Acta Oto-Laryngologica

ISSN: 0001-6489 (Print) 1651-2251 (Online) Journal homepage: http://www.tandfonline.com/loi/ioto20

Interaction Between the Saccules and the Vertical Semicircular Canals J. Siegborn To cite this article: J. Siegborn (1976) Interaction Between the Saccules and the Vertical Semicircular Canals, Acta Oto-Laryngologica, 81:1-2, 83-90, DOI: 10.3109/00016487609107481 To link to this article: http://dx.doi.org/10.3109/00016487609107481

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Date: 16 March 2016, At: 01:02

Acta Otolaryngol 8 1 :83-90, 1976

INTERACTION BETWEEN THE SACCULES AND THE VERTICAL SEMICIRCULAR CANALS J . Siegborn From the Department

of Anatomy, Karolinska Instituter and the Department of Otolaryngology. Karolinska Sjukhuset. Stockholm, Sweden

(Received May 20, 1975)

For the experiments 39 cats were used. Selective sectioning of either the anterior or the posterior vertical ampullar nerves was performed bilaterally. Additionally in some cats the utricular nerves were cut, or the saccule extirpated on one or both sides. The otolith organs were stimulated by tilting around the bitemporal axis of the animals. Bilateral sectioning of the anterior ampullar nerve induced vertical nystagmus upwards, which disappeared, if the animals were tilted upside down. When the posterior ampullar nerves were cut bilaterally a vertical nystagmus downwards was obtained, and if the animals were tilted upside down there was a large increase in nystagmus frequency. After unilateral extirpation of the saccule, vertical nystagmus downwards was observed in 50 percent of these experiments. This nystagmus was modulated by tilting. However. if the saccules on both sides were extirpated, no nystagrnus could be elicited. The cause of these results is discussed.

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Abstract.

Opinions regarding the function of the saccule have differed widely. In 1883 Sewall opened the saccule of the ray with a knife and found that this caused serious disturbances in the animal’s equilibrium. Later, Versteegh ( 1927) was unable to observe any changes in the vestibular reflexes after destruction of both saccules in the rabbit. He therefore suggested that the saccule has no vestibular function. Other investigators have attributed hearing functions to the saccule. Ashcroft & Hallpike (1934) obtained action potentials from the saccular nerve after subjecting a frog’s labyrinth to low frequency vibrations. Von Bekesy ( 1935) observed, after exposing human subjects to loud sound beats, head movements that were synchronous with the beats. He

states that this was caused by a stimulation of the saccular otoliths. Jongkees (1950) rejected however, the idea of a cochlear function and suggested that sounds of low frequency might be regarded as rapidly changing linear accelerations, which stimulate the saccule. On the basis of morphological investigations, Lorente de Nb (1933) maintained that an acoustic function of the saccule cannot be accepted, because it has no connection with the auditory pathways and centres. Adrian (1942) demonstrated, that if the saccular otoliths were stimulated by linear acceleration, the activity in the vestibular nuclei changed. Subsequently, several other authors have shown that the saccule reacts to linear acceleration (Benjamins & Huizinga, 1927; H uizinga, I955 ;J ongkee s, 1950; Loewenstein, 1950; Magnus & de Kleyn, 1926; Perlman, 1940; Szentagothai , 1952). One of the first to observe the saccular influence on oculomotor reactions was Kubo (1906). He stimulated the saccule in the shark with a piece of cotton, which resulted in distinct eye movements. Quix (1924) considered that the rotating eye movements, in animals with their eyes in a lateral position, were released from the utricle, whereas Magnus & de Kleyn (1926) thought that these reactions originated from the saccule. Szentagothai (1952) demonstrated on dogs distinct eye movements after mechanical stimulaActa OIolaryngnl81

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J . Sieghorn

INF.

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Fig. 1 . Schematic diagram of the anatomical orientation of the two saccular areas on the left side.

tion of the otolith membrane in the saccule. Huizinga (1955) and Benjamins & Huizinga (1927, 1928) observed that counter-rolling of the eyes in pigeons disappeared after destruction of the saccule. Jongkees (1950) reported that rabbits react normally to thermal and rotatory stimuli after both unilateral and bilateral destruction of the saccules. Nor was Janeke (1968) able to find any alteration in the labyrinth responses provoked by rotation around a cephalocaudal axis in rabbits. Consequently he concluded that the function of the saccule is overshadowed by the intact utricle. Owada & Shizu (1960) resected the saccular nerve in rabbits, and found that the compensatory deviation of the eyeball was influenced by the saccule. In recent years it has become much easier to understand the function of the saccule, as more knowledge of the morphology of this organ has been acquired. Loewenstein et al. (1964) have shown that the saccular surface can be divided into two areas, depending on the orientation of the kinocilia and the stereocilia (Fig. I). In the superior area the kinocilia are oriented upwards in relation to the stereocilia, and in the inferior area downwards. It is known that these sensory cells are stimulated when the stereocilia bend towards the kinocilia (Loewenstein & Wersall, 1959). Fluur & Mellstrom (1970) demonstrated that it was possible, by electrical stimulation of the inferior area, to release eye movements Actu Otolaryngol81

downwards. If the superior area was stimulated, they observed eye movements upwards, and in some experiments, even vertical nystagmus directed downwards. In earlier experiments Fluur & Siegborn (1973a, b, c, d , 1974a, h ) investigated the interaction between the utricles and the semicircular canals, and demonstrated a very intimate cooperation between these sensory receptors. Thus, the aim of this investigation has been to find out if the same relation exists between the saccule and the vertical semicircular canals, and whether the saccule, as such is able to induce nystagmus. EXPERIMENTAL PRINCIPLES As previously mentioned electrical stimulation of the two areas of the saccule releases distinct eye movements upwards or downwards. Therefore it was decided to study the saccular influence on the vertical semicircular canals. Accordingly either the anterior or the posterior vertical ampullar nerve was selectively sectioned bilaterally. The superior area of the saccule was stimulated by tilting the animals upside down around their bitemporal axis. In some experiments the utricular interference was eliminated by sectioning the utricular nerves bilaterally. In other experiments the vestibular balance was disturbed by extirpation of the saccule on one, or both sides. MATERIALS A N D METHODS For the experiments 39 healthy cats were used. After intubation during ether anesthesia the cats were given Ketamine (Ketalar@, Parke-Davis) during the operation and the recording of eye movements. Ketamine is a nonbarbituric anesthetic with pronounced analgesic properties and a minimal effect on the vestibulo-ocular reflexes (Fluur & Siegborn, 1 9 7 4 ~ ) .The investigation was divided into four parts: I . Selective sectioning of either the anterior or the posterior vertical ampullar nerves, com-

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Interaction between saccules and semicircular canals

Fig. 2. Consecutive curves from a cat after selective

bilateral sectioning of the anterior ampullar nerves, followed by tilting upside down. The upper curve shows

bined with sectioning of the utricular nerves, followed by tilting the animal upside down around its bitemporal axis. 11. Selective sectioning of the anterior vertical ampullar nerves, followed by tilting the animal upside down around its bitemporal axis. 111. Selective sectioning of the posterior vertical ampullar nerves, followed by tilting the animal upside down around its bitemporal axis. IV. Unilateral and bilateral extirpation of the saccule, followed by tilting the animal upside down around its bitemporal axis. When sectioning the anterior ampullar nerve or the utricular nerve a small fenestration was made above the oval window according to a method described earlier by Fluur & Siegborn (1973u, d ) . For the sectioning of the posterior ampullar nerve, the bulla was explored and a fenestration was made behind the round

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electronystagrnography and the lower curve tilting of the table.

window according to the method described by Fluur & Siegborn ( 1 9 7 4 ~ ) .As it is almost impossible to selectively section the saccular nerve, the saccule was extirpated through the oval window. The animals were operated on a tilting table, where it was afterwards possible to stimulate the otolith organs by tilting the table all round the animals bitemporal axis. The angle of tilting was measured in degrees, where 0" was the normal position, 90" the nose-up position, 180" the upside-down position, and 270" the nose-down position. The eye movements were studied by electronystagmographical recordings with electrodes above and below the eye, and by visual inspection. RESULTS Selective sectioning of either anterior or posterior vertical ampullar nerves, combined with sectioning of utricular nerves, followed by Aria Otolaryngol 81

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J . Siegborn

Fig. 3. Consecutive curves from a cat after selective

bilateral sectioning of the posterior ampullar nerves, followed by tilting upside down. The upper curve shows

tilting the animal upside down around its bilateral axis Initially, both the anterior ampullar and the utricular nerves were sectioned bilaterally in 4 cats. This resulted in a very weak nystagmus upwards, which was totally inhibited if the animals were tilted upside down. In another series the posterior ampullar and the utricular nerves were cut bilaterally in 5 animals, which resulted in a total disappearance of nystagmus. If they were tilted upside down, nystagmus downwards was developed. Because of the weak nystagmus that occurred in these series, the following experiments included only sectioning of the vertical ampullar nerves. Selective sectioning of anterior vertical ampullar nerves, followed by tilting the animal upside down around its bitemporal axis After selective sectioning of the anterior ampullar nerves, 8 cats presented vertical Acta Otolaryngol81

electronystagrnography and the lower curve tilting of the table.

nystagmus upwards. The animals were then tilted to the 90" position around the bitemporal axis, which caused an increase in nystagmus frequency; whereas a decrease, amounting almost to a total inhibition, was observed in the 270" position. If the cats were then tilted from the nose-up position to the 180" position, the nystagrnus was totally inhibited. This inhibitive action on nystagmus frequency was observed already at the 135" position. However, if the animals were tilted forwards to the 270" position, the nystagmus was inhibited and remained so, until the 180" position was passed (Fig. 2). Selective sectioning of posterior vertical ampullar nerves, followed by tilting the animal upside down around its bitemporal axis At the next stage of the experiment, the posterior ampullar nerves were sectioned bilaterally in 8 cats, whereafter a weak vertical

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Interaction between succules and semicircular canals

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Fig. 4 . Schematic diagram of the labyrinth after bilateral

selective sectioning of the anterior ampullar nerves, in resting position, and when the animal is tilted upside down. The arrows indicate the orientation of the cells, i.e.

nystagmus downwards occurred. When the animals were tilted to the 90" position the nystagmus frequency decreased in 5 cats, and nystagmus was totally inhibited in 3 cats. On tilting the animals further backwards around the bitemporal axis, nystagmus reappeared successively after the 135" position was passed, and increased to a maximum, when the cats were in the upside-down position. On the other hand, if they were tilted forwards the nystagmus increased, and reached a maximum when the table was at the 210" position. Tilting from an initial position of 180" to the 150" position resulted in a slight decrease in nystagmus intensity. Tilting, in the opposite direction, to the 210" position caused an increase in nystagmus frequency (Fig. 3).

Unilateral and bilateral extirpation of the saccule, followed by tilting the unimul upside down around its bitemporul axis In 14 cats the saccule was extirpated on one side. A vertical nystagmus downwards was

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the direction in which they increase the discharge frequency. The number of arrows symbolizes discharge frequency.

observed in 7 animals, which increased in the upside down position, while in the other 7 no nystagmus was detectable in any position. In the cats with nystagmus, an increase was also seen at the 270" position, whereas a reduction in nystagmus frequency was observed in the nose-up position. Then the other saccule was also extirpated, which resulted in a total disappearance of nystagmus, which it was impossible to induce again by tilting.

DISCUSSION

In order to eliminate t h e influence from the utricles during tilting, the utricular nerves were cut in addition to bilateral sectioning of either the anterior or the posterior ampullar nerves. In these experiments no nystagmus or only a weak nystagmus developed, probably because the intensity of the impulses from the periphery were too low to trigger the nystagmus reflex. This seems especially to have been Acta Otolaryngol81

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88 J . Siegborn

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Fig. 5. Schematic diagram of the labyrinth after bilateral

selective sectioning of the posterior ampullar nerves, in resting position, and when the animal is tilted upside

the case after sectioning the posterior ampullar and the utricular nerves. This could be due either to diminished total input from the vestibular organs, or to the fact that the activity from the remaining, anterior vertical semicircular canals was antagonistic to the activity from the inferior saccular area, when the cats were in the normal position. From this stage of the experiment it may be concluded that, even in the absence of the utricles, the saccules are able to influence the activity from the vertical semicircular canals, so that a nystagmus induced by the latter can be changed. However, if only the anterior vertical ampullar nerves were cut, a vertical nystagmus upwards occurred as a result of the activity from the posterior, vertical semicircular canals. When the animals were tilted upside down the nystagmus was totally inhibited. In this position the superior saccular area, which causes eye movements upwards, is stimulated. Thus, the activity released from this area is antagonistic to the activity from the posterior semicircular canals (Fig. 4). Acto Otolaryngol 81

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down. Arrow indication the same as in Fig. 4. The number of arrows symbolizes discharge frequency.

There was also a combined influence on the activity from the posterior vertical semicircular canals from both the utricles and the saccules, which was demonstrated at the 150" and the 210" positions. At the next stage of this investigation the posterior, vertical ampullar nerves were sectioned bilaterally, and vertical nystagmus downwards was seen, which was due to the activity from the remaining anterior semicircular canals. When these animals were tilted upside down the nystagmus intensity increased. This could be explained by the fact that the anterior, vertical semicircular canals release eye movements upwards, i.e. in the same direction as those from the superior saccular area. Thus, these activities are synergistic in their effects on the extra ocular muscles (Fig. 5 ) . At the 150" and the 210" position, a combined activity of the saccules and the utricles on the activity from the anterior vertical semicircular canals was demonstrated. Finally, at the last stage of this investigation

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tnteruction between saccules and semicircular cunuls

the saccule was extirpated unilaterally, which in 50 percent of the cases induced a nystagmus downwards. Although the activities of the two saccules were synergistic, this unilateral destruction must have caused a disturbance in the balance between the two vestibulo-ocular reflex arcs, which induces nystagmus. However, a bilateral extirpation of the saccules does not seem to have disturbed the vestibular activity. These results are in accordance with those obtained by Fluur & Mellstrom (1970). They reported that in some cases, when electrically stimulating the superior area of the saccule they occasionally observed vertical nystagmus downwards. Thus, the results of this investigation have shown that, in principle, the saccule, as such, can not induce nystagmus, but this might be elicited by unilateral saccular damage. When studying the interaction between the saccules and the vertical semicircular canals, only the superior saccular area was stimulated. because it is not possible to stimulate the inferior area without relatively complicated equipment, since this has to be stimulated with forces exceeding 1 g in the direction of the sensory cells in this area. The results of these experiments lead to the general conclusion that the saccular activity modulates the impulses released from either the anterior or the posterior, vertical semicircular canals. Moreover, these results show that, like the utricles, the saccules play an important integrative role together with the vertical semicircular canals in the vestibular system. ZUSAMMENFASSUNG Fur die Versuche wurden 39 Katzen verwendet. Eine selektive Durchtrennung der anterioren oder posterioren vertikalen Ampullennerven wurde beidseitig durchgefuhrt. Zusitzlich wurden bei einigen Katzen die Utricularnerven oder der Sacculus auf einer Seite oder auf beiden Seiten entfernt. Die Stirnulierung der Otolithenorgane erfolgte durch Neigung der Tiere in der bitemporalen Achse. Bilaterale Durchschneidung der anterioren Ampullennerven induzierte einen vertikalen Nystagmus nach oben, der aufhorte. wenn die Tiere mit der Unterseite nach oben geneigt wurden. Wenn der posteriore

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Ampullennerv beidseitig abgetrennt wurde, erfolgte ein vertikaler Nystagmus nach unten, und bei Neigung der Tiere mit der Unterseite nach oben kam e s zu einer starken Zunahme der Nystagmusfrequenz. Nach unilateraler Entfernung des Sacculus wurde bei 50% der Versuche ein vertikaler Nystagmus nach unten beobachtet. Dieser Nystagmus konnte durch Kippung moduliert werden. Wurde jedoch der Sacculus auf beiden Seiten entfernt. konnte kein Nystagmus erzeugt werden. Der kausale Zusammenhang dieser Ergebnisse wird diskutiert.

REFERENCES Adrian, E. D. 1942. Discharges from the vestibular receptors in the cat. J Physiol (Lond) 101, 389. Ashcroft, D. W.& Hallpike, C. S. 1934. On the function of the saccule. J Laryngol Ofol49,450. Bekesy, G. von, 1935. Uber akustische Reizung des Vestibularisapparates. Pfliigers Arch 236, 59. Benjamins. C. E. & Huizinga, E. 1927. Untersuchungen uber die Funktion der Vestibularisapparates bei der Taube. Pfliigers Arch 217, 105. - 1928. Untersuchungen iiber die Funktion des Vestibularisapparates bei der Taube. Pfliigers Arch 220, 565.

Fluur, E. & Mellstrom, A. 1970. Saccular stimulation and oculomotor reactions. Larvngoscope 80, 1713. Fluur, E. & Siegborn, J . 1 9 7 3 ~ Interaction . between the utricles and the horizontal semicircular canals. Unilateral selective sectioning of the horizontal ampullar nerve, followed by tilting around the longitudinal axis. Actci Ofolarvngol (Stockh) 75, 17. 1973b. Interaction between the utricles and the horizontal semicircular canals. Unilateral selective sectioning of the horizontal ampullar nerve and the utricular nerve, followed by tilting around the longitudinal axis. Acfa Ofolaryngol (Stockh) 75, 393. 1 9 7 3 ~ Interaction . between the utricles and the horizontal semicircular canals. Sectioning of the horizontal ampullar nerve on one side and of the utricular nerve on the other, followed by tilting around the longitudinal axis. Acfa Ofolaryngol (Stockh) 75, 485. 1973d. The otolith organs and the nystagmus problem. Acfu Ofolarvngol (Stockh) 76, 438. 19740. Interaction between the utricles and the vertical semicircular canals. Bilateral selective sectioning of anterior and posterior ampullar nerves or unilateral selective sectioning of two vertical ampullar nerves followed by tilting around their bitemporal or longitudinal axis. Acra Otolaryngol (Stockh) 77, 80. 19746. Interaction between the utricles and the vertical semicircular canals. Unilateral selective sectioning of the horizontal and vertical ampullar nerves, followed bv tilting around the longitudinal axis. Acfn Ofolarynkol (Stockh) 77, 167. -. - 1 9 7 4 ~Ketamine . anesthesia in physiological studies of the vestibular apparatus in the cat.E.rp Neuro/43, 594. Huizinga, E. 1955. The physiological and clinical importance of experimental work on the pigeon's labyrinth. J Laryngol Ofol69, 260. Janeke, J. B. 1968. On nystagmus and otoliths. Thesis. Ams terdarn. Acra Otolaryngol81

90 J . Siegborn Jongkees, L. B. W. 1950. On the function of the saccule. Acta Otolaryngol (Stockh)38, 18. Kubo, I. 1906. Die vom N . acusticus ausgelosten Augenbewegungen. Pjiigers Arch 115, 457. Lorente de NO, R. 1933. Vestibulo-ocular reflex arc. Arch Neurol30, 245. Loewenstein, 0 . 1950. Labyrinth and equilibrium. Symp Soc Exp Biol4. 60. Loewenstein, 0. & Wersall, J. 1959. A functional interpretation of the electronmicroscopic structure of the sensory hairs in the cristae of the Elasmobranch Raja Clavata in terms of directional sensitivity. Nature (Lond)4701. 1807. Loewenstein, O., Osborne, M. & Wersdl, J. 1964. Structure and innervation of the sensory epithelia of the labyrinth in the Thornback Ray (Raja Clavata). Proc R Soc Lond (Biol) 160, I . Magnus, R. & de Kleyn, A. 1926. Function des Bogengangs und Otolithenapparates bei Saugern. Handh Norm Pathol Physiol 1 1 , 868. Owada, K. & Shim, S. I%O. The eye movement as a saccular function. Acta Otolaryngol (Stockh) 52, 63.

Perlman, H. B., 1940. The saccule observation from a differentiated reinforced area of the saccular wall in man. Acta Otolaryngol (Stockh) 32, 678. Quix, F. H . , 1924. Die Otolithenfunction in der Otologie. Z Hals Nas Ohrenheilkd 8 . 5 16. Sewall, H . 1883. Experiments upon the ears of fishes with reference to the function of equilibrium. J Physiol (Lond)B, 339. Siegborn, J. 1975. Interaction between the otolith organs and the semicircular canals. A n experimental study in the cat. Thesis. Stockholm. Szentagothai, J . 1952. Die Rolle der einzelnen Labyrinthreceptoren bei Orientation von Augen und Kopf im Raume. Akademiai Kiado, Budapest, Hungary. Versteegh. C. 1927. Ergebnisse partieller Labyrinthexstirpation bei Kaninchen. Actu Otolaryngol (Stockh) I / , 393. J . Siegborn, M . D . Dept. of Otolaryngology Karolinska Sjukhuser S-10401 Stockholm 60

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Acfa Ololaryngol81

Interaction between the saccules and the vertical semicircular canals.

For the experiments 39 cats were used. Selective sectioning of either the anterior or the posterior vertical ampullar nerves was performed bilaterally...
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