The Korean Journal of Physiology and Pharmacology

The Korean Society of Pharmacology (대한약리학회)
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Analysis of temperature-dependent abnormal bursting patterns of neurons in Aplysia

  • Hyun, Nam Gyu (Department of Physics, Jeju National University) ;
  • Hyun, Kwangho (Jeju Eastern Health Center) ;
  • Oh, Saecheol (Department of Anesthesiology and Pain Medicine, Daejeon St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Lee, Kyungmin (Laboratory for Behavioral Neural Circuitry and Physiology, Department of Anatomy, Brain Science and Engineering Institute, School of Medicine, Kyungpook National University)
  • Received : 2020.04.07
  • Accepted : 2020.05.29
  • Published : 2020.07.01
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Abstract

Temperature affects the firing pattern and electrical activity of neurons in animals, eliciting diverse responses depending on neuronal cell type. However, the mechanisms underlying such diverse responses are not well understood. In the present study, we performed in vitro recording of abdominal ganglia cells of Aplysia juliana, and analyzed their burst firing patterns. We identified atypical bursting patterns dependent on temperature that were totally different from classical bursting patterns observed in R15 neurons of A. juliana. We classified these abnormal bursting patterns into type 1 and type 2; type 1 abnormal single bursts are composed of two kinds of spikes with a long interspike interval (ISI) followed by short ISI regular firing, while type 2 abnormal single bursts are composed of complex multiplets. To investigate the mechanism underlying the temperature dependence of abnormal bursting, we employed simulations using a modified Plant model and determined that the temperature dependence of type 2 abnormal bursting is related to temperature-dependent scaling factors and activation or inactivation of potassium or sodium channels.

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References

  1. Burrows M. Effects of temperature on a central synapse between identified motor neurons in the locust. J Comp Physiol A. 1989;165:687-695. https://doi.org/10.1007/BF00611000
  2. Dalton JC, Hendrix DE. Effects of temperature on membrane potentials of lobster giant axon. Am J Physiol. 1962;202:491-494. https://doi.org/10.1152/ajplegacy.1962.202.3.491
  3. Frankenhaeuser B, Moore LE. The effect of temperature on the sodium and potassium permeability changes in myelinated nerve fibres of Xenopus laevis. J Physiol. 1963;169:431-437. https://doi.org/10.1113/jphysiol.1963.sp007269
  4. Heitler WJ, Edwards DH. Effect of temperature on a voltage-sensitive electrical synapse in crayfish. J Exp Biol. 1998;201(Pt 4):503-513. https://doi.org/10.1242/jeb.201.4.503
  5. Hodgkin AL, Katz B. The effect of temperature on the electrical activity of the giant axon of the squid. J Physiol. 1949;109:240-249. https://doi.org/10.1113/jphysiol.1949.sp004388
  6. Kerkut GA, Ridge RM. The effect of temperature changes on the activity of the neurones of the snail Helix aspersa. Comp Biochem Physiol. 1962;5:283-295. https://doi.org/10.1016/0010-406X(62)90057-9
  7. Hyun NG, Hyun KH, Hyun KB, Han JH, Lee K, Kaang BK. A computational model of the temperature-dependent changes in firing patterns in Aplysia neurons. Korean J Physiol Pharmacol. 2011;15:371-382. https://doi.org/10.4196/kjpp.2011.15.6.371
  8. Hyun NG, Hyun KH, Hyun KB, Lee K. Temperature-dependent bursting pattern analysis by modified Plant model. Mol Brain. 2014;7:50. https://doi.org/10.1186/s13041-014-0050-5
  9. Hyun NG, Hyun KH, Lee K, Kaang BK. Temperature dependence of action potential parameters in Aplysia neurons. Neurosignals. 2012;20:252-264. https://doi.org/10.1159/000334960
  10. Lim CS, Chung DY, Kaang BK. Partial anatomical and physiological characterization and dissociated cell culture of the nervous system of the marine mollusc Aplysia kurodai. Mol Cells. 1997;7:399-407.
  11. Lee SH, Lim CS, Park H, Lee JA, Han JH, Kim H, Cheang YH, Lee SH, Lee YS, Ko HG, Jang DH, Kim H, Miniaci MC, Bartsch D, Kim E, Bailey CH, Kandel ER, Kaang BK. Nuclear translocation of CAMassociated protein activates transcription for long-term facilitation in Aplysia. Cell. 2007;129:801-812. https://doi.org/10.1016/j.cell.2007.03.041
  12. Plant RE. Bifurcation and resonance in a model for bursting nerve cells. J Math Biol. 1981;11:15-32. https://doi.org/10.1007/BF00275821
  13. Plant RE, Kim M. Mathematical description of a bursting pacemaker neuron by a modification of the Hodgkin-Huxley equations. Biophys J. 1976;16:227-244. https://doi.org/10.1016/S0006-3495(76)85683-4
  14. Finke C, Freund JA, Rosa E Jr, Braun HA, Feudel U. On the role of subthreshold currents in the Huber-Braun cold receptor model. Chaos. 2010;20:045107. https://doi.org/10.1063/1.3527989
  15. Rinzel J, Lee YS. Dissection of a model for neuronal parabolic bursting. J Math Biol. 1987;25:653-675. https://doi.org/10.1007/BF00275501
  16. Picardo MC, Weragalaarachchi KT, Akins VT, Del Negro CA. Physiological and morphological properties of Dbx1-derived respiratory neurons in the pre-Botzinger complex of neonatal mice. J Physiol. 2013;591:2687-2703. https://doi.org/10.1113/jphysiol.2012.250118
  17. Pace RW, Mackay DD, Feldman JL, Del Negro CA. Inspiratory bursts in the preBotzinger complex depend on a calcium-activated non-specific cation current linked to glutamate receptors in neonatal mice. J Physiol. 2007;582(Pt 1):113-125. https://doi.org/10.1113/jphysiol.2007.133660
  18. Paton JF, Abdala AP, Koizumi H, Smith JC, St-John WM. Respiratory rhythm generation during gasping depends on persistent sodium current. Nat Neurosci. 2006;9:311-313. https://doi.org/10.1038/nn1650
  19. Rubin JE, Hayes JA, Mendenhall JL, Del Negro CA. Calcium-activated nonspecific cation current and synaptic depression promote network-dependent burst oscillations. Proc Natl Acad Sci U S A. 2009;106:2939-2944. https://doi.org/10.1073/pnas.0808776106
  20. Hou N, Armstrong GA, Chakraborty-Chatterjee M, Sokolowski MB, Robertson RM. $Na^{+}$-$K^{+}$-ATPase trafficking induced by heat shock pretreatment correlates with increased resistance to anoxia in locusts. J Neurophysiol. 2014;112:814-823. https://doi.org/10.1152/jn.00201.2014
  21. Money TG, Rodgers CI, McGregor SM, Robertson RM. Loss of potassium homeostasis underlies hyperthermic conduction failure in control and preconditioned locusts. J Neurophysiol. 2009;102:285-293. https://doi.org/10.1152/jn.91174.2008
  22. Pulver SR, Griffith LC. Spike integration and cellular memory in a rhythmic network from $Na^{+}$/$K^{+}$ pump current dynamics. Nat Neurosci. 2010;13:53-59. https://doi.org/10.1038/nn.2444
  23. Money TG, Anstey ML, Robertson RM. Heat stress-mediated plasticity in a locust looming-sensitive visual interneuron. J Neurophysiol. 2005;93:1908-1919. https://doi.org/10.1152/jn.00908.2004
  24. Maingret F, Lauritzen I, Patel AJ, Heurteaux C, Reyes R, Lesage F, Lazdunski M, Honore E. TREK-1 is a heat-activated background $K^{+}$ channel. EMBO J. 2000;19:2483-2491. https://doi.org/10.1093/emboj/19.11.2483