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Diversity of dynamic voltage patterns in neuronal dendrites revealed by nanopipette electrophysiology.

Published version
Peer-reviewed

Repository DOI


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Authors

Makarchuk, Stanislaw 
Fernandez-Villegas, Ana 
Kaminski Schierle, Gabriele S  ORCID logo  https://orcid.org/0000-0002-1843-2202

Abstract

Dendrites and dendritic spines are the essential cellular compartments in neuronal communication, conveying information through transient voltage signals. Our understanding of these compartmentalized voltage dynamics in fine, distal neuronal dendrites remains poor due to the difficulties inherent to accessing and stably recording from such small, nanoscale cellular compartments for a sustained time. To overcome these challenges, we use nanopipettes that permit long and stable recordings directly from fine neuronal dendrites. We reveal a diversity of voltage dynamics present locally in dendrites, such as spontaneous voltage transients, bursting events and oscillating periods of silence and firing activity, all of which we characterized using segmentation analysis. Remarkably, we find that neuronal dendrites can display spontaneous hyperpolarisation events, and sustain transient hyperpolarised states. The voltage patterns were activity-dependent, with a stronger dependency on synaptic activity than on action potentials. Long-time recordings of fine dendritic protrusions show complex voltage dynamics that may represent a previously unexplored contribution to dendritic computations.

Description

Acknowledgements: The authors thank Elena Dossi, Charles Felix-Calvo, Julien Moulard and Giampaolo Milior for discussion and technical help. J. Mc H. acknowledges funding from AFOSR (Grant No. FA9550-17-1-0118), ANR programme Investissements d'avenir (ANR-10-LABX-54 MEMOLIFE and ANR-IO-IDEX0001-02 PSL Research University) and from FRM (SPF202005011994). D. M. acknowledges funding from Q-life (ANR-17-CONV-0005). G. S. K. S. acknowledges funding from the Michael J Fox Foundation (16238). U. F. K. is supported by ERC Consolidator Grant (DesignerPores n° 647144). D. H. acknowledges funding from the European Research Council (ERC Advanced Grant OrganellenanoComp n° 882673) under the European Union's Horizon 2020 research and innovation programme, Plan Cancer-INSERM (19CS145-00) and ANR (ANR-18-NEUC-0001). N. R. and C. F. K. acknowledge funding from Cam-PSL-French Embassy. N. R. and D. H. acknowledge funding from ANR (ANR-22-CE16-0027) and ANR programme Investissements d'avenir (ANR-10-LABX-54 MEMOLIFE and ANR-IO-IDEX0001-02 PSL Research University). N. R. acknowledges the Service Enseignement Supérieur, Recherche et Innovation de l'Ambassade de France and Churchill College for the French government oversea fellowship.

Keywords

Neurons, Dendrites, Action Potentials, Electrophysiology

Journal Title

Nanoscale

Conference Name

Journal ISSN

2040-3364
2040-3372

Volume Title

Publisher

Royal Society of Chemistry (RSC)
Sponsorship
European Research Council (647144)
European Office of Aerospace Research and Development (EOARD) (FA9550-17-1-0118)