J. Anat. (1983), 137, 1, pp. 71-83 71 With 10 figures Printed in Great Britain Do the Purkinje cells have a special type of oligodendrocyte as satellites? R. A. F. MONTEIRO* Department of Anatomy, Medical School, University of the Witwatersrand, Hospital St., Johannesburg 2001, South Africa (Accepted 25 October 1982) INTRODUCTION In a recent study on the structure and distribution of all common glial cell types in the cerebellar cortex of the rat, it was concluded that the presence of two types of oligodendrocytes is a constant feature (Monteiro, 1981). In the cerebellar cortex of other species, Mugnaini (1972) has reported a variant of oligodendrocytes (with paler nuclei) which according to him appears only occasionally. No special relation- ship has yet been described between different types of cerebellar cortex oligodendro- cytes and specific types of neuronal elements. Further studies on the distribution of both types of oligodendrocytes within the layers of the cortex, and at several levels in these layers, have now been carried out. An attempt was undertaken to correlate any preponderance of an oligodendrocyte type with particular neuronal cell bodies or processes found in the same region. The results strongly suggest that there is a close anatomical relationship between one of the two types of oligodendrocytes and the Purkinje cells. MATERIALS AND METHODS Preparation of tissue Six adult male Sprague-Dawley rats, 13 months old, were perfused, through the heart, with 2-5 % glutaraldehyde in 0 1 M S0rensen's phosphate buffer (pH 7 3) con- taining 0.1 % sucrose. Samples from Crus I and II were removed and immersed in the same fixative for two further hours. The samples were rinsed overnight in the same buffer (0-2 M), the pH of which was lowered to 6-9 by adding sodium dihydro- gen phosphate solution; sodium chloride was added to 0 5 %. Secondary fixation was carried out in 1 % osmium tetroxide in the same buffer (0-2 M) at pH 7-3 for 1 hour at 0-4 °C followed by another hour at room temperature. After a brief wash in the above mentioned rinsing solution, the tissue was dehydrated in ethanol, passed through propylene oxide and embedded in Epon 812 according to Luft's method (1961). Ultrathin sections were doubly stained with uranyl acetate (saturated solution in 50 % methanol) for 15 minutes and lead citrate (Reynolds, 1963) for 7 minutes. The grids were used for ultrastructural studies and for counting purposes. Statistical analysis The percentages of oligodendrocytes among all common glial cell types were calculated from counts of cells sectioned through the nuclei. Precautions were taken * Present address: Department of Anatomy, Institute of Biomedical Sciences, University of Oporto, Largo Professor Abel Salazar, 2, 4000 Porto, Portugal.
Transcript
J. Anat. (1983), 137, 1, pp. 71-83 71With 10 figuresPrinted in Great Britain
Do the Purkinje cells have a special type ofoligodendrocyte as satellites?
R. A. F. MONTEIRO*Department ofAnatomy, Medical School, University of the Witwatersrand,
Hospital St., Johannesburg 2001, South Africa
(Accepted 25 October 1982)
INTRODUCTION
In a recent study on the structure and distribution of all common glial cell typesin the cerebellar cortex of the rat, it was concluded that the presence of two typesof oligodendrocytes is a constant feature (Monteiro, 1981). In the cerebellar cortexof other species, Mugnaini (1972) has reported a variant of oligodendrocytes (withpaler nuclei) which according to him appears only occasionally. No special relation-ship has yet been described between different types of cerebellar cortex oligodendro-cytes and specific types of neuronal elements.
Further studies on the distribution of both types of oligodendrocytes within thelayers of the cortex, and at several levels in these layers, have now been carried out.An attempt was undertaken to correlate any preponderance of an oligodendrocytetype with particular neuronal cell bodies or processes found in the same region. Theresults strongly suggest that there is a close anatomical relationship between one ofthe two types of oligodendrocytes and the Purkinje cells.
MATERIALS AND METHODS
Preparation of tissueSix adult male Sprague-Dawley rats, 13 months old, were perfused, through the
heart, with 2-5 % glutaraldehyde in 0 1 M S0rensen's phosphate buffer (pH 7 3) con-taining 0.1 % sucrose. Samples from Crus I and II were removed and immersed inthe same fixative for two further hours. The samples were rinsed overnight in thesame buffer (0-2 M), the pH of which was lowered to 6-9 by adding sodium dihydro-gen phosphate solution; sodium chloride was added to 0 5 %. Secondary fixation wascarried out in 1 % osmium tetroxide in the same buffer (0-2 M) at pH 7-3 for 1 hourat 0-4 °C followed by another hour at room temperature. After a brief wash in theabove mentioned rinsing solution, the tissue was dehydrated in ethanol, passedthrough propylene oxide and embedded in Epon 812 according to Luft's method(1961). Ultrathin sections were doubly stainedwith uranyl acetate (saturated solutionin 50% methanol) for 15 minutes and lead citrate (Reynolds, 1963) for 7 minutes.The grids were used for ultrastructural studies and for counting purposes.
Statistical analysisThe percentages of oligodendrocytes among all common glial cell types were
calculated from counts of cells sectioned through the nuclei. Precautions were taken* Present address: Department of Anatomy, Institute of Biomedical Sciences, University of Oporto,
Largo Professor Abel Salazar, 2, 4000 Porto, Portugal.
R. A. F. MONTEIRO
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Fig. 1. Cell bodies of granule cells (G) surrounding one oligodendrocyte Type I. Note that thenucleus (N) of the glial cell is eccentric, the nuclear contour is smooth and the perinuclearcistema (straight arrows) and the nuclear pores (curved arrows) are clearly visible. The granulecell nuclei exhibit rough contours and unclear perinuclear cisternae. x 17000.
Fig. 2. An oligodendrocyte T)pe I of the granular layer. The nucleus (N) is eccentric andelliptical. x 11000.Fig. 3. An oligodendrocyte Type II of the molecular layer. Note that the cytoplasm is moreelectron-dense and the perinuclear cistema wider than in oligodendrocytes Type I (see Figs. 1and 2). The nucleus (N) has an irregular outline. Arrow, dense body. x 18000.
73
not to count the same cell more than once. The cells of Bergmann and the cells ofFananas were omitted from consideration. The distribution of oligodendrocytes inthe associated white matter was also studied for purposes of comparison.The standard error (S.E.) of percentages was obtained with the formula
S.E. = j(P(O-P))
where P is the percentage and n is the total number of glial cells counted in a certainarea. The comparison between the percentages (P1 and P2) was carried out by ana-lysing the standard error of the difference (S.E.D.):
S.E.D. = (Pi(lOOJiP) +P2(1 P2))
ni n2
Then, the critical ratio, i.e. z = (jP1_ P2J)/(S.E.D.) was examined by a 'two-tailed'test with a Z probability table.
Because the molecular layer lacked ordinary astrocytes, in comparing the percent-age of oligodendrocytes in this layer with the percentages of these cells in thegranular layer and white matter, astrocytes were included in the total in one set ofcalculations, but excluded in a recalculated second set. Both sets of figures were usedfor these comparisons.
RESULTS
Ultrastructure of oligodendrocytesAll the oligodendrocytes showed polymorphic contours. The nuclei had a smooth
outline and were rounded, elliptical (Figs. 1, 2) or irregular in shape (Fig. 3). Theyhad many chromatin granules, clumped either throughout the nucleoplasm or againstthe nuclear membrane. The fibrous lamina was thin. Characteristically, the peri-nuclear cisterna was clearly visible as were the nuclear pores (Fig. 1). In most casesthe cytoplasm had accumulated at one side of the cell where the majority of theorganelles were found. A considerable number of the processes arose from thisregion. The cytoplasm was, as a rule, electron-dense chiefly owing to the presenceof large numbers of microtubules, rather than to an abundance of ribosomes. Never-theless, the oligodendrocytes were the glial cells which had the larger content ofribosomes, whether free, as rosettes, or attached to the endoplasmic reticulum.Cisternae of rough endoplasmic reticulum were mostly short and dilated, withclear contents (Fig. 4). The cells lacked filaments, and dense bodies (Fig. 3) werefrequent.The two types of oligodendrocytes encountered were arbitrarily designated as
Types I and II. When compared with Type II cells, oligodendrocytes of Type I(Figs. 1, 2, 6) exhibited paler cytoplasm and nuclei; the latter were usually rounded
Fig. 4. An oligodendrocyte Type II showing a clearly visible perinuclear cisterna (straightarrows), one pore (curved arrow) and a narrow fibrous lamina beneath the nuclear membrane.Note in the nucleus (N), the heavily clumped heterochromatin and in the cytoplasm, the plentifulribosomes and rough endoplasmic reticulum forming short and dilated cistemae filled withclear contents. x 29000.Fig. 5. Interstitial form of microglia. Note the poorly visible perinuclear cistema and the rela-tive lack of contrast between the two kinds of chromatin in the nucleus (N). The characteristicaggregation of dense bodies (d) is obvious, as is the presence of long and narrow cisternae ofrough endoplasmic reticulum (arrows) filled with dark contents. x 14000.
74 R. A. F. MONTEIRO
Oligodendrocytes of Purkinje cells 75
or elliptical. The cisternae of rough endoplasmic reticulum were frequently shorterand less numerous. In the majority of cases, the ribosomes were more evenly dis-persed and the heterochromatin was less clumped. In oligodendrocytes of Type II(Figs. 3, 4, 6, 7, 8, 9) the nuclei were generally much more irregular in shape, some-times with bizarre configurations, the perinuclear cisternae were wider, and hetero-chromatic masses were heavily clumped, contrasting strongly with zones which wererich in euchromatin. The cell outline was more irregular than that of Type I cells.Long cisternae of rough endoplasmic reticulum with a parallel arrangement weremore common in Type II cells. The latter cells frequently were in contact with thecell bodies and processes (Fig. 7) of Purkinje cells.
Precautions were taken not to confuse Type I cells with granule cells (Fig. 1), andType II cells with interstitial forms of microglial cells (Fig. 5). In the first case, theshape and size of Type I cells and those of granule cells were often similar, so thatthe relatively unclear perinuclear cisternae and the roughly contoured nuclearmembrane of the granule cells became important features in identification. Apartfrom this, the granule cells were poorer in endoplasmic reticulum than were Type Icells. In the second case, although microglial cells, like Type II cells, were dark inappearance, they were generally smaller and had a limited number of ribosomes(Fig. 5). In addition, microglial cells exhibited perinuclear cisternae which were notso evident, and dense bodies were more frequently seen. Characteristically, the latterstructures were closely agglomerated. The presence in microglial cells of a few longnarrow units of rough endoplasmic reticulum, filled with dark contents, alloweddistinction between them and oligodendrocytes Type II.
Distribution of oligodendrocytesData on the distribution of oligodendrocytes are provided in Table 1.In the cerebellar cortex as a whole, oligodendrocytes of Type I were much more
numerous than those of Type II. The same was true for the granular layer, but thereverse pertained in the molecular layer. Hence, the larger number of Type I cellsfound in the whole cortex was derived from the relative abundance of these cells inthe granular layer.Within the granular layer itself a progressive increase in the percentage of Type I
cells was evident from the superior to the inferior level. On the other hand, a decreasein the percentage of Type II cells was observed.The statistical analysis of the percentages of oligodendrocytes of Types I and II
in the cortex and associated white matter is summarized in Table 2.In only one case, that of the comparison between Type II cells in the inferior
molecular and superior granular layers (see Table 2), was the statistical result affectedby exclusion of astrocytes from the calculations. The result obtained when astrocyteswere omitted was the one considered in the interpretation presented in the Discussion,because the percentage of Type II cells is otherwise under-estimated for the layerwhich does contain astrocytes.
Fig. 6. Oligodendrocytes of both types (Type I, OII; Type II, Ol11) in close contact. Thedifferences in cytoplasmic tone, nuclear outline and the degree of chromatin clumping areevident. The Type I cell presents here an unclear perinuclear cisterna, but the nuclear contourretains a smooth appearance. x 22000.Fig. 7 An oligodendrocyte Type II (N, nucleus) contacting a dendrite of a Purkinje cell (Pd).x 23000.
Fig. 8. An accumulation of oligodendrocytes Type II (arrows) in the superior granular layerwithin the infraganglionic plexus of the recurrent collaterals of Purkinje cells. V, vessel dis-tended by the perfusion process. x 5000.Fig. 9. An oligodendrocyte Type II showing the irregular contour of the nucleus (N) and con-tacts with myelinated axons (M) of the infraganglionic plexus. x 15000.
Oligodendrocytes of Purkinje cells
Table 1. Crude counts and percentages (±2 S.E.) of oligodendrocytes Types I and 11,in relation to all common glial cell types, in the cerebellar cortex and in the associatedwhite matter of the rat
Number of grids scanned: 100.Total number of glial cells counted (including pericytes): 971, cortex; 230, white matter.(*), recalculated percentages.
Table 2. Statistical differences between the percentages of oligodendrocytes Types Iand II in the layers and levels of the cerebellar cortex and in the associated whitematter of the rat
Type I Type II Type I Type IIcells cells cells cells
Superior granular layer P < 0 001 P < 0 001 White matter versus P < 0 001 P < 0-001versus middle granular whole granular layerlayer
Superior granular layer P < 0001 P < 0001 White matter versus P < 0-001 P < 0001versus inferior granular superior granular layerlayerMiddle granular layer NS NS White matter versus P < 0-001 NSversus inferior granular middle granular layerlayer
Inferior molecular layer P < 0001 White matter versus P < 0-001 NSversus superior P < 0 001 inferior granular layergranular layer NS (*)
Inferior molecular layer P < 0-001 P < 0 001 White matter versus P < 0-001 P < 0 001versus middle granular inferior molecular layerlayer
Inferior molecular layer P < 0 001 P < 0 001versus inferior granularlayerNS = not significant.(*), result obtained from recalculation ignoring astrocyte population. (This is the only case in which
P was affected by this recalculation.)
DISCUSSION
The cerebellar cortex is not rich in glial cells (Testut & Latarjet, 1948; Marini-Abreu, 1973) but all three neuroglial cell types are nevertheless present.
Oligodendrocytes are a glial entity well described at both the ultrastructural(Schultz, 1964; Wendell-Smith, Blunt & Baldwin, 1966; Kruger & Maxwell, 1966;Maxwell & Kruger, 1966; Mori & Leblond, 1970; Mugnaini, 1972; Palay & Chan-Palay, 1974; Constantinides, 1974; Sturrock, 1981; and others) and the light micro-
79
R. A. F. MONTEIRO
V/P
Fig. 10. A hypothetical diagram showing the possible relationship between oligodendrocytesType II (black spots) and Purkinje cells. The approximate relative proportions of oligodendro-cytes Type II found in the various zones of the cerebellar cortex and in the white matter arerepresented (see Table 1). ml, molecular layer; gl, granular layer; wm, white matter; P, Purkinjecell; curved arrow, supraganglionic plexus; straight arrow, infraganglionic plexus.
scopical levels (Cammermeyer, 1960, 1966; Mori & Leblond, 1970; Ling et al. 1973;Sturrock & McRae, 1980; and others). Pessacq (1964), however, raised doubts as towhether these cells and astrocytes constituted a single cell type or not. Furthermore,the relationship between oligodendrocytes and myelin sheaths, confirmed by Hirano(1968), is universally accepted.
It is generally agreed that the Purkinje cells have special astrocytes as satellites -the cells of Bergmann and the cells of Fananas. Mugnaini (1972) did not differentiatebetween these two types of cells, because he considered that the Fananas cells areBergmann cells displaced to the inferior molecular layer; Penfield (1965) was of thesame opinion. Petersen (1969), however, believed that only the Fan-anas cells aretruly satellites of the Purkinje cells. A related question is whether the Purkinje cellshave a special kind of oligodendrocyte as satellites as well. In the rat, the existenceof two different types of oligodendrocytes has now been revealed. The distinction isnot artifactual because they co-exist in the same areas, sometimes even in close con-tact (Fig. 6). The variability of oligodendrocytes has indeed been observed by anumber of workers (Kruger & Maxwell, 1966; Mori & Leblond, 1970; Mugnaini,1972; Ling et al. 1973).Mugnaini (1972) described two types of oligodendrocytes but in a different species,
the cat. In the present study, Type II cells seem to correspond to Mugnaini's commontype, being similar in shape, chromatin pattern and distribution of ribosomes.However, neither Type I nor Type II cells of this study fit Mugnaini's description ofan oligodendrocyte variant with paler nuclei. Compared with this variant form, thecytoplasm of Type I cells have an analogous tone, but more electron-dense nucleiin which the chromatin is more clumped; the shape of the nuclei and the cell bodies
80
Oligodendrocytes of Purkinje cells 81themselves are more irregular in Mugnaini's variant than in Type I cells. Besides,the latter are far more numerous than that variant, which is rare.The oligodendrocytes seen in the present study are not evenly dispersed. Fox,
Hillman, Siegesmund & Dutta (1967) observed, in the monkey, that oligodendro-cytes are rarely found in the molecular layer and that they are concentrated in thetransitional zone between the granular and molecular layers. Mugnaini (1972), whoused the cat and the chicken, agreed that oligodendrocytes are sparse in the molecularlayer, being more abundant in its inferior level. The results of the present study onthe rat are in accord with the above observations. However, neither Mugnaini nor Foxet al. mentioned any special type of oligodendrocyte as being abundant in this region.
There is a significant difference in the distribution of Type II cells between theinferior molecular and superior granular layers, on the one hand, and the remaininggranular levels, on the other. This is noteworthy because the myelinated supra- andinfraganglionic plexuses of the recurrent collaterals of Purkinje cell axons are presentin the inferior molecular and superior granular layers, respectively. Chan-Palay(1971) stated that the supraganglionic plexus is rudimentary; the infraganglionicplexus is, however, extensive. Because the oligodendrocytes are necessary for my-elination of the recurrent collaterals, it would be expected that oligodendrocytesType II would be significantly more numerous in the superior granular layer. Never-theless, this appears not to be so. Because, in this study, it- has been shown thatoligodendrocytes Type II frequently are in contact with cell bodies, axons and den-drites of the Purkinje cells, it is contended that they are satellites of these cells. Thosecontacting the dendrites of Purkinje cells could account for the unexpectedly highpercentage of Type II cells in the inferior molecular layer. Furthermore, there isno statistically significant difference in the percentage distribution of Type II cellsbetween the middle and inferior granular levels or between either of them and thewhite matter. To explain this, it is suggested that Type II cells in these regionsmyelinate the continuations of the Purkinje cell axons, the collaterals of which formonly a sparse plexus at these levels.A comparison of the percentages of Type IL cells between the superior molecular
layer and other regions is unrewarding because there are so few neuroglial cells, and,in particular, so few oligodendrocytes, present in the superior molecular layer.Therefore, it does not seem reasonable to seek any relationship between the per-centages of Type II cells and anatomical features in the superior molecular layer.The percentages of Type I cells in the middle and inferior levels of the granular
layer are significantly different from those found in the superior granular and inferiormolecular layers. It should be pointed out that, in the middle and inferior levels ofthe granular layer, the mossy and climbing fibres are predominantly myelinated. Thepercentage of Type I cells is lower in the superior granular layer where the fibresare, for the most part, unmyelinated. It must be stressed that Type I cells discloselittle affinity for the recurrent collaterals of the Purkinje cells, i.e. the lowest percen-tage of Type I cells within the granular layer occurred in the superior level, wherethe most copious plexus is located. In the associated white matter, Type I cells are sig-nificantly in excess of those found in any level of the cortex. This is in agreementwith the fact that probably every afferent axon is myelinated in the white matter.With regard to the levels of the molecular layer, Lange (1976) has stated that there
are some myelinated parallel fibres in the inferior level but the parallel fibres in thesuperior level are unmyelinated. This could explain why Type I cells are encounteredin the inferior but not in the superior molecular layer.
82 R. A. F. MONTEIRO
The author is tempted to conclude that oligodendrocytes Type II constitute aspecial kind of glial cell and serve as satellites to Purkinje cells (see Fig. 10). Myelina-tion of axons and satellite support of other neuronal structures would depend onoligodendrocytes Type I.
SUMMARY
Two types of oligodendrocytes considered to be a constant feature in the cerebellarcortex of the rat are described. One cell type (I) exhibits rounded or elliptical nuclei,whereas the other type (II) presents more irregular nuclear and cellular contours andwider perinuclear cisternae. The latter cell type shows a more electron-dense cyto-plasm with more heavily clumped heterochromatin, contrasting strongly with theeuchromatin; also long and parallel cisternae of rough endoplasmic reticulum aremore frequent.The percentages of both types of oligodendrocytes in relation to the total popula-
tion of common glial cell types were calculated in the cortical layers and at severallevels in these layers. The distribution of oligodendrocytes in the associated whitematter was also carried out for purposes of comparison. The results provide evidencethat the Purkinje cells may have a special kind of oligodendrocyte (Type II) assatellites.
I am most grateful to Professor Ann Andrew and Dr R. M. T. Simmons for theirconstructive criticism, indispensable advice and correction of the manuscript. Thiswork was partially supported by a University Research Grant from the Universityof the Witwatersrand, Johannesburg. The paper is part of a thesis to be submittedfor the degree of Ph.D. in Medicine at the University of the Witwatersrand.
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