Chapter 22
The Vestibular System
Peripheral Vestibular Labyrinth
Morphologic Polarization of Hair Cells
Semicircular Canals and Otolith Organs
Function of Semicircular Canals
Rotational Vestibuloocular Reflex
Vestibulothalamocortical Network
Humans have the ability to control posture and movements of the body and eyes relative to the external environment. The vestibular system mediates these motor activities through a network of receptors and neural elements. This system integrates peripheral sensory information from vestibular, somatosensory, visceromotor, and visual receptors as well as motor information from the cerebellum and cerebral cortex. Central processing of these inputs occurs rapidly, with the output of the vestibular system providing an appropriate signal to coordinate relevant movement reflexes. Although the vestibular system is considered to be a special sense, most vestibular activity is conducted at a subconscious level. However, in situations producing unusual or novel vestibular stimulation, such as rough air in a plane flight or wave motion on ships, vestibular perception becomes acute, with dizziness, vertigo, or nausea often resulting.
OVERVIEW
The vestibular system is an essential component in the production of motor responses that are crucial for daily function and survival. Throughout evolution, the highly conserved nature of the vestibular system is revealed through striking similarities in the anatomic organization of receptors and neuronal connections in fish, reptiles, birds, and mammals.
For the present discussion, the vestibular system can be divided into five components:
1. The peripheral receptor apparatus resides in the inner ear and is responsible for transducing head motion and position into neural information.
4. The vestibulospinal network coordinates head movements, axial musculature, and postural reflexes.
PERIPHERAL VESTIBULAR LABYRINTH
The vestibular labyrinth contains specialized sensory receptors and is located lateral and posterior to the cochlea in the inner ear (Fig. 22-1). The vestibular labyrinth consists of five separate receptor structures, three semicircular canals and two otolith organs, which are contained in the petrous portion of the temporal bone. The labyrinth is actually composed of two distinct components. The bony labyrinth is a surrounding shell that contains and protects the sensitive underlying vestibular sensory structures (Fig. 22-1). In humans, the bony labyrinth can be visualized only on excision of the mastoid process. Inside the bony labyrinth is a closed, fluid-filled system, the membranous labyrinth, which consists of connecting tubes and prominences (Fig. 22-2). Vestibular receptors are located in specialized regions of the membranous labyrinth.
Figure 22-1. A cross section of the outer, middle, and inner ear.
Between the membranous labyrinth and bony labyrinth is a space containing fluid called perilymph, which is similar to cerebrospinal fluid. Perilymph has a high sodium content (150 mM) and a low potassium content (7 mM), and it bathes the vestibular portion of the eighth cranial nerve.
The membranous labyrinth is filled with a different type of fluid, called endolymph, which covers the specialized sensory receptors of both the vestibular and the auditory systems. Endolymph has a high concentration of potassium (150 mM) and a low concentration of sodium (16 mM). It is important to note the differences in these two fluids because both are involved in the normal functioning of the vestibular system. Disturbances in the distribution or ionic content of endolymph often lead to vestibular disease.
Vestibular Receptor Organs
The five vestibular receptor organs in the inner ear complement each other in function. The semicircular canals (horizontal, anterior, and posterior) transduce rotational head movements (angular accelerations). The otolith organs (utricle and saccule) respond to translational head movements (linear accelerations) or to the orientation of the head relative to gravity. Each semicircular canal and otolith organ is spatially aligned to be most sensitive to movements in specific planes in three-dimensional space.
In humans, the horizontal semicircular canal and the utricle both lie in a plane that is slightly tilted anterodorsally relative to the nasooccipital plane (Fig. 22-3). When a person walks or runs, the head is normally declined (pitched downward) by approximately 30 degrees, so that the line of sight is directed a few meters in front of the feet. This orientation causes the plane of the horizontal canal and utricle to be parallel with the earth and perpendicular to gravity. The anterior and posterior semicircular canals and the saccule are arranged vertically in the head, orthogonal to the horizontal semicircular canal and utricle (Fig. 22-3). The two vertical canals in each ear are positioned orthogonal to each other, whereas the plane of the anterior canal on one side of the head is coplanar with the plane of the contralateral posterior canal (Fig. 22-3).
The receptor cells in each vestibular organ are innervated by primary afferent fibers that join with those from the cochlea to comprise the vestibulocochlear (eighth) cranial nerve. The cell bodies of these bipolar vestibular afferent neurons are in the vestibular ganglion (Scarpa ganglion), which lies in the internal acoustic meatus (Fig. 22-4). The central processes of these bipolar cells enter the brainstem and terminate in the ipsilateral vestibular nuclei and cerebellum.
The blood supply to the labyrinth is primarily via the labyrinthine artery, usually a branch of the anterior inferior cerebellar artery. This vessel enters the temporal bone through the internal auditory meatus. Although it is not as important as the labyrinthine artery, the stylomastoid artery also provides branches to the labyrinth, mainly to the semicircular canals. An interruption of blood supply to the labyrinth will compromise vestibular (and cochlear) function, resulting in labyrinth-associated symptoms, such as vertigo or oscillopsia, and clinical signs, such as nystagmus or unstable gait.
Membranous Labyrinth
The membranous labyrinth is supported inside the bony labyrinth by connective tissue. The three ducts of the semicircular canals connect to the utricle, and each duct ends with a single prominent enlargement, the ampulla (Fig. 22-2). Sensory receptors for the semicircular canals reside in a neuroepithelium at the base of each ampulla. The receptors in the utricle are oriented longitudinally along its base, and in the saccule they are oriented vertically along the medial wall (Fig. 22-2). Endolymph in the labyrinth is drained into the endolymphatic sinus via small ducts. In turn, this sinus communicates through the endolymphatic duct with the endolymphatic sac, which is located adjacent to the dura mater (Fig. 22-2). The saccule is also connected to the cochlea by the ductus reuniens.
Meniere Disease
The balance between the ionic contents of endolymph and perilymph is maintained by specialized secretory cells in the membranous labyrinth and the endolymphatic sac. In cases of advanced Meniere disease, there is disruption of normal endolymph volume, resulting in endolymphatic hydrops (an abnormal distention of the membranous labyrinth). Symptoms of Meniere disease include severe vertigo (a sense of spinning in space), positional nystagmus, and nausea. Affected persons often have unpredictable attacks of auditory and vestibular symptoms, including vomiting, tinnitus (ringing in the ears), and a complete inability to make head movements or even to stand passively. For patients with frequent debilitating attacks, the first course of treatment is often administration of a diuretic (e.g., hydrochlorothiazide) and a salt-restricted diet to reduce the hydrops. If persistent symptoms of Meniere disease continue, second treatment options include either the implantation of a small shunt into the abnormally swollen endolymphatic sac or the delivery of a vestibulotoxic agent such as gentamicin into the perilymph.
Semicircular Canal Dehiscence
On occasion, a condition may develop in which a portion of the temporal bone overlying either the anterior or the posterior semicircular canal thins so much that an opening (dehiscence) is created next to the dura (Fig. 22-5). In affected patients, the canal dehiscence exposes the normally closed bony labyrinth to the extradural space. Symptoms can include vertigo and oscillopsia (a sense that objects are moving to and fro, oscillating, in the visual fields) in response to loud sounds (the Tullio phenomenon) or in response to maneuvers that change middle ear or intracranial pressure. The eye movements evoked by these stimuli (nystagmus) align with the plane of the dehiscent superior canal. Surgical closure of the defect by bone replacement is often performed.
VESTIBULAR SENSORY RECEPTORS
Hair Cell Morphology
The sensory receptor cells in the vestibular system, like those in the auditory system, are called hair cells because of the stereocilia that project from the apical surface of the cell (Fig. 22-6A). Each hair cell contains 60 to 100 hexagonally arranged stereocilia and a single longer kinocilium. The stereocilia are oriented in rows of ascending height, with the tallest lying next to the lone kinocilium. The stereocilia arise from a region of dense actin, the cuticular plate, located at the apical end of the hair cell. The cuticular plate acts as an elastic spring to return the stereocilia to the normal upright position after bending. Each stereocilium is connected to its neighbor by small filaments.
There are two types of hair cells, and they differ in their pattern of innervation by fibers of the eighth cranial nerve (Fig. 22-6A). Type I hair cells are chalice shaped and typically are surrounded by an afferent terminal that forms a nerve calyx. Type II hair cells are cylindric and are innervated by simple synaptic boutons. Excitatory amino acids such as aspartate and glutamate are the neurotransmitters at the receptor cell–afferent fiber synapses. Both types of hair cells, or their afferents, receive synapses from vestibular efferent fibers that control the sensitivity of the receptor. These efferent fibers contain acetylcholine and calcitonin gene–related peptide as neurotransmitters. Efferent cell bodies are located in the brainstem just rostral to the vestibular nuclei and lateral to the abducens nucleus. They are activated by behaviorally arousing stimuli or by trigeminal stimulation.
Within each ampulla, the hair cells and their supporting cells lie embedded in a saddle-shaped neuroepithelial ridge, the crista, which extends across the base of the ampulla (Fig. 22-6B). Type I hair cells are concentrated in central regions of the crista, and type II hair cells are more numerous in peripheral areas. Arising from the crista and completely enveloping the stereocilia of the hair cells is a gelatinous structure, the cupula. The cupula attaches to the roof and walls of the ampulla, forming a fluid-tight partition that has the same specific density as that of endolymph. Rotational head movements produce angular accelerations that cause the endolymph in the membranous ducts to be displaced so that the cupula is pushed to one side or the other like the skin of a drum. These cupular movements displace the stereocilia (and kinocilium) of the hair cells in the same direction.
For the otolith organs, a structure analogous to the crista, the macula, contains the receptor hair cells (Fig. 22-6C). The hair cell stereocilia of otolith organs extend into a gelatinous coating called the otolith membrane, which is covered by calcium carbonate crystals called otoconia (from the Greek, meaning “ear stones”). Otoconia are about three times as dense as the surrounding endolymph, and they are not displaced by normal endolymph movements. Instead, changes in head position relative to gravity or linear accelerations (forward-backward, upward-downward) produce displacements of the otoconia, resulting in bending of the underlying hair cell stereocilia.
Hair Cell Transduction
The response of hair cells to deflection of their stereocilia is highly polarized (Figs. 22-7 and 22-8A). Movements of the stereocilia toward the kinocilium cause the hair cell membranes to depolarize, which results in an increased rate of firing in the vestibular afferent fibers. If the stereocilia are deflected away from the kinocilium, however, the hair cell is hyperpolarized and the afferent firing rate decreases.
Figure 22-7. Physiologic responses of vestibular hair cells and their vestibular afferent fibers. Asp, aspartate; Glu, glutamate.
The mechanisms underlying the depolarization and hyperpolarization of vestibular hair cells depend, respectively, on the potassium-rich character of endolymph and the potassium-poor character of the perilymph that bathes the basal and lateral portions of the hair cells. Deflection of the stereocilia toward the kinocilium causes potassium channels in the apical portions of the stereocilia to open. Potassium flows into the cell from the endolymph, depolarizing the cell membrane (Fig. 22-7
