Three sources of sensory information are used by the nervous system in the maintenance of equilibrium. They are the eyes, proprioceptive endings throughout the body, and the vestibular apparatus of the internal ear. The role of the vestibular system, especially in relation to visual information, is illustrated by a person who has congenital atresia of the vestibular apparatus, usually accompanied by cochlear atresia and deaf-mutism. Such a person can orient himself satisfactorily by visual guidance but becomes disoriented in the dark or if submerged while swimming. In addition, vestibular impulses caused by motion of the head contribute to appropriate movements of the eyes to maintain fixation on an object in the visual field. These functions require a neural pathway from the vestibular labyrinth to motor neurons through pathways in the spinal cord, brain stem, and cerebellum, and there is also a projection to the cerebral cortex.
Whereas the static labyrinth, represented by the utricle and saccule, detects the position of the head with respect to gravity, the kinetic labyrinth represented by the semicircular ducts detects movement of the head. Both parts of the membranous labyrinth serve to maintain equilibrium, and the kinetic labyrinth has a special role in coordination of eye movement with rotation of the head.
The utricle and saccule are endolymph-containing dilations of the membranous labyrinth, enclosed by the vestibule of the bony labyrinth (see Figs. 21-1 and 21-2). The utricle and saccule, which are derived from the otic vesicle of the embryo, are suspended from the wall of the vestibule by connective tissue trabeculae, and they are surrounded by space containing perilymph. Each dilatation includes a specialized area of sensory epithelium, the macula, about 2 by 3 mm in size. The macula utriculi is located in the floor of the utricle and parallel with the base of the skull, and the macula sacculi is vertically disposed on the anteromedial wall of the saccule. The two maculae are histologically identical (Fig. 22-1).
The columnar supporting cells of the maculae are continuous with the cuboidal epithelium
that lines the utricle and saccule elsewhere. The sensory hair cells, of which two types have been identified in electron micrographs, are somewhat similar to hair cells in the organ of Corti (see Chapter 21). Type 1 hair cells are flask shaped, and type 2 hair cells are cylindrical. From 30 to 50 hairs project from each cell, together with a long cilium (thekinocilium) that arises from a centriole (see Fig. 22-2A). (Kinocilia are characteristic of vestibular hair cells. They do not occur in the organ of Corti.) The hairs, also calledstereocilia, are large microvilli, 0.25 µm wide and up to 100 µm long. The lengths of the hairs increase toward the side of the bundle where the kinocilium emerges. The tips of the hairs and kinocilium are embedded in the gelatinous otolithic membrane, in which there are irregularly shaped concretions composed of protein and calcium carbonate. These are known as otoliths.
FIGURE 22-1 Structure of the macula utriculi.
The otoliths give the otolithic membrane a higher specific gravity than the endolymph, thereby causing bending of the hairs in one direction or another, except when the macula is in a strictly horizontal plane. In each hair cell, the kinocilium is situated at one side of the tuft of hairs, and the position of the kinocilium at the periphery of the hairs differs from one region of the macula to another (see Fig. 22-2B). The hair cells are excited when the hairs are bent in the direction of the kinocilium, and they are inhibited when the deflection is in the opposite direction (see Fig. 22-2A). The pattern of action potentials conducted by the axons of the vestibular nerve differs, therefore, according to the orientation of the macula to the direction of gravitational pull. The appropriate changes in muscle tone follow, as required to maintain equilibrium. The molecular mechanism of transduction of the mechanical stimulus by the stereocilia is the same as for the cochlear hair cells, described in Chapter 21.
Although the macula is predominantly a static organ, the higher specific gravity of the otolithic membrane with respect to the endolymph allows the macula to respond to linear acceleration and deceleration. Motion sickness is initiated by prolonged, fluctuating stimulation of the maculae.
The bipolar cell bodies of the primary sensory neurons are located in the vestibular ganglion (Scarpa's ganglion) at the lateral end of the internal acoustic meatus. The peripheral neurites enter the maculae and end on the hair cells (see Fig. 22-2A). In addition, efferent cholinergic axons in the vestibular nerve end as presynaptic terminals on the type 2 hair cells and on the sensory nerve endings that are postsynaptic to the type 1 cells. These axons, which are inhibitory,
originate from an unnamed group of neurons medial to the vestibular nuclei.
FIGURE 22-2 Vestibular hair cells, with their afferent and efferent innervation. (A) The two types of hair cells in a macula. Excitation occurs when the bundle of hairs or microvilli (a) bends in the direction of the kinocilium (b). Inhibition of the hair cell occurs when the hair bundle bends in the opposite direction. (B) Surfaces of the maculae of the utricle (above) and saccule (below), showing the positioning of the kinocilia (heads of arrows) relative to the tufts of hairs. Each arrow indicates the direction of gravitational pull for excitation of hair cells in that location. In the macula utriculi, the kinocilia of the hair cells face a central stripe, the striola. In the macula sacculi, the kinocilia face away from the striola. Hair cells are absent from the striola itself.
The three semicircular ducts are attached to the utricle and are enclosed in the semicircular canals of the bony labyrinth (see Figs. 21-1 and 21-2). The anterior and posterior semicircular ducts are in vertical planes; the former is transverse to and the latter is parallel with the long axis of the petrous part of the temporal bone. The lateral semicircular duct slopes downward and backward at an angle of 30° to the horizontal plane. The sensory areas of the semicircular ducts respond only to movement, and the response is maximal when movement is in the plane of the duct.
Each semicircular duct has an expansion or ampulla at one end, in which the crista ampullaris or sensory epithelium is supported by a transverse septum of connective tissue projecting into the lumen (Fig. 22-3). Among the columnar supporting cells are the sensory hair cells, whose structural details and mode of innervation conform to those already described for hair cells of the static labyrinth. The hairs and kinocilium of each hair cell are embedded
in gelatinous material that forms the cupula, in which otoliths are lacking. The cupula has the same specific gravity as the endolymph and is therefore not pulled on by gravity.
FIGURE 22-3 Structure of a crista ampullaris.
The cristae are sensors of rotary movement of the head, sometimes called angular movement, especially when accompanied by acceleration or deceleration. At the beginning of a movement in or near the plane of a semicircular duct, the endolymph lags because of inertia, and the cupula swings like a door in a direction opposite to that of the movement of the head. The momentum of the endolymph causes the cupula to swing momentarily in the opposite direction when the movement ceases. The hairs and kinocilia of the sensory cells bend accordingly. Depending on the direction of movement, this may reduce the membrane potentials of the hair cells, causing release of their chemical transmitter and the initiation of action potentials in the sensory nerve endings.
The kinocilium is consistently on the side of the tuft of hairs nearest the opening of the ampulla into the utricle. The excitation of hair cells occurs when the flow of endolymph is from the ampulla into the adjacent utricle; there is inhibition of the hair cells when the flow is in the opposite direction. The hair cells of the cristae, similar to those of the maculae, are supplied by primary sensory neurons whose bipolar cell bodies are situated in the vestibular ganglion.
On entering the brain stem at the junction of the medulla and pons, most of the vestibular nerve fibers bifurcate in the usual manner of afferent fibers and end in the vestibular nuclear complex. The remaining fibers go to the cerebellum through the inferior cerebellar peduncle.
The vestibular nuclei are situated in the rostral medulla and caudal pons, partly beneath the lateral area of the floor of the fourth ventricle (see Figs. 6-3 and 22-4). Four vestibular nuclei are recognized on the basis of cytoarchitecture and the details of afferent and efferent connections. The lateral vestibular
nucleus, also known as Deiters' nucleus, consists mainly of large multipolar neurons with long axons. The superior, medial, and inferior vestibular nuclei consist of small- and medium-sized cells. The positions of the vestibular nuclei are described and illustrated in Chapter 7. The primary afferent vestibular neurons are excitatory to the neurons in the vestibular nuclei.
FIGURE 22-4 Vestibular pathways to the spinal cord and to the nuclei of the oculomotor nerves.
CONNECTIONS WITH THE CEREBELLUM
The vestibulocerebellum, consisting of the flocculonodular lobe, adjacent region of the inferior vermis and fastigial nuclei, receives its afferents from the superior, medial, and inferior vestibular nuclei in addition to a few axons directly from the vestibular nerve. In the reverse direction, efferent fibers of the vestibulocerebellum terminate throughout the vestibular nuclear complex (see Chapter 10 and Fig. 10-13). Some cerebellovestibular fibers are the axons of Purkinje cells (inhibitory); others are from the fastigial nucleus (excitatory). These afferent and efferent fibers of the vestibulocerebellum occupy the medial part of the inferior cerebellar peduncle. The role of the cerebellum in maintaining equilibrium is exerted mainly through pathways from the vestibular nuclei to the spinal cord.
CONNECTIONS WITH THE SPINAL CORD
The connection between the vestibular nuclei and the spinal cord is through descending fibers in the vestibulospinal tract and the medial longitudinal fasciculus. (Sometimes these tracts are called the lateral and medial vestibulospinal tracts, respectively.)
The vestibulospinal tract, which is uncrossed, originates exclusively in the lateral vestibular nucleus. The fibers descend in the medulla dorsal to the inferior olivary nucleus and continue into the ventral funiculus of the spinal cord. Vestibulospinal fibers terminate in the medial part of the ventral horn at all levels but most abundantly in the cervical and lumbosacral enlargements. A few vestibulospinal fibers synapse with medially located motor neurons that supply the axial musculature.
The vestibulospinal tract is of prime importance in regulating the tone of muscles involved in posture so that balance is maintained. Stimulation of the lateral vestibular nucleus causes excitation of motor neurons that supply extensor muscles of the ipsilateral lower limb. Flexors are inhibited, and the foot is pressed more firmly on the ground.
Axons from each medial vestibular nucleus project toward the midline and turn caudally in the descending component of the medial longitudinal fasciculus of both sides. This bundle of fibers is adjacent to the midline close to the floor of the fourth ventricle and ventral to the central canal of the medulla more caudally. The fibers continue into the medial part of the ventral funiculus of the spinal cord. They influence cervical motor neurons so that the head moves in a way that assists in maintaining equilibrium and fixation of gaze.
CONNECTIONS WITHIN THE BRAIN STEM
The ascending component of the medial longitudinal fasciculus is adjacent to the midline in the pons and midbrain, ventral to the floor of the fourth ventricle and the periaqueductal gray matter. The constituent axons connect the vestibular nuclei with the nuclei of the abducens, trochlear, and oculomotor nerves and with the accessory oculomotor nuclei of the midbrain. Some of the ascending fibers are uncrossed; others cross the midline at the level of the vestibular nuclei. The medial longitudinal fasciculus provides for conjugate movement of the eyes, coordinated with movement of the head, to maintain visual fixation. Signals received by the vestibular nuclei from the cristae ampullares are responsible for the ocular adjustments to movement of the head. A small rotation of the head is accompanied by movement of the eyes through the same angle but in the opposite direction; this is called the vestibulo-ocular reflex.
The medial longitudinal fasciculus also contains the axons of internuclear neurons, which interconnect the nuclei of cranial nerves III, IV, and VI and fibers that originate in the paramedian pontine reticular formation. These connections and the effects of lesions of the medial longitudinal fasciculus are described in Chapter 8.
Excessive or prolonged stimulation of the vestibular system may cause nausea and vomiting. The connections responsible for these effects may be projections of vestibular nuclei to the solitary nucleus and the dorsal nucleus of the vagus nerve. Excessive input from the labyrinth to the vestibular nuclei is probably reduced to some extent by a feedback through the efferent inhibitory fibers in the vestibular nerve.
The vestibular system acts mainly on the brain stem, cerebellum, and spinal cord, but a significant pathway to the cerebral cortex is also present. This provides for conscious awareness of position and movement of the head.
The ascending pathway from the vestibular nuclei is predominantly crossed and runs close to the medial lemniscus. The thalamic relay for the cortical projection is in the medial division of the ventral posterior nucleus (VPm), which also receives somatosensory fibers for the head. The vestibular cortical field is presumed to contribute information for use in higher motor regulation and for conscious spatial orientation. There is no known cortical area activated exclusively by vestibular stimulation.
Evoked potentials have been recorded in monkeys during electrical stimulation of the vestibular nerve. Two areas are thus identified
as receiving vestibular information: one is located in the posterior part of the insula, extending onto the parietal operculum, where it is coextensive with part of the second somatosensory area (see Chapter 15). The other area is located in the cortex that forms the anterior end of the intraparietal sulcus. Vertigo has been reported by human subjects after electrical stimulation at various sites in the parietal and temporal lobes. In positron emission tomography (PET) and functional nuclear magnetic resonance imaging (fMRI) studies, caloric stimulation of the human kinetic labyrinth has caused increased activation in various cortical areas. When the control subjects were patients whose vestibulocochlear nerves had been surgically removed (eliminating auditory as well as tactile and thermal sensations), significant cortical activation by caloric stimulation was detected only in the posterior insula and adjacent parietal operculum. The latter region is coextensive with the second somatosensory area (see Chapter 15).
Caloric Testing and Doll's Eyes
The caloric test is used when there is a reason to suspect a tumor of the vestibulocochlear nerve or a lesion that interrupts the vestibular pathway in the brain stem. This procedure separately tests the pathway from each internal ear. The head is positioned so that the lateral semicircular duct is in a vertical plane, and the external acoustic meatus is irrigated with warm or cold water to induce convection currents in the endolymph. The ampulla of the duct is near the bone that is undergoing a change of temperature, and the endolymph “rises” or “falls,” depending on whether it is warmed or cooled. In a conscious subject, the procedure causes nystagmus if the vestibular pathway for the side tested is intact. This nystagmus is a series of slow conjugate eye movements (driven by the vestibular nuclei), each followed by a rapid movement (driven by the cerebral cortex) to restore the original direction of gaze.
In a comatose patient with intact pathways in the brain stem, caloric stimulation with warm water makes the eyes deviate to the opposite side; cold water causes a conjugate deviation toward the cooled side. The deviation is the isolated slow component of a nystagmus. The fast component, which is a voluntary compensation, is prevented by the absence of consciousness.
The doll's eyes phenomenon, which is a vestibulo-ocular reflex uncomplicated by voluntary eye movements, is another clinical sign useful in the diagnosis of coma. If the vestibular apparatus, nuclei, and nerve; the medial longitudinal fasciculus; and the abducens and oculomotor nuclei are all intact, movement of the head will be accompanied by conjugate movement of the eyes in the opposite direction. Loss of caloric responses and of the doll's eyes reflex are two signs that can contribute to a diagnosis of brain stem death.
Tracing experiments in monkeys reveal that neurons in various cortical regions (parts of the parietal lobe, insula, and premotor cortex of the frontal lobe) have axons that end in the vestibular nuclei. These descending projections may suppress vestibular reflexes (i.e., movements of the eyes and neck) during the performance of voluntary movements.
Practical Aspects of the Vestibular System
The vestibular projections to nuclei that supply extraocular muscles and motor neurons in the spinal cord can be demonstrated by strong stimulation of the labyrinth. This may be done by rotating a subject around a vertical axis about 10 times in 20 seconds and then abruptly stopping the rotation. The responses are most pronounced if the head is bent forward 30 degrees to bring the lateral semicircular ducts in a horizontal plane. On stopping rotation, momentum acquired by the endolymph causes it to flow past (and deflect) the cupulae of the lateral semicircular ducts more suddenly and rapidly than for most movements.
Labyrinthine irritation causes vertigo (an illusion of revolving motion), sometimes accompanied by nausea and vomiting, pallor, a cold sweat, and nystagmus. Paroxysms of labyrinthine irritation occur in Ménière's disease, a condition of obscure cause in which the endolymphatic pressure is abnormally high. Affected patients also have tinnitus (buzzing or ringing in the ears) and eventual deafness caused by degeneration of the receptor cells.
Benign paroxysmal positional vertigo is a common condition in which brief episodes of vertigo follow certain movements of the head. The condition is attributed to a particle of debris, such as a detached otolith, that has entered the endolymph of a semicircular duct. A sequence of head movements contrived to allow the particle to fall from the posterior semicircular duct into the utricle (the Dix-Hallpike maneuver) usually provides prolonged relief.
Sudden unilateral loss of vestibular function causes vertigo with considerable postural instability as well as a tendency to fall toward the abnormal side. This results from undue downward pressure on one foot, perhaps caused by excessive activity in the vestibulospinal tract of the normal side. The brain eventually accommodates to input from only one vestibular apparatus.
The responses of the hair cells in the cristae ampullares produce the following signs immediately after rotation ceases. Impulses conveyed by the ascending axons of the medial longitudinal fasciculus cause nystagmus, which is an oscillatory movement of the eyes consisting of fast and slow components.
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