Anoxia-induced extracellular ionic changes in CNS white matters: the role of glial cells

1992 ◽  
Vol 70 (S1) ◽  
pp. S181-S189 ◽  
Author(s):  
Bruce R. Ransom ◽  
Daniel M. Philbin Jr.
Keyword(s):  
Optic Nerve ◽  
Glial Cells ◽  
Gray Matter ◽  
Glucose Concentration ◽  
Temporal Association ◽  
Small Magnitude ◽  
Brain White Matter ◽  
Average Maximum ◽  
Ionic Changes ◽  
Induced Changes

The rapid changes in brain extracellular ion concentrations that occur with anoxia are important in understanding the pathophysiology of anoxic – ischemic brain injury. While previous studies have focused on the ionic changes that occur in gray matter areas of the brain, white matter (WM) is also damaged by anoxia. We describe the changes in extracellular K+ concentration ([K+]o) and extracellular pH (pHo) that accompany anoxia in WM, and present new results indicating that glial cells directly contribute to the observed fluctuations of these ions. Anoxia-induced changes in [K+]o and pHo were measured with ion-selective microelectrodes in the isolated rat optic nerve, a typical WM tract. To assess the contribution of glial cells, recordings were also made in optic nerves that contained only glial cells (produced by neonatal enucleation). Anoxia in WM produced less extreme changes in [K+]o and pHo than are known to occur in gray matter; in WM during anoxia, the average maximum [K+]o was 14 ± 2.9 mM (bath [K+]o = 3 mM) and the average maximum acid shift was 0.31 ± 0.07 pH unit. These extracellular ionic changes were accompanied by rapid shrinkage of extracellular space volume. The ability of optic nerve axons to conduct action potentials was lost in temporal association with the increase in [K+]o. Increasing bath glucose concentration from 10 to 20 mM resulted in a much larger acid shift during anoxia (0.58 ± 0.08 pH unit) and a smaller average increase in [K+]o (9.2 ± 2.6 mM). The increased glucose concentration presumably enhanced anaerobic metabolism, leading to extracellular lactate accumulation and a greater acid shift. More ATP would be available for operation of ion pumps, including the sodium pump, and this would result in less dramatic changes in [K+]o. The optic nerve showed significantly less irreversible damage after 60 min of anoxia in the presence of 20 mM glucose compared with 10 mM glucose. In the pure glial nerve, anoxia caused a 1.2 ± 1.1 mM increase in [K+]o and a 0.10 ± 0.04 unit decline in pHo, with time courses similar to the analogous changes in intact nerves. The small magnitude of these anoxia-induced changes in the glial preparation probably results in part from technical factors having to do with the small size of the pure glial nerves. The magnitude of the changes in the pure glial nerves was influenced by bath glucose concentration, with anoxia in 0 mM glucose producing a 1.7 ± 0.4 mM increase in [K+]o, and a 0.05 ± 0.06 unit decrease in pHo. We conclude that glial cells directly contribute to the ionic changes observed during anoxia in WM.Key words: ions, ischemia, glucose, optic nerve, compound action potential, ion-selective electrodes.

scholarly journals Anoxia-Induced Changes in Extracellular K+ and pH in Mammalian Central White Matter

1992 ◽  
Vol 12 (4) ◽  
pp. 593-602 ◽  
Author(s):  
Bruce R. Ransom ◽  
Wolfgang Walz ◽  
Peter K. Davis ◽  
Walter G. Carlini
Keyword(s):  
White Matter ◽  
Optic Nerve ◽  
Action Potential ◽  
Glucose Concentration ◽  
Anaerobic Metabolism ◽  
Compound Action Potential ◽  
Average Maximum ◽  
Ionic Changes ◽  
Induced Changes ◽  
Compound Action

In gray matter (GM), anoxia induces prominent extracellular ionic changes that are important in understanding the pathophysiology of this insult. White matter (WM) is also injured by anoxia but the accompanying changes in extracellular ions have not been studied. To provide such information, the time course and magnitude of anoxia-induced changes in extracellular K+ concentration ([K+]o) and extracellular pH (pHo) were measured in the isolated rat optic nerve, a representative central WM tract, using ion-selective microelectrodes. Anoxia produced less extreme changes in [K+]o and pHo in WM than are known to occur in GM; in WM during anoxia, the average maximum [K+]o was 14 ± 2.9 m M (bath [K+]o = 3 m M) and the average maximum acid shift was 0.31 ± 0.07 pH unit. The extracellular space volume rapidly decreased by ∼20% during anoxia. Excitability of the rat optic nerve, monitored as the amplitude of the supramaximal compound action potential, was lost in close temporal association with the increase in [K+]o Increasing the bath glucose concentration from 10 to 20 m M resulted in a much larger acid shift during anoxia (0.58 ± 0.08 pH unit) and a smaller average increase in [K+]o (9.2 ± 2.6 m M). The increased extracellular glucose concentration presumably provided more substrate for anaerobic metabolism, resulting in more extracellular lactate accumulation (although not directly measured) and a greater acid shift. Enhanced anaerobic metabolism during anoxia would provide energy for operation of ion pumps, including the sodium pump, that would result in smaller changes in [K+]o. These effects were probably responsible for the observation that the optic nerve showed significantly less damage after 60 min of anoxia in the presence of 20 m M glucose compared to 10 m M glucose. Under normoxic conditions, increasing bath K+ concentration to 30 m M (i.e., well beyond the level shown to occur with anoxia) for 60 min caused abrupt loss of excitability during the period of application but minimal change in the amplitude of the compound action potential following the period of exposure. The anoxia-induced increase in [K+]o, therefore, was not itself directly responsible for irreversible loss of optic nerve function. These observations indicate that major qualitative differences exist between mammalian GM and WM with regard to anoxia-induced extracellular ionic changes.

Cultures of glial cells from optic nerve of two adult teleost fish: Astatotilapia burtoni and Danio rerio

2021 ◽  
Vol 353 ◽  
pp. 109096
Author(s):  
Laura DeOliveira-Mello ◽  
Andreas F. Mack ◽  
Juan M. Lara ◽  
Rosario Arévalo
Keyword(s):  
Optic Nerve ◽  
Glial Cells ◽  
Danio Rerio ◽  
Teleost Fish ◽  
Astatotilapia Burtoni

Glutamate depolarization of glial cells in Necturus optic nerve

1986 ◽  
Vol 63 (3) ◽  
pp. 300-304 ◽  
Author(s):  
Cha-Min Tang ◽  
Richard K. Orkand
Keyword(s):  
Optic Nerve ◽  
Glial Cells

scholarly journals Benthic Habitat Morphodynamics-Using Remote Sensing to Quantify Storm-Induced Changes in Nearshore Bathymetry and Surface Sediment Texture at Assateague National Seashore

2019 ◽  
Vol 7 (10) ◽  
pp. 371 ◽  
Author(s):  
Arthur Trembanis ◽  
Alimjan Abla ◽  
Ken Haulsee ◽  
Carter DuVal
Keyword(s):  
Multiple Scales ◽  
Habitat Type ◽  
Hurricane Sandy ◽  
Temporal Association ◽  
Benthic Habitat ◽  
Offshore Area ◽  
Side Scan Sonar ◽  
Marine Habitats ◽  
Induced Changes ◽  
National Seashore

This study utilizes repeated geoacoustic mapping to quantify the morphodynamic response of the nearshore to storm-induced changes. The aim of this study was to quantitatively map the nearshore zone of Assateague Island National Seashore (ASIS) to determine what changes in bottom geomorphology and benthic habitats are attributable to storm events including hurricane Sandy and the passage of hurricane Joaquin. Specifically, (1) the entire domain of the National Parks Service offshore area was mapped with side-scan sonar and multibeam bathymetry at a resolution comparable to that of the existing pre-storm survey, (2) a subset of the benthic stations were resampled that represented all sediment strata previously identified, and (3) newly obtained data were compared to that from the pre-storm survey to determined changes that could be attributed to specific storms such as Sandy and Joaquin. Capturing event specific dynamics requires rapid response surveys in close temporal association of the before and after period. The time-lapse between the pre-storm surveys for Sandy and our study meant that only a time and storm integrated signature for that storm could be obtained whereas with hurricane Joaquin we could identify impacts to the habitat type and geomorphology more directly related to that particular storm. This storm impacts study provides for the National Park Service direct documentation of storm-related changes in sediments and marine habitats on multiple scales: From large scale, side-scan sonar maps and interpretation of acoustic bottom types, to characterize as fully as possible habitats from 1 to 10 m up to many kilometer scales, as well as from point benthic samples within each sediment stratum and these results can help guide management of the island resources.

scholarly journals Effects of Temperature on Evoked Electrical Activity and Anoxic Injury in CNS White Matter

1992 ◽  
Vol 12 (6) ◽  
pp. 977-986 ◽  
Author(s):  
Peter K. Stys ◽  
Stephen G. Waxman ◽  
Bruce R. Ransom
Keyword(s):  
White Matter ◽  
Optic Nerve ◽  
Functional Outcome ◽  
Gray Matter ◽  
Functional Recovery ◽  
Temperature Sensitive ◽  
Anoxic Injury ◽  
Intracellular Ca ◽  
Effects Of Temperature ◽  
The Brain

Temperature is known to influence the extent of anoxic/ischemic injury in gray matter of the brain. We tested the hypothesis that small changes in temperature during anoxic exposure could affect the degree of functional injury seen in white matter, using the isolated rat optic nerve, a typical CNS white matter tract (Foster et al., 1982). Functional recovery after anoxia was monitored by quantitative assessment of the compound action potential (CAP) area. Small changes in ambient temperature, within a range of 32 to 42°C, mildly affected the CAP of the optic nerve under normoxic conditions. Reducing the temperature to <37°C caused a reversible increase in the CAP area and in the latencies of all three CAP peaks; increasing the temperature to >37°C had opposite effects. Functional recovery of white matter following 60 min of anoxia was strongly influenced by temperature during the period of anoxia. The average recovery of the CAP, relative to control, after 60 min of anoxia administered at 37°C was 35.4 ± 7%; when the temperature was lowered by 2.5°C (i.e., to 34.5°C) for the period of anoxic exposure, the extent of functional recovery improved to 64.6 ± 15% ( p < 0.00001). Lowering the temperature to 32°C during anoxic exposure for 60 min resulted in even greater functional recovery (100.5 ± 14% of the control CAP area). Conversely, if temperature was increased to >37°C during anoxia, the functional outcome worsened, e.g., CAP recovery at 42°C was 8.5 ± 7% ( p < 0.00001). Hypothermia (i.e., 32°C) for 30 min immediately following anoxia at 37°C did not improve the functional outcome. Many processes within the brain are temperature sensitive, including O2 consumption, and it is not clear which of these is most relevant to the observed effects of temperature on recovery of white matter from anoxic injury. Unlike the situation in gray matter, the temperature dependency of anoxic injury cannot be related to reduced release of excitotoxins like glutamate, because neurotransmitters play no role in the pathophysiology of anoxic damage in white matter (Ransom et al., 1990 a). It is more likely that temperature affects the rate of ion transport by the Na+–Ca2+ exchanger, the transporter responsible for intracellular Ca2+ loading during anoxia in white matter, and/or the rate of some destructive intracellular enzymatic mechanism(s) activated by pathological increases in intracellular Ca2+.

scholarly journals Pressure-Induced Changes in Astrocyte GFAP, Actin, and Nuclear Morphology in Mouse Optic Nerve

2020 ◽  
Vol 61 (11) ◽  
pp. 14 ◽  
Author(s):  
Yik Tung Tracy Ling ◽  
Mary E. Pease ◽  
Joan L. Jefferys ◽  
Elizabeth C. Kimball ◽  
Harry A. Quigley ◽  
...  
Keyword(s):  
Optic Nerve ◽  
Nuclear Morphology ◽  
Induced Changes

scholarly journals An epithelium-type cytoskeleton in a glial cell: astrocytes of amphibian optic nerves contain cytokeratin filaments and are connected by desmosomes.

1989 ◽  
Vol 109 (2) ◽  
pp. 705-716 ◽  
Author(s):  
E Rungger-Brändle ◽  
T Achtstätter ◽  
W W Franke
Keyword(s):  
Optic Nerve ◽  
Glial Cells ◽  
Cytoskeletal Proteins ◽  
Membrane Domains ◽  
Glial Differentiation ◽  
Amphibian Species ◽  
Glial Development ◽  
Lower Vertebrates ◽  
Filament Protein ◽  
Brain And Spinal Cord

In higher vertebrates the cytoskeleton of glial cells, notably astrocytes, is characterized (a) by masses of intermediate filaments (IFs) that contain the hallmark protein of glial differentiation, the glial filament protein (GFP); and (b) by the absence of cytokeratin IFs and IF-anchoring membrane domains of the desmosome type. Here we report that in certain amphibian species (Xenopus laevis, Rana ridibunda, and Pleurodeles waltlii) the astrocytes of the optic nerve contain a completely different type of cytoskeleton. In immunofluorescence microscopy using antibodies specific for different IF and desmosomal proteins, the astrocytes of this nerve are positive for cytokeratins and desmoplakins; by electron microscopy these reactions could be correlated to IF bundles and desmosomes. By gel electrophoresis of cytoskeletal proteins, combined with immunoblotting, we demonstrate the cytokeratinous nature of the major IF proteins of these astroglial cells, comprising at least three major cytokeratins. In this tissue we have not detected a major IF protein that could correspond to GFP. In contrast, cytokeratin IFs and desmosomes have not been detected in the glial cells of brain and spinal cord or in certain peripheral nerves, such as the sciatic nerve. These results provide an example of the formation of a cytokeratin cytoskeleton in the context of a nonepithelial differentiation program. They further show that glial differentiation and functions, commonly correlated with the formation of GFP filaments, are not necessarily dependent on GFP but can also be achieved with structures typical of epithelial differentiation; i.e., cytokeratin IFs and desmosomes. We discuss the cytoskeletal differences of glial cells in different kinds of nerves in the same animal, with special emphasis on the optic nerve of lower vertebrates as a widely studied model system of glial development and nerve regeneration.

Sign in / Sign up

Export Citation Format

Share Document