» Articles » PMID: 32001507

Removing a Single Neuron in a Vertebrate Brain Forever Abolishes an Essential Behavior

Overview
Specialty Science
Date 2020 Feb 1
PMID 32001507
Citations 22
Authors
Affiliations
Soon will be listed here.
Abstract

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.

Citing Articles

Stabilizing selection in an identified multisensory neuron in blind cavefish.

Hildebrandt M, Kotewitsch M, Kaupp S, Salomon S, Schuster S, Machnik P Proc Natl Acad Sci U S A. 2024; 121(49):e2415854121.

PMID: 39556758 PMC: 11626160. DOI: 10.1073/pnas.2415854121.


Thymosin β4 promotes zebrafish Mauthner axon regeneration by facilitating actin polymerization through binding to G-actin.

Song Z, Han A, Hu B BMC Biol. 2024; 22(1):244.

PMID: 39443925 PMC: 11515629. DOI: 10.1186/s12915-024-02045-2.


MicroRNA-9 promotes axon regeneration of mauthner-cell in zebrafish via her6/ calcium activity pathway.

Shen Y, Chen X, Song Z, Yao H, Han A, Zhang Y Cell Mol Life Sci. 2024; 81(1):104.

PMID: 38411738 PMC: 10899279. DOI: 10.1007/s00018-024-05117-2.


The archerfish predictive C-start.

Schuster S J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2023; 209(5):827-837.

PMID: 37481772 PMC: 10465633. DOI: 10.1007/s00359-023-01658-2.


Recordings in an integrating central neuron reveal the mode of action of isoeugenol.

Machnik P, Biazar N, Schuster S Commun Biol. 2023; 6(1):309.

PMID: 36959338 PMC: 10036640. DOI: 10.1038/s42003-023-04695-4.


References
1.
DiDomenico R, Eaton R . Seven principles for command and the neural causation of behavior. Brain Behav Evol. 1988; 31(3):125-40. DOI: 10.1159/000116580. View

2.
Nakayama H, Oda Y . Common sensory inputs and differential excitability of segmentally homologous reticulospinal neurons in the hindbrain. J Neurosci. 2004; 24(13):3199-209. PMC: 6730040. DOI: 10.1523/JNEUROSCI.4419-03.2004. View

3.
Edwards D, Heitler W, Krasne F . Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish. Trends Neurosci. 1999; 22(4):153-61. DOI: 10.1016/s0166-2236(98)01340-x. View

4.
Howland H . Optimal strategies for predator avoidance: the relative importance of speed and manoeuvrability. J Theor Biol. 1974; 47(2):333-50. DOI: 10.1016/0022-5193(74)90202-1. View

5.
Papadopoulou M, Cassenaer S, Nowotny T, Laurent G . Normalization for sparse encoding of odors by a wide-field interneuron. Science. 2011; 332(6030):721-5. PMC: 3242050. DOI: 10.1126/science.1201835. View