Optogenetic dissection of a behavioural module in the vertebrate spinal cord

Claire Wyart, Filippo Del Bene, Erica Warp, Ethan K. Scott, Dirk Trauner, Herwig Baier, Ehud Y. Isacoff

Research output: Contribution to journalArticle

Abstract

Locomotion relies on neural networks called central pattern generators (CPGs) that generate periodic motor commands for rhythmic movements. In vertebrates, the excitatory synaptic drive for inducing the spinal CPG can originate from either supraspinal glutamatergic inputs or from within the spinal cord. Here we identify a spinal input to the CPG that drives spontaneous locomotion using a combination of intersectional gene expression and optogenetics in zebrafish larvae. The photo-stimulation of one specific cell type was sufficient to induce a symmetrical tail beating sequence that mimics spontaneous slow forward swimming. This neuron is the Kolmer-Agduhr cell, which extends cilia into the central cerebrospinal-fluid-containing canal of the spinal cord and has an ipsilateral ascending axon that terminates in a series of consecutive segments. Genetically silencing Kolmer-Agduhr cells reduced the frequency of spontaneous free swimming, indicating that activity of Kolmer-Agduhr cells provides necessary tone for spontaneous forward swimming. Kolmer-Agduhr cells have been known for over 75 years, but their function has been mysterious. Our results reveal that during early development in zebrafish these cells provide a positive drive to the spinal CPG for spontaneous locomotion.

Original languageEnglish (US)
Pages (from-to)407-410
Number of pages4
JournalNature
Volume461
Issue number7262
DOIs
StatePublished - Sep 17 2009

Fingerprint

Optogenetics
Central Pattern Generators
Vertebrates
Dissection
Spinal Cord
Locomotion
Zebrafish
Cilia
Larva
Axons
Cerebrospinal Fluid
Tail
Gene Expression
Neurons

ASJC Scopus subject areas

  • Medicine(all)
  • General

Cite this

Wyart, C., Bene, F. D., Warp, E., Scott, E. K., Trauner, D., Baier, H., & Isacoff, E. Y. (2009). Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature, 461(7262), 407-410. https://doi.org/10.1038/nature08323

Optogenetic dissection of a behavioural module in the vertebrate spinal cord. / Wyart, Claire; Bene, Filippo Del; Warp, Erica; Scott, Ethan K.; Trauner, Dirk; Baier, Herwig; Isacoff, Ehud Y.

In: Nature, Vol. 461, No. 7262, 17.09.2009, p. 407-410.

Research output: Contribution to journalArticle

Wyart, C, Bene, FD, Warp, E, Scott, EK, Trauner, D, Baier, H & Isacoff, EY 2009, 'Optogenetic dissection of a behavioural module in the vertebrate spinal cord', Nature, vol. 461, no. 7262, pp. 407-410. https://doi.org/10.1038/nature08323
Wyart C, Bene FD, Warp E, Scott EK, Trauner D, Baier H et al. Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature. 2009 Sep 17;461(7262):407-410. https://doi.org/10.1038/nature08323
Wyart, Claire ; Bene, Filippo Del ; Warp, Erica ; Scott, Ethan K. ; Trauner, Dirk ; Baier, Herwig ; Isacoff, Ehud Y. / Optogenetic dissection of a behavioural module in the vertebrate spinal cord. In: Nature. 2009 ; Vol. 461, No. 7262. pp. 407-410.
@article{54c6b3a0dfb64924aaf1d3c1cfe7f1a7,
title = "Optogenetic dissection of a behavioural module in the vertebrate spinal cord",
abstract = "Locomotion relies on neural networks called central pattern generators (CPGs) that generate periodic motor commands for rhythmic movements. In vertebrates, the excitatory synaptic drive for inducing the spinal CPG can originate from either supraspinal glutamatergic inputs or from within the spinal cord. Here we identify a spinal input to the CPG that drives spontaneous locomotion using a combination of intersectional gene expression and optogenetics in zebrafish larvae. The photo-stimulation of one specific cell type was sufficient to induce a symmetrical tail beating sequence that mimics spontaneous slow forward swimming. This neuron is the Kolmer-Agduhr cell, which extends cilia into the central cerebrospinal-fluid-containing canal of the spinal cord and has an ipsilateral ascending axon that terminates in a series of consecutive segments. Genetically silencing Kolmer-Agduhr cells reduced the frequency of spontaneous free swimming, indicating that activity of Kolmer-Agduhr cells provides necessary tone for spontaneous forward swimming. Kolmer-Agduhr cells have been known for over 75 years, but their function has been mysterious. Our results reveal that during early development in zebrafish these cells provide a positive drive to the spinal CPG for spontaneous locomotion.",
author = "Claire Wyart and Bene, {Filippo Del} and Erica Warp and Scott, {Ethan K.} and Dirk Trauner and Herwig Baier and Isacoff, {Ehud Y.}",
year = "2009",
month = "9",
day = "17",
doi = "10.1038/nature08323",
language = "English (US)",
volume = "461",
pages = "407--410",
journal = "Nature Cell Biology",
issn = "1465-7392",
publisher = "Nature Publishing Group",
number = "7262",

}

TY - JOUR

T1 - Optogenetic dissection of a behavioural module in the vertebrate spinal cord

AU - Wyart, Claire

AU - Bene, Filippo Del

AU - Warp, Erica

AU - Scott, Ethan K.

AU - Trauner, Dirk

AU - Baier, Herwig

AU - Isacoff, Ehud Y.

PY - 2009/9/17

Y1 - 2009/9/17

N2 - Locomotion relies on neural networks called central pattern generators (CPGs) that generate periodic motor commands for rhythmic movements. In vertebrates, the excitatory synaptic drive for inducing the spinal CPG can originate from either supraspinal glutamatergic inputs or from within the spinal cord. Here we identify a spinal input to the CPG that drives spontaneous locomotion using a combination of intersectional gene expression and optogenetics in zebrafish larvae. The photo-stimulation of one specific cell type was sufficient to induce a symmetrical tail beating sequence that mimics spontaneous slow forward swimming. This neuron is the Kolmer-Agduhr cell, which extends cilia into the central cerebrospinal-fluid-containing canal of the spinal cord and has an ipsilateral ascending axon that terminates in a series of consecutive segments. Genetically silencing Kolmer-Agduhr cells reduced the frequency of spontaneous free swimming, indicating that activity of Kolmer-Agduhr cells provides necessary tone for spontaneous forward swimming. Kolmer-Agduhr cells have been known for over 75 years, but their function has been mysterious. Our results reveal that during early development in zebrafish these cells provide a positive drive to the spinal CPG for spontaneous locomotion.

AB - Locomotion relies on neural networks called central pattern generators (CPGs) that generate periodic motor commands for rhythmic movements. In vertebrates, the excitatory synaptic drive for inducing the spinal CPG can originate from either supraspinal glutamatergic inputs or from within the spinal cord. Here we identify a spinal input to the CPG that drives spontaneous locomotion using a combination of intersectional gene expression and optogenetics in zebrafish larvae. The photo-stimulation of one specific cell type was sufficient to induce a symmetrical tail beating sequence that mimics spontaneous slow forward swimming. This neuron is the Kolmer-Agduhr cell, which extends cilia into the central cerebrospinal-fluid-containing canal of the spinal cord and has an ipsilateral ascending axon that terminates in a series of consecutive segments. Genetically silencing Kolmer-Agduhr cells reduced the frequency of spontaneous free swimming, indicating that activity of Kolmer-Agduhr cells provides necessary tone for spontaneous forward swimming. Kolmer-Agduhr cells have been known for over 75 years, but their function has been mysterious. Our results reveal that during early development in zebrafish these cells provide a positive drive to the spinal CPG for spontaneous locomotion.

UR - http://www.scopus.com/inward/record.url?scp=70349295632&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=70349295632&partnerID=8YFLogxK

U2 - 10.1038/nature08323

DO - 10.1038/nature08323

M3 - Article

VL - 461

SP - 407

EP - 410

JO - Nature Cell Biology

JF - Nature Cell Biology

SN - 1465-7392

IS - 7262

ER -