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Neuromodulatory selection of motor neuron recruitment patterns in a visuomotor behavior increases speed

View ORCID ProfileUrvashi Jha, View ORCID ProfileVatsala Thirumalai
doi: https://doi.org/10.1101/683649
Urvashi Jha
1National Centre for Biological Sciences, Tata Institute of Fundamental Research; Bangalore; Karnataka-560065; India
2SASTRA Deemed University; School of Chemical and Biotechnology; Thanjavur; Tamil Nadu-613401; India
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  • ORCID record for Urvashi Jha
Vatsala Thirumalai
1National Centre for Biological Sciences, Tata Institute of Fundamental Research; Bangalore; Karnataka-560065; India
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  • ORCID record for Vatsala Thirumalai
  • For correspondence: vatsala@ncbs.res.in
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Summary

Animals generate locomotion at different speeds to suit their behavioral needs. Spinal circuits generate locomotion at these varying speeds by sequential activation of different spinal interneurons and motor neurons. Larval zebrafish can generate slow swims for prey capture and exploration by activation of secondary motor neurons and much faster and vigorous swims during escapes and struggles via the additional activation of primary motor neurons. Neuromodulators are known to alter motor output of spinal circuits yet their precise role in speed regulation is not understood well. Here, in the context of optomotor response (OMR), an innate, evoked locomotor behavior, we show that dopamine (DA) provides an additional layer to regulation of swim speed in larval zebrafish. Activation of D1-like receptors increases swim speed during OMR in free-swimming larvae. By analysing tail bend kinematics in head-restrained larvae, we show that the increase in speed is actuated by larger tail bends. Whole cell patch clamp recordings from motor neurons reveal that during OMR, typically only secondary motor neurons are active while primary motor neurons are quiescent. Activation of D1-like receptors increases motor drive from secondary motor neurons by decreasing spike threshold and latency. In addition, D1-like receptor activation enhances excitability and recruits quiescent primary motor neurons. Our findings provide an example of neuromodulatory reconfiguration of spinal motor neuron speed modules such that members are selectively recruited and motor drive is increased to effect changes in locomotor speed.

Highlights

  • Zebrafish larvae generate swims of increased speed during optomotor response when D1-like receptors are activated.

  • D1-like receptor activation increases the extent of tail bending during forward swims and turns resulting in increased swim speed.

  • Neuromodulation via D1-like receptors increases motor drive by enhancing excitability of ‘slow’ motor neurons. In addition, D1-like receptor activation recruits quiescent ‘fast’ motor neurons to increase swim speed.

  • This demonstrates neuromodulatory selection of motor neurons belonging to different ‘speed’ modules to alter swimming behavior.

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Footnotes

  • To remove autotext that appeared on top of the figures in the PDF generated by biorxiv.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted June 28, 2019.
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Neuromodulatory selection of motor neuron recruitment patterns in a visuomotor behavior increases speed
Urvashi Jha, Vatsala Thirumalai
bioRxiv 683649; doi: https://doi.org/10.1101/683649
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Neuromodulatory selection of motor neuron recruitment patterns in a visuomotor behavior increases speed
Urvashi Jha, Vatsala Thirumalai
bioRxiv 683649; doi: https://doi.org/10.1101/683649

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