The function of the vestibular apparatus is to translate gravitational forces and movement into nerve impulses that the brain can process in order to determine the position of the head in space and, therefore, co-ordinate movements of the head with the motor reflexes responsible for stability and the position of the eyes. The functions of the vestibular apparatus are categorised under the name of “special proprioception”. Special proprioception is a sensory function and, therefore, information from peripheral receptors is carried by the afferent fibres of the vestibulo-cochlear nerve to central structures in the brain stem, where it is processed.
From an anatomical point of view the vestibular apparatus is divided into a peripheral and a central part. The peripheral part comprises the structures in the inner ear, the vestibule and semicircular canals, and the vestibular part of the VIIIth pair of cranial nerves. The central part is situated in the brain stem, where the four vestibular nuclei are located, and in the cerebellum, which contains the flocculonodular lobe and the fastigial nucleus.
PERIPHERAL PART
The ear of the dog and cat consists of three anatomically connected parts: the outer ear, the middle ear and the inner ear (labyrinth). These parts have two important functions: hearing, a special exteroceptive sense related to the cochlear part, and balance, a special proprioceptive sense related to the vestibular part. The VIIIth cranial nerve, which collects the sensory efferents from the ear, has two clearly distinct parts and is, therefore, named the vestibulo-cochlear nerve. This nerve is, in fact, formed by two divisions, whose origins, central connections and functions are completely different: the vestibular nerve and the cochlear nerve. From a functional point of view, the outer and middle ear are dedicated to hearing, while the inner ear is the only part that normally participates directly in both hearing and balance. The anatomical structures involved in the function of balance are described here below.
The inner ear
The inner ear, or labyrinth, is located within the petrous portion of the temporal bone and comprises the bony labyrinth and the membranous labyrinth. The bony labyrinth is composed of the vestibule, three semicircular canals, and the cochlea; it contains perilymph, a fluid the composition of which is similar to that of cerebrospinal fluid. The perilymph separates the bony labyrinth from an internal mould of the same form but much more delicate, the membranous labyrinth. This internal mould also contains a fluid, the endolymph, which differs chemically from the perilymph; the main difference is that perilymph resembles an extracellular fluid, with a high content of sodium and a low concentration of potassium, while endolymph is similar to an intracellular fluid with a high concentration of potassium and a low concentration of sodium (Fig. 1; with kind permission from Elsevier). The vestibule is a small oval-shaped cavity located between the middle ear and the internal auditory meatus, which communicates with the semicircular canals and the cochlea. It contains two sensory areas positioned deeply within the membranous labyrinth: rostrally the saccule and, caudally, the utricle. The saccule is nested in the spheroid recess of the vestibular bone and has a spheroid shape; it has two small orifices, one ventral, the origin of the canalis reuniens of Hansen, which connects it to the cochlear duct, and the other, posterior, which gives rise to a small, short duct which, uniting in a V with a similar duct from the utricle, forms the endolymphatic duct. The endolymphatic duct continues medially and terminates with a blind-ended dilation, the endolymphatic sac, situated externally to the dura mater close to the petrous portion of the temporal bone. The utricle is larger than the saccule and is located dorsally to this latter; it has an elongated shape and occupies the recessus ellipticus of the vestibule itself. It receives the openings of the semicircular ducts, and gives rise to a small duct that contributes to the formation of the endolymphatic duct.
The three semicircular ducts are located in the caudal part of the labyrinth. They are named anterior (vertical), posterior (vertical) and lateral (horizontal). Each semicircular duct is oriented at right-angles with respect to the others; rotation of the head around each plane therefore causes movement of the endolymph in one or more of the ducts. Each canal forms an arch which is about two-thirds of a circle and is connected to the vestibule at its two ends, but not separately (i.e., there are less than six connections with the vestibule). There is a dilation, the ampulla, at one extremity of each canal. The ends without the ampulla of the posterior (caudal) and anterior (dorsal) canals unite to form a common trunk or arm, which is attached to the vestibule. The end of the lateral (horizontal) canal without an ampulla and the end of the posterior canal with the ampulla unite for a short tract caudally to the vestibule. (Fig. 2; with kind permission from Elsevier).
Receptor structures
Each part of the membranous labyrinth of the vestibular system contains specialised receptor structures: there are two of these specialised areas, which are called maculae, inside the vestibule, one in the utricle and one in the saccule; other specialised receptor structures are found in each of the ampullae of the three semicircular ducts: these structures are called cristae ampullares or ampullary crests.
The macula of the utricle is a hook-shaped structure oriented vertically when the head is in a normal position, while the macula of the saccule, which is kidney-shaped, is oriented horizontally. Microscopically, the structures of the specialised and non-specialised areas do not differ between the saccule and utricle. The non-specialised areas have a simple squamous epithelium in which light cells and dark cells can be distinguished; these latter appear to control the ionic composition of the endolymph.
The epithelium in the saccule and utricle changes structure in the maculae: from a single layer it becomes double-layered, with a deep layer, whose cells, called supporting cells, lie on the basement membrane, and a superficial layer, formed of special cells, called hair cells, which do not reach the basement membrane. The hair cells function as transducers, having a high sensitivity to mechanical stimuli (i.e., they are mechanoreceptors) and a marked degree of directional sensitivity. Morphologically, there are two types of cell projections: the stereocilia, which are actually microvilli, and the kinocilia or cilia. Each hair cell has about 70 stereocilia, arranged in rows, and only one kinocilium, which is longer than the stereocilia and is located at one end of the specialised surface of the cell. The stereocilia are much shorter at the extremity of the surface opposite the kinocilium and their length gradually increases as they near the kinocilium itself.
The extremity of each stereocilium is connected to a neighbouring stereocilium in the next, higher row by a thin filament, called a tip link. When the stereocilia are bent towards to the kinocilium, they tend to depolarise; that is, they become excited with a consequent increase in the barrage of impulses in the fibre associated with that particular cell. When the stereocilia are bent away from the kinocilium, they are hyperpolarised (with resulting inhibition of the associated nerve fibre). The cilia and microvilli of hair cells are embedded in a glycoprotein-based gelatinous substance that contains microscopic particles of calcium carbonate, statocones or otoliths, named the otolithic membrane.
The movement of the otoliths away from the cellular projections is the event that gives rise to an impulse in the dendritic zone of the vestibular neurones, which synapse with the base of the hair cells. The saccular macula is oriented in a vertical direction (sagittal plane), while the utricular macula is oriented in a horizontal direction (dorsal plane); the forces of gravity, therefore, continuously influence the position of the otoliths with respect to the hair cells. These are responsible for the sensation of the position and linear acceleration and deceleration of the head.
The microscopic structure of the membranous semicircular ducts is very similar to that of the saccule and utricle (simple squamous cell epithelium). In each ampulla there is an area of specialised epithelium, the crista ampullaris, equivalent to the auditory macula. The crista ampullaris does, however, have its own particular characteristics. It is the most prominent part of the sensory epithelium that rests on a bed of thickened connective tissue which protrudes into the lumen of the ampulla. This portion of neuroepithelium is also formed of two types of cells, hair cells and supporting cells, as described above.
The surface of the crista ampullaris is covered by a gelatinous substance composed of protein-polysaccharide material, called the cupula, which extends across the lumen of the ampulla. In reality, the cilia cross a small space (filled with endolymph) that separates the cupula from the epithelium and each cilia is in a duct (filled with endolymph) that extends to the apex of the cupula itself. The cupula can fluctuate according to the flow of the endolymph. A change in the velocity of rotation of the head causes deflection of the cupula in one or more ducts of the membranous labyrinth, with consequent movement of the cilia, which, in their turn, generate action potentials in the underlying nerve endings which transmit the impulses related to direction and rotation of the head to the brain. Since each of the three semicircular ducts is at right-angles to the others, head movements in any plane and angular rotation of the head stimulate the cristae ampullares and vestibular neurones. These function in dynamic equilibrium.
Function of the maculae and cristae ampullares. The saccular and utricular maculae play a role in static equilibrium by detecting the exact position of the head with respect to gravitational forces and linear acceleration and deceleration. The utricular macula seems to be more important with regards to changes in head position compared to the saccular macula, which is more sensitive to vibrations.
In normal resting conditions, the nerve fibres in contact with the hair cells continuously transmit impulses at a constant frequency. When the head moves, the weight of the otoliths bends the cilia of the hair cells in the direction of the force of gravity. When the hair cells are bent in one direction, the frequency of nerve impulses increases, and when they are bent in the opposite direction, the frequency of the impulses decreases. In each macula, the various hair cells are oriented in different directions so that a different pattern of stimulation occurs with the different positions of the head. The impulses are transmitted through the vestibular nerve to the central nervous system, informing the brain of the position of the head and inducing changes in the position of the eyes, trunk and limbs.
For example, when the head is in a horizontal position, the input from every side is equal. When the head rotates to the left, the hair cells of the left inner ear are excited and those of the right inner ear are inhibited. All this produces a stimulation of the left vestibulospinal tracts that activate the anti-gravitational muscles of the left side of the neck, trunk and limbs which bring the head and body back into balance. When the head is moved abruptly (in the sense of linear acceleration), the statocones, which have greater inertia than the fluid surrounding them, bend the cilia of the hair cells depending on the direction of movement. The consequent pattern of impulses is sent to the brain, providing the sensation of linear acceleration. This induces the vestibulospinal tracts to activate the muscles necessary to maintain the normal position of the body and head during the acceleration.
The cristae ampullares, in contrast, contain hair cells specialised in the transduction of rotational movements into nerve impulses. In normal resting conditions, the hair cells of the ampullary crests also continuously emit nerve discharges at a constant frequency.
When the head starts to rotate in any direction (angular acceleration), the endolymph in the semicircular ducts tends to remain stationary because of its inertia, while the ducts move accompanying the movement of the head. The consequence is a relative flow of fluid in the direction opposite to that of the rotation of the head. This flow of fluid bends the cilia of the hair cells, changing the frequency of the nerve discharges. The flow in a given direction increases (stimulates) neuronal activity, while flow in the opposite direction decreases (inhibits) the activity of the nerves. After the head has been rotating for a few seconds, the endolymph and semicircular canals move in unison, the cilia return to their resting position, and the nerve impulses return to basal activity. The opposite happens when the rotation of the head stops. The endolymph continues its movement, while the canals stop. In this situation the cilia are bent in the opposite direction, producing an exactly opposite pattern of nerve discharges to the previous pattern. After a few seconds, the endolymph stops moving and the system returns to the resting state.
The most effective stimulus for activating the receptors of the semicircular ducts is rotation of the head in the same plane as that of the duct. Given that every duct is oriented in a different plane of rotation, rotation of the head in different directions stimulates at least one duct. In addition, each semicircular duct on one side is functionally paired with one duct on the other side because of their shared position on the same plane. Rotational movements on one plane stimulate the hair cells of the specific duct on one side and inhibit those on the contralateral side. The brain uses these patterns of nerve discharges to detect when the head starts to rotate. The macula and saccule can detect an abnormal position of the head once this occurs, while the semicircular ducts can detect the rotation of the head at the start of the movement. This enables the brain to activate the appropriate anti-gravitational muscles to prevent an abnormal position before it occurs.
The vestibulo-cochlear nerve and the vestibular ganglion
The vestibular nerve is a proprioceptive nerve that carries impulses from the utricular and saccular maculae, as well as from the cristae ampullares of the semicircular ducts, transmitting them to the vestibular nuclei of the brainstem. The sensory neurones whose fibres form the vestibular nerve are bipolar neurones that are found along the nerve pathway in the inner auditory meatus, where they form the vestibular ganglion (of Scarpa).
The hair cells of the utricular and saccular maculae, as well as those of the cristae ampullares are in contact with the dendrites of the neurones of the vestibular ganglion. The impulses from the hair cells are transmitted to the dendritic part of the neurones of the vestibular ganglion and then conveyed to the central nervous system through centripetal axons which, departing from the ganglion, constitute the vestibular nerve.
Having left the petrous bone through the internal auditory meatus together with the cochlear division of the vestibule-cochlear nerve, the axons of the vestibular nerve pass over the lateral surface of the rostral part of the medulla oblongata, at the cerebellomedullary angle. This is located at the level of the trapezoid body and the attachment of the caudal cerebellar peduncle to the cerebellum. The fibres of the vestibular nerve penetrate the medulla oblongata between the caudal cerebellar peduncle and the spinal tract of the trigeminal nerve. Most of them terminate in the vestibular nuclei. Some enter the cerebellum directly through the caudal peduncle, with terminations in the fastigial nucleus and in the flocculonodular lobe. These axons form the direct vestibulocerebellar tract.
CENTRAL PART:VESTIBULAR NUCLEI AND PROJECTIONS TO OTHER REGIONS OF THE CENTRAL NERVOUS SYSTEM
The four vestibular nuclei are located in the area of the rhomboid fossa (floor of the fourth ventricle) on each side of the brainstem. The nuclei are named, according to their position, as rostral, medial, lateral and caudal. The numerous projections originating from these nuclei can be grouped, according to the part of the central nervous system in which they run, into: spinal medulla, brainstem, and cerebellar (Fig. 3; with kind permission from Elsevier).
Projections in the spinal medulla
The vestibulospinal tract descends in the ipsilateral ventral funiculus along the whole spinal cord, terminating in every spinal segment on interneurones in the ventral grey columns. These interneurones are facilitatory for the ipsilateral alpha and gamma motor neurones that innervate the extensor muscles, while they are inhibitory for the ipsilateral alpha motor neurones that innervate the flexor muscles; some interneurones cross over to the ventral grey column of the spinal cord on the other side where they are inhibitory to the contralateral alpha and gamma motor neurones to extensor muscles. Thus, the effects of stimulating neurones from which the vestibulospinal tract originates are an increase in ipsilateral extensor tone and inhibition of contralateral tone. In the healthy animal, the mechanism is bilateral, balanced and symmetrical. It is clear that impaired function of one vestibulospinal tract can cause an imbalance of extensor tone between the two halves of the body, with loss of extensor tone and falling of the subject towards the affected side.
The medial vestibular nucleus projects axons in the medial longitudinal fasciculus, which descends in the dorsal part of the ventral funiculus through the cervical and cranial spinal cord segments, influencing the alpha and gamma motor neurones through interneuronal activation. The position and motor activity of the trunk and limbs are co-ordinated with the movements of the head through these spinal cord pathways.
Projections in the brainstem
The axons run in a rostral direction in the medial longitudinal fasciculus and in the reticular formation to influence the nuclei of cranial nerves VI, IV and III. This guarantees co-ordinated conjugate movements of the eyes in relation to changes in head position. These projections are responsible for normal vestibular nystagmus, abnormal spontaneous nystagmus, and positional strabismus.
Some axons project from the vestibular nuclei into the reticular formation and of these, some enter the vomiting centre, thus being responsible for the phenomenon of kinetosis (motion sickness). It is easy to understand that unbalanced or excessive stimuli can cause vomiting or other signs of intolerance of movement. The conscious perception of balance is produced through pathways that have not yet been well defined. It is thought that fibres ascend from the vestibular nuclei to the thalamic integration centres and from here to the temporal cortex.
Projections in the cerebellum
The axons of the vestibular nuclear neurones project towards the cerebellum through the caudal cerebellar peduncle and most terminate in the flocculus and the nodule of the caudal vermis (theflocculonodular lobe), as well as in the fastigial nucleus. The efferent pathways from the cerebellar nuclei to the vestibular nuclei are ipsilateral, as are the afferent pathways; these major projections give the cerebellum a strong influence on the activity of the vestibular nuclei. Through these pathways, the vestibular system is functionally involved in co-ordinating the limbs, trunk and eyes with the movements of the head. It maintains balance during active and passive movements and when the head is in the resting position.
Suggested reading
- Baron R. (2006): Anatomia degli animali domestici. Ed. italiana a cura di R. Bortolami. Edagricole.
- Bortolami, Callegari, Beghelli (2006): Occhio e Orecchio. Anatomia e Fisiologia degli Animali Domestici. Edagricole.
- De Lahunta A., (2008): Vestibular system – special proprioception. Veterinary neuroanatomy and clinical neurology. Philadelphia: W.B. Saunders.
- King A.S. (1994): Special Sensis. Phisiological and clinical anatomy of the domestic animals. Oxford University Press.
- Foss I. e Flottorp G. (2000): Anatomia microscopica veterinaria. Dellmann H.D. Eurell J.A. Ed. italiana a cura di R. Bortolami-M.L. Lucchi. Ambrosiana.
- Jenkins TW (1989): Orecchio Udito ed Equilibrio. Neuroanatomia funzionale dei mammiferi. Ed. Italiana a cura di R. Bortolami-E.Callegari. Edagricole.