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Emergence of Coordinated Activity in the Developing Entorhinal–Hippocampal Network

Correlated activity in the entorhinal–hippocampal neuronal networks, supported by oscillatory and intermittent population activity patterns is critical for learning and memory. However, when and how correlated activity emerges in these networks during development remains largely unknown. Here, we fo...

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Autores principales: Valeeva, Guzel, Janackova, Sona, Nasretdinov, Azat, Rychkova, Veronika, Makarov, Roman, Holmes, Gregory L, Khazipov, Roustem, Lenck-Santini, Pierre-Pascal
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6319314/
https://www.ncbi.nlm.nih.gov/pubmed/30535003
http://dx.doi.org/10.1093/cercor/bhy309
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author Valeeva, Guzel
Janackova, Sona
Nasretdinov, Azat
Rychkova, Veronika
Makarov, Roman
Holmes, Gregory L
Khazipov, Roustem
Lenck-Santini, Pierre-Pascal
author_facet Valeeva, Guzel
Janackova, Sona
Nasretdinov, Azat
Rychkova, Veronika
Makarov, Roman
Holmes, Gregory L
Khazipov, Roustem
Lenck-Santini, Pierre-Pascal
author_sort Valeeva, Guzel
collection PubMed
description Correlated activity in the entorhinal–hippocampal neuronal networks, supported by oscillatory and intermittent population activity patterns is critical for learning and memory. However, when and how correlated activity emerges in these networks during development remains largely unknown. Here, we found that during the first postnatal week in non-anaesthetized head-restrained rats, activity in the superficial layers of the medial entorhinal cortex (MEC) and hippocampus was highly correlated, with intermittent population bursts in the MEC followed by early sharp waves (eSPWs) in the hippocampus. Neurons in the superficial MEC layers fired before neurons in the dentate gyrus, CA3 and CA1. eSPW current-source density profiles indicated that perforant/temporoammonic entorhinal inputs and intrinsic hippocampal connections are co-activated during entorhinal–hippocampal activity bursts. Finally, a majority of the entorhinal–hippocampal bursts were triggered by spontaneous myoclonic body movements, characteristic of the neonatal period. Thus, during the neonatal period, activity in the entorhinal cortex (EC) and hippocampus is highly synchronous, with the EC leading hippocampal activation. We propose that such correlated activity is embedded into a large-scale bottom-up circuit that processes somatosensory feedback resulting from neonatal movements, and that it is likely to instruct the development of connections between neocortex and hippocampus.
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spelling pubmed-63193142019-01-10 Emergence of Coordinated Activity in the Developing Entorhinal–Hippocampal Network Valeeva, Guzel Janackova, Sona Nasretdinov, Azat Rychkova, Veronika Makarov, Roman Holmes, Gregory L Khazipov, Roustem Lenck-Santini, Pierre-Pascal Cereb Cortex Original Articles Correlated activity in the entorhinal–hippocampal neuronal networks, supported by oscillatory and intermittent population activity patterns is critical for learning and memory. However, when and how correlated activity emerges in these networks during development remains largely unknown. Here, we found that during the first postnatal week in non-anaesthetized head-restrained rats, activity in the superficial layers of the medial entorhinal cortex (MEC) and hippocampus was highly correlated, with intermittent population bursts in the MEC followed by early sharp waves (eSPWs) in the hippocampus. Neurons in the superficial MEC layers fired before neurons in the dentate gyrus, CA3 and CA1. eSPW current-source density profiles indicated that perforant/temporoammonic entorhinal inputs and intrinsic hippocampal connections are co-activated during entorhinal–hippocampal activity bursts. Finally, a majority of the entorhinal–hippocampal bursts were triggered by spontaneous myoclonic body movements, characteristic of the neonatal period. Thus, during the neonatal period, activity in the entorhinal cortex (EC) and hippocampus is highly synchronous, with the EC leading hippocampal activation. We propose that such correlated activity is embedded into a large-scale bottom-up circuit that processes somatosensory feedback resulting from neonatal movements, and that it is likely to instruct the development of connections between neocortex and hippocampus. Oxford University Press 2019-02 2018-12-07 /pmc/articles/PMC6319314/ /pubmed/30535003 http://dx.doi.org/10.1093/cercor/bhy309 Text en © The Author(s) 2018. Published by Oxford University Press. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Original Articles
Valeeva, Guzel
Janackova, Sona
Nasretdinov, Azat
Rychkova, Veronika
Makarov, Roman
Holmes, Gregory L
Khazipov, Roustem
Lenck-Santini, Pierre-Pascal
Emergence of Coordinated Activity in the Developing Entorhinal–Hippocampal Network
title Emergence of Coordinated Activity in the Developing Entorhinal–Hippocampal Network
title_full Emergence of Coordinated Activity in the Developing Entorhinal–Hippocampal Network
title_fullStr Emergence of Coordinated Activity in the Developing Entorhinal–Hippocampal Network
title_full_unstemmed Emergence of Coordinated Activity in the Developing Entorhinal–Hippocampal Network
title_short Emergence of Coordinated Activity in the Developing Entorhinal–Hippocampal Network
title_sort emergence of coordinated activity in the developing entorhinal–hippocampal network
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6319314/
https://www.ncbi.nlm.nih.gov/pubmed/30535003
http://dx.doi.org/10.1093/cercor/bhy309
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