2AMemorySynaptic plasticityGene expressionImmediate early genesExperience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleepinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleengreponame:Repositório Institucional da UFRNinstname:Universidade Federal do Rio Grande do Norte (UFRN)instacron:UFRNinfo:eu-repo/semantics/openAccessORIGINALRibeiro_Inst_Cerebro_Experience-dependent_2015.pdfRibeiro_Inst_Cerebro_Experience-dependent_2015.pdfArtigo principalapplication/pdf1569543https://repositorio.ufrn.br/bitstream/123456789/18982/1/Ribeiro_Inst_Cerebro_Experience-dependent_2015.pdfcc0f68f0a667046b45a5fda6042e7642MD51LICENSElicense.txtlicense.txttext/plain; charset=utf-81563https://repositorio.ufrn.br/bitstream/123456789/18982/5/license.txt2fca3d993fd069474a9dfb5156c39499MD55CC-LICENSElicense_urllicense_urltext/plain; charset=utf-849https://repositorio.ufrn.br/bitstream/123456789/18982/2/license_url924993ce0b3ba389f79f32a1b2735415MD52license_textlicense_texttext/html; charset=utf-822864https://repositorio.ufrn.br/bitstream/123456789/18982/3/license_text8e37d7b9d509ac90b985587e2924ad4fMD53license_rdflicense_rdfapplication/rdf+xml; charset=utf-823748https://repositorio.ufrn.br/bitstream/123456789/18982/4/license_rdfb92763cfc0af52c7c868455edfaf3266MD54TEXTRibeiro_Inst_Cerebro_Experience-dependent_2015.pdf.txtRibeiro_Inst_Cerebro_Experience-dependent_2015.pdf.txtExtracted texttext/plain54967https://repositorio.ufrn.br/bitstream/123456789/18982/10/Ribeiro_Inst_Cerebro_Experience-dependent_2015.pdf.txt064c7bf57bab87e59ce9a75af5529560MD510THUMBNAILRibeiro_Inst_Cerebro_Experience-dependent_2015.pdf.jpgRibeiro_Inst_Cerebro_Experience-dependent_2015.pdf.jpgIM Thumbnailimage/jpeg9511https://repositorio.ufrn.br/bitstream/123456789/18982/11/Ribeiro_Inst_Cerebro_Experience-dependent_2015.pdf.jpge4a9f0bab2b0d703b96ec23d5728264dMD511123456789/189822021-07-10 19:10:16.442oai:https://repositorio.ufrn.br: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ório de PublicaçõesPUBhttp://repositorio.ufrn.br/oai/opendoar:2021-07-10T22:10:16Repositório Institucional da UFRN - Universidade Federal do Rio Grande do Norte (UFRN)false
dc.title.pt_BR.fl_str_mv Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep
title Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep
spellingShingle Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep
Calais, Julien Braga
Sleep
Protein phosphatase 2A
Memory
Synaptic plasticity
Gene expression
Immediate early genes
title_short Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep
title_full Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep
title_fullStr Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep
title_full_unstemmed Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep
title_sort Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep
author Calais, Julien Braga
author_facet Calais, Julien Braga
Ojopi, Elida Benquique
Morya, Edgard
Sameshima, Koichi
Ribeiro, Sidarta Tollendal Gomes
author_role author
author2 Ojopi, Elida Benquique
Morya, Edgard
Sameshima, Koichi
Ribeiro, Sidarta Tollendal Gomes
author2_role author
author
author
author
dc.contributor.author.fl_str_mv Calais, Julien Braga
Ojopi, Elida Benquique
Morya, Edgard
Sameshima, Koichi
Ribeiro, Sidarta Tollendal Gomes
dc.subject.por.fl_str_mv Sleep
Protein phosphatase 2A
Memory
Synaptic plasticity
Gene expression
Immediate early genes
topic Sleep
Protein phosphatase 2A
Memory
Synaptic plasticity
Gene expression
Immediate early genes
description Sleep is beneficial to learning, but the underlying mechanisms remain controversial. The synaptic homeostasis hypothesis (SHY) proposes that the cognitive function of sleep is related to a generalized rescaling of synaptic weights to intermediate levels, due to a passive downregulation of plasticity mechanisms. A competing hypothesis proposes that the active upscaling and downscaling of synaptic weights during sleep embosses memories in circuits respectively activated or deactivated during prior waking experience, leading to memory changes beyond rescaling. Both theories have empirical support but the experimental designs underlying the conflicting studies are not congruent, therefore a consensus is yet to be reached. To advance this issue, we used real-time PCR and electrophysiological recordings to assess gene expression related to synaptic plasticity in the hippocampus and primary somatosensory cortex of rats exposed to novel objects, then kept awake (WK) for 60 min and finally killed after a 30 min period rich in WK, slow-wave sleep (SWS) or rapid-eye-movement sleep (REM). Animals similarly treated but not exposed to novel objects were used as controls. We found that the mRNA levels of Arc, Egr1, Fos, Ppp2ca and Ppp2r2d were significantly increased in the hippocampus of exposed animals allowed to enter REM, in comparison with control animals. Experience-dependent changes during sleep were not significant in the hippocampus for Bdnf, Camk4, Creb1, and Nr4a1, and no differences were detected between exposed and control SWS groups for any of the genes tested. No significant changes in gene expression were detected in the primary somatosensory cortex during sleep, in contrast with previous studies using longer post-stimulation intervals (>180 min). The experience-dependent induction of multiple plasticity-related genes in the hippocampus during early REM adds experimental support to the synaptic embossing theory.
publishDate 2015
dc.date.accessioned.fl_str_mv 2015-03-17T13:40:32Z
dc.date.available.fl_str_mv 2015-03-17T13:40:32Z
dc.date.issued.fl_str_mv 2015
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
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dc.identifier.citation.fl_str_mv CALAIS, Julien Braga; et al. Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep. Neurobiology of Learning and Memory. 2015. Disponível em: .Doi: 10.1016/j.nlm.2015.01.002
dc.identifier.uri.fl_str_mv https://repositorio.ufrn.br/jspui/handle/123456789/18982
dc.identifier.issn.none.fl_str_mv 1074-7427
identifier_str_mv CALAIS, Julien Braga; et al. Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep. Neurobiology of Learning and Memory. 2015. Disponível em: .Doi: 10.1016/j.nlm.2015.01.002
1074-7427
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dc.publisher.none.fl_str_mv Elsevier
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