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Optimization of the mechanical performance of a two-duct semicircular duct system--part 2: excitation of endolymph movements.

The endolymph flow inside the semicircular ducts is analytically investigated by considering a system of two hydrodynamically interconnected ducts. Rotation of this system adds an amount of motion (momentum) to parts of it. This results in an endolymph flow in generally all vestibular parts. The "external impulses" are the impulses which emerge by rotation of exclusively a particular vestibular part. The real impulses can be calculated from a set of equations which contain the external impulses. Analytical expressions are derived for the initial velocities in the ducts and for the maximum endolymph displacements. These formulae contain the external impulses and the ratios of: (1) the radii of crus commune and ducts (gamma), (2) the lengths of crus commune and ducts (lambda). It was proven that an interconnected system composed of two ducts, and also a system composed of two such semicircular duct systems, behaves as a pure rotation transducer (like a single duct does), also when it is rotated excentrically. Duct systems with polygonal and circular geometries were used to evaluate whether an optimal value of lambda would exist (gamma was already considered elsewhere). Optimum values of lambda in a range of about 0.10-0.52 were found. This rather wide range of values agrees with values from measurements. Optimization of an interconnected duct system appeared to be equal to optimization of a system composed of separate ducts.

Animals↗

Optimization of the mechanical performance of a two-duct semicircular duct system--part 1: dynamics and duct dimensions.

The classical representation of the semicircular duct system consists of three separate duct circuits. The ducts are, however, in reality, hydrodynamically interconnected. Muller & Verhagen (1988a,b) derived equations for the mechanical behaviour of an interconnected system with three ducts (anterior, posterior and horizontal). An analytical solution of these equations would, however, be too complex to provide surveyable formulae. A system of two interconnected ducts avoids this complexity whilst keeping the essentials of the coupling of ducts intact. The solution of the equation of motion leads to expressions for time constants and maximal endolymph excursions which are functions of morphological parameters, viz. the ratios of radii (gamma) and lengths (lambda) of the common vestibular part (crus commune or utriculus) and the ducts. The system possesses two short time constants which are shown to have similar values. The maximum endolymph displacements in the two ducts after a steplike stimulus are the products of the respective initial velocities and combinations of time constants. The initial velocities depend strongly on the position of the labyrinth with respect to the excitating rotation vector. Measured data of gamma and lambda are compared with the theoretical results. For gamma, excellent agreement was found. lambda is treated elsewhere.

Animals↗

Optimization of the mechanical performance of a two-duct semicircular duct system--part 3: the positioning of the ducts in the head.

In the majority of vertebrates, the horizontal duct of the vestibular system lies approximately in the yawing plane of the head. The positioning of the vertical ducts, however, is not in the pitch- and roll planes but the vertical ducts generally lie under an angle of about 30-45 degrees relative to the medial plane. Using the equations for a hydrodynamically interconnected two-duct system, optimal positions of the vertical and horizontal ducts in different vertebrate groups can be derived. It was stated that the mean response of the vertical ducts should be optimized. This leads to a symmetrical positioning of the vertical ducts with respect to the medial plane. In all observed vertebrate groups, a solution of mu =(pi-alpha)/2 is found (mu is the angle of the vertical ducts relative to the medial plane, alpha is the angle between the vertical duct planes). For alpha=90 degrees, this provides an equal sensitivity for pitch- and roll- movements. For alpha>90 degrees, a larger sensitivity for pitch movements is obtained, at the expense of a lower sensitivity for roll movements. It is argued that the angle alpha between the vertical ducts may vary from 90 to 120 degrees. In most vertebrates, the centre of mass is stabilized by e.g. fins, tri- or quadrupedal stability, a crawling body or upside-down resting positions (e.g. bats). Birds are generally biped, so in walking they are also rather sensitive to roll. These features are related to labyrinth positioning in the head.

Animals↗

Size limitations in semicircular duct systems

The present article discusses mechanical requirements and limitations which are applicable to the construction of the system of semicircular ducts, especially to its size. The simplified case of a single, uniform duct system has been considered which can be described by a second order equation of motion. The principal functional quantities for this rotation-sensor are: (1) response speed; (2) sensitivity; and (3) regular flow. The response speed of a single, uniform semicircular duct is characterized by the short time constant (T2) which is dependent on the duct radius (r). Its estimated range is from 0.04 ms in the smallest to 140 ms in the largest known labyrinth. The sensitivity is characterized by the maximal endolymph displacement after a step stimulus (xmax). Its estimated range is from 0.0016 &mgr;m to 5.97 mm (6.56 decades!), assuming an input angular velocity of omega=1 rad s-1. The Reynolds number is a measure for an undisturbed laminar flow. Its estimated range varies from 7.38.10(-4)to 45.1 for omega=1 rad s-1. The above data follow from graphs in which, for a single uniform duct, circuit radius (R) is plotted against duct radius (r) for labyrinths of 233 species belonging to different vertebrate-groups. A relation R =38.9. r1.60was determined. The smallest labyrinth was found in a carp larva (Cyprinus), the largest in a whale shark (Rhincodon). Large whales possess labyrinths of average mammalian size. It is revealed that semicircular duct size is bound by requirements concerning regular flow and by a too low response speed for large labyrinths, and by a too low sensitivity for small labyrinths. Other important quantities are mechanical amplification factors which are a consequence of more complex vestibular constructions than a single uniform duct circuit. Allometric relationships are interpreted as compromises between the quantities mentioned. A hypothesis for the relatively large semicircular duct sizes of fishes, especially Elasmobranchii, compared with mammals and birds is presented. Copyright 1999 Academic Press.

Journal Article↗

Experimental endolymphatic hydrops and its relief by interrupting the lateral semicircular duct in guinea pigs.

It has been demonstrated that endolymphatic hydrops can be produced in guinea pigs by obliteration of the endolymphatic sac and this phenomenon was reproduced in our own laboratory. Interruption of the lateral semicircular duct of animals with labyrinthine hydrops produced a diminution of the hydrops in 4 out of 8 cases, and these did not show any collapse in the cochlear duct. It was considered that the hydrops was diminished by drainage of the surplus endolymph into the perilymphatic space, and that the cochlear duct was kept secure from collapse because of its distance from the operated lateral semicircular duct and of the utriculo-endolymphatic valve. Persistence of hydrops in the other four cases was thought to be due to closure of the operated lateral semicircular duct or to labyrinthitis. Although this series is not comprehensive enough, it seems to indicate that interruption of the lateral semicircular duct has a possibility of diminishing labyrinthine hydrops, as in cases of Ménière's disease, without hearing disturbance, provided that complications do not develop. Further investigation with many more animals, for a longer period of time after the operation, is required to gain more precisely detailed information.

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Functional allometry of the semicircular ducts in subterranean mole-rats Cryptomys (Bathyergidae, Rodentia).

BACKGROUND: Since the spatial mobility of subterranean mole-rats is restricted and their skull strongly modified, morpho-functional regression of their vestibular organ may be expected. On the other hand, vestibular sense may be indispensable for orientation in a world deprived of most external sensory cues. Since vestibular sensitivity is determined by the size of the labyrinth, morphometrical analysis may be employed to assess the sensitivity and to test whether the organ is degenerate or progressively specialized. METHODS: We analyzed the shape and size of the membranous labyrinth of vestibular organs in toto in three species of African subterranean blind mole-rats of the genus Cryptomys (Bathyergidae) differing in body size yet not in habitats, ways of life, or employed orientation and locomotory strategies. The mechanical sensitivity of the cupula was estimated according to Oman et al. (1987. Acta Otolaryngol. (Stockh.), 103:1-13) for each of the three semicircular ducts. RESULTS: The size and shape of the vestibular organ changed predictably depending on species-specific (yet not individual) body mass. In some aspects, particularly the cross-sectional area, the ducts were larger than expected for a mammal of a comparable body size. In all species examined, the anterior semicircular ducts exhibited the highest sensitivity. CONCLUSIONS: The vestibular organs of blind subterranean mole-rats are not regressed morpho-functionally.

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Dimensions of the horizontal semicircular duct, ampulla and utricle in rat and guinea pig.

The dimensions of the membranous labyrinth partly determine the mechanical operation of the semicircular canal system. This study provides, for the first time, extensive measures in individual specimens of the sizes, cross-sectional shapes and areas of the horizontal semicircular duct, ampulla and utricle in the rat and the guinea pig. The membranous labyrinths were fixed in Karnovsky's fixative, exposed, photographed, sectioned, oriented perpendicular to the line of sight and then measured using a calibrated graticule in the eye piece of an operating microscope. As well as the expected size differences between these species, there are major differences in the shape of the utricle.

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A new quantitative model of total endolymph flow in the system of semicircular ducts.

1. A new concept of endolymph flow in the vertebrate vestibular system is presented. This approach describes quantitatively the flow in the entire system of three semicircular ducts interconnected by the utriculus and the crus commune. This approach is quite distinct from the classical theory in which the labyrinth is generally conceived to consist of three separate duct circuits. 2. The present approach shows the following set of distinct differences to the classical view: (a) In a labyrinth composed of three ducts perpendicular to each other the flow is non-zero in the other ducts when the labyrinth is rotated in the plane of a particular duct. (b) In a labyrinth with two equal ducts and with the duct planes under approximately 73 degrees the flow in one duct is zero when the rotation takes place in the plane of the other duct. Previous measurements of duct angles reflect this value surprisingly well. An obtuse or sharp angle between duct planes can lead to better performance of a particular labyrinth because the "external impulses" in the different ducts may amplify or compensate each other. (c) The behaviour of the flow in the entire labyrinth is a non-linear function of direction or rotation (cf. points (d), (e]. (d) Six time constants for the entire labyrinth can be distinguished (three long, three short); the flow in a particular duct is composed of six terms with these time constants. The composition of this flow and thus the relative importance of the terms depends on the positioning of the labyrinth with respect to the rotation vector. (e) The time constants also depend, for different labyrinths, on a shared influence of the dimensions of the ducts and the elastic properties of all three cupulae. (f) The forces in a particular duct depend also on the amount of motion the fluid will acquire in the other ducts. (g) The sensitivity of a particular duct depends also on the dimensions of the other parts in the vestibular system. 3. Equations for a system consisting of two ducts and for the classical single duct system are also given. Both systems are special cases of the three-duct system. The single duct equations are equivalent with equations given by Oman (1980) and Oman et al. (1987) which include the contribution of a wide utriculus. 4. The present theory of endolymph flow is mainly supported by the outcome of previously performed experiments concerning time constants and rotation of human subjects in different planes.(ABSTRACT TRUNCATED AT 400 WORDS)

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Dimensions of the horizontal semicircular duct, ampulla and utricle in the human.

This study provides measurements in individual specimens of the sizes, cross-sectional shapes and areas all around the path of fluid flow through the human horizontal semicircular duct, ampulla and utricle. These data were obtained from multiple measurements on individual specimens which had been fixed by immersion in Karnovsky's fixative and microdissected. The results are compared with similar measurements in the rat and guinea pig.

Animals↗

A mathematical approach enabling the calculation of the total endolymph flow in the semicircular ducts.

1. A mathematical treatment of the flow inside the vertebrate labyrinth is given. The main difference to former theories (e.g. the "torsion pendulum" theory) is that the entire system formed by the three semicircular ducts, interconnected by the crus commune and the utriculus, is considered, instead of a single duct circuit. 2. The theory consists of a geometrical description of a labyrinth rotating in space, the solution of the continuity equation, determination of the initial velocities in all the ducts in a "cupulometry" experiment and derivation of the equation of motion (e.o.m.). 3. Equations for a system consisting of two ducts and for the classical single-duct system are special cases of the three-duct system. 4. Three different methods for the solution of the e.o.m. are described: an analytical one, a Runge-Kutta simulation and an "asymptotic" method. The last method includes approximations of the solution of the e.o.m. on a long and a short time scale. Its advantage is that it gives an insight based on rather manageable formulae. 5. The physiological basis of the presented theory, biological applications and verification are given in a separate paper (Muller & Verhagen, 1988).

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A calcareous concretion in the posterior semicircular duct of a human labyrinth.

Temporal bones were acquired four hours post mortem from a 67-year-old cancer patient. During dissection of the left vestibular labyrinth, a glistening white, spherical concretion was found in the posterior semicircular duct near the ampulla. The object was subsequently studied by light and scanning electron microscopy, x-ray diffraction, and x-ray energy dispersive elemental analysis. It was composed of four concentric layers: an outer zone of tabular vaterite crystals, a colorless intermediate zone of spherulitic octacalcium phosphate (OCP), and a cloudy core with inner and outer zones both composed of OCP. Examination of the vestibular receptor organs revealed severe loss of hair cells on all three cristae. Very few otoconia were present in the utricle, although the gelatinous layer of the otoconial membrane was intact on the macular surface. During the year preceding his death, the patient had received 800 mg of the potentially ototoxic drug cis-platinum. The concretion described in this report was, however, probably connected with age-related degeneration rather than with any effect of the drug.

Aged↗

The organization of the horizontal semicircular duct, ampulla and utricle in the rat and guinea pig.

Microdissections of the labyrinth of the guinea pig and rat were carried out with the labyrinth in place in the skull. This enabled photographs to be taken from a standardized identified orientation so as to show the relation of the horizontal semicircular duct and utricle to the planes of the head, and changes in the horizontal duct and utricle during development. It was also possible to show, for the first time, the relation of the horizontal duct and utricle to major brainstem structures. Photographic evidence is presented of the distribution of dark cells around the horizontal duct and ampulla in the guinea pig and of postnatal developmental changes in dark cells in the rat.

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Semicircular duct and ampulla dimensions in cat, guinea pig and man.

Predictions from the classic theory of semicircular canal operation, the torsion pendulum model, depend upon labyrinthine dimensions and the physical properties of the endolymph. The dimensions of the semicircular canal, duct and ampulla in cat, guinea pig and man were determined from measurements of magnified sections of decalcified temporal bones. Estimates of the effect of shrinkage were obtained from measures in fresh material and it appears shrinkage is probably only a fairly small factor. The dimensions so obtained were used to provide new estimates of the short time constant and other mechanical parameters of the torsion pendulum model in the three species.

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