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Research ArticleResearch Article: New Research, Sensory and Motor Systems

Spatiotemporal Transition in the Role of Synaptic Inhibition to the Tail Beat Rhythm of Developing Larval Zebrafish

Yann Roussel, Melissa Paradis, Stephanie F. Gaudreau, Ben W. Lindsey and Tuan V. Bui
eNeuro 31 January 2020, 7 (1) ENEURO.0508-18.2020; DOI: https://doi.org/10.1523/ENEURO.0508-18.2020
Yann Roussel
1Brain and Mind Research Institute, Centre for Neural Dynamics, Department of Biology, University of Ottawa, Ottawa K1N 6N5, Canada
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Melissa Paradis
1Brain and Mind Research Institute, Centre for Neural Dynamics, Department of Biology, University of Ottawa, Ottawa K1N 6N5, Canada
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Stephanie F. Gaudreau
1Brain and Mind Research Institute, Centre for Neural Dynamics, Department of Biology, University of Ottawa, Ottawa K1N 6N5, Canada
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Ben W. Lindsey
1Brain and Mind Research Institute, Centre for Neural Dynamics, Department of Biology, University of Ottawa, Ottawa K1N 6N5, Canada
2Rady Faculty of Health Sciences, Max Rady College of Medicine, Department of Human Anatomy and Cell Science, University of Manitoba, Winnipeg R3E 0J9, Canada
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Tuan V. Bui
1Brain and Mind Research Institute, Centre for Neural Dynamics, Department of Biology, University of Ottawa, Ottawa K1N 6N5, Canada
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Abstract

Significant maturation of swimming in zebrafish (Danio rerio) occurs within the first few days of life when fish transition from coiling movements to burst swimming and then to beat-and-glide swimming. This maturation occurs against a backdrop of numerous developmental changes - neurogenesis, a transition from predominantly electrical to chemical-based neurotransmission, and refinement of intrinsic properties. There is evidence that spinal locomotor circuits undergo fundamental changes as the zebrafish transitions from burst to beat-and-glide swimming. Our electrophysiological recordings confirm that the operation of spinal locomotor circuits becomes increasingly reliant on glycinergic neurotransmission for rhythmogenesis governing the rhythm of tail beats. This transition occurred at the same time that we observed a change in rhythmicity of synaptic inhibition to spinal motoneurons (MNs). When we examined whether the transition from weakly to strongly glycinergic dependent rhythmogenesis occurred at a uniform pace across the length of the spinal cord, we found that this transition occurred earlier at caudal segments than at rostral segments of the spinal cord. Furthermore, while this rhythmogenic transition occurred when fish transition from burst swimming to beat-and-glide swimming, these two transitions were not interdependent. These results suggest that there is a developmental transition in the operation of spinal locomotor circuits that is gradually set in place in the spinal cord in a caudo-rostral temporal sequence.

  • motor maturation
  • network oscillators
  • spinal locomotor circuits
  • swimming
  • synaptic inhibition
  • zebrafish

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by the Canadian Institutes of Health Research Postdoctoral Fellowship MFE-158137 and the Natural Sciences and Engineering Research Council of Canada Discovery Grant RGPIN-2015–06403.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Spatiotemporal Transition in the Role of Synaptic Inhibition to the Tail Beat Rhythm of Developing Larval Zebrafish
Yann Roussel, Melissa Paradis, Stephanie F. Gaudreau, Ben W. Lindsey, Tuan V. Bui
eNeuro 31 January 2020, 7 (1) ENEURO.0508-18.2020; DOI: 10.1523/ENEURO.0508-18.2020

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Spatiotemporal Transition in the Role of Synaptic Inhibition to the Tail Beat Rhythm of Developing Larval Zebrafish
Yann Roussel, Melissa Paradis, Stephanie F. Gaudreau, Ben W. Lindsey, Tuan V. Bui
eNeuro 31 January 2020, 7 (1) ENEURO.0508-18.2020; DOI: 10.1523/ENEURO.0508-18.2020
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Keywords

  • motor maturation
  • network oscillators
  • spinal locomotor circuits
  • swimming
  • synaptic inhibition
  • zebrafish

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