Decoding a neural circuit controlling global animal state in C. elegans.

ELife
Patrick LaurentMario de Bono

Abstract

Brains organize behavior and physiology to optimize the response to threats or opportunities. We dissect how 21% O2, an indicator of surface exposure, reprograms C. elegans' global state, inducing sustained locomotory arousal and altering expression of neuropeptides, metabolic enzymes, and other non-neural genes. The URX O2-sensing neurons drive arousal at 21% O2 by tonically activating the RMG interneurons. Stimulating RMG is sufficient to switch behavioral state. Ablating the ASH, ADL, or ASK sensory neurons connected to RMG by gap junctions does not disrupt arousal. However, disrupting cation currents in these neurons curtails RMG neurosecretion and arousal. RMG signals high O2 by peptidergic secretion. Neuropeptide reporters reveal neural circuit state, as neurosecretion stimulates neuropeptide expression. Neural imaging in unrestrained animals shows that URX and RMG encode O2 concentration rather than behavior, while the activity of downstream interneurons such as AVB and AIY reflect both O2 levels and the behavior being executed.

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Citations

Aug 5, 2015·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·Christopher Fang-YenAravinthan D T Samuel
Sep 27, 2016·Current Opinion in Neurobiology·Sophie Rengarajan, Elissa A Hallem
Feb 2, 2017·Proceedings of the National Academy of Sciences of the United States of America·Heeun JangCornelia I Bargmann
Mar 23, 2017·Immunity·Noah J Silverstein, Jun R Huh
Jan 19, 2017·Nature·Changchun ChenMario de Bono
Jun 24, 2017·Science·Annika L A NicholsManuel Zimmer
Feb 6, 2017·Nature Reviews. Neuroscience·Manuel SchröterEdward T Bullmore
Apr 25, 2018·Proceedings of the National Academy of Sciences of the United States of America·Tianqi XuQuan Wen
Nov 5, 2019·Journal of Neuroendocrinology·Kelly J RobinsonMike Ludwig
Nov 14, 2019·ELife·May DobosiewiczCornelia I Bargmann
Jul 1, 2018·Proceedings of the National Academy of Sciences of the United States of America·Patrick LaurentMario de Bono
Sep 12, 2018·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·Harris S KaplanManuel Zimmer
Dec 24, 2018·Nature Methods·Jeffrey B LeeSharad Ramanathan
Oct 8, 2020·Genetics·Steven W FlavellYoung-Jai You
Nov 5, 2020·Journal of Neurogenetics·Douglas S Portman
Sep 16, 2019·IScience·Rony SotoCheryl Van Buskirk
May 7, 2021·Genetics·Steven W FlavellYoung-Jai You
Sep 10, 2021·ELife·Thanh Thi Vuong-BrenderMario de Bono

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Methods Mentioned

BETA
GTPase
FRET
transgenic

Software Mentioned

Micromanger
TopHat
Cuffdiff
Cuffmerge
FastQC
custom Perl scripts
Cufflinks
Zentracker
Matlab
Neuron Analyzer

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