Propagation of spreading depression among dendrites and somata of the same cell population

The propagation of sustained potential shifts associated with spreading depression (SD) was studied by microelectrodes placed in diverse layers at different locations in hippocampus of anesthetized rats. SD was induced by raising interstitial potassium concentration ([K+]0) focally in the CA1 region of the dorsal hippocampus either by microdialysis or by microinjection. Recurrent waves of SD propagated from the dialysis site throughout the hippocampus. Potential shifts (delta V0) associated with SD usually began earlier and were always of larger amplitude and longer duration in stratum (st.) radiatum (layer of apical dendrites) than in st. pyramidale (layer of pyramidal cell somata). The velocity of propagation in the two layers differed and varied independently one from the other. When SD was provoked by orthodromic train stimuli, the apparent direction of propagation in st. pyramidale was opposite that in st. radiatum. Microinjection of high K+ solution was more likely to provoke SD when placed in the st. radiatum, 50-100 microns ventral to st. pyramidale, than in other cytoarchitectonic layers. In about half the trials after 30 to 90 min of high K+ dialysis, a prolonged depressed state developed during which the potential in st. radiatum shifted at irregular intervals between near-rest level and a strongly negative level, while delta V0 shifts in st. pyramidale were smaller and more irregular in amplitude. This state is termed prolonged unstable SD". When the NMDA receptor antagonist CPP was dialyzed together with high K+, the onset of SD was postponed and delta V0 waves propagated in st. pyramidale without corresponding waves in st. radiatum; less frequently the other way around.(ABSTRACT TRUNCATED AT 250 WORDS)

[1]  O Herreras,et al.  Mechanism of spreading depression: a review of recent findings and a hypothesis. , 1992, Canadian journal of physiology and pharmacology.

[2]  O. Herreras,et al.  Synaptic transmission at the Schaffer-CA1 synapse is blocked by 6,7-dinitro-quinoxaline-2,3-dione. An in vivo brain dialysis study in the rat , 1989, Neuroscience Letters.

[3]  P. Schwartzkroin,et al.  Role of Na-K pump potassium regulation and IPSPs in seizures and spreading depression in immature rabbit hippocampal slices. , 1990, Journal of neurophysiology.

[4]  S. Goldring,et al.  Intracellular potentials from "idle" cells in cerebral cortex of cat. , 1966, Electroencephalography and clinical neurophysiology.

[5]  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.

[6]  G. Somjen,et al.  Prolonged Unstable Depression: A Modified Manifestation of Spreading Depression in Rat Hippocampus , 1993 .

[7]  L. Leung Orthodromic activation of hippocampal CA1 region of the rat , 1979, Brain Research.

[8]  C. Nicholson,et al.  Extracellular ionic variations during spreading depression , 1978, Neuroscience.

[9]  P. Aitken,et al.  The ionic and metabolic responses associated with neuronal depression of Leão's type in cerebral cortex and in hippocampal formation. , 1984, Anais da Academia Brasileira de Ciencias.

[10]  G. Somjen,et al.  Ion channel involvement in hypoxia-induced spreading depression in hippocampal slices , 1991, Brain Research.

[11]  G. Somjen,et al.  Potassium and calcium concentrations in interstitial fluid of hippocampal formation during paroxysmal responses. , 1985, Journal of neurophysiology.

[12]  S. Ochs The Nature of Spreading Depression in Neural Networks , 1962 .

[13]  G. G. Somjen,et al.  Effects of prolonged elevation of potassium on hippocampus of anesthetized rats , 1993, Brain Research.

[14]  G. G. Somjen,et al.  Analysis of potential shifts associated with recurrent spreading depression and prolonged unstable spreading depression induced by microdialysis of elevated K+ in hippocampus of anesthetized rats , 1993, Brain Research.

[15]  J. McNamara,et al.  Sustained potential shifts and paroxysmal discharges in hippocampal formation. , 1985, Journal of neurophysiology.

[16]  Jan Bureš,et al.  Systemic ketamine blocks cortical spreading depression but does not delay the onset of terminal anoxic depolarization in rats , 1987, Brain Research.

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

[18]  J. Lerma,et al.  Characteristics of CA1 activation through the hippocampal trisynaptic pathway in the unanaesthetized rat , 1987, Brain Research.

[19]  C. Nicholson,et al.  Tetrodotoxin resistant propagation and extracellular sodium changes during spreading depression in rat cerebellum , 1982, Brain Research.

[20]  F. H. Lopes da Silva,et al.  Anatomic organization and physiology of the limbic cortex. , 1990, Physiological reviews.

[21]  R. D. do Carmo,et al.  Spreading depression of Leão probed with ion-selective microelectrodes in isolated chick retina. , 1984, Anais da Academia Brasileira de Ciencias.

[22]  I. Módy,et al.  Low extracellular magnesium induces epileptiform activity and spreading depression in rat hippocampal slices. , 1987, Journal of neurophysiology.

[23]  O Herreras,et al.  Propagating dendritic action potential mediates synaptic transmission in CA1 pyramidal cells in situ. , 1990, Journal of neurophysiology.

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

[25]  H. Collewijn,et al.  Membrane potential of cerebral cortical cells during reading depression and asyxia. , 1966, Experimental neurology.

[26]  G. Somjen,et al.  Whole‐cell membrane current and membrane resistance during hypoxic spreading depression , 1992, Neuroreport.

[27]  K. Schaffer Beitrag zur Histologie der Ammonshornformation , 1892 .

[28]  W. Kamphuis,et al.  Current source density of sustained potential shifts associated with electrographic seizures and with spreading depression in rat hippocampus , 1992, Brain Research.

[29]  O. Burešová,et al.  The mechanism and applications of Leão's spreading depression of electroencephalographic activity , 1974 .

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

[31]  M. Mayer,et al.  Kinetic analysis of antagonist action at N-methyl-D-aspartic acid receptors. Two binding sites each for glutamate and glycine. , 1991, Biophysical journal.