Dendritic excitations govern back-propagation via a spike-rate accelerometer

Abstract Dendrites on neurons support electrical excitations, but the computational significance of these events is not well understood. We developed molecular, optical, and computational tools for all-optical electrophysiology in dendrites. We mapped sub-millisecond voltage dynamics throughout the...

Full description

Saved in:
Bibliographic Details
Main Authors: Pojeong Park, J. David Wong-Campos, Daniel G. Itkis, Byung Hun Lee, Yitong Qi, Hunter C. Davis, Benjamin Antin, Amol Pasarkar, Jonathan B. Grimm, Sarah E. Plutkis, Katie L. Holland, Liam Paninski, Luke D. Lavis, Adam E. Cohen
Format: Article
Language:English
Published: Nature Portfolio 2025-02-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-55819-9
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1823861790455365632
author Pojeong Park
J. David Wong-Campos
Daniel G. Itkis
Byung Hun Lee
Yitong Qi
Hunter C. Davis
Benjamin Antin
Amol Pasarkar
Jonathan B. Grimm
Sarah E. Plutkis
Katie L. Holland
Liam Paninski
Luke D. Lavis
Adam E. Cohen
author_facet Pojeong Park
J. David Wong-Campos
Daniel G. Itkis
Byung Hun Lee
Yitong Qi
Hunter C. Davis
Benjamin Antin
Amol Pasarkar
Jonathan B. Grimm
Sarah E. Plutkis
Katie L. Holland
Liam Paninski
Luke D. Lavis
Adam E. Cohen
author_sort Pojeong Park
collection DOAJ
description Abstract Dendrites on neurons support electrical excitations, but the computational significance of these events is not well understood. We developed molecular, optical, and computational tools for all-optical electrophysiology in dendrites. We mapped sub-millisecond voltage dynamics throughout the dendritic trees of CA1 pyramidal neurons under diverse optogenetic and synaptic stimulus patterns, in acute brain slices. Our data show history-dependent spike back-propagation in distal dendrites, driven by locally generated Na+ spikes (dSpikes). Dendritic depolarization created a transient window for dSpike propagation, opened by A-type KV channel inactivation, and closed by slow NaV inactivation. Collisions of dSpikes with synaptic inputs triggered calcium channel and N-methyl-D-aspartate receptor (NMDAR)-dependent dendritic plateau potentials and accompanying complex spikes at the soma. This hierarchical ion channel network acts as a spike-rate accelerometer, providing an intuitive picture connecting dendritic biophysics to associative plasticity rules.
format Article
id doaj-art-2d3d5a4a894b42dd8dabb687dc5d6158
institution Kabale University
issn 2041-1723
language English
publishDate 2025-02-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-2d3d5a4a894b42dd8dabb687dc5d61582025-02-09T12:43:56ZengNature PortfolioNature Communications2041-17232025-02-0116112010.1038/s41467-025-55819-9Dendritic excitations govern back-propagation via a spike-rate accelerometerPojeong Park0J. David Wong-Campos1Daniel G. Itkis2Byung Hun Lee3Yitong Qi4Hunter C. Davis5Benjamin Antin6Amol Pasarkar7Jonathan B. Grimm8Sarah E. Plutkis9Katie L. Holland10Liam Paninski11Luke D. Lavis12Adam E. Cohen13Department of Chemistry and Chemical Biology, Harvard UniversityDepartment of Chemistry and Chemical Biology, Harvard UniversityDepartment of Chemistry and Chemical Biology, Harvard UniversityDepartment of Chemistry and Chemical Biology, Harvard UniversityDepartment of Chemistry and Chemical Biology, Harvard UniversityDepartment of Chemistry and Chemical Biology, Harvard UniversityDepartments of Statistics and Neuroscience, Columbia UniversityDepartments of Statistics and Neuroscience, Columbia UniversityJanelia Research Campus, Howard Hughes Medical InstituteJanelia Research Campus, Howard Hughes Medical InstituteJanelia Research Campus, Howard Hughes Medical InstituteDepartments of Statistics and Neuroscience, Columbia UniversityJanelia Research Campus, Howard Hughes Medical InstituteDepartment of Chemistry and Chemical Biology, Harvard UniversityAbstract Dendrites on neurons support electrical excitations, but the computational significance of these events is not well understood. We developed molecular, optical, and computational tools for all-optical electrophysiology in dendrites. We mapped sub-millisecond voltage dynamics throughout the dendritic trees of CA1 pyramidal neurons under diverse optogenetic and synaptic stimulus patterns, in acute brain slices. Our data show history-dependent spike back-propagation in distal dendrites, driven by locally generated Na+ spikes (dSpikes). Dendritic depolarization created a transient window for dSpike propagation, opened by A-type KV channel inactivation, and closed by slow NaV inactivation. Collisions of dSpikes with synaptic inputs triggered calcium channel and N-methyl-D-aspartate receptor (NMDAR)-dependent dendritic plateau potentials and accompanying complex spikes at the soma. This hierarchical ion channel network acts as a spike-rate accelerometer, providing an intuitive picture connecting dendritic biophysics to associative plasticity rules.https://doi.org/10.1038/s41467-025-55819-9
spellingShingle Pojeong Park
J. David Wong-Campos
Daniel G. Itkis
Byung Hun Lee
Yitong Qi
Hunter C. Davis
Benjamin Antin
Amol Pasarkar
Jonathan B. Grimm
Sarah E. Plutkis
Katie L. Holland
Liam Paninski
Luke D. Lavis
Adam E. Cohen
Dendritic excitations govern back-propagation via a spike-rate accelerometer
Nature Communications
title Dendritic excitations govern back-propagation via a spike-rate accelerometer
title_full Dendritic excitations govern back-propagation via a spike-rate accelerometer
title_fullStr Dendritic excitations govern back-propagation via a spike-rate accelerometer
title_full_unstemmed Dendritic excitations govern back-propagation via a spike-rate accelerometer
title_short Dendritic excitations govern back-propagation via a spike-rate accelerometer
title_sort dendritic excitations govern back propagation via a spike rate accelerometer
url https://doi.org/10.1038/s41467-025-55819-9
work_keys_str_mv AT pojeongpark dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer
AT jdavidwongcampos dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer
AT danielgitkis dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer
AT byunghunlee dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer
AT yitongqi dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer
AT huntercdavis dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer
AT benjaminantin dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer
AT amolpasarkar dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer
AT jonathanbgrimm dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer
AT saraheplutkis dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer
AT katielholland dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer
AT liampaninski dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer
AT lukedlavis dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer
AT adamecohen dendriticexcitationsgovernbackpropagationviaaspikerateaccelerometer