Anatomical and physiological studies on the growth of the inner ear of the albino rat 2 (1923)

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Wada T. Anatomical and physiological studies on the growth of the inner ear of the albino rat. (1923) Memoirs of the Wistar Institute of Anatomy and Biology, No. 10, Philadelphia. Rat Inner Ear (1923): I. Cochlea growth | II. Inception of hearing and cochlea growth | III. Growth of largest nerve cells in ganglion vestibulare | Final Summary | Literature Cited

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Anatomical and Physiological Studies on the Growth of the Inner Ear of the Albino Rat

II. Correlation Between the Inception of Hearing and the Growth of the Cochlea

The present study aims merely to compare in the rat the size of each element of the cochlea just before and just after the appearance of hearing and to ascertain the changes in the cochlea which take place during this phase. The rats which have sense of hearing show the so-called ' Ohrmuschelreflex ' of Preyer and other responses to auditory tests. Both the guinea- pig and rat react most evidently to sounds. The former animal responds usually five to six hours after birth. In the rat, however, the development of the function is, as already stated, relatively retarded and usually first appears at about ten days of age.

To test the presence of hearing there are several methods, as for example, Preyer V Ohrmuschelreflex' and the reflex closure of the eyelid, and these I used in making my observations. As the source of the sound I selected the hand clap, a whistle (Triller-pfeife, about c 4 ) and a low sound made by drawing in the breadth with nearly closed lips (about c 1 ).

Since it is my purpose merely to determine the first appear- ance of a response to sound, it is not nescessary to carry out such refined examinations as did Hunter ('14, '15, '18) Watson ('07), and others on white rats, and Marx ('09) on the guinea- pig, nor was it necessary to use the tuning-fork which by the way is not so good for tests on animals as for those on man. Since sometimes we may have a defect of hearing in animals, as shown by many investigators, it was deemed necessary to use several sources of sound and to take care not to produce ah* currents striking the test animal or to touch it in any way. For this purpose a large sheet of glass was placed between the source of sound and the rats to be tested. While the rat was resting I suddenly produced the sound and noted whether the rat responded. When the animals already had their eyes open the test was made from behind to avoid visual reflexes.

Observations

Rats at birth show no response to auditory stimuli. Most of them respond at twelve days of age very clearly, sometimes at ten to eleven days Under certain circumstances, the time of the reflex can be rather accurately noted. For example, while in the morning at ten days no reflex was noted it was present in the evening of the same day. Fortunately, I obtained five nine-day-old rats belonging to one litter and in nearly the same condition of nourishment and developnent. One of these responded to the test very evidently at noon on the ninth day, but the others did not. The sound which was effective was fairly intense, but to a faint and low-pitched sound this rat did not respond. In this case the external auditory canal was open. In the others there was in some a small open canal, but more or less closed by a cellular plug. In the latter cases I removed this obstruction without much difficulty or damage by washing, yet no reaction could be obtained to the stimuli. As it was to be expected, that also in the latter the reflexes would very shortly appear, all the cochleas of these young rats, both the not-hearing and hearing, were fixed by the method pre- viously described and later examined.

In chapter 1, in which I followed the growth changes in the constituents of the membranous cochlea and in its ganglion cells from birth to maturity, including ' not hearing ' and ' hearing ' rats, very evident differences were observed in rats between nine and twelve days of age. In view of this, it will be of in- terest to compare the measurements obtained from the 'not hearing' and 'hearing' rats nine days old and members of the same litter. From the differences thus obtained we can conclude concerning the developmental changes in the cochlea requisite for the first appearance of hearing, provided there are no obstacles in the sound-conducting apparatus or deficiencies in the central organ.

In table 113 are given the values for the size of the several constituents of the cochlea 'from a rat which did not hear and one which did, at nine days. The former data are the averages from four cochleas, while the latter are from two. The table shows in a striking way that where there is a significant differ- ence. The values obtained from the rat which could hear are usually larger than those of the rat which could not hear.

Among these measurements we see sometimes very marked and sometimes only slight differences. Only the radial distance between the labium vestibulare and the inner edge of the head of the inner pillar cell in the first two turns and the diameter of the nuclei of the inner and outer hair cells are in the former smaller than in the latter. In both instances, however, these smaller

TABLE 113

Comparison of the dimensions of the constituents of the cochlea in a hearing rat (H.) with those in a rat not hearing (N.) at nine days of age measurements

in micro

BAT

AGE

BODY WEIGHT

(N.) (H.)

days 9 9

grams 10 11

(N.) (H.)

1430 1434

Average

distance between two spiral ligaments

Breadth of membrana tectoria

TURN I

II

III

IV

Average

Th ids ness

(N.) (H.)

243

242

270 268

304 308

306 314

281 283

27 27

Breadth of membrana basilaris

TURN I

II

III

IV

AVERAGE

ZONA ZONA ARCUATA PECTINATA

(N.) (H.)

169 171

189 186

202 214

201 204

191 196

79 112 93 103

Distance between the habenula perforata and the outer corner of the inner hair cell

TURN I

II

III

IV

AVERAGE

(N.) (H.)

38 40

38 42

44

58

49 60

42 50

Distance between habenula perforata and the outer corner ol the outer pillar cell at foot*

TURN I

II

ill

IV

Average

(N.) (H.)

70

79

76

88

86 103

86 102

79 93

Height of greater epithelial ridge

TURN I

II

III

IV

AVERAGE

(N.) (H.)

36 42

40 43

41

48

42 50

40 46

Distance between the labium vestibulare and the habenula perforata

TURN I

II

III

IV

Average

(x.)

(H.)

83

85

108 104

137 140

145 150

118 120

TABLE 113 Continued

Distance between the labium vestibulare and the inner edge of the head of the

inner pillar cell

TURN I

II

III

IV

Average

(N.) (H.)

94

78

131

108

168 170

179 210

143 142

Height from basal plane to surface of pillar cells

TURN I

II

III

IV

AVERAGE

(N.) (H.)

32 40

33

42

35

45

36 45

34 43

Height of tunnel of Corti

TURN I

II

III

IV

AVERAGE

(N.) (H.)

20

18

14

11

16

Height of papilla spiralis at the third series of outer hair cells

TURN I

II

III

IV

AVERAGE

(N.) (H.)

28 42

28 43

27 39

28 36

28

40

Height of Hensen's cells

TURN I

II

ill

IV

AVERAGE

(N.) (H.)

20 42

23 45

23

38

24 30

23

39

Angle of lamina basilaris with plane of membrana basilaris degrees

TURN I

II

HI

IV

AVERAGE

(N.) (H.)

+7

+4

-8

7

Length of the inner and outer pillar cells

INNER

TURN I

II

III

IV

AVERAGE

(N.) (H.)

35 36

39 39

41 42

40 45

39

41

OUTER TURN I

II

III

IV

AVERAGE

WEIGHTED AVERAGE

(N.) (H.)

26 45

26

54

29 50

29 40

28 47

30 46

Volume of inner and outer hair cells

INNER: AVERAGE

OUTER: AVERAGE

WEIGHTED AVERAGE

(N.) (H.)

1798 1815

1277 1279

1407 1428

150

TABLE 113 Concluded Diameter of nuclei of the inner and outer hair cells

INNER: AVERAGE

OUTER: AVERAGE

WEIGHTED AVERAGE

(N.) (H.)

8.3 8.2

8.0 7.4

8.1

7.6

DEITERS' CELLS:

VOLUME M '

DIAMETER OF NUCLEI

LENGTH OF CELL BODY

PHALANGEAL PROCESS

(N.) (H.)

518 1193

7.0

7.2

14 32

22 22

Ganglion spirale: diameters computed

CELLS

NUCLEI

(N.) (H.)

13.6 13.7

8.5 8.6

values are marks of maturity. These changes in size accord with the results given in chapter 1 at twelve days of age, though there are some differences between them in the absolute values.

Figures 7 and 8 illustrate the outlines of the tympanic wall of the membranous cochlea in nine-day-old rats which could not and could hear, respectively. These figures have been drawn from the corresponding sections at the beginning of the middle turn of the cochlea and are comparable with figures 3 to 6 and 9 to 12. On comparing figures 7 and 8, the more noticeable differences appear to be the following.

The membrana tectoria is a bit longer in the hearing rat. The appearance and the position of it with reference to the surface of the papilla spiralis is also different. In the not-hearing cochlea it has an infantile look.

The outer end of the main part does not yet reach the second row of the outer hair cells and connects with the Hensen's prominence by a thick thread. There are also many fine fibers to be seen between the basal surface of the membrane and the papilla. In the hearing rat the fine fibers are absent. The membrane reaches already the row of the outer hair cells and there is a strong connection between this part and the terminal

ame (Schlussrahmen) of the lamina reticularis by a thick read as shown in figure 8 Thus the position of the membrane above the papilla depends a little bit upon the increase of the length of the membrane itself, but chiefly upon other factors such as the inward shifting of the papilla. The membrana basilaris as a whole shows a small increase o" breadth in the hearing rat. The zona arcuate, however, increases much in its breadth, while the zona pectinata rather decreases. This is due to the development of the pillar cells. The base of the inner and outer pillar cell spread much on the membrane. At the same time the length of the cells, especially of the outer, increases nearly twice as much as in the not-hearing rat.

Thus the foot of the outer pillar cell moves out ward, as Bottcher ('69, 72) stated, while the inner corner of the inner pillar cell does not move in any way, as the habenula perforata stands at a fixed point. This results in a change in the form of the arch of Corti. The hitherto outward inclined arch tends to bend inward and between both inner and outer cells arises a space, the tunnel of Corti. The appearance of the tunnel seems to have some relation to hearing. The tunnel is always present in the cochleas of hearing rats. Sometimes the tunnel is present in the lower turns, but not in the upper turns in the not-hearing rats. We can say, therefore, that it probably appears through all the turns before the special function of the cochlea begins. In this way the zona arcuata of the membrana basilaris increases its breadth.

The next striking change is the rapid increase in the size of the Deiters' cells, Hensen's cells, and the resultant change of the form, with an inward shifting, of the papilla spiralis.

The Deiters' cells increase their height very rapidly; the length of the cell body becomes over twice that in the not-hearing rat, but the processus phalangeus changes only slightly. Hen- sen's cells develop also, but not so much as Deiters' cells. The papilla spiralis thus increases in height. On the other hand, the greater epithelial ridge vanishes inwards from the inner supporting cells and appears as a furrow the sulcus spiralis internus. Through the pressure of these outward-lying cells the papilla spiralis swings inward as a whole, without really moving on the membrana basilaris. The lamina reticularis becomes inclined inward instead of outward and subtends a slight angle with the plane of the membrana basilaris. The distance from the labium vestibulare to the inner edge of the head of the inner pillar cell becomes smaller through the inward shifting of the papilla.

In the hair cells and the cells of the ganglion spirale we see a smaller difference between the hearing and not-hearing rats. Only the diameter of the nuclei of the hair cells in the hearing rat diminishes a little, as it continues to do in the adult cochlea.

All the changes just enumerated begin at the base of the cochlea and progress to the apex. Therefore we see the high and outward ascending papilla spiralis in turn I, while in the upper turns the papilla is not yet so developed, is smaller in all the constituents, and shows in general the characters of a younger and less mature cochlea conditions which disappear with age. This upper and immature part seems not to respond to the test for hearing. Indeed, my testing result is positive for sounds of high pitch, but not for low pitch. Therefore we conclude that the papilla spiralis develops functionally from base to apex and that when the papilla spiralis has developed in the basal turns, but not in the upper turns, it responds to sounds of high pitch alone.

Discussion

If we assume that our tests for hearing are trustworthy, then the differences between the size of the constituents of the cochlea in nine-day-old rats which could and could not hear will indicate what developmental changes in the cochlea of the albino rat are necessary for the appearance of the hearing reflex. Whether all the differences found by us are necessary is difficult to determine, and the problem is open for further study; but as the matter stands, our results give the closest correlation between structural changes and the appearance of function which has as yet been reported.

Kreidl and Yanase ('07) studied the differences between the not-hearing and hearing rat and summarized their results on page 509: "Kurz vor Eintritt des Horreflexes ist das Cortische Organ im wesentlichen fertig ausgebildet. " They publish no measurements nor data. The condition of the development of the organ of Corti described as 'fertig ausgebildet' is not suffi- ciently precise.

Further, on the same page they say, "Der auffalligste und, soweit die Untersuchungen bis jetzt eregben haben, einzige Unterchied, der zwischen dem anatomischen Bild des Labyrinthes eines neugeborenen Tieres, das den Reflex eben nochnichtaufweist, und dem eines solchen, dasdenselben zum ersten Male eben erkenn- an lasst, ist der, dass beim ersteren noch ein Zusammenhang zwis- chen Cortischem Organ und Cortischer Membran besteht, beim letzteren dagegen dieser Zusammenhang bereits gelost oder gelock- ert ist." Their observation is quite different from mine. In my case the papilla spiralis shows in the development of its constituent elements pretty large differences between the not-hearing and hearing rats. Therefore it seems probable that the changes in the growth and form of the papilla just before the first appearance of the special function, take place very quickly. Also we cannot agree to then* statement concerning the relation of the membrana tectoria to the papilla spiralis. In our preparations there is still a connection of the membrane with the terminal frame of the lamina reticularis through a thick thread in the cochlea of the rat which could hear (fig. 8) and also in that of the rat which could not hear (fig. 7).

This is a point on which opinions differ. While one opinion, represented by Kishi ('07) and others, is to the effect that this connection remains through life, the other, represented by Kolliker('67) and others, asserts the membrane projects free in the endolymph. I have never seen this connection in the adult cochlea, nor have I found such a connection of the membrane with the hairs of the hair cells, as Shambaugh ('10) described in the pig. In the young rats, at fifteen days for example, we very often see upon the terminal frame the broken remainder of this connecting thread. Whether this break arises through natural development or is the result of artificial manipulation it is hard to say. At any rate, Held's assertion ('90), that in an animal capable of hearing the membrana tectoria is never connected with the papilla spiralis, is not supported by my observation. That the freeing of the outer zone of the membrane is not absolutely necessary for the mediation of auditory impulses is demonstrated in the cochlea of birds, as shown by Hasse ('66), Retzius ('84), Sato ('17), and others. In these forms the membrane remains through life attached to the epithelial ridge.

My results agree with those of Hardesty ('15) on this point, though he obtained a tectorial membrane which floats free in the endolymph with its outer zone. Lane ('17) studied the correlation between the structure of the papilla spiralis and the appearance of hearing in the albino rat, but his description is brief and does not touch on this relation of the papilla to the tectorial membrane.

Thus the inception of hearing does not coincide with the detachment of the tectorial membrane from the papilla spiralis, but with the development of each constituent of the papilla spiralis and the membrane tectoria, as has been described. As these changes occur first at the base and then pass to the apex, the animal can perceive at first only the sounds of high pitch. One or two days later development is complete in all the turns, and then the rat can hear the sounds of lower pitch also. Thus the process of the development of the cochlea does not support the ' telephone theory' of audition, but on the contrary agrees with the conclusion that the papilla in different locations in the turns of the cochlea responds to sounds of a definite pitch, as Wittmaack ('07), Yoshii ('09), Hoessli ('12), and others have shown by experimental studies on the mammals.

Concerning the exact age of the first appearance of the function in the rat, there are several different statements. Lane ('17) found no response to sound before the twelfth day after birth, and on the sixteenth day he reports hearing well established. Kreidl and Yanase ('07) state that hearing begins in the rat at from twelve to fourteen days. My rats responded usually at ten to twelve days, but one at nine days. These differences depend in all probability on the vigor of the young during the first days of postnatal life, and it seems probable that exceptionally well-nourished young might develop precociously in this respec t. The intensity of the stimulus is important in determining the hearing reflex, as Small ('99) has stated. In my cases the young rats responded very evidently to intense sounds, while they reacted weakly or not at all to those which were faint. Thus only the intense sounds were perceived by the rat of nine days.

Conclusions

1. The hearing reflex was never obtained in rats less than nine days of age.

2. At nine days a single rat, one of five in a litter, responded to a sharp sound like clapping the hands and to a whistle of high pitch; the other four did not respond. At the tenth day some of the four reacted, and at the twelfth day all could hear.

3. The hearing reflex probably occurs early in young rats that are vigorous and well nourished.

4. To obtain the first hearing reflexes it is necessary to have rather strong sounds of high pitch.

5. A comparison of the histological structure of the cochlea in rats of nine days, one of which could hear and the other could not, shows clear differences in its development of the cochlea. These consist not in the detachment of the tectorial membrane from the papilla spiralis, but in the degree of differentiation of the constituents of the papilla. The tectorial membrane is connected in both cases at its outer end with the terminal frame of the lamina reticularis by a thick thread. The papilla is more differentiated in the hearing rat in several characters. The tectorial membrane has reached with its outer end the outermost row of the outer hair cells, but in the not-hearing rat it has not yet reached the second row of the cells.

6. The form of the papilla and its relation to the surrounding structures, especially to the tectorial membrane, are in the hearing rat at nine days very similar to those in the rat at twelve days of age, though there are some differences between them in ab- solute size.

7. The freeing of the tectorial membrane from the papilla spiralis is not necessary to the appearance of the hearing reflex, but the differentiation of the papilla, its shifting inward, its change in form and position under the membrana tectoria, appear to be important.

8. Since the papilla develops from the base toward the apex, it first reaches in the lower turn a high degree of differentiation, and this part first begins to function. Therefore the rat can hear only sounds of high pitch when it first responds.

9. This result accords with that well-known fact that the papilla in the lower turn responds to sounds of a high pitch, while in the upper turn it responds to sounds of low pitch.