Distinct Synchronous Network Activity During the Second Postnatal Week of Medial Entorhinal Cortex Development

The medial entorhinal cortex (MEC) contains specialized cell types whose firing is tuned to aspects of an animal’s position and orientation in the environment, reflecting a neuronal representation of space. The spatially tuned firing properties of these cells quickly emerge during the third postnata...

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Main Authors: Julia Dawitz, Tim Kroon, J. J. Johannes Hjorth, Huib D. Mansvelder, Rhiannon M. Meredith
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-04-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fncel.2020.00091/full
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spelling doaj-fc7e79facb774e07985442c17f1c10a12020-11-25T02:34:38ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022020-04-011410.3389/fncel.2020.00091527822Distinct Synchronous Network Activity During the Second Postnatal Week of Medial Entorhinal Cortex DevelopmentJulia DawitzTim KroonJ. J. Johannes HjorthHuib D. MansvelderRhiannon M. MeredithThe medial entorhinal cortex (MEC) contains specialized cell types whose firing is tuned to aspects of an animal’s position and orientation in the environment, reflecting a neuronal representation of space. The spatially tuned firing properties of these cells quickly emerge during the third postnatal week of development in rodents. Spontaneous synchronized network activity (SSNA) has been shown to play a crucial role in the development of neuronal circuits prior to week 3. SSNA in MEC is well described in rodents during the first postnatal week, but there are little data about its development immediately prior to eye opening and spatial exploration. Furthermore, existing data lack single-cell resolution and are not integrated across layers. In this study, we addressed the question of whether the characteristics and underlying mechanisms of SSNA during the second postnatal week resemble that of the first week or whether distinct features emerge during this period. Using a combined calcium imaging and electrophysiology approach in vitro, we confirm that in mouse MEC during the second postnatal week, SSNA persists and in fact peaks, and is dependent on ionotropic glutamatergic signaling. However, SSNA differs from that observed during the first postnatal week in two ways: First, EC does not drive network activity in the hippocampus but only in neighboring neocortex (NeoC). Second, GABA does not drive network activity but influences it in a manner that is dependent both on age and receptor type. Therefore, we conclude that while there is a partial mechanistic overlap in SSNA between the first and second postnatal weeks, unique mechanistic features do emerge during the second week, suggestive of different or additional functions of MEC within the hippocampal-entorhinal circuitry with increasing maturation.https://www.frontiersin.org/article/10.3389/fncel.2020.00091/fulldevelopmentmedial entorhinal cortexgiant depolarizing potentialsearly network oscillationsGABAsynchronization
collection DOAJ
language English
format Article
sources DOAJ
author Julia Dawitz
Tim Kroon
J. J. Johannes Hjorth
Huib D. Mansvelder
Rhiannon M. Meredith
spellingShingle Julia Dawitz
Tim Kroon
J. J. Johannes Hjorth
Huib D. Mansvelder
Rhiannon M. Meredith
Distinct Synchronous Network Activity During the Second Postnatal Week of Medial Entorhinal Cortex Development
Frontiers in Cellular Neuroscience
development
medial entorhinal cortex
giant depolarizing potentials
early network oscillations
GABA
synchronization
author_facet Julia Dawitz
Tim Kroon
J. J. Johannes Hjorth
Huib D. Mansvelder
Rhiannon M. Meredith
author_sort Julia Dawitz
title Distinct Synchronous Network Activity During the Second Postnatal Week of Medial Entorhinal Cortex Development
title_short Distinct Synchronous Network Activity During the Second Postnatal Week of Medial Entorhinal Cortex Development
title_full Distinct Synchronous Network Activity During the Second Postnatal Week of Medial Entorhinal Cortex Development
title_fullStr Distinct Synchronous Network Activity During the Second Postnatal Week of Medial Entorhinal Cortex Development
title_full_unstemmed Distinct Synchronous Network Activity During the Second Postnatal Week of Medial Entorhinal Cortex Development
title_sort distinct synchronous network activity during the second postnatal week of medial entorhinal cortex development
publisher Frontiers Media S.A.
series Frontiers in Cellular Neuroscience
issn 1662-5102
publishDate 2020-04-01
description The medial entorhinal cortex (MEC) contains specialized cell types whose firing is tuned to aspects of an animal’s position and orientation in the environment, reflecting a neuronal representation of space. The spatially tuned firing properties of these cells quickly emerge during the third postnatal week of development in rodents. Spontaneous synchronized network activity (SSNA) has been shown to play a crucial role in the development of neuronal circuits prior to week 3. SSNA in MEC is well described in rodents during the first postnatal week, but there are little data about its development immediately prior to eye opening and spatial exploration. Furthermore, existing data lack single-cell resolution and are not integrated across layers. In this study, we addressed the question of whether the characteristics and underlying mechanisms of SSNA during the second postnatal week resemble that of the first week or whether distinct features emerge during this period. Using a combined calcium imaging and electrophysiology approach in vitro, we confirm that in mouse MEC during the second postnatal week, SSNA persists and in fact peaks, and is dependent on ionotropic glutamatergic signaling. However, SSNA differs from that observed during the first postnatal week in two ways: First, EC does not drive network activity in the hippocampus but only in neighboring neocortex (NeoC). Second, GABA does not drive network activity but influences it in a manner that is dependent both on age and receptor type. Therefore, we conclude that while there is a partial mechanistic overlap in SSNA between the first and second postnatal weeks, unique mechanistic features do emerge during the second week, suggestive of different or additional functions of MEC within the hippocampal-entorhinal circuitry with increasing maturation.
topic development
medial entorhinal cortex
giant depolarizing potentials
early network oscillations
GABA
synchronization
url https://www.frontiersin.org/article/10.3389/fncel.2020.00091/full
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