Theta-phase modulates different high-frequency oscillations in the CA1 region of the hippocampus during both waking and rapid-eye movement sleep.

Detalhes bibliográficos
Autor(a) principal: Teixeira, Robson Scheffer
Data de Publicação: 2010
Outros Autores: Souza, Bryan C., Belchior, Hindiael, Ribeiro, Sidarta Tollendal Gomes, Tort, Adriano Bretanha Lopes
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UFRN
Texto Completo: https://repositorio.ufrn.br/jspui/handle/123456789/24051
Resumo: Recent evidence suggests that not only the brain rhythms per se, but also the interactions among them are involved in the execution of cognitive tasks, mainly those requiring selective attention, information transmission and memory consolidation. However, still little is known about the general characteristics of cross-frequency coupling (CFC) in several brain regions. In the present work, we aimed to characterize phase-amplitude CFC in the CA1 region of rats (n=9) during different stages of the sleep-wake cycle: wake (WK), slow-wave sleep (SWS), and rapid-eye movement sleep (REM). Local field potentials were recorded using multielectrode arrays implanted in the dorsal hippocampus for chronic neural recordings. Electrode positioning was verified by histological analysis of cresyl-stained brain sections. Phase-amplitude coupling was assessed by means of the comodulogram analysis, a CFC tool we have recently developed. Our results show that (1) each sleep-wake state contains characteristic patterns of phase-amplitude CFC that are robust across all animals studied. (2) The CFC patterns obtained during WK and REM are similar and characterized by theta-phase (5 – 10 Hz) modulation of multiple higher frequencies; on the other hand, comodulograms from SWS period exhibited a distinct pattern, characterized by the modulation of very fast oscillations (> 100 Hz) by delta-phase (0 – 4 Hz), consistent with the occurrence of sharp wave-ripple complexes. All these patterns were stable across electrodes and days. Interestingly, during WK and REM, our results indicate that (3) theta-phase modulation comprises two non-overlapping, circumscribed higher frequency ranges: oscillations in the high-gamma (HG, 60 – 100 Hz) frequency range and oscillations between 120 – 160 Hz, which were defined as high-frequency oscillations (HFO). Moreover, (4) theta-phase preferentially modulated more HG or HFO depending on the spatial position of the electrode, with a clear switching between one and another as a function of electrode location, which was also stable across days. Further analyses indicated that (5) electrodes exhibiting HG or HFO modulation during WK and REM can also be differentiated by other electrophysiological features, such as power spectrum, phase-relations, and SWS comodulograms. We argue that the HFO we observed, though presenting overlapping frequency range with ripple oscillations, are distinct from the latter, which only appear in periods of rest and sleep associated to sharp-wave complexes. Therefore, while characterizing the patterns of rhythmic interactions in different cognitive states, the present work also reveals novel hippocampal oscillations that could only be detected by the use of the new CFC tools. We speculate that the different amplitude-modulated bands correspond to different biophysical processes occurring in CA1: HFO would result from entorhinal synaptic inputs to CA1, and HG from CA3 inputs.
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spelling Teixeira, Robson SchefferSouza, Bryan C.Belchior, HindiaelRibeiro, Sidarta Tollendal GomesTort, Adriano Bretanha Lopes2017-10-13T13:27:42Z2017-10-13T13:27:42Z2010-09https://repositorio.ufrn.br/jspui/handle/123456789/24051engComodulogramHigh frequency oscillationHippocampusThetaTheta-phase modulates different high-frequency oscillations in the CA1 region of the hippocampus during both waking and rapid-eye movement sleep.info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleRecent evidence suggests that not only the brain rhythms per se, but also the interactions among them are involved in the execution of cognitive tasks, mainly those requiring selective attention, information transmission and memory consolidation. However, still little is known about the general characteristics of cross-frequency coupling (CFC) in several brain regions. In the present work, we aimed to characterize phase-amplitude CFC in the CA1 region of rats (n=9) during different stages of the sleep-wake cycle: wake (WK), slow-wave sleep (SWS), and rapid-eye movement sleep (REM). Local field potentials were recorded using multielectrode arrays implanted in the dorsal hippocampus for chronic neural recordings. Electrode positioning was verified by histological analysis of cresyl-stained brain sections. Phase-amplitude coupling was assessed by means of the comodulogram analysis, a CFC tool we have recently developed. Our results show that (1) each sleep-wake state contains characteristic patterns of phase-amplitude CFC that are robust across all animals studied. (2) The CFC patterns obtained during WK and REM are similar and characterized by theta-phase (5 – 10 Hz) modulation of multiple higher frequencies; on the other hand, comodulograms from SWS period exhibited a distinct pattern, characterized by the modulation of very fast oscillations (> 100 Hz) by delta-phase (0 – 4 Hz), consistent with the occurrence of sharp wave-ripple complexes. All these patterns were stable across electrodes and days. Interestingly, during WK and REM, our results indicate that (3) theta-phase modulation comprises two non-overlapping, circumscribed higher frequency ranges: oscillations in the high-gamma (HG, 60 – 100 Hz) frequency range and oscillations between 120 – 160 Hz, which were defined as high-frequency oscillations (HFO). Moreover, (4) theta-phase preferentially modulated more HG or HFO depending on the spatial position of the electrode, with a clear switching between one and another as a function of electrode location, which was also stable across days. Further analyses indicated that (5) electrodes exhibiting HG or HFO modulation during WK and REM can also be differentiated by other electrophysiological features, such as power spectrum, phase-relations, and SWS comodulograms. We argue that the HFO we observed, though presenting overlapping frequency range with ripple oscillations, are distinct from the latter, which only appear in periods of rest and sleep associated to sharp-wave complexes. Therefore, while characterizing the patterns of rhythmic interactions in different cognitive states, the present work also reveals novel hippocampal oscillations that could only be detected by the use of the new CFC tools. We speculate that the different amplitude-modulated bands correspond to different biophysical processes occurring in CA1: HFO would result from entorhinal synaptic inputs to CA1, and HG from CA3 inputs.info:eu-repo/semantics/openAccessreponame:Repositório Institucional da UFRNinstname:Universidade Federal do Rio Grande do Norte (UFRN)instacron:UFRNORIGINALSBNeC 2010_theta-phase modulates.pdfSBNeC 2010_theta-phase modulates.pdfapplication/pdf134375https://repositorio.ufrn.br/bitstream/123456789/24051/1/SBNeC%202010_theta-phase%20modulates.pdf72a26ef654ce2546f70beedb72bf6361MD51LICENSElicense.txtlicense.txttext/plain; charset=utf-81748https://repositorio.ufrn.br/bitstream/123456789/24051/2/license.txt8a4605be74aa9ea9d79846c1fba20a33MD52TEXTSBNeC 2010_theta-phase modulates.pdf.txtSBNeC 2010_theta-phase modulates.pdf.txtExtracted texttext/plain3774https://repositorio.ufrn.br/bitstream/123456789/24051/5/SBNeC%202010_theta-phase%20modulates.pdf.txt044d909f253cc92d286cd9b3552ec5fcMD55THUMBNAILSBNeC 2010_theta-phase modulates.pdf.jpgSBNeC 2010_theta-phase modulates.pdf.jpgIM Thumbnailimage/jpeg5932https://repositorio.ufrn.br/bitstream/123456789/24051/6/SBNeC%202010_theta-phase%20modulates.pdf.jpg035d5fd6a072977afc00e2494e9a278eMD56123456789/240512017-11-04 20:48:39.875oai:https://repositorio.ufrn.br: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Repositório de PublicaçõesPUBhttp://repositorio.ufrn.br/oai/opendoar:2017-11-04T23:48:39Repositório Institucional da UFRN - Universidade Federal do Rio Grande do Norte (UFRN)false
dc.title.pt_BR.fl_str_mv Theta-phase modulates different high-frequency oscillations in the CA1 region of the hippocampus during both waking and rapid-eye movement sleep.
title Theta-phase modulates different high-frequency oscillations in the CA1 region of the hippocampus during both waking and rapid-eye movement sleep.
spellingShingle Theta-phase modulates different high-frequency oscillations in the CA1 region of the hippocampus during both waking and rapid-eye movement sleep.
Teixeira, Robson Scheffer
Comodulogram
High frequency oscillation
Hippocampus
Theta
title_short Theta-phase modulates different high-frequency oscillations in the CA1 region of the hippocampus during both waking and rapid-eye movement sleep.
title_full Theta-phase modulates different high-frequency oscillations in the CA1 region of the hippocampus during both waking and rapid-eye movement sleep.
title_fullStr Theta-phase modulates different high-frequency oscillations in the CA1 region of the hippocampus during both waking and rapid-eye movement sleep.
title_full_unstemmed Theta-phase modulates different high-frequency oscillations in the CA1 region of the hippocampus during both waking and rapid-eye movement sleep.
title_sort Theta-phase modulates different high-frequency oscillations in the CA1 region of the hippocampus during both waking and rapid-eye movement sleep.
author Teixeira, Robson Scheffer
author_facet Teixeira, Robson Scheffer
Souza, Bryan C.
Belchior, Hindiael
Ribeiro, Sidarta Tollendal Gomes
Tort, Adriano Bretanha Lopes
author_role author
author2 Souza, Bryan C.
Belchior, Hindiael
Ribeiro, Sidarta Tollendal Gomes
Tort, Adriano Bretanha Lopes
author2_role author
author
author
author
dc.contributor.author.fl_str_mv Teixeira, Robson Scheffer
Souza, Bryan C.
Belchior, Hindiael
Ribeiro, Sidarta Tollendal Gomes
Tort, Adriano Bretanha Lopes
dc.subject.por.fl_str_mv Comodulogram
High frequency oscillation
Hippocampus
Theta
topic Comodulogram
High frequency oscillation
Hippocampus
Theta
description Recent evidence suggests that not only the brain rhythms per se, but also the interactions among them are involved in the execution of cognitive tasks, mainly those requiring selective attention, information transmission and memory consolidation. However, still little is known about the general characteristics of cross-frequency coupling (CFC) in several brain regions. In the present work, we aimed to characterize phase-amplitude CFC in the CA1 region of rats (n=9) during different stages of the sleep-wake cycle: wake (WK), slow-wave sleep (SWS), and rapid-eye movement sleep (REM). Local field potentials were recorded using multielectrode arrays implanted in the dorsal hippocampus for chronic neural recordings. Electrode positioning was verified by histological analysis of cresyl-stained brain sections. Phase-amplitude coupling was assessed by means of the comodulogram analysis, a CFC tool we have recently developed. Our results show that (1) each sleep-wake state contains characteristic patterns of phase-amplitude CFC that are robust across all animals studied. (2) The CFC patterns obtained during WK and REM are similar and characterized by theta-phase (5 – 10 Hz) modulation of multiple higher frequencies; on the other hand, comodulograms from SWS period exhibited a distinct pattern, characterized by the modulation of very fast oscillations (> 100 Hz) by delta-phase (0 – 4 Hz), consistent with the occurrence of sharp wave-ripple complexes. All these patterns were stable across electrodes and days. Interestingly, during WK and REM, our results indicate that (3) theta-phase modulation comprises two non-overlapping, circumscribed higher frequency ranges: oscillations in the high-gamma (HG, 60 – 100 Hz) frequency range and oscillations between 120 – 160 Hz, which were defined as high-frequency oscillations (HFO). Moreover, (4) theta-phase preferentially modulated more HG or HFO depending on the spatial position of the electrode, with a clear switching between one and another as a function of electrode location, which was also stable across days. Further analyses indicated that (5) electrodes exhibiting HG or HFO modulation during WK and REM can also be differentiated by other electrophysiological features, such as power spectrum, phase-relations, and SWS comodulograms. We argue that the HFO we observed, though presenting overlapping frequency range with ripple oscillations, are distinct from the latter, which only appear in periods of rest and sleep associated to sharp-wave complexes. Therefore, while characterizing the patterns of rhythmic interactions in different cognitive states, the present work also reveals novel hippocampal oscillations that could only be detected by the use of the new CFC tools. We speculate that the different amplitude-modulated bands correspond to different biophysical processes occurring in CA1: HFO would result from entorhinal synaptic inputs to CA1, and HG from CA3 inputs.
publishDate 2010
dc.date.issued.fl_str_mv 2010-09
dc.date.accessioned.fl_str_mv 2017-10-13T13:27:42Z
dc.date.available.fl_str_mv 2017-10-13T13:27:42Z
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