{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T03:47:29Z","timestamp":1790221649264,"version":"4.1.0"},"reference-count":37,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,10,27]],"date-time":"2023-10-27T00:00:00Z","timestamp":1698364800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Mol. Neurosci."],"abstract":"<jats:p>The surrounding thermal environment is highly important for the survival and fitness of animals, and as a result most exhibit behavioral and neural responses to temperature changes. We study signals generated by thermosensory neurons in <jats:italic>Drosophila<\/jats:italic> larvae and also the physical and sensory effects of temperature variation on locomotion and navigation. In particular we characterize how sensory neuronal and behavioral responses to temperature variation both change across the development of the larva. Looking at a wide range of non-nociceptive isotropic thermal environments, we characterize the dependence of speed, turning rate, and other behavioral components on temperature, distinguishing the physical effects of temperature from behavior changes based on sensory processing. We also characterize the strategies larvae use to modulate individual behavioral components to produce directed navigation along thermal gradients, and how these strategies change during physical development. Simulations based on modified random walks show where thermotaxis in each developmental stage fits into the larger context of possible navigation strategies. We also investigate cool sensing neurons in the larva's dorsal organ ganglion, characterizing neural response to sine-wave modulation of temperature while performing single-cell-resolution 3D imaging. We determine the sensitivity of these neurons, which produce signals in response to extremely small temperature changes. Combining thermotaxis results with neurophysiology data, we observe, across development, sensitivity to temperature change as low as a few thousandths of a \u00b0C per second, or a few hundredths of a \u00b0C in absolute temperature change.<\/jats:p>","DOI":"10.3389\/fnmol.2023.1275469","type":"journal-article","created":{"date-parts":[[2023,10,27]],"date-time":"2023-10-27T22:05:18Z","timestamp":1698444318000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":17,"title":["Temperature sensitivity and temperature response across development in the Drosophila larva"],"prefix":"10.3389","volume":"16","author":[{"given":"Anastasiia","family":"Evans","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anggie J.","family":"Ferrer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erica","family":"Fradkov","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joseph W.","family":"Shomar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Josh","family":"Forer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mason","family":"Klein","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,10,27]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"e2119872119","DOI":"10.1073\/pnas.2119872119","article-title":"A general theory for temperature dependence in biology","volume":"119","author":"Arroyo","year":"2022","journal-title":"Proc. Natl. Acad. Sci. U. S. A"},{"key":"B2","volume-title":"Random Walks in Biology","author":"Berg","year":"1993"},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.69205","article-title":"Mechanical vibration patterns elicit behavioral transitions and habituation in crawling Drosophila larvae","author":"Berne","year":"2023","journal-title":"eLife"},{"key":"B4","doi-asserted-by":"publisher","first-page":"738","DOI":"10.1016\/j.neuron.2018.12.022","article-title":"ionotropic receptors specify the morphogenesis of phasic sensors controlling rapid thermal preference in Drosophila","volume":"101","author":"Budelli","year":"2019","journal-title":"Neuron"},{"key":"B5","doi-asserted-by":"publisher","first-page":"813","DOI":"10.1098\/rsif.2008.0014","article-title":"Random walk models in biology","volume":"5","author":"Codling","year":"2008","journal-title":"J. R. Soc. Interface"},{"key":"B6","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1146\/annurev.neuro.29.051605.112958","article-title":"TRP Ion channels and temperature sensation","volume":"29","author":"Dhaka","year":"2006","journal-title":"Annu. Rev. Neurosci"},{"key":"B7","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1002\/gene.10150","article-title":"GAL4 system in Drosophila: a fly geneticist's swiss army knife","volume":"34","author":"Duffy","year":"2002","journal-title":"Genesis"},{"key":"B8","doi-asserted-by":"publisher","first-page":"614","DOI":"10.1016\/j.cell.2011.01.028","article-title":"The coding of temperature in the Drosophila brain","volume":"144","author":"Gallio","year":"2011","journal-title":"Cell"},{"key":"B9","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1038\/nmeth.1853","article-title":"Controlling airborne cues during small animal navigation","volume":"9","author":"Gershow","year":"2012","journal-title":"Nat. Methods"},{"key":"B10","doi-asserted-by":"publisher","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":"Gomez-Marin","year":"2012","journal-title":"Curr. Opin. Neurobiol"},{"key":"B11","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1038\/nature07001","article-title":"An internal thermal sensor controlling temperature preference in Drosophila","volume":"454","author":"Hamada","year":"2008","journal-title":"Nature"},{"key":"B12","doi-asserted-by":"publisher","first-page":"eabg6707","DOI":"10.1126\/sciadv.abg6707","article-title":"Synchronous and opponent thermosensors use flexible cross-inhibition to orchestrate thermal homeostasis","volume":"7","author":"Hernandez-Nunez","year":"2021","journal-title":"Sci. Adv"},{"key":"B13","doi-asserted-by":"publisher","first-page":"991","DOI":"10.1016\/j.celrep.2012.09.011","article-title":"A GAL4-driver line resource for Drosophila neurobiology","volume":"2","author":"Jenett","year":"2012","journal-title":"Cell Rep"},{"key":"B14","doi-asserted-by":"publisher","first-page":"487","DOI":"10.1016\/S0959-4388(03)00101-6","article-title":"Lessons from peppers and peppermint: the molecular logic of thermosensation","volume":"13","author":"Jordt","year":"2003","journal-title":"Curr. Opin. Neurobiol"},{"key":"B15","doi-asserted-by":"publisher","first-page":"E3868","DOI":"10.1073\/pnas.1215295110","article-title":"Sensorimotor structure of Drosophila larva phototaxis","volume":"110","author":"Kane","year":"2013","journal-title":"Proc. Natl. Acad. Sci. U. S. A"},{"key":"B16","doi-asserted-by":"publisher","first-page":"104","DOI":"10.1016\/j.tins.2011.11.003","article-title":"Seeing the light: photobehavior in fruit fly larvae","volume":"35","author":"Keene","year":"2012","journal-title":"Trends Neurosci"},{"key":"B17","doi-asserted-by":"publisher","first-page":"e220","DOI":"10.1073\/pnas.1416212112","article-title":"Sensory determinants of behavioral dynamics in Drosophila thermotaxis","volume":"112","author":"Klein","year":"2015","journal-title":"Proc. Natl. Acad. Sci. U. S. A"},{"key":"B18","doi-asserted-by":"publisher","first-page":"e30503","DOI":"10.7554\/eLife.30503","article-title":"Exploratory search during directed navigation in C. elegans and Drosophila larva","volume":"6","author":"Klein","year":"2017","journal-title":"eLife"},{"key":"B19","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1016\/j.neuron.2008.06.010","article-title":"Translation of sensory input into behavioral output via an olfactory system","volume":"59","author":"Kreher","year":"2008","journal-title":"Neuron"},{"key":"B20","doi-asserted-by":"publisher","first-page":"e23180","DOI":"10.1371\/journal.pone.0023180","article-title":"Two alternating motor programs drive navigation in Drosophila larva","volume":"6","author":"Lahiri","year":"2011","journal-title":"PLoS ONE"},{"key":"B21","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1038\/nn1009","article-title":"Identification and function of thermosensory neurons in Drosophila larvae","volume":"6","author":"Liu","year":"2003","journal-title":"Nat. Neurosci"},{"key":"B22","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1038\/nn.4416","article-title":"TRPA1 mediates sensation of the rate of temperature change in Drosophila larvae","volume":"20","author":"Luo","year":"2017","journal-title":"Nat. Neurosci"},{"key":"B23","doi-asserted-by":"publisher","first-page":"4261","DOI":"10.1523\/JNEUROSCI.4090-09.2010","article-title":"Navigational decision making in Drosophila thermotaxis","volume":"30","author":"Luo","year":"2010","journal-title":"J. Neurosci"},{"key":"B24","doi-asserted-by":"publisher","first-page":"e13254","DOI":"10.7554\/eLife.13254","article-title":"The ionotropic receptors IR21a and IR25a mediate cool sensing in Drosophila","volume":"5","author":"Ni","year":"2016","journal-title":"eLife"},{"key":"B25","doi-asserted-by":"publisher","first-page":"e71706","DOI":"10.1371\/journal.pone.0071706","article-title":"High-throughput analysis of stimulus-evoked behaviors in Drosophila larva reveals multiple modality-specific escape strategies","volume":"8","author":"Ohyama","year":"2013","journal-title":"PLoS ONE"},{"key":"B26","doi-asserted-by":"publisher","first-page":"1023492","DOI":"10.3389\/fnmol.2022.1023492","article-title":"Cool and warm ionotropic receptors control multiple thermotaxes in Drosophila larvae","volume":"15","author":"Omelchenko","year":"2022","journal-title":"Front. Mol. Neurosci"},{"key":"B27","doi-asserted-by":"publisher","first-page":"e26607","DOI":"10.7554\/eLife.26607","article-title":"Mechanism of bidirectional thermotaxis in Escherichia coli","volume":"6","author":"Paulick","year":"2017","journal-title":"Elife"},{"key":"B28","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1111\/j.1570-8703.2006.00474.x","article-title":"Drosophila melanogaster: the model organism","volume":"121","author":"Roberts","year":"2006","journal-title":"Entomol. Exp. Appl"},{"key":"B29","doi-asserted-by":"publisher","first-page":"14668","DOI":"10.1073\/pnas.0805041105","article-title":"Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster","volume":"105","author":"Rosenzweig","year":"2008","journal-title":"Proc. Natl. Acad. Sci. U.S.A"},{"key":"B30","doi-asserted-by":"publisher","first-page":"R304","DOI":"10.1016\/j.cub.2013.03.009","article-title":"Sensing temperature","volume":"23","author":"Sengupta","year":"2013","journal-title":"Curr. Biol"},{"key":"B31","doi-asserted-by":"publisher","first-page":"336","DOI":"10.1016\/j.celrep.2016.09.028","article-title":"A switch in thermal preference in Drosophila larvae depends on multiple rhodopsins","volume":"17","author":"Sokabe","year":"2016","journal-title":"Cell Rep"},{"key":"B32","doi-asserted-by":"publisher","first-page":"261","DOI":"10.1016\/S0092-8674(03)00272-1","article-title":"Painless, a Drosophila gene essential for nociception","volume":"113","author":"Tracey","year":"2003","journal-title":"Cell"},{"key":"B33","doi-asserted-by":"publisher","first-page":"e0209577","DOI":"10.1371\/journal.pone.0209577","article-title":"Injury-induced cold sensitization in Drosophila larvae involves behavioral shifts that require the TRP channel Brv1","volume":"13","author":"Turner","year":"2018","journal-title":"PLoS ONE"},{"key":"B34","doi-asserted-by":"publisher","first-page":"921","DOI":"10.1038\/nature09576","article-title":"Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall","volume":"468","author":"Xiang","year":"2010","journal-title":"Nature"},{"key":"B35","doi-asserted-by":"publisher","first-page":"e86585","DOI":"10.7554\/eLife.86585","article-title":"Continuous, long-term crawling behavior characterized by a robotic transport system","volume":"12","author":"Yu","year":"2023","journal-title":"Elife"},{"key":"B36","doi-asserted-by":"publisher","first-page":"13612","DOI":"10.1073\/pnas.1312477110","article-title":"Sound response mediated by the TRP channels NOMPC, NANCHUNG, and INACTIVE in chordotonal organs of Drosophila larvae","volume":"110","author":"Zhang","year":"2013","journal-title":"PNAS"},{"key":"B37","doi-asserted-by":"crossref","first-page":"20230279","DOI":"10.1098\/rsif.2023.0279","article-title":"Thermotaxis in an Apolar, Non-neuronal Animal","volume":"20","author":"Zhong","year":"2023","journal-title":"J. R. Soc. Interface"}],"container-title":["Frontiers in Molecular Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnmol.2023.1275469\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,27]],"date-time":"2023-10-27T22:05:21Z","timestamp":1698444321000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnmol.2023.1275469\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,10,27]]},"references-count":37,"alternative-id":["10.3389\/fnmol.2023.1275469"],"URL":"https:\/\/doi.org\/10.3389\/fnmol.2023.1275469","relation":{},"ISSN":["1662-5099"],"issn-type":[{"value":"1662-5099","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,10,27]]},"article-number":"1275469"}}