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Coordinated electrical activity in the olfactory bulb gates the oscillatory entrainment of entorhinal networks in neonatal mice

Although the developmental principles of sensory and cognitive processing have been extensively investigated, their synergy has been largely neglected. During early life, most sensory systems are still largely immature. As a notable exception, the olfactory system is functional at birth, controlling...

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Autores principales: Gretenkord, Sabine, Kostka, Johanna K., Hartung, Henrike, Watznauer, Katja, Fleck, David, Minier-Toribio, Angélica, Spehr, Marc, Hanganu-Opatz, Ileana L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6354964/
https://www.ncbi.nlm.nih.gov/pubmed/30703080
http://dx.doi.org/10.1371/journal.pbio.2006994
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author Gretenkord, Sabine
Kostka, Johanna K.
Hartung, Henrike
Watznauer, Katja
Fleck, David
Minier-Toribio, Angélica
Spehr, Marc
Hanganu-Opatz, Ileana L.
author_facet Gretenkord, Sabine
Kostka, Johanna K.
Hartung, Henrike
Watznauer, Katja
Fleck, David
Minier-Toribio, Angélica
Spehr, Marc
Hanganu-Opatz, Ileana L.
author_sort Gretenkord, Sabine
collection PubMed
description Although the developmental principles of sensory and cognitive processing have been extensively investigated, their synergy has been largely neglected. During early life, most sensory systems are still largely immature. As a notable exception, the olfactory system is functional at birth, controlling mother–offspring interactions and neonatal survival. Here, we elucidate the structural and functional principles underlying the communication between olfactory bulb (OB) and lateral entorhinal cortex (LEC)—the gatekeeper of limbic circuitry—during neonatal development. Combining optogenetics, pharmacology, and electrophysiology in vivo with axonal tracing, we show that mitral cell–dependent discontinuous theta bursts in OB drive network oscillations and time the firing in LEC of anesthetized mice via axonal projections confined to upper cortical layers. Acute pharmacological silencing of OB activity diminishes entorhinal oscillations, whereas odor exposure boosts OB–entorhinal coupling at fast frequencies. Chronic impairment of olfactory sensory neurons disrupts OB–entorhinal activity. Thus, OB activity shapes the maturation of entorhinal circuits.
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spelling pubmed-63549642019-02-15 Coordinated electrical activity in the olfactory bulb gates the oscillatory entrainment of entorhinal networks in neonatal mice Gretenkord, Sabine Kostka, Johanna K. Hartung, Henrike Watznauer, Katja Fleck, David Minier-Toribio, Angélica Spehr, Marc Hanganu-Opatz, Ileana L. PLoS Biol Research Article Although the developmental principles of sensory and cognitive processing have been extensively investigated, their synergy has been largely neglected. During early life, most sensory systems are still largely immature. As a notable exception, the olfactory system is functional at birth, controlling mother–offspring interactions and neonatal survival. Here, we elucidate the structural and functional principles underlying the communication between olfactory bulb (OB) and lateral entorhinal cortex (LEC)—the gatekeeper of limbic circuitry—during neonatal development. Combining optogenetics, pharmacology, and electrophysiology in vivo with axonal tracing, we show that mitral cell–dependent discontinuous theta bursts in OB drive network oscillations and time the firing in LEC of anesthetized mice via axonal projections confined to upper cortical layers. Acute pharmacological silencing of OB activity diminishes entorhinal oscillations, whereas odor exposure boosts OB–entorhinal coupling at fast frequencies. Chronic impairment of olfactory sensory neurons disrupts OB–entorhinal activity. Thus, OB activity shapes the maturation of entorhinal circuits. Public Library of Science 2019-01-31 /pmc/articles/PMC6354964/ /pubmed/30703080 http://dx.doi.org/10.1371/journal.pbio.2006994 Text en © 2019 Gretenkord et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Gretenkord, Sabine
Kostka, Johanna K.
Hartung, Henrike
Watznauer, Katja
Fleck, David
Minier-Toribio, Angélica
Spehr, Marc
Hanganu-Opatz, Ileana L.
Coordinated electrical activity in the olfactory bulb gates the oscillatory entrainment of entorhinal networks in neonatal mice
title Coordinated electrical activity in the olfactory bulb gates the oscillatory entrainment of entorhinal networks in neonatal mice
title_full Coordinated electrical activity in the olfactory bulb gates the oscillatory entrainment of entorhinal networks in neonatal mice
title_fullStr Coordinated electrical activity in the olfactory bulb gates the oscillatory entrainment of entorhinal networks in neonatal mice
title_full_unstemmed Coordinated electrical activity in the olfactory bulb gates the oscillatory entrainment of entorhinal networks in neonatal mice
title_short Coordinated electrical activity in the olfactory bulb gates the oscillatory entrainment of entorhinal networks in neonatal mice
title_sort coordinated electrical activity in the olfactory bulb gates the oscillatory entrainment of entorhinal networks in neonatal mice
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6354964/
https://www.ncbi.nlm.nih.gov/pubmed/30703080
http://dx.doi.org/10.1371/journal.pbio.2006994
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