Cortical spreading depression in the feline brain following sustained and transient stimuli studied using diffusion-weighted imaging

Journal of Physiology

Volumn 544, Issue 1, 2002, Pages 39-56

  Bradley, Daniel P ^a   Smith, Justin M ^a,e   Smith, Martin I ^b   Bockhorst, Kurt H J ^a,d   Papadakis, Nikolas G ^a,f   Hall, Laurance D ^a   Parsons, Andrew A ^b   James, Michael F ^b   Huang, Christopher L H ^a,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b GLAXOSMITHKLINE   (United Kingdom)

^c PHYSIOLOGICAL LABORATORY   (United Kingdom)

^d UNIVERSITY OF BREMEN   (Germany)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f NORTHERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHLORIDE;

ANIMAL TISSUE; BRAIN CORTEX; BRAIN DEPTH STIMULATION; BRAIN MAPPING; CAT; CONTROLLED STUDY; DIFFUSION COEFFICIENT; DIFFUSION WEIGHTED IMAGING; HEMISPHERE; NERVE CONDUCTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVIEW; SPREADING CORTICAL DEPRESSION; SUPRASYLVIAN GYRUS; AMPLITUDE MODULATION; ANIMAL EXPERIMENT; APPARENT DIFFUSION COEFFICIENT; ARTICLE; CAT BREED; FEMALE; IMAGE ANALYSIS; IMAGE QUALITY; NEUROIMAGING; RADIOLOGICAL PARAMETERS; SIGNAL NOISE RATIO; STIMULUS; SUSTAINED STIMULUS; SYLVIAN FISSURE; TRANSIENT STIMULUS;

ANIMALS; BRAIN MAPPING; CATS; CEREBRAL CORTEX; DIFFUSION MAGNETIC RESONANCE IMAGING; DRUG ADMINISTRATION SCHEDULE; FEMALE; POTASSIUM CHLORIDE; REACTION TIME; SPREADING CORTICAL DEPRESSION;

EID: 0036794283     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2002.025353     Document Type: Review

References (74)

1. ATKINS, P. W. (1983). Physical Chemistry. Oxford University Press, Oxford.
2. AURORA, S. K., CAO, Y., BOWYER, S. M. & WELCH, K. M. (1999). The occipital cortex is hyperexcitable in migraine: Experimental evidence. Headache 39, 469-476.
3. BASARSKY, T. A., FEIGHAN, D. & MACVICAR, B. A. (1999). Glutamate release through volume-activated channels during spreading depression. Journal of Neuroscicnce 19, 6439-6445.
4. BILLUPS, B., ROSSI, D., OSHIMA, T., WARR, O., TAKAHASHI, M., SARANTIS, M., SZATKOWSKI, M. & ATTWELL, D. (1998). Physiological and pathological operation of glutamate transporters. In Glutamate Synapse as a Therapeutical Target. Molecular Organization and Pathology of the Glutamate Synapse, vol. 116, pp. 45-47.
5. BOCKHORST, K. H. J., SMITH, J. M., SMITH, M. I., BRADLEY, D. P., HOUSTON, G. C., CARPENTER, T. A., HALL, L. D., PAPADAKIS, N. G., PARSONS, A. A., HUANG, C. L.-H. & JAMES, M. F. (2000). A quantitative analysis of cortical spreading depression events in the feline brain characterized with diffusion weighted MRI. Journal of Magnetic Resonance Imaging 12, 722-733.
6. BOWYER, S. M., OKADA, Y. C., PAPUASHVILI, N., MORAN, J. E., BARKLEY, G. L., WELCH, K. M. A. & TEPLEY, N. (1999a). Analysis of MEG signals of spreading cortical depression with propagation constrained to a rectangular cortical strip I. Lissencephalic rabbit model. Brain Research 843, 71-78.
7. BOWYER, S. M., TEPLEY, N., PATUASHVILI, N., KATO, S., BARKLEY, G. L., WELCH, K. M. A. & OKADA, Y. C. (1999b). Analysis of MEG signals of spreading cortical depression with propagation constrained to a rectangular cortical strip II. Gyrencephalic swine model. Brain Research 843, 79-86.
8. BUREŠ J., BUREŠOVÁ, O. & KŘIVǍNEK, J. (1974). The Mechanisms and Applications of Leão's Spreading Depression of Electroencephalograph ic Activity. Academia, Prague.
9. BUREŠ J., BUREŠOVÁ, O. & KŘIVÁNEK, J. (1984). The meaning and significance of Leão's SD. Annals of the Acadcmy of Brazilian Science 56, 385-400.
10. CAO, Y., WELCH, K. M. A., AURORA, S. & VIKINGSTAD, E. M. (1999). Functional MRI-BOLD of visually triggered headache in patients with migraine. Archives of Neurology 56, 548-554.
11. DE CRESPIGNY, A., RÖTHER, J., VAN BRUGGEN, N., BEAULIEU, C. & MOSELY, M. E. (1996). Simultaneous measurement of diffusion, perfusion and direct current potential during cortical spreading depression. In Fourth Scientific Meeting of the International Society of Magnetic Resonance in Medicine, p. 315. John Wiley, New York.
12. DE CRESPIGNY, A., RÖTHER, J., VAN BRUGGEN, N., BEAULIEU, C. & MOSELEY, M. E. (1998). Magnetic resonance imaging assessment of cerebral hemodynamics during spreading depression in rats. Journal of Cerebral Blood Flow and Metabolism 18, 1008-1017.
13. 19F NMR. Magnetic Resonance in Medicine 40, 1-13.
14. EBERSBERGER, A., SCHAIBLE, H. G., AVERBECK, B. & RICHTER, F. (2001). Is there a correlation between spreading depression, neurogenic inflammation, and nociception that might cause migraine headache? Annals of Neurology 49, 7-13.
15. FABRICIUS, M., JENSEN, L. H. & LAURITZEN, M. (1993). Microdialysis of interstitial amino acids during spreading depression and anoxic depolarisation in rat neocortex. Brain Research 612, 61-69.
16. FROES, M. M. & CAMPOS DE CAVALHO, A. C. (1998). Gap junction-mediated loops of neuronal-glial interactions. Glia 24, 97-107.
17. GARDNER-MEDWIN, A. R. (1983). Analysis of potassium dynamics in mammalian brain tissue. Journal of Physiology 335, 393-426.
18. GARDNER-MEDWIN, A. R., VAN BRUGGEN, N., WILLIAMS, S. R. & AHIER, R. G. (1994). Magnetic resonance imaging of propagating waves of spreading depression in the anaesthetised rat. Journal of Cerebral Blood Flow and Metabolism 14, 7-11.
19. GORJI, A. (2001). Spreading depression: a review of the clinical relevance. Brain Research Reviews 38, 33-60.
20. GORJI, A., SCHELLER, D., STRAUB, H., TEGTMEIER, F., KOHLING, R., HOHLING, J. M., TUXHORN, I., EBNER, A., WOLF, P., PANNECK, H. W., OPPEL, F. & SPECKMANN, E. J. (2001). Spreading depression in human neocortical slices. Brain Research 906, 74-83.
21. GORRY, P. A. (1990). General least-squares smoothing and differentiation by the convolution (Savitzky-Golay) method. Analytical Chemistry 62, 570-573.
22. GRAFSTEIN, B. (1956). Mechanisms of spreading depression. Journal of Neurophysiology 19, 154-171.
23. HADJIKHANI, N., DEL RIO, M. S., WU, O., SCHWARTZ, D., BAKKER, D., FISCHL, B., KWONG, K. K., CUTRER, F. M., ROSEN, B. R., TOOTELL, R. B. H., SORENSEN, A. G. & MOSKOWITZ, M. A. (2001). Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proceedings of the National Academy of Sciences of the USA 98, 4687-4692.
24. HARDEBO, J. (1991). On pain mechanisms in cluster headache. Headache 31, 91-106.
25. HERRERAS, H. & SOMJEN, G. G. (1993). Effects of prolonged elevation of potassium on hippocampus of anaesthetised rats. Brain Research 617, 194-204.
26. HOSSMAN, K. A. (1996). Peri-infarct Depolarisations. Brain Metabolism Reviews 727,195-208.
27. IADECOLA, C. & KRAIG, R. P. (1991). Focal elevations in neocortical interstitial potassium produced by stimulation of the fastigial nucleus in rat. Brain Research 563, 273-277.
28. JAMES, M. F., SMITH, M. L, BOCKHORST, K. H. J., HALF, L. D., HOUSTON, G. C., PAPADAKIS, N. G., SMITH, J. M., WILLIAMS, E. J., XING, D., PARSONS, A. A., HUANG, C. L.-H. & CARPENTER, T. A. (1999). Cortical spreading depression in the gyrencephalic feline brain studied by magnetic resonance imaging. Journal of Physiology 519, 415-425.
29. KAUBE, K. & GOADSBY, P. J. (1994). Anti-migraine compounds fail to modulate the propagation of cortical spreading depression in the cat. European Neurology 34, 30-35.
30. KITAHARA, Y., TAGA, K., ABE, H. & SHIMOJI, K. (2001). The effects of anesthetics on cortical spreading depression elicitation and c-fos expression in rats. Journal of Neurosurgical Anesthesiology 13, 26-32.
31. KRUGER, H., LUHMANN, H. J. & HEINEMANN, U. (1996). Repetitive spreading depression causes selective suppression of GABAergic function. NeuroReport 7, 2733-2736.
32. KUGE, Y., HASEGAWA, Y., YOKOTA, C., MINEMATSU, K., HASHIMOTO, N., MIYAKE, Y. & YAMAGUCHI, T. (2000). Effects of single and repetitive spreading depression on cerebral blood flow and glucose metabolism in cats: a PET study. Journal of Neurological Sciences 176, 114-123.
33. LAMBERT, G. A., MICHALICEK, J., STORER, R. J. & ZAGAMI, A. S. (1999). Effect of cortical spreading depression on activity of trigeminovascular sensory neurons. Cephalalgia 19, 631-638.
34. LARGO, C., CUEVAS, P., SOMJEN, G. G., DELRIO, R. M. & HERRERAS, O. (1996). The effect of depressing glial function in rat brain in situ on ion homeostasis, synaptic transmission, and neuron survival. Journal of Neuroscience 16, 1219-1229.
35. LARGO, C., TOMBAUGH, G. C., AITKEN, P. G., HERRERAS, O. & SOMJEN, G. G. (1997). Heptanol but not fluoroacetate prevents the propagation of spreading depression in rat hippocampal slices. Journal of Neurophysiology 77, 9-16.
36. LASHLEY, K. S. (1941). Patterns of cerebral integration indicated by the scotomas of migraine. Archives of Neurology and Psychiatry 46, 331-339.
37. LAURITZEN, M. (1994). Pathophysiology of migraine aura: The spreading depression theory. Brain 117, 199-210.
38. LEÃO, A. A. P. (1944). Spreading depression activity in the cerebral cortex. Journal of Neurophysiology 7, 359-390.
39. LEÃO, A. A. P. (1947). Further observations on the spreading depression of activity in the cerebral cortex. Journal of Neurophysiology 10, 409-414.
40. LEÃO, A. A. P. & MORRISON, R. S. (1945). Propagation of spreading cortical depression. Journal of Neurophysiology 8, 33-45.
41. LEHMANKÜHLER, A. & RICHTER, F. (1993). Spreading depression in upper and lower depths of the rat cerebral cortex and its possible implications on the type of human migraine. In Migraine: Basic Mechanisms and Treatment, ed. LEHMANKÜHLER, A., GROTEMEYER, K.-H. & TEGTMEIER, F., pp. 267-278. Urban & Schwarzberg, Munich, Vienna, Baltimore.
42. MANTZ, J., CORDIER, J. & GIAUME, C. (1993). Effects of general anaesthetics on intercellular communications mediated by gap-junctions between astrocytes in primary culture. Anesthesiology 78, 892-901.
43. MARSHALL, W. H. (1959). Spreading cortical depression of Leão. Physiological Reviews 39, 239-279.
44. MARTINS-FERREIRA, H. & DO CARMO, R. J. (1987). Retinal spreading depression and the extracellular milieu. Canadian Journal of Physiology and Pharmacology 65, 1092-1098.
45. MAYEVSKY, A., DORON, A., MANOR, T., MELLEN, S., ZARCHIN, N. & OUAKNINE, G. E. (1996). Cortical spreading depression recorded from the human brain using a multiparametric monitoring system. Brain Research 740, 268-274.
46. MENNA, G., TONG, C. K. & CHESLER, M. (2000). Extracellular pH changes and accompanying cation shifts during ouabain-induced spreading depression. Journal of Neurophysiology 83, 1338-1345.
47. MILNER, P. M. (1958). Note on a possible correspondence between the scotomas of migraine and spreading depression of Leão. Electroencephalography and Clinical Neurophysiology 10, 705.
48. MOSKOWITZ, M. A. & MACFARLANE, R. (1993). Neurovascular and molecular mechanisms in migraine headaches. Cerebrovasculature and Brain Metabolism Review 5, 159-177.
49. NALLET, H., MacKENZIE, E. T. & ROUSSEL, S. (1999). The nature of penumbral depolarizations following focal cerebral ischemia in the rat. Brain Research 842, 148-158.
50. NEDERGAARD, M. & HANSEN, A. J. (1988). Spreading depression is not associated with neuronal injury in the normal brain. Brain Research 449, 395-398.
51. NICHOLSON, C. & KRAIG, R. P. (1981). The behaviour of extracellular ions during spreading depression. In The Application of Ion Selective Microelectrodes, ed. ZEUTHEN, T., pp. 217-238. Elsevier/North Holland Biomedical Press, Amsterdam.
52. NICHOLSON, C. & SYKOVt́iA, E. (1998). Extracellular space analysis revealed by diffusion analysis. Trends in Neurosciences 21, 207-215.
53. 2+ levels following cortical compression contusion trauma in rats. Journal of Cerebral Blood Flow and Metabolism 13, 183-192.
54. OBRENOVITCH, T. P. & ZILKHA, E. (1995). High extracellular potassium, and not extracellular glutamate, is required for the propagation of spreading depression. Journal of Neurophysiology 73, 2107-2114.
55. OCHS, S. (1962). The nature of spreading depression in neural networks. International Reviews in Neurobiology 4, 1-69.
56. PAPE, L. G. & KATZMAN, R. (1972). Responses of glia in cat sensorimotor cortex to increased extracellular potassium. Brain Research 38, 71-92.
57. + from astrocyte endfeet regulate cerebral blood flow? Science 237, 896-898.
58. PIPER, R. D. & LAMBERT, G. A. (1996). Inhalational anesthetics inhibit spreading depression: relevance to migraine. Cephalalgia 16, 87-92.
59. PIPER, R. D., LAMBERT, G. A. & DUCKWORTH, J. W. (1991). Cortical blood flow changes during spreading depression in cats. American Journal of Physiology 261, H96-102.
60. READ, S. J., SMITH, M. L, CHAN, W. N., THOMPSON, M., HUNTER, A. J., PARSONS, A. A. & UPTON, N. (1999). SB-220453 Inhibits cortical spreading depression in the anaesthetised cat. Neurology 52, A275.
61. REID, K. H., MARRANNES, R. & WAUQUIER, A. (1988). Spreading depression and central nervous-system pharmacology. Journal of Pharmacological Methods 19, 1-21.
62. RÖTHER, J., DECRESPIGNY, A. J., D'ARCEUIL, H. & MOSELEY, M. E. (1996). MR detection of cortical spreading depression immediately after focal ischemia in the rat. Journal of Cerebral Blood Flow and Metabolism 16, 214-220.
63. SAITO, R., GRAF, R., HUBEL, K., TAGUCHI, J., ROSNER, G., FUJITA, T. & HEISS, W.-D. (1995). Halothane, but not alpha-chloralose, blocks potassium-evoked cortical spreading depression in cats. Brain Research 699, 109-115.
64. SMITH, M. I., READ, S. J., CHAN, W. N., THOMPSON, M., HUNTER, A. J., UPTON, N. & PARSONS, A. A. (2000). Repetitive cortical spreading depression in a gyrencephalic feline brain: inhibition by the novel benzoylamino-benzopyran SB-220453. Cephalalgia 20, 546-553.
65. SOMJEN, G. G. (2001). Mechanisms of spreading depression and hypoxic spreading depression-like depolarisation. Physiological Reviews 81, 1065-1096.
66. SYKOVǍ, E. (1992). Ionic and Volume Changes in the Microenvironment of Nerve and Receptor Cells. Springer-Verlag, New York.
67. SYKOVǍ, E. (1997). The extracellular space in the CNS: its regulation, volume and geometry in normal and pathological neuronal function. Neuroscientist 3, 28-41.
68. SYKOVÁ, E., MAZEL, T., VARGOVÁ, L., VOŘIŠEK, I. & PROKOPOVÁ, Š. (2000). Extracellular space diffusion and pathological states. Volume Transmission Revisited. Progress in Brain Research 125, 155-178.
69. SZATKOWSKI, M., BARBOUR, B. & ATTWELL, D. (1990). Non-vesicular release of glutamate from glial-cells by reversed electrogenic glutamate uptake. Nature 348, 443-446.
70. +- role of glia. Brain Research 542, 259-265.
71. TOWER, D. B. & YOUNG, O. M. (1973). The activities of butyrylcholinesterase and carbonic anhydrase, the rate of anaerobic glycolysis, and the question of a constant density of glial cells in cerebral cortices of various mammalian species from mouse to whale. Journal of Neurochemistry 20, 269-278.
72. WALZ, W. (2000). Role of astrocytes in the clearance of excess extracellular potassium. Neurochemistry International 36, 291-300.
73. XING, D., PAPADAKIS, N. G., HUANG, C.-L. H., LEE, V. M., CARPENTER, T. A. & HALL, L. D. (1997). Optimised diffusion-weighting for measurement of apparent diffusion coefficient (ADC) in human brain. Magnetic Resonance Imaging 15, 771-784.
74. ZAHS, K. R. (1998). Heterotypic coupling between glial cells of the mammalian central nervous system. Glia 24, 84-96.