Cited by 15Neuroscience and Neuropharmacology ResearchNeural dynamics and brain functionNeurobiology and Insect Physiology Research

Repeated applications of high potassium elicit long-term changes in a motor circuit from the crab, Cancer borealis

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Rue, Mara C.P., Alonso, Leandro M., Marder, Eve·2022·iScience

Abstract

Neuronal circuits must be capable of balancing adaptation to perturbation with physiological stability in the face of an ever-changing environment. Here we examined the effects of altered extracellular potassium concentration on the short and long-term behavior of the well-studied pyloric circuit in the crab, Cancer borealis. Pyloric neurons of the crab stomatogastric ganglion (STG) initially become quiescent, then recover spiking and bursting activity in high potassium saline (2.5x[K+], He et al. 2020). These changes in circuit robustness are maintained after the perturbation is removed; pyloric neurons are more robust to subsequent potassium perturbations even after several hours of wash in control saline. Despite these long-term changes in circuit robustness, or “memory” of the stimulus history, no differences in neuronal activity are seen under control conditions. The circuit’s adaptation to high potassium is erased by a hyperpolarizing stimulus of low potassium saline (0.4x[K+]) or direct hyperpolarizing current. Thus, perturbation, followed by recovery of normal activity, can hide cryptic changes in neuronal properties that are only revealed by subsequent challenges.

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  • Biological systems are degenerate.

    “Because biological systems are degenerate”

    From A feature and not a bug: Replication failures can lead to new biology (2026) · cites this paper as [44]

    The Discussion section, “Persistent, cryptic memory in neurons following perturbation” (page unavailable), says that seemingly identical neuronal activity patterns can arise from widely variable underlying parameters, which describes degeneracy in neurons. It does not extend that statement to biological systems generally. (LLM, conf=0.82)

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  • Biological systems that appear similar when unperturbed might respond to perturbations in unanticipated different ways.

    “biological systems that appear similar when unperturbed might respond to perturbations in unanticipated different ways [43-45]”
  • Biological systems that appear similar when unperturbed may show hidden 'cryptic' changes that are variable but only revealed when perturbed.

    “may show hidden 'cryptic' changes that are variable but only revealed when perturbed [44,45]”

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Research works printed but not linked: 64

  1. Alonso L.M. Marder E. Visualization of currents in neural models with similar behavior and different conductance densities Elife 8 2019 e42722 10.7554/eLife.42722 30702427 PMC6395073 · DOI · Paper page
  2. Arnold R. Pussell B.A. Howells J. Grinius V. Kiernan M.C. Lin C.S.Y. Krishnan A.V. Evidence for a causal relationship between hyperkalaemia and axonal dysfunction in end-stage kidney disease Clin. Neurophysiol. 125 2014 179 185 10.1016/j.clinph.2013.06.022 23867066 · DOI
  3. Ataman B. Ashley J. Gorczyca M. Ramachandran P. Fouquet W. Sigrist S.J. Budnik V. Rapid activity-dependent modifications in synaptic structure and function require bidirectional Wnt signaling Neuron 57 2008 705 718 10.1016/j.neuron.2008.01.026 18341991 PMC2435264 · DOI
  4. Ballerini L. Galante M. Grandolfo M. Nistri A. Generation of rhythmic patterns of activity by ventral interneurones in rat organotypic spinal slice culture J. Physiol. 517 1999 459 475 10.1111/j.1469-7793.1999.0459t.x 10332095 PMC2269349 · DOI
  5. Baylor D.A. Nicholls J.G. Changes in extracellular potassium concentration produced by neuronal activity in the central nervous system of the leech J. Physiol. 203 1969 555 569 10.1113/jphysiol.1969.sp008879 5387026 PMC1351530 · DOI
  6. Benda J. Longtin A. Maler L. Spike-frequency adaptation separates transient communication signals from background oscillations J. Neurosci. 25 2005 2312 2321 10.1523/JNEUROSCI.4795-04.2005 15745957 PMC6726095 · DOI
  7. Brickley S.G. Revilla V. Cull-Candy S.G. Wisden W. Farrant M. Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance Nature 409 2001 88 92 10.1038/35051086 11343119 · DOI
  8. Capera J. Serrano-Novillo C. Navarro-Pérez M. Cassinelli S. Felipe A. The potassium channel odyssey: mechanisms of traffic and membrane arrangement Int. J. Mol. Sci. 20 2019 734 10.3390/ijms20030734 PMC6386995 30744118 · DOI
  9. Chauvette S. Soltani S. Seigneur J. Timofeev I. In vivo models of cortical acquired epilepsy J. Neurosci. Methods 260 2016 185 201 10.1016/j.jneumeth.2015.08.030 26343530 PMC4744568 · DOI
  10. Childress J. Cowles D. Favuzzi J. Mickel T. Metabolic rates of benthic deep-sea decapod crustaceans decline with increasing depth primarily due to the decline in temperature Deep-Sea Res., Part A 37 1990 929 949 10.1016/0198-0149(90)90104-4 · DOI
  11. Darlington T.R. Tokiyama S. Lisberger S.G. Control of the strength of visual-motor transmission as the mechanism of rapid adaptation of priors for Bayesian inference in smooth pursuit eye movements J. Neurophysiol. 118 2017 1173 1189 10.1152/jn.00282.2017 28592689 PMC5547260 · DOI
  12. Desai N.S. Homeostatic plasticity in the CNS: synaptic and intrinsic forms J. Physiol. Paris 97 2003 391 402 10.1016/j.jphysparis.2004.01.005 15242651 · DOI
  13. Dissanayake A. Ishimatsu A. Synergistic effects of elevated CO2 and temperature on the metabolic scope and activity in a shallow-water coastal decapod (Metapenaeus joyneri; Crustacea: penaeidae) ICES J. Mar. Sci. 68 2011 1147 1154 10.1093/icesjms/fsq188 · DOI
  14. Ewald D.A. Williams A. Levitan I.B. Modulation of single Ca2+-dependent K+-channel activity by protein phosphorylation Nature 315 1985 503 506 10.1038/315503a0 2582272 · DOI
  15. Fernández-Fernández D. Lamas J.A. Metabotropic modulation of potassium channels during synaptic plasticity Neuroscience 456 2021 4 16 10.1016/j.neuroscience.2020.02.025 32114098 · DOI
  16. Frank C.A. Kennedy M.J. Goold C.P. Marek K.W. Davis G.W. Mechanisms underlying the rapid induction and sustained expression of synaptic homeostasis Neuron 52 2006 663 677 10.1016/j.neuron.2006.09.029 17114050 PMC2673733 · DOI · Paper page
  17. Fröhlich F. Bazhenov M. Iragui-Madoz V. Sejnowski T.J. Potassium dynamics in the epileptic cortex: new insights on an old topic Neuroscientist 14 2008 422 433 10.1177/1073858408317955 18997121 PMC2854295 · DOI
  18. Golowasch J. Abbott L.F. Marder E. Activity-dependent regulation of potassium currents in an identified neuron of the stomatogastric ganglion of the crab Cancer borealis J. Neurosci. 19 1999 RC33 10.1523/JNEUROSCI.19-20-j0004.1999 10516335 PMC6782763 · DOI
  19. Grubb M.S. Burrone J. Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability Nature 465 2010 1070 1074 10.1038/nature09160 20543823 PMC3196626 · DOI
  20. Gutierrez G.J. Grashow R.G. Cancer borealis stomatogastric nervous system dissection J. Vis. Exp. 2009 1207 10.3791/1207 19308017 PMC2705892 · DOI
  21. Haddad S.A. Marder E. Circuit robustness to temperature perturbation is altered by neuromodulators Neuron 100 2018 609 623.e3 10.1016/j.neuron.2018.08.035 30244886 PMC6613981 · DOI
  22. Haley J.A. Hampton D. Marder E. Two central pattern generators from the crab, Cancer borealis, respond robustly and differentially to extreme extracellular pH Elife 7 2018 e41877 10.7554/eLife.41877 30592258 PMC6328273 · DOI
  23. Harris-Warrick R.M. Marder E. Selverston A.I. Moulins M. Dynamic Biological Networks: The Stomatogastric Nervous System 1992 MIT press
  24. Hartigan J.A. Hartigan P.M. The dip test of unimodality Ann. Statist. 13 1985 70 84 10.1214/aos/1176346577 · DOI
  25. He L.S. Rue M.C.P. Morozova E.O. Powell D.J. James E.J. Kar M. Marder E. Rapid adaptation to elevated extracellular potassium in the pyloric circuit of the crab, Cancer borealis J. Neurophysiol. 123 2020 2075 2089 10.1152/jn.00135.2020 32319837 PMC7444919 · DOI
  26. Hengen K.B. Lambo M.E. Van Hooser S.D. Katz D.B. Turrigiano G.G. Firing rate homeostasis in visual cortex of freely behaving rodents Neuron 80 2013 335 342 10.1016/j.neuron.2013.08.038 24139038 PMC3816084 · DOI
  27. Hooper S.L. Thuma J.B. Guschlbauer C. Schmidt J. Büschges A. Cell dialysis by sharp electrodes can cause nonphysiological changes in neuron properties J. Neurophysiol. 114 2015 1255 1271 10.1152/jn.01010.2014 26063785 PMC4725110 · DOI
  28. Iguchi N. Ikeda T. Growth, metabolism and growth efficiency of a euphausiid crustacean Euphausia pacifica in the southern Japan Sea, as influenced by temperature J. Plankton Res. 17 1995 1757 1769 10.1093/plankt/17.9.1757 · DOI
  29. Katayama Y. Becker D.P. Tamura T. Hovda D.A. Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury J. Neurosurg. 73 1990 889 900 10.3171/jns.1990.73.6.0889 1977896 · DOI
  30. Lalive A.L. Munoz M.B. Bellone C. Slesinger P.A. Lüscher C. Tan K.R. Firing modes of dopamine neurons drive bidirectional GIRK channel plasticity J. Neurosci. 34 2014 5107 5114 10.1523/JNEUROSCI.5203-13.2014 24719090 PMC3983796 · DOI
  31. Lane B.J. Samarth P. Ransdell J.L. Nair S.S. Schulz D.J. Synergistic plasticity of intrinsic conductance and electrical coupling restores synchrony in an intact motor network Elife 5 2016 e16879 10.7554/eLife.16879 27552052 PMC5026470 · DOI
  32. Li C.Y. Lu J.T. Wu C.P. Duan S.M. Poo M.M. Bidirectional modification of presynaptic neuronal excitability accompanying spike timing-dependent synaptic plasticity Neuron 41 2004 257 268 10.1016/S0896-6273(03)00847-X 14741106 · DOI
  33. Marder E. Goaillard J.-M. Variability, compensation and homeostasis in neuron and network function Nat. Rev. Neurosci. 7 2006 563 574 10.1038/nrn1949 16791145 · DOI · Paper page
  34. Matzel L.D. Rogers R.F. Talk A.C. Bidirectional regulation of neuronal potassium currents by the G-protein activator aluminum fluoride as a function of intracellular calcium concentration Neuroscience 74 1996 1175 1185 10.1016/0306-4522(96)00188-1 8895884 · DOI
  35. Mease R.A. Famulare M. Gjorgjieva J. Moody W.J. Fairhall A.L. Emergence of adaptive computation by single neurons in the developing cortex J. Neurosci. 33 2013 12154 12170 10.1523/JNEUROSCI.3263-12.2013 23884925 PMC3721832 · DOI
  36. Misonou H. Mohapatra D.P. Park E.W. Leung V. Zhen D. Misonou K. Anderson A.E. Trimmer J.S. Regulation of ion channel localization and phosphorylation by neuronal activity Nat. Neurosci. 7 2004 711 718 10.1038/nn1260 15195093 · DOI
  37. Moody W.J. Jr. Futamachi K.J. Prince D.A. Extracellular potassium activity during epileptogenesis Exp. Neurol. 42 1974 248 263 10.1016/0014-4886(74)90023-5 4824976 · DOI
  38. Morris L.G. Hooper S.L. Muscle response to changing neuronal input in the lobster (Panulirus interruptus) stomatogastric system: spike number-versus spike frequency-dependent domains J. Neurosci. 17 1997 5956 5971 10.1523/JNEUROSCI.17-15-05956.1997 9221792 PMC6573197 · DOI
  39. Morrison B. III Elkin B.S. Dollé J.P. Yarmush M.L. In vitro models of traumatic brain injury Annu. Rev. Biomed. Eng. 13 2011 91 126 10.1146/annurev-bioeng-071910-124706 21529164 · DOI
  40. O'Leary T. Marder E. Mapping neural activation onto behavior in an entire animal Science 344 2014 372 373 10.1126/science.1253853 24763581 · DOI
  41. O'Leary T. Marder E. Temperature-robust neural function from activity-dependent ion channel regulation Curr. Biol. 26 2016 2935 2941 10.1016/j.cub.2016.08.061 27746024 PMC5111818 · DOI
  42. O’Leary T. van Rossum M.C.W. Wyllie D.J.A. Homeostasis of intrinsic excitability in hippocampal neurones: dynamics and mechanism of the response to chronic depolarization: homeostatic regulation of intrinsic excitability J. Physiol. 588 2010 157 170 10.1113/jphysiol.2009.181024 19917565 PMC2821556 · DOI
  43. Park K.S. Mohapatra D.P. Misonou H. Trimmer J.S. Graded regulation of the Kv2.1 potassium channel by variable phosphorylation Science 313 2006 976 979 10.1126/science.1124254 16917065 · DOI
  44. Powell D. Haddad S.A. Gorur-Shandilya S. Marder E. Coupling between fast and slow oscillator circuits in Cancer borealis is temperature-compensated Elife 10 2021 e60454 10.7554/eLife.60454 33538245 PMC7889077 · DOI
  45. Prinz A.A. Neuronal plasticity: how do neurons know what to do? Curr. Biol. 24 2014 R1044 R1046 10.1016/j.cub.2014.09.064 25517368 · DOI
  46. Prinz A.A. Bucher D. Marder E. Similar network activity from disparate circuit parameters Nat. Neurosci. 7 2004 1345 1352 10.1038/nn1352 15558066 · DOI · Paper page
  47. Rannals M.D. Kapur J. Homeostatic strengthening of inhibitory synapses is mediated by the accumulation of GABAA receptors J. Neurosci. 31 2011 17701 17712 10.1523/JNEUROSCI.4476-11.2011 22131430 PMC3396123 · DOI
  48. Ratliff J. Franci A. Marder E. O’Leary T. Neuronal oscillator robustness to multiple global perturbations Biophys. J. 120 2021 1454 1468 10.1016/j.bpj.2021.01.038 33610580 PMC8105708 · DOI
  49. Rezer E. Moulins M. Expression of the crustacean pyloric pattern generator in the intact animal J. Comp. Physiol. 153 1983 17 28 10.1007/BF00610338 · DOI
  50. Roach J.P. Sander L.M. Zochowski M.R. Memory recall and spike-frequency adaptation Phys. Rev. E 93 2016 052307 10.1103/PhysRevE.93.052307 27300910 PMC4911895 · DOI
  51. Rodgers C.I. Armstrong G.A.B. Shoemaker K.L. LaBrie J.D. Moyes C.D. Robertson R.M. Stress preconditioning of spreading depression in the locust CNS PLoS One 2 2007 e1366 10.1371/journal.pone.0001366 18159249 PMC2137934 · DOI
  52. Rodríguez-Sosa L. de la Vega M.T. Vergara P. Aréchiga H. Seasonal rhythm of red pigment concentrating hormone in the crayfish Chronobiol. Int. 14 1997 639 645 10.3109/07420529709001453 9360029 · DOI
  53. Ruangkittisakul A. Panaitescu B. Ballanyi K. K+ and Ca2+ dependence of inspiratory-related rhythm in novel "calibrated" mouse brainstem slices Respir. Physiol. Neurobiol. 175 2011 37 48 10.1016/j.resp.2010.09.004 20833274 · DOI
  54. Rybak I.A. Molkov Y.I. Jasinski P.E. Shevtsova N.A. Smith J.C. Rhythmic bursting in the pre-bötzinger complex Prog. Brain Res. 209 2014 1 23 10.1016/B978-0-444-63274-6.00001-1 24746040 PMC4059190 · DOI
  55. Sakurai A. Tamvacakis A.N. Katz P.S. Hidden synaptic differences in a neural circuit underlie differential behavioral susceptibility to a neural injury Elife 3 2014 e02598 10.7554/eLife.02598 PMC4084405 24920390 · DOI
  56. Schulz D.J. Goaillard J.-M. Marder E. Variable channel expression in identified single and electrically coupled neurons in different animals Nat. Neurosci. 9 2006 356 362 10.1038/nn1639 16444270 · DOI · Paper page
  57. Seeburg D.P. Sheng M. Activity-induced Polo-like kinase 2 is required for homeostatic plasticity of hippocampal neurons during epileptiform activity J. Neurosci. 28 2008 6583 6591 10.1523/JNEUROSCI.1853-08.2008 18579731 PMC3844828 · DOI
  58. Sharma N. Gabel H.W. Greenberg M.E. A shortcut to activity-dependent transcription Cell 161 2015 1496 1498 10.1016/j.cell.2015.06.009 26091031 · DOI
  59. Soofi W. Goeritz M.L. Kispersky T.J. Prinz A.A. Marder E. Stein W. Phase maintenance in a rhythmic motor pattern during temperature changes in vivo J. Neurophysiol. 111 2014 2603 2613 10.1152/jn.00906.2013 24671541 PMC4044431 · DOI · Paper page
  60. Temporal S. Lett K.M. Schulz D.J. Activity-dependent feedback regulates correlated ion channel mRNA levels in single identified motor neurons Curr. Biol. 24 2014 1899 1904 10.1016/j.cub.2014.06.067 25088555 · DOI
  61. Turrigiano G.G. Leslie K.R. Desai N.S. Rutherford L.C. Nelson S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons Nature 391 1998 892 896 10.1038/36103 9495341 · DOI · Paper page
  62. Turrigiano G.G. Nelson S.B. Homeostatic plasticity in the developing nervous system Nat. Rev. Neurosci. 5 2004 97 107 10.1038/nrn1327 14735113 · DOI · Paper page
  63. Verstynen T. Sabes P.N. How each movement changes the next: an experimental and theoretical study of fast adaptive priors in reaching J. Neurosci. 31 2011 10050 10059 10.1523/JNEUROSCI.6525-10.2011 21734297 PMC3148097 · DOI
  64. Yang J. Lee J. Lisberger S.G. The interaction of Bayesian priors and sensory data and its neural circuit implementation in visually guided movement J. Neurosci. 32 2012 17632 17645 10.1523/JNEUROSCI.1163-12.2012 23223286 PMC3527106 · DOI

Cited by

Sorted by citations

Authors
Rue, M. C. P., Alonso, L. M., & Marder, E.
Affiliations
Brandeis University (US)
Corresponding author
Marder, Eve
Venue
iScience
Publisher
Elsevier BV
Published
2022-09
Volume
25
Issue
9
Pages
104919
ISSN
2589-0042 (ISSN-L)
OpenAlex
W4293744914
Cited by
15
References
1
Citations by year
2026: 5 · 2025: 2 · 2024: 5 · 2023: 3
FWCI
1.11
Type
journal article
Language
en
Open access
Locations
  • iScience (publishedVersion, cc-by)
  • SSRN Electronic Journal (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
National Institutes of Health (R35 NS097343, R01 MH046742, F31-NS113383)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Keywords
pyloric circuit, Cancer borealis, extracellular potassium, burst firing, hyperpolarizing current, seasonal variation, neuronal sensitivity

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