Minimum conditions for the induction of cortical spreading depression in brain slices

Journal of Neurophysiology

Volumn 112, Issue 10, 2014, Pages 2572-2579

  Tang, Yujie T ^a   Mendez, Jorge M ^b   Theriot, Jeremy J ^b   Sawant, Punam M ^b   López Valdés, Héctor E ^c   Ju, Y Sungtaek ^a   Brennan, K C ^b  

^a University of California   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cortical spreading depression; Microfluidics; Migraine

Indexed keywords

POTASSIUM ION; POTASSIUM;

ACTIVE TRANSPORT; ANALYTICAL PARAMETERS; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN SLICE; CONTROLLED STUDY; DEPOLARIZATION; DIFFRACTION; DIFFUSION COEFFICIENT; ELECTRIC POTENTIAL; ELECTROENCEPHALOGRAM; EXTRACELLULAR SPACE; GENERAL DEVICE; ION CURRENT; LASER MICROSCOPY; LIGHT SCATTERING; MALE; MECHANICAL STIMULATION; MICROFLUIDIC DEVICE; MICROFLUIDICS; MOUSE; NONHUMAN; OPTICS; POTASSIUM CELL LEVEL; SPREADING CORTICAL DEPRESSION; ANIMAL; BIOLOGICAL MODEL; BRAIN; C57BL MOUSE; COMPUTER SIMULATION; DEVICES; EQUIPMENT DESIGN; FLUORESCENCE IMAGING; INTRACELLULAR SPACE; METABOLISM; MICROFLUIDIC ANALYSIS; PHYSIOLOGY; TISSUE CULTURE TECHNIQUE;

ANIMALS; BRAIN; COMPUTER SIMULATION; CORTICAL SPREADING DEPRESSION; EQUIPMENT DESIGN; EXTRACELLULAR SPACE; INTRACELLULAR SPACE; MALE; MICE, INBRED C57BL; MICROFLUIDIC ANALYTICAL TECHNIQUES; MODELS, NEUROLOGICAL; OPTICAL IMAGING; POTASSIUM; TISSUE CULTURE TECHNIQUES;

EID: 84910127869     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00205.2014     Document Type: Article

References (54)

1. Aitken PG, Tombaugh GC, Turner DA, Somjen GG. Similar propagation of SD and hypoxic SD-like depolarization in rat hippocampus recorded optically and electrically. J Neurophysiol 80: 1514-1521, 1998.
2. Armstrong GA, Rodgers CI, Money TG, Robertson RM. Suppression of spreading depression-like events in locusts by inhibition of the NO/cGMP/PKG pathway. J Neurosci 29: 8225-8235, 2009.
3. Ayata C, Jin H, Kudo C, Dalkara T, Moskowitz MA. Suppression of cortical spreading depression in migraine prophylaxis. Ann Neurol 59: 652-661, 2006.
4. Baker PF. Recent experiments on the properties of the Na efflux from squid axons. J Gen Physiol 51: 172-179, 1968.
5. Binder DK, Papadopoulos MC, Haggie PM, Verkman AS. In vivo measurement of brain extracellular space diffusion by cortical surface photobleaching. J Neurosci 24: 8049-8056, 2004.
6. Bowyer SM, Aurora KS, Moran JE, Tepley N, Welch KM. Magnetoencephalographic fields from patients with spontaneous and induced migraine aura. Ann Neurol 50: 582-587, 2001.
7. Brennan KC, Romero Reyes M, López-Valdés HE, Arnold AP, Charles AC. Reduced threshold for cortical spreading depression in female mice. Ann Neurol 61: 603-606, 2007.
8. Cao Y, Welch KM, Aurora S, Vikingstad EM. Functional MRI-BOLD of visually triggered headache in patients with migraine. Arch Neurol 56: 548-554, 1999.
9. Charles AC, Brennan KC. Cortical spreading depression-new insights and persistent questions. Cephalalgia 29: 1115-1124, 2009.
10. Cordingley GE, Somjen GG. The clearing of excess potassium from extracellular space in spinal cord and cerebral cortex. Brain Res 151: 291-306, 1978.
11. Dahlem MA, Hadjikhani N. Migraine aura: retracting particle-like waves in weakly susceptible cortex. PLoS One 4: e5007, 2009.
12. Dahlem MA, Isele TM. Transient localized wave patterns and their application to migraine. J Math Neurosci 3: 7, 2013.
13. FitzHugh R. Mathematical models of threshold phenomena in the nerve membrane. Bull Math Biophys 17: 257-278, 1955.
14. Hadjikhani N, Sanchez Del Rio M, Wu O., Schwartz D, Bakker D, Fischl B, Kwong KK, Cutrer FM, Rosen BR, Tootell RB, Sorensen AG, Moskowitz MA. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci USA 98: 4687-4692, 2001.
15. Heinemann U, Lux HD, Gutnick MJ. Extracellular free calcium and potassium during paroxsmal activity in the cerebral cortex of the cat. Exp Brain Res 27: 237-243, 1977.
16. Heinemann U, Lux HD. Ceiling of stimulus induced rises in extracellular potassium concentration in the cerebral cortex of cat. Brain Res 120: 231-249, 1977.
17. Heinemann U. Excitatory amino acids and epilepsy-induced changes in extracellular space size. Adv Exp Med Biol 203: 449-460, 1986.
18. Helmchen F, Denk W. Deep tissue two-photon microscopy. Nat Methods 2: 932-940, 2005.
19. Holthoff K, Witte OW. Directed spatial potassium redistribution in rat neocortex. Glia 29: 288-292, 2000.
20. Knot HJ, Zimmermann PA, Nelson MT. Extracellular K(+)-induced hyperpolarizations and dilatations of rat coronary and cerebral arteries involve inward rectifier K(+) channels. J Physiol 492.2: 419-430, 1996.
21. Kofuji P, Newman EA. Potassium buffering in the central nervous system. Neuroscience 129: 1045-1056, 2004.
22. Kraig RP, Nicholson C. Extracellular ionic variations during spreading depression. Neuroscience 3: 1045-1059, 1978.
23. Largo C, Cuevas P, Somjen GG, Martin del Rio R., Herreras O. The effect of depressing glial function in rat brain in situ on ion synaptic transmission, and neuron survival. J Neurosci 16: 12219-1229, 1996.
24. Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ. 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, 2011.
25. Leão AA. The slow voltage variation of cortical spreading depression of activity. Electroencephalogr Clin Neurophysiol 3: 315-321, 1951.
26. MacAulay N, Zeuthen T. Glial K(+) clearance and cell swelling: key roles for cotransporters and pumps. Neurochem Res 37: 2299-2309, 2012.
27. Marshall WH, Hanna C, Barnard G. The relation of dehydration of the brain to the spreading depression of Leao. Electroencephalogr Clin Neurophysiol 2: 177-185, 1950.
28. Marshall WH. Spreading cortical depression of Leão. Physiol Rev 39: 239, 1959.
29. Matsuura T, Bureš J. The minimum volume of depolarized neural tissue required for triggering cortical spreading depression in rat. Exp Brain Res 12: 238-249, 1971.
30. Mountcastle VB. The columnar organization of the neocortex. Brain 120: 701-722, 1997.
31. Nicholson C, Tao L. Hindered diffusion of high molecular weight compounds in brain extracellular microenvironment measured with integrative optical imaging. Biophys J 65: 2277-2290, 1993.
32. Nicholson C. Ion-selective microelectrodes and diffusion measurements as tools to explore the brain cell microenvironment. J Neurosci Methods 48: 199-213, 1993.
33. Nimmerjahn A, Kirchhoff F, Kerr JND, Helmchen F. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods 1: 31-37, 2004.
34. Oheim M, Beaurepaire E, Chaigneau E, Mertz J, Charpak S. Two-photon microscopy in brain tissue: parameters influencing the imaging depth. J Neurosci Methods 111: 29-37, 2001.
35. Olesen J, Larsen B, Lauritzen M. Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine. Ann Neurol 9: 344-352, 1981.
36. Pologruto TA, Sabatini BL, Svoboda K. ScanImage: flexible software for operating laser scanning microscopes. Biomed Eng Online 2: 13, 2003.
37. Rodgers CI, Armstrong GAB, Shoemaker KL, LaBrie JD, Moyes CD, Robertson RM. Stress preconditioning of spreading depression in the locust CNS. PLoS One 2: e1366, 2007.
38. Russell MB, Olesen J. A nosographic analysis of the migraine aura in a general population. Brain 119: 355-361, 1996.
39. Somjen GG, Rosenthal M, Cordingley GE, LaManna J, Lothman E. Potassium, neuroglia, and oxidative metabolism in central gray matter. Fed Proc 35: 1266-1271, 1976.
40. Somjen GG. Extracellular potassium in the mammalian central nervous system. Ann Rev Physiol 41: 159-177, 1979.
41. Somjen GG. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 81: 1065-1096, 2001.
42. Syková E, Nicholson C. Diffusion in brain extracellular space. Physiol Rev 88: 1277-1340, 2008.
43. Taddeucci A, Martelli F, Barilli M, Ferrari M, Zaccanti G. Optical properties of brain tissue. J Biomed Optics 1: 117-123, 1996.
44. Tang YT, Kim J, López-Valdés HE, Brennan KC, Ju YS. Development and characterization of a microfluidic chamber incorporating fluid ports with active suction for localized chemical stimulation of brain slices. Lab Chip 11: 2247-2254, 2011.
45. Tsai PS, Kaufhold JP, Blinder P, Friedman B, Drew PJ, Karten HJ, Lyden PD, Kleinfeld D. Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of nuclei and vessels. J Neurosci 29: 14553-14570, 2009.
46. Világi I, Klapka N, Luhmann HJ. Optical recording of spreading depression in rat neocortical slices. Brain Res 898: 288-296, 2001.
47. Walz W, Hertz L. Ouabain-sensitive and ouabain-resistant net uptake of potassium into astrocytes and neurons in primary cultures. J Neurochem 39: 70-77, 1982.
48. Walz W. Chloride/anion channels in glial cell membranes. Glia 40: 1-10, 2002.
49. Woods RP, Iacoboni M, Mazziotta JC. Bilateral spreading cerebral hypoperfusion during spontaneous migraine headache. N Engl J Med 331: 1689-1692, 1994.
50. Woolsey TA, Rovainen CM, Cox SB, Henegar MH, Liang GE, Liu D, Moskalenko YE, Sui J, Wei L. Neuronal units linked to microvascular modules in cerebral cortex: response elements for imaging the brain. Cereb Cortex 6: 647-660, 1996.
51. Xiong Z, Stringer JL. Sodium pump activity, not glial spatial buffering, clears potassium after epileptiform activity induced in the dentate gyrus. J Neurophysiol 83: 1443-1451, 2000.
52. Yaroslavsky AN, Schulze PC, Yaroslavsky IV, Schober R, Ulrich F, Schwarzmaier HJ. Optical properties of selected native and coagulated human brain tissues in vitro in the visible and near infrared spectral range. Phys Med Biol 47: 2059-2073, 2002.
53. Young W. Spreading depression in elasmobranch cerebellum. Brain Res 199: 113-126, 1980.
54. Zador Z, Magzoub M, Jin S, Manley GT, Papadopoulos MC, Verkman AS. Microfiberoptic fluorescence photobleaching reveals size-dependent macromolecule diffusion in extracellular space deep in brain. FASEB J 22: 870-879, 2008.