Literature DB >> 24430127

Mechanistic analysis of the search behaviour of Caenorhabditis elegans.

Liliana C M Salvador1, Frederic Bartumeus, Simon A Levin, William S Ryu.   

Abstract

A central question in movement research is how animals use information and movement to promote encounter success. Current random search theory identifies reorientation patterns as key to the compromise between optimizing encounters for both nearby and faraway targets, but how the balance between intrinsic motor programmes and previous environmental experience determines the occurrence of these reorientation behaviours remains unknown. We used high-resolution tracking and imaging data to describe the complete motor behaviour of Caenorhabditis elegans when placed in a novel environment (one in which food is absent). Movement in C. elegans is structured around different reorientation behaviours, and we measured how these contributed to changing search strategies as worms became familiar with their new environment. This behavioural transition shows that different reorientation behaviours are governed by two processes: (i) an environmentally informed 'extrinsic' strategy that is influenced by recent experience and that controls for area-restricted search behaviour, and (ii) a time-independent, 'intrinsic' strategy that reduces spatial oversampling and improves random encounter success. Our results show how movement strategies arise from a balance between intrinsic and extrinsic mechanisms, that search behaviour in C. elegans is initially determined by expectations developed from previous environmental experiences, and which reorientation behaviours are modified as information is acquired from new environments.

Entities:  

Keywords:  Caenorhabditis elegans; environmental uncertainty; reorientation patterns; search behaviour; stochasticity; superdiffusion

Mesh:

Year:  2014        PMID: 24430127      PMCID: PMC3899880          DOI: 10.1098/rsif.2013.1092

Source DB:  PubMed          Journal:  J R Soc Interface        ISSN: 1742-5662            Impact factor:   4.118


  33 in total

1.  From molecular noise to behavioural variability in a single bacterium.

Authors:  Ekaterina Korobkova; Thierry Emonet; Jose M G Vilar; Thomas S Shimizu; Philippe Cluzel
Journal:  Nature       Date:  2004-04-01       Impact factor: 49.962

2.  Optimizing the success of random searches.

Authors:  G M Viswanathan; S V Buldyrev; S Havlin; M G da Luz; E P Raposo; H E Stanley
Journal:  Nature       Date:  1999-10-28       Impact factor: 49.962

3.  A circuit for navigation in Caenorhabditis elegans.

Authors:  Jesse M Gray; Joseph J Hill; Cornelia I Bargmann
Journal:  Proc Natl Acad Sci U S A       Date:  2005-02-02       Impact factor: 11.205

4.  Computer-driven automatic identification of locomotion states in Caenorhabditis elegans.

Authors:  Katsunori Hoshi; Ryuzo Shingai
Journal:  J Neurosci Methods       Date:  2006-06-05       Impact factor: 2.390

5.  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

Review 6.  Genetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans.

Authors:  I Mori
Journal:  Annu Rev Genet       Date:  1999       Impact factor: 16.830

Review 7.  Neuronal substrates of complex behaviors in C. elegans.

Authors:  Mario de Bono; Andres Villu Maricq
Journal:  Annu Rev Neurosci       Date:  2005       Impact factor: 12.449

8.  Quantitative classification and natural clustering of Caenorhabditis elegans behavioral phenotypes.

Authors:  Wei Geng; Pamela Cosman; Joong-Hwan Baek; Charles C Berry; William R Schafer
Journal:  Genetics       Date:  2003-11       Impact factor: 4.562

9.  Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans.

Authors:  Thomas Hills; Penelope J Brockie; Andres V Maricq
Journal:  J Neurosci       Date:  2004-02-04       Impact factor: 6.167

10.  An automated system for measuring parameters of nematode sinusoidal movement.

Authors:  Christopher J Cronin; Jane E Mendel; Saleem Mukhtar; Young-Mee Kim; Robert C Stirbl; Jehoshua Bruck; Paul W Sternberg
Journal:  BMC Genet       Date:  2005-02-07       Impact factor: 2.797

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  16 in total

1.  Long-range correlations and fractal dynamics in C. elegans: Changes with aging and stress.

Authors:  Luiz G A Alves; Peter B Winter; Leonardo N Ferreira; Renée M Brielmann; Richard I Morimoto; Luís A N Amaral
Journal:  Phys Rev E       Date:  2017-08-29       Impact factor: 2.529

2.  Modelling the ballistic-to-diffusive transition in nematode motility reveals variation in exploratory behaviour across species.

Authors:  Stephen J Helms; W Mathijs Rozemuller; Antonio Carlos Costa; Leon Avery; Greg J Stephens; Thomas S Shimizu
Journal:  J R Soc Interface       Date:  2019-08-28       Impact factor: 4.118

3.  Farming and public goods production in Caenorhabditis elegans populations.

Authors:  Shashi Thutupalli; Sravanti Uppaluri; George W A Constable; Simon A Levin; Howard A Stone; Corina E Tarnita; Clifford P Brangwynne
Journal:  Proc Natl Acad Sci U S A       Date:  2017-02-09       Impact factor: 11.205

4.  Individual exploration and selective social learning: balancing exploration-exploitation trade-offs in collective foraging.

Authors:  Ketika Garg; Christopher T Kello; Paul E Smaldino
Journal:  J R Soc Interface       Date:  2022-04-27       Impact factor: 4.293

5.  A stochastic neuronal model predicts random search behaviors at multiple spatial scales in C. elegans.

Authors:  Steven B Augustine; Kristy J Lawton; Theodore H Lindsay; Tod R Thiele; William M Roberts; Eduardo J Izquierdo; Serge Faumont; Rebecca A Lindsay; Matthew Cale Britton; Navin Pokala; Cornelia I Bargmann; Shawn R Lockery
Journal:  Elife       Date:  2016-01-29       Impact factor: 8.140

6.  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

7.  Resolving coiled shapes reveals new reorientation behaviors in C. elegans.

Authors:  Onno D Broekmans; Jarlath B Rodgers; William S Ryu; Greg J Stephens
Journal:  Elife       Date:  2016-09-20       Impact factor: 8.140

8.  Hierarchical compression of Caenorhabditis elegans locomotion reveals phenotypic differences in the organization of behaviour.

Authors:  Alex Gomez-Marin; Greg J Stephens; André E X Brown
Journal:  J R Soc Interface       Date:  2016-08       Impact factor: 4.118

9.  Changes in Postural Syntax Characterize Sensory Modulation and Natural Variation of C. elegans Locomotion.

Authors:  Roland F Schwarz; Robyn Branicky; Laura J Grundy; William R Schafer; André E X Brown
Journal:  PLoS Comput Biol       Date:  2015-08-21       Impact factor: 4.475

10.  Searching for motifs in the behaviour of larval Drosophila melanogaster and Caenorhabditis elegans reveals continuity between behavioural states.

Authors:  Balázs Szigeti; Ajinkya Deogade; Barbara Webb
Journal:  J R Soc Interface       Date:  2015-12-06       Impact factor: 4.118

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