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Membrane Potential Dynamics of CA1 Pyramidal Neurons during Hippocampal Ripples in Awake Mice

Hulse, Brad K. and Moreaux, Laurent C. and Lubenov, Evgueniy V. and Siapas, Athanassios G. (2016) Membrane Potential Dynamics of CA1 Pyramidal Neurons during Hippocampal Ripples in Awake Mice. Neuron, 89 (4). pp. 800-813. ISSN 0896-6273. PMCID PMC5167572. doi:10.1016/j.neuron.2016.01.014. https://resolver.caltech.edu/CaltechAUTHORS:20160219-101434308

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Abstract

Ripples are high-frequency oscillations associated with population bursts in area CA1 of the hippocampus that play a prominent role in theories of memory consolidation. While spiking during ripples has been extensively studied, our understanding of the subthreshold behavior of hippocampal neurons during these events remains incomplete. Here, we combine in vivo whole-cell and multisite extracellular recordings to characterize the membrane potential dynamics of identified CA1 pyramidal neurons during ripples. We find that the subthreshold depolarization during ripples is uncorrelated with the net excitatory input to CA1, while the post-ripple hyperpolarization varies proportionately. This clarifies the circuit mechanism keeping most neurons silent during ripples. On a finer timescale, the phase delay between intracellular and extracellular ripple oscillations varies systematically with membrane potential. Such smoothly varying delays are inconsistent with models of intracellular ripple generation involving perisomatic inhibition alone. Instead, they suggest that ripple-frequency excitation leading inhibition shapes intracellular ripple oscillations.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1016/j.neuron.2016.01.014DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5167572PubMed CentralArticle
ORCID:
AuthorORCID
Hulse, Brad K.0000-0002-7117-7036
Moreaux, Laurent C.0000-0003-1276-5062
Lubenov, Evgueniy V.0000-0002-1099-944X
Siapas, Athanassios G.0000-0001-8837-678X
Additional Information:© 2016 Elsevier Inc. Received: July 28, 2015; Revised: October 26, 2015; Accepted: January 6, 2016; Published: February 17, 2016. We thank Stijn Cassenaer, Andreas Hoenselaar, Gilles Laurent, Maria Papadopoulou, Jacob Reimer, Britton Sauerbrei, and Kevin Shan for helpful discussion and comments on the manuscript; Andreas Hoenselaar and Mike Walsh for help with instrumentation; Lee-Peng Mok for help with immunohistochemistry; and Stephan Junek and the Max Planck Institute for Brain Science in Frankfurt for help with Figure 1B. All other confocal imaging was performed in the Caltech Biological Imaging Facility, with the support of the Caltech Beckman Institute and the Beckman Foundation. This work was supported by the Mathers Foundation, the Moore Foundation, NIH 1DP1OD008255/5DP1MH099907, and NSF IOS-1146871. B.K.H., L.C.M., E.V.L., and A.G.S. designed the experiments. B.K.H. performed the experiments. L.C.M. helped implement whole-cell recordings in awake mice. B.K.H., E.V.L., and A.G.S. analyzed the data. B.K.H. wrote the analysis programs and generated the figures. B.K.H., L.C.M., E.V.L., and A.G.S. wrote the paper.
Funders:
Funding AgencyGrant Number
G. Harold and Leila Y. Mathers Charitable FoundationUNSPECIFIED
Gordon and Betty Moore FoundationUNSPECIFIED
NIH1DP1OD008255/5DP1MH099907
NSFIOS-1146871
Caltech Beckman InstituteUNSPECIFIED
Arnold and Mabel Beckman FoundationUNSPECIFIED
Issue or Number:4
PubMed Central ID:PMC5167572
DOI:10.1016/j.neuron.2016.01.014
Record Number:CaltechAUTHORS:20160219-101434308
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20160219-101434308
Official Citation:Brad K. Hulse, Laurent C. Moreaux, Evgueniy V. Lubenov, Athanassios G. Siapas, Membrane Potential Dynamics of CA1 Pyramidal Neurons during Hippocampal Ripples in Awake Mice, Neuron, Volume 89, Issue 4, 17 February 2016, Pages 800-813, ISSN 0896-6273, http://dx.doi.org/10.1016/j.neuron.2016.01.014.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:64606
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:19 Feb 2016 18:27
Last Modified:05 May 2022 18:36

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