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A command-like descending neuron that coordinately activates backward and inhibits forward locomotion

Carreira-Rosario, Arnaldo and Zarin, Aref Arzan and Clark, Matthew Q. and Manning, Laurina and Fetter, Richard and Cardona, Albert and Doe, Chris Q. (2018) A command-like descending neuron that coordinately activates backward and inhibits forward locomotion. . (Unpublished) http://resolver.caltech.edu/CaltechAUTHORS:20181030-083159533

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Abstract

Command-like descending neurons can induce many behaviors, such as backward locomotion, escape, feeding, courtship, egg-laying, or grooming. In most animals it remains unknown how neural circuits switch between these antagonistic behaviors: via top-down activation/inhibition of antagonistic circuits or via reciprocal inhibition between antagonistic circuits. Here we use genetic screens, intersectional genetics, circuit reconstruction by electron microscopy, and functional optogenetics to identify a bilateral pair of larval “mooncrawler descending neurons” (MDNs) with command-like ability to coordinately induce backward locomotion and block forward locomotion; the former by activating a backward-specific premotor neuron, and the latter by disynaptic inhibition of a forward-specific premotor neuron. In contrast, direct reciprocal inhibition between forward and backward circuits was not observed. Thus, MDNs coordinate a transition between antagonistic larval locomotor behaviors. Interestingly, larval MDNs persist into adulthood, where they can trigger backward walking. Thus, MDNs induce backward locomotion in both limbless and limbed animals.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/339556DOIDiscussion Paper
ORCID:
AuthorORCID
Zarin, Aref Arzan0000-0003-0484-3622
Clark, Matthew Q.0000-0002-1113-9388
Fetter, Richard0000-0002-1558-100X
Cardona, Albert0000-0003-4941-6536
Doe, Chris Q.0000-0001-5980-8029
Additional Information: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 4.0 International license. bioRxiv preprint first posted online Jun. 5, 2018. We thank Jim Truman and Matthieu Louis for unpublished fly lines targeting MDN and Pair1 neurons. We thank Brandon Mark for MATLAB scripts. We thank Todd Laverty, Gerry Rubin, Barry Dickson, Ben White, Miki Fujioka, Julie Simpson and Adam Claridge-Chang for fly stocks, and Barry Dickson, Shawn Lockery, Matthieu Louis, and Tory Herman for comments on the manuscript. We thank Avinash Kandelwal and Laura Herren for annotating neurons, and Keiko Hirono for generating transgenic constructs. Transgenic lines were generated by BestGene (Chino Hills, CA) or Genetivision (Houston, TX). Stocks obtained from the Bloomington Drosophila Stock Center (NIH P40OD018537) were used in this study. Funding was provided by HHMI (CQD, AC-R, AAZ, LM), NIH HD27056 (CQD, MQC), F32NS105350-01A1 (AC-R), T32HD007348-24 (MQC), and T32GM007413-36 (MQC). Author Contributions: MQC conceived of the project; MQC, LM, AC-R, AAZ performed experiments; RF generated the ssTEM volume; AAZ and AC annotated neurons in CATMAID; MQC, AC-R, AAZ, AC and CQD wrote the paper. All authors commented and approved of the manuscript.
Funders:
Funding AgencyGrant Number
NIHP40OD018537
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NIHHD27056
NIH Postdoctoral FellowshipF32NS105350-01A1
NIH Predoctoral FellowshipT32HD007348-24
NIH Predoctoral FellowshipT32GM007413-36
Subject Keywords:behavioral switching, backward locomotion, crawling, walking, sensorimotor, wave propagation, descending interneuron, aversion, neural circuit, Drosophila
Record Number:CaltechAUTHORS:20181030-083159533
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20181030-083159533
Official Citation:A command-like descending neuron that coordinately activates backward and inhibits forward locomotion. Chris Q Doe, Aref Arzan Zarin, Arnaldo Carreira-Rosario, Matthew Q Clark, Laurina Manning, Albert Cardona, Richard D Fetter. bioRxiv 339556; doi: https://doi.org/10.1101/339556
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:90490
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:30 Oct 2018 17:04
Last Modified:30 Oct 2018 17:04

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