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A conserved neuropeptide system links head and body motor circuits to enable adaptive behavior

View ORCID ProfileShankar Ramachandran, Navonil Banerjee, Raja Bhattacharya, Michele L Lemons, Jeremy Florman, Christopher M. Lambert, Denis Touroutine, Kellianne Alexander, Liliane Schoofs, View ORCID ProfileMark J Alkema, Isabel Beets, View ORCID ProfileMichael M. Francis
doi: https://doi.org/10.1101/2020.04.27.064550
Shankar Ramachandran
1Department of Neurobiology 715 Lazare Research Building University of Massachusetts Medical School 364 Plantation St. Worcester, MA 01605
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  • ORCID record for Shankar Ramachandran
Navonil Banerjee
1Department of Neurobiology 715 Lazare Research Building University of Massachusetts Medical School 364 Plantation St. Worcester, MA 01605
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Raja Bhattacharya
1Department of Neurobiology 715 Lazare Research Building University of Massachusetts Medical School 364 Plantation St. Worcester, MA 01605
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Michele L Lemons
2Department of Biological and Physical Sciences Assumption University Worcester, MA 01609
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Jeremy Florman
1Department of Neurobiology 715 Lazare Research Building University of Massachusetts Medical School 364 Plantation St. Worcester, MA 01605
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Christopher M. Lambert
1Department of Neurobiology 715 Lazare Research Building University of Massachusetts Medical School 364 Plantation St. Worcester, MA 01605
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Denis Touroutine
1Department of Neurobiology 715 Lazare Research Building University of Massachusetts Medical School 364 Plantation St. Worcester, MA 01605
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Kellianne Alexander
1Department of Neurobiology 715 Lazare Research Building University of Massachusetts Medical School 364 Plantation St. Worcester, MA 01605
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Liliane Schoofs
3Department of Biology University of Leuven (KU Leuven) Leuven, Belgium
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Mark J Alkema
1Department of Neurobiology 715 Lazare Research Building University of Massachusetts Medical School 364 Plantation St. Worcester, MA 01605
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Isabel Beets
3Department of Biology University of Leuven (KU Leuven) Leuven, Belgium
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Michael M. Francis
1Department of Neurobiology 715 Lazare Research Building University of Massachusetts Medical School 364 Plantation St. Worcester, MA 01605
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  • For correspondence: michael.francis@umassmed.edu
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SUMMARY

Neuromodulators promote adaptive behaviors that are often complex and involve concerted activity changes across circuits that are often not physically connected. It is not well understood how neuromodulatory systems accomplish these tasks. Here we show that the C. elegans NLP-12 neuropeptide system shapes responses to food availability by modulating the activity of head and body wall motor neurons through alternate G-protein coupled receptor (GPCR) targets, CKR-1 and CKR-2. We show ckr-2 deletion reduces body bend depth during movement under basal conditions. We demonstrate CKR-1 is a functional NLP-12 receptor and define its expression in the nervous system. In contrast to basal locomotion, biased CKR-1 GPCR stimulation of head motor neurons promotes turning during local searching. Deletion of ckr-1 reduces head neuron activity and diminishes turning while specific ckr-1 overexpression or head neuron activation promote turning. Thus, our studies suggest locomotor responses to changing food availability are regulated through conditional NLP-12 stimulation of head or body wall motor circuits.

Impact statement Investigation of neuromodulatory control of ethologically conserved area-restricted food search behavior shows that NLP-12 stimulation of the head motor circuit promotes food searching through the previously uncharacterized CKR-1 GPCR.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Funding: This work was supported by NIH R21NS093492 (MMF), European Research Council 340318 and Research Foundation Flanders grant G0C0618N (IB).

  • Disclosure Statement: The authors have nothing to declare.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted November 03, 2021.
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A conserved neuropeptide system links head and body motor circuits to enable adaptive behavior
Shankar Ramachandran, Navonil Banerjee, Raja Bhattacharya, Michele L Lemons, Jeremy Florman, Christopher M. Lambert, Denis Touroutine, Kellianne Alexander, Liliane Schoofs, Mark J Alkema, Isabel Beets, Michael M. Francis
bioRxiv 2020.04.27.064550; doi: https://doi.org/10.1101/2020.04.27.064550
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A conserved neuropeptide system links head and body motor circuits to enable adaptive behavior
Shankar Ramachandran, Navonil Banerjee, Raja Bhattacharya, Michele L Lemons, Jeremy Florman, Christopher M. Lambert, Denis Touroutine, Kellianne Alexander, Liliane Schoofs, Mark J Alkema, Isabel Beets, Michael M. Francis
bioRxiv 2020.04.27.064550; doi: https://doi.org/10.1101/2020.04.27.064550

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