{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T05:03:54Z","timestamp":1772168634982,"version":"3.50.1"},"reference-count":59,"publisher":"The Company of Biologists","issue":"18","license":[{"start":{"date-parts":[[2024,9,15]],"date-time":"2024-09-15T00:00:00Z","timestamp":1726358400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.biologists.com\/user-licence-1-1\/"}],"funder":[{"name":"National Science Foundation","award":["IOS-1755098"],"award-info":[{"award-number":["IOS-1755098"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,9,15]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>While temperature fluctuations pose significant challenges to the nervous system, many vital neuronal systems in poikilothermic animals function over a broad temperature range. Using the gastric mill pattern generator in the Jonah crab, we previously demonstrated that temperature-induced increases in leak conductance disrupt neuronal function and that neuropeptide modulation provides thermal protection. Here, we show that neuropeptide modulation also increases temperature robustness in Dungeness and green crabs. As in Jonah crabs, higher temperatures increased leak conductance in both species' pattern-generating lateral gastric neuron and terminated rhythmic gastric mill activity. Likewise, increasing descending modulatory projection neuron activity or neuropeptide transmitter application rescued rhythms at elevated temperatures. However, decreasing input resistance using dynamic clamp only restored the rhythm in half of the experiments. Thus, neuropeptide modulation increased temperature robustness in both species, demonstrating that neuropeptide-mediated temperature compensation is not limited to one species, although the underlying cellular compensation mechanisms may be distinct.<\/jats:p>","DOI":"10.1242\/jeb.247266","type":"journal-article","created":{"date-parts":[[2024,8,30]],"date-time":"2024-08-30T04:17:47Z","timestamp":1724991467000},"source":"Crossref","is-referenced-by-count":1,"title":["Neuromodulator-induced temperature robustness in a motor pattern: a comparative study between two decapod crustaceans"],"prefix":"10.1242","volume":"227","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8876-7537","authenticated-orcid":false,"given":"Wolfgang","family":"Stein","sequence":"first","affiliation":[{"name":"Illinois State University 1 School of Biological Sciences , , Normal, IL 61790 , USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1761-6296","authenticated-orcid":false,"given":"Carola","family":"St\u00e4dele","sequence":"additional","affiliation":[{"name":"Institute for Neuro- and Sensory Physiology, University of G\u00f6ttingen Medical Center 2 , 37073 G\u00f6ttingen, Lower Saxony , Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"237","published-online":{"date-parts":[[2024,9,17]]},"reference":[{"key":"2024091807352823200_JEB247266C1","doi-asserted-by":"publisher","first-page":"e55470","DOI":"10.7554\/eLife.55470","article-title":"Temperature compensation in a small rhythmic circuit","volume":"9","author":"Alonso","year":"2020","journal-title":"Elife"},{"key":"2024091807352823200_JEB247266C2","doi-asserted-by":"publisher","first-page":"2247","DOI":"10.1523\/JNEUROSCI.17-07-02247.1997","article-title":"Intercircuit control of motor pattern modulation by presynaptic inhibition","volume":"17","author":"Bartos","year":"1997","journal-title":"J. Neurosci."},{"key":"2024091807352823200_JEB247266C3","doi-asserted-by":"publisher","first-page":"6650","DOI":"10.1523\/JNEUROSCI.19-15-06650.1999","article-title":"Coordination of fast and slow rhythmic neuronal circuits","volume":"19","author":"Bartos","year":"1999","journal-title":"J. Neurosci."},{"key":"2024091807352823200_JEB247266C4","doi-asserted-by":"publisher","first-page":"6741","DOI":"10.1523\/JNEUROSCI.1682-04.2004","article-title":"Mechanosensory activation of a motor circuit by coactivation of two projection neurons","volume":"24","author":"Beenhakker","year":"2004","journal-title":"J. Neurosci."},{"key":"2024091807352823200_JEB247266C5","doi-asserted-by":"publisher","first-page":"2474","DOI":"10.1523\/JNEUROSCI.3607-05.2006","article-title":"Neuronal basis of the slow (&lt;1 Hz) oscillation in neurons of the nucleus reticularis thalami in vitro","volume":"26","author":"Blethyn","year":"2006","journal-title":"J. Neurosci."},{"key":"2024091807352823200_JEB247266C6","doi-asserted-by":"publisher","first-page":"11381","DOI":"10.1523\/JNEUROSCI.3219-04.2004","article-title":"Different sensory systems share projection neurons but elicit distinct motor patterns","volume":"24","author":"Blitz","year":"2004","journal-title":"J. Neurosci."},{"key":"2024091807352823200_JEB247266C7","doi-asserted-by":"publisher","first-page":"1000","DOI":"10.1242\/jeb.015222","article-title":"A newly identified extrinsic input triggers a distinct gastric mill rhythm via activation of modulatory projection neurons","volume":"211","author":"Blitz","year":"2008","journal-title":"J. Exp. Biol."},{"key":"2024091807352823200_JEB247266C8","doi-asserted-by":"publisher","first-page":"9329","DOI":"10.1523\/JNEUROSCI.1427-07.2007","article-title":"TASK-3 two-pore domain potassium channels enable sustained high-frequency firing in cerebellar granule neurons","volume":"27","author":"Brickley","year":"2007","journal-title":"J. Neurosci."},{"key":"2024091807352823200_JEB247266C9","doi-asserted-by":"publisher","first-page":"2279","DOI":"10.1242\/jeb.200.17.2279","article-title":"Two novel tachykinin-related peptides from the nervous system of the crab Cancer borealis","volume":"200","author":"Christie","year":"1997","journal-title":"J. Exp. Biol."},{"key":"2024091807352823200_JEB247266C10","doi-asserted-by":"publisher","first-page":"502","DOI":"10.1038\/378502a0","article-title":"A switch between two modes of synaptic transmission mediated by presynaptic inhibition","volume":"378","author":"Coleman","year":"1995","journal-title":"Nature"},{"key":"2024091807352823200_JEB247266C11","first-page":"579","article-title":"The biology of the shore crab, Carcinus maenas (L.). 2. The life of the adult crab","volume":"2","author":"Crothers","year":"1968","journal-title":"Field Stud."},{"key":"2024091807352823200_JEB247266C12","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/S0306-4565(98)00008-4","article-title":"Thermal tolerance of two species of marine crab, Cancer pagurus and Carcinus maenas","volume":"23","author":"Cuculescu","year":"1998","journal-title":"J. Therm. Biol."},{"key":"2024091807352823200_JEB247266C13","doi-asserted-by":"publisher","first-page":"10580","DOI":"10.1523\/JNEUROSCI.22-24-10580.2002","article-title":"Bursting in leech heart interneurons: cell autonomous and network based mechanisms","volume":"22","author":"Cymbalyuk","year":"2002","journal-title":"J. Neurosci."},{"key":"2024091807352823200_JEB247266C14","doi-asserted-by":"publisher","first-page":"7607","DOI":"10.1523\/JNEUROSCI.0101-21.2021","article-title":"Neuropeptide modulation increases dendritic electrical spread to restore neuronal activity disrupted by temperature","volume":"41","author":"Demaegd","year":"2021","journal-title":"J. Neurosci."},{"key":"2024091807352823200_JEB247266C15","doi-asserted-by":"publisher","first-page":"12013","DOI":"10.1523\/JNEUROSCI.1060-13.2013","article-title":"Motor circuit-specific burst patterns drive different muscle and behavior patterns","volume":"33","author":"Diehl","year":"2013","journal-title":"J. Neurosci."},{"key":"2024091807352823200_JEB247266C16","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1242\/jeb.186.1.157","article-title":"Switching in the activity state of an interneuron that controls coordination of the hearts in the medicinal leech (Hirudo medicinalis)","volume":"186","author":"Gramoll","year":"1994","journal-title":"J. Exp. Biol."},{"key":"2024091807352823200_JEB247266C17","doi-asserted-by":"publisher","first-page":"e1207","DOI":"10.3791\/1207","article-title":"Cancer borealis stomatogastric nervous system dissection","volume":"25","author":"Gutierrez","year":"2009","journal-title":"J. Vis. Exp."},{"key":"2024091807352823200_JEB247266C18","doi-asserted-by":"publisher","first-page":"336","DOI":"10.3389\/fnins.2019.00336","article-title":"The temperature dependence of sleep","volume":"13","author":"Harding","year":"2019","journal-title":"Front. Neurosci."},{"key":"2024091807352823200_JEB247266C19","doi-asserted-by":"publisher","first-page":"2866","DOI":"10.1152\/jn.00618.2009","article-title":"Differential activation of projection neurons by two sensory pathways contributes to motor pattern selection","volume":"102","author":"Hedrich","year":"2009","journal-title":"J. Neurophysiol."},{"key":"2024091807352823200_JEB247266C20","doi-asserted-by":"publisher","first-page":"1671","DOI":"10.1152\/jn.01105.2010","article-title":"Gastric and pyloric motor pattern control by a modulatory projection neuron in the intact crab Cancer pagurus","volume":"105","author":"Hedrich","year":"2011","journal-title":"J. Neurophysiol."},{"key":"2024091807352823200_JEB247266C21","doi-asserted-by":"publisher","first-page":"1255","DOI":"10.1152\/jn.01010.2014","article-title":"Cell dialysis by sharp electrodes can cause nonphysiological changes in neuron properties","volume":"114","author":"Hooper","year":"2015","journal-title":"J. Neurophysiol."},{"key":"2024091807352823200_JEB247266C22","volume-title":"A Biological Synopsis of the European Green Crab, Carcinus maenas","author":"Klassen","year":"2007"},{"key":"2024091807352823200_JEB247266C23","doi-asserted-by":"publisher","first-page":"2353","DOI":"10.1523\/JNEUROSCI.3553-07.2008","article-title":"Functional imaging, spatial reconstruction, and biophysical analysis of a respiratory motor circuit isolated in vitro","volume":"28","author":"Koizumi","year":"2008","journal-title":"J. Neurosci."},{"key":"2024091807352823200_JEB247266C24","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/j.jembe.2014.02.013","article-title":"Temperature preference and acclimation in the Jonah Crab, Cancer borealis","volume":"455","author":"Lewis","year":"2014","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"2024091807352823200_JEB247266C25","first-page":"E100","article-title":"Differential behavior, habitat destruction, and stress tolerance in three populations of Carcinus maenas","volume":"57","author":"Logan","year":"2017","journal-title":"Integr. Comp. Biol."},{"key":"2024091807352823200_JEB247266C26","doi-asserted-by":"publisher","first-page":"eaat3272","DOI":"10.1126\/sciadv.aat3272","article-title":"Projected changes in persistent extreme summer weather events: the role of quasi-resonant amplification","volume":"4","author":"Mann","year":"2018","journal-title":"Sci. Adv."},{"key":"2024091807352823200_JEB247266C27","doi-asserted-by":"publisher","first-page":"10213","DOI":"10.1523\/JNEUROSCI.1261-21.2021","article-title":"From the neuroscience of individual variability to climate change","volume":"41","author":"Marder","year":"2021","journal-title":"J. Neurosci."},{"key":"2024091807352823200_JEB247266C28","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1111\/j.1749-6632.1998.tb09052.x","article-title":"Frequency control of a slow oscillatory network by a fast rhythmic input: pyloric to gastric mill interactions in the crab stomatogastric nervous system","volume":"860","author":"Marder","year":"1998","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"2024091807352823200_JEB247266C29","doi-asserted-by":"publisher","first-page":"443","DOI":"10.1007\/s00360-012-0730-3","article-title":"A review of gastric processing in decapod crustaceans","volume":"183","author":"Mcgaw","year":"2013","journal-title":"J. Comp. Physiol. B"},{"key":"2024091807352823200_JEB247266C30","doi-asserted-by":"publisher","first-page":"570","DOI":"10.1016\/j.jtherbio.2012.07.003","article-title":"Effects of acclimation and acute temperature change on specific dynamic action and gastric processing in the green shore crab, Carcinus maenas","volume":"37","author":"Mcgaw","year":"2012","journal-title":"J. Therm. Biol."},{"key":"2024091807352823200_JEB247266C31","doi-asserted-by":"publisher","first-page":"e74363","DOI":"10.7554\/eLife.74363","article-title":"Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation","volume":"11","author":"Morozova","year":"2022","journal-title":"Elife"},{"key":"2024091807352823200_JEB247266C32","article-title":"Modulatory projection neurons","volume-title":"Encyclopedia of Neuroscience","author":"Nusbaum","year":"2013"},{"key":"2024091807352823200_JEB247266C33","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1038\/417343a","article-title":"A small-systems approach to motor pattern generation","volume":"417","author":"Nusbaum","year":"2002","journal-title":"Nature"},{"key":"2024091807352823200_JEB247266C34","doi-asserted-by":"publisher","first-page":"1324","DOI":"10.1038\/s41467-018-03732-9","article-title":"Longer and more frequent marine heatwaves over the past century","volume":"9","author":"Oliver","year":"2018","journal-title":"Nat. Commun."},{"key":"2024091807352823200_JEB247266C35","doi-asserted-by":"publisher","first-page":"591","DOI":"10.1016\/0300-9629(79)90201-9","article-title":"Respiration and thermal tolerance of the Dungeness crab, Cancer magister dana","volume":"63","author":"Prentice","year":"1979","journal-title":"Comp. Biochem. Physiol. Part A: Physiol."},{"key":"2024091807352823200_JEB247266C36","doi-asserted-by":"publisher","first-page":"304","DOI":"10.1126\/science.221982","article-title":"Nonimpulse-mediated synaptic transmission during the generation of a cyclic motor program","volume":"205","author":"Raper","year":"1979","journal-title":"Science"},{"key":"2024091807352823200_JEB247266C37","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0065-2881(09)56001-4","article-title":"Chapter 1. Impacts of the oceans on climate change","volume":"56","author":"Reid","year":"2009","journal-title":"Adv. Mar. Biol."},{"key":"2024091807352823200_JEB247266C38","doi-asserted-by":"publisher","first-page":"767","DOI":"10.1152\/physrev.2000.80.2.767","article-title":"Synaptic control of motoneuronal excitability","volume":"80","author":"Rekling","year":"2000","journal-title":"Physiol. Rev."},{"key":"2024091807352823200_JEB247266C39","doi-asserted-by":"publisher","first-page":"724","DOI":"10.1016\/j.conb.2012.01.008","article-title":"Temperature and neuronal circuit function: compensation, tuning and tolerance","volume":"22","author":"Robertson","year":"2012","journal-title":"Curr. Opin. Neurobiol."},{"key":"2024091807352823200_JEB247266C40","doi-asserted-by":"publisher","first-page":"101055","DOI":"10.1016\/j.cois.2023.101055","article-title":"A cold and quiet brain: mechanisms of insect CNS arrest at low temperatures","volume":"58","author":"Robertson","year":"2023","journal-title":"Curr. Opin. Insect Sci."},{"key":"2024091807352823200_JEB247266C41","first-page":"357","article-title":"Reliable circuits from irregular neurons: a dynamical approach to understanding central pattern generators","volume":"94","author":"Selverston","year":"2000","journal-title":"J. Physiol. (Lond.)"},{"key":"2024091807352823200_JEB247266C42","doi-asserted-by":"publisher","first-page":"992","DOI":"10.1152\/jn.1993.69.3.992","article-title":"Dynamic clamp: computer-generated conductances in real neurons","volume":"69","author":"Sharp","year":"1993","journal-title":"J. Neurophysiol."},{"key":"2024091807352823200_JEB247266C43","doi-asserted-by":"publisher","first-page":"912","DOI":"10.1242\/jeb.037473","article-title":"The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine \u2018winners\u2019 and \u2018losers","volume":"213","author":"Somero","year":"2010","journal-title":"J. Exp. Biol."},{"key":"2024091807352823200_JEB247266C44","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1146\/annurev-marine-120710-100935","article-title":"The physiology of global change: linking patterns to mechanisms","volume":"4","author":"Somero","year":"2012","journal-title":"Ann. Rev. Mar. Sci."},{"key":"2024091807352823200_JEB247266C45","doi-asserted-by":"publisher","first-page":"2603","DOI":"10.1152\/jn.00906.2013","article-title":"Phase maintenance in a rhythmic motor pattern during temperature changes in vivo","volume":"111","author":"Soofi","year":"2014","journal-title":"J. Neurophysiol."},{"key":"2024091807352823200_JEB247266C46","doi-asserted-by":"crossref","DOI":"10.1093\/acrefore\/9780190264086.013.153","article-title":"Stomatogastric nervous system","volume-title":"Oxford Research Encyclopedia","author":"Stein","year":"2017"},{"key":"2024091807352823200_JEB247266C47","doi-asserted-by":"publisher","first-page":"125887","DOI":"10.1016\/j.zool.2020.125887","article-title":"The neurobiology of ocean change - insights from decapod crustaceans","volume":"144","author":"Stein","year":"2021","journal-title":"Zoology (Jena)"},{"key":"2024091807352823200_JEB247266C48","doi-asserted-by":"publisher","first-page":"1148","DOI":"10.1111\/j.1460-9568.2007.05744.x","article-title":"Divergent co-transmitter actions underlie motor pattern activation by a modulatory projection neuron","volume":"26","author":"Stein","year":"2007","journal-title":"Eur. J. Neurosci."},{"key":"2024091807352823200_JEB247266C49","article-title":"Evolutionary aspects of motor control and coordination: the central pattern generators in the crustacean stomatogastric and swimmeret systems","volume-title":"Structure and Evolution of Invertebrate Nervous Systems","author":"Stein","year":"2016"},{"key":"2024091807352823200_JEB247266C50","doi-asserted-by":"publisher","first-page":"776","DOI":"10.1152\/jn.00545.2021","article-title":"The dynamic range of voltage-dependent gap junction signaling is maintained by Ih-induced membrane potential depolarization","volume":"127","author":"Stein","year":"2022","journal-title":"J. Neurophysiol."},{"key":"2024091807352823200_JEB247266C51","doi-asserted-by":"publisher","first-page":"1263591","DOI":"10.3389\/fncel.2023.1263591","article-title":"Thermal acclimation and habitat-dependent differences in temperature robustness of a crustacean motor circuit","volume":"17","author":"Stein","year":"2023","journal-title":"Front. Cell Neurosci."},{"key":"2024091807352823200_JEB247266C52","doi-asserted-by":"publisher","first-page":"849160","DOI":"10.3389\/fncel.2022.849160","article-title":"Neuromodulation enables temperature robustness and coupling between fast and slow oscillator circuits","volume":"16","author":"St\u00e4dele","year":"2022","journal-title":"Front. Cell Neurosci."},{"key":"2024091807352823200_JEB247266C53","doi-asserted-by":"publisher","first-page":"e1002265","DOI":"10.1371\/journal.pbio.1002265","article-title":"Neuromodulation to the rescue: compensation of temperature-induced breakdown of rhythmic motor patterns via extrinsic neuromodulatory input","volume":"13","author":"St\u00e4dele","year":"2015","journal-title":"PLoS Biol."},{"key":"2024091807352823200_JEB247266C54","doi-asserted-by":"publisher","first-page":"2997","DOI":"10.1152\/jn.91033.2008","article-title":"Effects of temperature acclimation on a central neural circuit and its behavioral output","volume":"100","author":"Szabo","year":"2008","journal-title":"J. Neurophysiol."},{"key":"2024091807352823200_JEB247266C55","doi-asserted-by":"publisher","first-page":"e1000469","DOI":"10.1371\/journal.pbio.1000469","article-title":"Precise temperature compensation of phase in a rhythmic motor pattern","volume":"8","author":"Tang","year":"2010","journal-title":"PLoS Biol."},{"key":"2024091807352823200_JEB247266C56","doi-asserted-by":"publisher","first-page":"1762","DOI":"10.1152\/jn.00764.2005","article-title":"Red pigment concentrating hormone strongly enhances the strength of the feedback to the pyloric rhythm oscillator but has little effect on pyloric rhythm period","volume":"95","author":"Thirumalai","year":"2006","journal-title":"J. Neurophysiol."},{"key":"2024091807352823200_JEB247266C57","doi-asserted-by":"publisher","first-page":"2844","DOI":"10.1152\/jn.00752.2003","article-title":"Hyperthermia modulates respiratory pacemaker bursting properties","volume":"92","author":"Tryba","year":"2004","journal-title":"J. Neurophysiol."},{"key":"2024091807352823200_JEB247266C58","doi-asserted-by":"publisher","first-page":"4","DOI":"10.3390\/fishes5010004","article-title":"Life history and population dynamics of green crabs (Carcinus maenas)","volume":"5","author":"Young","year":"2020","journal-title":"Fishes"},{"key":"2024091807352823200_JEB247266C59","doi-asserted-by":"publisher","first-page":"21","DOI":"10.3389\/fnbeh.2010.00021","article-title":"Pacemaker neuron and network oscillations depend on a neuromodulator-regulated linear current","volume":"4","author":"Zhao","year":"2010","journal-title":"Front. Behav. Neurosci."}],"container-title":["Journal of Experimental Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.247266\/3563015\/jeb247266.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.247266\/3566505\/jeb247266.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.247266\/3566505\/jeb247266.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,18]],"date-time":"2024-09-18T03:35:42Z","timestamp":1726630542000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/jeb\/article\/227\/18\/jeb247266\/362072\/Neuromodulator-induced-temperature-robustness-in-a"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,15]]},"references-count":59,"journal-issue":{"issue":"18","published-print":{"date-parts":[[2024,9,15]]}},"URL":"https:\/\/doi.org\/10.1242\/jeb.247266","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2023.11.23.568465","asserted-by":"object"}]},"ISSN":["0022-0949","1477-9145"],"issn-type":[{"value":"0022-0949","type":"print"},{"value":"1477-9145","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,15]]},"article-number":"jeb247266"}}