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Published January 3, 2017 | Published + Supplemental Material
Journal Article Open

Brain State Dependence of Hippocampal Subthreshold Activity in Awake Mice

Abstract

Monitoring the membrane potential of individual neurons has uncovered how single-cell properties contribute to network processing across different brain states in neocortex. In contrast, the subthreshold modulation of hippocampal neurons by brain state has not been systematically characterized. To address this, we combined whole-cell recordings from dentate granule cells and CA1 pyramidal neurons with multisite extracellular recordings and behavioral measurements in awake mice. We show that the average membrane potential, amplitude of subthreshold fluctuations, and distance to spike threshold are all modulated by brain state. Furthermore, even within individual states, rapid variations in arousal are reflected in membrane potential fluctuations. These factors produce depolarizing ramps in the membrane potential of hippocampal neurons that precede ripples and mirror transitions to a network regime conducive for ripple generation. These results suggest that there are coordinated shifts in the subthreshold dynamics of individual neurons that underlie the transitions between distinct modes of hippocampal processing.

Additional Information

© 2017 The Author(s). This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Received 26 July 2016, Revised 7 November 2016, Accepted 30 November 2016, Available online 3 January 2017. We thank Stijn Cassenaer, Koichiro Kajikawa, Maria Papadopoulou, 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 Koichiro Kajikawa for help with dentate experiments. Confocal imaging was performed in the Caltech Biological Imaging Facility with the support of the Caltech Beckman Institute and the Beckman Foundations. This work was supported by the Mathers Foundation, the Moore Foundation, NIH grant 1DP1OD008255/5DP1MH099907, NSF grant IOS-1146871, and the iARPA contract D16PC00003.

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Supplemental Material - mmc1.pdf

Supplemental Material - mmc2.mp4

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