Cited by 8Neural dynamics and brain functionIon channel regulation and functionNeuroscience and Neuropharmacology Research

Ih block reveals separation of timescales in pyloric rhythm response to temperature changes in Cancer borealis

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Schapiro, Kyra, Rittenberg, JD, Kenngott, Max, Marder, Eve·2024·eLife

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Abstract

Motor systems operate over a range of frequencies and relative timing (phase). We studied the role of the hyperpolarization-activated inward current (I h ) in regulating these features in the pyloric rhythm of the stomatogastric ganglion (STG) of the crab, Cancer borealis, as temperature was altered from 11°C to 21°C. Under control conditions, rhythm frequency increased monotonically with temperature, while the phases of the pyloric dilator (PD), lateral pyloric (LP), and pyloric (PY) neurons remained constant. Blocking I h with cesium (Cs + ) phase advanced PD offset, LP onset, and LP offset at 11°C, and the latter two further advanced as temperature increased. In Cs + the frequency increase with temperature diminished and the Q 10 of the frequency dropped from ~1.75 to ~1.35. Unexpectedly in Cs + , the frequency dynamics became non-monotonic during temperature transitions; frequency initially dropped as temperature increased, then rose once temperature stabilized, creating a characteristic ‘jag’. Interestingly, these jags persisted during temperature transitions in Cs + when the pacemaker was isolated by picrotoxin, although the temperature-induced change in frequency recovered to control levels. Overall, these data suggest that I h plays an important role in maintaining smooth transitory responses and persistent frequency increases by different mechanisms in the pyloric circuitry during temperature fluctuations.

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  • Many biological processes vary considerably over 4-5 °C, well within the range of what is normally considered room temperature.

    “because many biological processes vary considerably over 4-5 • C [40,55-59], well within the range of what is normally considered room temperature.”

    From A feature and not a bug: Replication failures can lead to new biology (2026) · cites this paper as [59]

    The Results report that pyloric rhythm frequency increased with temperature, and the Temperature protocol describes measurements in 2°C steps from 11°C to 21°C (page not specified in our copy). This supports temperature sensitivity in one biological process, but not the broader claim about many processes or the characterization of a 4–5°C change as within room temperature. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

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  1. Alonso LM, Marder E. 2019. Visualization of currents in neural models with similar behavior and different conductance densities. eLife 8:e42722. DOI: https://doi.org/10.7554/eLife.42722, PMID: 30702427 · DOI · Paper page
  2. Alonso LM, Marder E. 2020. Temperature compensation in a small rhythmic circuit. eLife 9:e55470. DOI: https:// doi.org/10.7554/eLife.55470, PMID: 32484437 · DOI · Paper page
  3. Angstadt JD, Calabrese RL. 1989. A hyperpolarization-activated inward current in heart interneurons of the medicinal leech. The Journal of Neuroscience 9:2846-2857. DOI: https://doi.org/10.1523/JNEUROSCI.09-08- 02846.1989, PMID: 2769368 · DOI
  4. Anwar H, Martinez D, Bucher D, Nadim F. 2022. Inter-animal variability in activity phase is constrained by synaptic dynamics in an oscillatory network. Eneuro 9:ENEURO.. DOI: https://doi.org/10.1523/ENEURO.0027- 22.2022 · DOI
  5. Ballo AW, Keene JC, Troy PJ, Goeritz ML, Nadim F, Bucher D. 2010. Dopamine modulates Ih in a motor axon. The Journal of Neuroscience 30:8425-8434. DOI: https://doi.org/10.1523/JNEUROSCI.0405-10.2010, PMID: 20573890 · DOI
  6. Bidaut M. 1980. Pharmacological dissection of pyloric network of the lobster stomatogastric ganglion using picrotoxin. Journal of Neurophysiology 44:1089-1101. DOI: https://doi.org/10.1152/jn.1980.44.6.1089, PMID: 6256507 · DOI
  7. Biel M, Wahl-Schott C, Michalakis S, Zong X. 2009. Hyperpolarization-activated cation channels: from genes to function. Physiological Reviews 89:847-885. DOI: https://doi.org/10.1152/physrev.00029.2008, PMID: 19584315 · DOI
  8. Bose A, Manor Y, Nadim F. 2004. The activity phase of postsynaptic neurons in a simplified rhythmic network. Journal of Computational Neuroscience 17:245-261. DOI: https://doi.org/10.1023/B:JCNS.0000037685.71759. 1a, PMID: 15306742 · DOI
  9. Brown HF, DiFrancesco D, Noble SJ. 1979. How does adrenaline accelerate the heart? Nature 280:235-236. DOI: https://doi.org/10.1038/280235a0, PMID: 450140 · DOI
  10. Brown DA, Adams PR. 1980. Muscarinic suppression of a novel voltage-sensitive K + current in a vertebrate neurone. Nature 283:673-676. DOI: https://doi.org/10.1038/283673a0, PMID: 6965523 · DOI
  11. Calabrese RL, Nadim F, Olsen ØH. 1995. Heartbeat control in the medicinal leech: a model system for understanding the origin, coordination, and modulation of rhythmic motor patterns. Journal of Neurobiology 27:390-402. DOI: https://doi.org/10.1002/neu.480270311 · DOI
  12. Clay JR, Shlesinger MF. 1984. Analysis of the effects of cesium ions on potassium channel currents in biological membranes. Journal of Theoretical Biology 107:189-201. DOI: https://doi.org/10.1016/s0022-5193(84) 80021-1, PMID: 6325824 · DOI
  13. Coggan JS, Purnyn SL, Knoper SR, Kreulen DL. 1994. Muscarinic inhibition of two potassium currents in guinea-pig prevertebral neurons: differentiation by extracellular cesium. Neuroscience 59:349-361. DOI: https://doi.org/10.1016/0306-4522(94)90601-7, PMID: 8008197 · DOI
  14. Cohen AH, Ermentrout GB, Kiemel T, Kopell N, Sigvardt KA, Williams TL. 1992. Modelling of intersegmental coordination in the lamprey central pattern generator for locomotion. Trends in Neurosciences 15:434-438. DOI: https://doi.org/10.1016/0166-2236(92)90006-t, PMID: 1281350 · DOI
  15. Connor JA. 1975. Neural repetitive firing: a comparative study of membrane properties of crustacean walking leg axons. Journal of Neurophysiology 38:922-932. DOI: https://doi.org/10.1152/jn.1975.38.4.922, PMID: 1159472 · DOI
  16. Connor JA, Walter D, McKown R. 1977. Neural repetitive firing: modifications of the Hodgkin-Huxley axon suggested by experimental results from crustacean axons. Biophysical Journal 18:81-102. DOI: https://doi.org/ 10.1016/S0006-3495(77)85598-7, PMID: 856318 · DOI
  17. Connor JA. 1978. Slow repetitive activity from fast conductance changes in neurons. Federation Proceedings 37:2139-2145 PMID: 658453.
  18. DiFrancesco D. 1985. The cardiac hyperpolarizing-activated current, if. Origins and developments. Progress in Biophysics and Molecular Biology 46:163-183. DOI: https://doi.org/10.1016/0079-6107(85)90008-2 · DOI
  19. DiFrancesco D, Tromba C. 1987. Acetylcholine inhibits activation of the cardiac hyperpolarizing-activated current, if. Pflügers Archiv 410:139-142. DOI: https://doi.org/10.1007/BF00581906, PMID: 2825112 · DOI
  20. Eisen JS, Marder E. 1982. Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. III. Synaptic connections of electrically coupled pyloric neurons. Journal of Neurophysiology 48:1392-1415. DOI: https://doi.org/10.1152/jn.1982.48.6.1392, PMID: 6296329 · DOI
  21. Eisen JS, Marder E. 1984. A mechanism for production of phase shifts in A pattern generator. Journal of Neurophysiology 51:1375-1393. DOI: https://doi.org/10.1152/jn.1984.51.6.1375, PMID: 6145759 · DOI
  22. Goaillard JM, Taylor AL, Schulz DJ, Marder E. 2009. Functional consequences of animal-to-animal variation in circuit parameters. Nature Neuroscience 12:1424-1430. DOI: https://doi.org/10.1038/nn.2404, PMID: 19838180 · DOI
  23. Goaillard JM, Taylor AL, Pulver SR, Marder E. 2010. Slow and persistent postinhibitory rebound acts as an intrinsic short-term memory mechanism. The Journal of Neuroscience 30:4687-4692. DOI: https://doi.org/10. 1523/JNEUROSCI.2998-09.2010 · DOI
  24. Goeritz ML, Ouyang Q, Harris-Warrick RM. 2011. Localizatio n and function of Ih channels in a small neural network. Journal of Neurophysiology 106:44-58. DOI: https://doi.org/10.1152/jn.00897.2010.-Sub · DOI
  25. Golowasch J, Abbott LF, Marder E. 1999a. Activity-dependent regulation of potassium currents in an identified neuron of the stomatogastric ganglion of the crab Cancer borealis. The Journal of Neuroscience 19:RC33. DOI: https://doi.org/10.1523/JNEUROSCI.19-20-j0004.1999, PMID: 10516335 · DOI
  26. Golowasch J, Casey M, Abbott LF, Marder E. 1999b. Network stability from activity-dependent regulation of neuronal conductances. Neural Computation 11:1079-1096. DOI: https://doi.org/10.1162/ 089976699300016359, PMID: 10418158 · DOI
  27. Gorur-Shandilya S, Cronin EM, Schneider AC, Haddad SA, Rosenbaum P, Bucher D, Nadim F, Marder E. 2022. Mapping circuit dynamics during function and dysfunction. eLife 11:e76579. DOI: https://doi.org/10.7554/ eLife.76579, PMID: 35302489 · DOI · Paper page
  28. Greenberg I, Manor Y. 2005. Synaptic depression in conjunction with A-current channels promote phase constancy in A rhythmic network. Journal of Neurophysiology 93:656-677. DOI: https://doi.org/10.1152/jn. 00640.2004, PMID: 15356180 · DOI
  29. Grillner S. 1981. Control of locomotion in bipeds, tetrapods, and fish. Wiley. DOI: https://doi.org/10.1002/cphy. · DOI
  30. cp010226 · DOI
  31. Gutierrez GJ, Grashow RG. 2009. Cancer borealis stomatogastric nervous system dissection. J Visualized Experiments 25:1207. DOI: https://doi.org/10.3791/1207 · DOI
  32. Haddad SA, Marder E. 2018. Circuit robustness to temperature perturbation is altered by neuromodulators. Neuron 100:609-623.. DOI: https://doi.org/10.1016/j.neuron.2018.08.035, PMID: 30244886 · DOI
  33. Hagiwara N, Irisawa H. 1989. Modulation by intracellular Ca2 + of t he hyperpolarization-activated inward current in rabbit single sino-atrial node cells. J Physiol 409:121-141. DOI: https://doi.org/10.1113/JPHYSIOL.1989. · DOI
  34. SP017488 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. DOI: https://doi.org/10.1523/ENEURO.0058-14.2015, PMID: · DOI
  35. Harding SD, Armstrong JF, Faccenda E, Southan C, Alexander SPH, Davenport AP, Spedding M, Davies JA. 2024. The IUPHAR/BPS guide to pharmacology in 2024. Nucleic Acids Research 52:D1438-D1449. DOI: https://doi.org/10.1093/nar/gkad944 · DOI · Paper page
  36. 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. DOI: https://doi.org/10.1523/JNEUROSCI.15-01-00342.1995, PMID: 7823140 · DOI
  37. Hartline DK. 1979. Pattern generation in the lobster (Panulirus) stomatogastric ganglion. II. Pyloric network simulation. Biological Cybernetics 33:223-236. DOI: https://doi.org/10.1007/BF00337411, PMID: 227480 · DOI
  38. Hartline DK, Gassie DV. 1979. Pattern generation in the lobster (Panulirus) stomatogastric ganglion. I. Pyloric neuron kinetics and synaptic interactions. Biological Cybernetics 33:209-222. DOI: https://doi.org/10.1007/ BF00337410, PMID: 497265 · DOI
  39. Hooper SL. 1997. Phase maintenance in the pyloric pattern of the lobster (Panulirus interruptus) stomatogastric ganglion. Journal of Computational Neuroscience 4:191-205. DOI: https://doi.org/10.1023/a:1008822218061, PMID: 9257232 · DOI
  40. Hooper RM, Tikidji-Hamburyan RA, Canavier CC, Prinz AA. 2015. Feedback control of variability in the cycle period of a central pattern generator. Journal of Neurophysiology 114:2741-2752. DOI: https://doi.org/10. 1152/jn.00365.2015, PMID: 26334008 · DOI
  41. Johnson BR, Brown JM, Kvarta MD, Lu JYJ, Schneider LR, Nadim F, Harris-Warrick RM. 2011. Differential modulation of synaptic strength and timing regulate synaptic efficacy in a motor network. Journal of Neurophysiology 105:293-304. DOI: https://doi.org/10.1152/jn.00809.2010, PMID: 21047938 · DOI
  42. Khammash M. 2016. An engineering viewpoint on biological robustness. BMC Biology 14:22. DOI: https://doi. org/10.1186/s12915-016-0241-x, PMID: 27007299 · DOI
  43. Krenz WDC, Rodgers EW, Baro DJ. 2015. Tonic 5nM DA stabilizes neuronal output by enabling bidirectional activity-dependent regulation of the hyperpolarization activated current via PKA and calcineurin. PLOS ONE 10:e0117965. DOI: https://doi.org/10.1371/journal.pone.0117965, PMID: 25692473 · DOI
  44. MacLean JN, Zhang Y, Goeritz ML, Casey R, Oliva R, Guckenheimer J, Harris-Warrick RM. 2005. Activity- independent coregulation of IA and Ih in rhythmically active neurons. Journal of Neurophysiology 94:3601- 3617. DOI: https://doi.org/10.1152/jn.00281.2005, PMID: 16049145 · DOI
  45. Mamiya A, Nadim F. 2004. Dynamic interaction of oscillatory neurons coupled with reciprocally inhibitory synapses acts to stabilize the rhythm period. The Journal of Neuroscience 24:5140-5150. DOI: https://doi.org/ 10.1523/JNEUROSCI.0482-04.2004, PMID: 15175383 · DOI
  46. 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. DOI: https://doi.org/10.1523/ JNEUROSCI.17-14-05610.1997, PMID: 9204942 · DOI
  47. Manor Y, Bose A, Booth V, Nadim F. 2003. Contribution of synaptic depression to phase maintenance in a model rhythmic network. Journal of Neurophysiology 90:3513-3528. DOI: https://doi.org/10.1152/jn.00411.2003, PMID: 12815020 · DOI
  48. Marder E, Calabrese RL. 1996. Principles of rhythmic motor pattern generation. Physiological Reviews 76:687- 717. DOI: https://doi.org/10.1152/physrev.1996.76.3.687, PMID: 8757786 · DOI
  49. Marder E, Bucher D. 2007. Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annual Review of Physiology 69:291-316. DOI: https://doi.org/10.1146/annurev.physiol.69.031905. 161516, PMID: 17009928 · DOI · Paper page
  50. Marder E, Rue MCP. 2021. From the neuroscience of individual variability to climate change. The Journal of Neuroscience 41:10213-10221. DOI: https://doi.org/10.1523/JNEUROSCI.1261-21.2021 · DOI · Paper page
  51. Marder E, Kedia S, Morozova EO. 2022. New insights from small rhythmic circuits. Current Opinion in Neurobiology 76:102610. DOI: https://doi.org/10.1016/j.conb.2022.102610, PMID: 35986971 · DOI
  52. Martinez D, Anwar H, Bose A, Bucher DM, Nadim F. 2019. Short-term synaptic dynamics control the activity phase of neurons in an oscillatory network. eLife 8:e46911. DOI: https://doi.org/10.7554/eLife.46911, PMID: 31180323 · DOI
  53. McCormick DA, Pape HC. 1990a. Noradrenergic and serotonergic modulation of a hyperpolarization-activated cation current in thalamic relay neurones. The Journal of Physiology 431:319-342. DOI: https://doi.org/10. 1113/jphysiol.1990.sp018332, PMID: 1712844 · DOI
  54. McCormick DA, Pape HC. 1990b. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. The Journal of Physiology 431:291-318. DOI: https://doi.org/ 10.1113/jphysiol.1990.sp018331, PMID: 1712843 · DOI
  55. McGaw IJ, Curtis DL. 2013. A review of gastric processing in decapod crustaceans. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 183:443-465. DOI: https://doi.org/10. 1007/s00360-012-0730-3, PMID: 23266655 · DOI
  56. Morozova E, Newstein P, Marder E. 2022. Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation. eLife 11:e74363. DOI: https://doi.org/10.7554/eLife.74363, PMID: 35103594 · DOI
  57. Mouser C, Nadim F, Bose A. 2008. Maintaining phase of the crustacean tri-phasic pyloric rhythm. Journal of Mathematical Biology 57:161-181. DOI: https://doi.org/10.1007/s00285-007-0150-2, PMID: 18084765 · DOI
  58. Nadim F, Olsen ØH, de Schutter E, Calabrese RL. 1995. Modeling the leech heartbeat elemental oscillator I. Interactions of intrinsic and synaptic currents. Journal of Computational Neuroscience 2:215-235. DOI: https:// doi.org/10.1007/BF00961435 · DOI
  59. Nadim F, Zhao S, Zhou L, Bose A. 2011. Inhibitory feedback promotes stability in an oscillatory network. Journal of Neural Engineering 8:065001. DOI: https://doi.org/10.1088/1741-2560/8/6/065001, PMID: 22058272 · DOI
  60. Pape HC. 1996. Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annual Review of Physiology 58:299-327. DOI: https://doi.org/10.1146/annurev.ph.58.030196.001503 · DOI
  61. Peck JH, Gaier E, Stevens E, Repicky S, Harris-Warrick RM. 2006. Amine modulation of Ih in a small neural network. Journal of Neurophysiology 96:2931-2940. DOI: https://doi.org/10.1152/jn.00423.2005, PMID: 16943317 · DOI
  62. Powell D, Haddad SA, Gorur-Shandilya S, Marder E. 2021. Coupling between fast and slow oscillator circuits in Cancer borealis is temperature-compensated. eLife 10:e60454. DOI: https://doi.org/10.7554/eLife.60454 · DOI
  63. Prinz AA, Bucher D, Marder E. 2004. Similar network activity from disparate circuit parameters. Nature Neuroscience 7:1345-1352. DOI: https://doi.org/10.1038/nn1352, PMID: 15558066 · DOI · Paper page
  64. Rabbah P, Nadim F. 2005. Synaptic dynamics do not determine proper phase of activity in a central pattern generator. The Journal of Neuroscience 25:11269-11278. DOI: https://doi.org/10.1523/JNEUROSCI.3284-05. 2005, PMID: 16339022 · DOI
  65. Rinberg A, Taylor AL, Marder E. 2013. The effects of temperature on the stability of a neuronal oscillator. PLOS Computational Biology 9:e1002857. DOI: https://doi.org/10.1371/journal.pcbi.1002857, PMID: 23326223 · DOI
  66. Robinson RB, Siegelbaum SA. 2003. Hyperpolarization-activated cation currents: from molecules to physiological function. Annual Review of Physiology 65:453-480. DOI: https://doi.org/10.1146/annurev.physiol.65.092101. 142734, PMID: 12471170 · DOI
  67. Rodgers EW, Fu JJ, Krenz WDC, Baro DJ. 2011. Tonic nanomolar dopamine enables an activity-dependent phase recovery mechanism that persistently alters the maximal conductance of the hyperpolarization-activated current in a rhythmically active neuron. The Journal of Neuroscience 31:16387-16397. DOI: https://doi.org/10. 1523/JNEUROSCI.3770-11.2011, PMID: 22072689 · DOI
  68. 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. DOI: https://doi.org/10.1038/nn1639, PMID: 16444270 · DOI · Paper page
  69. 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. DOI: https://doi. org/10.1073/pnas.0705827104, PMID: 17652510 · DOI · Paper page
  70. 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. DOI: https://doi.org/ 10.1152/jn.00906.2013, PMID: 24671541 · DOI · Paper page
  71. Soofi W, Prinz AA. 2015. Differential effects of conductances on the phase resetting curve of a bursting neuronal oscillator. Journal of Computational Neuroscience 38:539-558. DOI: https://doi.org/10.1007/S10827-015- 0553-9/TABLES/ · DOI
  72. Stent GS, Thompson WJ, Calabrese RL. 1979. Neural control of heartbeat in the leech and in some other invertebrates. Physiological Reviews 59:101-136. DOI: https://doi.org/10.1152/physrev.1979.59.1.101, PMID: 220645 · DOI
  73. 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. DOI: https://doi.org/10.1371/journal.pbio.1000469, PMID: 20824168 · DOI · Paper page
  74. Thirumalai V, Prinz AA, Johnson CD, Marder E. 2006. Red pigment concentrating hormone strongly enhances the strength of the feedback to the pyloric rhythm oscillator but has little effect on pyloric rhythm period. Journal of Neurophysiology 95:1762-1770. DOI: https://doi.org/10.1152/jn.00764.2005, PMID: 16319213 · DOI
  75. Thoby-Brisson M, Telgkamp P, Ramirez JM. 2000. The role of the hyperpolarization-activated current in modulating rhythmic activity in the isolated respiratory network of mice. The Journal of Neuroscience 20:2994- 3005. DOI: https://doi.org/10.1523/JNEUROSCI.20-08-02994.2000, PMID: 10751452 · DOI
  76. Thoby-Brisson M, Cauli B, Champagnat J, Fortin G, Katz DM. 2003. Expression of functional tyrosine kinase B receptors by rhythmically active respiratory neurons in the pre-Bötzinger complex of neonatal mice. The Journal of Neuroscience 23:7685-7689. DOI: https://doi.org/10.1523/JNEUROSCI.23-20-07685.2003, PMID: 12930808 · DOI
  77. Tierney AJ, Harris-Warrick RM. 1992. Physiological role of the transient potassium current in the pyloric circuit of the lobster stomatogastric ganglion. Journal of Neurophysiology 67:599-609. DOI: https://doi.org/10.1152/jn. 1992.67.3.599, PMID: 1578246 · DOI
  78. Tobin AE, Calabrese RL. 2005. Myomodulin increases Ih and inhibits the NA/K pump to modulate bursting in leech heart interneurons. Journal of Neurophysiology 94:3938-3950. DOI: https://doi.org/10.1152/jn.00340. 2005, PMID: 16093342 · DOI
  79. Tsien RW, Giles W, Greengard P. 1972. Cyclic AMP mediates the effects of adrenaline on cardiac purkinje fibres. Nature 240:181-183. DOI: https://doi.org/10.1038/newbio240181a0, PMID: 4343950 · DOI
  80. Weaver AL, Hooper SL. 2003. Follower neurons in lobster (Panulirus interruptus) pyloric network regulate pacemaker period in complementary ways. Journal of Neurophysiology 89:1327-1338. DOI: https://doi.org/10. 1152/jn.00704.2002, PMID: 12611999 · DOI
  81. Wenning A, Cymbalyuk GS, Calabrese RLHC. 2004. Heartbeat control in leeches. I. constriction pattern and neural modulation of blood pressure in intact animals. Journal of Neurophysiology 91:382-396. DOI: https:// doi.org/10.1152/jn.00526.2003, PMID: 13679406 · DOI
  82. Wischmeyer E, Karschin A. 1997. A novel slow hyperpolarization-activated potassium current (IK(SHA)) from A mouse hippocampal cell line. The Journal of Physiology 504 (Pt 3):591-602. DOI: https://doi.org/10.1111/j. 1469-7793.1997.591bd.x, PMID: 9401967 · DOI
  83. Yanagihara K, Irisawa H. 1980. Inward current activated during hyperpolarization in the rabbit sinoatrial node cell. Pflügers Archiv 385:11-19. DOI: https://doi.org/10.1007/BF00583909, PMID: 7191093 · DOI
  84. Zhang Y, Oliva R, Gisselmann G, Hatt H, Guckenheimer J, Harris-Warrick RM. 2003. Overexpression of a hyperpolarization-activated cation current (Ih) channel gene modifies the firing activity of identified motor neurons in a small neural network. The Journal of Neuroscience 23:9059-9067. DOI: https://doi.org/10.1523/ JNEUROSCI.23-27-09059.2003, PMID: 14534239 · DOI
  85. Zhu L, Selverston AI, Ayers J. 2016. Role of Ih in differentiating the dynamics of the gastric and pyloric neurons in the stomatogastric ganglion of the lobster, Homarus americanus. Journal of Neurophysiology 115:2434-2445. DOI: https://doi.org/10.1152/jn.00737.2015, PMID: 26912595 · DOI

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Authors
Schapiro, K., Rittenberg, J., Kenngott, M., & Marder, E.
Affiliations
Brandeis University (US)
Corresponding author
Schapiro, Kyra
Venue
eLife
Published
2024-10-15
Volume
13
ISSN
2050-084X (ISSN-L)
OpenAlex
W4403430281
Cited by
8
References
0
Citations by year
2026: 7 · 2025: 1
Type
posted content
Language
en
Open access
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
National Institute of Neurological Disorders and Stroke (T32NS007292, R35NS097343)
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
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
hyperpolarization-activated current, pyloric rhythm, stomatogastric ganglion, Cancer borealis, temperature effects, cesium block, pyloric dilator neuron, lateral pyloric neuron, cardiac pacemaker, Q10, time-scale separation, crustacean motor control

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Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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