Otolithic membrane

Last updated
Otolithic membrane
Balance Disorder Illustration B.png
Details
System Vestibular system
Location Inner ear
Identifiers
Latin membrana statoconiorum
MeSH D010037
TA98 A15.3.03.085
FMA 75573
Anatomical terminology

The otolithic membrane is a fibrous structure located in the vestibular system of the inner ear. It plays a critical role in the brain's interpretation of equilibrium. The membrane serves to determine if the body or the head is tilted, in addition to the linear acceleration of the body. The linear acceleration could be in the horizontal direction as in a moving car or vertical acceleration such as that felt when an elevator moves up or down.

Contents

Structure

The utricle (left) is approximately horizontally oriented; the saccule (center) lies approximately vertical. The arrows indicate the local on-directions of the hair cells; and the thick black lines indicate the location of the striola. On the right you see a cross-section through the otolith membrane. Otoliths w CrossSection.jpg
The utricle (left) is approximately horizontally oriented; the saccule (center) lies approximately vertical. The arrows indicate the local on-directions of the hair cells; and the thick black lines indicate the location of the striola. On the right you see a cross-section through the otolith membrane.

The otolithic membrane is part of the otolith organs in the vestibular system. The otolith organs include the utricle and the saccule. The otolith organs are beds of sensory cells in the inner ear, specifically small patches of hair cells. Overlying the hair cells and their hair bundles is a gelatinous layer and above that layer is the otolithic membrane. [1] The utricle serves to measure horizontal accelerations and the saccule responds to vertical accelerations. The reason for this difference is the orientation of the macula in the two organs. The utricular macula lie horizontal in the utricle, while the saccular macula lies vertical in the saccule. Every hair cell in these sensory beds consist of 40-70 stereocilia and a kinocilium. [2] The stereocilia and kinocilium are embedded in the otolithic membrane and are essential in the function of the otolith organs. The hair cells are deflected by structures called otoconia.

Otoconia

Otoconia are crystals of calcium carbonate and make the otolithic membrane heavier than the structures and fluids surrounding it. [1] The otoconia are composite crystallites that overlie the macular sensory epithelium of the gravity receptors of most vertebrates and are required for optimal stimulus input of linear acceleration and gravity. [3] Fishes often have a single large crystal called an otolith, but otoconia from higher vertebrates have numerous crystals, and each apparently single crystal in fact has multiple crystallites that are composed of organic and inorganic components. Ultra-high resolution transmission electron microscopy of rat otoconia shows that the crystallites are 50-100 nm in diameter, have round edges and are highly ordered into laminae. [3] Biomineralization of otoliths and otoconia results mainly from the release of soluble calcium ions, which is in turn precipitated as calcium carbonate crystals. [4]

The mechanical coupling of the otoconia to the hair cell sensory stereocilia at the surface of the vestibular sensory epithelium is mediated by two layers of the extracellular matrix, each on with a specific role in the mechanical transduction process. [5] The first of these layers is the otolithic membrane which uniformly distributes the force of inertia of the non-uniform otoconia mass to all stereocilia bundles. The second layer formed by columnar filaments secures the membrane above the surface of the epithelium. [5]

Function

When the head tilts, gravity causes the otolithic membrane to shift relative to the sensory epithelium (macula). The resulting shearing motion between the otolithic membrane and the macula displaces the hair bundles, which are embedded in the lower, gelatinous surface of the membrane. This displacement of the hair bundles generates a receptor potential in the hair cells. [1] In addition to aiding in the sensing of tilting, the otolithic membrane helps the body detect linear accelerations. The greater relative mass of the membrane, due to the presence of the otoconia, causes it to lag behind the macula temporarily, leading to transient displacement of the hair bundle. [1]

One consequence of the similar effects exerted on otolithic hair cells by certain head tilts and linear accelerations is that otolith afferents cannot convey information that distinguishes between these two types of stimuli. Consequently, one might expect that these different stimuli would be rendered perceptually equivalent when visual feedback is absent, as occurs in the dark or when the eyes are closed. However, this is not the case because blindfolded subjects can discriminate between these two types of stimuli. [1]

The structure of the otolith organs enables them to sense both static displacements, as would be caused by tilting the head relative to the gravitational axis, and transient displacements caused by translational movements of the head. [1] The mass of the otolithic membrane relative to the surrounding endolymph, as well as the membrane's physical uncoupling from the underlying macula, means that hair bundle displacement will occur transiently in response to linear accelerations, and tonically in response to tilting of the head. [1] Prior to tilting, the axon has a high firing rate, which increases or decreases depending on the direction of tilt. When the head is returned to its original position, the firing level returns to baseline value. In similar fashion, transient increases or decreases in firing rate from spontaneous levels signal the direction of linear accelerations of the head. [1]

The range of orientations of hair cells within the utricle and saccule combine to effectively gauge the linear forces acting on the head at any moment, in all three dimensions. Tilts of the head off the horizontal plane and translational movements of the head in any direction stimulate a distinct subset of hair cells in the saccular and utricular maculae, while simultaneously suppressing responses of other hair cells in these organs. Ultimately, variations in hair cell polarity within the otolith organs produce patterns of vestibular nerve fiber activity that, at a population level, unambiguously encode head position and the forces that influence it. [1]

Hair bundles and the otolithic membrane

Studies performed by a team at the University of California, Los Angeles elucidated the movement of the active hair bundle under the otolithic membrane, as well as the coupling between the hair bundles and the membrane. [6] The researchers concluded that when coupled and loaded by the otolithic membrane, hair bundles of the bullfrog sacculus do not oscillate spontaneously but are poised in a dormant regime. However, when stimulated by a sinusoidal pulse, the bundles in the coupled system exhibit an active biphasic response similar to the "twitch" observed in individual bundles. The active bundle motion can generate sufficient force to move the otolithic membrane. Furthermore, the almost perfect entrainment between the hair bundles and the membrane demonstrates that coupling between the two is elastic rather than viscous. [6] A further study further demonstrated that the motion evoked in the hair cell bundles induced by the otolithic membrane, was found to be highly phase-locked which was consistent over large portions of the sensory epithelium. [7]

Clinical significance

Although the pathophysiology of otolithic dysfunction is poorly understood, a disorder of otolith function, at a peripheral or central level, may be suspected when a patient describes symptoms of false sensations of linear motion or tilt or shows signs of specific derangements of ocular motor and postural, orienting and balancing responses. When disorientation is severe the patient may describe symptoms which sound bizarre, raising doubts over the organic basis of the disease. It is important to understand otolithic involvement in a wider neurological context through knowledge of the otolith physiology and the characteristics of proven otolithic syndromes. [8]

Benign paroxysmal positional vertigo (BPPV) is the most common vestibular system disorder and occurs as a result of otoconia detaching from the otolithic membrane in the utricle and collecting in one of the semicircular canals. It is generally associated with natural age-related degeneration of the otolithic membrane. When the head is still, gravity causes the otoconia to clump and settle. When the head moves, the otoconia shift, which stimulates the cupula to send false signals to the brain, producing vertigo and triggering nystagmus. In addition to vertigo, symptoms of BPPV include dizziness, imbalance, difficulty concentrating, and nausea. [9]

The otolithic membrane can be affected in patients with Ménière's disease. Sudden falls without loss of consciousness (drop attacks) may be experienced by some people in the later stages of the disease, when they are referred to as Tumarkin attacks, or as Tumarkin's otolithic crisis. [10] [11] Those who experience such attacks (probably less than 10% of people with Meniere's disease) may report a sensation of being pushed sharply to the floor from behind. [12] The phenomenon is thought to be triggered by a sudden mechanical disturbance of the otolithic membrane that activates motoneurons in the vestibulospinal tract. [12]

Otolithic function can also be compromised after unilateral vestibular neurectomy. The illusion is that during centrifugal stimulation, a small luminous bar, fixed with respect to the observer, appears to be roll-tilited by the same amount that the observer feels to be roll-tilted. This illusion is felt symmetrically in normal patients, but after vestibular neuroectomy, patients perceive a reduce illusion when the force is directed toward their operated ear. [13]

Other animals

Otolithic membrane structure has been frequently studied in amphibians and reptiles in order to elucidate the differences and to understand how the membrane has evolved in various otolith organs. Otolithic membranes of utricles in reptiles and amphibians represent thin plates of non-uniform structure, while the otolithic membrane in the saccule resembles a large cobble-stone-like conglomerate of otoconia. In fish, amphibians and reptiles there is also a third otolith organ that is not present in humans, and is called the lagena. The otolithic membrane in the lagena of amphibians is poorly differentiated, but well differentiated in reptiles. This difference corresponds to the fact that when vertebrates began to inhabit the earth surface there was a reorganization of the membrane. [14] Over time, there was two changes that occurred in parallel when referring to the evolution of the otolithic membrane. First, otoliths that were present in amphibians and reptiles were replaced by a structurally differentiated otolithic membrane. Second, the spindle-shaped aragonitic otoconia were replaced by calcitic barrel-shaped otoconia. These two changes are referred to as the two directions of evolution of the otolithic membrane. [14]

Research

Finite element models

There are currently several techniques to model the otolithic membrane that all serve as a way for researchers, scientists and health professionals to illustrate and understand the membrane's structure and function. One of these techniques is referred to as a finite element method which divides the membrane into triangles and a computer is used to determine the linear combination of the functions that represent the displacement which solves a complex system of equations. [15] The finite element method was initially developed for use in fields such as mechanical engineering and civil engineering to solve elliptic partial differential equations (PDEs) and has had enormous success. The finite element method opposes another technique for solving PDEs, the finite difference method and has been shown to be more effective in modeling the otolithic membrane by several studies, but has also been opposed by other researchers. [15] Similar models have even been developed to take into account varying acceleration of gravity to model the effect of the otolithic membrane in environments with changing gravitational effects such as space, the Moon and other planets. [16]

Finite difference models

The alternative method used for modeling the otolithic membrane is the finite difference method, while the finite element method has advantages in handling complicated geometry, while difference method is more easily implemented. Difference models impose a rectangular grid over the shape of the otolithic membrane and use different boundary extrapolation schemes applied to boundary conditions. Another method uses an optimization technique to generate a non-uniform grid which conforms to the shape of the membrane, and then generates a grid via general coordinate transformations. [17] The main steps of such models include 1) place a set of points on the membrane (usually modeled as an irregular ellipse, 2) discretize partial differential equations and 3) solve the discrete equations. [18] There are also several parameters of the otolithic membrane that are important for the modeling process. Common parameters for similar models include, the modulus of elasticity, Poisson's ratio and the specific density of the otoconia. [19]

Other modeling techniques

One final type of model that researchers have used to understand the otolithic membrane is related to the membrane-hair cell bundle interaction. In the model, the membrane is treated as a Kelvin–Voigt material, meaning that it has both properties of viscosity and elasticity. For this technique, the process of transformation of information in the chain sensing linear acceleration is taken into account, starting from an external acceleration and ending at hair cell depolarization. The model shows that a response is dependent on two factors which are the spatial dependence of gel displacement and the spatial distribution of stereocilia height in the hair cell bundle. [20]

Related Research Articles

<span class="mw-page-title-main">Inner ear</span> Innermost part of the vertebrate ear

The inner ear is the innermost part of the vertebrate ear. In vertebrates, the inner ear is mainly responsible for sound detection and balance. In mammals, it consists of the bony labyrinth, a hollow cavity in the temporal bone of the skull with a system of passages comprising two main functional parts:

<span class="mw-page-title-main">Sense of balance</span> Physiological sense regarding posture

The sense of balance or equilibrioception is the perception of balance and spatial orientation. It helps prevent humans and nonhuman animals from falling over when standing or moving. Equilibrioception is the result of a number of sensory systems working together; the eyes, the inner ears, and the body's sense of where it is in space (proprioception) ideally need to be intact.

<span class="mw-page-title-main">Vestibulocochlear nerve</span> Cranial nerve VIII, for hearing and balance

The vestibulocochlear nerve or auditory vestibular nerve, also known as the eighth cranial nerve, cranial nerve VIII, or simply CN VIII, is a cranial nerve that transmits sound and equilibrium (balance) information from the inner ear to the brain. Through olivocochlear fibers, it also transmits motor and modulatory information from the superior olivary complex in the brainstem to the cochlea.

<span class="mw-page-title-main">Semicircular canals</span> Organ located in innermost part of ear

The semicircular canals or semicircular ducts are three semicircular, interconnected tubes located in the innermost part of each ear, the inner ear. The three canals are the horizontal, superior and posterior semicircular canals.

<span class="mw-page-title-main">Utricle (ear)</span> Membranous labyrinth in the vestibule of ear

The utricle and saccule are the two otolith organs in the vertebrate inner ear. They are part of the balancing system in the vestibule of the bony labyrinth. They use small stones and a viscous fluid to stimulate hair cells to detect motion and orientation. The utricle detects linear accelerations and head-tilts in the horizontal plane. The word utricle comes from Latin uter 'leather bag'.

<span class="mw-page-title-main">Saccule</span> Bed of sensory cells in the inner ear

The saccule is a bed of sensory cells in the inner ear. It translates head movements into neural impulses for the brain to interpret. The saccule detects linear accelerations and head tilts in the vertical plane. When the head moves vertically, the sensory cells of the saccule are disturbed and the neurons connected to them begin transmitting impulses to the brain. These impulses travel along the vestibular portion of the eighth cranial nerve to the vestibular nuclei in the brainstem.

<span class="mw-page-title-main">Vestibular system</span> Sensory system that facilitates body balance

The vestibular system, in vertebrates, is a sensory system that creates the sense of balance and spatial orientation for the purpose of coordinating movement with balance. Together with the cochlea, a part of the auditory system, it constitutes the labyrinth of the inner ear in most mammals.

Spatial disorientation is the inability to determine position or relative motion, commonly occurring during periods of challenging visibility, since vision is the dominant sense for orientation. The auditory system, vestibular system, and proprioceptive system collectively work to coordinate movement with balance, and can also create illusory nonvisual sensations, resulting in spatial disorientation in the absence of strong visual cues.

<span class="mw-page-title-main">Hair cell</span> Auditory sensory receptor nerve cells

Hair cells are the sensory receptors of both the auditory system and the vestibular system in the ears of all vertebrates, and in the lateral line organ of fishes. Through mechanotransduction, hair cells detect movement in their environment.

<span class="mw-page-title-main">Otolith</span> Inner-ear structure in vertebrates which detects acceleration

An otolith, also called statoconium or otoconium or statolith, is a calcium carbonate structure in the saccule or utricle of the inner ear, specifically in the vestibular system of vertebrates. The saccule and utricle, in turn, together make the otolith organs. These organs are what allows an organism, including humans, to perceive linear acceleration, both horizontally and vertically (gravity). They have been identified in both extinct and extant vertebrates.

<span class="mw-page-title-main">Stereocilia (inner ear)</span> Mechanosensing organelles of hair cells

In the inner ear, stereocilia are the mechanosensing organelles of hair cells, which respond to fluid motion in numerous types of animals for various functions, including hearing and balance. They are about 10–50 micrometers in length and share some similar features of microvilli. The hair cells turn the fluid pressure and other mechanical stimuli into electric stimuli via the many microvilli that make up stereocilia rods. Stereocilia exist in the auditory and vestibular systems.

<span class="mw-page-title-main">Vestibular nerve</span> Branch of the vestibulocochlear nerve

The vestibular nerve is one of the two branches of the vestibulocochlear nerve. In humans the vestibular nerve transmits sensory information transmitted by vestibular hair cells located in the two otolith organs and the three semicircular canals via the vestibular ganglion of Scarpa. Information from the otolith organs reflects gravity and linear accelerations of the head. Information from the semicircular canals reflects rotational movement of the head. Both are necessary for the sensation of body position and gaze stability in relation to a moving environment.

<span class="mw-page-title-main">Sensory illusions in aviation</span> Misjudgment of true orientation by pilots

Human senses are not naturally geared for the inflight environment. Pilots may experience disorientation and loss of perspective, creating illusions that range from false horizons to sensory conflict with instrument readings or the misjudging of altitude over water.

A kinocilium is a special type of cilium on the apex of hair cells located in the sensory epithelium of the vertebrate inner ear.

The saccule is the smaller sized vestibular sac ; it is globular in form, and lies in the recessus sphæricus near the opening of the scala vestibuli of the cochlea. Its anterior part exhibits an oval thickening, the macula of saccule, to which are distributed the saccular filaments of the acoustic nerve.

The vestibular evoked myogenic potential is a neurophysiological assessment technique used to determine the function of the otolithic organs of the inner ear. It complements the information provided by caloric testing and other forms of inner ear testing. There are two different types of VEMPs. One is the oVEMP and another is the cVEMP. The oVEMP measures integrity of the utricule and superior vestibular nerve and the cVemp measures the saccule and the inferior vestibular nerve.

The righting reflex, also known as the labyrinthine righting reflex, is a reflex that corrects the orientation of the body when it is taken out of its normal upright position. It is initiated by the vestibular system, which detects that the body is not erect and causes the head to move back into position as the rest of the body follows. The perception of head movement involves the body sensing linear acceleration or the force of gravity through the otoliths, and angular acceleration through the semicircular canals. The reflex uses a combination of visual system inputs, vestibular inputs, and somatosensory inputs to make postural adjustments when the body becomes displaced from its normal vertical position. These inputs are used to create what is called an efference copy. This means that the brain makes comparisons in the cerebellum between expected posture and perceived posture, and corrects for the difference. The reflex takes 6 or 7 weeks to perfect, but can be affected by various types of balance disorders.

<span class="mw-page-title-main">Otopetrin family</span>

The otopetrin family is a group of proteins that were first identified based on their essential role in the vestibular system, and were later shown to form proton-selective ion channels expressed in many different tissues, including taste receptor cells. They are named after the Greek word "o̱tós," which means ear and "pétrā," which means rock, in reference to their role in the formation of otoconia/otoliths in the inner ear.

Dark cells are specialized nonsensory epithelial cells found on either side of the vestibular organs and lining the endolymphatic space. These dark-cell areas in the vestibular organ are structures involved in the production of endolymph, an inner ear fluid, secreting potassium towards the endolymphatic fluid. Dark cells take part in fluid homeostasis to preserve the unique high-potassium and low-sodium content of the endolymph and also maintain the calcium homeostasis of the inner ear.

<span class="mw-page-title-main">Otoconin</span> Protein family

Otoconin is a structural glycoprotein found in the otoconial membrane of vertebrates. It is the major protein component of the otoconia.

References

  1. 1 2 3 4 5 6 7 8 9 Purves, Dale (2012). Neuroscience. Sinauer Associates, Inc. pp. 307–309. ISBN   978-0-87893-695-3.
  2. ↑ Krstic, Radivoj (1997). Human Microscopic Anatomy: An Atlas for Students of Medicine and Biology. Berlin: Springer-Verlag. ISBN   978-3-540-53666-6.
  3. 1 2 Lundberg, Y.W.; Zhao, X.; Yamoah, E.N. (2006). "Assembly of the otoconia complex to the macular sensory epithelium of the vestibule". Brain Research. 1091 (1): 47–57. doi:10.1016/j.brainres.2006.02.083. PMID   16600187. S2CID   7363238.
  4. ↑ Parmentier, E.; Cloots, R.; Warin, R.; Henrist, C. (2007). "Otolith crystals (in Carapidae): Growth and habit". Journal of Structural Biology. 159 (3): 462–473. doi:10.1016/j.jsb.2007.05.006. PMID   17616468.
  5. 1 2 Kachar, B.; Parakkal, M.; Fex, J. (1990). "Structural basis for mechanical transduction in the frog vestibular sensory apparatus: I. The otolithic membrane". Hearing Research. 45 (3): 179–190. doi:10.1016/0378-5955(90)90119-a. PMID   2358412. S2CID   4701712.
  6. 1 2 Strimbu, C.E.; Fredrickson-Hemsing, L.; Bozovic, D. (2011). Active Motion of Hair Bundles Coupled to the Otolithic Membrane in the Frog Sacculus. What Fire is in Mine Ears: Progress in Auditory Biomechanics: Proceedings of the 11th International Mechanics of Hearing Workshop. Vol. 1403. p. 133. Bibcode:2011AIPC.1403..133S. doi: 10.1063/1.3658073 .
  7. ↑ Strimbu, C.E.; Ramunno-Johnson, D.; Fredrickson, L.; Arisaka, K.; Bozovic, D. (2009). "Correlated movement of hair bundles coupled to the otolithic membrane in the bullfrog sacculus". Hearing Research. 256 (1–2): 58–63. doi:10.1016/j.heares.2009.06.015. PMID   19573584. S2CID   205100849.
  8. ↑ Gresty, M.A.; Bronstein, A.M.; Brandt, T.; Dieterich, M. (1992). "Neurology of Otolith Function - Peripheral and Central Disorders". Brain. 115 (3): 647–673. doi:10.1093/brain/115.3.647. PMID   1628197.
  9. ↑ "BPPV is the most common vestibular disorder". Vestibular Disorders Association. Retrieved 19 November 2013.
  10. ↑ Ruckenstein, MJ; Shea, JJ Jr (1999). Harris, JP (ed.). Meniere's Disease. Kugler Publications. p. 266. ISBN   978-90-6299-162-4.
  11. ↑ Hayback, PJ. "Mèniére's Disease". vestibular.org. Vestibular Disorders Association. Retrieved 22 September 2015.
  12. 1 2 Harcourt J, Barraclough K, Bronstein AM (2014). "Meniere's disease". BMJ (Clinical Research Ed.). 349: g6544. doi:10.1136/bmj.g6544. PMID   25391837. S2CID   5099437.
  13. ↑ Curthoys, I.S.; M.J. Dai; G.M. Halmagyi (1990). "Human otolithic function before and after unilateral vestibular neurectomy". Journal of Vestibular Research: Equilibrium & Orientation. 1 (2): 199–209.
  14. 1 2 Lychakov, D.V. (2004). "Evolution of otolithic membrane. Structure of otolithic membrane in amphibians and reptilians". Journal of Evolutionary Biochemistry and Physiology. 40 (3): 331–342. doi:10.1023/b:joey.0000042638.35785.f3. S2CID   23316994.
  15. 1 2 Twizell, E.H.; Curran, D.A.S. (1977). "A finite model of the otolith membrane". Computers in Biology and Medicine. 7 (2): 131–141. doi:10.1016/0010-4825(77)90018-x. PMID   852276.
  16. ↑ Twizell, E.H. (1980). "A variable gravity model of the otolith membrane". Applied Mathematical Modelling. 4 (2): 82–86. doi:10.1016/0307-904x(80)90110-9.
  17. ↑ Castillo, J.; McDermott, G.; McEachern, M.; Richardson, J. (1992). "A comparative analysis of numerical techniques applied to a model of the otolithic membrane". Computers & Mathematics with Applications. 24 (7): 133–141. doi: 10.1016/0898-1221(92)90162-b .
  18. ↑ Castillo, J.; McEachern, M.; Richardson, J.; Steinberg, S. (1994). "Modeling the otolithic membrane using boundary-fitted coordinates". Applied Mathematical Modelling. 18 (7): 391–399. doi: 10.1016/0307-904x(94)90225-9 .
  19. ↑ Hudetz, W.J. (1973). "A computer simulation of the otolith membrane". Computers in Biology and Medicine. 3 (4): 355–369. doi:10.1016/0010-4825(73)90002-4. PMID   4777732.
  20. ↑ Kondrachuk, A.V. (2002). "Models of otolithic membrane-hair cell bundle interaction". Hearing Research. 166 (1–2): 96–112. doi:10.1016/s0378-5955(02)00302-7. PMID   12062762. S2CID   29651716.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.