Literature DB >> 27222228

Regulation of two motor patterns enables the gradual adjustment of locomotion strategy in Caenorhabditis elegans.

Ingrid Hums1, Julia Riedl1, Fanny Mende1, Saul Kato1, Harris S Kaplan1, Richard Latham1, Michael Sonntag1, Lisa Traunmüller1, Manuel Zimmer1.   

Abstract

In animal locomotion a tradeoff exists between stereotypy and flexibility: fast long-distance travelling (LDT) requires coherent regular motions, while local sampling and area-restricted search (ARS) rely on flexible movements. We report here on a posture control system in C. elegans that coordinates these needs. Using quantitative posture analysis we explain worm locomotion as a composite of two modes: regular undulations versus flexible turning. Graded reciprocal regulation of both modes allows animals to flexibly adapt their locomotion strategy under sensory stimulation along a spectrum ranging from LDT to ARS. Using genetics and functional imaging of neural activity we characterize the counteracting interneurons AVK and DVA that utilize FLP-1 and NLP-12 neuropeptides to control both motor modes. Gradual regulation of behaviors via this system is required for spatial navigation during chemotaxis. This work shows how a nervous system controls simple elementary features of posture to generate complex movements for goal-directed locomotion strategies.

Entities:  

Keywords:  C. elegans; locomotion; motor control; neuromodulation; neuroscience

Mesh:

Substances:

Year:  2016        PMID: 27222228      PMCID: PMC4880447          DOI: 10.7554/eLife.14116

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  59 in total

1.  Sensorimotor control during isothermal tracking in Caenorhabditis elegans.

Authors:  Linjiao Luo; Damon A Clark; David Biron; L Mahadevan; Aravinthan D T Samuel
Journal:  J Exp Biol       Date:  2006-12       Impact factor: 3.312

2.  The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis.

Authors:  J T Pierce-Shimomura; T M Morse; S R Lockery
Journal:  J Neurosci       Date:  1999-11-01       Impact factor: 6.167

3.  Experience-dependent modulation of C. elegans behavior by ambient oxygen.

Authors:  Benny H H Cheung; Merav Cohen; Candida Rogers; Onder Albayram; Mario de Bono
Journal:  Curr Biol       Date:  2005-05-24       Impact factor: 10.834

4.  Hypoxia and the HIF-1 transcriptional pathway reorganize a neuronal circuit for oxygen-dependent behavior in Caenorhabditis elegans.

Authors:  Andy J Chang; Cornelia I Bargmann
Journal:  Proc Natl Acad Sci U S A       Date:  2008-05-13       Impact factor: 11.205

5.  Global brain dynamics embed the motor command sequence of Caenorhabditis elegans.

Authors:  Saul Kato; Harris S Kaplan; Tina Schrödel; Susanne Skora; Theodore H Lindsay; Eviatar Yemini; Shawn Lockery; Manuel Zimmer
Journal:  Cell       Date:  2015-10-17       Impact factor: 41.582

6.  Neuropeptides function in a homeostatic manner to modulate excitation-inhibition imbalance in C. elegans.

Authors:  Tamara M Stawicki; Seika Takayanagi-Kiya; Keming Zhou; Yishi Jin
Journal:  PLoS Genet       Date:  2013-05-02       Impact factor: 5.917

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

Authors:  Patrick Laurent; Zoltan Soltesz; Geoffrey M Nelson; Changchun Chen; Fausto Arellano-Carbajal; Emmanuel Levy; Mario de Bono
Journal:  Elife       Date:  2015-03-11       Impact factor: 8.140

8.  Automated monitoring and analysis of social behavior in Drosophila.

Authors:  Heiko Dankert; Liming Wang; Eric D Hoopfer; David J Anderson; Pietro Perona
Journal:  Nat Methods       Date:  2009-03-08       Impact factor: 28.547

9.  Serotonin and the neuropeptide PDF initiate and extend opposing behavioral states in C. elegans.

Authors:  Steven W Flavell; Navin Pokala; Evan Z Macosko; Dirk R Albrecht; Johannes Larsch; Cornelia I Bargmann
Journal:  Cell       Date:  2013-08-22       Impact factor: 41.582

10.  Directional locomotion of C. elegans in the absence of external stimuli.

Authors:  Margherita Peliti; John S Chuang; Shai Shaham
Journal:  PLoS One       Date:  2013-11-05       Impact factor: 3.240

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  16 in total

1.  Unsupervised learning of control signals and their encodings in Caenorhabditis elegans whole-brain recordings.

Authors:  Charles Fieseler; Manuel Zimmer; J Nathan Kutz
Journal:  J R Soc Interface       Date:  2020-12-09       Impact factor: 4.118

2.  Dynamic structure of locomotor behavior in walking fruit flies.

Authors:  Alexander Y Katsov; Limor Freifeld; Mark Horowitz; Seppe Kuehn; Thomas R Clandinin
Journal:  Elife       Date:  2017-07-25       Impact factor: 8.140

3.  Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire.

Authors:  Athira Athira; Daniel Dondorp; Jerneja Rudolf; Olivia Peytral; Marios Chatzigeorgiou
Journal:  PLoS Biol       Date:  2022-08-04       Impact factor: 9.593

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

Authors:  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
Journal:  Elife       Date:  2021-11-12       Impact factor: 8.713

5.  Functionally asymmetric motor neurons contribute to coordinating locomotion of Caenorhabditis elegans.

Authors:  Oleg Tolstenkov; Petrus Van der Auwera; Wagner Steuer Costa; Olga Bazhanova; Tim M Gemeinhardt; Amelie Cf Bergs; Alexander Gottschalk
Journal:  Elife       Date:  2018-09-11       Impact factor: 8.140

6.  Modulation of sensory information processing by a neuroglobin in Caenorhabditis elegans.

Authors:  Shigekazu Oda; Yu Toyoshima; Mario de Bono
Journal:  Proc Natl Acad Sci U S A       Date:  2017-05-23       Impact factor: 11.205

7.  Parallel Multimodal Circuits Control an Innate Foraging Behavior.

Authors:  Alejandro López-Cruz; Aylesse Sordillo; Navin Pokala; Qiang Liu; Patrick T McGrath; Cornelia I Bargmann
Journal:  Neuron       Date:  2019-02-26       Impact factor: 18.688

8.  Neuroendocrine modulation sustains the C. elegans forward motor state.

Authors:  Maria A Lim; Jyothsna Chitturi; Valeriya Laskova; Jun Meng; Daniel Findeis; Anne Wiekenberg; Ben Mulcahy; Linjiao Luo; Yan Li; Yangning Lu; Wesley Hung; Yixin Qu; Chi-Yip Ho; Douglas Holmyard; Ni Ji; Rebecca McWhirter; Aravinthan Dt Samuel; David M Miller; Ralf Schnabel; John A Calarco; Mei Zhen
Journal:  Elife       Date:  2016-11-18       Impact factor: 8.140

9.  Methods for analyzing neuronal structure and activity in Caenorhabditis elegans.

Authors:  Scott W Emmons; Eviatar Yemini; Manuel Zimmer
Journal:  Genetics       Date:  2021-08-09       Impact factor: 4.562

Review 10.  Sensorimotor integration in Caenorhabditis elegans: a reappraisal towards dynamic and distributed computations.

Authors:  Harris S Kaplan; Annika L A Nichols; Manuel Zimmer
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2018-09-10       Impact factor: 6.237

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