Unification of neuronal spikes, seizures, and spreading depression

Journal of Neuroscience

Volumn 34, Issue 35, 2014, Pages 11733-11743

  Wei, Yina ^a   Ullah, Ghanim ^c,d   Schiff, Steven J ^a,b,d  

^a The Center for Nanotechnology Education and Utilization   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

Ion concentrations; Oxygen; Seizures; Spikes; Spreading depression; Volume

Indexed keywords

CHLORIDE ION; OXYGEN; POTASSIUM ION; SODIUM ION;

ARTICLE; DEPRESSION; ELECTROENCEPHALOGRAPHY; GOLDMAN HODGKIN KATZ MODEL; HODGKIN HUXLEY EQUATION; ION CONDUCTANCE; ION TRANSPORT; MATHEMATICAL MODEL; MEMBRANE POTENTIAL; OSMOLALITY; OXYGEN CONCENTRATION; PRIORITY JOURNAL; PUMP CURRENT; SEIZURE; SPIKE WAVE; VOLUME FRACTION;

ION CONCENTRATIONS; OXYGEN; SEIZURES; SPIKES; SPREADING DEPRESSION; VOLUME;

CORTICAL SPREADING DEPRESSION; MODELS, NEUROLOGICAL; MODELS, THEORETICAL; NEURONS; SEIZURES;

EID: 84906539438     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0516-14.2014     Document Type: Article

References (62)

1. Albowitz R. (1939) The theory of emergence. Chicago: University of Chicago.
2. Allgower E., Georg K (1980) Simplicial and continuation methods for approximating fixed points and solutions to systems of equations. Siam Rev 22:28-85. CrossRef
3. Anderson T. R, Andrew RD (2002) Spreading depression: imaging and blockade in the rat neocortical brain slice. J Neurophysiol 88:2713-2725. CrossRef Medline
4. Arumugam T. V, Okun E, MattsonMP (2010) Basis of ionic dysregulation in cerebral ischemia. In: New strategies in stroke intervention, Chap 1 (Annunziato L, ed), pp 1-11. Totowa, NJ: Humana.
5. Attwell D., Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133-1145. CrossRef Medline
6. Barreto E., Cressman JR (2011) Ion concentration dynamics as a mechanism for neuronal bursting. J Biol Phys 37:361-373. CrossRef Medline
7. Berger H. (1933) Über das elektrenkephalogramm des menschen. Archiv für Psychiatrie und Nervenkrankheiten 98:231-254. CrossRef
8. Canals S., Makarova I, López-Aguado L, Largo C, Ibarz JM, Herreras O (2005) Longitudinal depolarization gradients along the somatodendritic axis of CA1 pyramidal cells: a novel feature of spreading depression. J Neurophysiol 94:943-951. CrossRef Medline
9. Cressman J. R Jr, Ullah G, Žiburkus J, Schiff SJ, Barreto E (2009) The influence of sodium and potassium dynamics on excitability, seizures, and the stability of persistent states: I. Single neuron dynamics. J Comput Neurosci 26:159-170. CrossRef Medline
10. Czéh G., Aitken PG, SomjenGG (1993) Membrane currents in CA1 pyramidal cells during spreading depression (SD) and SD-like hypoxic depolarization. Brain Res 632:195-208. CrossRef Medline
11. Dreier J. P (2011) The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med 17:439-447. CrossRef Medline
12. Endresen L., Hall K, Høye JS, Myrheim J (2000) A theory for the membrane potential of living cells. Eur Biophys J 29:90-103. CrossRef Medline
13. Erecińska M., Dagani F (1990) Relationships between the neuronal sodium/ potassium pump and energy metabolism. J Gen Physiol 95:591-616. CrossRef Medline
14. Ermentrout G. (2002) Simulating, analyzing, and animating dynamical systems: a guide to XPPAUT for researchers and students. Philadelphia: Society for Industrial and Applied Mathematics.
15. Gloor S. M (1997) Relevance of Na, K-ATPase to local extracellular potassium homeostasis and modulation of synaptic transmission. FEBS Lett 412:1-4. CrossRef Medline
16. Gloveli T., Dugladze T, Saha S, Monyer H, Heinemann U, Traub RD, Whittington MA, Buhl EH (2005) Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro. J Physiol 562:131-147. CrossRef Medline
17. Haglund M. M, Schwartzkroin PA (1990) Role of Na-K pump potassium regulation and IPSPs in seizures and spreading depression in immature rabbit hippocampal slices. J Neurophysiol 63:225-239. Medline
18. Hansen A. J, Zeuthen T (1981) Extracellular ion concentrations during spreading depression and ischemia in the rat brain cortex. Acta Physiol Scand 113:437-445. CrossRef Medline
19. Hibino H., Inanobe A, Furutani K, Murakami S, Findlay I, Kurachi Y (2010) Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol Rev 90:291-366. CrossRef Medline
20. Hille B. (2001) Ion channels of excitable membranes. Sunderland, MA: Sinauer.
21. Hodgkin A. L, Katz B (1949) The effect of sodium ions on the electrical activity of the giant axon of the squid. J Physiol 108:37-77. Medline
22. Hodgkin A. L, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500-544. Medline
23. Homer L., Shelton JB, Williams TJ (1983) Diffusion of oxygen in slices of rat brain. Am J Physiol 244:R15-R22. Medline
24. Hund T. J, Kucera JP, Otani NF, Rudy Y (2001) Ionic charge conservation and long-term steady state in the Luo-Rudy dynamic cell model. Biophys J 81:3324-3331. CrossRef Medline
25. Ingram J. M, Zhang C, Xu J, Schiff SJ (2013) FRET excited ratiometric oxygen sensing in living tissue. J Neurosci Methods 214:45-51. CrossRef Medline
26. Jing J., Aitken PG, Somjen GG (1994) Interstitial volume changes during spreading depression (SD) and SD-like hypoxia depolarization in hippocampal tissue slices. J Neurophysiol 71:2548-2551. Medline
27. Jirsa V. K, Stacey WC, Quilichini PP, Ivanov AI, Bernard C (2014) On the nature of seizure dynamics. Brain 137:2210-2230. CrossRef Medline
28. Kager H., Wadman WJ, Somjen GG (2000) Simulated seizures and spreading depression in a neuron model incorporating interstitial space and ion concentrations. J Neurophysiol 84:495-512. Medline
29. Kager H., Wadman WJ, Somjen GG (2002) Conditions for the triggering of spreading depression studied with computer simulations. J Neurophysiol 88:2700-2712. CrossRef Medline
30. Kager H., Wadman WJ, Somjen GG (2007) Seizure-like afterdischarges simulated in a model neuron. J Comput Neurosci 22:105-128. CrossRef Medline
31. Kneller J., Ramirez RJ, Chartier D, Courtemanche M, Nattel S (2002) Timedependent transients in an ionically based mathematical model of the canine atrial action potential. Am J Physiol Heart Circ Physiol 282: H1437-H1451. CrossRef Medline
32. Kramer M. A, Truccolo W, Eden UT, Lepage KQ, Hochberg LR, Eskandar EN, Madsen J. R, Lee JW, Maheshwari A, Halgren E, Chu CJ, Cash SS (2012) Human seizures self-terminate across spatial scales via a critical transition. Proc Natl Acad Sci U S A 109:21116-211121. CrossRef Medline
33. Krishnan G. P, BazhenovM (2011) Ionic dynamics mediate spontaneous termination of seizures and postictal depression state. J Neurosci 31:8870-8882. CrossRef Medline
34. Lauf P. K, Adragna NC (2000) K-Cl cotransport: properties and molecular mechanism. Cell Physiol Biochem 10:341-354. CrossRef Medline
35. Lauritzen M., Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ (2011) Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J Cereb Blood Flow Metab 31:17-35. CrossRef Medline
36. Leao A. (1944) Spreading depression of activity in the cerebral cortex. J Neurophysiol 7:359-390.
37. Lee J., Kim SJ (2010) Spectrum measurement of fast optical signal of neural activity in brain tissue and its theoretical origin. Neuroimage 51:713-722. CrossRef Medline
38. Lennie P. (2003) The cost of cortical computation. Curr Biol 13:493-497. CrossRef Medline
39. Lewes G. (1874) Problems of life and mind. Cambridge: Welch Bigelow.
40. Nardou R., Ferrari DC, Ben-Ari Y (2013) Mechanisms and effects of seizures in the immature brain. Semin Fetal Neonatal Med 18:175-184. CrossRef Medline
41. Østby I., Øyehaug L, Einevoll GT, Nagelhus EA, Plahte E, Zeuthen T, Lloyd CM, Ottersen OP, Omholt SW (2009) Astrocytin mechanisms explaining neural-activity-induced shrinkage of extracneuronal space. PLoS Comput Biol 5:e1000272. CrossRef Medline
42. Øyehaug L., Østby I, Lloyd CM, Omholt SW, Einevoll GT (2012) Dependence of spontaneous neuronal firing and depolarisation block on astroglial membrane transport mechanisms. J Comput Neurosci 32:147-165. CrossRef Medline
43. Payne J. A, Rivera C, Voipio J, Kaila K (2003) Cation-chloride cotransporters in neuronal communication, development and trauma. Trends Neurosci 26:199-206. CrossRef Medline
44. Petrushanko I. Y, Bogdanov NB, Lapina N, Boldyrev AA, Gassmann M, Bogdanova AY (2007) Oxygen-induced regulation of Na/K ATPase in cerebellar granule cells. J Gen Physiol 130:389-398. CrossRef Medline
45. Prinz A. A, Bucher D, Marder E (2004) Similar network activity from disparate circuit parameters. Nat Neurosci 7:1345-1352. CrossRef Medline
46. Rogawski M. A (2010) Migraine and epilepsy: shared mechanisms? Epilepsia 51:80. CrossRef
47. Ros A. GC, Fluschnik T, Kropp J (2014) Variance-based control of regime shifts: bistability and oscillations. arXiv:1401.2034 [nlin. AO] 1:1-21.
48. Rubin J. E, Terman D (2004) High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J Comput Neurosci 16:211-235. CrossRef Medline
49. Scheffer M., Carpenter SR, Lenton TM, Bascompte J, Brock W, Dakos V, van de Koppel J, van de Leemput IA, Levin SA, van Nes EH, Pascual M, Vandermeer J. (2012) Anticipating critical transitions. Science 338:344-348. CrossRef Medline
50. Schiff S. J (2012) Neural control engineering. Cambridge: MIT.
51. Scott A., Sørensen M, Christiansen P (1999) Nonlinear science: emergence and dynamics of coherent structures. New York: Oxford UP.
52. Somjen G. G (2004) Ions in the brain. New York: Oxford UP.
53. Somjen G. G (2001) Mechanism of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 81:1065-1096. Medline
54. Su G., Kintner DB, Sun D (2002) Contribution of Na+-K+-Cl-cotransporter to high-[K+]o induced swelling and EAA release in astrocytes. Am J Physiol Cell Physiol 282:C1136-C1146. CrossRef Medline
55. Syková E., NicholsonC (2008) Diffusion in brain extracellular space. Physiol Rev 88:1277-1340. CrossRef Medline
56. Traub R. D, Wong RK, Miles R, Michelson H (1991) A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. J Neurophysiol 66:635-650. Medline
57. Traynelis S. F, Dingledine R (1988) Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J Neurophysiol 59:259-276. Medline
58. Wei Y., Ullah G, Ingram J, Schiff SJ (2014) Oxygen and seizure dynamics: II. Computational modeling. J Neurophysiol 112:213-223. CrossRef Medline
59. Witthoft A., Filosa JA, Karniadakis GE (2013) Potassium buffering in the neurovascular unit: models and sensitivity analysis. Biophys J 105:2046-2054. CrossRef Medline
60. Zandt B. J, ten Haken B, van Dijk JG, van Putten MJ (2011) Neural dynamics during anoxia and the "wave of death. " PloS One 6:e22127. CrossRef Medline
61. Zhou N., Gordon GR, Feighan D, MacVicar BA (2010) Transient swelling, acidification, and mitochondrial depolarization occurs in neuruons but not astrocytes during spreading depression. Cereb Cortex 20:2614-2624. CrossRef Medline
62. Žiburkus J., Cressman JR, Barreto E, Schiff SJ (2006) Interneuron and pyramidal cell interplay during in vitro seizure-like events. J Neurophysiol 95:3948-3954. CrossRef Medline