Publication: Generation of Sustained Field Potentials by Gradients of Polarization Within Single Neurons: A Macroscopic Model of Spreading Depression
Loading...
Full text at PDC
Publication Date
2010-05
Advisors (or tutors)
Editors
Journal Title
Journal ISSN
Volume Title
Publisher
American Physiological Society
Citations
Exportar
Abstract
Makarova J, Makarova VA, Herreras O. Generation of sustained field potentials by gradients of polarization within single neurons: a macroscopic model of spreading depression. J Neurophysiol 103: 2446-2457, 2010. First published March 10, 2010; doi: 10.1152/jn.01045.2009. Spreading depression (SD) is a pathological wave of depolarization of the neural tissue producing a negative macroscopic field potential (V(o)), used as a marker for diagnostic purposes. The cellular basis of SD and neuronal mechanisms of generation of V(o) at the microscopic level are poorly understood. Using a CA1 mathematical model and experimental verification, we examined how transmembrane currents in single cells scale up in the extracellular space shaping V(o). The model includes an array of 17,000 realistically modeled neurons (responsible for generating transmembrane currents) dynamically coupled to a virtual aggregate/extracellular space (responsible for V(o)). The SD wave in different tissue bands is simulated by imposing membrane shunts in the corresponding dendritic elements as suggested by experimentally assessed drop in membrane resistance. We show that strong isopotential depolarization of wide domains (as in the main SD phase) produce broad central cancellation of axial and transmembrane currents in single cells. When depolarization is restricted to narrow dendritic domains (as in the late SD phase), the internal cancellation shrinks and the transmembrane current increases. This explains why in the laminated CA1 the V(o) is smaller in the main phase of SD, when both dendritic layers are seized, than in the SD tail restricted to an apical band. Moreover, scattering of the neuronal somatas (as in cortical regions) further decreases the aggregate V(o) due to the volume averaging. Although mechanistically the V(o) associated to SD is similar to customary transient fields, its changes maybe related to spatial factors in single cells rather than cell number or depolarization strength.
Description
UCM subjects
Unesco subjects
Keywords
Citation
Almeida AC, Texeira HZ, Duarte MA, Infantosi AF. Modeling extracellular space electrodiffusion during Leao’s spreading depression. IEEE Trans Biomed Eng 51: 450–458, 2004.
Bannister NJ, Larkman AU. Dendritic morphology of CA1 pyramidal neurons from the rat hippocampus. I. Branching patterns. J Comp Neurol 360: 150–160, 1995.
Boss BD, Turlejski K, Stanfield BB, Cowan WM. On the numbers of neurons in fields CA1 and CA3 of the hippocampus of Sprague-Dawley and Wistar rats. Brain Res 406: 280–287, 1987.
Bureš J, Burešová O, Krivánek J. The Mechanism and Application of Leão’s Spreading Depression of Electroencephalographic Activity. Prague: Academia, 1974.
Canals S, Makarova J, López-Aguado L, Largo C, Ibarz JM, Herreras O. Longitudinal depolarization gradients along the somatodendritic axis of CA1 pyramidal cells: a novel feature of spreading depression. J Neurophysiol 94: 943–951, 2005.
Czéh G, Aitken PG, Somjen GG. Membrane currents in CA1 pyramidal cells during spreading depression (SD) and SD-like hypoxic depolarization. Brain Res 632: 195–208, 1993.
Dahlem MA, Hadjikhani N. Migraine aura: retracting particle-like waves in weakly susceptible cortex. PLoS One 4: e5007, 2009.
Dietzel I, Heinemann U, Lux HD. Relations between slow extracellular potential changes, glial potassium buffering, and electrolyte and cellular volume changes during neuronal hyperactivity in cat brain. Glia 2: 25–44, 1989
do Carmo RJ, Martins-Ferreira H. Spreading depression of Leão probe with ion-selective microelectrodes in isolated chick retina. An Acad Brasil Sci 56: 401–421, 1984.
Fabricius M, Fuhr S, Bhatia R, Boutelle M, Hashemi P, Strong AJ, Lauritzen M. Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain 129: 778–790, 2006.
Grafstein B. Mechanism of spreading cortical depression. J Neurophysiol 19: 154–171, 1956.
Herreras O. Propagating dendritic action potential mediates synaptic transmission in CA1 pyramidal cells in situ. J Neurophysiol 64: 1429–1441, 1990.
Herreras O, Makarova J, Canals S, Ibarz JM. Subcellular mechanisms of spreading depression: from membrane channels to the DC voltage signal. In: Recent Advances and New Strategies in Stroke Research, edited by Erdõ F. Kerala. India: Transworld Research Network, 2008.
Herreras O, Somjen GG. Analysis of potentials shifts associated with recurrent spreading depression and prolonged unstable SD induced by microdialysis of elevated K in hippocampus of anesthetized rats. Brain Res 610: 283–294, 1993a.
Herreras O, Somjen GG. Propagation of spreading depression among dendrites and somata of the same cell population. Brain Res 610: 276–282, 1993b.
Ibarz JM, Makarova J, Herreras O. Relation of apical dendritic spikes to output decision in CA1 pyramidal cells during synchronous activation: a computational study. Eur J Neurosci 23: 1219–1233, 2006.
Iijima T, Mies G, Hossmann KA. Repeated negative DC deflections in rat cortex following middle cerebral artery occlusion are abolished by MK-801.Effect on volume of ischemic injury. J Cereb Blood Flow Metab 12: 727–733, 1992.
Jack JJB, Noble D, Tsien RW. Electric Current Flow in Excitable Cells. Oxford: University Press, 1975.
Kager H, Wadman WJ, Somjen GG. Simulated seizures and spreading depression in a neuron model incorporating interstitial space and ion concentrations. J Neurophysiol 84: 495–512, 2000.
Kager H, Wadman WJ, Somjen GG. Conditions for the triggering of spreading depression studied with computer simulations. J Neurophysiol 88: 2700–2712, 2002.
Kraig RP, Nicholson C. Extracellular ionic variations during spreading depression. Neuroscience 3: 1045–1059.
Leão AAP. Spreading depression of activity in the cerebral cortex. J Neurophysiol 7: 359–390, 1944.
Leão AAP. The slow voltage variation of cortical spreading depression of activity. Electroenceph Clin Neurophysiol 3: 315–321, 1951.
Largo C, Cuevas P, Somjen GG, Martín del Río R, Herreras O. The effect of depressing glial function on rat brain in situ on ion homeostasis, synaptic transmission and neuronal survival. J Neurosci 16: 1219–1229, 1996.
Largo C, Ibarz JM, Herreras O. Effects of the gliotoxin fluorocitrate on spreading depression and glial membrane potential in rat brain in situ. J Neurophysiol 78: 295–307, 1997.
López-Aguado L, Ibarz JM, Herreras O. Activity-dependent changes of tissue resistivity in the CA1 region in vivo are layer-specific: modulation of evoked potentials.Neuroscience 108: 249-262.
López-Aguado L, Ibarz JM, Varona P, Herreras O. Structural inhomogeneities differentially modulate action currents and population spikes initiated in the axon or dendrites. J Neurophysiol 88: 2809–2820, 2002.
Lorente de Nó R. Analysis of the distribution of action currents of nerves in volume conductors. In: A Study of Nerve Physiology. New York: Rockefeller Institute, 1947, part 2, vol. 132, p. 384–477.
Makarova J, Gómez-Galán M, Herreras O. Layer specific changes in tissue resistivity and spatial cancellation of transmembrane currents shape the voltage signal during spreading depression in the CA1 vivo. Eur J Neurosci 27: 444-456, 2008.
Makarova J, Ibarz JM, Canals S, Herreras O. A steady-state model of spreading depression predicts the importance of an unknown conductance in specific dendritic domains. Biophys J 92: 1–17, 2007.
Müller M. Effects of chloride transport inhibition and chloride substitution on neuron function and on hypoxic spreading-depressionlike depolarization in rat hippocampal slices. Neuroscience 97: 33–45, 2000.
Peters O, Schipke C, Hashimoto Y, Kettenmann H. Different mechanisms promote astrocyte Ca2 waves and spreading depression in the mouse neocortex. J Neurosci 23: 9888–9896, 2003.
Phillips JM, Nicholson C. Anion permeability in spreading depression investigated with ion-sensitive microelectrodes. Brain Res 173: 567–571, 1979.
Rall W, Shepherd GM. Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J Neurophysiol 31: 884–915, 1968.
Shapiro BE. Osmotic forces and gap junctions in spreading depression: a computational model. J Comput Neurosci 10: 99–120, 2001.
Somjen GG. Electrogenesis of sustained potentials. Prog Neurobiol 1: 199– 237, 1973.
Somjen GG. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 81: 1065–1096, 2001.
Somjen GG, Kager H, Wadman WJ. Calcium sensitive non-selective cation current promotes seizure-like discharges and spreading depression in a model neuron. J Comput Neurosci 26: 139–147, 2009.
Strong AJ, Anderson PJ, Watts HR, Virley DJ, Lloyd A, Irving EA, Nagafuji T, Ninomiya M, Nakamura H, Dunn AK, Graf R. Peri-infarct depolarizations lead to loss of perfusion in ischaemic gyrencephalic cerebral cortex. Brain 30: 995–1008, 2007.
Sugaya E, Takato M, Noda Y. Neuronal and glial activity during spreading depression in cerebral cortex of cat. J Neurophysiol 38: 822–841, 1975.
Tomita T. Spreading depression potential (SDP) in the frog retina. An Acad Brasil Ciênc 56: 505–518, 1984.
Trommald M, Jensen V, Andersen P. Analysis of dendritic spines in rat CA1 pyramidal cells intracellularly filled with a fluorescent dye. J Comp Neurol 353: 260–274, 1995.
Tuckwell HC, Miura RM. A mathematical model for spreading depression. Biophys J 23: 257–276, 1978.
Varona P, Ibarz JM, López-Aguado L, Herreras O. Macroscopic and subcellular factors shaping CA1 population spikes. J Neurophysiol 83: 2192–2208, 2000.
Wadman WJ, Juta AJA, Kamphuis W, Somjen GG. Current source density of sustained potential shifts associated with electrographic seizures and with spreading depression in rat hippocampus. Brain Res 570: 85–91, 1992