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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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 cellmediated 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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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 cellmediated 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.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1918578117</identifier><identifier>PMID: 32001507</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Ablation ; Animals ; Axons ; Axons - physiology ; Biological Sciences ; Brain ; Cell survival ; Embryo, Nonmammalian - physiology ; Escape behavior ; Escape Reaction - physiology ; Larva - physiology ; Nervous system ; Nervous System - growth & development ; Neurons ; Neurons - cytology ; Neurons - physiology ; Survival ; Survival value ; Vertebrates ; Zebrafish</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2020-02, Vol.117 (6), p.3254-3260</ispartof><rights>Copyright © 2020 the Author(s). Published by PNAS.</rights><rights>Copyright National Academy of Sciences Feb 11, 2020</rights><rights>Copyright © 2020 the Author(s). 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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 cellmediated 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.</description><subject>Ablation</subject><subject>Animals</subject><subject>Axons</subject><subject>Axons - physiology</subject><subject>Biological Sciences</subject><subject>Brain</subject><subject>Cell survival</subject><subject>Embryo, Nonmammalian - physiology</subject><subject>Escape behavior</subject><subject>Escape Reaction - physiology</subject><subject>Larva - physiology</subject><subject>Nervous system</subject><subject>Nervous System - growth & development</subject><subject>Neurons</subject><subject>Neurons - cytology</subject><subject>Neurons - physiology</subject><subject>Survival</subject><subject>Survival value</subject><subject>Vertebrates</subject><subject>Zebrafish</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc2LFDEQxYMo7uzq2ZPS4MVL71a-k4sgi67CgiDqNSS91TsZepIx6R7wvzfDrOPHJQWvfnlU1SPkBYVLCppf7ZKvl9RSI7WhVD8iKwqW9kpYeExWAEz3RjBxRs5r3QCAlQaekjPOAKgEvSLfv-A272O673xXW5mwS7iUnLqYmrTHMmMofsauvU0ac8Emdj7kKdY11s6nDmvFNEc_dQHXfh9zeUaejH6q-PyhXpBvH95_vf7Y336--XT97rYfJNi5FwEVV340GHQQyggwVg-BI47eSk41eDYIYyVazYQKg1VBBq3EXRiM4IpfkLdH390Stng3tDGKn9yuxK0vP1320f3bSXHt7vPeaWCMGmgGbx4MSv6xYJ3dNtYBp8knzEt1jMvD1YQ0DX39H7rJS0ltvQMlDLPc6kZdHamh5FoLjqdhKLhDZu6QmfuTWfvx6u8dTvzvkBrw8ghs6pzLqc-UZUZryX8BfmqdRQ</recordid><startdate>20200211</startdate><enddate>20200211</enddate><creator>Hecker, Alexander</creator><creator>Schulze, Wolfram</creator><creator>Oster, Jakob</creator><creator>Richter, David O.</creator><creator>Schuster, Stefan</creator><general>National Academy of Sciences</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6537-6055</orcidid></search><sort><creationdate>20200211</creationdate><title>Removing a single neuron in a vertebrate brain forever abolishes an essential behavior</title><author>Hecker, Alexander ; 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subjects | Ablation Animals Axons Axons - physiology Biological Sciences Brain Cell survival Embryo, Nonmammalian - physiology Escape behavior Escape Reaction - physiology Larva - physiology Nervous system Nervous System - growth & development Neurons Neurons - cytology Neurons - physiology Survival Survival value Vertebrates Zebrafish |
title | Removing a single neuron in a vertebrate brain forever abolishes an essential behavior |
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