Trigeminal Ganglion. Fine Structure of Nerve-Cell Bodies and Satellite Cells in the
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1 Fine Structure of Nerve-Cell Bodies and Satellite Cells in the Trigeminal Ganglion ANDREW D. DIXON* Department of Anatomy, Medical School, University of Manchester, England A solution to some of the major problems of the structure of cytoplasmic elements in nerve cells has been one result of improvements in the techniques of electron microscopy, and the dorsal root ganglia of spinal nerves have been used frequently as a suitable source of sensory-nerve cells.'-3 While some authors4 have suggested that certain nerve-cell constituents, such as the Nissl bodies and neurofibrils, are carefully cultivated fixation artifacts, there is now general agreement that these and other intracellular structures are features of the normal living nerve cell.5' 6 Various techniques, such as the use of the phase-contrast microscope,7 have been applied to substantiate the light microscope and electron-optical appearances, and attempts have been made to alter the normal content of certain organelles in nerve cells under experimental conditions.8 Occasional investigations of cranial-nerve ganglia have been carried out, concerned with the significance of perikaryal myelin sheath formation in the ganglia of the eighth cranial nerve9 10 and the role of the nuclear envelope in the developing cells of the avian trigeminal ganglion." The purpose of the present investigation was to determine the electron-micrographic features of normal neurons and their satellite cells in the trigeminal ganglion, as part of a wider investigation into the nervous pathways associated with nerve terminations and plexuses in the oral mucosa.'2 13 The nature of the nerve cells in the ganglion is of particular interest, not only because of their functional importance in the transmission of painful and other stimuli from oral and facial tissues to the central nervous system but also because of their possible association with the significant unmyelinated nervefiber population in the ganglion, which has been described recently.'4 MATERIALS AND METHODS Trigeminal ganglia were removed as rapidly as possible from anesthetized normal rats, whose ages ranged from 3 to 48 days, and small pieces were fixed for 1-2 hours at 40 C. for electron microscopy. The fixative used was either a 2 per cent osmium tetroxide solution, which had been buffered to ph ,15 or a 1 per cent chrome-osmium tetroxide solution to which saponin had been added.'6 After dehydration, tissue blocks This investigation was supported by grant M828 from the College of Medicine Trust Fund, University of Iowa, Iowa City, Iowa. Received for publication January 7, * Present address: School of Dentistry, University of North Carolina, Chapel Hill, North Carolina.
2 Vol. 42, No. 4 NERVE AND SATELLITE CELLS IN GANGLION 991 were imbedded in resin,* ultrathin sections were prepared and examined, without prior staining, in an electron microscopes In addition to the material prepared specifically for electron microscopy, trigeminal ganglia from several animals covering a similar age range were fixed in neutralized formol-saline. Subsequently, paraffin sections were cut and stained by routine histologic techniques. This material was used for correlation of electron-micrographic appearances with those seen by more conventional histologic methods. Hematoxylin and eosin stain was employed to determine details of the total histologic picture, while a cresyl violet staining technique was used to demonstrate the distribution of cytoplasmic granules in the perikarya of the nerve cells. RESULTS The distribution of nerve-cell bodies and nerve fibers in the trigeminal ganglion closely paralleled the arrangement found in the sensory ganglia associated with the dorsal roots of spinal nerves. The majority of the nerve-cell bodies were concentrated at the periphery of the ganglion, leaving a broad central zone rich in nerve fibers and interspersed with isolated columns of perikarya (Fig. 1). In the predominantly cellular zone the nerve cells were closely packed together, and, when cells were sectioned equatorially, large, circular nuclei with well-defined nucleoli and a pale particulate nucleoplasm were revealed (Fig. 2). On the outer aspect of the cell membrane the nuclei of several satellite or capsule cells were evident, and often these cells appeared to be connected to one another by delicate protoplasmic prolongations. The nerve cells contained granular material (Nissl substance), which was scattered throughout the cytoplasm, except in the region of the axon hillock. The Nissl substance was seen to best advantage when the cresyl violet staining technique was employed and also when the variability in the size of the Nissl granules was demonstrated more clearly (Fig. 3). In the intervals between adjacent groups of nerve cells, clusters of small nuclei were observed, belonging to fibroblasts or the Schwann cells associated with nerve-fiber bundles (Figs. 2, 3). In low-magnification electron micrographs (Fig. 4), many of the features seen in routine histologic preparations were confirmed. The cytoplasm of the satellite cells formed thin layers on the surface of the nerve cells, except where more than two cells adjoined. In these positions either the interval between adjacent nerve cells was completely filled by the satellite cells or small tissue clefts persisted. Sometimes in the larger of these intercellular spaces unmyelinated axons were observed (Fig. 4). The nuclei of the satellite cells were smaller than and differed in electron density from those of the nerve cells, because of a finer granularity of the satellite nucleoplasm (Figs. 4, 5). Frequently, the nuclear membranes of the nerve cells were folded, and, when present in the plane of section, the pronounced electron density of the nucleolus was a prominent feature (Fig. 4). Striking variations in the electron density of the cytoplasm of neighboring nerve cells were noted also (Figs. 4-6) and appeared to be dependent on the relative concentrations of contained formed elements. In the "dark" type of cytoplasm, mitochondrial profiles were numerous, and there was an abundance of the ribonucleoprotein granules, which formed an important constitutent of the Nissl substance. In the "pale" type of * Araldite, Ciba Ltd., Duxford, England. t RCA EMU 3F, Radio Corporation of America, Camden, New Jersey.
3 Fic. 1.-Longitudinal section through the commencement of the mandibular division (MD) of the trigeminal nerve in an adult rat. The majority of the nerve cells (C) are concentrated at the periphery of the ganglion. (Cresyl violet stain; orig. mag. X 2 7). FIG. 2. A group of nerve cells in the trigeminal ganglion of a 4-day-old rat. Several of the largest cells have pale nuclei, with heavily stained nucleoli, and a granular cytoplasm. A smaller type of cell (A) possesses a scanty, more homogeneous cytoplasm. Nuclei of satellite cells (S) lie on the outer aspect of the nerve-cell membrane. (Stain H and E; orig. mag. X590.) FIc. 3. Four nerve-cell bodies in the trigeminal ganglion of an 11-day-old rat, stained to show Nissl granules in the cytoplasm. One of the cells (arrow) is of the small agranular type. (Cresyl violet stain; orig. mag. X590.) FIG. 4.-Trigeminal nerve cells in an 8-day-old rat, showing nuclei (N) with dense nucleoli (NU). In the cytoplasm (C) abundant mitochondria and aggregations of ribonucleoprotein granules are evident. The nerve cells are surrounded by a thin layer of satellite-cell cytoplasm (SC). Small clefts (arrows) persist between adjacent cells. Toward the right of the field, an unmyclinated axon (AX) and the nucleus of a satellite cell (SN) are indicated. (Orig. mag. X3670.)
4 Vol. 42, No. 4 NERVE AND SATELLITE CELLS IN GANGLION 993 cytoplasm the granular aggregates were more widely dispersed, and mitochondrial profiles were less numerous. In many cells of both types the majority of the mitochondria were concentrated in the perinuclear zone, so that the Nissl substance was most obvious toward the periphery of the cell, as was also the case in optical microscope preparations (Figs. 2, 3). Several neuron cell bodies are shown in Figure 5, and the cytoplasm of the rectangular-shaped cell that occupies the center of the field is distinctly paler than the surrounding cells. At the upper left corner of this pale cell, an unmyelinated nerve fiber lies in a shallow concavity of the nerve cell and is partly enveloped by a cytoplasmic extension of a neighboring satellite cell. Other unmyelinated nerve fibers occupy the upper part of the electron micrograph, separated from the neuronal cell bodies by a slender fibroblast. In contrast, myelinated axons are seen toward the upper right and lower left of the field. The rectangular area outlined in Figure 5 has been reproduced at higher magnification in Figure 6, to show greater detail of the variations in cytoplasmic electron density. Parts of three adjoining cells have been included, extending from the edge of the nucleus of the pale cell (Fig. 6, PC) through the cytoplasm of two dark cells to include the nucleus of the second of these neurons (Fig. 6, D2). Both nuclei were bounded by smooth, double, nuclear membranes, while the cell membranes, particularly of the dark cells, were noticeably folded. The external limiting membranes of the satellite cells of successive neurons were separated by a narrow interval and took the form of fine parallel lines (Fig. 6). Elsewhere the membranes could be followed for short distances only, because of the plane of section and the undulations of cell boundaries. The sparse distribution of ribonucleoprotein granules in the pale cell was in complete contrast to the dense packing of the protein aggregates in the remaining two cells. Particularly in the intermediate cell (Fig. 6, Dl), the granules were in the form of small clusters that lay on, as well as between, the short, parallel membranes that bounded the cisternae of the endoplasmic reticulum. Although the cisternae lay in various planes throughout the cytoplasm, adjacent cisternae in localized areas tended to have a similar orientation. In one cell some cisternae formed a whorl-like structure of agranular membranes (Fig. 6, Dl). The profiles of mitochondria of the nerve cells were circular or ovoid in shape and showed well-defined internal cristae. Mitochondria in the dark cells had an over-all electron-dense internal structure compared with those in the pale cells. The cytoplasm of the satellite cells contained similar elements, and, in addition, a number of small vesicular structures were evident. Small vesicles were seen close to the nuclear membrane of the satellite cell (Fig. 7). Elongated cisternae of the endoplasmic reticulum were present in the cytoplasm, and a duplication of the satellite-cell membrane was evident on the aspect of the cell opposed to the neuron body. Many of the cytoplasmic organelles and inclusions that were found in trigeminal nerve cells are displayed in Figure 7 and include mitochondria, Nissl bodies, elements of the Golgi apparatus, dense inclusion bodies, and neurofilaments. In Figure 7 mitochondria vary considerably in size and are most evident in the cytoplasm that intervenes between adjacent masses of Nissl substance. They have pale interiors, in contrast to the darker mitochondria of the satellite cell. All gradations in shape between circular and elongated outlines were noted, and they were bounded by distinct limiting membranes, from which were derived the shelflike mitochondrial crests
5 FIG. 5. Trigeminal neurons in a 4-day-old rat, showing a pale cell (PC) and parts of four dark cells (Dl-D4). An unmyelinated axon (A) can be seen at the upper part of the pale cell, separated from a group of similar axons (AX) by an elongated fibroblast (F). Myelinated nerve fibers (M) are visible, and a small blood vessel (V) lies close to the surface of the nerve cells. (Orig. mag. X3870.) Fre. 6.-An enlargement of the area outlined in Fig. 5, to show greater detail of the distinction between the cytoplasm of the pale cell (PC) and the darker cells (Di and D2). Double nuclear membranes are seen toward the top and bottom of the micrograph. The undulating nerve-cell boundaries (arrows) are separated by thin zones of satellite-cell cytoplasm (Si and S2). That (Si) between the pale cell and its neighbor (Dl) shows a number of tiny vesicles. Mitochondria (M) and protein granules are abundant in the dark cells. (Orig. mag. X 11,300.) FIG. 7.-Part of a nerve-cell body and a satellite cell (S) in the trigeminal ganglion of a 4-day-old rat. Within the nerve cell are found mitochondria (M), Nissl bodies (NB), elements of the Golgi apparatus (G), and dense inclusion bodies (L). A cluster of vesicles (V) occupies a juxtanuelear position in the satellite cell, whose limiting membrane is layered (arrows). (Orig. mag. x )
6 Vol. 42, No. 4 NERVE AND SATELLITE CELLS IN GANGLION 995 that incompletely subdivided each mitochondrial cavity. Usually the cristae were arranged at right angles to the long axes of the mitochondria (Fig. 7). Nissl bodies (Figs. 7-9) consisted of discrete aggregates of ribonucleoprotein particles, often in the form of tiny rosettes of 5-7 particles arrayed on or between parallel membranes of the endoplasmic reticulum. The boundaries of the Nissl bodies were somewhat indistinct, at the electron-microscope level of magnification, as a direct result of their particulate nature. Some appeared as discrete bodies, while others merged imperceptibly into one another. The double membranes, which formed an essential part of the Nissl body structure, were scattered randomly throughout the Nissl substance, and individual lamellae could be traced for only a short distance (Fig. 8). Sometimes, however, the lamellae showed a definite degree of orientation and consisted of double membranes, which formed a layered series of parallel, flattened cisternae (Figs. 6, 9). The lumina of the cisternae were freely interconnected and, at the sites where branching occurred, occasional dilatations were observed. High-magnification electron micrographs showed that, for the most part, the characteristic clusters of ribonucleoprotein granules of the Nissl substance were dispersed evenly throughout the cytoplasm between adjacent cisternae, rather than a linear distribution of the granules along the surfaces of the endoplasmic membranes. Elements of the Golgi apparatus were not observed in a particular location of the nerve cells but appeared to be widely scattered throughout the cytoplasm (Figs. 7, 8, 10). Each mass consisted of a number of narrow, smooth-membraned cisternae that were closely packed together. The extremities of some of these slightly curved vacuoles were distended (Fig. 10), and marked enlargement of the cisternae (Fig. 7) may have been an artifact appearance. Associated with the elongated cisternae, which were fenestrated, there were considerable numbers of small, circular microvesicles. None of the vacuoles of the Golgi apparatus possessed granules comparable with the protein particles of the Nissl substance. The long axes of the larger vesicles of the Golgi elements were not oriented in any constant direction with reference to the nuclear or cell membranes but lay parallel to them (Fig. 8), or at right angles to the general direction of the much folded nuclear membrane, in which could be seen nuclear pores (Fig. 10). Dense inclusion bodies were noted in some neurons and satellite cells (Figs. 7, 9). Those with a homogeneous structure and devoid of a limiting membrane were considered to be lipoid droplets. Others that showed evidence of an internal structure, as well as a limiting membrane, were thought to represent some stage in mitochondrial formation or function. In areas of the cytoplasm between adjacent Nissl bodies, especially where the formed elements were few in number, fine threadlike neurofilaments formed a delicate meshwork (Fig. 9). They crossed one another repeatedly and appeared to be homogeneous and agranular throughout their length. Because of the thinness of the tissue sections, coupled with their irregular course, the neurofilaments could be traced for only short distances. DISCUSSION The features of nerve cells that have been described in the foregoing account establish a set of criteria that will be of value in the analysis of the results of experimental interference with the trigeminal pathway. The fine structure of mammalian trigeminal
7 ... FIG. 8.-Cytoplasm of a nerve cell in the trigeminal gangijon of a 3-day-old rat, demonstrating the form of Nissl bodies (NB). Ribonucleoprotein granules are clustered around short, parallel membranes of the endoplasmic reticulum (arrows). Other organelles include mitochondria (M) and elements of the Golgi apparatus (G). The margin of the nucleus (N) can be seen at the lower right of the figure. (Orig. mag. X 14,000.) FIn. 9.-A Nissi body in a trigeminal nerve cell of a 48-day-old rat. The two components are seen clearly, viz., the interconnecting cisternae of the endoplasmic reticulum (ER), between which are small aggregates or rosettes of protein granules (RP). In areas of cytoplasm devoid of Nissl substance, mitochondria (M), or dense bodies (L), fine neurofilaments (arrows) form a delicate meshwork. (Orig. mag. X26,500.) Fie. 10.-Agranular membranes of the Golgi apparatus in a trigeminal nerve cell for a 4-day-old rat. A series of flattened cisternae (C) shows dilatations, and a number of microvesicles (MV) are evident. In addition to mitochondria (M), note the folded nuclear membrane (N) with nuclear pores (arrows). (Orig. mag. X 18,900.)
8 Vol. 42, No. 4 NERVE AND SATELLITE CELLS IN GANGLION 997 neurons has not been described previously in the literature. The current study has emphasized the close structural and, hence, functional affinities between these cells and those of the dorsal root ganglia of spinal nerves. The form of mitochondria, Nissl bodies, elements of the Golgi apparatus, and neurofilaments closely resemble those described in cells of spinal ganglia2 and the cerebellar cortex and medulla oblongata.5 Nissl bodies, considered by many to be the structural basis for protein synthesis in the nerve cell, are a prominent feature in trigeminal neurons, and they consistently have a distinctively organized form, although their profiles of endoplasmic reticulum are seldom as highly oriented as described for motor neurons.3 The double nuclear membrane of the trigeminal neuron varies considerably in appearance, from a curved, slightly undulating outline (Figs. 5, 8) to a type that is markedly folded, with the formation of deep indentations (Figs. 4, 10). Likewise, the cell membrane may be elaborately modified (Figs. 6, 7), to a degree that masks the exact position of the cell surface. Similar indentations of the neuron surface, with resultant interdigitation with its satellite cells, have been noted in spinal ganglion cells by Palayl7 and may be associated with the transfer of nutritional materials between the nerve cell and the intercellular spaces, through the medium of the surrounding satellite cytoplasm. The small vesicular structures that have been seen in the satellite cells of the trigeminal ganglion may be involved in this transfer mechanism, for similar vesicles (680 A diameter) have been described by De Robertis and Bennett18 in the satellite cells of sympathetic neurons and were thought to be important in the exchange of materials from one cell surface to another. In this investigation no conclusive evidence has accumulated that confirms the presence of myelin sheaths around the surface of trigeminal neurons, such as has been reported by Scharf,'9 using special staining techniques and polarized light. Rosenbluth and Palay9 have shown clearly that perikaryal myelin sheaths exist around the cell bodies of the eighth cranial nerve ganglion, consisting of multiple layers of Schwann cell cytoplasm, of compact myelin lamellae, or a combination of both forms. In association with some of the cells of the trigeminal ganglion, a layering of the satellite-cell membrane adjoining the neuron surface has been observed (Fig. 7). However, thus far, this has always been a simple formation, and compact myelin has not been seen during the examination of a large number of trigeminal neurons, although adjacent satellite cells often meet and overlap one another in a complex fashion. The interpretation of this aspect of satellite-cell structure is being continued, and the findings will be the subject of a future communication. One of the principal points of interest that have arisen from the present study is the existence of two distinct morphologic types of neuron in the trigeminal ganglion, which depend on the over-all electron density of the cell cytoplasm imparted by the distribution of organelles and inclusions. Two corresponding types of cells-light and dark cells-have been distinguished in spinal ganglion cells by Dawson, Hossack, and Wyburn2 on the basis of the different distribution of the Nissl substance. In their light cells the Nissl substance formed discrete aggregates of dense material, while in the dark cell the Nissl substance was dispersed evenly throughout the cytoplasm. Two cell types have been described in the acoustic ganglion by Rosenbluth,10 viz., granular and filamented neurons, the latter of which was ensheathed by a layer of compact myelin.
9 998 DIXON.7. dent. Res. July-August IP6.3 Trigeminal neurons appear to conform to the types described in spinal ganglia, for the dark type of cell shows an abundance of ribonucleoprotein granules throughout the cytoplasm, in contrast to the reduced concentration of ribosomes and the occurrence of granule-free zones in the paler type of cell. It has been suggested that these appearances may be a result of improper fixation.10 However, pale and dark cells have been seen in a single area, and the nuclei of both types have a normal, well-fixed appearance. Reference to light-microscope preparations shows that, after hemotoxylin and eosin staining, as well as in material stained with cresyl violet, two types of nerve cell can be distinguished. These are large cells with coarse cytoplasmic granules and smaller cells possessing a more homogeneous cytoplasm. Small cells in spinal ganglia have been considered to play a visceral afferent function (Crosby, Humphrey, and Lauer0), or they may represent postganglionic parasympathetic cells (Kure, Saegusa, Kawaguchi, and Shiraishi20) concerned with trophic functions, sweat secretion, and peripheral vasodilation (Sheehan21). In the trigeminal ganglion similar explanations seem probable, especially in view of the significant number of unmyelinated nerve fibers that have been found in the ganglion.'4 A study of normal ganglia will aid, but not solve, this problem. Currently an attempt is being made to investigate experimentally the exact relationship of these nerve-cell and fiber types. SUMMARY Electron micrographs were prepared from ultrathin sections of normal trigeminal ganglia, which were removed from rats, whose ages ranged fom 3 to 48 days, to determine the fine structure of neuron-cell bodies and their related satellite cells. The findings were correlated with light-microscope preparations that had been stained by routine histologic methods. Cytoplasmic features that were examined included mitochondria, Nissl bodies, the Golgi apparatus, dense inclusion bodies, and neurofilaments. These were compared with corresponding structures in the satellite cells. Two morphologically distinct nerve-cell types were recognized, viz., dark cells, with an abundance of ribonucleoprotein granules throughout the cytoplasm, and pale cells, in which the granular material formed discrete aggregations. The possible correlation between the two cell types and the presence of myelinated and unmyelinated nerve fibers in the ganglion are discussed. The author is indebted to Dr. W. R. Ingram, Professor and head of the Department of Anatomy, University of Iowa, Iowa City, for the provision of the excellent facilities that enabled this study to be carried out. REFERENCES 1. BEAMS, H. W., BREEMEN, V. L. VON, NEWFANG, D. M., and EVANS, T. C. A Correlated Study on Spinal Ganglion Cells and Associated Nerve Fibers with the Light and Electron Microscopes, J. comp. Neurol., 96:249-81, DAWSON, I. M., HOSSACK, J., and WYBUIRN, G. M. Observations on the Nissl's Substance, Cytoplasmic Filaments and the Nuclear Membrane of Spinal Ganglion Cells, Proc. roy. Soc. B., 144: , PALAY, S. L., and PALADE, G. E. The Fine Structure of Neurons, J. biophys. biochem. Cytol., 1:69-88, PEASE, D. C., and BAKER, R. F. Electron Microscopy of Nervous Tissue, Anat. Rec., 110:505-29, 1951.
10 Vol. 42, No. 4 NERVE AND SATELLITE CELLS IN GANGLION PALAY, S. L. Structure and Function in the Neuron. In Progress in Neurobiology. 1. Neurochemistry, ed. S. KOREY and J. I. NURNBERGER, chap. 6, pp New York: Hoeber, CROSBY, E. C., HUMPHREY, T., and LAUER, E. W. In Correlative Anatomy of the Nervous System, pp New York: Macmillan Co., DEITCE, A. D., and MURRAY, M. R. The Nissl Substance of Living and Fixed Spinal Ganglion Cells. 1. A Phase Contrast Study, J. biophys. biochem. Cytol., 2:433-44, ANDERSON, E., and BREEMEN, V. L. VON. Electron Microscopic Observations on Spinal Ganglion Cells of Rana pipiens after Injection of Malononitrile, J. biophys. biochem. Cytol., 4:83-86, ROSENBLUTH, J., and PALAY, S. L. The Fine Structure of Nerve Cell Bodies and Their Myelin Sheaths in the Eighth Nerve Ganglion of the Goldfish, J. biophys. biochem. Cytol., 9:853-77, ROSENBLUTH, J. The Fine Structure of Acoustic Ganglia in the Rat, J. Cell. Biol., 12:329-59, MERRIAM, R. W., and KOCH, W. E. The Relative Concentration of Solids in the Nucleolus, Nucleus and Cytoplasm of the Developing Nerve Cell of the Chick, J. biophys. biochem. Cytol., 7:151-60, DIXoN, A. D. Sensory Nerve Terminations in the Oral Mucosa, Arch. oral Biol., 5:105-14, The Position, Incidence and Origin of Sensory Nerve Terminations in Oral Mucous Membrane, ibid., 7:39-48, Ultrastructure of Nerve Fibers in the Trigeminal Ganglion of the Rat, J. Ultrastruct. Res., 8:107-21, PALADE, G. E. A Study of Fixation for Electron Microscopy, J. exp. Med., 95:285-98, LUSE, S. A. Fixation and Embedding of Mammalian Brain and Spinal Cord for Electron Microscopy, J. Ultrastruct. Res., 4:108-12, PALAY, S. L. Contributions of Electron Microscopy to Neuroanatomy. In New Research Techniques in Neuroanatomy, ed. W. F. WINDLE, pp Springfield:Thomas, DE ROBERTIS, E. D. P., and BENNETT, H. S. A Submicroscopic Vesicular Component of Schwann Cells and Nerve Satellite Cells, Exp. Cell Res., 6:543-45, SCHARF, J. H. Sensible Ganglien. In Handbuch der mikroskopischen Anatomie des Menschen, ed. W. VON MOLLENDORF and W. BARGMANN, p Berlin: Springer-Verlag, Kupti, K., SAEGUSA, G., KAWAGUCHI, K., and SHIRAISHI, K. On the Parasympathetic (Spinal Parasympathetic) Fibers in the Dorsal Roots and Their Cells of Origin in the Spinal Cord, Quart. J. exp. Physiol., 20:51-66, SHEEHAN, D. On Myelinated Fibers in the Spinal Nerves, Anat. Rec., 55:111-16, 1933.
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