Functional architecture of intracellular oscillations in hippocampal dendrites

Zhenrui Liao, Kevin C. Gonzalez, Deborah M. Li, Catalina M. Yang, Donald Holder, Natalie E. McClain, Guofeng Zhang, Stephen W. Evans, Mariya Chavarha, Jane Simko, Christopher D. Makinson, Michael Z. Lin, Attila Losonczy () and Adrian Negrean ()
Additional contact information
Zhenrui Liao: Columbia University
Kevin C. Gonzalez: Columbia University
Deborah M. Li: Columbia University
Catalina M. Yang: Columbia University
Donald Holder: Columbia University
Natalie E. McClain: Columbia University
Guofeng Zhang: Stanford University
Stephen W. Evans: Stanford University
Mariya Chavarha: Stanford University
Jane Simko: Columbia University
Christopher D. Makinson: Columbia University
Michael Z. Lin: Stanford University
Attila Losonczy: Columbia University
Adrian Negrean: Columbia University

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract Fast electrical signaling in dendrites is central to neural computations that support adaptive behaviors. Conventional techniques lack temporal and spatial resolution and the ability to track underlying membrane potential dynamics present across the complex three-dimensional dendritic arbor in vivo. Here, we perform fast two-photon imaging of dendritic and somatic membrane potential dynamics in single pyramidal cells in the CA1 region of the mouse hippocampus during awake behavior. We study the dynamics of subthreshold membrane potential and suprathreshold dendritic events throughout the dendritic arbor in vivo by combining voltage imaging with simultaneous local field potential recording, post hoc morphological reconstruction, and a spatial navigation task. We systematically quantify the modulation of local event rates by locomotion in distinct dendritic regions, report an advancing gradient of dendritic theta phase along the basal-tuft axis, and describe a predominant hyperpolarization of the dendritic arbor during sharp-wave ripples. Finally, we find that spatial tuning of dendritic representations dynamically reorganizes following place field formation. Our data reveal how the organization of electrical signaling in dendrites maps onto the anatomy of the dendritic tree across behavior, oscillatory network, and functional cell states.

Date: 2024
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DOI: 10.1038/s41467-024-50546-z

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