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ON THE FUNCTION OF THE SACCULE
BY L. B. W. JONGKEES UTRECHT, HOLLAND
fter V e r s t e e g h (1927) found by experiment, no changes in the vestibular A reflexes in rabbits following the destruction of one or both maculae sacculi, i t has been generally accepted that the saccule plays no part in the maintenance of equilibrium.
However some data seem to suggest the possibility that an equilibrium- function in relation to the perception of linear accelerations does indeed exist ( J o n g k e e s & G r o e n 1946).
By means of the centrifuge it is possible to throw the saccular otoliths off their maculae, and, since this can be brought about by a centrifugal force, it seems highly probable that smaller linear accelerations which are within physio- logical limits, for example the gravitational force, have essentially the same effect and produce a change of pressure of the otolith on its macula.
The experiments of A s h c r o f t and H a l l p i k e (1934) on the frog showed that action potentials could be obtained from the saccular nerve when vibrations of rather low frequency (up to 1000 c. p. s.) reached the preparation. As sound is essentially an intermittent pressure, these vibrations submit the otolith to quickly changing linear accelerations. As higher tones give no saccular-nerve response and because hearing, as distinct from vibratory sense, has its highest sensitivity a t frequencies of about 3000 c. p. s. it is not at all improbable that the varying linear accelerations stimulate the saccule. I t is therefore under- standable how U n d r i t z & S a s s o s o w (1935) were able to damage the otolith organs by using very loud sounds or infra sound frequencies.
v. BPkPsy (1935) was able to produce movements of the head in subjects who were listening to very loud beaths (110-120 db above threshold) the movements being synchronous with the heats. He accepts the theory that this phenomenon is due to the production of an eddycurrent which causes pressure on the saccule.
A d r i a n (1943) measured electrical discharges from the vestibular receptors in the brainstem of cats. The number of discharges increased when the pressure of the saccular otolith on its macula was diminished by the action of linear accelerations or gravitational force.
L o w e n s t e i n (1949) found that in the ray the electrical discharges of the saccular nerve were influenced by vibrations and hy linear accelerations such as gravity.
Another argument was brought forward by P e r 1 m a n (1940) who had found a re-enforced area in the saccular wall in man. This area is placed in such a
From the Clinic for diseases of the ear, nose and throat (director: Prof. Dr. A. A. J . vmt
E g w m i d ) ond the Institute for Pharmacology (dirrctor: Prof . Dr. U . G. N i j l s m u ) University of UtrPcht, th(, ;\,*dherlaizds.
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L. B. W. J o n g ’ k e e s : On the Function of the Saccule 19
way that variations in pressure, caused by normal moyements of the stapes, are largely prevented from reaching the saccule.
Although V e r s t e e g h was not able to demonstrate changes i n rabhits fol- lowing destruction of the saccule, B e n j a m i n s and H u i z i n g a (1927) proved that the counter-rolling of the eyes of pigeons disappeared after destruction of the saccule, but not after destruction of the utricule. H a s e g a w a (1937) noted the disappearance of reactions to dorso-ventral accelerations after destruction of the sacculi of guinea pigs and frogs. The position of the head of the animal at rest also changes in these circumstances, the nose I)eing held at a higher level.
In summarizing the pros. and cons. of the attribution of vestibular function to the saccule the following condensation may lie of value.
Eqiiilihriziwz-f ziwtioti.
pro The S. has the same structure as the
utricule. Some utricular nerve-fibres pass through
the S. nerve. Destruction of the S. is brought about
by centrifuging and by infrasound frequencies.
The experiments of B e n j a m i n s & H u i z i n g a .
The experiments of H a s e g a w a. The experiments of A d r i a n . Totally deaf albino cats have normal S.
( L u r i e 1939). Following destruction of the utricular
nerve in rabbits, ( V e r s t e e g h 1.c.) the so-called progressive reactions and counter rotation of the eyes are still partly intact.
of the Sacciile ( S )
con The S. is a part of the pars inferior
Some S. nerve fibres run together with
The destruction of the S. by strong
The exper#iments of V e r s t e e g h. The experiments of A s h c r o f t & H a 11-
labyrinthi (,d e B u r 1 e t) (1935).
the cochlear nerve.
sounds.
p i k e .
L o r e n t e d e N b (1933) states: “An acoustic function (of the saccule) cannot be accepted because, although it has connections with the centres and pathways involved in the regulation of equilibrium, it has no connections with the pathways and centres involved in hearing”.
Thus we may conclude that there are many strong arguments in support of a vestibular function tieing possessed 1)y the saccule. That this was not found in the experiments of V e r s t e e g h (I. c.) may either be due to the fact that the utricule in mammals takes over the function of a destroyed saccule or alternatively that compensation conceals the effect on ordinary examination. In the latter case it might therefore be possible to find quantitative deviations.
For this reason I repeated Versteegh’s” experiments and tried to find quantitative changes in the reactions of the animals.
* I wish here to express my gratitude to Mr. Versteegh for his kindness in teaching me the operative procedure he used in his famous experiments.
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20 A c t a O t o - L a r y n g o l o g i c a
A4etli ods
The bulla ossea of the ear of rabbits is opened from the central side of the head, while the animal is under paraldehyde narcosis (1112 cc/kg by mouth). The lateral wall of the cochlea is then removed with a small hook brought into the round window; the oval window is opened and the stapes removed, the upper margin of the oval window being left intact. By means of a curette the lamina spiralis ossea is taken away so as to expose to view the whole utricular macula and its nerve. Then, with the aid of a sharp hook the saccular macula is destroyed. The operation is performed under a binocular microscope.
Fig. I .
In another series of aniinals the saccule was left intact as well as the superior part of the labyrinth and a small steel ball was placed in the opened vestibule. The size of the ball (weight about 7 mg) is so small that it cannot he handled with a forceps or pincette and therefore a magnetic device was employed to bring the ball into position. This device is a soft iron bar, magnetised by means of a coil encircling one end. An alternating current which may be sivitched on and off is passed through the coil. .4n alternating current is used in order that the iron bar should lose its magnetism as quickly as possible. The other end of the iron bar is excavated to fit the steel ball. When the ball is brought into its desired position it is disconnected by sivitcliing off the successfully done.
Since sterilizing this ball in spirit is followed by strong vestibular reaction hy the superior part of the labyrinth, it is necessary that i t be sterilized by boiling instead, which is best done in a small bottle lest it should get lost.
Twenty operations to destroy the saccule were performed. In 3 animals the operation was successful on both sides, in one other animal only on one side. In the remainder either too much or too little was destroyed.
9 halls were placed in the vestibule 1)ut only two operations proved to be successfully clone.
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L. R. W. J o n g ’ k e e s : On the Function of the Saccule 21
Results
I lvas able to corroborate V e r s t e e g h’s conclusion that destruction of one or both saccules has no influence on the spontaneous movements and position of the animal. Caloric reactions are essentially unchanged after the operation, as well as the cupulograms for nystagmus (horizontal, vertical and rotatory) in the turning test (fig. 2). The total counter rotation of the eyes is only decreased about 10 %. Lift and jumping reactions are normal; only on one occasion was a transient vertical positional nystagmus ohserved ( Jon g l tees
rc’evertheless some differences existed between the normal and the olxrated 1949).
animals.
I m pulse O/stc~nd
Fig. 2. Cupulograms. --- pre operative cupulogram for the horizontal and rotatory nystagmus. - - - idem post operative. - - - - - - pre operative cupulogram for the vertical
nystagmus. - - - - - idem post operative.
Experirne9ats 01% the parallel-szviitg ( J o n g k e e s Fr Groet i , 1946)
When a normal rabbit is put on the parallel swing and to this swing an excursion of up to 2 M (i. e. a linear acceleration of about 600 cm/sec2) is given, it is impossible to throw the animal off its balance. Its normal reactions are :
I . To place the long axis of its body in the direction of the acceleration. 2. To lay down on its abdomen with its legs wide apart. 3. After stopping the movements the animal stays in the same crouching
position for some time (1-2 minutes). The animals with destroyed saccules showed none of these reactions and
were easily thrown down at accelerations of about 300-400 cm/sec*. The animals did not lie down on the abdomen, and their legs maintained the normal position. After stopping the swing they were able to move about immediately. Following unilateral destruction no special tendency to move towards or away form the operated side was observed.
Exper imeuts with centrifugal force
When a normal rabbit is rotated in a centrifuge it adopts such a position that the component of gravity and the centrifugal force forms its new “vertical” plane.
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22 A c t a O t o - L a i y n g o l o g i c a
Tn a rabbit with destroyed left saccule the effect was as follows: Rotating with the left ear towards the centre, distance centre to the ear
is I M : At a speed of go'/sec the first deviation from the objective vertical plane
is to l)e seen. At 120' sec the deviation is 2 5 O . When the right ear faces the centre the first deviation is visihle a t 6oo/sec. At Izoo/sec it is 40'. This reaction is normal.
Bulbocapnine i ~ t jectioizs
As described 3y S p i e g e l and S c a l a small differences in tone may be
A rabbit with destroyed left saccule, seemingly quite normal in all its
I 1.55hi-s quick respiration, normal postural position, normal gait. rz.oohrs the head is turned to the right to an angle of 20' with the body
and simultaneously the head is tilted the left side being uppermost, making an angle of 20' with the horizontal plane.
12.05hr-s When the animal is brought into left side position, the correction is slightly but clearly quicker then when it is brought into right side position. When the body is placed in the side positions the head being free, the position of the head is normal in the left side position, hut there is a slight under- correction in the right side position.
detected with the aid of bulliocapnine.
reactions received an injection of 25 mg/kg bulbocapnine at I Ihrs.
The spontaneous position is normal. 12.15hrs No deviations. In the case of a bilaterally operated animal with the same dose of bulbo-
capnine, no unilateral predominance could be observed but for some 10 minutes the animal walked with its head nodding markedly up and down so that its Ioiver jaw struck the ground each time.
Following this observation we noticed that the same phenomenon was present in the other animals with destroyed saccules but only to a limited extent. I t is possible that this is the same phenomenon as the lifted head of H a s e g a w a ' s (I . c.) bi-desacculated frogs.
When the hi-desacculated rabbits are 1)lind-folded, their movements are extremely careful, being much more so than in normal blindfolded animals. In addition, they continually move their heads up and down.
Expevimertts with a steel ball
As the result of these experiments only point in a certain direction without providing any proof, I tried to obtain more definite information by stimulating the intact saccule in the living animal. A small steel ball placed in the opened vestibule and attracted by an oculists magnet produced results, mhich seem to me to be conclusive.
In two animals the operation proved to he successful as shown on X-ray film during life and by histological post mortem examination. In these animals no spontaneous deviations were found (fig. 3 and fig. 4).
On bringing the animals into the magnetic field, when the magnetic force pushed the 1)all medio cranially, the head moved in the direction of the acting
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L. B. W. J o n g , k e e s : O,n the Function of the Saccule 23
cochlea I :est
round window
middle ear
destroyed saccule
Fig. 3 A. Histological preparation showing the destructed saccule.
magnetic force with the operated side inclined towards the axis. When the current of the magnet was switched off the head moved back towards the normal position and so on ad libitum (fig. 5).
After two to three days these reactions gradually disappeared. As in the post mortem examination no trace of sensory cells could he found, the likely solution seems to be that this reaction originates from the saccule. However the saccule gradually dies and with this process the magnetic reaction dis- appears. If the reaction were utricular in origin there would have been no reason why it should later disappear, since the superior part of the labyrinth remains intact.
The trauyatic lesion to the vestibule together with the steel ball acting as foreign body are sufficient reasons for the production of marked damage to the saccule.
During the time in which the rabbits responded to magnetic action some other phenomena could also he observed.
I . O n the parallel swing the animals turn their heads until the operated side is horizontal to the floor of the swing.
2 . Side position with the operated side on top is corrected much more quicltly than side position with the normal side uppermost.
3. On the turning platform at I M distance from the centre there is a great difference between the reaction of the animals to rotation with the operated side and the normal side towards the axis. In the latter case the reactions are quite normal; in the former case the animals noticeably incline their bodies towards the centre. One example may illustrate this point, namely rabbit number 15. One day after operation on left labyrinth:
Rotation ( I M from axis) with left ear towards the centre at 6oo/sec. 30' deviation.
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24 A c t a O t o - L a r y n g o l o g i c a
COC
saccular nerve ~ round window
eel hall
imontory bone
Fig. 3B. Histological preparation showing the position of the steel ball in the inner ear.
At 180'/sec. with right ear towards centre 90' deviation. When a linear acceleration is given to an animal in the side to side direction,
a very strong reaction results when the acceleration is directed away from the operated ear, a normal one when it is directed away from the normal ear.
Conclusiolzs
Experiments on the parallel swing and on the turning table (centrifugal force) seem to prove that the presence of a normal saccule is necessary for normal reaction to stimulation by linear accelerations acting from one ear to the other.
When one saccule is destroyed the animal reacts less strongly to stimuli which cause an increased pressure of the otolith on the saccular macula. When a steel hall is introduced into the vestibule the reaction to mass forces caused by linear accelerations and to a magnetic force which cause a pressure of the ball on the saccule, is extremely strong, the reaction being a movement of the head away from the pressing ball, as if the animal attempts to decrease this pressure.
That no deviations in the normal behaviour of the aimal can be observed is perhaps due to the fact that linear accelerations acting from one side to the other are not frequently met with in normal life. The reactions to these stimuli must therefore be especially looked for. On the other .hand it may well be that the utricule takes over a part of the function normally carried out by the saccule.
The experiments of V e r s t e e g h , in which the normal behaviour of rabbits with destroyed sacculi remained unchanged, are verified, but when special
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L. R. W. J o n g i k e e s : On the Function of the Saccde 25
investigations are carried out deviations are found indicating that an increased pressure of the saccular otolith on its macula causes movements which attempt to decrease this pressure.
A I3
Fig. 5. Schematic drawing of the action of a magnet on the steel ball, brought into the pars inferior labyrinthi.
hl = magnet. S saccule. U = utricule. B = steel ball. P = promontory.
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26 A c t a O t o - L a r y n g o l o g i c a
SUMMARY
These experiments on rabbits suggest that: I. The destruction of one or two saccules does not alter the “normal”
vestibular reactions of rabbits. They sit and move normally, and thermal and rotating stimuli result in normal reactions.
2. Reactions to linear accelerations directed from one ear to the other are diminished after destruction of the sacculi. This is proved by experiments on the parallel swing, and on the centrifuge.
3. Reactions to linear acccelerations from one ear to the other are much stronger than normal when a steel ball brought into the vestibule without destruction of the saccule is pushed towards the saccular macula. Magnetic influence results in the same phenomena.
4. Increased pressure on the saccular macula causes movements which tend to decrease this pressure.
5. The saccule has a vestibular function and reacts to linear accelerations acting from one ear to the other.
REFERENCES
A d r i a n , E. D. 1943, J. Physiol. 101-389. A s h c r o f t , D. W. & H a l l p i k e , C. S. 1934, J. Laryng. & Otol. 49-450. v o n BCkesy , G. 1935, Pflugers Arch. ges. Physiol. 236-59. B e n j a r n i n s , C. E. & H u i z i n g a , E. 1927, Pflugers Arch. ges. Physiol. 247-105 d e B u r l e t , H. M. 1935, Acta Oto-laryng. 22-28:. H a s e g a w a, T. 1932, Zeitschr. Hals-Nasen-Ohrenheilk. 43-1%. J o a g k e e s , L. B. W. & G r o e n , J. J. 1946, J. Laryngol. & otol. 61-529. J o n g k e e s , L. B. W. 1949, J. physiol. in the press. d e K l e y n , A. & V e r s t e e g h , C. 1935, Acta Oto-Lar. 2 2 - 3 2 7 . L o r e n t e d e Nb, R. 1933, Laryngoscope 43-1. L ci w e n s t e i n , 0. 1949, Nederl. Keel-neus-oorheelk. Vereniging: Session: May. L LI r i e, M H. 1939, Laryngoscope 49-558. P e r l m a n , H. B. 1940, Arch. Oto-laryng. 5 2 4 7 8 . T i n d r i t z , W. & S a s s o s o w , R. 1935, Acta Oto-Lar. Stockh. 21-487. V e r s t e e g h, C. 1927, Acta Oto-laryng. 9-393.
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