Literature DB >> 26824391

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

Steven B Augustine1, Kristy J Lawton2, Theodore H Lindsay3, Tod R Thiele4, William M Roberts5, Eduardo J Izquierdo6, Serge Faumont5, Rebecca A Lindsay7, Matthew Cale Britton8, Navin Pokala9, Cornelia I Bargmann10, Shawn R Lockery5.   

Abstract

Random search is a behavioral strategy used by organisms from bacteria to humans to locate food that is randomly distributed and undetectable at a distance. We investigated this behavior in the nematode Caenorhabditis elegans, an organism with a small, well-described nervous system. Here we formulate a mathematical model of random search abstracted from the C. elegans connectome and fit to a large-scale kinematic analysis of C. elegans behavior at submicron resolution. The model predicts behavioral effects of neuronal ablations and genetic perturbations, as well as unexpected aspects of wild type behavior. The predictive success of the model indicates that random search in C. elegans can be understood in terms of a neuronal flip-flop circuit involving reciprocal inhibition between two populations of stochastic neurons. Our findings establish a unified theoretical framework for understanding C. elegans locomotion and a testable neuronal model of random search that can be applied to other organisms.
© 2016, Roberts et al.

Entities:  

Keywords:  C. elegans; computational biology; hidden Markov model; locomotion; neuroscience; spatial orientation; stochastic neural network; systems biology

Year:  2016        PMID: 26824391      PMCID: PMC4798983          DOI: 10.7554/eLife.12572

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


  97 in total

1.  Activity of reticulospinal neurons during locomotion in the freely behaving lamprey.

Authors:  T G Deliagina; P V Zelenin; P Fagerstedt; S Grillner; G N Orlovsky
Journal:  J Neurophysiol       Date:  2000-02       Impact factor: 2.714

2.  Photo-inducible cell ablation in Caenorhabditis elegans using the genetically encoded singlet oxygen generating protein miniSOG.

Authors:  Yingchuan B Qi; Emma J Garren; Xiaokun Shu; Roger Y Tsien; Yishi Jin
Journal:  Proc Natl Acad Sci U S A       Date:  2012-04-24       Impact factor: 11.205

3.  Chemotaxis in Escherichia coli analysed by three-dimensional tracking.

Authors:  H C Berg; D A Brown
Journal:  Nature       Date:  1972-10-27       Impact factor: 49.962

4.  Impulse responses in bacterial chemotaxis.

Authors:  S M Block; J E Segall; H C Berg
Journal:  Cell       Date:  1982-11       Impact factor: 41.582

5.  Neural Mechanisms for Evaluating Environmental Variability in Caenorhabditis elegans.

Authors:  Adam J Calhoun; Ada Tong; Navin Pokala; James A J Fitzpatrick; Tatyana O Sharpee; Sreekanth H Chalasani
Journal:  Neuron       Date:  2015-04-09       Impact factor: 17.173

6.  Thermal avoidance in Caenorhabditis elegans: an approach to the study of nociception.

Authors:  N Wittenburg; R Baumeister
Journal:  Proc Natl Acad Sci U S A       Date:  1999-08-31       Impact factor: 11.205

7.  Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons.

Authors:  David M Tobin; David M Madsen; Amanda Kahn-Kirby; Erin L Peckol; Gary Moulder; Robert Barstead; Andres V Maricq; Cornelia I Bargmann
Journal:  Neuron       Date:  2002-07-18       Impact factor: 17.173

8.  A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans.

Authors:  Kirthi C Reddy; Erik C Andersen; Leonid Kruglyak; Dennis H Kim
Journal:  Science       Date:  2009-01-16       Impact factor: 47.728

9.  VAV-1 acts in a single interneuron to inhibit motor circuit activity in Caenorhabditis elegans.

Authors:  Amanda L Fry; Jocelyn T Laboy; Kenneth R Norman
Journal:  Nat Commun       Date:  2014-11-21       Impact factor: 14.919

10.  Specific expression of channelrhodopsin-2 in single neurons of Caenorhabditis elegans.

Authors:  Cornelia Schmitt; Christian Schultheis; Navin Pokala; Steven J Husson; Jana F Liewald; Cornelia I Bargmann; Alexander Gottschalk
Journal:  PLoS One       Date:  2012-08-30       Impact factor: 3.240

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  39 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.  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

Review 4.  Micro-connectomics: probing the organization of neuronal networks at the cellular scale.

Authors:  Manuel Schröter; Ole Paulsen; Edward T Bullmore
Journal:  Nat Rev Neurosci       Date:  2017-02-02       Impact factor: 34.870

Review 5.  Algorithms for Olfactory Search across Species.

Authors:  Keeley L Baker; Michael Dickinson; Teresa M Findley; David H Gire; Matthieu Louis; Marie P Suver; Justus V Verhagen; Katherine I Nagel; Matthew C Smear
Journal:  J Neurosci       Date:  2018-10-31       Impact factor: 6.167

6.  A quantitative model of conserved macroscopic dynamics predicts future motor commands.

Authors:  Connor Brennan; Alexander Proekt
Journal:  Elife       Date:  2019-07-11       Impact factor: 8.140

Review 7.  Microcircuits in respiratory rhythm generation: commonalities with other rhythm generating networks and evolutionary perspectives.

Authors:  Jan-Marino Ramirez; Tatiana Dashevskiy; Ibis Agosto Marlin; Nathan Baertsch
Journal:  Curr Opin Neurobiol       Date:  2016-08-30       Impact factor: 6.627

8.  Collapse of Global Neuronal States in Caenorhabditis elegans under Isoflurane Anesthesia.

Authors:  Mehraj R Awal; Gregory S Wirak; Christopher V Gabel; Christopher W Connor
Journal:  Anesthesiology       Date:  2020-07       Impact factor: 7.892

9.  Chemosensory signal transduction in Caenorhabditis elegans.

Authors:  Denise M Ferkey; Piali Sengupta; Noelle D L'Etoile
Journal:  Genetics       Date:  2021-03-31       Impact factor: 4.562

Review 10.  Quantifying behavior to solve sensorimotor transformations: advances from worms and flies.

Authors:  Adam J Calhoun; Mala Murthy
Journal:  Curr Opin Neurobiol       Date:  2017-08-30       Impact factor: 6.627

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