{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,13]],"date-time":"2026-04-13T01:57:31Z","timestamp":1776045451798,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1007916","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,1,21]],"date-time":"2021-01-21T00:00:00Z","timestamp":1611187200000}}],"reference-count":46,"publisher":"Public Library of Science (PLoS)","issue":"1","license":[{"start":{"date-parts":[[2021,1,8]],"date-time":"2021-01-08T00:00:00Z","timestamp":1610064000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/publicdomain\/zero\/1.0\/"}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>\n                    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\n                    <jats:italic>C<\/jats:italic>\n                    .\n                    <jats:italic>elegans<\/jats:italic>\n                    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\n                    <jats:italic>C<\/jats:italic>\n                    .\n                    <jats:italic>elegans<\/jats:italic>\n                    . 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\n                    <jats:italic>C<\/jats:italic>\n                    .\n                    <jats:italic>elegans<\/jats:italic>\n                    . 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.\n                  <\/jats:p>","DOI":"10.1371\/journal.pcbi.1007916","type":"journal-article","created":{"date-parts":[[2021,1,8]],"date-time":"2021-01-08T15:54:10Z","timestamp":1610121250000},"page":"e1007916","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":4,"title":["Persistent thermal input controls steering behavior in Caenorhabditis elegans"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3063-5683","authenticated-orcid":true,"given":"Muneki","family":"Ikeda","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9896-4817","authenticated-orcid":true,"given":"Hirotaka","family":"Matsumoto","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2008-290X","authenticated-orcid":true,"given":"Eduardo J.","family":"Izquierdo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2021,1,8]]},"reference":[{"key":"pcbi.1007916.ref001","volume-title":"The Orientation of Animals: Kineses, Taxes and Compass Reactions.","author":"FS Gottfried","year":"1961"},{"key":"pcbi.1007916.ref002","doi-asserted-by":"crossref","DOI":"10.1093\/acprof:oso\/9780199640386.001.0001","volume-title":"Migration: the biology of life on the move.","author":"H. Dingle","year":"2014"},{"key":"pcbi.1007916.ref003","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1038\/ncomms1455","article-title":"Active sampling and decision making in Drosophila chemotaxis.","volume":"2","author":"A Gomez-Marin","year":"2011","journal-title":"Nat Commun"},{"key":"pcbi.1007916.ref004","doi-asserted-by":"crossref","first-page":"2056","DOI":"10.1603\/029.102.0606","article-title":"Designation of Chemicals in Terms of the Locomotor Responses They Elicit From Insects: An Update of Dethier","volume":"102","author":"JR Miller","year":"2009","journal-title":"J Econ Entomol"},{"key":"pcbi.1007916.ref005","doi-asserted-by":"crossref","first-page":"817","DOI":"10.1073\/pnas.70.3.817","article-title":"Chemotaxis by the nematode Caenorhabditis elegans: identification of attractants and analysis of the response by use of mutants","volume":"70","author":"S. Ward","year":"1973","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1007916.ref006","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1016\/0092-8674(93)80053-H","article-title":"Odorant-selective genes and neurons mediate olfaction in C. elegans","volume":"74","author":"CI Bargmann","year":"1993","journal-title":"Cell"},{"key":"pcbi.1007916.ref007","doi-asserted-by":"crossref","first-page":"4061","DOI":"10.1073\/pnas.72.10.4061","article-title":"Normal and mutant thermotaxis in the nematode Caenorhabditis elegans","volume":"72","author":"EM Hedgecock","year":"1975","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1007916.ref008","doi-asserted-by":"crossref","first-page":"5370","DOI":"10.1523\/JNEUROSCI.3633-08.2009","article-title":"Parallel use of two behavioral mechanisms for chemotaxis in Caenorhabditis elegans","volume":"29","author":"Y Iino","year":"2009","journal-title":"J Neurosci"},{"key":"pcbi.1007916.ref009","article-title":"Context-dependent operation of neural circuits underlies a navigation behavior in Caenorhabditis elegans","author":"M Ikeda","year":"2020","journal-title":"Proc Natl Acad Sci"},{"key":"pcbi.1007916.ref010","doi-asserted-by":"crossref","first-page":"e25546","DOI":"10.4161\/worm.25546","article-title":"Complex RIA calcium dynamics and its function in navigational behavior.","volume":"2","author":"M Hendricks","year":"2013","journal-title":"Worm"},{"key":"pcbi.1007916.ref011","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1016\/j.neuron.2017.12.042","article-title":"Sensorimotor Integration for Decision Making: How the Worm Steers","volume":"97","author":"HS Kaplan","year":"2018","journal-title":"Neuron"},{"key":"pcbi.1007916.ref012","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1038\/nature11081","article-title":"Compartmentalized calcium dynamics in a C. elegans interneuron encode head movement","volume":"487","author":"M Hendricks","year":"2012","journal-title":"Nature"},{"key":"pcbi.1007916.ref013","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1016\/j.neuron.2017.12.003","article-title":"Cholinergic Sensorimotor Integration Regulates Olfactory Steering","volume":"97","author":"H Liu","year":"2018","journal-title":"Neuron"},{"key":"pcbi.1007916.ref014","article-title":"A Gate-and-Switch Model for Head Orientation Behaviors in Caenorhabditis elegans.","volume":"5","author":"M-H Ouellette","year":"2018","journal-title":"eNeuro"},{"key":"pcbi.1007916.ref015","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1038\/nature11431","article-title":"Controlling interneuron activity in Caenorhabditis elegans to evoke chemotactic behaviour","volume":"490","author":"A Kocabas","year":"2012","journal-title":"Nature"},{"key":"pcbi.1007916.ref016","doi-asserted-by":"crossref","first-page":"15631","DOI":"10.1523\/JNEUROSCI.1757-14.2014","article-title":"Regulation of Experience-Dependent Bidirectional Chemotaxis by a Neural Circuit Switch in Caenorhabditis elegans","volume":"34","author":"Y Satoh","year":"2014","journal-title":"J Neurosci"},{"key":"pcbi.1007916.ref017","unstructured":"Monteith JL. Principles of Environmental Physics. Elsevier, New York; 1973. Available: https:\/\/books.google.co.jp\/books\/about\/Principles_of_Environmental_Physics.html?id=zPVEAQAAIAAJ&redir_esc=y"},{"key":"pcbi.1007916.ref018","doi-asserted-by":"crossref","first-page":"2571","DOI":"10.1523\/JNEUROSCI.2837-15.2016","article-title":"Reconstruction of Spatial Thermal Gradient Encoded in Thermosensory Neuron AFD in Caenorhabditis elegans","volume":"36","author":"Y Tsukada","year":"2016","journal-title":"J Neurosci"},{"key":"pcbi.1007916.ref019","doi-asserted-by":"crossref","first-page":"e1002890","DOI":"10.1371\/journal.pcbi.1002890","article-title":"Connecting a connectome to behavior: an ensemble of neuroanatomical models of C. elegans klinotaxis.","volume":"9","author":"EJ Izquierdo","year":"2013","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1007916.ref020","doi-asserted-by":"crossref","first-page":"12908","DOI":"10.1523\/JNEUROSCI.2606-10.2010","article-title":"Evolution and analysis of minimal neural circuits for klinotaxis in Caenorhabditis elegans","volume":"30","author":"EJ Izquierdo","year":"2010","journal-title":"J Neurosci"},{"key":"pcbi.1007916.ref021","doi-asserted-by":"crossref","DOI":"10.1093\/oso\/9780195099713.001.0001","volume-title":"Evolutionary algorithms in theory and practice: evolution strategies, evolutionary programming, genetic algorithms.","author":"T. B\u00e4ck","year":"1996"},{"key":"pcbi.1007916.ref022","doi-asserted-by":"crossref","first-page":"9557","DOI":"10.1523\/JNEUROSCI.19-21-09557.1999","article-title":"The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis","volume":"19","author":"JT Pierce-Shimomura","year":"1999","journal-title":"J Neurosci"},{"key":"pcbi.1007916.ref023","doi-asserted-by":"crossref","first-page":"616","DOI":"10.1016\/j.neuron.2013.11.020","article-title":"Temporal responses of C. elegans chemosensory neurons are preserved in behavioral dynamics","volume":"81","author":"S Kato","year":"2014","journal-title":"Neuron"},{"key":"pcbi.1007916.ref024","doi-asserted-by":"crossref","first-page":"4652","DOI":"10.1242\/jeb.02590","article-title":"Sensorimotor control during isothermal tracking in Caenorhabditis elegans","volume":"209","author":"L Luo","year":"2006","journal-title":"J Exp Biol"},{"key":"pcbi.1007916.ref025","doi-asserted-by":"crossref","first-page":"1291","DOI":"10.1016\/j.cub.2004.06.060","article-title":"The C. elegans thermosensory neuron AFD responds to warming","volume":"14","author":"KD Kimura","year":"2004","journal-title":"Curr Biol"},{"key":"pcbi.1007916.ref026","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1016\/j.conb.2011.11.008","article-title":"Active sensation during orientation behavior in the Drosophila larva: more sense than luck","volume":"22","author":"A Gomez-Marin","year":"2012","journal-title":"Curr Opin Neurobiol"},{"key":"pcbi.1007916.ref027","doi-asserted-by":"crossref","first-page":"e0140397","DOI":"10.1371\/journal.pone.0140397","article-title":"Information Flow through a Model of the C. elegans Klinotaxis Circuit.","volume":"10","author":"EJ Izquierdo","year":"2015","journal-title":"PLoS One."},{"key":"pcbi.1007916.ref028","doi-asserted-by":"crossref","unstructured":"Dahlberg BA, Izquierdo EJ. Contributions from parallel strategies for spatial orientation in C. elegans. The 2020 Conference on Artificial Life. Cambridge, MA: MIT Press; 2020. pp. 16\u201324. doi: 10.1162\/isal_a_00346","DOI":"10.1162\/isal_a_00346"},{"key":"pcbi.1007916.ref029","doi-asserted-by":"crossref","first-page":"4261","DOI":"10.1523\/JNEUROSCI.4090-09.2010","article-title":"Navigational Decision Making in Drosophila Thermotaxis","volume":"30","author":"L Luo","year":"2010","journal-title":"J Neurosci"},{"key":"pcbi.1007916.ref030","doi-asserted-by":"crossref","first-page":"E220","DOI":"10.1073\/pnas.1416212112","article-title":"Sensory determinants of behavioral dynamics in Drosophila thermotaxis","volume":"112","author":"M Klein","year":"2015","journal-title":"Proc Natl Acad Sci"},{"key":"pcbi.1007916.ref031","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1038\/nmeth.1630","article-title":"High-content behavioral analysis of Caenorhabditis elegans in precise spatiotemporal chemical environments.","volume":"8","author":"DR Albrecht","year":"2011","journal-title":"Nat Methods"},{"key":"pcbi.1007916.ref032","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/0167-2789(86)90031-X","article-title":"Extracting qualitative dynamics from experimental data.","volume":"20","author":"DS Broomhead","year":"1986","journal-title":"Phys D Nonlinear Phenom"},{"key":"pcbi.1007916.ref033","doi-asserted-by":"crossref","first-page":"1003","DOI":"10.1029\/2000RG000092","article-title":"Advanced spectral methods for climatic time series","volume":"40","author":"M. Ghil","year":"2002","journal-title":"Rev Geophys"},{"key":"pcbi.1007916.ref034","unstructured":"Ide T, Inoue K. Knowledge Discovery from Time-Series Data using Nonlinear Transformations. SIAM 2005 Data Mining Conference. 2004."},{"key":"pcbi.1007916.ref035","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1016\/0167-2789(89)90077-8","article-title":"Singular spectrum analysis in nonlinear dynamics, with applications to paleoclimatic time series.","volume":"35","author":"R Vautard","year":"1989","journal-title":"Phys D Nonlinear Phenom"},{"key":"pcbi.1007916.ref036","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1186\/1472-6785-4-6","article-title":"Intrinsic and climatic factors in North-American animal population dynamics.","volume":"4","author":"N Loeuille","year":"2004","journal-title":"BMC Ecol."},{"key":"pcbi.1007916.ref037","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/0167-2789(92)90103-T","article-title":"Singular-spectrum analysis: A toolkit for short, noisy chaotic signals.","volume":"58","author":"R Vautard","year":"1992","journal-title":"Phys D Nonlinear Phenom"},{"key":"pcbi.1007916.ref038","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1038\/s41467-017-00030-8","article-title":"Chaos as an intermittently forced linear system.","volume":"8","author":"SL Brunton","year":"2017","journal-title":"Nat Commun."},{"key":"pcbi.1007916.ref039","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1081\/SAC-120017494","article-title":"An algorithm based on singular spectrum analysis for change-point detection.","volume":"32","author":"V Moskvina","year":"2003","journal-title":"Commun Stat Part B Simul Comput"},{"key":"pcbi.1007916.ref040","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1177\/105971239500300405","article-title":"On the Dynamics of Small Continuous-Time Recurrent Neural Networks.","volume":"3","author":"RD Beer","year":"1995","journal-title":"Adapt Behav."},{"key":"pcbi.1007916.ref041","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1023\/A:1008857906763","article-title":"Computational rules for chemotaxis in the nematode C. elegans","volume":"6","author":"TC Ferr\u00e9e","year":"1998","journal-title":"J Comput Neurosci"},{"key":"pcbi.1007916.ref042","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1038\/nmeth.1625","article-title":"High-throughput behavioral analysis in C. elegans.","volume":"8","author":"NA Swierczek","year":"2011","journal-title":"Nat Methods"},{"key":"pcbi.1007916.ref043","doi-asserted-by":"crossref","first-page":"e1006122","DOI":"10.1371\/journal.pcbi.1006122","article-title":"Identification of animal behavioral strategies by inverse reinforcement learning.","volume":"14","author":"S Yamaguchi","year":"2018","journal-title":"PLOS Comput Biol"},{"key":"pcbi.1007916.ref044","doi-asserted-by":"crossref","first-page":"3009","DOI":"10.1162\/neco.2006.18.12.3009","article-title":"Parameter space structure of continuous-time recurrent neural networks","volume":"18","author":"RD Beer","year":"2006","journal-title":"Neural Comput"},{"key":"pcbi.1007916.ref045","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1002\/j.1538-7305.1948.tb01338.x","article-title":"A Mathematical Theory of Communication.","volume":"27","author":"CE Shannon","year":"1948","journal-title":"Bell Syst Tech J."},{"key":"pcbi.1007916.ref046","doi-asserted-by":"crossref","first-page":"1024","DOI":"10.1214\/aos\/1176349654","article-title":"Averaged Shifted Histograms: Effective Nonparametric Density Estimators in Several Dimensions.","volume":"13","author":"DW Scott","year":"1985","journal-title":"Ann Stat."}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1007916","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,1,21]],"date-time":"2021-01-21T00:00:00Z","timestamp":1611187200000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1007916","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,1,21]],"date-time":"2021-01-21T13:31:24Z","timestamp":1611235884000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1007916"}},"subtitle":[],"editor":[{"given":"Tosif","family":"Ahamed","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2021,1,8]]},"references-count":46,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,1,8]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1007916","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.04.29.067876","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,8]]}}}