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Glial Cells

Richard K. Orkand

10.1002/cphy.cp010123

Source: Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons

Originally published: 1977

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Physiological Properties
1.1 Criteria for Identification
1.2 Resting Membrane Potential
1.3 Membrane Electrical Properties
1.4 Electrical Connections Between Glial Cells
2 Interactions with Neurons
2.1 Detecting Nerve Activity
2.2 Contribution to Extracellular Potentials
2.3 Metabolic Effects of Increased Potassium
2.4 Neuron‐Glia Exchange
2.5 Control of Neuron Environment
3 Physiological Properties of Schwann Cells
4 Slow Changes in the Nervous System
4.1 Degeneration
4.2 Regeneration and Development
Figure 1. Figure 1.

Top: photomicrograph of live mammalian astrocyte in tissue culture and position of electrodes for recording (R) and stimulation (S). Outline of nuclear membrane lies outside the plane of focus; 35‐day‐old cultures; phase contrast.

From Hild et al. 71.] Bottom: Müller (glial) cell from Necturus retina, stained intracellularly with combination of Niagara sky blue, methyl blue, and Procion yellow. Current pulses of 10–20 nA were passed for about 45 s, at which time the electrode slipped out of the cell. The 3 micrographs on the left are different focal planes of the same cell to show extent of staining. A: column of dye in cell beginning at internal limiting membrane and extending to inner nuclear layer. B: Müller cell nucleus in inner nuclear layer that has also been stained. C: column of dye from Müller cell nucleus extending to outer nuclear layer. D: reconstruction of stained cell. [From Miller & Dowling 107
Figure 2. Figure 2.

Top: record of effect of changing K+ concentration in bathing fluid on membrane potential of glial cell. Resting potential in the standard 3 meq/liter K+ solution was 90 mV. Reducing K+ in bath to 0.3 meq/liter raised membrane potential by 35 mV to 125 mV. Increasing K+ 10 times to 30 meq/liter depolarized by 59 mV. Calibrations: vertical, 75 mV; horizontal, 30 s. From such measurements the relationship between membrane potential and K+ concentration was plotted.

From Kuffler et al. 95.] Bottom: relation between membrane potential and external potassium concentration (log scale) for nerve and glia. Solid line has slope of 59 mV according to the Nernst equation. Points are membrane potentials from glial cells in Necturus optic nerve 95. Dashed line is relation for frog myelinated nerve fibers 79. [From Orkand 114
Figure 3. Figure 3.

Selectivity pattern of permeation of monovalent cations through the potassium channel in nerve and glia. Ordinate: ratio of permeability of test cation to potassium (•). Abscissa: hydrated diameter of ion in angstroms. Top: ▪, data from squid axon 60; □, data from frog myelinated nerve 73. Bottom: ○, data from glial cells in Necturus 13. Fingerprints for all systems are almost identical.
Figure 4. Figure 4.

Electrical connections between glial cells in leech central nervous system. An intracellular current electrode (I) in the anterior median packet cell (containing the paired Retzius cells) delivered a 400‐ms2 pulse of 2.6 × 10−8 A. A: voltage recorded in the same packet cell. B: with voltage electrode inserted into the neighboring glial cell, potential rise was slowed and attenuated about 5 times. With voltage electrode just outside this glial cell (lowest sweep), no electrotonic potential was seen. Scale: 10 mV and 200 ms; temperature: 12°C

From Kuffler & Potter 96
Figure 5. Figure 5.

Top: record of 9 successive glial depolarizations in Necturus optic nerve set up by maximal nerve volleys at 1‐s intervals. Extrapolation of the falling phase of the first and seventh depolarization shown by dashed line. Depolarization is given in millivolts on left side of scale. Values of external K+ concentration (meq/liter) that would produce equivalent depolarizations (calculated from the Nernst equation) appear on right side of scale.

From Orkand et al. 117.] Bottom: K+ electrode potentials during long train of 0.8/s cortical stimuli (bar); K+‐sensitive electrode in extracellular space of cat cortex. Stimulation continuous, but 50‐s section of recording omitted. Dashed line: 3 mM K+ level. [From Prince et al. 126
Figure 6. Figure 6.

Top: schematic representation of experimental arrangement. Desheathed optic nerve of Necturus, which is represented by a single axon (A) and row of glial cells (G), was placed in a sucrose gap chamber consisting of 3 compartments. Two microelectrodes were inserted into glial cells in the left‐hand compartment. The one distant from the central compartment, or gap, was used for passing current pulses (Ig). In the second compartment, less than 90 μm from the gap, resulting changes in glial membrane potential (Vg) were recorded. Changes in surface potential were recorded simultaneously between two other electrodes, one on each side of the gap (Vg). Since glial cells are electrically coupled to each other, current injected into one cell spreads to neighboring cells causing their membrane potentials to change. Bottom: A, simultaneous potential changes recorded with an intracellular electrode (Vg) in a glial cell near the sucrose gap and with extracellular leads across the gap (Vg). The currents, monitored in the top trace (Ig), were injected into a glial cell 1,020 μm from the gap. Note similar time courses of the potentials, but Vg is about one‐half of Vg (see calibration). B, same conditions as in A, but current electrode was advanced into the intercellular space just outside the glial cell. Note the absence of significant potentials when current does not cross glial membrane

From Cohen 28
Figure 7. Figure 7.

Intracellular record (lower trace) from a glial cell and extracellular record (upper trace) from the surface of cerebral cortex of a cat during direct cortical stimulation of 8/s. Slow depolarization recorded from a presumed glial cells 200 μm deep; resting potential, −76 mV

From Ransom & Goldring 134
Figure 8. Figure 8.

Top: electron micrographs of normal and all‐glia optic nerves of Necturus. Note the large mass of glial cell cytoplasm after the axons have degenerated. The all‐glia nerve was fixed 65 days after removal of the eye. Bottom: left, experimental arrangement for continuous registration of NADH fluorescence in in vitro optic nerves. Technique is based on the observation that NADH fluoresces when excited with light at a wavelength of 355 nm and emits light with a peak wavelength of about 480 nm; NAD+ does not. Right, record of fluorescence decrease in glia when the external potassium concentration was raised from normal (3 meq/liter) to 6 meq/liter (top) and 12 meq/liter (bottom)

From Orkand et al. 115
Figure 9. Figure 9.

Effect of removal of the surrounding glia on the undershoot decrement of action potentials in a train. The same pressure cell was impaled before and after removing the glia [see 96]. Stimuli were applied to its axon in the posterior root. After removal of the glia (NAKED) the undershoots no longer showed a decrement during trains, although the action potential and the sensitivity of the undershoot to K (not shown) were unchanged

From Baylor & Nicholls 5
Figure 10. Figure 10.

Electron‐microscope autoradiogram illustrating the sites of GABA binding in lobster neuromuscular system. Labeled GABA was applied externally and, after uptake, was bound to the tissue with a fixative containing glutaraldehyde. The autoradiogram shows label over Schwann cell (S) and connective‐tissue components, not the axon (A) or the muscle (M)

From Orkand & Kravitz 116
Figure 11. Figure 11.

Schematic drawing of the developing cerebellar cortex in 10‐day‐old wild‐type (A), heterozygous (B), and homozygous (C) Weaver littermate mice. To highlight the main effects of the wv allele, the drawing has been grossly simplified by omitting dendrites and axons of Purkinje and granule cell neurons, and omitting entirely the other cell classes and afferent axons of the cerebellar cortex. A: in normal mice, cells migrate (arrows) from the external granular layer (EG) to the granular layer (G) along straight, radially oriented Bergmann glia (black cells) whose cytoplasmic processes span the entire thickness of the molecular layer (M). B: in heterozygous mice, a smaller than normal number of granule cell somas becomes successfully translocated. Many are oval or round and lie in contact with thickened and irregular Bergmann glial fibers; some of these granule cells remain permanently in the molecular layer or degenerate (fragmented cells). C: in homozygous affected weavers, almost no granule cells descend deep to the Purkinje cell bodies, and instead most of them degenerate at the border between the external granular layer and the molecular layer

From Rakic & Sidman 130
Figure 12. Figure 12.

Morphological differentiation induced by glial cell‐conditioned medium. The neuroblastoma cells were plated in dishes containing glass cover slips. After 16 h the incubation medium was replaced by fresh medium (A) or by glial cell‐conditioned medium (72 h) which had been filtered through a sterile 0.22 m Millipore membrane (B); 48 h later the coverslips were washed, fixed, dehydrated, metal coated, and examined in a scanning electron microscope

From Monard et al. 108


Figure 1.

Top: photomicrograph of live mammalian astrocyte in tissue culture and position of electrodes for recording (R) and stimulation (S). Outline of nuclear membrane lies outside the plane of focus; 35‐day‐old cultures; phase contrast.

From Hild et al. 71.] Bottom: Müller (glial) cell from Necturus retina, stained intracellularly with combination of Niagara sky blue, methyl blue, and Procion yellow. Current pulses of 10–20 nA were passed for about 45 s, at which time the electrode slipped out of the cell. The 3 micrographs on the left are different focal planes of the same cell to show extent of staining. A: column of dye in cell beginning at internal limiting membrane and extending to inner nuclear layer. B: Müller cell nucleus in inner nuclear layer that has also been stained. C: column of dye from Müller cell nucleus extending to outer nuclear layer. D: reconstruction of stained cell. [From Miller & Dowling 107


Figure 2.

Top: record of effect of changing K+ concentration in bathing fluid on membrane potential of glial cell. Resting potential in the standard 3 meq/liter K+ solution was 90 mV. Reducing K+ in bath to 0.3 meq/liter raised membrane potential by 35 mV to 125 mV. Increasing K+ 10 times to 30 meq/liter depolarized by 59 mV. Calibrations: vertical, 75 mV; horizontal, 30 s. From such measurements the relationship between membrane potential and K+ concentration was plotted.

From Kuffler et al. 95.] Bottom: relation between membrane potential and external potassium concentration (log scale) for nerve and glia. Solid line has slope of 59 mV according to the Nernst equation. Points are membrane potentials from glial cells in Necturus optic nerve 95. Dashed line is relation for frog myelinated nerve fibers 79. [From Orkand 114


Figure 3.

Selectivity pattern of permeation of monovalent cations through the potassium channel in nerve and glia. Ordinate: ratio of permeability of test cation to potassium (•). Abscissa: hydrated diameter of ion in angstroms. Top: ▪, data from squid axon 60; □, data from frog myelinated nerve 73. Bottom: ○, data from glial cells in Necturus 13. Fingerprints for all systems are almost identical.



Figure 4.

Electrical connections between glial cells in leech central nervous system. An intracellular current electrode (I) in the anterior median packet cell (containing the paired Retzius cells) delivered a 400‐ms2 pulse of 2.6 × 10−8 A. A: voltage recorded in the same packet cell. B: with voltage electrode inserted into the neighboring glial cell, potential rise was slowed and attenuated about 5 times. With voltage electrode just outside this glial cell (lowest sweep), no electrotonic potential was seen. Scale: 10 mV and 200 ms; temperature: 12°C

From Kuffler & Potter 96


Figure 5.

Top: record of 9 successive glial depolarizations in Necturus optic nerve set up by maximal nerve volleys at 1‐s intervals. Extrapolation of the falling phase of the first and seventh depolarization shown by dashed line. Depolarization is given in millivolts on left side of scale. Values of external K+ concentration (meq/liter) that would produce equivalent depolarizations (calculated from the Nernst equation) appear on right side of scale.

From Orkand et al. 117.] Bottom: K+ electrode potentials during long train of 0.8/s cortical stimuli (bar); K+‐sensitive electrode in extracellular space of cat cortex. Stimulation continuous, but 50‐s section of recording omitted. Dashed line: 3 mM K+ level. [From Prince et al. 126


Figure 6.

Top: schematic representation of experimental arrangement. Desheathed optic nerve of Necturus, which is represented by a single axon (A) and row of glial cells (G), was placed in a sucrose gap chamber consisting of 3 compartments. Two microelectrodes were inserted into glial cells in the left‐hand compartment. The one distant from the central compartment, or gap, was used for passing current pulses (Ig). In the second compartment, less than 90 μm from the gap, resulting changes in glial membrane potential (Vg) were recorded. Changes in surface potential were recorded simultaneously between two other electrodes, one on each side of the gap (Vg). Since glial cells are electrically coupled to each other, current injected into one cell spreads to neighboring cells causing their membrane potentials to change. Bottom: A, simultaneous potential changes recorded with an intracellular electrode (Vg) in a glial cell near the sucrose gap and with extracellular leads across the gap (Vg). The currents, monitored in the top trace (Ig), were injected into a glial cell 1,020 μm from the gap. Note similar time courses of the potentials, but Vg is about one‐half of Vg (see calibration). B, same conditions as in A, but current electrode was advanced into the intercellular space just outside the glial cell. Note the absence of significant potentials when current does not cross glial membrane

From Cohen 28


Figure 7.

Intracellular record (lower trace) from a glial cell and extracellular record (upper trace) from the surface of cerebral cortex of a cat during direct cortical stimulation of 8/s. Slow depolarization recorded from a presumed glial cells 200 μm deep; resting potential, −76 mV

From Ransom & Goldring 134


Figure 8.

Top: electron micrographs of normal and all‐glia optic nerves of Necturus. Note the large mass of glial cell cytoplasm after the axons have degenerated. The all‐glia nerve was fixed 65 days after removal of the eye. Bottom: left, experimental arrangement for continuous registration of NADH fluorescence in in vitro optic nerves. Technique is based on the observation that NADH fluoresces when excited with light at a wavelength of 355 nm and emits light with a peak wavelength of about 480 nm; NAD+ does not. Right, record of fluorescence decrease in glia when the external potassium concentration was raised from normal (3 meq/liter) to 6 meq/liter (top) and 12 meq/liter (bottom)

From Orkand et al. 115


Figure 9.

Effect of removal of the surrounding glia on the undershoot decrement of action potentials in a train. The same pressure cell was impaled before and after removing the glia [see 96]. Stimuli were applied to its axon in the posterior root. After removal of the glia (NAKED) the undershoots no longer showed a decrement during trains, although the action potential and the sensitivity of the undershoot to K (not shown) were unchanged

From Baylor & Nicholls 5


Figure 10.

Electron‐microscope autoradiogram illustrating the sites of GABA binding in lobster neuromuscular system. Labeled GABA was applied externally and, after uptake, was bound to the tissue with a fixative containing glutaraldehyde. The autoradiogram shows label over Schwann cell (S) and connective‐tissue components, not the axon (A) or the muscle (M)

From Orkand & Kravitz 116


Figure 11.

Schematic drawing of the developing cerebellar cortex in 10‐day‐old wild‐type (A), heterozygous (B), and homozygous (C) Weaver littermate mice. To highlight the main effects of the wv allele, the drawing has been grossly simplified by omitting dendrites and axons of Purkinje and granule cell neurons, and omitting entirely the other cell classes and afferent axons of the cerebellar cortex. A: in normal mice, cells migrate (arrows) from the external granular layer (EG) to the granular layer (G) along straight, radially oriented Bergmann glia (black cells) whose cytoplasmic processes span the entire thickness of the molecular layer (M). B: in heterozygous mice, a smaller than normal number of granule cell somas becomes successfully translocated. Many are oval or round and lie in contact with thickened and irregular Bergmann glial fibers; some of these granule cells remain permanently in the molecular layer or degenerate (fragmented cells). C: in homozygous affected weavers, almost no granule cells descend deep to the Purkinje cell bodies, and instead most of them degenerate at the border between the external granular layer and the molecular layer

From Rakic & Sidman 130


Figure 12.

Morphological differentiation induced by glial cell‐conditioned medium. The neuroblastoma cells were plated in dishes containing glass cover slips. After 16 h the incubation medium was replaced by fresh medium (A) or by glial cell‐conditioned medium (72 h) which had been filtered through a sterile 0.22 m Millipore membrane (B); 48 h later the coverslips were washed, fixed, dehydrated, metal coated, and examined in a scanning electron microscope

From Monard et al. 108
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Article Title: Glial Cells
 

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Richard K. Orkand. Glial Cells. Compr Physiol 2011, Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons: 855-875. First published in print 1977. doi: 10.1002/cphy.cp010123