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UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice

Kajikawa, Koichiro and Hulse, Brad K. and Siapas, Athanassios G. and Lubenov, Evgueniy V. (2022) UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice. eLife, 11 . Art.No. 69596. ISSN 2050-084X. PMCID PMC9275824. doi:10.7554/elife.69596. https://resolver.caltech.edu/CaltechAUTHORS:20220729-894444000

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Abstract

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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.7554/eLife.69596DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc9275824/PubMed CentralArticle
https://elifesciences.org/articles/69596/figures#filesPublisherSupporting Information
ORCID:
AuthorORCID
Kajikawa, Koichiro0000-0002-8626-4407
Hulse, Brad K.0000-0002-7117-7036
Siapas, Athanassios G.0000-0001-8837-678X
Lubenov, Evgueniy V.0000-0002-1099-944X
Additional Information:© 2022, Kajikawa et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Received: April 20, 2021. Preprint posted: April 22, 2021 (view preprint). Accepted: June 2, 2022. Version of Record published: July 12, 2022 (version 1). We thank Lee-Peng Mok for help with histological processing and immunohistochemistry, Maria Papadopoulou and Stijn Cassenear for help with imaging, insightful discussions and feedback on the manuscript, and Kevin Shan for help with the data processing pipeline and insightful discussion. Confocal imaging was performed at the Caltech Biological Imaging Facility. This work was supported by a Vannevar Bush Faculty Fellowship, the Mathers Foundation, the McKnight Foundation, and NIH grant RO1MH113016. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Author contributions. Koichiro Kajikawa, Brad K Hulse, Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing – review and editing; Athanassios G Siapas, Evgueniy V Lubenov, Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review and editing. Data availability. All data analyzed during this study are included in the manuscript and supporting files. Ethics. All procedures were approved by the Institutional Animal Care and Use Committee (IACUC) at Caltech (protocols 1465, 1771) and conformed to National Institutes of Health guidelines.
Funders:
Funding AgencyGrant Number
Vannevar Bush Faculty FellowshipUNSPECIFIED
Mathers FoundationUNSPECIFIED
McKnight FoundationUNSPECIFIED
NIHRO1MH113016
PubMed Central ID:PMC9275824
DOI:10.7554/elife.69596
Record Number:CaltechAUTHORS:20220729-894444000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220729-894444000
Official Citation:Koichiro KajikawaBrad K HulseAthanassios G SiapasEvgueniy V Lubenov (2022) UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice eLife 11:e69596.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:115980
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:01 Aug 2022 19:52
Last Modified:01 Aug 2022 19:52

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