Two-dimensional wave patterns of spreading depolarization: retracting, re-entrant, and stationary waves ✩

Abstract We present spatio-temporal characteristics of spreading depolarizations (SD) in two experimental systems: retracting SD wave segments observed with intrinsic optical signals in chicken retina, and spontaneously occurring re-entrant SD waves that repeatedly spread across gyrencephalic feline cortex observed by laser speckle flowmetry. A mathematical framework of reaction–diffusion systems with augmented transmission capabilities is developed to explain the emergence and transitions between these patterns. Our prediction is that the observed patterns are reaction–diffusion patterns controlled and modulated by weak nonlocal coupling such as long-range, time-delayed, and global coupling. The described spatio-temporal characteristics of SD are of important clinical relevance under conditions of migraine and stroke. In stroke, the emergence of re-entrant SD waves is believed to worsen outcome. In migraine, retracting SD wave segments cause neurological symptoms and transitions to stationary SD wave patterns may cause persistent symptoms without evidence from noninvasive imaging of infarction.

[1]  Eugene M. Izhikevich,et al.  Neural excitability, Spiking and bursting , 2000, Int. J. Bifurc. Chaos.

[2]  M. Dahlem,et al.  ECoG-based short-range recurrent stimulation techniques to stabilize tissue at risk of progressive damage: Theory based on clinical observations , 2009 .

[3]  S. Yoshizawa,et al.  An Active Pulse Transmission Line Simulating Nerve Axon , 1962, Proceedings of the IRE.

[4]  D. Lübbers,et al.  Regulation of microflow and behaviour of local tissue Po2 during activation and anoxia of the brain cortex. , 1977, Bibliotheca anatomica.

[5]  Markus A. Dahlem,et al.  Migraine aura dynamics after reverse retinotopic mapping of weak excitation waves in the primary visual cortex , 2003, Biological Cybernetics.

[6]  D. Attwell,et al.  Bidirectional control of CNS capillary diameter by pericytes , 2006, Nature.

[7]  B. Rosen,et al.  Mechanisms of migraine aura revealed by functional MRI in human visual cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Oscar Herreras,et al.  A steady-state model of spreading depression predicts the importance of an unknown conductance in specific dendritic domains. , 2007, Biophysical journal.

[9]  Eckehard Schöll,et al.  Nonlinear Spatio-Temporal Dynamics and Chaos in Semiconductors , 2001 .

[10]  J. Olesen,et al.  Ischaemia-induced (symptomatic) migraine attacks may be more frequent than migraine-induced ischaemic insults. , 1993, Brain : a journal of neurology.

[11]  M. Lauritzen,et al.  Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. , 2006, Brain : a journal of neurology.

[12]  O. Sakowitz,et al.  Spreading depolarizations occur in human ischemic stroke with high incidence , 2008, Annals of neurology.

[13]  H. Wilson Spikes, Decisions, and Actions: The Dynamical Foundations of Neuroscience , 1999 .

[14]  G. Somjen,et al.  Simulated seizures and spreading depression in a neuron model incorporating interstitial space and ion concentrations. , 2000, Journal of neurophysiology.

[15]  M. Moskowitz Defining a Pathway to Discovery from Bench to Bedside: The Trigeminovascular System and Sensitization , 2008, Headache.

[16]  K. Fuxe,et al.  Intercellular communication in the brain: Wiring versus volume transmission , 1995, Neuroscience.

[17]  M. Moskowitz The 2006 Thomas Willis lecture: the adventures of a translational researcher in stroke and migraine. , 2007, Stroke.

[18]  Kenneth Showalter,et al.  Feedback stabilization of unstable propagating waves. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[19]  Kevin Barraclough,et al.  I and i , 2001, BMJ : British Medical Journal.

[20]  D. Scheller,et al.  Dose‐dependent effects of tetraethylammonium on circling spreading depressions in chicken retina , 1998, Journal of neuroscience research.

[21]  S. Silberstein Atlas of Migraine and Other Headaches , 2005 .

[22]  Karma Universal limit of spiral wave propagation in excitable media. , 1991, Physical review letters.

[23]  K. Bonhoeffer ACTIVATION OF PASSIVE IRON AS A MODEL FOR THE EXCITATION OF NERVE , 1948, The Journal of general physiology.

[24]  E. Schöll,et al.  Two-dimensional spatiotemporal pattern formation in the double barrier resonant tunnelling diode , 2007 .

[25]  G. Houston,et al.  Cortical spreading depression in the gyrencephalic feline brain studied by magnetic resonance imaging , 1999, The Journal of physiology.

[26]  E Schöll,et al.  Efficient control of transient wave forms to prevent spreading depolarizations. , 2007, Journal of theoretical biology.

[27]  Eckehard Schöll,et al.  Controlling the onset of traveling pulses in excitable media by nonlocal spatial coupling and time-delayed feedback. , 2008, Chaos.

[28]  R. FitzHugh Impulses and Physiological States in Theoretical Models of Nerve Membrane. , 1961, Biophysical journal.

[29]  Bruce E. Shapiro,et al.  Osmotic Forces and Gap Junctions in Spreading Depression: A Computational Model , 2004, Journal of Computational Neuroscience.

[30]  J A Reggia,et al.  Modeling cortical spreading depression. , 1994, Proceedings. Symposium on Computer Applications in Medical Care.

[31]  M. Nitsche,et al.  After-effects of transcranial direct current stimulation (tDCS) on cortical spreading depression , 2006, Neuroscience Letters.

[32]  Markus Dahlem,et al.  Reaction‐diffusion waves in neuronal tissue and the window of cortical excitability , 2004 .

[33]  A. Karma,et al.  Theory of spiral wave dynamics in weakly excitable media: asymptotic reduction to a kinematic model and applications. , 1999, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[34]  Robert F. Miller Cell communication mechanisms in the vertebrate retina the proctor lecture. , 2008, Investigative ophthalmology & visual science.

[35]  I. Nakano,et al.  Topographical analysis of cortical neuronal loss associated with disseminated selective neuronal necrosis and infarction after repeated ischemia , 1997, Brain Research.

[36]  Johan Grasman,et al.  Relaxation Oscillations , 2009, Encyclopedia of Complexity and Systems Science.

[37]  G. Somjen Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. , 2001, Physiological reviews.

[38]  N. Hadjikhani,et al.  Migraine Aura and Related Phenomena: Beyond Scotomata and Scintillations , 2007, Cephalalgia : an international journal of headache.

[39]  M. Lauritzen,et al.  Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. , 2006, Brain : a journal of neurology.

[40]  Balth. van der Pol Jun. LXXXVIII. On “relaxation-oscillations” , 1926 .

[41]  C. Rebert Spreading depression in squirrel monkey lissencephalic cortex. , 1970, Physiology & behavior.

[42]  J. Cowan,et al.  A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue , 1973, Kybernetik.

[43]  J A Reggia,et al.  Spreading Depression in Focal Ischemia: A Computational Study , 1998, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[44]  W. Hanke,et al.  Pharmacological modulation of the refractory period of retinal spreading depression , 1998, Naunyn-Schmiedeberg's Archives of Pharmacology.

[45]  Erik Glatt,et al.  Variability-sustained pattern formation in subexcitable media. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[46]  Kenneth Showalter,et al.  Design and Control of Wave Propagation Patterns in Excitable Media , 2002, Science.

[47]  Erik Glatt,et al.  Variability-induced transition in a net of neural elements: From oscillatory to excitable behavior. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[48]  Nouchine Hadjikhani,et al.  Migraine Aura: Retracting Particle-Like Waves in Weakly Susceptible Cortex , 2008, PloS one.

[49]  H C Tuckwell,et al.  Simplified reaction-diffusion equations for potassium and calcium ion concentrations during spreading cortical depression. , 1981, The International journal of neuroscience.

[50]  F. Wilkinson Auras and other hallucinations: windows on the visual brain. , 2004, Progress in Brain Research.

[51]  M A Dahlem,et al.  Image processing techniques applied to excitation waves in the chicken retina. , 2000, Methods.

[52]  M. Lauritzen,et al.  Spreading and Synchronous Depressions of Cortical Activity in Acutely Injured Human Brain , 2002, Stroke.

[53]  A. Winfree Varieties of spiral wave behavior: An experimentalist's approach to the theory of excitable media. , 1991, Chaos.

[54]  A. Dunn,et al.  Peri-infarct depolarizations lead to loss of perfusion in ischaemic gyrencephalic cerebral cortex. , 2006, Brain : a journal of neurology.

[55]  A J Shepherd,et al.  Increased visual after-effects following pattern adaptation in migraine: a lack of intracortical excitation? , 2001, Brain : a journal of neurology.

[56]  J A Reggia,et al.  A computational model of visual hallucinations in migraine , 1996, Comput. Biol. Medicine.

[57]  H. Schuster,et al.  Nonlinear dynamics of nanosystems , 2010 .

[58]  D. Dodick,et al.  Why migraines strike. , 2008, Scientific American.

[59]  M. Moskowitz,et al.  Dynamic Imaging of Cerebral Blood Flow Using Laser Speckle , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[60]  Balth van der Pol Jun Docts. Sc.,et al.  LXXII. The heartbeat considered as a relaxation oscillation, and an electrical model of the heart , 1928 .

[61]  W. Hanke,et al.  Correlation of the electrical and intrinsic optical signals in the chicken spreading depression phenomenon , 2001, Neuroscience Letters.

[62]  Mikhailov,et al.  Bifurcation to traveling spots in reaction-diffusion systems. , 1994, Physical review letters.

[63]  J. Mcculloch,et al.  Comparison of the effects of potassium and pH on the calibre of cerebral veins and arteries , 1982, Pflügers Archiv.

[64]  M. Dahlem,et al.  Self-induced splitting of spiral-shaped spreading depression waves in chicken retina , 1997, Experimental Brain Research.

[65]  W. Hanke,et al.  Effects of antimigraine drugs on retinal spreading depression , 1996, Naunyn-Schmiedeberg's Archives of Pharmacology.

[66]  Eckehard Schöll,et al.  Failure of feedback as a putative common mechanism of spreading depolarizations in migraine and stroke. , 2008, Chaos.

[67]  M. Dahlem,et al.  A computational perspective on migraine aura , 2004, Progress in Neurobiology.

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

[69]  J Bures,et al.  Reverberation of cortical spreading depression along closed-loop pathways in rat cerebral cortex. , 1972, Journal of neurophysiology.

[70]  K. Hossmann Pathophysiology and Therapy of Experimental Stroke , 2006, Cellular and Molecular Neurobiology.

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

[72]  C. Nicholson,et al.  Diffusion in brain extracellular space. , 2008, Physiological reviews.

[73]  M. Lauritzen Cortical spreading depression as a putative migraine mechanism , 1987, Trends in Neurosciences.