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Chapter Three Vestibular System

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Chapter Three Vestibular System Chapter Three Vestibular System 3.1 Introduction The vestibular, visual, and proprioceptive systems work together to maintain postural equilibrium and visual stability while stationary and when moving. The peripheral vestibular apparatus, a component of the inner ear, has the ability to detect a wide range of angular and linear accelerations of the head, as well as changes in static head position with respect to gravity. The information obtained from the peripheral vestibular apparatus is utilized in central pathways to help generate appropriate postural and eye movement responses to changes in head position. The vestibulo-ocular pathways produce a number of reflexive eye movement responses to help maintain clear vision during head movement (see figure 3.1). These responses include “compensatory” responses to angular head accelerations (generated by the angular vestibulo-ocular reflex or aVOR) and linear head accelerations (generated by the linear vestibulo-ocular reflex or lVOR) (Raphan and Cohen 2002). The vestibulo- ocular pathways also produce “orienting” responses, serving to align the z-axis of the eye with the gravito-inertial acceleration (GIA) vector (Raphan and Cohen 2002). Vestibular-evoked eye movements have short latencies following the onset of head movement, reported to be as low as 5ms in some studies of the aVOR (Tabak et al. 1997). Compensatory smooth eye movements resulting from stimulation of the visual system or the neck proprioceptors are not seen until ≥80ms after the onset of head movement (Bronstein and Hood 1986; Carl and Gellman 1987), making the vestibular system critical for the generation of an early eye movement response to head movement stimuli. The aVOR has an additional advantage, in that it functions well in response to short duration, high frequency head movements, ensuring clear vision during commonly performed activities such as walking and running. The physician J.C. highlighted the importance of these functions by describing how he continuously experienced severe 23 oscillopsia while walking, following the complete loss of vestibular function after treatment with an aminoglycoside antibiotic (J.C. 1952). The anatomy and physiology of the peripheral and central components of the vestibular system are considered in this chapter. Emphasis is placed on the structure and function of the peripheral vestibular apparatus and on the central structures and pathways influencing the aVOR, as relevant to the current study. Figure 3.1 The vestibulo-ocular pathways produce reflexive eye movements that either compensate for head movement or change the orientation of the eye so that its z-axis aligns with the gravito-inertial acceleration (GIA) vector. A. The aVOR produces a rotational eye movement that compensates for rotation of the head. B. The lVOR produces a rotational eye movement to compensate for head translation. C. With the head upright, the head and eye z-axes (denoted by arrows on top of the head and eyes, respectively) align with the GIA, which in turn aligns with the vector representing acceleration due to gravity. D. When the head is tilted, the eyes roll so that their z-axes align with the GIA. E. During horizontal linear acceleration (LINEAR ACC), which tilts the GIA relative to the head vertical, the eyes will again roll to align their z-axes with the GIA (from Raphan and Cohen 2002). 24 3.2 Anatomy of the Peripheral Vestibular System The inner ear lies deep within the petrous temporal bone, in a chamber of communicating ducts and cavities known as the bony labyrinth. The inner ear, or membranous labyrinth, a fluid-filled membranous structure with a shape similar to that of the bony labyrinth, is suspended within the bony labyrinth by a supportive network of connective tissue. The space between the bony labyrinth and the membranous labyrinth is filled with perilymph, a fluid with a high concentration of sodium ions and a low concentration of potassium ions (Smith et al. 1954), making it similar in composition to extracellular fluid. The membranous labyrinth, on the other hand, is filled with endolymph, a fluid with a high concentration of potassium ions and a low concentration of sodium ions, making it similar to intracellular fluid in its ionic composition (Smith et al. 1954). The ionic composition of endolymph is vital to the normal functioning of the sensory cells of the inner ear (Corey and Hudspeth 1979), as discussed below in section 3.3. The membranous labyrinth may be functionally and anatomically divided into two main portions: the peripheral auditory apparatus, or cochlea, and the peripheral vestibular apparatus. The peripheral vestibular apparatus incorporates five structures: the three semicircular canals (SCCs), and two otolith organs, the utricle and saccule (figure 3.2). The three SCCs (anterior, posterior, and lateral) are named for their positions in the head. The anterior SCC is also known as the superior SCC, while the lateral SCC is also known as the horizontal SCC. Neural signals from the sensory tissue of the SCCs and otolith organs pass to the brainstem in the primary (first-order) vestibular afferents, which comprise the vestibular nerve, one of the two nerves making up the eighth cranial nerve (CN VIII). The vestibular nerve may be divided into superior and inferior divisions. The primary vestibular afferents from the anterior SCC, lateral SCC, utricle, and part of the saccule pass to the brainstem in the superior division of the vestibular nerve, while those from the posterior SCC and remainder of the saccule pass to the brainstem in the inferior division. The nuclei of the afferents comprising the superior and inferior divisions of the vestibular nerve are found in the superior and inferior vestibular ganglia of Scarpa, respectively. 25 Figure 3.2 A line drawing of the left inner ear, viewed from the lateral aspect. The semicircular canals, otolith organs (utricle and saccule), and cochlea are illustrated, as are the nerves and other structures closely associated with the inner ear. A narrow channel, the ductus reuniens (unlabelled), joins the cochlea and the peripheral vestibular apparatus (from Kandel et al. 1991). 3.3 Sensory Epithelium and Vestibular Afferents The sensory epithelium of the peripheral vestibular apparatus consists of highly specialized hair cells (Wersäll 1956). Each hair cell has a hexagonal array of 60-100 stereocilia and one kinocilium protruding from its apical surface. The stereocilia are asymmetrically arranged, gradually increasing in height in a staircase fashion, with the tallest stereocilia being located near the kinocilium and the shortest being located at the opposite end of the cell surface. The kinocilium is the longest apical process extending from the hair cell. The arrangement of the stereocilia with respect to the kinocilium results in each hair cell having a morphological axis of polarity (Flock 1964). When the stereocilia of the hair cell are in their resting position, a certain number of mechanically-gated transduction channels on the stereocilia are open, allowing potassium ions from the endolymph to move into the cell and depolarize it. Consequently, the cell has a resting discharge of transmitter. When the stereocilia are deflected towards the kinocilium, more transduction 26 channels on the stereocilia open by a mechanical process that is mediated by tip links connecting the stereocilia (Corey and Hudspeth 1983), leading to further depolarization (Flock 1965) and increased release of transmitter (Corey and Hudspeth 1979; figure 3.3). Deflection of the stereocilia away from the kinocilium results in the opposite response, with hyperpolarization of the hair cell (Flock et al. 1973) and decreased transmitter release (Corey and Hudspeth 1979). The hair cell receptors show greater sensitivity and linearity of response for small deflections of the stereocilia away from their resting position (see figure 3.3), with larger deflections resulting in saturation and non-linearity. The saturation effect is particularly evident with deflections of the stereocilia away from the kinocilium (see figure 3.3). Figure 3.3 Intracellular voltage changes (in mV) resulting from displacement/flexion of the cilia of a hair cell. Flexion towards the kinocilium (positive) results in depolarization, while flexion away (negative) results in hyperpolarization (from Hudspeth and Corey 1977). The resting discharge of transmitter from the hair cells results in the primary vestibular afferents also having a resting discharge. The resting discharge rate of primary vestibular afferents is about 91Hz in squirrel monkeys, and is thought to be approximately the same in humans (Goldberg and Fernández 1971a, 1971b). Depolarization of a hair cell results in an increase in the afferent firing rate due to increased transmitter release 27 from the hair cell, while hyperpolarization of the cell will produce a decrease in the afferent firing rate due to decreased transmitter release (see figure 3.4). Thus, neural signals coding deflections of the stereocilia both toward and away from the kinocilium can be communicated to the central nervous system via the primary vestibular afferents (Löwenstein and Sand 1940; Money and Scott 1962). Figure 3.4 The hair cell receptor potential and the firing rate of the primary vestibular afferent both depend on the orientation of the cilia on the hair cell. Deflections of the stereocilia towards the kinocilium result in depolarization and increased firing rate, while deflections in the opposite direction result in hyperpolarization and decreased firing rate (from Kandel et al. 1991). 3.4 Semicircular Canals The SCCs are tubular structures that are roughly semicircular in shape (Curthoys et al. 1977a). At one end of each canal is an enlargement known as the ampulla (figure 3.5a). Within each ampulla, a collection of hair cells makes up the saddle-shaped ampullary crest (also known as the crista ampullaris). The cilia of these hair cells project towards the centre of the canal lumen into a gelatinous membrane known as the cupula. The cupula extends across the lumen of the SCC and is adherent to the SCC wall, forming a watertight seal (Dohlman 1971; Lim 1973).
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