Synaptic Homeostasis and Restructuring across the Sleep-Wake Cycle
Autor(a) principal: | |
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Data de Publicação: | 2015 |
Outros Autores: | , , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Institucional da UFRN |
Texto Completo: | https://repositorio.ufrn.br/jspui/handle/123456789/19073 |
Resumo: | Sleep is critical for hippocampus-dependent memory consolidation. However, the underlying mechanisms of synaptic plasticity are poorly understood. The central controversy is on whether long-term potentiation (LTP) takes a role during sleep and which would be its specific effect on memory. To address this question, we used immunohistochemistry to measure phosphorylation of Ca2+/calmodulin-dependent protein kinase II (pCaMKIIα) in the rat hippocampus immediately after specific sleep-wake states were interrupted. Control animals not exposed to novel objects during waking (WK) showed stable pCaMKIIα levels across the sleep-wake cycle, but animals exposed to novel objects showed a decrease during subsequent slow-wave sleep (SWS) followed by a rebound during rapid-eye-movement sleep (REM). The levels of pCaMKIIα during REM were proportional to cortical spindles near SWS/REM transitions. Based on these results, we modeled sleep-dependent LTP on a network of fully connected excitatory neurons fed with spikes recorded from the rat hippocampus across WK, SWS and REM. Sleep without LTP orderly rescaled synaptic weights to a narrow range of intermediate values. In contrast, LTP triggered near the SWS/REM transition led to marked swaps in synaptic weight ranking. To better understand the interaction between rescaling and restructuring during sleep, we implemented synaptic homeostasis and embossing in a detailed hippocampal-cortical model with both excitatory and inhibitory neurons. Synaptic homeostasis was implemented by weakening potentiation and strengthening depression, while synaptic embossing was simulated by evoking LTP on selected synapses. We observed that synaptic homeostasis facilitates controlled synaptic restructuring. The results imply a mechanism for a cognitive synergy between SWS and REM, and suggest that LTP at the SWS/REM transition critically influences the effect of sleep: Its lack determines synaptic homeostasis, its presence causes synaptic restructuring. |
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Blanco, WilfredoM. Pereira, CatiaR. Cota, ViniciusC. Souza, AnnieRennó-Costa, CésarSantos, SharleneDias, GabriellaGuerreiro, Ana M. G.Tort, Adriano Bretanha LopesD. Neto, AdriãoRibeiro, Sidarta Tollendal Gomes2015-06-02T13:00:26Z2015-06-02T13:00:26Z2015-05-28Blanco W, Pereira CM, Cota VR, Souza AC, Rennó-Costa C, Santos S, et al. (2015) Synaptic Homeostasis and Restructuring across the SleepWake Cycle. PLoS Comput Biol 11(5): e1004241. doi:10.1371/journal.pcbi.10042411553-734Xhttps://repositorio.ufrn.br/jspui/handle/123456789/19073Sleep is critical for hippocampus-dependent memory consolidation. However, the underlying mechanisms of synaptic plasticity are poorly understood. The central controversy is on whether long-term potentiation (LTP) takes a role during sleep and which would be its specific effect on memory. To address this question, we used immunohistochemistry to measure phosphorylation of Ca2+/calmodulin-dependent protein kinase II (pCaMKIIα) in the rat hippocampus immediately after specific sleep-wake states were interrupted. Control animals not exposed to novel objects during waking (WK) showed stable pCaMKIIα levels across the sleep-wake cycle, but animals exposed to novel objects showed a decrease during subsequent slow-wave sleep (SWS) followed by a rebound during rapid-eye-movement sleep (REM). The levels of pCaMKIIα during REM were proportional to cortical spindles near SWS/REM transitions. Based on these results, we modeled sleep-dependent LTP on a network of fully connected excitatory neurons fed with spikes recorded from the rat hippocampus across WK, SWS and REM. Sleep without LTP orderly rescaled synaptic weights to a narrow range of intermediate values. In contrast, LTP triggered near the SWS/REM transition led to marked swaps in synaptic weight ranking. To better understand the interaction between rescaling and restructuring during sleep, we implemented synaptic homeostasis and embossing in a detailed hippocampal-cortical model with both excitatory and inhibitory neurons. Synaptic homeostasis was implemented by weakening potentiation and strengthening depression, while synaptic embossing was simulated by evoking LTP on selected synapses. We observed that synaptic homeostasis facilitates controlled synaptic restructuring. The results imply a mechanism for a cognitive synergy between SWS and REM, and suggest that LTP at the SWS/REM transition critically influences the effect of sleep: Its lack determines synaptic homeostasis, its presence causes synaptic restructuring.: Support obtained from Financiadora de Estudos e Projetos (http://www.finep.gov.br/) Grant # 01.06.1092.00 to SR; Conselho Nacional de Desenvolvimento Científico e Tecnológico (http:// www.cnpq.br/): Grants 481506/2007-1, 481351/2011- 6 and 306604/2012-4 to SR, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (http://www.capes.gov.br/) and Ciencias sem Fronteiras (http://www.cienciasemfronteiras.gov.br/ web/csf/home) to AT and CRC; Fundação de Amparo à Pesquisa do Rio Grande do Norte (http://wwwfapern.rn.gov.br/): Grant Pronem 003/2011 to SR; Fundação de Amparo à Pesquisa do Estado de São Paulo (http://www.fapesp.br/): Grant #2013/ 07699-0 - Center for Neuromathematics to SR; CMP and VRC supported by post-doctoral fellowships from Fundação de Amparo à Pesquisa do Rio Grande do Norte /CNPq. Additional support obtained from the Federal University of Rio Grande do Norte (www.ufrn. br); Ministry of Science, Technology and Innovation (http://www.mcti.gov.br/); Associação Alberto Santos Dumont de Apoio à Pesquisa (http://natalneuro.com/ associacao/index.asp); Pew Latin American Fellows Program (http://www.pewtrusts.org/en/projects/pewlatin-american-fellows/) to SR; Informatics Department of the Instituto Federal de Educação, Ciência e Tecnologia do Rio Grande do Norte (http:// portal.ifrn.edu.br/) to WB. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscriptAldo A Faisal, Imperial College London, UNITED KINGDOMSynaptic HomeostasisSleep-Wake CycleSynaptic Homeostasis and Restructuring across the Sleep-Wake Cycleinfo: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/openAccessORIGINALSidartaRibeiro_ICE_Synaptic_Homeostasis_2015.pdfSidartaRibeiro_ICE_Synaptic_Homeostasis_2015.pdfArtigo completoapplication/pdf9825563https://repositorio.ufrn.br/bitstream/123456789/19073/1/SidartaRibeiro_ICE_Synaptic_Homeostasis_2015.pdf69bb141ae2f398be43ab00538ceb2c42MD51LICENSElicense.txtlicense.txttext/plain; charset=utf-81563https://repositorio.ufrn.br/bitstream/123456789/19073/2/license.txt2fca3d993fd069474a9dfb5156c39499MD52TEXTSidartaRibeiro_ICE_Synaptic_Homeostasis_2015.pdf.txtSidartaRibeiro_ICE_Synaptic_Homeostasis_2015.pdf.txtExtracted texttext/plain94056https://repositorio.ufrn.br/bitstream/123456789/19073/7/SidartaRibeiro_ICE_Synaptic_Homeostasis_2015.pdf.txt2a11bbbbd32eb0aa2cc5075113d60df1MD57THUMBNAILSidartaRibeiro_ICE_Synaptic_Homeostasis_2015.pdf.jpgSidartaRibeiro_ICE_Synaptic_Homeostasis_2015.pdf.jpgIM Thumbnailimage/jpeg12079https://repositorio.ufrn.br/bitstream/123456789/19073/8/SidartaRibeiro_ICE_Synaptic_Homeostasis_2015.pdf.jpg356427009ab5e8e77ee4523eb032acb4MD58123456789/190732021-07-10 19:11:23.4oai:https://repositorio.ufrn.br:123456789/19073TElDRU7Dh0EgREUgRElTVFJJQlVJw4fDg08gTsODTy1FWENMVVNJVkEKCkFvIGFzc2luYXIgZSBlbnRyZWdhciBlc3RhIGxpY2Vuw6dhLCBvL2EgU3IuL1NyYS4gKGF1dG9yIG91IGRldGVudG9yIGRvcyBkaXJlaXRvcyBkZSBhdXRvcik6CgphKSBDb25jZWRlIMOgIFVuaXZlcnNpZGFkZSBGZWRlcmFsIGRvIFJpbyBHcmFuZGUgZG8gTm9ydGUgbyBkaXJlaXRvIG7Do28tZXhjbHVzaXZvIGRlCnJlcHJvZHV6aXIsIGNvbnZlcnRlciAoY29tbyBkZWZpbmlkbyBhYmFpeG8pLCBjb211bmljYXIgZS9vdQpkaXN0cmlidWlyIG8gZG9jdW1lbnRvIGVudHJlZ3VlIChpbmNsdWluZG8gbyByZXN1bW8vYWJzdHJhY3QpIGVtCmZvcm1hdG8gZGlnaXRhbCBvdSBpbXByZXNzbyBlIGVtIHF1YWxxdWVyIG1laW8uCgpiKSBEZWNsYXJhIHF1ZSBvIGRvY3VtZW50byBlbnRyZWd1ZSDDqSBzZXUgdHJhYmFsaG8gb3JpZ2luYWwsIGUgcXVlCmRldMOpbSBvIGRpcmVpdG8gZGUgY29uY2VkZXIgb3MgZGlyZWl0b3MgY29udGlkb3MgbmVzdGEgbGljZW7Dp2EuIERlY2xhcmEKdGFtYsOpbSBxdWUgYSBlbnRyZWdhIGRvIGRvY3VtZW50byBuw6NvIGluZnJpbmdlLCB0YW50byBxdWFudG8gbGhlIMOpCnBvc3PDrXZlbCBzYWJlciwgb3MgZGlyZWl0b3MgZGUgcXVhbHF1ZXIgb3V0cmEgcGVzc29hIG91IGVudGlkYWRlLgoKYykgU2UgbyBkb2N1bWVudG8gZW50cmVndWUgY29udMOpbSBtYXRlcmlhbCBkbyBxdWFsIG7Do28gZGV0w6ltIG9zCmRpcmVpdG9zIGRlIGF1dG9yLCBkZWNsYXJhIHF1ZSBvYnRldmUgYXV0b3JpemHDp8OjbyBkbyBkZXRlbnRvciBkb3MKZGlyZWl0b3MgZGUgYXV0b3IgcGFyYSBjb25jZWRlciDDoCBVbml2ZXJzaWRhZGUgRmVkZXJhbCBkbyBSaW8gR3JhbmRlIGRvIE5vcnRlIG9zIGRpcmVpdG9zIHJlcXVlcmlkb3MgcG9yIGVzdGEgbGljZW7Dp2EsIGUgcXVlIGVzc2UgbWF0ZXJpYWwgY3Vqb3MgZGlyZWl0b3Mgc8OjbyBkZQp0ZXJjZWlyb3MgZXN0w6EgY2xhcmFtZW50ZSBpZGVudGlmaWNhZG8gZSByZWNvbmhlY2lkbyBubyB0ZXh0byBvdQpjb250ZcO6ZG8gZG8gZG9jdW1lbnRvIGVudHJlZ3VlLgoKU2UgbyBkb2N1bWVudG8gZW50cmVndWUgw6kgYmFzZWFkbyBlbSB0cmFiYWxobyBmaW5hbmNpYWRvIG91IGFwb2lhZG8KcG9yIG91dHJhIGluc3RpdHVpw6fDo28gcXVlIG7Do28gYSBVbml2ZXJzaWRhZGUgRmVkZXJhbCBkbyBSaW8gR3JhbmRlIGRvIE5vcnRlLCBkZWNsYXJhIHF1ZSBjdW1wcml1IHF1YWlzcXVlciBvYnJpZ2HDp8O1ZXMgZXhpZ2lkYXMgcGVsbyByZXNwZWN0aXZvIGNvbnRyYXRvIG91IGFjb3Jkby4KCkEgVW5pdmVyc2lkYWRlIEZlZGVyYWwgZG8gUmlvIEdyYW5kZSBkbyBOb3J0ZSAgaWRlbnRpZmljYXLDoSBjbGFyYW1lbnRlIG8ocykgc2V1IChzKSBub21lKHMpIGNvbW8gbyAocykgYXV0b3IgKGVzKSBvdSBkZXRlbnRvciAoZXMpIGRvcyBkaXJlaXRvcyBkbyBkb2N1bWVudG8KZW50cmVndWUsIGUgbsOjbyBmYXLDoSBxdWFscXVlciBhbHRlcmHDp8OjbywgcGFyYSBhbMOpbSBkYXMgcGVybWl0aWRhcyBwb3IKZXN0YSBsaWNlbsOnYS4KRepositório de PublicaçõesPUBhttp://repositorio.ufrn.br/oai/opendoar:2021-07-10T22:11:23Repositório Institucional da UFRN - Universidade Federal do Rio Grande do Norte (UFRN)false |
dc.title.pt_BR.fl_str_mv |
Synaptic Homeostasis and Restructuring across the Sleep-Wake Cycle |
title |
Synaptic Homeostasis and Restructuring across the Sleep-Wake Cycle |
spellingShingle |
Synaptic Homeostasis and Restructuring across the Sleep-Wake Cycle Blanco, Wilfredo Synaptic Homeostasis Sleep-Wake Cycle |
title_short |
Synaptic Homeostasis and Restructuring across the Sleep-Wake Cycle |
title_full |
Synaptic Homeostasis and Restructuring across the Sleep-Wake Cycle |
title_fullStr |
Synaptic Homeostasis and Restructuring across the Sleep-Wake Cycle |
title_full_unstemmed |
Synaptic Homeostasis and Restructuring across the Sleep-Wake Cycle |
title_sort |
Synaptic Homeostasis and Restructuring across the Sleep-Wake Cycle |
author |
Blanco, Wilfredo |
author_facet |
Blanco, Wilfredo M. Pereira, Catia R. Cota, Vinicius C. Souza, Annie Rennó-Costa, César Santos, Sharlene Dias, Gabriella Guerreiro, Ana M. G. Tort, Adriano Bretanha Lopes D. Neto, Adrião Ribeiro, Sidarta Tollendal Gomes |
author_role |
author |
author2 |
M. Pereira, Catia R. Cota, Vinicius C. Souza, Annie Rennó-Costa, César Santos, Sharlene Dias, Gabriella Guerreiro, Ana M. G. Tort, Adriano Bretanha Lopes D. Neto, Adrião Ribeiro, Sidarta Tollendal Gomes |
author2_role |
author author author author author author author author author author |
dc.contributor.author.fl_str_mv |
Blanco, Wilfredo M. Pereira, Catia R. Cota, Vinicius C. Souza, Annie Rennó-Costa, César Santos, Sharlene Dias, Gabriella Guerreiro, Ana M. G. Tort, Adriano Bretanha Lopes D. Neto, Adrião Ribeiro, Sidarta Tollendal Gomes |
dc.subject.por.fl_str_mv |
Synaptic Homeostasis Sleep-Wake Cycle |
topic |
Synaptic Homeostasis Sleep-Wake Cycle |
description |
Sleep is critical for hippocampus-dependent memory consolidation. However, the underlying mechanisms of synaptic plasticity are poorly understood. The central controversy is on whether long-term potentiation (LTP) takes a role during sleep and which would be its specific effect on memory. To address this question, we used immunohistochemistry to measure phosphorylation of Ca2+/calmodulin-dependent protein kinase II (pCaMKIIα) in the rat hippocampus immediately after specific sleep-wake states were interrupted. Control animals not exposed to novel objects during waking (WK) showed stable pCaMKIIα levels across the sleep-wake cycle, but animals exposed to novel objects showed a decrease during subsequent slow-wave sleep (SWS) followed by a rebound during rapid-eye-movement sleep (REM). The levels of pCaMKIIα during REM were proportional to cortical spindles near SWS/REM transitions. Based on these results, we modeled sleep-dependent LTP on a network of fully connected excitatory neurons fed with spikes recorded from the rat hippocampus across WK, SWS and REM. Sleep without LTP orderly rescaled synaptic weights to a narrow range of intermediate values. In contrast, LTP triggered near the SWS/REM transition led to marked swaps in synaptic weight ranking. To better understand the interaction between rescaling and restructuring during sleep, we implemented synaptic homeostasis and embossing in a detailed hippocampal-cortical model with both excitatory and inhibitory neurons. Synaptic homeostasis was implemented by weakening potentiation and strengthening depression, while synaptic embossing was simulated by evoking LTP on selected synapses. We observed that synaptic homeostasis facilitates controlled synaptic restructuring. The results imply a mechanism for a cognitive synergy between SWS and REM, and suggest that LTP at the SWS/REM transition critically influences the effect of sleep: Its lack determines synaptic homeostasis, its presence causes synaptic restructuring. |
publishDate |
2015 |
dc.date.accessioned.fl_str_mv |
2015-06-02T13:00:26Z |
dc.date.available.fl_str_mv |
2015-06-02T13:00:26Z |
dc.date.issued.fl_str_mv |
2015-05-28 |
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.citation.fl_str_mv |
Blanco W, Pereira CM, Cota VR, Souza AC, Rennó-Costa C, Santos S, et al. (2015) Synaptic Homeostasis and Restructuring across the SleepWake Cycle. PLoS Comput Biol 11(5): e1004241. doi:10.1371/journal.pcbi.1004241 |
dc.identifier.uri.fl_str_mv |
https://repositorio.ufrn.br/jspui/handle/123456789/19073 |
dc.identifier.issn.none.fl_str_mv |
1553-734X |
identifier_str_mv |
Blanco W, Pereira CM, Cota VR, Souza AC, Rennó-Costa C, Santos S, et al. (2015) Synaptic Homeostasis and Restructuring across the SleepWake Cycle. PLoS Comput Biol 11(5): e1004241. doi:10.1371/journal.pcbi.1004241 1553-734X |
url |
https://repositorio.ufrn.br/jspui/handle/123456789/19073 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
dc.publisher.none.fl_str_mv |
Aldo A Faisal, Imperial College London, UNITED KINGDOM |
publisher.none.fl_str_mv |
Aldo A Faisal, Imperial College London, UNITED KINGDOM |
dc.source.none.fl_str_mv |
reponame:Repositório Institucional da UFRN instname:Universidade Federal do Rio Grande do Norte (UFRN) instacron:UFRN |
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Universidade Federal do Rio Grande do Norte (UFRN) |
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UFRN |
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UFRN |
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Repositório Institucional da UFRN |
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Repositório Institucional da UFRN |
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