Cortical spreading depression in the gyrencephalic feline brain studied by magnetic resonance imaging

1 Time‐lapse diffusion‐weighted magnetic resonance imaging (DWI) was used to detect and characterize complex waves of cortical spreading depression (CSD) evoked with KCl placed upon the suprasylvian gyrus of anaesthetized cats. 2 The time‐lapse representations successfully demonstrated primary CSD waves that propagated with elliptical wavefronts selectively over the ipsilateral cerebral hemispheres with a velocity of 3.8 ± 0.70 mm min−1 (mean ± s.e.m. of 5 experiments). 3 In contrast, the succeeding secondary waves often remained within the originating gyrus, were slower (velocity 2.0 ± 0.18 mm min−1), more fragmented and varied in number. 4 Computed traces of the apparent diffusion coefficients (ADCs) showed negative deflections followed by monotonic decays (amplitudes: primary wave, ‐19.9 ± 2.8 %; subsequent waves, ‐13.6 ± 1.9 %; duration at half‐maximal decay, 150‐200 s) when determined from regions of interest (ROIs) through which both primary and succeeding CSD waves propagated. 5 The passage of both the primary and the succeeding waves often correlated with transient DC potential deflections recorded from the suprasylvian gyrus. 6 The detailed waveforms of the ADC and the T2*‐weighted (blood oxygenation level‐dependent: BOLD) traces showed a clear reciprocal correlation. These imaging features that reflect disturbances in cellular water balance agree closely with BOLD measurements that followed the propagation velocities of the first and subsequent CSD events. They also provide a close physiological correlate for clinical observations of cortical blood flow disturbances associated with human migraine.

[1]  E Sugaya,et al.  Neuronal and glial activity during spreading depression in cerebral cortex of cat. , 1975, Journal of neurophysiology.

[2]  G. Mies,et al.  Repeated Negative DC Deflections in Rat Cortex following Middle Cerebral Artery Occlusion are Abolished by MK-801: Effect on Volume of Ischemic Injury , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[3]  A Villringer,et al.  Systemic Nitric Oxide Synthase Inhibition Does Not Affect Brain Oxygenation during Cortical Spreading Depression in Rats: A Noninvasive Near-Infrared Spectroscopy and Laser-Doppler Flowmetry Study , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[4]  Risto A. Kauppinen,et al.  Quantitative assessment of blood flow, blood volume and blood oxygenation effects in functional magnetic resonance imaging , 1998, Nature Medicine.

[5]  A. A. Leão,et al.  SPREADING DEPRESSION OF ACTIVITY IN THE CEREBRAL CORTEX , 1944 .

[6]  M. Lauritzen,et al.  Regional cerebral blood flow during cortical spreading depression in rat brain: increased reactive hyperperfusion in low‐flow states , 1987, Acta neurologica Scandinavica.

[7]  J. Szerb Glutamate release and spreading depression in the fascia dentata in response to microdialysis with high K+: role of glia , 1991, Brain Research.

[8]  B. Rosen,et al.  Perfusion‐weighted imaging defects during spontaneous migrainous aura , 1998, Annals of neurology.

[9]  A. A. Parsons Recent advances in mechanisms of spreading depression. , 1998, Current opinion in neurology.

[10]  T P Obrenovitch,et al.  High extracellular potassium, and not extracellular glutamate, is required for the propagation of spreading depression. , 1995, Journal of neurophysiology.

[11]  R. S. Morison,et al.  PROPAGATION OF SPREADING CORTICAL DEPRESSION , 1945 .

[12]  M. Lauritzen,et al.  Cerebral blood flow in migraine and cortical spreading depression. , 1987, Acta neurologica Scandinavica. Supplementum.

[13]  S. Watanabe,et al.  A comparative study of membrane potential changes in neurons and neuroglial cells during spreading depression in the rabbit. , 1974, Brain research.

[14]  C. Giaume,et al.  Effects of General Anesthetics on Intercellular Communications Mediated by Gap Junctions between Astrocytes in Primary Culture , 1993, Anesthesiology.

[15]  C. Weiller,et al.  Brain stem activation in spontaneous human migraine attacks , 1995, Nature Medicine.

[16]  M. I. Smith,et al.  The dynamics of nitric oxide release measured directly and in real time following repeated waves of cortical spreading depression in the anaesthetised cat , 1997, Neuroscience Letters.

[17]  T. Olsen,et al.  Pathophysiology of the migraine aura: the spreading depression theory. , 1995, Brain : a journal of neurology.

[18]  R. Morison,et al.  PROPAGATION OF SPREADING CORTICAL DEPRESSION , 1945 .

[19]  K. Hossmann,et al.  Cortical Negative DC Deflections following Middle Cerebral Artery Occlusion and KCl-Induced Spreading Depression: Effect on Blood Flow, Tissue Oxygenation, and Electroencephalogram , 1994, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[20]  P. Milner Note on a possible correspondence between the scotomas of migraine and spreading depression of Leão. , 1958, Electroencephalography and clinical neurophysiology.

[21]  D. B. Tower,et al.  THE ACTIVITIES OF BUTYRYLCHOLINESTERASE AND CARBONIC ANHYDRASE, THE RATE OF ANAEROBIC GLYCOLYSTS, AND THE QUESTION OF A CONSTANT DENSITY OF GLIAL CELLS IN CEREBRAL CORTICES OF VARIOUS MAMMALIAN SPECIES FROM MOUSE TO WHALE , 1973, Journal of neurochemistry.

[22]  J. Urenjak,et al.  Intracerebral Microdialysis: Electrophysiological Evidence of a Critical Pitfall , 1995, Journal of neurochemistry.

[23]  G. Lambert,et al.  Inhalational Anesthetics Inhibit Spreading Depression: Relevance to Migraine , 1996, Cephalalgia : an international journal of headache.

[24]  I. Duncan,et al.  Induction of sodium channel clustering by oligodendrocytes , 1997, Nature.

[25]  P. Goadsby,et al.  Anti-migraine compounds fail to modulate the propagation of cortical spreading depression in the cat. , 1994, European neurology.

[26]  A. Lehmenkühler,et al.  Spreading depression can be restricted to distinct depths of the rat cerebral cortex , 1993, Neuroscience Letters.

[27]  P. Grafe,et al.  Ion activities and potassium uptake mechanisms of glial cells in guinea‐pig olfactory cortex slices. , 1987, The Journal of physiology.

[28]  S. Ochs,et al.  Apical dendrites and propagation of spreading depression in cerebral cortex. , 1960, Journal of neurophysiology.

[29]  B. Meldrum,et al.  The Use of In Vivo Fluorescence Image Sequences to Indicate the Occurrence and Propagation of Transient Focal Depolarizations in Cerebral Ischemia , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[30]  K. Hossmann,et al.  Imaging of the apparent diffusion coefficient for the evaluation of cerebral metabolic recovery after cardiac arrest. , 1995, Magnetic resonance imaging.

[31]  A. R. Gardner-Medwin,et al.  Journal of Cerebral Blood Flow and Metabolism Magnetic Resonance Imaging of Propagating Waves of Spreading Depression in the Anaesthetised Rat , 2022 .

[32]  Avraham Mayevsky,et al.  Cortical spreading depression recorded from the human brain using a multiparametric monitoring system , 1996, Brain Research.

[33]  N Tepley,et al.  Central neurogenic mechanisms of migraine , 1993, Neurology.

[34]  F. Pfrieger,et al.  Synaptic efficacy enhanced by glial cells in vitro. , 1997, Science.

[35]  M. Moskowitz,et al.  Cerebral Blood Flow Changes during Cortical Spreading Depression are Not Altered by Inhibition of Nitric Oxide Synthesis , 1994, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[36]  The meaning and significance of Leão's spreading depression. , 1984, Anais da Academia Brasileira de Ciencias.

[37]  K. Welch,et al.  Imaging the brain of migraine sufferers , 1997, Current opinion in neurology.

[38]  Lance Jw,et al.  Current concepts of migraine pathogenesis. , 1993 .

[39]  C. Sotak,et al.  Spreading waves of decreased diffusion coefficient lifter cortical stimulation in the rat brain , 1994, Magnetic resonance in medicine.

[40]  J. Lance,et al.  Current concepts of migraine pathogenesis , 1993, Neurology.

[41]  C. Beaulieu,et al.  Magnetic Resonance Imaging Assessment of Cerebral Hemodynamics during Spreading Depression in Rats , 1998, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[42]  W. Heiss,et al.  Halothane, but not α-chloralose, blocks potassium-evoked cortical spreading depression in cats , 1995, Brain Research.

[43]  M. Lauritzen Long-Lasting Reduction of Cortical Blood Flow of the Rat Brain after Spreading Depression with Preserved Autoregulation and Impaired CO2 Response , 1984, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[44]  M. Moskowitz,et al.  Neurovascular and molecular mechanisms in migraine headaches. , 1993, Cerebrovascular and brain metabolism reviews.

[45]  W. Heiss,et al.  Halothane, but not alpha-chloralose, blocks potassium-evoked cortical spreading depression in cats. , 1995, Brain research.

[46]  Helen D'Arceuil,et al.  MR Detection of Cortical Spreading Depression Immediately after Focal Ischemia in the Rat , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[47]  K. Lashley PATTERNS OF CEREBRAL INTEGRATION INDICATED BY THE SCOTOMAS OF MIGRAINE , 1941 .

[48]  W. H. Marshall,et al.  Spreading cortical depression of Leao. , 1959, Physiological reviews.

[49]  L. Hertz Features of Astrocytic Function Apparently Involved in the Response of Central Nervous Tissue to Ischemia-Hypoxia , 1981, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[50]  M. Nedergaard,et al.  Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. , 1994, Science.

[51]  T. A. Carpenter,et al.  Optimised diffusion-weighting for measurement of apparent diffusion coefficient (ADC) in human brain. , 1997, Magnetic resonance imaging.

[52]  K. Hossmann,et al.  Periinfarct depolarizations. , 1996, Cerebrovascular and brain metabolism reviews.

[53]  L. L. Yuan,et al.  A glial-neuronal signaling pathway revealed by mutations in a neurexin-related protein. , 1999, Science.

[54]  Christopher H. Sotak,et al.  Spreading Waves of a Reduced Diffusion Coefficient of Water in Normal and Ischemic Rat Brain , 1995, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.