Cell Tiss. Res. 157, 115--124 (1975) �9 by Springer-Verlag 1975

Cell Number and Cell Density in the Cerebellar Cortex of Man and Some Other Mammals*

W. Lange

Anatomisches Institut der Universit/it Kiel

Received October 23, 1974

Summary. The number of cells per unit volume was determined in the cerebellar cortex of man and 19 other mammals. The cell density (i.e. the number of cells per unit volume) decreases from mammals with a low brain weight to those with a higher brain weight. This decrease in the number of cells is found to be proportional for all three layers of the cerebellar cortex. In addition, the ratio of Purkinje cells to granule cells was determined. In contrast to the decrease of all cell types with increasing brain weight, this ratio varies remarkably among the mammals and is not correlated with brain weight. In man, this ratio is 1:2991, while it is lower in all other mammals investigated. These differences in the ratio of Purkinje cells to granule cells and the decrease in cell density with increasing brain weight are discussed in relation to brain evolution.

Key words: Cerebellar cortex - - Man and other mammals - - Number of cells - - Evolution of cerebellar cortex - - Quantitative analysis.

I n recent years , cell dens i ty in the cerebral cor tex and in var ious subcort ical nuclei in m a n and o ther m a m m a l s has been e s t ima ted by several au thors (v. Economo, 1926; Haug , 1958; Tower, 1954; Brizzee and Jacobs , 1959; Schlote, 1959; Treff, 1964; Gunschmann, 1972; Wiedemeyer , 1974; Tjan , 1974). I n mos t of these s tudies the objec t of the counts was to ob ta in informat ion abou t the archi tec tonic fea tures and the degree of evolu t ion of the m a m m a l i a n brain. The f indings of these s tudies indicate t ha t the number of cells pe r uni t volume decreases wi th the level of evolut ion, whereas the volume f rac t ion of the neuropil , which conta ins the synap t ic connections, increases (Haug, 1967c).

I n the crebel lar cortex, cell dens i ty has been e s t ima ted only rare ly . Most inves t iga tors have ca lcula ted only the number of Purk in je cells (Kreuzfuchs, 1902, m a n ; Lodja , 1955, man ; Inuka i , 1928, r a t ; Arms t rong and Schild, 1970, rat) . Only F o x and B a r n a r d (1957), Bra i t enberg and A twood (1958), F r i ede (1963), Smol jau inov (1966), Pa lkovi t s , Magyar and Szen tago tha i (1971a, b, c) and Lange (1972) also de t e rmined the number of o ther neurons in the cerebel lar cor tex (i.e. granule cells, Golgi cells, baske t cells and s te l la te cells) in a few species (man, rhesus monkey , cat, rat) . Consequent ly , the cell dens i ty a t p resen t does not p rovide a basis for compar ing the degrees of evolu t ion in the cerebral and in the cerebel lar cortex.

Since evolu t ion of the m a m m a l i a n bra in is not res t r i c ted to the cerebral cor tex and subcor t ica l nuclei, bu t also involves o ther regions such as the cere-

Send o//print requests to: Prof. Dr. Winfried Lange, Anatomisches Institut der Universit~t D-23 Kiel, Neue Universit/it, Federal Republic of Germany. * Supported by the Deutsche Forschungsgemeinschaft.

8*

116 W. Lange

Fig. 1. (a) Parasagittal section of the cerebellar vermis in the rat. The triangle indicates the vermal part of the lobule IX, which was investigated in the rat and other mammals. (b) The three cortical layers of the cerebellar cortex are marked. Exact (]elimination of the cortical

layers is necessary in order to obtain comparable results in the different mammals

bel lum (Starck, 1955), it seems desirable to determine, whether evolut ionary phenomena in the cerebellar cortex run along the same lines as in the cerebral

cortex. Thus, in the following invest igat ion the n u m b e r of cells per un i t volume was

determined in the crebellar cortex, and compared with the data of Haug (1967c) I n addit ion, quant i ta t ive data per t inen t to the evolut ionary position of the h u m a n

brain were also sought.

Materials and Methods

The following species and number of cerebella were used for this study: Man (Homo sapiens) 5, elephant (Loxodonta a/ricana) 1, pilot whale (Globicephala makro-

rhyncha) 2, bottle-nose dolphin (Tursiops truncatus) 2, common purpoise (Phocaena phocaena) 1, horse (Equus caballus) 2, bull (Bos taurus) 2, pig (Sus domestica) 2, sheep (Ovis aries) 2, rhesus monkey (Macaca mulatta) 2, vervet monkey (Cercopithecus aethiops) 2, fox (vulpes vulpes) 2, squirrel monkey (Saimiri sciureus) 2, cat (Falls domestica) 2, rabbit (Oryctolagus cuniculus) 2, opossum (Didelphys virginiana) 2, guinea pig (Cavia cobaya) 2, hedgehog (Erinaceus europaeus) 2, rat (Rattus norvegicus) 2, mole (Talpa europaea) 2, mouse (Mus musculus domesticus) 2.

After weighing the brains and their parts (Prosencephalon, Rhombencephalon, Cerebellum), the cerebella were fixed in buffered formalin. Then the vermal part of lobule IX (uvula, Fig. I a) was removed and embedded in paraffin.

5 Ez and 10 [z sections were stained according the procedure of Einarson (1932). Cell counts in the three layers of the cerebellar cortex (Fig. 1 b) were performed according to the methods of Haug (1967a, b) and the counts corrected by the Floderus formula (1944).

Since the brains of the elephant, of the aquatic mammals, and of man could not be fixed immediately after death, it was not always possible to differentiate neurons from glial cells

Cell Number and Cell Density in the Cerebellar Cortex 117

Fig. 2. Granular layer of the cerebellum in the elephant (Fig. 2a), in the rhesus monkey (Fig. 2b), and in the rat (Fig. 2c). Note the different cell densities in the three mammals.

• 1100

118 W. Lange

ELEPHANT

RHESUS MONKEY

RAT

1000 p m w Fig. 3. Distances between Purkinje cells in the elephant, rhesus monkey and rat. Note also

the decrease in size from the larger to smaller mammals

and pericytes in the molecular layer in these brains. Consequently, only the total number of all cells was determined within this layer.

Although regional differences in the cytoarchitecture of the cerebellar cortex at this time are well known (Jakob, 1928; Brodal and Drablos, 1963; Lange, 1972; Spacek, Parizek and Lieberman, 1973 ; Lange, 1974), the cell number was determined in the uvula alone (Fig. I a). This would seem to be justified, because the mean value of the cell density in various parts of the cerebellar cortex is nearly equivalent to the number of cells per unit volume in the uvula (Lange, 1972).

Results

Comparison of the g ranu la r l ayer in the e lephan t (Fig. 2a), in the rhesus m o n k e y (Fig. 2b), and in the ra t (Fig. 2c) indica tes t ha t cell dens i ty in this layer varies cons iderably in different mammals . This dens i ty increases from the e lephant and rhesus m o n k e y to the smal ler mammal s with a lower b ra in weight. Differences in cell size among var ious m a m m a l s are not ve ry d is t inc t in this layer . As to the Purk in je cells, there is a s ignif icant increase in cell size from animals with a smal ler brain, l ike the ra t , to those with a high bra in weight (Fig. 3). Besides this, the re are r emarkab le differences in the spacing of the Purk in je cells. I n sections per- pendicu la r to the axis of the folium, the Purk in je cells all lie v i r tua l ly in the same plane. Each 1000 ~ of this plane contains 5 Purk in je cells wi th cross-sect ioned nuclei in the e lephant , 7 in the rhesus monkey , and 13 in the ra t . Differences in cell dens i ty in the molecular l ayer are not as obvious, bu t can be clear ly shown b y count ing the number of cells pe r uni t volume.

The cell numbers in the different layers of the cerebel lar cor tex and the number of Purk in je cells in the inves t iga ted m a m m a l s are summar ized in Table 1. The m a m m a l s in Table 1 are l is ted according to the weight of the cerebel lum, beginning with the e lephan t with the highest cerebel lum weight. I t is thus easy to recognize, t h a t the number of cells per uni t volume increases wi th the

Cell Number and Cell Density in the Cerebellar Cortex 119

Table 1. Number of cells per 0.001 mm a in the different layers and cell density per 0.001 mm a in the cerebellar cortex. (M.L. ~ molecular layer, P.C.L. = Purkinje cell layer, P.C. ~ Purkinje cells, G.L. = granular layer, total = number of cells per 0.001 mm 3 in the cerebellar cortex)

M.L. P.C.L. P.C. G.L. Total

Elephant 28.88 (Loxodonta a/ricana) -- 3.31

Pilot whale 30.77 (Globicephala macrohyncha) • 2.78

Bottle-nose dolphin 43.75 ( Tursiops truncatus) • 5.17

Man 27.15 (Homo sapiens) -- 1.76

Common purpoise 51.07 ( Phocaena phocaena) J_ 6.43

Horse 34.50 ( Equus caballus) -- 4.07

Bull 37.63 ( Bos taurus) -- 3.17

Sheep 42.73 (Ovis aries) • 3.87

Rhesus monkey 46.25 ( M acaca mulatta ) -- 4.59

Vervet monkey 45.26 ( Cercopithecus aethiops) • 5.12

Fox 58.62 ( Vulpes vulpes) ~- 6.32

Cat 54.38 (Felis domestica) -- 5.17

Squirrel monkey 107.67 (Saimiri sciureus) i 9.67

Rabbit 81.47 (Oryctolagus cuniculus) • 7.44

Opposum 72.25 ( Didelphys virginiana) • 6.84

Guinea pig 47.92 (Cavia cobaya) • 3.97

Hedgehog 62.70 (Erinaceus europaeus) -- 5.46

Rat 131.20 ( Rattus norvegicus) -[- 11.64

Mole 66.04 ( Talpa europaea) • 7.11

Mouse 120.11 (Mus musculus domesticus) -- 11.41

151.95 7.81 807.00 335.33 • 17.85 :E 1.15 -- 76.43 • 41.76

201.92 10.22 1105.62 515.63 • 24.63 • 0.97 ~- 134.46 -- 54.53

211.20 11.16 1083.73 571.74 :J_ 18.61 • • i 5 1 . 3 2

248.41 7.49 1609.58 720.79 -- 22.45 -- 0.67 -- 171.88 • 69.46

297.99 13.39 1254.46 747.12 -- 26.84 • 1.07 -- 116.26 -t- 81.45

228.13 11.72 1503.18 574.62 ~- 19.67 -- 0.96 -- 165.21 -- 55.83

248.93 11.46 1 416.02 560.33 -- 19.76 4- 1.08 -- 141.51 -- 53.67

283.80 10.36 1205.36 583.09 -- 21.05 • 1.04 -- 131.94 ~ 61.36

284.73 11.59 2099.57 889.47 • ~0 .90 --211.18 J 91.43

264.80 11.21 1 888.73 922.69 • 24.33 • 1.26 • 179.83 • 93.46

366.95 15.02 2267.99 1118.31 --41.78 • 1.43 --204.56 •

339.61 14.17 2147.30 921.19 J_ 41.85 -- 1.51 • 196.58 • 94.57

357.73 13.98 2990.46 1392.09 32.48 • 1.51 -- 301.71 -- 128.74

474.23 17.82 2420.43 927.39 • 43.19 • 1.67 • 251.88 -- 88.63

298.44 18.75 2287.75 932.47 • -- 1.91 j 231.56 •

300.86 18.65 1675.43 900.04 • 28.44 :J: 1.73 • 171.33 • 87.98

342.44 20.83 1 807.29 746.60 33.61 • 1.88 ~: 175.43 • 71.22

437.52 26.56 3216.54 1324.28 • 39.87 • 2.42 ~- 287.96 • 126.59

400.26 24.74 2 526.04 1 097.67 --37.66 • • --111.47

349.50 25.57 3111.84 1332.18 36.48 • 2.58 -- 341.28 • 127.47

120 W. Lange

y = 9 7 3 . 5 9 . x -0,11 r = - 0 , 7 9

number o f c e l l s

p e r 0,001 m m s

2000 -

1000

500

g E E

~o ~ s g E

o . >~ : E �9 ~ - ~ z ~ . ~ ~ ~ ~ ,~ .~ ~ ~ ~ . - ~ ' , , ~ -

g

I00 , ~ 1i0 r I , 0,01 0,1 1 100 1000 10000 g

Fig. 4. Correlation between the number of cells per 0.001 mm 3 and the weight of the cerebellum

10000- numberof ceils per 0,001 m m ~

1000 -

100-

10-

y = 2231,10. x-O, 11 ~ + . + + ~ r = - 0 , 8 5

+

~ , _ ~ - �9 y = 3 4 2 , 7 0 . x - O , 0 8 ' ~ 1 4 9 �9 r = - 0 , 8 3

~ ' ~ P.C.L.

y = 68,95 �9 x -0 .13 r = - 0,83

�9 - ~ r - ~ . ~ . ~ y = 17,71' x -0,11 . ~ . r = - 0,91

ol

c

~ e cl ~ *5 #

f

i I i 0,1 1 llO 100 10100

1 t 0,0~ lO000g

Fig. 5. Correlation between the number of cells in the different layers of the cerebellar cortex and the weight of the cerebellum. Most of the regression lines have the same slope

decreasing weight of the cerebellum. A proportional increase occurs in all three layers. The only exception to this appears to be the squirrel monkey, in which the number of cells seems to be too high in relation to cerebellar weight.

The close numerical relationship between the number of cells per unit vo lume and the weight of the cerebellum is not seriously affected by this exception. As Fig. 4 indicates, there exists a linear correlation between the number of cells

Cell Number and Cell Density in the Cerebellar Cortex 121

and the weight of the cerebellum in the mammals investigated. This correlation can be expressed by the following equation:

Y(number of cells) = a(973.59), x(cerebellum weight) -0"11.

Another indicator for the close relationship between the number of cells and the weight of the cerebellum is the correlation coefficient r, which in our investiga- tion = - - 0.80.

A similar mathematical relationship can be established between the cell density in the different layers of the cerebellar cortex and the weight of the cerebellum (Fig. 5). The regression line for all three layers and for the number of Purk[nje cells has the same slope and also the correlation coefficient for all four curves is about r = - - 0 . 8 0 . This means that the increase in the number of cells per unit volume is almost proportional for all three layers of the cerebellar cortex.

Discussion

In 1967 Haug published some data concerning the cell density of the cerebral cortex in man and some other mammalian species. The close relationship between the brain weight and the number of cells in the cerebral cortex which could be established in his investigation, shed some light on the evolution and organization level of the cerebral cortex. Haug (1967c) could demonstrate that the evolution and organization level of the cerebral cortex is in some way correlated with a decrease in the number o/cells and a decrease in cell size.

On the basis of our present data, the same principle for the cerebellar cortex can be demonstrated, if we assume according to Wirz (1950) and Mangold-Wirz (1966) that brain evolution progresses from smaller to larger brains. But this principle only can be considered as a "rule of thumb ". If the number of cells per unit volume alone is taken into account as the only parameter for the organiza- tion level of a brain, the elephant or some aquatile mammals would appear to show a higher degree of brain evolution than man.

Looking at the ratio of different cell types to one another, we obtain some new information. In the cerebellar cortex, the ratio of Purkinje cells to granule cells is important in understanding the neuronal circuit (Palkovits, Magyar and Szentagothai 1971b). This ratio shows phylogenetic variations and is specific for the cerebellar cortex of individual mammals (Smoljaninov, 1966). But the ratios given by earlier investigators seem to be too low, probably due to inappro- priate correction procedures adapted by these authors (Palkovits et al., 1971b). So at present we know only the following ratios: cat 1:1700 (Palkovits et al., 1971b), 1 : 1580 (Lange, 1972), man 1 : 2 991 (Lange, 1972), rhesus monkey i : 1898 (Lange, 1972). The very similar results of Palkovits et al. (1971b) and of Lange (1972) for the cat are noteworthy.

On the basis of our cell counts and the volumes of the three layers of the cerebellar cortex in man and other mammals (Lange, 1970), we can now calculate the ratio of Purkinje cells to granule cells and show that this ratio increases during phylogenesis and brain evolution (Table 2). The sequence in which the mammals are listed in Table 2, based on the ratio of Purkinje cells to granule cells, greatly differs from the sequence in Table 1, based on the weight of the

122 W. Lange

Table 2. Ratio of Purkinje cells to granule cell in man and some other mammals

Man 1 : 2991 (Homo sapiens)

Vervet monkey 1 : 2128 ( Cercopithecus aethiops)

Rhesus monkey 1 : 1898 ( Macaca mulatta)

Elephant 1 : 1866 ( Loxodonta a/ricana)

Squirrel monkey 1 : 1864 (Saimiri sciureus)

Bottle-nose dolphin 1 : 1812 ( Tursiops truncatus)

Pilot whale 1 : 1790 (Globicephala macrorhyncha)

Common porpoise 1 : 1762 ( Phocaena phocaena)

Fox 1 : 1739 ( Vulpes vulpes)

Horse 1 : 1612 ( Equus caballus)

Cat 1 : 1580 (Felis domestica)

Sheep 1 : 1568 (Ovis aries)

Bull 1 : 1508 ( Bos taurus)

Guinea pig 1 : 959 (Cavia cobaya)

Opossum 1 : 952 (Didelphys virginiana)

Rabbit 1 : 931 ( Oryctolagus cuniculus)

Rat 1 : 897 ( Rattus norvegicus)

Mouse 1 : 778 ( Mus musculus domesticus)

Mole 1 : 706 ( Talpa europaea)

Hedgehog 1 : 609 (Erinaceus europaeus)

cerebellum and the number of cells per un i t volume. Nevertheless, it is in fairly good accordance with the range established by Wirz (1950) and Mangold-Wirz (1966) on the basis of the so called " S t a m m r e s t " of the brain.

The decrease with evolut ionary level in the number of cells in the cerebellar cortex is correlated with a decrease in the number of cells in the cerebellar nuclei : F ix (1967) showed tha t in pr imates the n u m b e r of cells per un i t volume in the cerebellar nuclei decreases with increase in bra in complexity. This similar phylo- genetic t rends can be recognized in the cerebral cortex, in the cerebellar cortex and in the cerebellar nuclei. But this rule seems not to be restricted to mammals . Kle inen (1974) pointed out tha t in the cerebellar cortex of birds cell densi ty varies in a similar fashion. I n the ostrich, with the highest cerebellum weight among birds, the n u m b e r of cells is very low and can be compared with tha t in the whale. I n contrast , in the t i tmouse, the n u m b e r of cells is higher t h a n in the mouse. This identical t rend in the cerebellar cortex of mammals and birds reflects tha t this is probably the only way in which the neuropil, containing the syuapt ic connections, can increase during phylogenesis.

But we always have to be aware, tha t the n u m b e r of cells per un i t volume is only a "ru le of t h u m b ", which may indicate the direction of bra in evolution. To get more information, we have to realize, tha t brain evolut ion is not restricted to one par t of the brain, bu t includes the whole. So it seems necessary to include also the spinal cord and other subcortical grey areas in future investigations, in order to shed some light on the relationship between brain size and body size, which

Cell Number and Cell Density in the Ccrebellar Cortex 123

has to be cons ide red if t h e n u m b e r of cells pe r un i t v o l u m e a n d t h e b r a in we igh t

a re d i scussed in t h e l igh t of phylogenes i s .

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