Literature DB >> 33417596

Persistent thermal input controls steering behavior in Caenorhabditis elegans.

Muneki Ikeda1,2,3, Hirotaka Matsumoto4,5, Eduardo J Izquierdo6.   

Abstract

Motile organisms actively detect environmental signals and migrate to a preferable environment. Especially, small animals convert subtle spatial difference in sensory input into orientation behavioral output for directly steering toward a destination, but the neural mechanisms underlying steering behavior remain elusive. Here, we analyze a C. elegans thermotactic behavior in which a small number of neurons are shown to mediate steering toward a destination temperature. We construct a neuroanatomical model and use an evolutionary algorithm to find configurations of the model that reproduce empirical thermotactic behavior. We find that, in all the evolved models, steering curvature are modulated by temporally persistent thermal signals sensed beyond the time scale of sinusoidal locomotion of C. elegans. Persistent rise in temperature decreases steering curvature resulting in straight movement of model worms, whereas fall in temperature increases curvature resulting in crooked movement. This relation between temperature change and steering curvature reproduces the empirical thermotactic migration up thermal gradients and steering bias toward higher temperature. Further, spectrum decomposition of neural activities in model worms show that thermal signals are transmitted from a sensory neuron to motor neurons on the longer time scale than sinusoidal locomotion of C. elegans. Our results suggest that employments of temporally persistent sensory signals enable small animals to steer toward a destination in natural environment with variable, noisy, and subtle cues.

Entities:  

Mesh:

Year:  2021        PMID: 33417596      PMCID: PMC7819614          DOI: 10.1371/journal.pcbi.1007916

Source DB:  PubMed          Journal:  PLoS Comput Biol        ISSN: 1553-734X            Impact factor:   4.475


  32 in total

Review 1.  Active sensation during orientation behavior in the Drosophila larva: more sense than luck.

Authors:  Alex Gomez-Marin; Matthieu Louis
Journal:  Curr Opin Neurobiol       Date:  2011-12-12       Impact factor: 6.627

2.  The C. elegans thermosensory neuron AFD responds to warming.

Authors:  Koutarou D Kimura; Atsushi Miyawaki; Kunihiro Matsumoto; Ikue Mori
Journal:  Curr Biol       Date:  2004-07-27       Impact factor: 10.834

3.  Sensory determinants of behavioral dynamics in Drosophila thermotaxis.

Authors:  Mason Klein; Bruno Afonso; Ashley J Vonner; Luis Hernandez-Nunez; Matthew Berck; Christopher J Tabone; Elizabeth A Kane; Vincent A Pieribone; Michael N Nitabach; Albert Cardona; Marta Zlatic; Simon G Sprecher; Marc Gershow; Paul A Garrity; Aravinthan D T Samuel
Journal:  Proc Natl Acad Sci U S A       Date:  2014-12-30       Impact factor: 11.205

4.  Cholinergic Sensorimotor Integration Regulates Olfactory Steering.

Authors:  He Liu; Wenxing Yang; Taihong Wu; Fengyun Duan; Edward Soucy; Xin Jin; Yun Zhang
Journal:  Neuron       Date:  2017-12-28       Impact factor: 17.173

5.  Computational rules for chemotaxis in the nematode C. elegans.

Authors:  T C Ferrée; S R Lockery
Journal:  J Comput Neurosci       Date:  1999 May-Jun       Impact factor: 1.621

6.  Complex RIA calcium dynamics and its function in navigational behavior.

Authors:  Michael Hendricks; Yun Zhang
Journal:  Worm       Date:  2013-07-12

7.  High-throughput behavioral analysis in C. elegans.

Authors:  Nicholas A Swierczek; Andrew C Giles; Catharine H Rankin; Rex A Kerr
Journal:  Nat Methods       Date:  2011-06-05       Impact factor: 28.547

8.  Active sampling and decision making in Drosophila chemotaxis.

Authors:  Alex Gomez-Marin; Greg J Stephens; Matthieu Louis
Journal:  Nat Commun       Date:  2011-08-23       Impact factor: 14.919

9.  Context-dependent operation of neural circuits underlies a navigation behavior in Caenorhabditis elegans.

Authors:  Muneki Ikeda; Shunji Nakano; Andrew C Giles; Linghuan Xu; Wagner Steuer Costa; Alexander Gottschalk; Ikue Mori
Journal:  Proc Natl Acad Sci U S A       Date:  2020-03-02       Impact factor: 11.205

10.  Identification of animal behavioral strategies by inverse reinforcement learning.

Authors:  Shoichiro Yamaguchi; Honda Naoki; Muneki Ikeda; Yuki Tsukada; Shunji Nakano; Ikue Mori; Shin Ishii
Journal:  PLoS Comput Biol       Date:  2018-05-02       Impact factor: 4.475

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