Cargando…
UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice
Hippocampal ripples are transient population bursts that structure cortico-hippocampal communication and play a central role in memory processing. However, the mechanisms controlling ripple initiation in behaving animals remain poorly understood. Here we combine multisite extracellular and whole-cel...
Autores principales: | , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9275824/ https://www.ncbi.nlm.nih.gov/pubmed/35819409 http://dx.doi.org/10.7554/eLife.69596 |
_version_ | 1784745571022536704 |
---|---|
author | Kajikawa, Koichiro Hulse, Brad K Siapas, Athanassios G Lubenov, Evgueniy V |
author_facet | Kajikawa, Koichiro Hulse, Brad K Siapas, Athanassios G Lubenov, Evgueniy V |
author_sort | Kajikawa, Koichiro |
collection | PubMed |
description | Hippocampal ripples are transient population bursts that structure cortico-hippocampal communication and play a central role in memory processing. However, the mechanisms controlling ripple initiation in behaving animals remain poorly understood. Here we combine multisite extracellular and whole-cell recordings in awake mice to contrast the brain state and ripple modulation of subthreshold dynamics across hippocampal subfields. We find that entorhinal input to the dentate gyrus (DG) exhibits UP and DOWN dynamics with ripples occurring exclusively in UP states. While elevated cortical input in UP states generates depolarization in DG and CA1, it produces persistent hyperpolarization in CA3 neurons. Furthermore, growing inhibition is evident in CA3 throughout the course of the ripple buildup, while DG and CA1 neurons exhibit depolarization transients 100 ms before and during ripples. These observations highlight the importance of CA3 inhibition for ripple generation, while pre-ripple responses indicate a long and orchestrated ripple initiation process in the awake state. |
format | Online Article Text |
id | pubmed-9275824 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
spelling | pubmed-92758242022-07-13 UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice Kajikawa, Koichiro Hulse, Brad K Siapas, Athanassios G Lubenov, Evgueniy V eLife Neuroscience Hippocampal ripples are transient population bursts that structure cortico-hippocampal communication and play a central role in memory processing. However, the mechanisms controlling ripple initiation in behaving animals remain poorly understood. Here we combine multisite extracellular and whole-cell recordings in awake mice to contrast the brain state and ripple modulation of subthreshold dynamics across hippocampal subfields. We find that entorhinal input to the dentate gyrus (DG) exhibits UP and DOWN dynamics with ripples occurring exclusively in UP states. While elevated cortical input in UP states generates depolarization in DG and CA1, it produces persistent hyperpolarization in CA3 neurons. Furthermore, growing inhibition is evident in CA3 throughout the course of the ripple buildup, while DG and CA1 neurons exhibit depolarization transients 100 ms before and during ripples. These observations highlight the importance of CA3 inhibition for ripple generation, while pre-ripple responses indicate a long and orchestrated ripple initiation process in the awake state. eLife Sciences Publications, Ltd 2022-07-12 /pmc/articles/PMC9275824/ /pubmed/35819409 http://dx.doi.org/10.7554/eLife.69596 Text en © 2022, Kajikawa et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited. |
spellingShingle | Neuroscience Kajikawa, Koichiro Hulse, Brad K Siapas, Athanassios G Lubenov, Evgueniy V UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice |
title | UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice |
title_full | UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice |
title_fullStr | UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice |
title_full_unstemmed | UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice |
title_short | UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice |
title_sort | up-down states and ripples differentially modulate membrane potential dynamics across dg, ca3, and ca1 in awake mice |
topic | Neuroscience |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9275824/ https://www.ncbi.nlm.nih.gov/pubmed/35819409 http://dx.doi.org/10.7554/eLife.69596 |
work_keys_str_mv | AT kajikawakoichiro updownstatesandripplesdifferentiallymodulatemembranepotentialdynamicsacrossdgca3andca1inawakemice AT hulsebradk updownstatesandripplesdifferentiallymodulatemembranepotentialdynamicsacrossdgca3andca1inawakemice AT siapasathanassiosg updownstatesandripplesdifferentiallymodulatemembranepotentialdynamicsacrossdgca3andca1inawakemice AT lubenovevgueniyv updownstatesandripplesdifferentiallymodulatemembranepotentialdynamicsacrossdgca3andca1inawakemice |