Dynamics of ionic shifts in cortical spreading depression

Cerebral Cortex

Volumn 25, Issue 11, 2015, Pages 4469-4476

  Enger, Rune ^a,b   Tang, Wannan ^b,c   Vindedal, Gry Fluge ^b   Jensen, Vidar ^b   Helm, P Johannes ^b   Sprengel, Rolf ^c   Looger, Loren L ^d   Nagelhus, Erlend A ^a,b,c  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Astrocytes; Calcium; Glutamate; Migraine; Potassium

Indexed keywords

CALCIUM ION; GLUTAMIC ACID; POTASSIUM CHLORIDE; POTASSIUM ION; GLIAL FIBRILLARY ACIDIC PROTEIN; ION; PHOTOPROTEIN; POTASSIUM; SYNAPSIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN CELL; BRAIN ELECTROPHYSIOLOGY; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONTROLLED STUDY; CRANIOTOMY; DIFFUSION; DYNAMICS; FLUORESCENCE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SPREADING CORTICAL DEPRESSION; VISUAL CORTEX; ANALYSIS OF VARIANCE; ANIMAL; BRAIN CORTEX; C57BL MOUSE; DOSE RESPONSE; DRUG EFFECTS; GENETIC TRANSDUCTION; GENETICS; METABOLISM; NERVE CELL; NONLINEAR SYSTEM; PATCH CLAMP TECHNIQUE; PHYSIOLOGY;

ANALYSIS OF VARIANCE; ANIMALS; CEREBRAL CORTEX; CORTICAL SPREADING DEPRESSION; DOSE-RESPONSE RELATIONSHIP, DRUG; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; IONS; LUMINESCENT PROTEINS; MALE; MICE; MICE, INBRED C57BL; NEURONS; NONLINEAR DYNAMICS; PATCH-CLAMP TECHNIQUES; POTASSIUM; SYNAPSINS; TRANSDUCTION, GENETIC;

EID: 84944800222     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhv054     Document Type: Article

References (35)

1. Aiba I, Shuttleworth CW. 2012. Sustained NMDA receptor activation by spreading depolarizations can initiate excitotoxic injury in metabolically compromised neurons. J Physiol. 590:5877-5893.
2. Andersen P, Silfvenius H, Sundberg SH, Sveen O, Wigstrom H. 1978. Functional characteristics of unmyelinated fibres in the hippocampal cortex. Brain Res. 144:11-18.
3. Buzsaki G, Kandel A. 1998. Somadendritic backpropagation of action potentials in cortical pyramidal cells of the awake rat. J Neurophysiol. 79:1587-1591.
4. Charles AC, Baca SM. 2013. Cortical spreading depression and migraine. Nat Rev Neurol. 9:637-644.
5. Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V, et al. 2013. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature. 499:295-300.
6. Chuquet J, Hollender L, Nimchinsky EA. 2007. High-resolution in vivo imaging of the neurovascular unit during spreading depression. J Neurosci. 27:4036-4044.
7. Dreier JP. 2011. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med. 17:439-447.
8. Fabricius M, Jensen LH, Lauritzen M. 1993. Microdialysis of interstitial amino acids during spreading depression and anoxic depolarization in rat neocortex. Brain Res. 612:61-69.
9. Grafstein B. 1956. Mechanism of spreading cortical depression. J Neurophysiol. 19:154-171.
10. Hadjikhani N, Sanchez Del Rio M, Wu O, Schwartz D, Bakker D, Fischl B, Kwong KK, Cutrer FM, Rosen BR, Tootell RB, et al. 2001. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci USA. 98: 4687-4692.
11. Herreras O, Largo C, Ibarz JM, Somjen GG, Martin del Rio R. 1994. Role of neuronal synchronizing mechanisms in the propagation of spreading depression in the in vivo hippocampus. J Neurosci. 14:7087-7098.
12. Hirrlinger J, Scheller A, Hirrlinger PG, Kellert B, TangW,Wehr MC, Goebbels S, Reichenbach A, Sprengel R, Rossner MJ, et al. 2009. Split-cre complementation indicates coincident activity of different genes in vivo. PloS One. 4:e4286.
13. Kasischke KA, Lambert EM, Panepento B, Sun A, Gelbard HA, Burgess RW, Foster TH, Nedergaard M. 2011. Two-photon NADH imaging exposes boundaries of oxygen diffusion in cortical vascular supply regions. J Cereb Blood Flow Metab. 31:68-81.
14. Kitahara Y, Taga K, Abe H, Shimoji K. 2001. The effects of anesthetics on cortical spreading depression elicitation and c-fos expression in rats. J Neurosurg Anesthesiol. 13:26-32.
15. Kudo C, Toyama M, Boku A, Hanamoto H, Morimoto Y, Sugimura M, Niwa H. 2013. Anesthetic effects on susceptibility to cortical spreading depression. Neuropharmacology. 67:32-36.
16. Leão AAP. 1944. Spreading depression of activity in the cerebral cortex. J Neurophysiol. 7:359-390.
17. Leibowitz DH. 1992. The glial spike theory. I. On an active role of neuroglia in spreading depression and migraine. Proc Biol Sci. 250:287-295.
18. Marvin JS, Borghuis BG, Tian L, Cichon J, Harnett MT, Akerboom J, Gordus A, Renninger SL, Chen TW, Bargmann CI, et al. 2013. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat Methods. 10:162-170.
19. Nedergaard M. 1994. Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science. 263:1768-1771.
20. Peters O, Schipke CG, Hashimoto Y, Kettenmann H. 2003. Different mechanisms promote astrocyte Ca2+ waves and spreading depression in the mouse neocortex. J Neurosci. 23: 9888-9896.
21. Pietrobon D, Moskowitz MA. 2014. Chaos and commotion in the wake of cortical spreading depression and spreading depolarizations. Nat Rev Neurosci. 15:379-393.
22. Reeves AM, Shigetomi E, Khakh BS. 2011. Bulk loading of calcium indicator dyes to study astrocyte physiology: key limitations and improvements using morphological maps. J Neurosci. 31:9353-9358.
23. Sakadzic S, Roussakis E, Yaseen MA, Mandeville ET, Srinivasan VJ, Arai K, Ruvinskaya S, Devor A, Lo EH, Vinogradov SA, et al. 2010. Two-photon high-resolution measurement of partial pressure of oxygen in cerebral vasculature and tissue. Nat Methods. 7:755-759.
24. Shevtsova Z, Malik JM, Michel U, Bahr M, Kugler S. 2005. Promoters and serotypes: targeting of adeno-associated virus vectors for gene transfer in the rat central nervous system in vitro and in vivo. Exp Physiol. 90:53-59.
25. Smith RH, Levy JR, Kotin RM. 2009. A simplified baculovirus-AAV expression vector system coupled with one-step affinity purification yields high-titer rAAV stocks from insect cells. Mol Ther. 17:1888-1896.
26. Somjen GG. 2001. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev. 81:1065-1096.
27. Sykova E, Nicholson C. 2008. Diffusion in brain extracellular space. Physiol Rev. 88:1277-1340.
28. Takano T, Nedergaard M. 2009. Deciphering migraine. J Clin Invest. 119:16-19.
29. Takano T, Tian GF, Peng W, Lou N, Libionka W, Han X, Nedergaard M. 2006. Astrocyte-mediated control of cerebral blood flow. Nat Neurosci. 9:260-267.
30. Takano T, Tian GF, Peng W, Lou N, Lovatt D, Hansen AJ, Kasischke KA, Nedergaard M. 2007. Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci. 10:754-762.
31. TangW, Ehrlich I, Wolff SB, Michalski AM, Wolfl S, Hasan MT, Luthi A, Sprengel R. 2009. Faithful expression of multiple proteins via 2A-peptide self-processing: A versatile and reliable method for manipulating brain circuits. J Neurosci. 29:8621-8629.
32. Van Harreveld A. 1959. Compounds in brain extracts causing spreading depression of cerebral cortical activity and contraction of crustacean muscle. J Neurochem. 3:300-315.
33. Voipio J, Pasternack M, MacLeod K. 1994. Ion-sensitive microelectrodes. In: Ogden D, editors. The Plymouth Workshop Handbook, 2nd ed. Cambridge, UK: Company of Biologists. p 275-316.
34. Vyskocil F, Kritz N, Bures J. 1972. Potassium-selective microelectrodes used for measuring the extracellular brain potassium during spreading depression and anoxic depolarization in rats. Brain Res. 39:255-259.
35. Yaseen MA, Srinivasan VJ, Sakadzic S, Radhakrishnan H, Gorczynska I, WuW, Fujimoto JG, Boas DA. 2011. Microvascular oxygen tension and flow measurements in rodent cerebral cortex during baseline conditions and functional activation. J Cereb Blood Flow Metab. 31:1051-1063.