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Published February 17, 2016 | Accepted Version + Supplemental Material
Journal Article Open

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

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.

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.

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Accepted Version - nihms750906.pdf

Supplemental Material - mmc1.pdf

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Created:
August 20, 2023
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October 17, 2023