Cargando…

Purkinje cell axonal swellings enhance action potential fidelity and cerebellar function

Axonal plasticity allows neurons to control their output, which critically determines the flow of information in the brain. Axon diameter can be regulated by activity, yet how morphological changes in an axon impact its function remains poorly understood. Axonal swellings have been found on Purkinje...

Descripción completa

Detalles Bibliográficos
Autores principales: Lang-Ouellette, Daneck, Gruver, Kim M., Smith-Dijak, Amy, Blot, François G. C., Stewart, Chloe A., de Vanssay de Blavous, Pauline, Li, Connie H., Van Eitrem, Carter, Rosen, Charlotte, Faust, Phyllis L., Schonewille, Martijn, Watt, Alanna J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8257784/
https://www.ncbi.nlm.nih.gov/pubmed/34226561
http://dx.doi.org/10.1038/s41467-021-24390-4
_version_ 1783718380842254336
author Lang-Ouellette, Daneck
Gruver, Kim M.
Smith-Dijak, Amy
Blot, François G. C.
Stewart, Chloe A.
de Vanssay de Blavous, Pauline
Li, Connie H.
Van Eitrem, Carter
Rosen, Charlotte
Faust, Phyllis L.
Schonewille, Martijn
Watt, Alanna J.
author_facet Lang-Ouellette, Daneck
Gruver, Kim M.
Smith-Dijak, Amy
Blot, François G. C.
Stewart, Chloe A.
de Vanssay de Blavous, Pauline
Li, Connie H.
Van Eitrem, Carter
Rosen, Charlotte
Faust, Phyllis L.
Schonewille, Martijn
Watt, Alanna J.
author_sort Lang-Ouellette, Daneck
collection PubMed
description Axonal plasticity allows neurons to control their output, which critically determines the flow of information in the brain. Axon diameter can be regulated by activity, yet how morphological changes in an axon impact its function remains poorly understood. Axonal swellings have been found on Purkinje cell axons in the cerebellum both in healthy development and in neurodegenerative diseases, and computational models predicts that axonal swellings impair axonal function. Here we report that in young Purkinje cells, axons with swellings propagated action potentials with higher fidelity than those without, and that axonal swellings form when axonal failures are high. Furthermore, we observed that healthy young adult mice with more axonal swellings learn better on cerebellar-related tasks than mice with fewer swellings. Our findings suggest that axonal swellings underlie a form of axonal plasticity that optimizes the fidelity of action potential propagation in axons, resulting in enhanced learning.
format Online
Article
Text
id pubmed-8257784
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-82577842021-07-23 Purkinje cell axonal swellings enhance action potential fidelity and cerebellar function Lang-Ouellette, Daneck Gruver, Kim M. Smith-Dijak, Amy Blot, François G. C. Stewart, Chloe A. de Vanssay de Blavous, Pauline Li, Connie H. Van Eitrem, Carter Rosen, Charlotte Faust, Phyllis L. Schonewille, Martijn Watt, Alanna J. Nat Commun Article Axonal plasticity allows neurons to control their output, which critically determines the flow of information in the brain. Axon diameter can be regulated by activity, yet how morphological changes in an axon impact its function remains poorly understood. Axonal swellings have been found on Purkinje cell axons in the cerebellum both in healthy development and in neurodegenerative diseases, and computational models predicts that axonal swellings impair axonal function. Here we report that in young Purkinje cells, axons with swellings propagated action potentials with higher fidelity than those without, and that axonal swellings form when axonal failures are high. Furthermore, we observed that healthy young adult mice with more axonal swellings learn better on cerebellar-related tasks than mice with fewer swellings. Our findings suggest that axonal swellings underlie a form of axonal plasticity that optimizes the fidelity of action potential propagation in axons, resulting in enhanced learning. Nature Publishing Group UK 2021-07-05 /pmc/articles/PMC8257784/ /pubmed/34226561 http://dx.doi.org/10.1038/s41467-021-24390-4 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Lang-Ouellette, Daneck
Gruver, Kim M.
Smith-Dijak, Amy
Blot, François G. C.
Stewart, Chloe A.
de Vanssay de Blavous, Pauline
Li, Connie H.
Van Eitrem, Carter
Rosen, Charlotte
Faust, Phyllis L.
Schonewille, Martijn
Watt, Alanna J.
Purkinje cell axonal swellings enhance action potential fidelity and cerebellar function
title Purkinje cell axonal swellings enhance action potential fidelity and cerebellar function
title_full Purkinje cell axonal swellings enhance action potential fidelity and cerebellar function
title_fullStr Purkinje cell axonal swellings enhance action potential fidelity and cerebellar function
title_full_unstemmed Purkinje cell axonal swellings enhance action potential fidelity and cerebellar function
title_short Purkinje cell axonal swellings enhance action potential fidelity and cerebellar function
title_sort purkinje cell axonal swellings enhance action potential fidelity and cerebellar function
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8257784/
https://www.ncbi.nlm.nih.gov/pubmed/34226561
http://dx.doi.org/10.1038/s41467-021-24390-4
work_keys_str_mv AT langouellettedaneck purkinjecellaxonalswellingsenhanceactionpotentialfidelityandcerebellarfunction
AT gruverkimm purkinjecellaxonalswellingsenhanceactionpotentialfidelityandcerebellarfunction
AT smithdijakamy purkinjecellaxonalswellingsenhanceactionpotentialfidelityandcerebellarfunction
AT blotfrancoisgc purkinjecellaxonalswellingsenhanceactionpotentialfidelityandcerebellarfunction
AT stewartchloea purkinjecellaxonalswellingsenhanceactionpotentialfidelityandcerebellarfunction
AT devanssaydeblavouspauline purkinjecellaxonalswellingsenhanceactionpotentialfidelityandcerebellarfunction
AT liconnieh purkinjecellaxonalswellingsenhanceactionpotentialfidelityandcerebellarfunction
AT vaneitremcarter purkinjecellaxonalswellingsenhanceactionpotentialfidelityandcerebellarfunction
AT rosencharlotte purkinjecellaxonalswellingsenhanceactionpotentialfidelityandcerebellarfunction
AT faustphyllisl purkinjecellaxonalswellingsenhanceactionpotentialfidelityandcerebellarfunction
AT schonewillemartijn purkinjecellaxonalswellingsenhanceactionpotentialfidelityandcerebellarfunction
AT wattalannaj purkinjecellaxonalswellingsenhanceactionpotentialfidelityandcerebellarfunction