Functional architecture of intracellular oscillations in hippocampal dendrites

• Published in: Nature communications Vol. 15; no. 1; pp. 6295 - 16
• Main Authors: Liao, Zhenrui, Gonzalez, Kevin C., Li, Deborah M., Yang, Catalina M., Holder, Donald, McClain, Natalie E., Zhang, Guofeng, Evans, Stephen W., Chavarha, Mariya, Simko, Jane, Makinson, Christopher D., Lin, Michael Z., Losonczy, Attila, Negrean, Adrian
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 26.07.2024; Nature Publishing Group; Nature Portfolio
• Subjects: 631/378/1595; 631/378/87; Animals; Behavior; Brain architecture; Brain mapping; CA1 Region, Hippocampal - cytology; CA1 Region, Hippocampal - physiology; Dendrites; Dendrites - metabolism; Dendrites - physiology; Dendritic structure; Electrophysiological recording; Functional morphology; Hippocampus; Hippocampus - cytology; Hippocampus - physiology; Humanities and Social Sciences; Hyperpolarization; Image reconstruction; In vivo methods and tests; Intracellular signalling; Locomotion; Locomotion - physiology; Male; Membrane potential; Membrane Potentials - physiology; Membranes; Mice; Mice, Inbred C57BL; Morphology; multidisciplinary; Navigation behavior; Neuroimaging; Neurosciences; Oscillations; Pyramidal cells; Pyramidal Cells - metabolism; Pyramidal Cells - physiology; Science; Science (multidisciplinary); Spatial discrimination; Spatial Navigation - physiology; Spatial resolution
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-50546-z

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. Neurons receive their input in three dimensions via their dendrites, but how electrical activity in dendrites is organized is unknown. Here, the authors work out the distinct rules that govern activity across this 3D structure in different brain states.