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Removing a single neuron in a vertebrate brain forever abolishes an essential behavior

The giant Mauthner (M) cell is the largest neuron known in the vertebrate brain. It has enabled major breakthroughs in neuroscience but its ultimate function remains surprisingly unclear: An actual survival value of M cell-mediated escapes has never been supported experimentally and ablating the cel...

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Autores principales: Hecker, Alexander, Schulze, Wolfram, Oster, Jakob, Richter, David O., Schuster, Stefan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7022180/
https://www.ncbi.nlm.nih.gov/pubmed/32001507
http://dx.doi.org/10.1073/pnas.1918578117
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author Hecker, Alexander
Schulze, Wolfram
Oster, Jakob
Richter, David O.
Schuster, Stefan
author_facet Hecker, Alexander
Schulze, Wolfram
Oster, Jakob
Richter, David O.
Schuster, Stefan
author_sort Hecker, Alexander
collection PubMed
description The giant Mauthner (M) cell is the largest neuron known in the vertebrate brain. It has enabled major breakthroughs in neuroscience but its ultimate function remains surprisingly unclear: An actual survival value of M cell-mediated escapes has never been supported experimentally and ablating the cell repeatedly failed to eliminate all rapid escapes, suggesting that escapes can equally well be driven by smaller neurons. Here we applied techniques to simultaneously measure escape performance and the state of the giant M axon over an extended period following ablation of its soma. We discovered that the axon survives remarkably long and remains still fully capable of driving rapid escape behavior. By unilaterally removing one of the two M axons and comparing escapes in the same individual that could or could not recruit an M axon, we show that the giant M axon is essential for rapid escapes and that its loss means that rapid escapes are also lost forever. This allowed us to directly test the survival value of the M cell-mediated escapes and to show that the absence of this giant neuron directly affects survival in encounters with a natural predator. These findings not only offer a surprising solution to an old puzzle but demonstrate that even complex brains can trust vital functions to individual neurons. Our findings suggest that mechanisms must have evolved in parallel with the unique significance of these neurons to keep their axons alive and connected.
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spelling pubmed-70221802020-02-21 Removing a single neuron in a vertebrate brain forever abolishes an essential behavior Hecker, Alexander Schulze, Wolfram Oster, Jakob Richter, David O. Schuster, Stefan Proc Natl Acad Sci U S A Biological Sciences The giant Mauthner (M) cell is the largest neuron known in the vertebrate brain. It has enabled major breakthroughs in neuroscience but its ultimate function remains surprisingly unclear: An actual survival value of M cell-mediated escapes has never been supported experimentally and ablating the cell repeatedly failed to eliminate all rapid escapes, suggesting that escapes can equally well be driven by smaller neurons. Here we applied techniques to simultaneously measure escape performance and the state of the giant M axon over an extended period following ablation of its soma. We discovered that the axon survives remarkably long and remains still fully capable of driving rapid escape behavior. By unilaterally removing one of the two M axons and comparing escapes in the same individual that could or could not recruit an M axon, we show that the giant M axon is essential for rapid escapes and that its loss means that rapid escapes are also lost forever. This allowed us to directly test the survival value of the M cell-mediated escapes and to show that the absence of this giant neuron directly affects survival in encounters with a natural predator. These findings not only offer a surprising solution to an old puzzle but demonstrate that even complex brains can trust vital functions to individual neurons. Our findings suggest that mechanisms must have evolved in parallel with the unique significance of these neurons to keep their axons alive and connected. National Academy of Sciences 2020-02-11 2020-01-30 /pmc/articles/PMC7022180/ /pubmed/32001507 http://dx.doi.org/10.1073/pnas.1918578117 Text en Copyright © 2020 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Hecker, Alexander
Schulze, Wolfram
Oster, Jakob
Richter, David O.
Schuster, Stefan
Removing a single neuron in a vertebrate brain forever abolishes an essential behavior
title Removing a single neuron in a vertebrate brain forever abolishes an essential behavior
title_full Removing a single neuron in a vertebrate brain forever abolishes an essential behavior
title_fullStr Removing a single neuron in a vertebrate brain forever abolishes an essential behavior
title_full_unstemmed Removing a single neuron in a vertebrate brain forever abolishes an essential behavior
title_short Removing a single neuron in a vertebrate brain forever abolishes an essential behavior
title_sort removing a single neuron in a vertebrate brain forever abolishes an essential behavior
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7022180/
https://www.ncbi.nlm.nih.gov/pubmed/32001507
http://dx.doi.org/10.1073/pnas.1918578117
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