oligodendrocytes in the normal and chronically de-afferented lateral geniculate body of the monkey

Z. Zellforsch. 135, 115--127 (1972) © by Springer-Verlag 1972

Oligodendrocytes in the Normal and Chronically De-Afferented Lateral Geniculate Body of the Monkey

Mahdi Hasan* and Paul Glees * *

Institute of Histology and Neuroanatomy of the University of GSttingen, Germany

Received August 24, 1972

Summary. Electron microscopical examination of the norma and de-afferented 'laterall geniculate body' of the monkey following paraformaldehyde-glutaraldehyde vascular perfusion revealed distinctive morphological features of different types of oligodendrocyte. These cells were normally situated as perineuronal satellites or in relation to axons and capillaries. A wide range of nuclear and cytoplasmic densities were displayed by both satellite and interfascicular oligodendroeytes. The following distinctive features for the identification of oligodendrocytes were utilised: the presence of large quantities of free ribosomes and ribosomal rosettes, microtubular profiles, dense marginal aggregation of nuclear chromatin together with light patches and numerous nuclear pores; but the absence of broad cytoplasmic processes, glycogen and gliofibrils. Circumferential perinuclear organization of the cytoplasmic organelles was typical of oligodendrocytes. Particular attention was paid to perinenronal satellite cells in view of the known transneuronal atrophy in the de-afferented geniculato body. Some cells having a nuclear pattern of oligodendrocytes but showing hyalini- sation of perikaryon were seen in de-afferented laminae. A notable feature was the presence of variegated "osmiophilic bodies" in the perikaryon of oligodendrocytes also situated in the de-afferented laminae. A cell type combining the features of oligodendrocytes and astrocytes was classified as 'intermediate neuroglia'.

Key words: Oligodendroglia - - Monkey - - De-afferentation - - Ultrastructure - - Dense- bodies.

Introduct ion

Per ineuronal glia cells are known to respond to neuronal chromatolysis which follows t raumat ic lesion of axones (Cammermeyer, 1970; Krentzberg, 1966). These findings indicate tha t changes in nerve cells affect neighbouring microgha in a dis t inct way bu t apparent ly no other type of neuroglia. While s tudying t ransneurona l changes in the lateral geniculate body of the monkey (Glees et al., 1967), we paid special a t t en t ion to al terat ions of ohgodendrocytes closely associated with groups of principal cells of the genicnlate. The term oligodendroglia was used by del Rio- Hortega (1921) to define those neuro-ectodermal glia cells which his specific impregnat ion method showed to have comparat ively few cellular processes. Ohgodendrocyte nuclei were found to be smaller t h a n those of astrocytes and richer in chromat in content . Wi th in only three years of this classical description, Penfie]d (1924) noticed glia cells which he in terpre ted as t rans i t ional forms between oligodendrocytes and astrocytes in young mammals . Andrew and Ashworth (1945) drew a t t en t ion to some adendroglial cells related to oligodendrocytes, which they thought represented main ly satellites and some interfascicular glia. I t was

* Fellow of the Alexander yon Humboldt Foundation, on Sabbatical leave from J. Nehru Medical College Aligarh, India. * * Recipient of the "Deutsche Forschungsgemeinschaft" Grant No. G./28/15. 8*

116 M. Hasan and P. Glees:

considered that this type of glia deserved a name of its own (Glees, 1955). With the advent of electron microscopy this problem was not solved. On the contrary further complications arose. A clear specification of the range of oligodendrocyte morphology has not yet been achieved. Whereas Luse (1958, 1962) and Vogel and Kemper (1961) designated the more dense g]ia elements as astrocytes, a great majority of investigators hold the view that the oligodendrocyte exhibits comparatively greater electron-density than the astrocyte (Farquhar and Hartmann, 1957 ; Sehultz et al., 1957 ; Hartmann, 1958 ; Schultz and Pease, 1959; Bunge et al., 1960; Peters, 1960; De l~obertis and Gerchenfeldt, 1961 ; Palay et al., 1962; Gray, 1964; Gr@goire, 1963; Terry and Weiss, 1963; Coulter, 1964; Herndon, 1964; Maxwell and Kruger, 1964; Schultz, 1964; Bodian, 1964; Mugnaini and Maxwell, 1964; Kruger and Maxwell, 1966; Wendell-Smith et al., 1966; ttirano, 1968). Palay (1958) had suggested that with completely satisfactory fixation of tissue these differences would tend to disappear. This has proved only partially correct. With the development of better methods of preparation, according to Wendell-Smith et al. (1966), "the identification of macroglial cell types has been tacitly assumed, without being formally proven". Maxwell and Kruger (1965a) have at tempted to clarify the confusion by first differentiating the g]ia cells into "as t rocy t ic" and non-astrocytic" types. Astrocytes have been identified with reasonable certainty by the unique presence of glycogen granules and bundles of approximately 60 A filaments in their cytoplasm (Maxwell and Kruger, 1965 a). The striking absence of these two components in other glial elements in formaldehyde or glutaraldehyde perfused material renders it possible to classify these cell types as non-astrocytie glia. This class of cells has been further observed to display wide range of nuclear and cytoplasmic densities. Kruger and Mexwell (1966) have, therefore, subdivided it into "light" and "dark" variety with a range of intermediate forms depending upon electron density. Those elements with lighter cytoplasm and nucleus were found to be present in larger numbers than the dark variety. Both were, however, observed to be abundantly surrounded by axons and formed a typical interfascicular row of cells (Kruger and Maxwell, 1966). In experimental allergic en- cephalomyelitis Bunge et al. (1960) described "reactive macroglia" which did not conform to classical picture of either astrocyte or the oligodendrocyte. More recently Maxwell and Kruger (1966), investigating the effect of alpha particle irradiation on the oligodendrocytes of rat cerebrum, have given a detailed account of a cell-type termed as "the reactive o]igodendrocyte". Once the ultrastruetural features of oligodendrocytes (or different morphological forms of oligodendrocytes) have been clearly defined, the way for investigations of regional differences as well as of differences between animal species will be opened (Mugnaini and Walberg, 1964).

The aims of the present report are to describe the fine structure of oligodendrocytes in the lateral genieulate body (LGB) of the monkey, to investigate reactions, if any, of optic nerve terminal degeneration on its ultrastructure and to classify the different morphological forms of oligodendrocytes.

Material and Methods Some of the material used in the present study h~s been described previously and has

been reexamined (Glees et al., 1967). In addition to this three male rhesus monkeys (Macaca

Oligodendrocytes in Lateral Geniculate Body 117

mulatta, weighing 2-3 kg) were used. The left eye was enucleated from each under sodium pentobarbital anaesthesia, and the animals were allowed to survive 1 month, 3 months and 16 months. They were then killed under anaesthesia by perfusion through the heart or through the abdominal aorta with a mixture of paraformMdehyde (4%) and glutalrMdehyde (2%) at pH 7.4. The head was severed and stored in a refrigerator for 3 hours before the lateral geniculate bodies were dissected out. Slices of LGB were immersed in the same fixative for 3 hours in a refrigerator. Thin rodlets of tissue from laminae receiving fibres from the ipsi- lateral (2, 3 and 5) and contrMaterM eyes (1, 4, and 6) were dissected out and cut into small pieces of about 1 mm a. The material was rinsed in phosphate buffer and post-fixed for 2-3 hours in chilled 1% osmium tetroxide solution. The specimens were then dehydrated in acetone-water series, and at the stage of 70 % acetone stained for 12 hours with uranyl acetate (0.5%) and phosphotungstic acid (1 To). The tissue was embedded in VestopM W. Ultrathin sections were obtained with an LKB ultramicrotome, stained with lead citrate (Reynolds, 1963) and studied with Siemens Ehniskop or Zeiss EM 9A electron microscope.

Results

1. Morphological Features o] Oligodendrocytes in the Normal Laminae o/the Lateral Geniculate Nucleus

The absence of broad cytoplasmic processes, glycogen granules and gliofibrils formed the basis for the differentiation of oligodendrocytes f rom the astrocytes. The positive features for its identification were the presence of abundant free ribosomes and ribosomal rosettes, microtubules in the perinuclear cytoplasm, relatively dilated cisternae of the endoplasmic reticulum, conspicuous Golgi complex, and large dilatations of the nuclear cleft (Bodian, 1964; Sehultz, 1964; Mugnaini and Walberg, 1964; Kruger and Maxwell, 1966). The nuclear and cytoplasmic matr ix densities displayed by this class of cells, suggest two different cell types with a range of intermediate forms. Both the ' l ight ' and 'dark ' varieties were usually found to be related to axons, al though the ' l ighter oligodendrocytes ' oceured more frequently in close proximity to neurons or blood capillaries (Fig. 1). The interfascicular oligodendrocytes were usually of the "darker" type (Fig. 2). The shape of the nucleus varied markedly, depending possibly on the plane of section. Although elongated or irregular nuclei were more commonly observed, fairly round nuclei with a narrow cytoplasmic rim were also frequently apparent. The highest density of inhomogeneously distributed chromat in material was detected close to the nuclear membrane. Irregular light patches interrupted the dense ehromatin at the nuclear membrane and were usually identified as the sites of nuclear pores. Free ribosomes and ribosomal rosettes were prominent in the perikaryon. The high cytoplasmic matr ix density, however, could not be account- ed for by the abundant ribosomal content alone. I n addit ion to it, a "dark background substance" appeared to be contributing to the comparat ively high cytoplasmic matr ix density. The Golgi membranes and profiles of dilated endo- plasmie ret iculum were prominent ly displayed.

I n general, the oligodendrocytes showed densely packed perinuclear circumferential organization of the organelles.

2. Altered Morphology o/Oligodendrocytes

The response of oligodendrocytcs to terminM degeneration in those laminae of the lateral geniculate body affected by optic nerve severance m a y facilitate the


Fig. 1. An oligodendrocyte (N) in the immediate neighbourhood of a capillary (C) and neurone. N u nucleus of neurone. Scale ~ 1 micrometer.

Fig. 2. An oligodendroeyte in the neuropil. N nucleus of oligodendrocyte; C capillary. Scale ~ i micrometer

01igodendrocytes in Lateral Geniculate Body 119

Fig. 3. Two oligodendrocytes in close apposition. The arrow points out the "junction" N nucleus. Scale ~ 1 micrometer

under s t and ing of the funct ional role of these cells. W h e n sections f rom the normal and de-afferented laminae were examined a l te rna te ly , an increase in the f requency of occurrence of o] igodendroeytes in the l a t t e r was clear ly discernible. F r e q u e n t l y two ol igodendrocytes were observed in such close p r o x i m i t y t h a t no in tercel lu lar space sepa ra t ed t hem (Fig. 3).

A n increase in the size and dens i ty of the pe r ika ryon was noticeable. Poly- morphic electron-dense cy toplasmic inclusions formed the chief character is t ics of such ' reac t ive ' o l igodendrocytes . Dense bodies of this t y p e were never observed in

Fig. 4. An oligodendroeyte showing granular dense bodies in the perikaryon. Scale = 0.5 micrometer

Fig. 5. An oligodendrocyte showing an eccentric nucleus (N) and striped dense body (D) in the organelle-rich perikaryon. Scale = 0.5 micrometer

Inset shows a higher magnification of the striped "dense body". Scale = 0.25 micrometer

M. Hasan and P. Glees: Oligodendrocytes ]n Lateral Geniculate Body 121

Fig. 6. Micrograph exhibiting a part of the cytoplasm of an oligodendroeyte. Note the irregular, lamellated and elongated dense bodies, in the immediate vicinity of ~ myelin~ted axon

(A) ; er endopl~smic reticulum. Scale ~ 1 micrometer

the normal material. The internal structure of the 'dense bodies' varied markedly from amorphous to granular, lamellar or peculiarly striped forms (Figs. 4, 5).

Ribosomal rosettes and microtubules appeared prominently in the perikaryon. ~uelear alterations were, however, less obvious but the inner and outer nuclear membranes were distinctly separated. Comparatively more elongated and eccentric nuclei were discernible. Irregularly shaped and laminated "dense inclusions" were also seen in some o]igodendrocyte perikarya (Fig. 6). Occasionally a type of cell exhibiting remarkable marginal clumping of the nuclear ehromatin and hyalinization of the perikaryon was seen (Fig. 7). Such cells were usually found related to myelinated axons and often in close proximity to a neurone. Blood capillaries were not detectable in their neighbourhood. This type of cell has been tentatively classified as a "modified form of oligodendrocyte" as the marginal clumping of nuclear chromatin resembled closely the pattern commonly encount- ered in oligodendrocytes.

3. Trans i t ional F o r m o / N e u r o g l i a

At times glia cells possessing the characteristics of both the oligodendrocyte and astrocyte were observed. Clumping of nuclear chromatin and marked dila- tation of the nuclear cleft conformed to the oligodendrocyte but the elongated nuclear profile and bundles of gliofibrils in the perikaryon tilted the balance in


Fig. 7. Modified type of oligodendrocyte (0) having dense perikaryon (arrow) related to myelinated axons and a neurone (N nucleus of the neurone). Scale = 0.5 micrometer

favour of an astrocyte. On the other hand, prominent ribosomal rosettes and microtubuli typical of oligodendrocytes were also apparent (Fig. 8).

Discussion

The Diversity o/ the Morphology o/ Oliffodendroglia is Evident by the above Description and Illustrations. This raises some questions concerlling alternative classifications and the possibility of transitional forms (RamSn-Moliner, 1958). At times the oligodendrocyte exhibiting low density resembles the astrocyte closely.

Classification of oligodendrocytes into "dark" and "pale" types, on the basis of their relative electron density has been attempted. However, a cautious approach is warranted in utilising the criterion of 'electron density' alone for the classification (Kruger and Maxwell, 1966). The presence of "dark" and "pale" oligoden-

Oligodencb'ocytes in Lateral Genieul~te Body 123

Fig. 8. Electron micrograph depicting a "transitional form of neurogliM cell". The a r r o w

points out the widely separated nuclear membranes. N nucleus, ] fibrillae. ScMe ~ 0.5 micrometer

d rocytes in the same section indicates t h a t the d ivers i ty in e lec t ron-dens i ty represents a real difference. The interfascicular and satel l i te ol igodendroeytes , however, do not exhibi t apprec iable differences in the i r fine s t ruc ture in re la t ion to the i r different location. On this poin t we agree wi th the f indings of MugnMni and Walbe rg (1964). The quest ion of ident i f ica t ion of the cel l- type exhib i t ing amorphous or hyal ine pe r ika ryon is cer ta in ly difficult. The nuclear character is t ics are more in favour of an ol igodendrocyte , bu t a t angent ia l sect ion th rough an endo- thel ia l cell or a per ieyte might exhibi t a s imilar profile, a l though t rac ing a conne- xion with a b lood vessel was unsucessful. Fur the rmore , such cells were commonly sur rounded b y mye l ina t ed axones or re la ted to a neurone. On the basis of thei r

. location and fine s t ructure , the des ignat ion of a "modi f ied t y p e of o l igodendrocyte" appears more reasonable. The cel l - type exhibi t ing hya l in iza t ion of the pe r ika ryon was de tec ted in the de-afferented laminae of the la te ra l genieulate body. In i t i a l ly we considered this t y p e of cell as a modif ied per icyte or microglia. Bu t as the character is t ic features of microglia es tabl ished b y Bar6n and Gallego (1972) are found to be lacking, we believe at this s tage t ha t this cel l - type should be t e r m e d as


a modified oligodendrocyte. Furthermore, Maxwell and Kruger (1965b) have suggested that microglia are nothing more than the cells described by del Rio- Hortega (1921) as oligodendrocytes. I t seems reasonable to infer that this alter- ation might be a late sequel of the trans-neuronal degeneration caused by optic denervation or by terminal optic degeneration.

Satellite Oligodendrocytes. The oligodendrocytes observed in the vicinity of neurones constitute the perineuronal satellites. These satellite cells frequently display lower nuclear and cytoplasmic densities than the interfascicular oligodendrocytes. Earlier, De Robertis et al. (1960) have described the occurrence of two satellite oligodendrocytes side by side in the cerebral cortex of rabbit. The occasion- al occurrence of two of these satellite cells in the de-afferented laminae of the genieulate body is of particular interest. The darker nuclear density and hyalinization of the perikaryon of some of the satellites deserves special reference in view of the known transneuronal atrophic changes in the de-afferented geniculatc neurones. Until more information is available on the functional interrelationship of satellite oligodendrocytes and neurones, it is advisable to collect all the detectable morphological data which are likely to elucidate the functional significance of satellite oligodendrocytes.

Intermediate _Forms o/Neuroglia. The existence of intermediate forms of macroglia was surmised by the light microscopists using metallic impregnation techni- ques (Penfield, 1924; Ram5n-Moliner, 1958). Examining Nissl-stained material, Kryspin-Exner (1943) assumed that certain nuclei which resembled oligodendrocytes were in fact astrocytes. Intermediate forms were also reported by Cammer- meyer (1960) who used PAS-gallocyanin method. The electron microscopical analysis conducted by Farquhar and Hartmann (1957) supported these observations. Cells were found containing filaments and glycogen particles in their cytoplasm, which was elsewhere rich in ribosomes and dense organelles. These findings have been more recently reiterated by Hartmann (1962). However, Mugnaini and Walberg (1964) deny the existence of "intermediate forms" in the normal material and prefer to identify this variety of macroglia as "the organelle-rich astrocyte". Their assumption is supported by the histoehemieal study of Blunt et al. (1966). Wendell-Smith et al. (1966), agree that modulations may occur or that intermediate or bivalent forms may exist under different circumstances and in different situations. The predominant form in tissue culture (Bunge et al., 1965 ; Ross et al., 1962) and in developing kitten seems to be a bivalent form with the dense matrices of the oligodendrocytes and glycogen particles and filaments of astrocytes. Bunge et al. (1961) designated the cells exhibiting a dense cytoplasm and fibrils as "the reactive macroglia". I t is thus conceivable that bivalent forms of maerogHa may appear in response to altered environment or functional requirements. Vaughn and Peters (1968) noted a striking resemblance between the "third neuroglial" cell type of the adult optic nerve and the presumed neuroglial precursors appearing during development. They postulated that, in the adult, the multipotential glial, cells may be retained, just as the multipotential cells in other mature tissues. According to Peters et al. (1970), the multipotentiality of this third neuroglial element was indicated by the fact that in adult optic nerves undergoing Wallerian degeneration these cells appeared to increase in number, surrounded degenerating myelin and contained lipid inclusion. Maxwell and Kruger (1966) considered the

01igodendrocytes in Lateral Geniculate Body 125

dense bodies of the o l igodendrocytes to be the p roduc ts of " n o r m a l " degenera t ive processes such as those re la ted to ageing. The accumula t ion of dense bodies following i r rad ia t ion or in pa thologica l condit ions might be assumed to be the resul t of accelera t ion of the degenera t ive process associa ted wi th senescence. Dense bodies of o l igodcndroeytes have thus been ident i f ied as l ipofusein granules b y Maxwell and Kruge r (1966). I n this context , i t is of pa r t i cu la r in te res t to note t h a t " b a n d e d dense bodies" as shown in Fig. 6 have not ye t been ident i f ied in the neurones a l though var ious other morphological pa t t e rn s of l ipofuscin have been r epor t ed (Hasan and Glees, 1972). We feel certain, on account of a sys temat ic s tudy of neuronal lipofuscin, t h a t the l amina ted , h ighly organised dense bodies found in o l igodendrocytes are f undamen ta l l y different f rom lipofusein. The l a t t e r are usua l ly found to be i n t ima t e ly re la ted to mi toehondr ia or a t t imes loca ted wi th in the mi toehondr ia l profiles whereas the l amina t ed or s t r i a t ed bodies never appear to be re la ted to mi tochondr ia . They are, on the other hand, in close re la t ion to r ibosomal organelles, Their layer ing appears to imi ta te , in grossly d i s to r t ed way, myel in l amina t ion and m a y represent an abor t ive p roduc t ion of myelin, a l though glial membrane windings are not visible. Phagocytos i s of myel in b y ol igodcndrocytes has never been observed b y us. The dense bodies of oligodendroeytes might concievably be the p roduc t of a l te red metabol i sm.

Acknowledgement. We wish to thank Miss E. Heyder for the technical assistance and Mrs. Ma. del Carmen Weinrichter for typing the manuscript.

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Prof. Dr. M. Hasan Institut ffir Histologie und Neuroanatomie der UniversitAt G6ttingen D-3400 GSttingen Kreuzbergring 36 Bundesrepublik Deutschland

Prof. Dr. P. Glees Direktor des Institutes fiir Histologie und Neuroanatomie der Universitiit GSttingen D-3400 GSttingen Kreuzbergring 36 Bundesrepublik Deutschland

oligodendrocytes in the normal and chronically de-afferented lateral geniculate body of the monkey

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