Cited by 86Neural dynamics and brain functionIon channel regulation and functionstochastic dynamics and bifurcation

Temperature compensation in a small rhythmic circuit

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Alonso, Leandro M, Marder, Eve·2020·eLife

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Abstract

Temperature affects the conductances and kinetics of the ionic channels that underlie neuronal activity. Each membrane conductance has a different characteristic temperature sensitivity, which raises the question of how neurons and neuronal circuits can operate robustly over wide temperature ranges. To address this, we employed computational models of the pyloric network of crabs and lobsters. We produced multiple different models that exhibit a triphasic pyloric rhythm over a range of temperatures and explored the dynamics of their currents and how they change with temperature. Temperature can produce smooth changes in the relative contributions of the currents to neural activity so that neurons and networks undergo graceful transitions in the mechanisms that give rise to their activity patterns. Moreover, responses of the models to deletions of a current can be different at high and low temperatures, indicating that even a well-defined genetic or pharmacological manipulation may produce qualitatively distinct effects depending on the temperature.

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Research works printed but not linked: 72

  1. Abrams TW Pearson KG 1982 Effects of temperature on identified central neurons that control jumping in the grasshopper The Journal of Neuroscience 2 1538 1553 10.1523/JNEUROSCI.02-11-01538.1982 6292375 PMC6564367 · DOI
  2. Alonso LM Marder E 2019 Visualization of currents in neural models with similar behavior and different conductance densities eLife 8 e42722 10.7554/eLife.42722 30702427 PMC6395073 · DOI · Paper page
  3. Bucher D Taylor AL Marder E 2006 Central pattern generating neurons simultaneously express fast and slow rhythmic activities in the stomatogastric ganglion Journal of Neurophysiology 95 3617 3632 10.1152/jn.00004.2006 16495367 · DOI
  4. Buchholtz F Golowasch J Epstein IR Marder E 1992 Mathematical model of an identified stomatogastric ganglion neuron Journal of Neurophysiology 67 332 340 10.1152/jn.1992.67.2.332 1373763 · DOI
  5. Caplan JS Williams AH Marder E 2014 Many parameter sets in a multicompartment model oscillator are robust to temperature perturbations The Journal of Neuroscience 34 4963 4975 10.1523/JNEUROSCI.0280-14.2014 24695714 PMC3972722 · DOI
  6. Connor JA 1975 Neural repetitive firing: a comparative study of membrane properties of crustacean walking leg axons Journal of Neurophysiology 38 922 932 10.1152/jn.1975.38.4.922 1159472 · DOI
  7. Cymbalyuk G Shilnikov A 2005 Coexistence of tonic spiking oscillations in a leech neuron model Journal of Computational Neuroscience 18 255 263 10.1007/s10827-005-0354-7 15830162 · DOI
  8. Fitzhugh R 1966 Theoretical effect of temperature on threshold in the Hodgkin-Huxley nerve model The Journal of General Physiology 49 989 1005 10.1085/jgp.49.5.989 5961362 PMC2195517 · DOI
  9. Frankenhaeuser B Moore LE 1963 The effect of temperature on the sodium and potassium permeability changes in myelinated nerve fibres of Xenopus laevis The Journal of Physiology 169 431 437 10.1113/jphysiol.1963.sp007269 14079679 PMC1368766 · DOI
  10. Garrett S Rosenthal JJ 2012 RNA editing underlies temperature adaptation in K+ channels from polar octopuses Science 335 848 851 10.1126/science.1212795 22223739 PMC4219319 · DOI
  11. Goaillard JM Taylor AL Schulz DJ Marder E 2009 Functional consequences of animal-to-animal variation in circuit parameters Nature Neuroscience 12 1424 1430 10.1038/nn.2404 19838180 PMC2826985 · DOI
  12. Goldman MS Golowasch J Marder E Abbott LF 2001 Global structure, robustness, and modulation of neuronal models The Journal of Neuroscience 21 5229 5238 10.1523/JNEUROSCI.21-14-05229.2001 11438598 PMC6762863 · DOI · Paper page
  13. Golowasch J Buchholtz F Epstein IR Marder E 1992 Contribution of individual ionic currents to activity of a model stomatogastric ganglion neuron Journal of Neurophysiology 67 341 349 10.1152/jn.1992.67.2.341 1373764 · DOI
  14. Golowasch J Abbott L Marder E 1999a Activity-dependent regulation of potassium currents in an identified neuron of the stomatogastric ganglion of the crab Cancer borealis Journal of Neuroscience 19 RC33 10.1523/JNEUROSCI.19-20-j0004.1999 PMC6782763 10516335 · DOI
  15. Golowasch J Casey M Abbott LF Marder E 1999b Network stability from activity-dependent regulation of neuronal conductances Neural Computation 11 1079 1096 10.1162/089976699300016359 10418158 · DOI
  16. Golowasch J 2019 Neuronal homeostasis: voltage brings it all together Current Biology 29 R641 R644 10.1016/j.cub.2019.05.029 31287985 · DOI
  17. Golowasch J Marder E 1992 Ionic currents of the lateral pyloric neuron of the stomatogastric ganglion of the crab Journal of Neurophysiology 67 318 331 10.1152/jn.1992.67.2.318 1373762 · DOI · Paper page
  18. Guttman R 1962 Effect of temperature on the potential and current thresholds of axon membrane The Journal of General Physiology 46 257 266 10.1085/jgp.46.2.257 13951483 PMC2195267 · DOI
  19. Guttman R 1966 Temperature characteristics of excitation in space-clamped squid axons The Journal of General Physiology 49 1007 1018 10.1085/jgp.49.5.1007 5961351 PMC2195523 · DOI
  20. Haddad SA Marder E 2018 Circuit robustness to temperature perturbation is altered by neuromodulators Neuron 100 609 623 10.1016/j.neuron.2018.08.035 30244886 PMC6613981 · DOI
  21. Haefner PA 1977 Aspects of the biology of the jonah crab, Cancer borealis Stimpson, 1859 in the mid-Atlantic Bight Journal of Natural History 11 303 320 10.1080/00222937700770221 · DOI
  22. Haley JA Hampton D Marder E 2018 Two central pattern generators from the crab, Cancer borealis, respond robustly and differentially to extreme extracellular pH eLife 7 e41877 10.7554/eLife.41877 30592258 PMC6328273 · DOI
  23. Hamood AW Haddad SA Otopalik AG Rosenbaum P Marder E 2015 Quantitative Reevaluation of the Effects of Short- and Long-Term Removal of Descending Modulatory Inputs on the Pyloric Rhythm of the Crab, Cancer borealis Eneuro 2 ENEURO.0058-14.2015 10.1523/ENEURO.0058-14.2015 PMC4408878 25914899 · DOI
  24. Harris-Warrick RM Coniglio LM Barazangi N Guckenheimer J Gueron S 1995 Dopamine modulation of transient potassium current evokes phase shifts in a central pattern generator network The Journal of Neuroscience 15 342 358 10.1523/JNEUROSCI.15-01-00342.1995 7823140 PMC6578330 · DOI
  25. Heitler WJ Goodman CS Rowell CHF 1977 The effects of temperature on the threshold of identified neurons in the locust Journal of Comparative Physiology ? A 117 163 182 10.1007/BF00612785 · DOI
  26. Hooper SL 1997 Phase maintenance in the pyloric pattern of the lobster (Panulirus interruptus) stomatogastric ganglion Journal of Computational Neuroscience 4 191 205 10.1023/a:1008822218061 9257232 · DOI
  27. Johnson BE Glauser DA Dan-Glauser ES Halling DB Aldrich RW Goodman MB 2011 Alternatively spliced domains interact to regulate BK potassium channel gating PNAS 108 20784 20789 10.1073/pnas.1116795108 22049343 PMC3251094 · DOI
  28. Klee MR Pierau FK Faber DS 1974 Temperature effects on resting potential and spike parameters of cat motoneurons Experimental Brain Research 19 478 492 10.1007/BF00236112 4854613 · DOI
  29. Krupczynski P Schuster S 2013 Precision of archerfish C-starts is fully temperature compensated Journal of Experimental Biology 216 3450 3460 10.1242/jeb.088856 23737557 · DOI
  30. Kukita F 1982 Properties of sodium and potassium channels of the squid giant axon far below 0 degrees C The Journal of Membrane Biology 68 151 160 10.1007/BF01872261 6286975 · DOI
  31. Lechner HA Baxter DA Clark JW Byrne JH 1996 Bistability and its regulation by serotonin in the endogenously bursting neuron R15 in Aplysia Journal of Neurophysiology 75 957 962 10.1152/jn.1996.75.2.957 8714668 · DOI
  32. LeMasson G Marder E Abbott LF 1993 Activity-dependent regulation of conductances in model neurons Science 259 1915 1917 10.1126/science.8456317 8456317 · DOI · Paper page
  33. Lin WH Baines RA 2015 Regulation of membrane excitability: a convergence on voltage-gated sodium conductance Molecular Neurobiology 51 57 67 10.1007/s12035-014-8674-0 24677068 PMC4309913 · DOI
  34. Liu Z Golowasch J Marder E Abbott LF 1998 A model neuron with activity-dependent conductances regulated by multiple calcium sensors The Journal of Neuroscience 18 2309 2320 10.1523/JNEUROSCI.18-07-02309.1998 9502792 PMC6793093 · DOI
  35. Malashchenko T Shilnikov A Cymbalyuk G 2011 Six types of multistability in a neuronal model based on slow calcium current PLOS ONE 6 e21782 10.1371/journal.pone.0021782 21814554 PMC3140973 · DOI
  36. Manor Y Nadim F Abbott LF Marder E 1997 Temporal dynamics of graded synaptic transmission in the lobster stomatogastric ganglion The Journal of Neuroscience 17 5610 5621 10.1523/JNEUROSCI.17-14-05610.1997 9204942 PMC6793824 · DOI
  37. Marder E Bucher D 2007 Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs Annual Review of Physiology 69 291 316 10.1146/annurev.physiol.69.031905.161516 17009928 · DOI · Paper page
  38. Marin B Barnett WH Doloc-Mihu A Calabrese RL Cymbalyuk GS 2013 High prevalence of multistability of rest states and bursting in a database of a model neuron PLOS Computational Biology 9 e1002930 10.1371/journal.pcbi.1002930 23505348 PMC3591289 · DOI
  39. Martin Anduaga A Evantal N Patop IL Bartok O Weiss R Kadener S 2019 Thermosensitive alternative splicing senses and mediates temperature adaptation in Drosophila eLife 8 e44642 10.7554/eLife.44642 31702556 PMC6890466 · DOI
  40. Maynard DM 1972 Simpler networks Annals of the New York Academy of Sciences 193 59 72 10.1111/j.1749-6632.1972.tb27823.x 4564740 · DOI
  41. Nadim F Manor Y Kopell N Marder E 1999 Synaptic depression creates a switch that controls the frequency of an oscillatory circuit PNAS 96 8206 8211 10.1073/pnas.96.14.8206 10393973 PMC22213 · DOI
  42. Nadim F Manor Y 2000 The role of short-term synaptic dynamics in motor control Current Opinion in Neurobiology 10 683 690 10.1016/S0959-4388(00)00159-8 11240276 · DOI
  43. Northcutt AJ Lett KM Garcia VB Diester CM Lane BJ Marder E Schulz DJ 2016 Deep sequencing of transcriptomes from the nervous systems of two decapod crustaceans to characterize genes important for neural circuit function and modulation BMC Genomics 17 868 10.1186/s12864-016-3215-z 27809760 PMC5096308 · DOI · Paper page
  44. O'Leary T Williams AH Caplan JS Marder E 2013 Correlations in ion channel expression emerge from homeostatic tuning rules PNAS 110 E2645 E2654 10.1073/pnas.1309966110 23798391 PMC3710808 · DOI · Paper page
  45. O'Leary T Williams AH Franci A Marder E 2014 Cell types, network homeostasis, and pathological compensation from a biologically plausible ion channel expression model Neuron 82 809 821 10.1016/j.neuron.2014.04.002 24853940 PMC4109293 · DOI
  46. O'Leary T Marder E 2016 Temperature-Robust neural function from Activity-Dependent ion channel regulation Current Biology 26 2935 2941 10.1016/j.cub.2016.08.061 27746024 PMC5111818 · DOI
  47. Paydarfar D Forger DB Clay JR 2006 Noisy inputs and the induction of on-off switching behavior in a neuronal pacemaker Journal of Neurophysiology 96 3338 3348 10.1152/jn.00486.2006 16956993 · DOI
  48. Press WH Teukolsky SA Vetterling WT Flannery BP 1988 Numerical Recipes in C Cambridge University Press
  49. Prinz AA Bucher D Marder E 2004 Similar network activity from disparate circuit parameters Nature Neuroscience 7 1345 1352 10.1038/nn1352 15558066 · DOI · Paper page
  50. Ranjan R Logette E Marani M Herzog M Tâche V Scantamburlo E Buchillier V Markram H 2019 A kinetic map of the homomeric Voltage-Gated potassium channel (Kv) Family Frontiers in Cellular Neuroscience 13 358 10.3389/fncel.2019.00358 31481875 PMC6710402 · DOI · Paper page
  51. Ratliff J Marder E O’Leary T 2018 Neural circuit robustness to acute, global physiological perturbations bioRxiv 10.1101/480830 · DOI
  52. Rinberg A Taylor AL Marder E 2013 The effects of temperature on the stability of a neuronal oscillator PLOS Computational Biology 9 e1002857 10.1371/journal.pcbi.1002857 23326223 PMC3542102 · DOI
  53. Robertson RM Money TG 2012 Temperature and neuronal circuit function: compensation, tuning and tolerance Current Opinion in Neurobiology 22 724 734 10.1016/j.conb.2012.01.008 22326854 · DOI
  54. Roemschied FA Eberhard MJ Schleimer JH Ronacher B Schreiber S 2014 Cell-intrinsic mechanisms of temperature compensation in a grasshopper sensory receptor neuron eLife 3 e02078 10.7554/eLife.02078 24843016 PMC4012639 · DOI
  55. Rosenthal JJ 2015 The emerging role of RNA editing in plasticity Journal of Experimental Biology 218 1812 1821 10.1242/jeb.119065 26085659 PMC4487009 · DOI
  56. Ruff RL 1999 Effects of temperature on slow and fast inactivation of rat skeletal muscle na + channels American Journal of Physiology-Cell Physiology 277 C937 C947 10.1152/ajpcell.1999.277.5.C937 10564086 · DOI · Paper page
  57. Santin JM Schulz DJ 2019 Membrane voltage is a direct feedback signal that influences correlated ion channel expression in neurons Current Biology 29 1683 1688 10.1016/j.cub.2019.04.008 31080077 PMC6677403 · DOI
  58. Schauf CL 1973 Temperature dependence of the ionic current kinetics of Myxicola giant axons The Journal of Physiology 235 197 205 10.1113/jphysiol.1973.sp010384 4778136 PMC1350739 · DOI
  59. Schulz DJ Goaillard JM Marder E 2006 Variable channel expression in identified single and electrically coupled neurons in different animals Nature Neuroscience 9 356 362 10.1038/nn1639 16444270 · DOI · Paper page
  60. Schulz DJ Goaillard JM Marder EE 2007 Quantitative expression profiling of identified neurons reveals cell-specific constraints on highly variable levels of gene expression PNAS 104 13187 13191 10.1073/pnas.0705827104 17652510 PMC1933263 · DOI · Paper page
  61. Sharp FR Massa SM Swanson RA 1999 Heat-shock protein protection Trends in Neurosciences 22 97 99 10.1016/S0166-2236(98)01392-7 10199631 · DOI
  62. Sjodin RA Mullins LJ 1958 Oscillatory behavior of the squid axon membrane potential The Journal of General Physiology 42 39 47 10.1085/jgp.42.1.39 13575773 PMC2194897 · DOI
  63. Soofi W Goeritz ML Kispersky TJ Prinz AA Marder E Stein W 2014 Phase maintenance in a rhythmic motor pattern during temperature changes in vivo Journal of Neurophysiology 111 2603 2613 10.1152/jn.00906.2013 24671541 PMC4044431 · DOI · Paper page
  64. Soto-Treviño C Rabbah P Marder E Nadim F 2005 Computational model of electrically coupled, intrinsically distinct pacemaker neurons Journal of Neurophysiology 94 590 604 10.1152/jn.00013.2005 15728775 PMC1941697 · DOI
  65. Stehlik L MacKenzie Jr C Morse W 1991 Distribution and abundance of four brachyuran crabs on the northwest Atlantic shelf Fishery Bulletin 89 473 492
  66. Tang LS Goeritz ML Caplan JS Taylor AL Fisek M Marder E 2010 Precise temperature compensation of phase in a rhythmic motor pattern PLOS Biology 8 e1000469 10.1371/journal.pbio.1000469 20824168 PMC2930868 · DOI · Paper page
  67. Tang LS Taylor AL Rinberg A Marder E 2012 Robustness of a rhythmic circuit to short- and long-term temperature changes Journal of Neuroscience 32 10075 10085 10.1523/JNEUROSCI.1443-12.2012 22815521 PMC3491657 · DOI · Paper page
  68. Taylor BJR Kerkut GA 1958 The effect of temperature changes on the activity of poikilotherms Behaviour 13 259 279 10.1163/156853957X00047 · DOI
  69. Temporal S Lett KM Schulz DJ 2014 Activity-dependent feedback regulates correlated ion channel mRNA levels in single identified motor neurons Current Biology 24 1899 1904 10.1016/j.cub.2014.06.067 25088555 · DOI
  70. Tran T Unal CT Severin D Zaborszky L Rotstein HG Kirkwood A Golowasch J 2019 Ionic current correlations are ubiquitous across phyla Scientific Reports 9 1687 10.1038/s41598-018-38405-6 30737430 PMC6368568 · DOI
  71. Turrigiano G Abbott LF Marder E 1994 Activity-dependent changes in the intrinsic properties of cultured neurons Science 264 974 977 10.1126/science.8178157 8178157 · DOI
  72. Turrigiano G LeMasson G Marder E 1995 Selective regulation of current densities underlies spontaneous changes in the activity of cultured neurons The Journal of Neuroscience 15 3640 3652 10.1523/JNEUROSCI.15-05-03640.1995 7538565 PMC6578228 · DOI

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Authors
Alonso, L. M., & Marder, E.
Affiliations
University Health Network (CA)
Corresponding author
Alonso, Leandro M
Venue
eLife
Published
2020-06-02
Volume
9
ISSN
2050-084X (ISSN-L)
OpenAlex
W3029791641
Cited by
86
References
1
Citations by year
2026: 17 · 2025: 19 · 2024: 20 · 2023: 11 · 2022: 7 · 2021: 12
FWCI
4.00
Type
journal article
Language
en
Open access
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Institutes of Health (T32 NS07292, MH046742, R35 NS097343)
  • Swartz Foundation (Swartz Foundation 2017)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
  • Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › stochastic dynamics and bifurcation
Keywords
temperature compensation, pyloric network, crustacean neuromodulation, membrane conductance, computational neuron model, crabs
MeSH terms
Cell Membrane, Membrane Potentials, Models, Biological, Temperature

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