Hippocampus-retrosplenial cortex interaction is increased during phasic REM and contributes to memory consolidation

Abstract Hippocampal (HPC) theta oscillation during post-training rapid eye movement (REM) sleep supports spatial learning. Theta also modulates neuronal and oscillatory activity in the retrosplenial cortex (RSC) during REM sleep. To investigate the relevance of theta-driven interaction between thes...

Full description

Bibliographic Details
Main Authors: Daniel Gomes de Almeida-Filho, Bruna Del Vechio Koike, Francesca Billwiller, Kelly Soares Farias, Igor Rafael Praxedes de Sales, Pierre-Hervé Luppi, Sidarta Ribeiro, Claudio Marcos Queiroz
Format: Article
Language:English
Published: Nature Portfolio 2021-06-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-91659-5
_version_ 1818844990898438144
author Daniel Gomes de Almeida-Filho
Bruna Del Vechio Koike
Francesca Billwiller
Kelly Soares Farias
Igor Rafael Praxedes de Sales
Pierre-Hervé Luppi
Sidarta Ribeiro
Claudio Marcos Queiroz
author_facet Daniel Gomes de Almeida-Filho
Bruna Del Vechio Koike
Francesca Billwiller
Kelly Soares Farias
Igor Rafael Praxedes de Sales
Pierre-Hervé Luppi
Sidarta Ribeiro
Claudio Marcos Queiroz
author_sort Daniel Gomes de Almeida-Filho
collection DOAJ
description Abstract Hippocampal (HPC) theta oscillation during post-training rapid eye movement (REM) sleep supports spatial learning. Theta also modulates neuronal and oscillatory activity in the retrosplenial cortex (RSC) during REM sleep. To investigate the relevance of theta-driven interaction between these two regions to memory consolidation, we computed the Granger causality within theta range on electrophysiological data recorded in freely behaving rats during REM sleep, both before and after contextual fear conditioning. We found a training-induced modulation of causality between HPC and RSC that was correlated with memory retrieval 24 h later. Retrieval was proportional to the change in the relative influence RSC exerted upon HPC theta oscillation. Importantly, causality peaked during theta acceleration, in synchrony with phasic REM sleep. Altogether, these results support a role for phasic REM sleep in hippocampo-cortical memory consolidation and suggest that causality modulation between RSC and HPC during REM sleep plays a functional role in that phenomenon.
first_indexed 2024-12-19T05:22:33Z
format Article
id doaj.art-ed298cbeaf4e4392add1a42be5f98fa9
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-12-19T05:22:33Z
publishDate 2021-06-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-ed298cbeaf4e4392add1a42be5f98fa92022-12-21T20:34:28ZengNature PortfolioScientific Reports2045-23222021-06-0111111410.1038/s41598-021-91659-5Hippocampus-retrosplenial cortex interaction is increased during phasic REM and contributes to memory consolidationDaniel Gomes de Almeida-Filho0Bruna Del Vechio Koike1Francesca Billwiller2Kelly Soares Farias3Igor Rafael Praxedes de Sales4Pierre-Hervé Luppi5Sidarta Ribeiro6Claudio Marcos Queiroz7Brain Institute, Federal University of Rio Grande do NorteBrain Institute, Federal University of Rio Grande do NorteUMR 5292 CNRS/U1028 INSERM, Center of Research in Neuroscience of Lyon, SLEEP Team, Université Claude Bernard Lyon I, Faculté de Médecine RTH LaennecBrain Institute, Federal University of Rio Grande do NorteBrain Institute, Federal University of Rio Grande do NorteUMR 5292 CNRS/U1028 INSERM, Center of Research in Neuroscience of Lyon, SLEEP Team, Université Claude Bernard Lyon I, Faculté de Médecine RTH LaennecBrain Institute, Federal University of Rio Grande do NorteBrain Institute, Federal University of Rio Grande do NorteAbstract Hippocampal (HPC) theta oscillation during post-training rapid eye movement (REM) sleep supports spatial learning. Theta also modulates neuronal and oscillatory activity in the retrosplenial cortex (RSC) during REM sleep. To investigate the relevance of theta-driven interaction between these two regions to memory consolidation, we computed the Granger causality within theta range on electrophysiological data recorded in freely behaving rats during REM sleep, both before and after contextual fear conditioning. We found a training-induced modulation of causality between HPC and RSC that was correlated with memory retrieval 24 h later. Retrieval was proportional to the change in the relative influence RSC exerted upon HPC theta oscillation. Importantly, causality peaked during theta acceleration, in synchrony with phasic REM sleep. Altogether, these results support a role for phasic REM sleep in hippocampo-cortical memory consolidation and suggest that causality modulation between RSC and HPC during REM sleep plays a functional role in that phenomenon.https://doi.org/10.1038/s41598-021-91659-5
spellingShingle Daniel Gomes de Almeida-Filho
Bruna Del Vechio Koike
Francesca Billwiller
Kelly Soares Farias
Igor Rafael Praxedes de Sales
Pierre-Hervé Luppi
Sidarta Ribeiro
Claudio Marcos Queiroz
Hippocampus-retrosplenial cortex interaction is increased during phasic REM and contributes to memory consolidation
Scientific Reports
title Hippocampus-retrosplenial cortex interaction is increased during phasic REM and contributes to memory consolidation
title_full Hippocampus-retrosplenial cortex interaction is increased during phasic REM and contributes to memory consolidation
title_fullStr Hippocampus-retrosplenial cortex interaction is increased during phasic REM and contributes to memory consolidation
title_full_unstemmed Hippocampus-retrosplenial cortex interaction is increased during phasic REM and contributes to memory consolidation
title_short Hippocampus-retrosplenial cortex interaction is increased during phasic REM and contributes to memory consolidation
title_sort hippocampus retrosplenial cortex interaction is increased during phasic rem and contributes to memory consolidation
url https://doi.org/10.1038/s41598-021-91659-5
work_keys_str_mv AT danielgomesdealmeidafilho hippocampusretrosplenialcortexinteractionisincreasedduringphasicremandcontributestomemoryconsolidation
AT brunadelvechiokoike hippocampusretrosplenialcortexinteractionisincreasedduringphasicremandcontributestomemoryconsolidation
AT francescabillwiller hippocampusretrosplenialcortexinteractionisincreasedduringphasicremandcontributestomemoryconsolidation
AT kellysoaresfarias hippocampusretrosplenialcortexinteractionisincreasedduringphasicremandcontributestomemoryconsolidation
AT igorrafaelpraxedesdesales hippocampusretrosplenialcortexinteractionisincreasedduringphasicremandcontributestomemoryconsolidation
AT pierreherveluppi hippocampusretrosplenialcortexinteractionisincreasedduringphasicremandcontributestomemoryconsolidation
AT sidartaribeiro hippocampusretrosplenialcortexinteractionisincreasedduringphasicremandcontributestomemoryconsolidation
AT claudiomarcosqueiroz hippocampusretrosplenialcortexinteractionisincreasedduringphasicremandcontributestomemoryconsolidation