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Enriched Environment Modulates Sharp Wave-Ripple (SPW-R) Activity in Hippocampal Slices

Behavioral flexibility depends on neuronal plasticity which forms and adapts the central nervous system in an experience-dependent manner. Thus, plasticity depends on interactions between the organism and its environment. A key experimental paradigm for studying this concept is the exposure of roden...

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Autores principales: Landeck, Lucie, Kaiser, Martin E., Hefter, Dimitri, Draguhn, Andreas, Both, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8678456/
https://www.ncbi.nlm.nih.gov/pubmed/34924964
http://dx.doi.org/10.3389/fncir.2021.758939
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author Landeck, Lucie
Kaiser, Martin E.
Hefter, Dimitri
Draguhn, Andreas
Both, Martin
author_facet Landeck, Lucie
Kaiser, Martin E.
Hefter, Dimitri
Draguhn, Andreas
Both, Martin
author_sort Landeck, Lucie
collection PubMed
description Behavioral flexibility depends on neuronal plasticity which forms and adapts the central nervous system in an experience-dependent manner. Thus, plasticity depends on interactions between the organism and its environment. A key experimental paradigm for studying this concept is the exposure of rodents to an enriched environment (EE), followed by studying differences to control animals kept under standard conditions (SC). While multiple changes induced by EE have been found at the cellular-molecular and cognitive-behavioral levels, little is known about EE-dependent alterations at the intermediate level of network activity. We, therefore, studied spontaneous network activity in hippocampal slices from mice which had previously experienced EE for 10–15 days. Compared to control animals from standard conditions (SC) and mice with enhanced motor activity (MC) we found several differences in sharp wave-ripple complexes (SPW-R), a memory-related activity pattern. Sharp wave amplitude, unit firing during sharp waves, and the number of superimposed ripple cycles were increased in tissue from the EE group. On the other hand, spiking precision with respect to the ripple oscillations was reduced. Recordings from single pyramidal cells revealed a reduction in synaptic inhibition during SPW-R together with a reduced inhibition-excitation ratio. The number of inhibitory neurons, including parvalbumin-positive interneurons, was unchanged. Altered activation or efficacy of synaptic inhibition may thus underlie changes in memory-related network activity patterns which, in turn, may be important for the cognitive-behavioral effects of EE exposure.
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spelling pubmed-86784562021-12-18 Enriched Environment Modulates Sharp Wave-Ripple (SPW-R) Activity in Hippocampal Slices Landeck, Lucie Kaiser, Martin E. Hefter, Dimitri Draguhn, Andreas Both, Martin Front Neural Circuits Neuroscience Behavioral flexibility depends on neuronal plasticity which forms and adapts the central nervous system in an experience-dependent manner. Thus, plasticity depends on interactions between the organism and its environment. A key experimental paradigm for studying this concept is the exposure of rodents to an enriched environment (EE), followed by studying differences to control animals kept under standard conditions (SC). While multiple changes induced by EE have been found at the cellular-molecular and cognitive-behavioral levels, little is known about EE-dependent alterations at the intermediate level of network activity. We, therefore, studied spontaneous network activity in hippocampal slices from mice which had previously experienced EE for 10–15 days. Compared to control animals from standard conditions (SC) and mice with enhanced motor activity (MC) we found several differences in sharp wave-ripple complexes (SPW-R), a memory-related activity pattern. Sharp wave amplitude, unit firing during sharp waves, and the number of superimposed ripple cycles were increased in tissue from the EE group. On the other hand, spiking precision with respect to the ripple oscillations was reduced. Recordings from single pyramidal cells revealed a reduction in synaptic inhibition during SPW-R together with a reduced inhibition-excitation ratio. The number of inhibitory neurons, including parvalbumin-positive interneurons, was unchanged. Altered activation or efficacy of synaptic inhibition may thus underlie changes in memory-related network activity patterns which, in turn, may be important for the cognitive-behavioral effects of EE exposure. Frontiers Media S.A. 2021-12-03 /pmc/articles/PMC8678456/ /pubmed/34924964 http://dx.doi.org/10.3389/fncir.2021.758939 Text en Copyright © 2021 Landeck, Kaiser, Hefter, Draguhn and Both. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Landeck, Lucie
Kaiser, Martin E.
Hefter, Dimitri
Draguhn, Andreas
Both, Martin
Enriched Environment Modulates Sharp Wave-Ripple (SPW-R) Activity in Hippocampal Slices
title Enriched Environment Modulates Sharp Wave-Ripple (SPW-R) Activity in Hippocampal Slices
title_full Enriched Environment Modulates Sharp Wave-Ripple (SPW-R) Activity in Hippocampal Slices
title_fullStr Enriched Environment Modulates Sharp Wave-Ripple (SPW-R) Activity in Hippocampal Slices
title_full_unstemmed Enriched Environment Modulates Sharp Wave-Ripple (SPW-R) Activity in Hippocampal Slices
title_short Enriched Environment Modulates Sharp Wave-Ripple (SPW-R) Activity in Hippocampal Slices
title_sort enriched environment modulates sharp wave-ripple (spw-r) activity in hippocampal slices
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8678456/
https://www.ncbi.nlm.nih.gov/pubmed/34924964
http://dx.doi.org/10.3389/fncir.2021.758939
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