Paper - Comparative studies on the growth of the cerebral cortex 8 (1918)

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Sugita N. Comparative studies on the growth of the cerebral cortex. VIII. General review of data for the thickness of the cerebral cortex and the size of the cortical cells in several mammals, together with some postnatal growth changes in these structures. (1918) J Comp. Neurol. 29: 241-.

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This 1917 eighth in a series of historic papers by Sugita on the development of the cortex in the rat.



More by this author: Sugita N. Comparative studies on the growth of the cerebral cortex. I. On the changes in the size and shape of the cerebrum during the postnatal growth of the brain. Albino rat. (1917) J Comp. Neurol. 28: 495-.

Sugita N. Comparative studies on the growth of the cerebral cortex. II. On the increases in the thickness of the cerebral cortex during the postnatal growth of the brain. Albino rat. (1917) J Comp. Neurol. 28: 511-.

Sugita N. Comparative studies on the growth of the cerebral cortex. III. On the size and shape of the cerebrum in the Norway rat (Mus norvegicus) and a comparison of these with the corresponding characters in the albino rat. (1918) J Comp. Neurol. 29: 1-.

Sugita N. Comparative studies on the growth of the cerebral cortex. IV. On the thickness of the cerebral cortex of the Norway rat (Mus norvegicus) and a comparison of the same with the cortical thickness in the albino rat. (1918) J Comp. Neurol. 29: 11-.

Sugita N. Comparative studies on the growth of the cerebral cortex. V. Part I. On the area of the cortex and on the number of cells in a unit volume, measured on the frontal and sagittal sections of the albino rat brain, together with the changes in these characters according to the growth of the brain. V. Part II. On the area of the cortex and on the number of cells in a unit volume, measured on the frontal and sagittal sections of the brain of the Norway rat (Mus norvegicus), compared with the c responding data for the albino rat. (1918) J Comp. Neurol. 29: 61-117.

Sugita N. Comparative studies on the growth of the cerebral cortex. VI. Part I. On the increase in size and on the developmental changes of some nerve cells in the cerebral cortex of the albino rat during the growth of the brain. VI. Part II. On the increase in size of some nerve cells in the cerebral cortex of the Norway rat (Mus norvegicus), compared with the corresponding changes in the albino rat. (1918) J Comp. Neurol. 29: 119-.

Sugita N. Comparative studies on the growth of the cerebral cortex. VII. On the influence of starvation at an early age upon the development of the cerebral cortex. Albino rat. (1918) J Comp. Neurol. 29: 177-.

Sugita N. Comparative studies on the growth of the cerebral cortex. VIII. General review of data for the thickness of the cerebral cortex and the size of the cortical cells in several mammals, together with some postnatal growth changes in these structures. (1918) J Comp. Neurol. 29: 241-.

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Comparative Studies on the Growth of the Cerebral Cortex

VIII. General Review Of Data For The Thickness Of The Cerebral Cortex And The Size Of The Cortical Cells In Several Mammals, Together With Some Postnatal Growth Changes In These Structures

Prof. Naoki Sugita (1887-1949)
Prof. Naoki Sugita (1887-1949)

Naoki Sugita

From The Wistar Institute of Anatomy and Biology

Three Figures And Two Charts

I. Introduction

Years ago Schwalbe ('81) pointed out as characteristic somatic expressions, which might be taken to indicate the grade of intelhgence of a species of animals, the following four measurements on the brain: 1) total weight of the brain; 2) total number of nerve cells in the brain; 3) total area of the surface of the hemispheres of the brain, and 4) the thickness of the cerebral cortex. Since then he and many other neurologists have endeavored to gather data on the morphological evidence for the development of mental ability. Donaldson and Hatai ('The Rat,' Donaldson, '15) have made systematic observations on the growth changes in the central nervous system as well as in other organs and systems, using exclusively the albino rat. As a result of their investigations, the postnatal growth of the brain and the spinal cord, in gross measurements, and the relations of these to the other systems during growth have been determined. In line with these studies, I also made further researches on the growth in the thickness of the cerebral cortex, the size and shape of the cortical nerve cells and the relative number of the cortical cells in both the Norway and albino rats. The results of these researches have been already presented (Sugita, '17,, '17 a, '18, '18 a, '18 b, '18 c, '18 d), with references to some similar studies by other authors. These data give us a general idea of the postnatal development of the cerebral cortex in a representative mammal (albino rat), and we may fairly infer that similar changes occur in other mammals during the growth of the brain. To test how^ far my conclusions on the mode of the development of the cerebral elements during postnatal life may be extended, I shall review and summarize in the present paper the results obtained by several authors on the development of the cortex in other mammals and make a comparison of their results with the data obtained by me.


II. Thickness of the Cerebral Cortex in the Albino Rat

The results obtained by me regarding the cortical thickness in the brain of the albino rat may be summarzed as follows (Sugita, '17 a):

1. The cortex at the frontal pole of the hemisphere is the thickest and that at the occipital pole is the thinnest. Speaking in general terms, the cortex diminishes in thickness from the frontal to the occipital pole and from the dorsal to the ventral aspect.

2. After birth, the general average of the cortical thickness increases very rapidly during the first ten days, thickening from 0.74 mm. at birth to 1.73 mm. at ten days, more than twice the thickness at birth, while the brain weight increases from 0.25 gram to 0.95 gram during the same period. This is designated by me the first phase of the cortical development.

3. Between the tenth and the tw^entieth day after birth, the cortical thickness increases more slowly, attaining at twenty days to within 4 per cent of the full thickness of the cortex, namely, 1.84 mm., or about 2.5 times the thickness at birth, while the brain weight increases to 1.15 grams. This is designated the second phase of the cortical development.

4. From the twentieth to the ninetieth day, the cortical thickness increases but little on the average, attaining at ninety days the thickness of 1.93 mm., or 2.6 times the thickness at birth, w^hile the brain weight has increased to about 1.80 grams. This is designated the third phase of the cortical development.


After the ninetieth day, there is no significant change in the thickness of the cortex, but the area of the cortex increases as the brain weight rises and at 2.0 grams is greater than at 1.15 grams (20 days) by about 45 per cent.

5. In the first phase the cortex increases its thickness by receiving some newly formed cells from the matrix and many already formed from the transitional layers and at the same time by the general enlargement of the neurons, especia ly the cell bodies; in the second phase, however, it grows main'y by the enlargement of the cell bodies and the growth of the axons and dendrites; while during the third phase it thickens only slightly, but extends in area as the result of the ingrowing axons and the formation of the myelin sheaths and non-nervous structures.

6. The cortex at the frontal pole increases its thickness very rapidly and steadily, continuing to do this even after the end of the second phase, while at all the other localities the cortex thickens in the same proportion, so that at the end of the second phase all the localities reach nearly the full thickness, but maintain their initial relations. The localities heterogeneous in their cell lamination show in the course of thickening some deviation from the localities which are typical.

7. The cortex generally attains nearly its full thickness before myelination, as shown by the Weigert staining method, occurs in it. In the Albino, the cortex has nearly its mature thickness at twenty days, just before the young rat is weaned and when the brain has attained only a trifle more than half its final weight. The growth of the cortex in thickness is therefore precocious.


III. Increase in Cortical Thickness during Growth of the Brains of the Mouse and the Guinea-Pig

Mouse

Isenschmid ('11) has made a study of the cortical cell lamination in the brain of the mouse and given a map of the topographic localization in the hemisphere, which is reproduced here as figure 1. De Vries ('12) and Rose ('12) have also presented a brain map of the mouse according to their studies on the cell architecture of the cortex ; a map which resembles that



Fig. 1 Cortical area of the mouse (Mus musculus) — reproduced from the original by Isenschmid ('11); the thickness of the cortex at each area designated on the map is tabulated in table 1 of this paper. Double lines show borders of three — the dorsolateral, the frontomedial, and the suboccipital — regions of the neopallium. Shaded parts (areas t, s, and h) do not lie in the same (median) plane as the other areas. A = Dorsal view of the right hemisphere; B = Lateral view of the right hemisphere; C = Medial view of the right hemisphere. B.olf. = Bulbus olfactorius; C = Corpus callosum; c.A. = Cornu Ammonis; cl. = Claustrum; s.;?. = Septum pellucidum. s — s' = the level corresponding to that from which the sagittal sections of the Albino brain were taken by me; /— /' = the evel corresponding to that from which the frontal sections of the Albino brain were taken by me; h — h' = the level corresponding to that from which the horizontal sections of the Albino were taken by me.



TABLE 1 Giving for each localiUj of the brain of the adult mouse the characteristics of the cell lamination, the thickness of the cortex on the slide as deterinined from the photograms given by Isenschmid {'11), and the relative thickness of the outer and inner layers as presented by the same author. For the localities consult figure 1 in this paper, which was reproduced from the original of Isenschmid {'11)


AKEA

(fig. 1)


CHARACTERISTICS OF. THE AREA IN CELL-LAMINATION


e

f

i

k

1

m

r

q

s t


Largest ganglion cells contained (18 X 20 m)- Not so large cells

IV layer thick

Transitional part

Paleopallium

IV layer not so well developed

Adjoins to fovea limbica, cell lamination not clear

Transitional part (ganglion cells: 13 X 15 m)At the corner (ganglion cells: 12 X 14 /u)

(Ganglion cells : 15 X 18 m)

Similar to area q


THICKNESS OF THE CORTEX


0.73

0.86 0.50 0.53


0.62 0.44 0.81 0.78 0.71-0.61 1.201 0.56 0.26 0.34


RELATIVE

THICKNESS OF

THE OUTER AND

INNER LAYERS

OF THE

CORTEX

outer: inner'


48:52

45:55 45:55 45:55


42:58


34:66 23:77

22:78 28:72


1 Section cut obliquely.

^ The outer layer = the lamina granularis externa plus the lamina pyramidalis plus the lamina granularis interna. The inner layer = the lamina ganglionaris plus the lamina multiformis.

of Isenschmid. Isenschmid ('11) has recorded the thickness of the cerebral cortex of the mouse on the sHde at every locahty mapped in his figure (fig. 1). But the actual thickness not being given explicitly for each locality, I calculated the values from the direct measurements made on the photograms. The brain was fixed in alcohol, imbedded in paraffine and cut in 10-micra sections and stained with kresyl- violet. The thicknesses of the cortex on the slide as thus obtained are given for each locality in table 1 and also are condensed in table 2, in which the data


246


NAOKI SUGITA


TABLE 2

A com'parison of the thicknesses of the cerebral cortex at several corresponding localities in the albino rat and in the mouse. The data for the albino rat were taken from table 11 in ?ny previous paper (Sugita, '17 a, p. 578) and the data for the mouse were taken from a paper by Isenschmid {'11). The order of increasing thickness is the same in both animals


ALBINO RAT


MOUSE


Locality


Average

thickness of

cortex by

locality


Corresponding locality


Thickness of cortex at each of the localities


Average

thickness of

cortex by

locality



mm .



mm.


mm.


V and XIII


1.24


C


0.50


0.50


IV


1.42


d


0.53


0.53


XII and VIII


1.67


e and i


0.65 and 0.44


0.55


III and XI


1.91


a and e


0.73 and 0.65


0.69


VI


2 01


1 (corner)


0.78


0.78


II and X


2.03


k and b


0.81 and 0.86


0.84


VII


2.29


b


0.86


0.86


I and IX


2.99


frontal pole


1.00


1.00


Average


1.94


Average


0.72




for the Albino are so entered that the cortical thicknesses at the corresponding localities in the two forms may be compared. The order of the localities is arranged according to the increasing thickness in the Albino (taken from table 11, Sugita, '17 a, p. 578). The average value of the cortical thickness in the mouse is, on the slide, 0.72 mm., and if corrected to the fresh condition would probably be somewhat thinner than one-half the average thickness of the Albino cortex. The order of the thickness according to localities is quite the same, so that in both forms the cortical thickness decreases from the frontal to the occipital pole and from the dorsal to the ventral aspect. Moreover, the cortex at the frontal pole is the thickest and has double the thickness of that at the occipital pole.

As seen in figure 1, the cerebral hemisphere is divided by Isenschmid into three main regions — the dorsolateral, frontomedial and suboccipital regions — separated by the double line in figure 1.

The average cortical thickness in the dorsolateral region (fig. 1 a) is 0.56 mm. at its hinder-medial part and 0.90 mm.



at its fore-lateral part, and in this region the lamina zonalis is about one-twelfth, the main outer layers (the lamina granulans externa plus the lamina pyramidalis plus the lamina granulans interna) about two-fifths and the main inner layers (the lamina ganglionaris plus the lamina multiformis) about one-half the total thickness of the cortex. In the frontomedial region (fig. 1 c) the cortical thickness at the frontal pole is 1.00 mm. and that at the caudal part is 0.35 mm., while in the suboccipital region the cortical thickness ranges between 0.2 and 0.3 mm.




Fig. 2 Showing diagrammatically the thickness of the cerebral cortex at locality a in the mouse at different ages. Reproduced from the original given by Isenschmid ('11). B = at birth. M = at maturity. The other arable numbers show the age in days. I = lamina zonalis; II = lamina granularis externa; III = lamina pyramidalis; IV = lamina granularis interna; V = lamina ganglionaris; VI = lamina multiformis. The cell outlines found between the last two diagrams indicate the relative size and shape of the cells in each cortical layer.

Isenschmid has given also diagrams illustrating the growth in cortical thickness at locality 'a' (fig. 1 a, corresponding approximately to locality III in my study, fig. 2, Sugita, '17 a, p. 525), sampled from material at several different ages and magnified uniformly. These are also reproduced here as figure 2. The diagrams show that as age advances the lamina pyramidalis (II and III) thickens steadily and continuously while the lamina ganglionaris (V) and especially the lamina multiformis (VI) grow much less rapidly. Chart 1 gives a comparison of the increase in the cortical thickness at corresponding localities (locality 'a' of the mouse and locality III of the albino rat) in the albino rat and the mouse, the data being from Isenschmid ('11) and Sugita ('17 a). In the Albino the cortex attains nearly its full thickness at twenty days (weaning time), while in the mouse this stage was reached between twelve and seventeen days of age, very closely corresponding to the weaning time of


mm. 2.0r

18

16

lA

J.2

1.0

0.8

0.6

0.4

Q2













Chart 1 Giving the cortical thickness of the albino rat and of the mouse according to age. The data for the albino rat are taken from Sugita ('17 a) at locality III measured on the sagittal section and the data for the mouse are taken from Isenschmid ('11) at locality 'a.' These two localities approximately correspond.

the mouse, which is fifteen days. The remarkable phase during which the rapid increase in cortical thickness takes place in the Albino (first ten days after birth) cannot be clearly identified on the graph for the mouse cortex. It must be recalled, however, that data on the mouse cortex have not been corrected for the action of the reagents, while the data for the rat have been so corrected. The outstanding fact, however, is that the cerebral cortex in both forms attains nearly its full thickness just before the weaning time.


Guinea-pig

I have had the opportunity at The Wistar Institute to examine the sections of the guinea-pig brains prepared by Allen ('04) for her study on the myelination of the nervous system of that animal. The sections were cut in series in the frontal plane from material fixed in Miiller's fluid, imbedded in celloidin and stained by Weigert's method for the myelin sheaths. The thickness of the cerebral cortex in the adult guinea-pig (body weight, 618 grams; brain weight not recorded) is on the average 1.90 mm. (1.80 mm., 1.88 mm,, and 2.01 mm., respectively, at the localities corresponding to localities VI, VII, and VIII examined by me on the frontal section of the Albino brain at the level of the commissura anterior). The corresponding measurements at birth (body weight, 108 grams) are 1.71 mm. (and 1.51 mm., 1.75 mm., and 1.86 mm., respectively) and those at thirty-five days (body weight, 250 grams) are 1.85 mm. (and 1.77 mm., 1.86 mm., and 1.92 mm., respectively). So, from birth on to the maturity, the cortical thickness has on the average increased only 11 per cent. According to Allen, the guineapig at birth is covered with hair, has complete muscular development, and is almost independent of the mother, the central nervous system being practically completely myelinated, whereas, by contrast, the albino rat is born quite naked, extremely helpless and undeveloped, and myelination in the brain has not begun. The guinea-pig is psychically mature soon after birth (three days after birth) ; the degree of development of the central nervous system of the new-born guinea-pig corresponds to that of the albino rat at twenty-three to twenty-seven days or its period of first psychical maturity. A new-born guinea-pig is fobnd to have a cerebral cortex in which the myelination is going on.

Comparing the sections from the guinea-pig brain with those from the albino rat brain, it appears that the new-born guinea-pig corresponds to the albino rat of about ten days in cortical thickness, but seems to be older when judged by the myelination of the cortex. This coincides with observation that the guineapig is, almost from the start, relatively independent of the mother.


250 NAOKI SUGITA

IV. THE CORTICAL THICKNESS AT SEVERAL LOCALITIES IN THE BRAINS OF SOME MAMMALS OTHER THAN THE RAT

Few papers have been published regarding the differences in the thickness of the cerebral cortex at given localities of the brain in mammals other than the rat, except for man. Yet even in these cases, the techniques of hardening, imbedding, and staining used by the different authors are dissimilar and their results are accordingly not precisely comparable. Despite this, however, it has seemed worth while to make a survey of the data at hand.

Rabbit. Bevan Lewis (^81) has given as the natural thickness^ of the cerebral cortex of the adult rabbit the following figures (table 3) according to localities. For the localities, the map made by him and reproduced by me in a previous paper (Sugita, '17 a, fig. 10, p. 544) should be here consulted. He has presented the thicknesses of every layer of the cortex separately, but here only the total cortical thicknesses, as computed by me from his data, are given in round numbers.

Pig. Lewis ('79) has also determined the cortical thickness at several localities in the pig brain (the names of the localities

TABLE 3

The thickness of the cerebral cortex of the rabbit, quoted from Bevan Lewis {'81)

Depth of cortex on a plane with genu of corpus callosum :

mm.

Gyrus fornicatus 1.72

Sagittal angle 2.23

Extra-limbic 2.81

Near limbic sulcus 2.31

Depth of cortex on a jilane with posterior border of corpus eallosum:

Gyrus fornicatus 1 . 70

Sagittal angle 1.91

Extra-limbic 2 . 46

Depth of cortex of the modified lower limbic t3'pe 2.23 to 2.47

Depth of cortex in the cornu Ammonis:

Anterior regions 2 . 27

Average at six different sites 2 . 23

1 Lewis measured the cortical thickness on sections cut by the freezing microtome from fresh material and then hardened by osmic acid, stained by aniline black and mounted in Canada balsam. According to his statement we obtain, by this method, the natural depth o"" the cortex, no shrinkage occurring if the preparations have been carefully made (Lewis, '78).


Limbic lobe <


Upper parietal convolutions <


Lower parietal convolutions.


GROWTH OF THE CEREBRAL CORTEX 251

TABLE 4

The thickness of the cerebral cortex of the pig, quoted from Bevan Lewis {'79)

Depth of cortex from before backward:

mm.

'4.97 4.48 3.70 4.98 3.53 3.77

Average 4.22

fa. 28 2.65 3.08 3.91 4.23 3.44

Average 3 .50

■3.44 3.91 3.95 3.35 3.02 3.67

Average 3.64

are analogous to those given for the rabbit brain, loc. cit.)- His results are summarized in table 4. These values are distinctly high compared with those for other mammals, as shown in the various tables in this paper. These results taken together with those for the rabbit just given, which are also noticeably high, suggest that the determination by Lewis are for some reason systematically too high.

Marsupials to man. Table 5 is quoted (slightly modified) from Brodmann ('09) and gives for several species of mammals, including man, the cortical thickness at six localities (areae precentralis, frontalis, parietalis, occipitaUs, hippocampica et retrosplenialis) in the brain of each animal. The sections were made by hardening the material in 4 per cent formaldehyde, imbedding in paraffine, and staining by the modified Nissl's method, and the cortical thickness was measured by the micrometer directly on the slide. The average thickness was calculated by me for the four areas, excluding the areae hippocampica et retrosplenialis which are heterogeneous in cell lamination.


252


NAOKI SUGITA


TABLE 5

The cortical thickness at the corresponding parts of the cerebral hemisphere in different mammals, quoted from Brodmann i'09). According to his nomenclature, area precentralis = type 4, area frontalis agranularis = typed, area parietalis = type 7, area occipitalis = type 17, area hippocampica = type 28, and area retrosplenialis = type 29, as given in his 'Hirnkarte' {Brodmann, '09)


Homo sapiens (man) Cercopithecus (longtailed ape)

Lemur

Hapale (marmoset) .

Pteropus edwardsii (vampire bat). . . .

Erinaceus europaeus (hedgehog)

Cercoleptes caudivolvulus (kinkajou)

Lepus cuniculus (rabbit)

Spermophilus citillus (ground squirrel)

Macropus giganteus (kangaroo). .


grams

60,000

2,500

1,800

200


375 700

2,000

2,200

200

5,000


grams

1,400

85 23


7 3.5


10


2.2


3.0-4.5

3.0 2.3 2.15


1.9 1.87

2.17

2.7

2.1

2.8-3.1


O < 03 t^


3.0-3.8

2.5 2.3

2.17


1.6 2.1

2.0

2.33

2.18


3.08

2.0

1.67

1.73


1.7 1.78

1.7 2.2 1.73 2.2


2.3-2.6

1.7

1.55

1.26


1.76 1.5

1.9


1.37


1.9


mm.

2.5

1.6

1.35

1.14


1.52 1.6

1.9 1.2 1.13 1.7


< 2


2.3

1.1

1.19

1.07


1.4-1.76 0.8

1.67

0.8-1.5

0.75

1.2


3.0

1.95 1.73 1.59


1.66 1.61

1.89 1.79 1.54 2.15


Reviewing this table, it is readily seen that, within each order, the animal which has a greater brain weight shows also a greater cortical thickness, but a fixed relation between the brain weight and the cortical thickness has not been here revealed. In different orders, this relation is not true; the lemur and the kangaroo have a similar brain weight (23 to 25 grams),


GROWTH OF THE CEREBRAL CORTEX


253


while the cortical thickness in the latter is much greater (by about 25 per cent).

Prosimiae and primates. The following table (table 6) is summarized from a paper by Marburg ('12) and shows for some species of the prosimiae and primates the total cortical thickness measured at four representative localities (gyri centralis, frontalis, temporalis et occipitalis) . The average values were taken by me.

TABLE 6

Thickness of the cerebral cortex at several localities in monkeys, as presented by

Marburg {'12). Averages are calculated by me


Simla satyrus

Hylobates (sp.?)

Semnopithecus nasicus. . .

Macacus rhesus

Cynocephalus hamadryas

Ateles niger

Lemur varius






AVEI


CENTRAL, GYRUS


FRONTAL GYRUS


TEMPORAL GYRUS


OCCIPITAL, GYRUS


Of the four

localities

m »i .


7n7n .


7)1 711 .


mm.


mm.


3.11


2.97


2.43




3.78


3.24


2.51


1.78


2.83


3.78


2.43


2.43


1.35


2.50


"2.84


2.70


2.15


1.49


2.30


2.97


2.70


2.03


1.35


2.26


2.97


2.84


2.43




1.30


1.76


1.76


1.67


1.62


Of the three localities


2.84 3.18 2.88 2.56 2.57 2.75 1.61


This table also suggests that, in the order of monkeys, the average thickness of the cortex varies so that those which have the greater brain weight have also t|ie greater thickness of the cerebral cortex, but the brain weights are not available for comparison.

V. THE THICKNESS OF THE CEREBRAL CORTEX IN MAN

Man. There are scores of papers giving the measurements of the thickness of the cerebral cortex in man, but they are diverse in the techniques used for preparing the material, in the localities selected for measurement, and also in the manner of measurement. The results published before 1891 were all summarized by Donaldson ('91), but the table is not reproduced here as, owing to the lack of the information necessary for the interpretation of the values found, it has mainly an historical interest.


254


NAOKI SUGITA


Donaldson ('91) measured also the thickness of the cerebral cortex at fourteen localities from each hemisphere of nine normal brains (six males and three females), as shown in figure 3 reproduced from his original paper, in order to obtain control




Fig. 3 This figure shows the localities on the hemispheres from which the samples of cortex were taken by Donaldson ('91). For the thickness of cortex at each locality see table 8 and chart 2. A = Lateral aspect. 3 is used to designate the insula, here not exposed. B = Ventral aspect; C = Mesial aspect.

values for the study of the brain of a blind deaf-mute, Laura Bridgeman. The technique employed by Donaldson was fixation in bichromate and alcohol (potassium bichromate 2| per cent plus I its volume of 95 per cent alcohol) for six to eight


GROWTH OF THE CEREBRAL CORTEX


255


TABLE 7

Giving the average cortical thickness of man, arranged according to age and sex, together with the brain weight. Quoted from Donaldson {'91)


BRAI^f WEIGHT


AVERAGE CORTICAL THICKNESS


Males


years


grams


7nm.


35


1419


2.81


35


1443


2.98


39


1393


2.82


45


1367


2.92


57


1464


2.94


?


1210


3.11


Females


40


1196


2.74


45


1173


2.90


?


1312


3.07


Average


1331


2.92


weeks, washing in water for twenty-four hours, 95 per cent alcohol for two days, final preservation in 80 per cent alcohol, and imbedding in celloidin. The sections were cut about 100 micra thick and measured unstained under a low magnifying power with a micrometer eyepiece, at the summit of the gyrus arid at the side, midway between the summit and the bottom of the bounding sulcus. To obtain the average thickness at the locality, the smaller figure was multiplied by 2, added to the larger figure, and the sum divided by 3.

Table 7 shows the average thickness of the cortex (taken from the fourteen localities) arranged according to sex and age, quoted from Donaldson ('91). If we take the nine cases in this table as the basis for computation, we find the mean thickness of the cortex to be 2.92 mm., with a probable error of the mean equal to ±0.026 mm.

I wish to cite also the average thickness of the cortex, as thus obtained by Donaldson ('91), according to locality (table 8). These localities are shown in figure 3 and the relative thickness


256


NAOKI SUGITA


of the cortex at each is graphically presented in chart 2. Generally summarized, the average thicknes of the cortex of the adult man is 2.92 mm.; females have a slightly thinner cortex than males (differences less than 1 per cent, or 0.02 mm.) and the right hemisphere usually has a cortex a few per cent less thick than the left (maximmn difference 7 per cent).

With the foregoing determinations are to be compared the measurements by three other observers.


wm


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Chart 2. -The curve was plotted according to table 8 to show the cortical thickness at each locality as measured by Donaldson ('91. The numbers placed by the ordinates indicate the thickness of the cortex in millimeters. The numbers for the localities are given below, and correspond to those in figure 3, A. B and C.

In accordance with this plan, the results obtained in a careful study by Hammarberg ('95) are tabulated in table 8. The material used for this study was a brain of a male, twenty-eight years old, mentally normal, and who died of typhoid fever. The technique employed was fixation in 95 per cent alcohol, imbedding in paraffine by means of xylol, sections 10 micra in


TABLE 8 Giving for several localities on the hemisphere of the adult human brain the thickness of the cortex, as measured by different authors. The general average thickness was taken, averaging all measurements presented by each author. For reasons given in the text, these averages as they stand are by no means comparable with each other. The data were taken from Donaldson ('91), Hammarberg {'95), Campbell {'05), and Brodmann {'08)



ocaJLtu


Au/A-<jT


Tlanaldsan


Hamtnurfc&rj


C(Xtm


pbel/


Brocf


T)ann


L


Ki^iti o/ secti'uTv


Cell


Cell


Cell


Fi ber


Cell


Fiber 1



U.n,U


rvvrn.


m^


m^


n\/yn.


«^



^


Gyi-ixs centralis


o/n tenor



2.?7


2.^-0


2.62.


a gi'


4 05

^.


Gyrus fenfroJIs pos/erior


oral sic^e


3.08


2.70


2.20


^.1:1,


/ ?6


/.9i


^


ir\Ter mediate p^rf


Z.9S


3./6



ccL^otf/ai. s^ale.


2.6


/■ <Jo


2.4 3


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2.?6







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a/0


2.62^


Z.SZ.


3.8 2


3.84


m-i^<J/e fjcw-r



3.93



fore fa^f



2.60


3.45



G^rus -fronfa/is


«ec/ius


3.09


3.4-0


2.A-0


%.I0


3.5 7



Gyrus froTitcdis i/nferioT


?iM-s ofjerccilarij


ao8


2.50




3.sa



Ta^s tria/*^£^a.fs


2.98


3.00




3.34



Po/rs or ()i Tali's






3.60



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2. J3





3.17



Frcmtal pole




2.37


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3.07



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Gyrus a^gn-laris



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3.3 5


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3.3 1


3.25


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2.6/


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2.50


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2.64

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3.8 3



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3.3 5


3.80


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3.57


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3 70


3.8 7


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257


THE JOUBNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 3


258 NAOKI SUGITA

thickness and staining with methyleneblue. Hammarberg claims that after twenty-four hours in 95 per cent alcohol the brain piece shrinks about 20.5 per cent in volume and the cortical thickness diminishes by 0.1 to 0.2 mm., but that during the subsequent procedures no significant size changes occur. According to his results, the gyri frontales have the thickest cortex (about 3.0 mm.) and the lobus centralis or insula is the thinnest among localities typical in cell lamination. This latter part as measured by Donaldson shows the thickest cortex.

Campbell ('05) gave two series of determinations of the cortical lamination of the human brain, after cell staining and after fiber staining, represented by uniformly magnified illustrations of the sections at the several localities. Making use of his illustrations, I obtained a series of cortical thicknesses at different localities (table 8), reduced to the actual thickness on the slide, by dividing the direct measurement on the illustration by the magnification. His sections were taken from the material fixed in Miiller's or Orth's fluid and imbedded in celloidin, cut at 25 micra, and stained with thionine. The general average thickness thus obtained, the two series combined, is about 2.3 mm.

Brodmann ('08) also has measured the thickness of the cortex on the human brains at forty-two different localities on sections prepared by two different methods: one set was fixed in 4 per cent formaldehyde, imbedded in paraffine, and stained by Nissl's method for cell study, and the other, fixed in Miiller's fluid, imbedded in celloidin, and stained by Weigert's method for the myelin sheaths. His results, which are the averages from brains between seventeen and forty-five years in age, are also tabulated in table 8 for a comparison. The general average thickness given by Brodmann is about 3.09 mm.

Kaes ('07) also studied the growth in thickness of the human cerebral cortex, measured at twelve different localities on the hemisphere, using sections fixed in Miiller's fluid and stained by Weigert's method. His results are remarkably high, giving 4.9 mm. on the general average. His method of measuring the cortex is so arbitrary and peculiar, however, that his results are not included in this table 8.


GROWTH OF THE CEREBRAL CORTEX 259

Bevan Lewis ('79) has given as the average depth of the human cortex the figures as high as 4,84 to 5.70 mm., a higher vahie even than that of Kaes. His results for both the pig and rabbit cortex were also very high, compared with those obtained for other mammals. These results suggest that his technique, which he claims gives the natural depth of the cortex, is likely to produce very high values.

Reviewing the table (table 8) , the values for the cortical thickness given for a fixed part of the hemisphere by different authors are by no means in accord ; the results by Brodmann stand close to the results by Donaldson, while those given by Campbell are the lowest, less than one-half the values given by Lewis. These differences are probably due mainly to differences in technique and are not to be attributed to variations within the sanie species, as the series of Donaldson (table 7) and my previous study (Sugita, '17 a) both have shown that individual variations in cortical thickness, obtained by the use of the same technique, are low as compared with the variations for other body measurements.

On the average, the figures given by Donaldson and Brodmann are fairly close and the former being somewhat lower, probably because Donaldson took the average from the values at the summit and at the sides of the gyrus, while Brodmann has measured the thickness at the summit only. The figures given by Hammarberg and Campbell are low, probably owing to the shrinkage of the material during preparation, as may be inferred from the descriptions by the authors and from the studies on the effects of fixing fluids by King ('10) and by me (Sugita, '17 a, '18 b, '18 c).

Despite the apparent irregularity among the figures given for the cortical thickness at different localities by the several authors, as shown in table 8, there are some general relations which are fairly clear. If we examine table 9 in which has been entered for each region the average thickness obtained by each author, it may be safely said that this table (and also table 6 for the monkeys) shows that in man (and the primates) the cerebral cortex differs normally according to locality. The


260


NAOKI SUGITA


TABLE 9

Giving the average cortical thickness for several lobes and regions {with typical cell lamination) of the cerebral hemisphere as given by different authors, and the order of localities according to the cortical thickness, together with the difference in thickness between. the temporal and occipital regions. R = regio Rolandica, F = lobus frontalis, P = lobus parietalis, = lobus occipitalis, T = lobus temporalis. Based on table 8 in this paper


LOCALITY


DONALDSON

('91) (Cell)


HAMMARBERG

('95) (Cell)


CAMPBELL

('05) (Cell)


CAMPBELL

('05) (Fiber)


BRODMANN

('08) (Cell)


BRODMANN

("08) (Fiber)


Regio Rolandica

Lobus frontalis

Lobus parietalis

Lobus occipitalis

Lobus temporalis


mm.

2.92 2 92

2.59 3.21


mm.

2.34 2.92

2.43

2.09

2.49


mm.

2.43 2.46

2.44

2.16

2.64


77im.

2.21 2.15

2.13

1.96

2.29


mm.

2.74 3.50

3.17

2.47

3.48


mtn.

2.93 3.84

3.12

2.54

3.75




Average


2.91


2.45


2.43


2.15


2.92


3.16


Order of the above five localities as to the thickness


TFRO?


FTPRO


TFPRO


TRFPO


FTPRO


FTPRO


Difference between T and


0.62


0.40


0.48


0.33


1.01


1.21




frontal and temporal regions have in all cases the thickest cortex and the occipital region is the thinnest, while the position for the cortex of the parietal and Rolandic regions is less fixed. These thickness relations support the earlier statement made by me for the rat cortex that the thickness diminishes from the frontal to the occipital pole and from the dorsal to the ventral aspect.

Brodmann ('08) has concluded from his careful study that regional characteristics for the cortical thickness clearly exist. Diese sind in alien normalen Gehirnen gesetzmassig und kon


GROWTH OF THE CEREBRAL CORTEX


261


stant und bilden ein Hauptmerkmal der struktuellen Verschiedenheiten der Gehirnoberflache; jedes Strukturfeld besitzt demnach eine bestimmte, mittlere Durchschnittsbreite, durch welche es sich von den Nachbarfeldern auszeichnet." On the other hand, local variations within a fixed area are small, while individual differences between different brains for each locality may run sometimes as high as 0.5 mm. or more.

VI. INCREASE IN CORTICAL THICKNESS DURING THE GROWTH OF THE BRAIN OF THE MAN


From the point of view of the growth changes, there have been only few studies on the human cerebral cortex ever published. Kaes ('05, '07, '09), employing forty-one human brains (twentyeight males and thirteen females, normal and pathological combined) of different ages and of different grades of intelligence, studied the cerebral cortex for the purpose of following the growth changes in it. He took his sections from twelve localities in each hemisphere, stained the fibers by Weigert's method and measured the so-called cortical thickness from the ectal border of the Meynert's arcuate fibers (or fibrae propriae) to the ectal border of the zonal layer. His conclusions on the growth

^ His ('04) has given the following values as the cortical thicknesses measured at different localities of the hemisphere of the human embryos in early months, at different stages of intrauterine development- — measured directly on the sections imbedded in paraffine.


AGE OF EMBRYOS


AT CORPUS STRIATUM

M


AT LATERAL WALL OP THALAMUS


AT LATERAL

WALL OF HEMISPHERE (BASAL PART)

M


AT LATERAL

WALL OF

HEMISPHERE

(MID PART)

M


AT MEDIAN

WALL OF HEMISPHERE


AT BOTTOM OF

SULCUS CINGULI

M


1 2


50-55 65-75


4 5 6

7 8


150

360

800

1300

2000


130

160 300 600 900


300

400


110 120 130

170 200


90 110

130


60

50 40 30 30


262 NAOKI SUGITA

changes, briefly stated, are as follows: The average thickness of the cortex diminishes rapidly from his first entry (three months old, 5.58 mm.) to the twenty-third year (4.44 mm.) and is followed by an increase up to the forty-fifth year (5.71 mm.), where it is to be noted that the thickness attained is even greater than that at birth. Then it undergoes a second thinning up to the old age (at ninety-seventh year, his last entry, 4.62 mm.).

These conclusions have been disputed by Donaldson ('08) and by Brodmann ('09), and I am in agreement with these critics that Kaes' results cannot be taken seriously.

Brodmann ('08), in his paper on the cortical measurement, has noted only in a general way the average cortical thickness at the lateral surface of the hemisphere at several ages, as shown in table 10 (columns A and C). Nevertheless, these data can be used for a comparison.

Donaldson ('08) has compared the albino rat with man in respect to the growth of the brain and reached the conclusion that man and the rat show growth curves for the brain which are similar in form when the data are compared at equivalent ages, and the condition of the brain of the rat at five days of age is taken as like that of the human brain at birth. The relative growth rates of the rat and man are as 30 to 1 and the brain of the child at one year corresponds to that of the albino rat at seventeen days of age in its stage of development (Donaldson, MS.). These statements are also confirmed by me for the cortical thickness, as shown in table 10 (see below), and I have already noted that the transitional cortical cell layers, which are no longer to be seen in a new-born child, do not disappear in the albino rat until after four days of age (Sugita, '17 a, p. 539).

From these relations, we conclude that the course of growth in the thickness of the cerebral cortex in man and the albino rat would probably be similar, if the brains were compared at the equivalent ages. Such a comparison is attempted in table 10. Here the increase in cortical thickness in man and in the albino rat is compared, employing data given by Brodmann ('08) and by me (Sugita, '17 a). From the age (column A) given by Brodmann, the approximate brain weight (column B) was de


GROWTH OF THE CEREBRAL CORTEX


263


TABLE 10

Giving a comparison in the course of increase in cortical thickness in ynan and in the albino rat, according to data given by Brodmann {'08) and by Sugita {'17 a). Approximate brain weight in man and in the Albino for the equivalent ages were assumed in round numbers according, respectively, to Vierordt {'90) and Donaldson {'08)


A


B


C


D


E


F


G


MAN


ALBINO RAT








Correspond




Approximate




ing cortical




Observed


brain



Thickness


thickness in



Approximate


thickness of


weight, at the


Equivalent


of the cortex


human brain,


Age


brain


the cortex.


equivalent


(observed)


at ages


when the



weight


Brodmann


(observed)


age


given in


adult values




('08)


ages (Donaldson)



Column E


in the both are taken as the standards



grains


m m .


grams


days


mm.


7nm,


Fetus








8-9 months



1.0-1.5



Birth


0.80


1.25


Birth


380


1.5-2.0


0.50


5


1.10


1.75


1 year


950


2.0-3.0


1.10


17


1.75


2.76


Adult


1400


2.0-4.0


1.90


Adult


1.90


3.00


termined according to Vierordt ('90) and then the final weight (1400 grams) was entered corresponding to the adult brain weight of the albino rat (1.9 grains). The other corresponding brain weights of the Albino of the equivalent ages were entered also according to Donaldson ('08) (column D). The cortical thickness (column F) for the given brain weights of the Albino were then entered according to my former determination (Sugita, '17 a). If the cortical thickness of the adult man be assumed as 3.00 mm. (the mean value of 2.0 to 4.0 mm.) and the corresponding thickness at each age be calculated on the basis of the course of increase in cortical thickness in the Albino (given in column F), the results given in column G — a mere inference, to be sure — are fairly in accord with the figures presented by Brodmann (column C).

In this connection, I had the opportunity, through the courtesy of Dr. W. H. F. Addison, to prepare sections and examine the cortical thickness at the dorsal part of the gyrus centralis anterior (regio Rolandica) from a child thirteen months old (material hardened in 4 per cent formaldehyde, imbedded in paraf


264 NAOKI SUGITA

fine, and stained by Nissl's method). The mean value of the cortical thickness at the summit of the gyrus was 3.55 mm., or within 10 per cent the value obtained by Brodmann at the same locality in the adult brain and on a section similarly prepared and measured (table 8) . So far, then, as this observation goes, it helps to support my conclusion presented earlier that the human cortex has attained nearly its full thickness at the age of fifteen months (Sugita, '17 a).^

VII. THE BRAIN WEIGHT, THE CORTICAL VOLUME, AND THE BODY

WEIGHT

Dhere and Lapicque ('98) and DuBois ('98 a, '98 b), working independently, found several important relations existing between the body and the brain weights in man and a number of other vertebrates. Recently DuBois ('13) has obtained results which he has formulated in following terms:

1) In species of vertebrates that are alike in organization of their nervous system and their shape, but differ in size, and also in the two sexes of one and the same species, the quantity of the brain increases; A) as the quotient of the superficial dimension divided by the cube root of the longitudinal dimension. B) as the product of the longitudinal dunension by the square of its cube root.

2) In individuals of one and the same species and of the same sex, but differing in size, the quantity of brain increases as the square of the cube root of the longitudinal dimension of the body.

So, briefly stated, 1) reads: in any species of vertebrates that are equal in organization, in form of activity and in shape, the weights of the respective brains are proportional to the 0.55 power

' According to a study by Fuchs ('83), the child is born without any myelinated fibers in the cerebral cortex. In the lamina zonalis the first myelination appears at five months, in the lamina pyramidalis at the end of the first year, while in the innermost layers we see some faintly stained fibers at two months. The fibrae arcuate (association fibers) appear clearly at seven months. Later the myelinated fibers increase in caliber and number as the age advances, and at eight years they attain nearly the appearance which they have in the adult cortex.


GROWTH OF THE CEREBRAL CORTEX 265

of the weights of bodies, and 2) the exponent of correlation within the same species is for all vertebrates the 0.22 power.

These relations were based on a series of observations, and this illuminating idea is now generally accepted as true.

The brain in general consists of the white and the gray matter, and in higher animals the gray matter as represented by the cerebral cortex occupies a relatively large part of the entire cerebrum. This cortex is the seat of a complex series of physiological nerve centers, and the possibility that it has definite quantitative relations with the body as a whole is suggested by the following statement made by Du Bois ('13) :

If the quantity of brain does not increase proportionally to the volume of the body, exprassed by the weight, it might be that this is really the case with regard to the superficial dimension, as being proportional with the receptive sensitive surfaces and with the sections of the muscles, thus measuring the passive and active relations of the animal to the outer world, for which in this waj" the quantity of brain can be a measure.

This statement, to be sure, is applied by DuBois to the weight or volume of the entire brain, but if the volume of the cortex stands in some definite relation to the volume of the entire brain, then the cortical volume should be also in a definite relation to the size or weight of the body.

The cortica' volume is determined by the area of surface of the cerebral hemisphere and the thickness of the cortex. The former factor is not easy to determine exactly, even in lissencephala, while in higher animals the hemispheres have many convolutions which increase still further the difficulty of this determination. In lissencephala, the surface area of the hemispheres in two brains, which are nearly similar in the form of cerebrum, are approximately comparable with squares of the corresponding diameters of the cerebra.

The cortical thickness, on the other hand, is not so hard to determine exactly. The average thickness of the cortex in different mammals is given in table 11, quoted from various sources, and, as seen from this table, it is not directly related to the size or weight of the brain, since, as Marburg's ('12) table shows, the


266 NAOKI SUGITA

cortical thickness in several primates ranges within rather narrow limits (2.3 mm. to 2.8 mm.), while the brain weight shows a distinctly wider range (82 grams to 400 grams) (table 11). In some cases indeed the smaller brain has a thicker cortex, even in the same family (e.g., the smaller hapale has a thicker cortex than the larger lemur) . But in general we may conclude with Brodmann ('09) that, within one and the same order or family of mammals, the large brain tends to have a larger average value for the cortical thickness.

The relative cortical volume has been formerly computed by me, employing the formula especially devised for this purpose, in the albino and the Norway rat brains, so that the two forms may be compared directly (Sugita, '18 b). The ratio of the cortical volumes in the adult Albino (brain weight, 2.0 grams) and the Norway (brain weight, 2.3 grams) is 1.31, as the relative cortical volumes are, respectively, 393 and 517 (Sugita, '18 b, table 15), and the ratio of the body surfaces in the two animals amounts also to 1.30, when the body weights of the adult albino and the Norway rats are taken as 300 grams and 450 grams, respectively. Moreover, the ratio of cortical volumes in the two forms at any given age will prove to be almost equal to the ratio of body surfaces of the two at the same age.'*

As above tested, the body weight and the cortical volume of the animals in the same family stand in a definite relation, at least in this instance. But, as we cannot compute the volume of the cortex in other mammals from the data given in table 11, the relation can not be tested further.

■' For example, according to my former presentation (Sugita, '18 b), the computed cortical volume in the Albino Group XV (brain weight, 1.54 grams) is about 346 and that in the Norway Group N XVIII (brain weight, 1.83 grams) is about 423, and according to another determination (Sugita, '18 a) these two groups may be regarded nearly equal in age, as the Albino brain weight would be about 18 per cent less than the Norway brain weight of the like age. The ratio in cortical volume of the above two is 1.22. The body weight corresponding to the brain weight of 1.54 grams in the albino rat is 64 grams and that corresponding to the brain weight of 1.83 grams in the Norway rat is 90 grams ('The Rat,' Donaldson, '15). The ratio of the body surface in the above two, therefore, is about 1.25, quite near to the ratio in cortical volume.


TABLE 11 Giving for several species of mammals the adult body weight and brain weight, the average cortical thickness and the name of author from whom the data for the cortical thickness or for the brain and body weights were cited, arranged in the order of decreasing body weight within each family of inammals. The abbreviations of the names of authors are as follows: B = Brodmann {'09), I — Isenschmid {'11), L = Lewis {'79), M= Marburg, {'12), S = Sugita {'17 a, '18 a, MS.)


OF MAMMALIA


Rodentia


Chiroptera


Marsvipialia


Primates


Prosimiae


Artiodactyla f et Carnivo- \ ra I


Insectivora


NAME OF SRECIES


Simia satyrus (orang-outang).

Hylobates

Cynocephalus hamadryas

Macacus rhesus (macaques). . .

Cercopithecus (long-tailed ape)

Lemur varius

Lemur

Hapale (marmoset)

Microcebus

Ovis musimon (sheep)

Felis domestica (cat)

Erinaceus europaeus (hedgehog)

Talpa europaea (mole)

Lepus cuniculus (rabbit)

Cavia cobaya (guinea-pig)

Mus norvegicus (Norway rat) . Mus norv. albinus (albino rat) Spermophilus citillus (groundsquirrel)

Mus musculus (mouse)

Pteropus edwardsii (vampire

bat)

Vespertilio murinus (bat)

Macropus giganteus (kangaroo)

Didelphys


BODY WEIGHT'


7,350 950 920 356

2,500

2,170

1,800

200

62

23,000 3,000


700 75

2,200 600 450 300

200 20


375 23


5,000 1,100


BR.\IN WEIGHT'


grains

400.0

130.0

142.0

82.0

85.0

28.7

23.0

8.0

1.9


100.0 30.0


3.5 1.3

10.0 4.5 2.5 2.0

2.2 0.4


AVERAGE CORTICAL THICKNESS


7.0 0.3


25.0 5.5


mm. 2.8 2.8 2.3 2.3

2.3 1.6 1.7 2.0 1.5

1.6(2.6)2

1.5(2.6)2


1.8 1.0

2.2 1.9 2.1 1.9

1.8 0.8


1.7 0.4


2.3 1.2


K tS

fa p S <


M

M M M

B M B B B

L L


1 The body and brain weights of some animals were not given by the author who has given the cortical thickness. In such cases the body and brain weights were taken from the list given by Weber ('96).

2 According to Lewis (79), the values given here without brackets were taken from Meynert and show the value measured on the slide and the values given within brackets were obtained by his own observation and represent the natural depth of the cortex.

267


268 NAOKI SUGITA

VIII. SIZE AND GROWTH CHANGES IN SOME NERVE CELLS IN THE

^VIAMMALIAN BRAIN

Albino rat. The results obtained by me regarding the size and the growth changes of the pyramidal cells and of the ganglion cells in the cerebral cortex of the albino rat were summarized in a previous study (Sugita, '18 c). Four of the conclusions are here quoted:

1. The full size of the pyramids in the lamina pyramidalis is cell body 21 x 27 m and nucleus 18 x 20 /x in the fresh condition (on the slide, respectively, 16 x 21 ju and 14xl5yu). The full size of the ganglion cells in the lamina ganglionaris is cell body 27 X 37 M and nucleus 23 x 25 ^ in the fresh condition (on the slide, respectively, 21 x 29 ^ and 18 x 19 m) 2. The cell body and the nucleus of the pyramids attain their maximum size at twenty to thirty days in age. Up to ten days they still retain their fetal morphology. After having passed the maximum size at about twenty-five daj^s, they diminish somewhat in size, but the internal structure differentiates as the age advances.

3. The cell body and the nucleus of the ganglion cells attain nearly their maximum size at ten days, when they remain still in fetal form. After this stage, the size of the cell body still increases slowly but steadily as the age advances, while the nucleus remains nearly unchanged in size throughout life.

4. Taking a general view of the data already presented in this series of studies, it is very interesting to observe that the thickness of the cortex, the total number of the cortical nerve cells, and the size of the cortical cells, all attain nearly their full values at the same age of twenty days; that is, at the weaning time of the albino rat.

For comparison with these results on the cells of the cerebral cortex, there are some observations by Addison ('11) on the postnatal growth of the Purkinje cells in the cerebellar cortex of the albino rat. His material was also obtained from the rat colony at The Wistar Institute and the cerebellum was fixed in Ohlmacher's solution, imbedded in paraffine, and stained with


GROWTH OF THE CEREBRAL CORTEX 269

carbol-thionine and acid fuchsin. A part of his results on the Purkinje cells is here quoted:

The Purkinje cells are easily distinguishable at birth along the inner boundary of the molecular layer by their relatively large size and lightly staining nucleus. These cells measure 12 x 7 m and nuclei 8 X 6.3 At. During the first week, there is great increase in size of both nucleus and cytoplasm. The main bulk of the latter is at the ectal pole and from it several fine processes radiate into the molecular layer. At eight days the cells measure 18 x 12 /x and nuclei 10 x 8 ^ to 12 x 9 IX. At eight to ten days there is definite change in form by the elongation of the cytoplasm of the ectal pole to form the main dendrite, the previously existing fine processes becoming its branches. At the same time all the dendries become arranged in one plane, and this plane is parallel to sections directed across the folia. Nissl granules appear in the cj^oplasm at eight to ten days. The arrangement of Purkinje cells changes with the increase in the surface area of the cortex. At birth they are arranged in two to three irregular rows; at three days in one to two irregular rows, and at five days in one continuous row. As growth of the cortex continues, the space intervening between the Purkinje cells becomes greater. Some nuclei reach their maximum size of 12 x 9 /x at eight days, while the cell bodies usually continue to grow, reaching a maximum size of 24 x 19 ^ at twenty days. The dendrites reach the outer limiting membrane when all the outer granule eel's have migrated (twenty-one to twentyfive days), and continue to develop new branches until a much later period as is .diown by a comparison of cells from a 31 day with cells from a 110-day cerebelhun.

From this it is plain that the Purkinje cells (cell bodies) of the albino rat cerebellum have also reached full size at about the weaning time (twenty days of age) .

From the foregoing, we see that the functional cortical cells both in the cerebrum and in the cerebellum reach their full size at an early age — before the weaning time — and though they continue to mature after that they change only slightly in size, sometimes even diminishing. Thus the cortical nerve elements are all precocious in their growth, which is nearly complete when the young become independent of the mother and their education begins. Addison ('11) has stated also that the development of motor control in the young rat is closely correlated with the completion of the cerebellum and the rat attains its full motor control when the cerebellum has attained structural


270 NAOKI SUGITA

maturity at twenty-one to twenty-five days of age. At that age the cells are nearly full size. We may conclude, therefore, at least regarding some of the nerve cells, that the beginning of functional education of the cells at twenty days is preceded by the attainment of nearly full size, and after this period there is very little change in size, though the internal structures mature as the age advances.

Mouse. A study in this field was made by Stefanowska ('98) on the cortical cells of the mouse. She stained the cells by the method of silver impregnation and studied mainly the development of the cell attachments. Her conclusions may be condensed as follows:

1. In the new-born mouse most of the cortical nerve cells have a simple morphology. 2. The cells are usually arranged in chains, disposed perpendicularly to the surface of the cortex. 3. Besides these, there are some groups of cells more advanced in developmen and having many dendrites, and cells which have the adult form having many, long, ramified dendrites. 4. The different parts of the cortex do not attain the same degree of development at the same time. Some cell groups are more precocious. 5. In the lamina multiformis and in the lamina ganglionaris, we find always the most advanced cells in large numbers. 6. In the lamina pyramidalis the development of the cells is very slow. On the ectal surface, near the pia mater, many cells not at all differentiated are often found. 7. At one day after birth, the dendrites of cortical cells are covered with varicosities. The axis-cylinders have also many nodal swellings. 8, As the neurons develop, the varicosities become more and more rare. At fifteen days, varicosities are no longer seen on the dendrites and the neurons at this age have completed their development. 9. The appearance of the piriform appendices on the dendrites is somewhat delayed. At ten days all pyramidal cells show these appendices. These latter are the constant feature of the neuron, while the varicosities are only a temporary formation. The piriform appendices may be the terminal apparatus of the dendrites. 10. The piriform appendices are the last element which appears on the cortical cells during growth. This fact seems to suggest the high importance of these appendices for this nerve function.

As seen from the foregoing, the morphological completeness in respect of the dendrites and the axis-cylinder of the cortical cells is attained at fifteen days or at the weaning time of the mouse also.


GROWTH OF THE CEREBRAL CORTEX


271


TABLE 12 Giving for man and other mammals the size of the largest ganglioncells in the lamina ganglionaris of the cerebral cortex as presented by different authors. Data are arranged according to the order of the average diameters


NAME OF SPECIES


Homo sapiens (man)

Homo sapiens (man)

Homo sapiens (man)

Homo sapiens (man)

Felis leo (lion)

Felis tigris (tiger)

Cercoleptiis caudivolvulus (kinkajou).

Ursus syriacus (bear)

Indris (babakoto)

Felis domestica (cat)

Cercopithecus mona (African monkey)

Elephas (elephant)

Lemur

Mus norvegicus (Norway rat)

Ovis musimon (sheep)

Sus (pig)

Mus norvegicus albinus (albino rat) . .

Lepus cuniculus (rabbit)

Lepus cuniculus (rabbit)

Pteropus edwardsii (vampire bat)

Mus musculus (mouse)


MAXIMUM SIZE


REPORTED IN MICBA


Linear diameters


Average

diameter or

square root

of the



product


60X120


85


55X126


83


53X106


75


40 X 80


57


60X133


90


60X100


78


50X110


74


53X100


73


44 X 80


59


32X106


58


40 X 72


54


35 X 60


46


SOX 70


46


33 X 48


40


23 X 65


39


27 X 48


36


30 X 42


36


18 X 60


33


18X 40


27


16X 36


24


18X 20


19


Author


Betz Lewis Brodmann Hammarberg

Brodmann

Brodmann

Brodmann

Brodmann

Brodmann

Lewis

Brodmann

Brodmann

Brodmann

Sugita

Lewis

Lewis

Sugita

Lewis

Brodmann

Brodmann

Isenschmid


There are no other systematic investigations on the postnatal development of the cortical nerve cells in mammals, although there are some studies on the growth of nerve cells in the fetus, among which the researches by His ('04) (see footnote 2), Koelliker ('96), and Vignal ('89) are the most important.

Table 12 was compiled by me in order to compare the size of the largest ganglion cells in the lamina ganglionaris (the fifth layer of Brodmann) of the cerebral cortex of man and some other mammals. The tabulated data were taken from Brodmann ('09), Lewis ('79, '82), Hammarberg ('95), and others.


272 NAOKI SUGITA

The results obtained by me (Sugita, '18 c) in the albino and the Norway rats have been also entered.

IX. THE SIZE OF THE LARGEST CORTICAL CELLS IN MAN AND SOME OTHER MAMMALS

From table 12 we can draw only very general conclusions as to the significance of the size of the largest cortical cells. The giant Betz cells even in man vary rather widely in size according to the different authors, probably owing largely to the different technical methods used, as has been pointed out repeatedly in the course of this paper.

From time to time attempts have been made to formulate a general interpretation of the size of the Betz cells and of the nerve cells in general. From the examination of table 12, it is seen that the values for the mean diameters do not, except in the very most general way, follow the size of the animal, but that the Felidae, even the cat, stand high in the series.

We are not able to contribute any general explanation for the size of these cells, although it may not be out of place to repeat that in the Norway rat with the heavier brain these cells are larger than in the albino rat with the lighter brain (Sugita, '18 c), and so will merely call attention to the various authors who have had something to say in the matter: Lewis ("79), Hughlings Jackson ('90), Schwalbe ('81), Barratt ('01), Dunn ('00, '02), Herrick ('02), Donaldson ('03), Campbell ('05), Boughton ('06), Johnston ('08), and Kidd ('15).

X. SUMMARY

1. In the present paper I have attempted to compare my conclusions regarding the development of the cortical elements in the brains of the albino and the Norway rats with the corresponding changes in other mammals. The data used for these comparisons were taken from various sources, but the comparisons are in many instances hampered by differences in technique or the lack of essential information.

2. The relations of the cortical thickness at different locali


GROWTH OF THE CEREBRAL CORTEX 273'

ties in the cerebrum are quite the same in the mouse and rabbit as in the rat. The development of the cortical thickness has proved to be similar in the mouse and guinea-pig: it attains nearly its full value at the weaning time of the animal.

3. The statement that the cortical thickness diminishes from the frontal to the occipital pole and from the dorsal to the ventral aspect probably holds true throughout mammals, including man.

4. The results given by different authors for the cortical thickness of human brain (averages or for each locality) are by no means in accord. Even for the same locality there are wide deviations. The best data indicate that the average cortical thickness of the adult human brain is about 3 mm.

5. The mode of increase in cortical thickness in man according to age appears to be similar to that in the albino rat, if the brains are compared at equivalent ages. The developmental stage of the brain of a new-born child corresponds to that of an albino rat of five days of age, and throughout the postnatal life the relative growth rate of the rat and man are as 30 to 1. The span of life 30 for man corresponds to 1 for the rat and the equivalent ages are represented by like fractions of the span of life. The human cortex probably attains nearly its full thickness at fifteen months, equivalent to twenty days of rat age.

6. The relative cortical volumes of the albino and the Norway rat brains, computed formerly by me (Sugita, '18 b), appear to be proportional to the surface areas of the entire bodies at the like age. This relation may be generally applicable within a given order of mammalia. The cortical thickness or the brain weight is in general only loosely correlated with the body weight or size of the animal.

7. The cortical nerve cells in the cerebruni and in the cerebellum of the albino rat are precocious in their growth, attaining almost the full size at twenty days, the weaning time. The maturation of the intracellular structures probably continues after the size is apparently completed. This process is shown also in the mouse.

8. The size of the Betz giant cells in the adult human cortex

THE JOURNAL OF COMPABATIVE NEUBOLOGT, VOL. 29, NO. 3


274 NAOKI SUGITA

(found ill the gyrus centralis anterior) is reported differently by different authors. The mean value is about 75 micra in average diameter.

9. The size of the cortical cells, especially the Betz motor ganglion cells, of adult animals has no clear relationship to brain size or body size. These cells are notably large in the Felidae.

10. As a general conclusion to this series of studies the following statement may be made:

The morphological organization of the cerebral cortex is generally precocious. The size of individual cortical nerve cells, the total number of cortical cells, and the thickness of the cortex, all attain nearly their full values at the same time and very early in life (corresponding to the weaning time in some rodents) , after which the maturation of internal structures of the cell body and the nucleus continues. The brain weight and the cortical volume continue to increase even after this stage throughout the postnatal life, though not so rapidly as during the early period. This later growth is due principally to the development of the cell attachments, intercellular tissues (neuroglia tissue and bloodvessels), the ingrowth of axons into the cortex and their myelination, which together separate the cells from each other, and cause an increase in cortical volume. The cortical volume is primarily dependent on the size of individual cortical cells and their total number and it appears in animals belonging to a given zoological order to have a definite relationship to the size (or area of surface) of the body of the animal.


GROWTH OF THE CEREBRAL CORTEX 275

LITERATURE CITED

Addison, VV. H. F. 1911 The development of the Purkinje cells and of the cortical layers in the cerebellum of the albino rat. Jour. Comp. Neur., vol. 21, no. 5.

Allen, Ezra 1912 The cessation of mitosis in the central nervous system of the albino rat. Jour. Comp. Neur., vol. 22, no. 6.

Allen, Jessie Blount 1904 The associative processes of the guinea-pig. A study of the psychical development of an animal with a nervous system well medullated at birth. Jour. Comp. Neur. and Psychol., vol. 14, no. 4.

Barratt, J. O. Wakelin 1901 Observations on the structure of the third, fourth, and sixth cranial nerves. Jour. Anat. and Physiol., vol. 35, p. 214.

BouGHTON, T. H. 1906 The increase in the number and size of the medullated fibers in the oculomotor nerve of the white rat and of the cat at different ages. Jour. Comp. Neur. and Psychol., vol. 16, pp. 153-165.

Brodmann, K. 1908 Uber Rindenmessungen. Centralbl. f. Nervenheilkunde u. Psychiatrie, Bd. 19.

1909 Vergleichende Lokalisationslehre der Grosshirnrinde. Leipzig. 1909 Antwort an Herrn Dr. Th. Kaes. tJber Rindenmessungen. Neurolog. Centralbl., Jahrgang 28, p. 635.

Campbell, A. W. 1905 Histological studies on the localisation of cortical function. Cambridge.

Dhere and Lapicque, Louis 1898 8ur le rapport entre la grandeur du corps et le developpement de I'encephale. Archives de Physiologie normale et pathologique, no. 4.

Donaldson, H. H. 1891 Cerebral localization. Am. Jour, of Psychol., vol. 4, no. 1.

1891 Anatomical observations on the brain and several sense-organs of the blind deaf-mute, Laura Dewey Bridgeman. II. On the thickness and structure of the cerebral cortex. Am. Jour, of Psychol., vol. 4, no. 2.

1897 The growth of the brain. New York.

1903 On a law determining the number of medullated nerve fibers innervating the thigh, shank, and foot of the frog— Rana virescens. Jour. Comp. Neur., vol. 13, no. 3.

1908 Review "Die Grosshirnrinde des Menschen" von Dr. Th. Kaes. Am. Jour. Anat., vol. 7, no. 4. Anat. Rec, no. 8. 1908 A comparison of the albino rat with man in respect to the growth of the brain and of the spinal cord. Jour. Comp. Neur., vol. 18, no. 4. 1915 The Rat. Memoirs of The Wistar Institute of Anatomy and Biology, no. 6. Dubois, Eugene 1898 Uber die Abhangigkeit des Hirngewichtes von der Korpergrosse bei den Saugetieren. Archiv f. Anthropologic, Bd. 25.

1898 tJber die Abhangigkeit des Hirngewichtes von der Korpergrosse beim Menschen. Archiv f. Anthropologie, Bd. 25.


276 NAOKI SUGITA

Dubois, EuGE^fE 1913 On the relation between the quantity of brain and the size of the body in vertebrates. Proceedings of the meeting of December 27, 1913. Koninklijke Akademie van Wetenschappen te Amsterdam, vol. 16.

Dunn, Elizabeth Hopkins 1900 The number and size of the nerve fibers innervating the skin and muscles of the thigh in the frog (Rana virescens brachycephala, Cope). Jour. Comp. Neur., vol. 10, no. 2. 1902 On the number and on the relation between diameter and distribution of the nerve fibers innervating the leg of the frog, Rana virescens brachycephala. Cope. Jour. Comp. Neur., vol. 12, no. 4.

FucHS, SiGMUND 1883 Zur Histogenese der menschlichen Grosshirnrinde. Sitzungsber. der K. Akad. der Wissenschaft, Wien., Bd. 88. III. Abtheil.

His, Wilhelm 1904 Die Entwickelung des menschlichen Gehirns wahrend der ersten Monate. Leipzig.

Hammarberg, Carl 1895 Studien liber Klinik und Pathologic der Idiotie nebst Untersuchungen tiber die normale Anatomie der Hirnrinde. Upsala.

Herrick, C. Judson 1902 A note on the significance of the size of nerve fibers in fishes. Jour. Comp. Neur., vol. 12.

Isenschmid, Robert 1911 Zur Kenntnis der Grosshirnrinde der Maus. Abh. Akad. Wiss. Berlin, physik-math. CI. Jahrg. 1911 Anh. no. 3.

Jackson, J. Huglings 1890 On convulsive seizures. British Medical Journal, vol. 1.

Johnston, J. B. 1908 On the significance of the caliber of the parts of the neurone in vertebrates. Jour. Comp. Neur. and Psychol., vol. 18, no. 6.

Kaes, Theodor 1905 Die Rindenbreite als wesentlicher Faktor zur Beurtheilung der Entwickelung des Gehirns und namentlich der Intelligenz. Neurolog. Centralbl., Jahrgang 24, Nr. 22. 1907 Die Grosshirnrinde des Menschen in ihren Massen und in ihren Fasergehalt. 2 volumes. Jena.

1909 tjber Rindenmessungen. Eine Erwiederung an Dr. K. Brodmann. Neurolog. Centralbl., Jahrgang 28, p. 178. 1909 Replik. Zu "Dr. Brodmanns Antwort an Rindenmessungen." Neurolog. Centralbl., Jahrgang 28, p. 639.

KiDD, Leonard J. 1915 Factors which determine the calibre of nerve cells and fibres. Review of Neurology and Psychiatry, vol. 13, pp. 1-27.

King, Helen Dean 1910 The effects of various fixatives on the brain of the albino rat, with an account of a method of preparing this material or a study of the cells in the cortex. Anat. Rec, vol. 4, pp. 214-244.

Lapicque, Louis 1907 Tableau gen6ra' du poids encephalique en ionction du poids du corps. Paris.

Lewis, W. Bevan 1878 Application of freezing methods to the microscopic examination of the brain. 'Brain,' Part 3, pp. 348-359. 1879 Re^arches on the comparative structure of the cortex cerebri. III. Phil. Trans., pp. 36-64.

1882 On the comparative structure of the brain in rodents. Phil. Trans., pp. 699-749.


GROWTH OF THE CEREBRAL CORTEX 277

Marburg, Otto 1907 Beitrage zui Kenntniss der Grosshirnrinde der Affen.

Arbeiten aus dem Neurologischen Institute an der Wiener UniversitJit

(Obersteiner). Bd. 16. Mayer, Otto 1912 Mikrometrische Untersuchungen iiberdie Zelldichtigkeit

der Grosshirnrinde bei den Affen. Jour. f. Psychol, u. Neurol., Bd.

19, Heft 6. Rose, M. 1912 Histologische Lokalisation der Grosshirnrinde bei kleinen

Saugetieren (Rodentia, Insectivora, Cheiroptera). Jour. f. Psychol.

u. Neurol., Bd. 19, Ergonzungshefte 2. ScHWALBE 1881 Lehrbuch der Neurologie. Erlangen. Stefanowska, Micheline 1898 Evolution des cellules nerveuses corticales

chez la souris apres la naissance. Annales de la Societe Royale des

Sciences med. et naturelles de Bruxelles, vo . 7. Sugita, Naoki 1917 Comparative studies on the growth of the cerebral cortex. I. On the changes in the size and shape of the cerebrum during

the postnatal growth of the brain. Albino rat. Jour. Comp. Neur.,

vol. 28, no. 3.

1917 a Comparative studies on the growth of the cerebral cortex.

II. On the increase in the thickness of the cerebral cortex during the postnatal growth of the brain. Albino rat. Jour. Comp. Neur., vol. 28, no. 3.

1918 Comparative studies on the growth of the cerebral cortex.

III. On the size and shape of the cerebrum in the Norway rat (Mus norvegicus) and a comparison of these with the corresponding characters in the albino rat. Jour. Comp. Neur., vol. 29, no. 1.

1918 a Comparative studies on the growth of the cerebral cortex.

IV. On the thickness of the cerebral cortex of the Norway rat (Mus norvegicus) and a comparison of the same with the cortical thickness in the Albino. Jour. Comp. Neur., vol. 29, no. 1.

1918 b Comparative studies on the growth of the cerebral cortex.

V. Part I. On the area of the cortex and on the number of cells in a unit volume, measured on the frontal and sagittal sections of the albino rat brain, together with the changes in these characters according to the growth of the brain. Part II. On the area of the cortex and on the number of cells in a unit volume, measured on the frontal and sagittal sections of the brain of the Norway rat (Mus norvegicus), compared with the corresponding data for the albino rat. Jour. Comp. Neur., vol. 29, no. 2.

1918 c Comparative studies on the growth of the cerebral cortex.

VI. Parti. On the increase in size and on the developmental changes of some nerve cells in the cerebral cortex of the albino rat during the growth of the brain. Part II. On the increase in size of some nerve cells in the cerebral cortex of the Norway rat (Mus norvegicus), compared with the corresponding changes in the albino rat. Jour. Comp.

. Neur., vol. 29, no. 2.

1918 d Comparative studies on the growth of the cerebral cortex.

VII. On the influence of starvation at an early age upon the development of the cerebral cortex. Albino rat. Jour. Comp. Neur., vol. 29, no. 3.


278 NAOKI SUGITA

ViERORDT, H. 1890 Das Massenwachstum der Korperorgane des Menschen.

Archiv f. Anatomie u. Physiologic, Anat. Abtheil., pp. 62-94. ViGNAL, William 1889 Developpement des elements du systeme nerveux

cerebro-spinal. Paris. De Vries, I. 1912 tjber die Zytoarchitektonik der Grosshirnrinde der Maus

und iiber die Beziehungen der einzelnen Zellschichten zum Corpus

Callosum auf Grund von experimentellen Ltisionen. Folia Neuro Biolog ca, Bd. 6, Nr. 4. Weber, Max 1896 Vorstudien iiber das Hirngew'cht der Saugetiere. Fest schr It iir Carl Gegenbaur. Pp. 105-12].


AUIHORS'S ABSTRACT OF THIS PAPER ISSUED BY THE BIBLIOGR.tPHIC SERVICE, .\PR1L 20


THE PERIPHERAL TERMINATIONS OF THE NERVUS LATERALIS IN SQUALUS SUCKLII

SYDNEY E. JOHNSON

From the Anatomical Laboratory of Northivestern University Medical School^

TEN FIGURES

The observations set forth below supplement the writer's previous paper on the structure and development of the lateral canal sense organs of Squalus acanthias and Mustelus canis.* In the investigation referred to the peripheral terminations of the lateral nerve were demonstrated in Mustelus canis, but not in Squalus acanthias, as fresh specimens of the latter species were unobtainable at that time. Last summer (July, '17), while at the Puget Sound Biological Station, I secured a number of living specimens of the Pacific coast dogfish, Squalus sucklii, which appears to be practically identical to the Atlantic form, Squalus acanthias. The histological structure of the lateral sense organs of these specimens was examined and the peripheral terminations of the lateral nerve were demonstrated by the pyridine silver method and also with methylene blue. These observations supply the omission which was necessitated in the paper referred to above.

The papers which deal specifically with the peripheral terminations of the nervus lateralis and which are of more than historic value are those of Retzius '92, v. Lenhossek '92, Bunker '97, Heilig '12, and Pfliller '14. They are discussed briefly in the writer's previous paper and need no further comment except to say that most attempts to stain the peripheral terminations of the lateral nerve have heretofore yielded rather meagre results.

1 Contribution No. 60.

-Jour. Comp. Neur., Vol. 28, No. 1.

279


280 SYDNEY E. JOHNSON

In comparing the lateral sensory canals of Mustelus canis and Squalls sucklii there are a number of differences to be noted. Perhaps the most striking is the difference in calibre of the sensory tubes. The sensory tubes (or canals) of Squalus are much smaller than would be found in a Mustelus specimen of the same size. The column of sensory epithelium is proportionately narrower in Squalus. A slight but apparently constant difference in the course of the lateral canals of the two species is seen in the slight elevation of the canal above the anal fin in Mustelus. There are other differences in the distribution of the canals, but they are less striking and have not been carefully examined. The lateral canals of both species lie chiefly in the dermis and their tubules pass directly ventrad for a short distance before making a sharp bend laterally to open on the surface of the integument. The surface tubules correspond in number with the ramuli of the lateral nerve and there are approximately five tubules for every four segments of the vertebral column.

The lateral nerve lies at a considerable depth from the sensory canal, especially in the anterior region, and its ramuli pass obliquely to the basilar membrane of the sensory column, where their fibers diverge caudad and cephalad to form a continuous longitudinal fiber zone just outside of the basilar membrane. This fiber zone differs from that described for Mustelus only in the fact that it contains a considerably smaller number of nerv^e fibers.

The sensory epithelium of Squalus sucklii differs considerably from that of Mustelus canis. It is much less extensive and the sensory cells are aggregated in smaller groups. This can be seen readily in transverse and longitudinal sections. In the former one to three sensory cells can ordinarily be seen in the cell clusters (fig. 1), and in the latter, usually three to six (figs. 2 and 10). The groups of sensory cells are somewhat more widely separated from each other than they are in Mustelus, and the sensory column appears to show a stronger tendency towards segmentation. This apparent segmentation of the column of sensory epithelium, however, bears no relationship to the normal body segments for there are usually more than ten


LATERAL SENSE ORGANS OF SQUALUS SUCKLII


281


clusters of these cells between adjacent surface tubules, and the tubules, in turn, are more numerous than the segments of the vertebral column. Nor is there any marked regularity in the number and size of the individual clusters of sensory cells. While the sensory column is thus essentially continuous throughout the entire length of the sensory canal it shows considerable



S71.G0L


FkZn


Fig. 1 Transverse section of the entire sensory canal of a Squalus sucklii garter. Camera lucida sketch. Iron haem. tech. X 432, | off. Can., canal wall; F6.Zn., longitudinal fiberzone; Sn.CL, secondary sensory cell; Sn. Col., sensory column; Spn., spindle cells.

variation in thickness. It becomes gradually thinner posteriorly and, as in Mustelus, it is usually thinner between adjacent ramuli of the lateral nerve. The base of the column of sensory cells is limited by a continuous basilar membrane.

The same types of cells can be distinguished in the lateral sensory epithelium of Squalus sucklii as were found in the sensory


282


SYDNEY E. JOHNSON


column of Mustelus and of Squalus acanthias. The hair cells or secondary sense cells are large, pear-shaped, and have centrally placed nuclei. In many specimens hair-like processes could be seen at their distal ends, but whether one or more for each cell has not been determined. The relative length of the cells is usually one-half to two-thirds the thickness of the sensory




T

fbZn



-Rml


Fig. 2 Longitudinal section o the lateral sensory column (Sii. Col.) of Squalus sucklii (adult). The sensory epithelium was drawn with the aid of a camera lucida from an iron haematoxylin preparation, and the nerve fibers were put in free hand from pyridine silver sections. The outlines of the canal wall {Can.) and the surface tubule {Tub.) are not drawn to scale but are greatly reduced in order to conserve space. For correct proportions, see figure 1. Sensory column, X 650, J off. Fhr., terminal fibrillae; Fb.Zn., longitudinal fiber zone; Gr-p., one group of secondary sensory cells (hair cells).

column. Spindle-shaped cells, basilar cells, and columnar cells constitute the supporting elements (see figs. 1, 2, 3 and 10). The rest of the canal wall is formed by a double layer of epithelial cells, both layers of which are continuous with the walls of the surface tubules and also with the columnar and stratified layers of the epidermis.


LATERAL SENSE ORGANS OF SQUALUS SUCKLII 283

The peripheral terminations of the lateral nerve. On reaching the base of the sensory column the fibers of the lateral ramuli diverge caudad and cephalad in the subbasilar fiber zone. This fiber zone is shown in longitudinal section in figures 2 and 4, and in transverse section in figures 1 and 3. The majority of the fibers are medullated but a few non-medullated fibers can be found. These can be traced back through the ramulus to the lateral nerve, which indicates that they are not simply nonmedullated branches of the large medullated fibers.

Two zones of distribution or branching of the nerve fibers appear well marked. Primary distribution takes place from the longitudinal fiber zone and the branching is almost entirely subbasilar (figs. 4 and 10), while a secondary zone of distribution or branching is located roughly between the limits marked by the .nuclei of the basilar cells and the proximal ends of the hair cells. It is from this zone that the fine fibrillae arise which pass out freely between the hair cells.

The primary branches are large and coarse as a rule (fig. 7), although many fine branches arise from this zone also (fig. 4). Branching of the fibers appears frequently to be dichotomous but not uncommonly three or more branches arise at the same level. This statement holds for both zones of distribution. Enlargements of considerable size are commonly seen at the level of branching of the nerve fibers (fig. 9), but it seems likely that the majority of these extra large varicosities" are caused by an over-deposit of silver at the points of branching. One or more fibers may rise from the subbasilar fiber zone to supply a single cluster of hair cells, and occasionally the fibrillae of a given fiber ramify in adjacent groups of hair cells (fig. 10). The medullary sheath is usually lost just outside of the basilar membrane.

The primary branches rise to a considerable height in the sensory epithelium — usually beyond the nuclei of the basal cells — where they form a rather rich plexiform network (figs. 4, 7, and 10) . This network forms the secondary zone of distribution and it is from it that the ultimate distribution of fibrillae to the hair cells takes place. While this secondary zone of distribution is present in the lateral sensory epithelium of Mustelus canis, it is


Grp.


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284


LATERAL SENSE ORGANS OF SQUALUS SUCKLII 285

not as uniformly developed and is much less conspicuous than it is in Squalus sucklii.

The fine fibrillae which arise from the secondary zone of distribution rise to various levels in the sensory epithelium. In many instances they can be traced to within a short distance of the outside limiting membrane (figs. 8 and 9). Varicosities of various sizes and shapes appear on the fibrillae at practically all levels and not infrequently at their distal extremities. In many cases the fibrillae appear to surround the bases of the hair cells (figs. 8 and 9), and in others, to pass out freely and separately between the hair cells.

The observations set forth above corroborate the results obtained on Mustelus canis. Only minor differences exist in the structure and innervation of the sensory epithelium of the two species. In Squalus sucklii the sensory epithelium is less extensive, there is a stronger suggestion of segmentation, and in nerve supply there is a more definite and conspicuously secondary zone of distribution.

A number of features which stand out in the embryonic and adult structure of the lateral canal system of Squalus and Mustelus appear to me to reflect doubt on the theory that this sytem of sense organs has a phylogenetic relationship with the segmental sense organs of certain invertebrates and that the system itself is segmental in the sense suggested by John Beard^ and W. H. Gaskell.^ The evidence, in part, against such a view may be

Fig. 3 Transverse section of the sensory column, showing the peculiar condition of two groups of hair cells (Grp.) existing side by side. Camera sketch, X 650. Nf., nerve fibers of the subbasilar fiber zone.

Fig. Longitudinal section of the lateral sensory column and the subbasilar fiber zone (Fb.Zn.). The secondary zone of distribution (Snd.Zn.) is also shown. Camera sketch. Pyridine silver tech. X 650, f off. Grp., group or cluster of hair cells; N.M.Fb., non-meduUated nerve fibers.

Fig. 5 Transverse section of the sensory column showing large fibers, and fibrillae diverging at a large varicosity. Pyridine silver tech. X 1525, | off.

Fig. 6 Transverse section of sensory epithelium showing long, fine fibers, and varicosities. Pyridine silver. X 650, j off.

3 See Zool. Anz., Bd. 7, 1884, p. 125 et seq., and also Bd. 8.

4 The Origin of Vertebrates, 1908.


286


SYDNEY E. JOHNSON


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LATERAL SENSE ORGANS OF SQUALUS SUCKLII 287

summarized briefly. The lateral sense organs do not develop in situ from successive or segmental patches of ectoderm along the side of the body, but each lateral sensory column arises from a thickened area of ectoderm located on the side of the head; this invades the posterior segments of the body not as a segmental structure, but in the form of a continuous column of epithelial cells. The grouping of the sensory cells in small clusters occurs comparatively late in the development of the embryo. It has been pointed out that these groups, when they do appear, are not segmental in the sense of the term as here employed. It is only in a degenerating or breaking down condition of the sensory ridges that isolated groups (pit-organs) of hair cells are found (e.g., dorsal series of sense organs in Squalus acanthias). These so called pit-organs show no relationship to the body segments either in their number or in their innervation. Further, their early development is identical with that of the lateral sense organs, the separated organs simply representing parts of what was earlier a continuous ridge of epithelium. So much for the developmental aspect.

The opinion has already been expressed that the slight tendency towards segmentation as seen in the lateral sensory column of the adult is probably of no significance as an argument for the segmentation theory. This is one of the anatomical features, however, which might be considered as pointing in that direction. Another one is seen in the innervation of the sensory epithelium by separate and successive ramuli (of the lateral nerve) which correspond in number and level with the surface tubules. The first condition named loses segmental significance when one remembers

Fig. 7 Longitudinal section of lateral sensory epithelium showing the extensive branching of a single large nerve fiber. Pyridine silver. X 1525, f off.

Fig. 8 Longitudinal section of a group of hair cells, showing various relations of the terminal fibrillae. Pyridine silver. X 650, J off. Var., varicosity.

Fig. 9 Section showing several slender fibrillae diverging from a large varicosity (Var.). Pyridine silver. X 650, I off.

Fig. 10 Longitudinal section of the lateral sensory column, showing two groups of hair cells (Grp.), and a network of fibers arising from the subbasilar fiber zone (Fb.Zn.). Pyridine silver. X 650, i off. B.CL, basal cell; N.M.Fb., non-meduUated nerve fibers.


288 SYDNEY E. JOHNSON

that there are from fifteen to twenty clusters of hair cells for every vertebral segment. Evidence based on the arrangement of the lateral ramuli and the surface tubules is unsatisfactory partly for the same reason and partly for other reasons. As shown above, the lateral ramuli and the surface tubules are considerably nore numerous than the vertebral segments and a constant ratio between the number of vertebrae and ramuli of the lateral nerve is wanting. Furthermore, these ramuli are merely the branches of distribution of a cranial nerve which differs from other cranial nerves only because of the fact that it supplies this remarkable type of sense organ and extends from the head to the caudal fin. In this connection it must be remembered that the fibers of the ramuli diverge at the ba§e of the sensory epithelium to form a continuous fiber zone from which the ultimate distribution takes place.

Further difficulty is met in attempting to relate the numerous organs of the head canals and of the cross-commissures to a corresponding number of ancestral segments.

In view of these considerations it seems improbable to me that the organs of the sensory canals have a phylogenetic history which would relate them either to the segmental sense organs of certain invertebrates, as claimed by Beard, Gaskell, and others, or to the posterior (body) segments of primitive vertebrates. To assume that the lateral sense organs have had such a past history involves the necessity of explaining why the innervation of the body organs should change from a segmental spinal nerve supply to a cranial nerve supply, and also, why the organs do not arise in situ on each segment of the body rather than from cephalic ectoderm which invades the posterior segments and carries with it its own nerve supply, probably from a corresponding primitive cephalic segment. It appears to me more likely that if the lateral sensory apparatus is segmental it is so only in relation to a limited number of cephalic segments. The several lines of organs, then, would represent simply an invasion or extension of a primitive cephalic sensory apparatus into other segments of the body.

Clearly the evidence at hand is not sufficient to warrant dogmatic statements or conclusions. The need is emphasized


LATERAL SENSE ORGANS OF SQUALUS SUCKLII 289

for further histological and embryological work, to be conducted on a comparative basis. The amphibia, especially, need further investigation along this line.

LITERATURE CITED

Bunker, F. S. 1897 On the structure of the sensory organs of the hxteral line

of Arneiurus nel)ulosus. Anat. Anz., Bd. 1.3. IIeilig, Karl 1912 ZurKenntnisderSeitenorgane von Fischen und Ampliihien.

Arch, fiir Anat. und Physiol. Lenhossek, M. v. 1892 Der feinere Bau und die Nervenendigungen der

Geschmacksknospen. Anat. Anz., Bd. 8. Pfuller, Albert 1914 Beitriige zur Kenntnis der Seitensinnesorgane und

Kopfanatomie der Macruriden. Jen. Zeitschr., Bd. 52. Retzius, G. 1892 Ueber die peripherische Endigungsweise des Gehornerven.

Biol. Unters., Bd. 1.


THE JOURNAL OF COMPARATIVE NECROLOOY, VOL. 29, NO. 3

author's abstract of this paper issued

BT THB bibliographic SERVICE, JUNE 1


ON THE DEVELOPMENT OF THE NERVE ENDORGANS IN THE EAR OF TRIGONOCEPHALUS JAPONICUS

TOKUYASU KUDO Anatomical Institute, Medical High School, Niigata, Echigo, Japan

ONE PLATE

The endorgans of the auditory nerve in reptiles have been investigated morphologically with considerable thoroughness. Many authors have interested themselves particularly in the macula neglecta (described for the Amphibia by Deiters in 1862 and given the name now in common use by Retzius) and this endorgan has been studied in various vertebrates, especially in the fishes, the Sauropsida, the mammals and even in man.

Relatively few embryological investigations, however, have been published on this subject. Concerning the genesis of the macula neglecta, Retzius and Alexander concluded that this organ originates from the crista acustica posterior, the former basing his opinion on its comparative anatomy and the latter on observations of its innervation. In Hertwig's Handbuch Krause briefly states that a small region of common neuroepithelium differentiates upon the separation of the saccular from the utricular portions. Fleissig, who, working on reptiles (Gecko), was the first to investigate extensively the development of the macula neglecta, disagrees with both of these statements and is of the opinion that the organ arises from the macula sacculi. The same conclusion is reached by Okagima in the case of Hynobius; but this author remarks that because in the Amphibia the macula neglecta lies within the sacculus, its origin in these forms is easier to determine than in the reptiles, where the macula is found in the utriculus. Corroboration of this view, according to which the macula neglecta arises from the neuroepithelium of the pars inferior, is found in Okagima's study of the salmon embryo and Wenig's recent work on Pelobates fuscus.

291


292 TOKUYASU KUDO

This simple interpretation of the genesis of the macula neglecta has been considerably complicated by the studies of P. and F. Sarasin, who claim to have found a second endorgan in the Caecillidae, for they distinguish two different maculae, one of which lies in a small evagination of the sacculus (macula neglecta of Retzius), the other in the floor of the utriculus (macula neglecta fundi utriculi). The existence of the latter was, however, denied by Retzius, in which opinion he is joined by Ayers. Retzius states: "Es geht nicht hervor, dass die am Boden des Utriculus der Caeciliiden gefundene Nervendstelle einer neu entdeckten Nervendstelle entspricht. Denn gerade am Boden des Utriculus liegt die von mir bei vielen Fischen, Reptilien und Vogeln entdeckte Nervendstelle, Welche von mir schon langst 'Macula neglecta ' genannt wurde. Es ist deshalb ganz unrichtig, wenn die Herren Sarasin die von ihnen bei Ichthyophis am Boden des Utriculis beschriebene Nervendstelle als von ihnen neu entdeckt bet achten und sie als eine 'Macula fundi utriculi' auffiihren. Die echte 'Macula neglecta' hegt am Boden des Utriculus oder Offnung des Canalis^utriculo-saccularis, oder auch-nach meiner Ansicht — bei den niederen Amphibien in der eigentiimlichen Ausstiilpung dieses Canalis, welches ich 'Pars neglecta' gennannt habe, bei den hoheren aber in einer von ihm abgetrennten Ausstiilpung der Sacculuswand." He adds that it would be interesting to know whether both of the endorgans as described by P. and F. Sarasin really do occur, in view of the fact that in all Amphibia that have been thoroughly studied a single macula neglecta occurs. Ayers contends that the new endorgan of the Sarasins is probably none other than the macula neglecta of Retzius. But Fleissig, from his study on the development of the labyrinth in Gecko, was able to demonstrate a transitional condition between the two described above. According to this author the macula neglecta of Retzius is to be regarded as a persisting organ in the sinus inferior, while only traces of the macula neglecta of the Sarasins occurs in adult individuals; and these traces may well be regarded as vestiges of Sarasin's macula, which is present as a developing organ only at a certain stage.


NERVE ENDORGANS IN THE EAR 293

To this much mooted and interesting question, then, I wish to contribute the modest results which I have been able to obtain from my study of Trigonocephalus japonicus.

The viperid embryos which were placed at my disposal comprise more than 27 stages^ (Suzuki-Okajimas series), of which I have employed four for the present study. The embryos were fixed in formol-alcohol, potassium bichromate-acetic and corrosive sublimate-acetic and were stored in alcohol until stained and imbedded in paraffin. Mainly frontal sections 10-15/* thick were made through the heads of the embryos. These were stained in toto with alcoholic borax carmine and Weigert's iron haematoxylin, and in the latter case orange G was employed as a counter stain. The two adult specimens were fixed in potassium bichromate, imbedded in celoidin and cut vertically through the head. These sections, 30/^ thick, were stained in haematoxylineosin and orange G.

Stage 1 (fig. 1). The embryo is coiled up in 4}-^ turns. Olfactory pit very deep. Wall of optic cup thickened anteriorly; lens solid. Fixation: corrosive-acetic. Stain: Weigert's iron haematoxylin ; sections 15^. Frontal sections of head and body.

The auditory vesicle, which is distended into a sac-like structure, is already oval in shape and, since it runs through 47 sections, is about 0.705 mm. in antero-posterior diameter. It lies some distance removed from the brain. Differentiation in the epithelial lining of the wall of the auditory vesicle is already apparent. Laterally the epithelium is flattened, while the medial and lower walls are stratified several cells deep and show here and there a mitotic figure. This thickened portion represents the common neuroepithelium which will later separate into the pars superior and the pars inferior. The ductus endolymphaticus is already tubular in form, with the dilated saccus endolymphaticus at the end.

Stage 2 (fig. 2) The embryo consists of 33^ coils. The parietal elevation is prominent. The lens is approximately as in the preceding stage; the retina moderately pigmented. The

^ The number includes 7 sectioned by the writer.


294 TOKUYASU KUDO

pocket-shaped olfactory pit is deep and the oral sinus deeply cleft. Fixation: formol-alcohol. Stain: alcoholic borax carmine. Sections 15^ in thickness cut frontally through head and entire body. The antero-posterior diameter of the auditory vesicle is calculated to be 0.48 mm., since it runs through 32 sections.

The auditory vesicle has at this stage undergone considerable development. The pars superior and the pars inferior are distinctly separated. The anterior and the posterior semicircular canals are now completely constricted off; but this is not the case with the lateral canal; i.e., this canal is not yet independent of, but still broadly in communication with the main lumen of the vesicle. The pars inferior is well differentiated and possesses an elongated oval swelling on the ventro-medial wall of the vesicle. The ductus endolymphaticus appears as a long slender tube.

In correspondence with the external change in form the epithelial lining is also well differentiated. The anterior canal, which is flattened in a medio-lateral (partly dorso-ventral) direction, widens out at its anterior end into an ampulla, and the crista acustica anterior is here represented by high epithelium which is continuous, without any decrease in thickness, with the macula utriculi. The same holds true for the crista laterahs, the epithelium of which is somewhat lower than that of the anterior crista. The medial and ventral walls of the utriculus are made up of especially high stratified epithelium, which, bending upon itself at the entrance of the pars inferior, passes over into this without any sharp boundary line. The tallest epithelium of the medial wall decreases somewhat in thickness as it passes over into the medial wall of the endolymphatic duct. The flattened lateral wall of the utriculus presents no points of especial interest. The crista posterior has moved back some distance and appears as a thickened zone of cells in several layers at the ventro-medial portion of the semicircular canal.

Stage 3 (fig. 3) The embryo consists of about 2| coils. On the surface of the body striations are observed which are transverse on the ventral and crossed on the dorsal surface. Fixation: Corrosive-acetic. Stain: alcoholic borax carmine.


NERVE ENDORGANS IN THE EAR 295

The 15 sections cut frontally through head and body. The membranous labyrinth runs through 102 sections and hence has an antero-posterior diameter of 1.53 mm.

The utriculus and the sacculus communicate by a narrow foramen, the canahs utriculo-saccularis ; the lateral semicircular canal is now an independent structure. * Each nerve endorgan is well developed. The crista anterior is mound-shaped; the crista lateralis is a thick cell mass which appears as a crescent in the sections. Both structures still maintain their connection with the crista utriculi.

The tall epithelium of the utricular froor, which diminishes in thickness as it passes upward, doubtless represents the first anlage of the macula neglecta Retzii. It is continuous with the macula partis inferioris through the still cylindrical epithelium of the canalis utriculo-saccularis. The macula partis inferior consists in this stage of an extended zone of neuroepithelium on the medial wall of the pars inferior and already there is to be seen on its margin several minimal though unmistakable points devoid of nuclei. The fine nerve-fiber bundles that arise from the ganglion acusticum show excellent mitotic figures where the fibers enter the macula. The low cylindrical epithelium of the ductus endolymphaticus is continuous with the tall neuroepithelium of the medial wall of the sacculus.

Stage 4 (fig. 4). The embryo, which is made up of 2^ coils, has the appearance of a fuUy developed individual. Its peculiar dermal spots are prominently displayed over the entire body. Fixation: formol. Stain: Alcoholic borax carmine. Sections: 15 M in thickness, cut frontally through the head.

The nerve endorgans are nearly all differentiated and on each the marginal zone free of nuclei may be recognized. The cristae anterior and posterior are separated from the macula utriculi by a low epithelium.

It is worthy of notice that the thick epithehum of the utricular wall shows clearly a border without nuclei and that it is differentiated from the epithelium of the canal by its greater thickness. It soon becomes thinner as it passes gradually over into the undifferentiated epithelium lining the vesicle. This thickening just


296 TOKUYASU KUDO

referred to may well be considered as the first anlage of the macula neglecta Retzii. In the wall of the canal there is no zone marked out by a cell-free border, although the epithelium is still rather thick, and this in turn is continuous with the mound-shaped swelling, the macula sacculi.

Corresponding to the external changes in form, the macula partis inferioris is now separated into the papillae basilaris and lagenae, which are still united by cubical epithelium. The crista posterior is quite separated from the macula sacculi by an unspecialized epithelium.

Stage 5. The embryo consists of 2| coils. The external characters are quite comparable to those of the preceding stage. Fixation: potassium bichromate. Stain: alcoholic borax carmine. The 15 M sections are cut frontally through the head.

The macula neglecta Retzii, which lies closely adjoining the canalis utriculo-saccularis, is mound-shaped and consists of two or three layers of cells. The maculae neglecta and sacculi are united by means of cubical epithelium except in the wall of the canal, where the epithelial cells are still tall.

The Adult Animal (fig. 5). Fixation in potassium bichromateacetic. Stain: haematoxylin-eosin and haematoxylin-orange G. The section are cut frontally through the head.

Among the endorgans the cristae anterior and posterior are composed of two- to three-layered epithelium and project as rounded protuberances into the lumen. The macula utriculi lies on the anterior-medial wall of the utriculus and is composed of auditory and supporting cells. The macula neglecta appears as a swelling in the proximity of the canalis utriculo-saccularis on the floor of the utriculus; its vesicular auditory cells rest upon one or two layers of supporting cells. The macula diminishes in thickness as it passes over into the simple cylindrical epithelium which makes up the wall of the canal and which is continued beyond in the wall of the sacculus. The tall epithelium found on the medial wall of the canal is also to be seen on and near the lateral wall. In several places within and near the canal the lining is thrown up into wave-like folds.


NERVE ENDORGANS IN THE EAR 297

DISCUSSION

The results of my studies, as presented above, agree on the origin of the macula neglecta with the view of Fleissig, for it has been shown that this macula is derived directly from the macula partis inferioris. Even after the neuroepithelium has been completely separated by the undifferentiated epithelium from the pars inferioris, the macula neglecta remains for a long time in connection with the macula sacculi.

The common neuroepithelium on the ventro-medial wall of the auditory vesicle of stage 1 begins to divide into the utricular and the saccular portions (stage 2), the histological changes in the epithelium keeping pace with the external changes in form. The more strictly utricular portion swells to form the crista anterior, crista lateralis and macula utriculi, which are united by means of a tall epithelium. The more strictly saccular portion, separated from the utricular portion by flattened epithe lium (stage 3) still extends from the medial wall of the canalis utriculo-saccularis upwards further into the floor of the utriculus.

After the macula saccularis has been differentiated (stage 3) the macula neglecta gradually protrudes more and more into the lumen and in stage 4 discloses a border free of nuclei, but is still connected by means of a cubical epithelial layer with the macula sacculi. Furthermore, the crista ampuUaris posterior becomes entirely free from the saccular portion, while the papillae basilaris and lagenae still maintain their connection with the macula saccularis by means of a bridge of cubical epithelium. In stage 5 the well developed macula neglecta may be seen as a moundshaped structure as in adult specimens.

The existence of two maculae neglectae I have failed to demonstrate in my Trigonocephalus material, although I have minutely examined the rather comprehensive series of the different stages. Fleissig says: "1) die macula sacculi, welche nicht mehr die ganze mediale Sacculuswand, sondem nur mehr deren unteresten Abschnitt einnimmt. Ein Epithel, das etwas hoher ist als das indifferente Wandepithel und ganz typisch in der Umgebung der Nervendstellen vorkommt, erstreckte sich von der Macula


298 TOKUYASU KUDO

sacculi nach aufwarts zum Foramen Utr.-Sacc, wo es zu einer zweiten Neuroepithelstelle — 2) Macula neglecta Sarasinianschwillt, die im Foramen Utr.- sacc. (an dessen hinterem Rand) gelegen, zum kleineren Teil in den Sacculus, zum grosseren in den Utriculus hineinragt. Von dieser erstreckt sich wieder ein niedriges Epithel in den Sinus inferior hinein zu persistierenden 3) Macula neglecta (Retzii). Beide Maculae neglectae stehen auf derselben Entwicklungsstufe."

Now even if the bulging endorgan found in the floor of the utriculus of stages 4 and 5 were not to be regarded as the macula neglecta Sarasini but rather as the macula neglecta Retzii, I would not feel justified in interpreting the thickened epithelium which extends through the canalis utriculo-saccularis to the macula saccularis as the macula Sarasini. The further the development progresses the thinner does the epithelium of the inner w^all of the alveus become as compared with the early stage of the auditoryvesicle. One may readily see that the medial wall of the alveus communis is lined with relatively taller epithelial cells in stage 2 than in stage 3. From this it is apparent that the neuroepithelium, except where it progressively develops into nerve endorgans, is destined to be reduced to indifferent epithelium, even though the time when it retrogresses be very variable.

According to my opinion, therefore, the tall epithelium of medial wall of the canal and its proximity represents a developmental stage in the neuroepithelium which later retrogresses. If this epithelium were to be interpreted as a nerve endorgan, the tall epithelium of other regions, as e.g., of the lateral wall of the canal and the medial wall of the utriculus and the ductus endolymphaticus, would have to be regarded as neuroepithelium, since these latter regions are quite similar in structure and arrangement of their epithelial cells to those in the medial wall of the canal. At any rate, the macula neglecta does not occur in my material as it has been pictured by Fleissig in his work. But it should be noted that in the adult snake the epithelium of the canalis utriculo-saccularis and its immediate environs is relatively much thicker as compared with the medial and lateral walls.


NERVE ENDORGANS IN THE EAR 299

From the above it appears, then, that the macula neglecta Retzii, which comes to He in the floor of the utriculus, arises from the neuroepithehum of the pars inferior, as was first estabhshed by Fleissig in the case of Gecko; but, as stated above, I am unable to demonstrate in my material any progressively developing endorgan which could represent the macula neglecta Sarasini.

Alexander has suggested that in the embryo of Echidna the tall epithelium at the mouth of the ductus endolymphaticus may represent the vestige of the Amphibian macula neglecta Sarasini. This tall epithelium, which is continuous with the neuroepithehum of the medial utricular wall, Fleissig has also observed in the embryo of Gecko, but his interpretation is a totally different one, for he does not consider it remarkable that the mouth of the ductus endolymphaticus, which is still in active growth, should possess tall epithelium where it passes suddenly into the neuroepithelial anlage of the medial utricular wall.

In conclusion I desire to record the observation that the three semicircular canals of Trigonocephalus japonicus do not develop synchronously, the medial and posterior canals anticipating the lateral canal in their development.

SUMMARY

1. The macula neglecta arises directly from the macula partis inferioris.

2. The occurrence of two maculae neglectae is not to be observed in my material : while the macula neglecta Retzii is well developed, there does not form a persistent macula Sarasini nor does this endorgan even develop temporarily as in Gecko (Fleissig).

3. The anterior and the posterior semicircular canals are separated off much earlier than the lateral canal,

Kyoto, Sept. 15, 1914.


300 TOKUYASU KUDO

LITERATURE CITED

The references marked with an asterisk (*) were available to the author.

ALEXA^^DER, G. 1900 tJber Entwickelung und Bau der Pars inferior labyrinthi der hoheren Wirbeltiere. Denkschr. d. k. Akad. d. Wiss. Math.Naturw. Kl. 70. Alexander, G. 1904 Entwickelung und Bau des inneren Gehororgans von Echidna aculeata. Jenaische Denkschr., Bd. 6.

1904 Zur Entwickelungsgeschichte und Anatomic des inneren Gehororgans der Monotremen. Centralbl. f. Phys. Bd. 17.

1905 Zur Frage der phylogenetischen, vicariierenden Ausbildung der Sinnesorgane (Talpa europaea und Spalax typhlus). Zeitschr. f. Psych, u. Phys. d. Sinnesorg. Bd. 38.

Ayers, H. 1892 Vertebrale Cephalogenesis. 2. A Contribution to the morphology of the Vertebrate Ear, etc. Journ. of Morph. vol. 6. 1893 The macula neglecta again. Anat. Anz. Bd. 8.

Deiters, D. 1862 Ueber das innere Gehororgan der Amphibien. Reichert u. Du Bois Re.ymonds Arch.

Fleissig, J. 1908 Die Entwickelung des Geckolabyrinthes. Ein Beitrag zur Entwickelung des Reptilienlabyrinthes. Anat. Hefte, Bd. 37.

Krause, R. 1906 Entwickelungsgeschichte des Gehororgans. Hertwigs Handbuch d. Vergl. u. Experim. Entw.-Lehre.

Krause, R. 1906 Das Gehororgan der Petromyzonten. Anat. Anz. Erg. -Heft 7. Bd. 29.

Okajima, K. 1911 Die Entwickelung des Gehororgans von Hynobius. Anat. Hefte. Bd. 45.

Okajima, K. 1911 Die Entwickelung der Macula neglecta beim Salmoembryo. Anat. Anz. Bd. 40.

Retzius, G. 1878 Zur Kenntniss von dem membranosen Gehorlabyrinth bei den Knorpelfischen. Arch. f. Anat. u. Phys. Anat. Abt. Jahrg.

Retzius, G. 1880 Zur Kenntniss des inneren Gehororgans der Wirbeltiere. Arch. f. Anat. u. Phys. Anat. Abt. Jahrg.

Sar.\sin, p. u. F. 1890 Ergebnisse naturwissenschaftlicher Forschungen auf Ceylon. Bd. 2.

Sarasin, p. u. F. 1892 Ueber das Gehororgan der Caeciliiden. Anat. Anz. Bd. 7.

StIjtz, L. 1912 Ueber sogenannte atypische Epithelformation im hautigen Labyrinth. -Eine rudimentiire Mac. negl. Morph. Jahrb. Bd. 44.

Wenig, J. 1913 Untersuchungen liber die Entwickelung der Gehororgane der Anamnia. Morph. Jahrb. Bd. 45.

WiTTMAACK 1911 Ueber sogenannte atypische Epithelformation im membranosen Labyrinth. Verh. d. Deutsch. Otol. Gesell.


PLATE


301


PLATE 1

Weigert's Iron haematoxylin, Leitz Achromat 6; Ocular I. Boraxcarmine. 3X1. Boraxcarmine. 3X1.


1 Stage 1. Stain:

2 Stage 2. Stain:

3 Stages. Stain:

4 Stage 4. Stain: Boraxcarmine. 3X1.

5 Adult. Stain: Haematoxylin-eosin, IXI,


ABBREVIATIONS


C.u.s. Canalis utriculo-saccularis

B., Brain

A. v., Auditory vesicle

Lag., Lagena

L.c, Lateral semicircular canal

A.c, Anterior semicircular canal

U., Utriculus


M.n., Macula neglecta M.S., Macula sacculi 0., Otolith P.i., Pars inferior P.S., Pars superior S., Sacculus