Abstract
Glial cells of the myenteric plexus from guinea pig small intestine were intracellulary filled with horseradish peroxidase (HRP), and histochemically stained. Camera lucida-like drawings of twenty cells were morphologically and morphometrically analyzed. The cells have very small ellipsoid, somata (85±0.7 μm equivalent diameter, i.e., about 330 μm3 volume), and send up to 20 thin and short processes (less than 26 to about 110 μm in length). The morphology of the cells appears to depend on their location within the plexus. Glial cells located within the ganglia are similar to CNS protoplasmic astrocytes; they are star-shaped, and their very short processes are irregularly, branched. In contrast, glial cells within the interganglionic fiber tracts resemble CNS fibrous astrocytes. They extend longer processes that are parallel to the fiber tracts, and show less tendency to branch. We propose that the morphology of enteric glia is determined by the structure of the microenvironment. Both cell types form several flat endfeet at a basal lamina either surrounding blood vessels or at the ganglionic border. Furthermore, the occurrence of “holes” in the glial cell processes suggests that particular neuronal cell processes may be enwrapped in a specific manner. Fractal analysis of camera lucida-like drawings of the cells showed that the cells have a highly complex surface structure, comparable to that of protoplasmic astrocytes in the brain. These tiny cells may possess a membrane surface area of ∼2000 μm2, almost 90% of which are contributed by the cell processes. This geometry may enable an intense exchange of metabolites and ions between neurons, glial cells, and the capillaries and/or environment of enteric ganglia.
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References
Andriezen WL (1893) The neuroglia elements of the brain. Br Med J 2:227–230
Black JA, Friedman B Waxman SG, Elmer LW, Angelides KJ (1989a) Immuno-ultrastructural localization of sodium channels at nodes of Ranvier and perinodal astrocytes in rat optic nerve. Proc R Soc Lond [Biol] 238:39–51
Black JA, Waxman SG, Friedman B, Elmer LW, Angelides KJ (1989b) Sodium channels in astrocytes of rat optic nerve in situ: immuno-electron microscopic studies. Glia 2:353–369
Broussard DL, Bannermann PGC, Tang C-M, Hardy M, Pleasure D (1993) Electrophysiologic and molecular properties of cultured enteric glia. J Neurosci Res 34:24–31
Cook RD, Burnstock G (1976) The ultrastructure of Auerbach's plexus in the guinea-pig. II. Non-neuronal elements. J Neurocytol 5:195–206
Dogiel AS (1899) Ueber den Bau der Ganglien in den Geflechten des Darmes und der Gallenblase des Menschen und der Säugetiere. Arch Anat Physiol Anat Abt 1899:130–158
Eberhardt W Reichenbach A (1987) Spatial buffering of potassium by retinal Müller (glial) cells of various morphologies calculated by a model. Neuroscience 22:687–696
Erde SM, Sherman D, Gershon MD (1985) Morphology and serotonergic innervation of physiologically identified cells of the guinea pig's myenteric plexus. J Neurosci 5:617–633
Ferri GL, Probert L, Cocchia D, Michetti F (1982) Evidence for the presence of S-100 protein in the glial component of the human enteric nervous system. Nature 297:409–410
Flook AG (1987) The use of dilation logic on the quantimet to achieve fractal dimension characterization of textured and structured profiles. Powder Technol 21:295–298
ffrench-Constant C, Miller RH, Kruse J, Schachner M, Raff MC (1986) Molecular specialization of astrocyte processes at nodes of Ranvier in rat optic nerve. J Cell Biol 102:844–852
Gabella G (1972) Fine structure of the myenteric plexus in the guinea-pig ileum. J Anat 111:69–97
Gabella G, Trigg P (1984) Size of neurons and glial cells in the enteric ganglia of mice, guinea-pigs, rabbits, and sheep. J Neurocytol 13:49–71
Gershon MD, Rothman TP (1991) Enteric glia. Glia 4:195–204
Grove EA, Williaas, PB, Li DR, Haji-Hosseini M, Friedrich A, Price J (1993) Multiple restricted lineages in the embryonic rat cerebral cortex. Development, 117:553–561
Hanani M, Baluk P, Burnstock G (1982) Myenteric neurons express electrophysiological and morphological diversity in tissue culture. J. Auton Nerv Syst 5:155–164
Hanani M, Chorev M, Gilon C, Selinger Z (1988) The action of receptor-selective substance P analogs on myenteric neurons: an electrophysiological investigation. Eur J Pharmacol 153:247–253
Hanani M, Zamir O, Baluk P (1989) Glial cells in the guinea pig myenteric plexus are dye coupled. Brain Res 497:245–249
Hildebrand C, Waxman SG (1983) Regional node-like membrane specializations in non-myelinated axons of rat retinal nerve fiber layer. Brain Res 258:23–32
Jessen KR, Mirsky R (1980) Glial cells in the enteric nervous system contain glial fibrillary acidic protein. Nature 286:736–737
Jessen KR, Mirsky R (1983) Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia. J Neurosci 3:2206–2218
Jessen KR, Thorpe R, Mirsky R (1984) Molecular identity, distribution and heterogeneity of glial fibrillary acidic protein: an immunoblotting and immunohistochemical study of Schwann cells satellite cells, enteric glia and astrocytes. J Neurocytol 13:187–200
Komuro T, Baluk P, Burnstock G (1982) An ultrastructural study of neurons and non-neuronal cells in the myenteric plexus of the rabbit colon. Neuroscience 7:1797–1806
Kosaka T, Hama K (1986) Three-dimensional structure of astrocytes in the rat dentate gyrus. J Comp Neurol 249:242–260
Lees GM, Mackenzie GM, Pearson GT (1992) Complex correlations between the morphology, electrophysiology and peptide immunohistochemistry of guinea-pig enteric neurones. Eur J Morphol 30:123–136
Mandelbrot BB (1982) The fractal geometry of nature. Freeman, New York
Maudlej N, Hanani M (1992) Modulation of dye coupling among glial cells in the myenteric and submucosal plexuses of the guinea pig. Brain Res 578:94–98
Miller RH, Liuzzi F (1986) Regional specialization of the radial glial cells of the adult frog spinal cord. J Neurocytol 15:187–196
Nishi S, North RA (1973) Intracellular recording from the myenteric plexus of the guinea-pig ileum. J Physiol (Lond) 231:471–491
Pomeranz HD, Rothman TP, Chalazonitis A, Tennyson VM, Gershon MD (1993) Neural crest-derived cells isolated from the gut by immunoselection develop neuronal and glial phenotypes when cultured on laminin. Dev Biol 156:341–361
Reichenbach A, Schippel K, Schumann R, Hagen E (1988) Ultrastructure of rabbit retinal nerve fibre layer — neuro-glial relationships, myelination, and nerve fibre spectrum. J Hirnforsch 29:481–491
Reichenbach A, Schneider H, Leibnitz L, reichelt W, Schaaf P, Schumann R, (1989) The structure of rabbit retinal Müller (glial) cells is adapted to the surrounding retinal layers. Anat Embryol 180:71–79
Reichenbach A, Siegel A, Senitz D, Smith TG Jr (1992) A comparative fractal analysis of various mammalian astroglial cell types. NeuroImage 1:69–77
Siegel A, Reichenbach A, Hanke S, Sentiz D, Brauer K, Smith TG Jr (1991) Comparative morphometry of Bergmann glial (Golgi epithelial) cells: a Golgi study. Anat Embryol 183:605–612
Smith TG Jr, Marks WB, Lange GD, Sheriff WH Jr, Neale EA (1989) Edge detection in images using Marr-Hildreth filtering techniques. J Neurosci Meth 26:75–82
Smith TG Jr, Marks WB, Lange GD, Sheriff WH Jr, Neale EA (1989) A fractal analysis of cell images. J Neurosci Meth 27:173–180
Stach W (1989) A revised morphological classification of neurons in the enteric nervous system. In: Singer MV, Goebell H (eds) Nerves and the gastrointestinal tract. MTP Press, Dordrecht, pp 29–45
Waxman SG (1986) The astrocyte as a component of the node of Ranvier. Trends Neuro Sci 9:250–253
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Hanani, M., reichenbach, A. Morphology of horseradish peroxidase (HRP)-injected glial cells in the myenteric plexus of the guinea-pig. Cell Tissue Res 278, 153–160 (1994). https://doi.org/10.1007/BF00305787
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DOI: https://doi.org/10.1007/BF00305787