Vestibular System Dr. Bill Yates Depts. Otolaryngology and Neuroscience 110 Eye and Ear Institute
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1 Vestibular System Dr. Bill Yates Depts. Otolaryngology and Neuroscience 110 Eye and Ear Institute What is the Vestibular System? The vestibular system is the sensory system, whose receptors are located in the inner ear, that detects head position and head movements. What Does It Do? Relays signals to motoneurons that control posture, to help prevent the loss of balance. Relays signals to motoneurons that innervate eye muscles (extraocular motoneurons) to aid in visual fixation during head movements. Provides for a sense of where we are in space, including an implicit knowledge of up and down. Helps to provide for changes in respiration and circulation that are necessary as we move and change posture. Why Can t Other Sensory Systems Do the Same Job? Teasing-out specific information about the location of the body in space and the direction and velocity of movements could be done by the visual system (along with the somatosensory and other sensory systems). However, this would require a tremendous amount of information processing by the cerebral cortex, which requires time (several hundredths of a second). Correction for changes in head and body position must be accomplished at faster speeds to allow for the maintenance of stable posture, visual fixation, and autonomic control. Furthermore, many mammals move-about in the dark, so they can t always depend on their visual system. Morphology of the Vestibular Apparatus The vestibular labyrinth consists of a system of interconnecting fluid-filled sacs (utriculus and sacculus) and 3 channels (semicircular canals) surrounded by a bony capsule of approximately the same shape. The epithelium comprising these fluid-filled sacs, which is called the membranous labyrinth, is simple, squamous epithelium. The outer bony capsule is called the bony labyrinth. The membranous labyrinth contains a peculiar fluid called endolymph, which has a high K+ and a low Na+ concentration and a positive charge (+80 mv); the cavity between the membranous and bony labyrinth contains a fluid with a composition similar to cerebrospinal fluid called perilymph. Systems Neurobiology Page 1 February 13, 2015
2 Hair cells are the receptor cells of the vestibular sensory organs. They have a structure much like auditory hair cells, including staircase-arranged rows of stereocilia. Unlikely the auditory hair cells, however, vestibular hair cells have a single long kinocilium. The hair cells are embedded into the membranous labyrinth, and their stereocilia are bathed by the endolymph found within the membranous labyrinth. The apical ends of the hair cells, along with the associated supporting cells, are joined together by tight junctions to allow for the segregation of endolymph and perilymph, which bathes the body of the hair cell. Vestibular hair cells make synapses onto afferents of the vestibular branch of the VIIIth cranial nerve. As in the auditory system, the stereocilia are physically coupled with mechanically-gated channels. At rest (when the stereocilia are unbent) some channels are open and some release of neurotransmitter occurs. Thus, the vestibular afferents in the VIIIth nerve have a resting discharge. Bending the stereocilia towards the kinocilium pulls more of the channels open, and the hair cell becomes more depolarized, leading to more release of neurotransmitter onto VIIIth nerve afferents (thus inducing them to fire more). Bending the stereocilia away from the kinocilium leads to closing of all channels, which reduces neurotransmitter release from the hair cell. As a result, firing in the VIIIth nerve afferents decreases. Bending the hairs from side to side with respect to the kinocilium has no effect on the release of neurotransmitter from the hair cell. Systems Neurobiology Page 2 February 13, 2015
3 It was originally believed that the mechanically-gated channels that are pulled-open during the bending of stereocilia were found at the base of the cilia. Subsequently, however, it was discovered that current flows from the extracellular space near the apical tips of the stereocilia. Today we know that channels near the tips of the stereocilia are connected to the next highest cilium by a thin filament. This arrangement both explains the mechanical sensitivity of the hair cell and the reason why the cilia are arranged in a staircase pattern. Thus, the hair cell is a very flexible element in the transduction of a number of stimuli. By changing the structure that is responsible for moving the stereocilia, the adequate stimulus for these receptors can be altered. Systems Neurobiology Page 3 February 13, 2015
4 Potassium is the main ion involved in depolarizing the hair cells following the bending of stereocilia towards the kinocilium. A release of glutamate is triggered by the rise of intracellular calcium concentration; calcium is imported through voltage-gated calcium channels. Types of Hair Cells Two general types of hair cells exist in the vestibular system: Type 1 and Type 2. The properties of these receptor elements are summarized in the following table and figure. Systems Neurobiology Page 4 February 13, 2015
5 Calyz and bouton afferent terminations have been labeled through intracellular injections of horseradish peroxidae. Calyz endings have a very complex shape, and totally engulf the body of the hair cell. Fiber Caliber and Afferent Response Classical morphologists appreciated that vestibular hair cells were innervated by thick, medium-sized and thin fibers. Thick fibers supply calyceal endings to type I hair cells. Thin fibers make bouton-type contacts with type II hair cells. Medium-sized fibers provide endings to both types of hair cells. More recently, it was discovered that different calibers of vestibular afferents have a distinct physiology. Thick fibers have an irregular spontaneous discharge, thin fibers have a regular spontaneous discharge, and medium fibers have mixed properties (some are regular, others are irregular). Irregular fibers have a much higher sensitivity than regular fibers. Regularly-firing vestibular afferents mainly innervate type II hair cells and have a low sensitivity. Irregular vestibular afferents have a higher sensitivity, and mainly innervate type I hair cells. Systems Neurobiology Page 5 February 13, 2015
6 How Are the Hair Cell Stereocilia Moved in the Vestibular Sensory Organs? Semicircular Canals: Three semicircular canals are found in each inner ear: the lateral (horizontal), superior (anterior), and inferior (posterior) canals. These are roughly located at right angles to each other. When the head is located in its "normal" upright position, the lateral semicircular canal is parallel with the floor. The hair cells are confined to a swelling at a central end of each semicircular canal, called the ampulla. Within the ampulla, the hair cells are arranged such that their kinocilia point towards the utricle (i.e., towards the central end of the ampulla). The stereocilia are embedded in a gelatinous mass called the cupula, which has the same specific gravity as the surrounding endolymph. The sensory epithelium within an ampulla is called the crista ampullaris. Because of this arrangement, the semicircular canals respond to angular acceleration. Angular acceleration results when a force is applied to an object which is constrained to move about an axis. The semicircular canals are subjected to angular acceleration whenever the head turns about the neck (i.e., you look around) or when the entire head and body is turned, as on an amusement ride than spins you about. When you turn your head to the left, the fluid in the horizontal semicircular canals lags behind the turning movement because of inertia. In effect, the fluid appears to be moving right with respect to the head. As a result, the cupula in the left semicircular canal is deflected so that the embedded stereocilia are pushed towards the kinocilia, and the firing rate of the vestibular afferents innervating the left horizontal crista ampullaris increases. In parallel, the firing rate of the right horizontal semicircular canal afferents decreases. Systems Neurobiology Page 6 February 13, 2015
7 Three factors are involved in establishing the discharge properties of semicircular canal afferents during angular head rotations: 1) The inertial reaction of the endolymph 2) The damping of endolymph movement by viscous forces of the fluid within the small canal lumen. 3) The springlike restoring force opposing deflections of the cupula. Constant velocity rotations (as you would experience if you were sitting on a large turntable for an extended period) produce no angular acceleration. After a short period of rotation, the movement of fluid in the semicircular canals no longer lags behind the head, there is no longer a deflection of the cupula, and the firing rate of the semicircular canal afferents on the two sides becomes equal. In general, all angular head movements affect semicircular canals on both sides of the head: By integrating changes in the firing patterns of the 3 pairs of semicircular canals, the central nervous system can determine the direction of angular head movements. What Information Isn't Provided by the Semicircular Canals? 1. Information concerning the static position of the head in space (location with respect to gravity). 2. Information regarding linear accelerations placed on the head, as occur during falling or when accelerating/stopping in a car. This information is provided by the otolith organs. There are two otolith organs: the utricle and the sacculus. These sensory organs differ from the semicircular canals in two important ways: 1. The stereocilia are embedded in a membrane (the otolithic membrane) that has a higher specific gravity than the surrounding fluid. The gelatinous membrane is filled with calcium carbonate crystals, called otoconia (which literally means "stone"), that make it very heavy. This membrane shifts in position when tilted, or when subjected to linear acceleration in its plane. 2. The hair cells do not all face in the same direction; many different orientations exist. Systems Neurobiology Page 7 February 13, 2015
8 Hair cells in the utricular macula are affected by linear acceleration in the horizontal plane (e.g., accelerating in a car) and by tilting the head with respect to gravity. Hair cells in the saccular macula are affected by linear acceleration in the vertical plane (e.g., accelerating in an elevator or falling) and by tilting the head with respect to gravity. Structure of the Otolith Organs Direction of polarization of hair cells in the utricle and sacculus. Note that the direction that the hair cells face reverses abruptly at a point (indicated by a line) called the striola. Systems Neurobiology Page 8 February 13, 2015
9 Differentiating Otolith and Canal Responses in the Laboratory Two types of rotations are used to determine if a vestibular afferent that is being recorded innervates otolith organs or semicircular canals. If a trapezoidal head rotation is delivered, the firing of afferents innervating canals near the plane of rotation will be affected only during the time when the head is moving. In contrast, trapezoidal rotations near the axis of polarization of an otolith hair cell will cause a change in firing rate in proportion to the amplitude of the rotation. Sinusoidal rotations can also be used to differentiate canal and otolith responses. Because the acceleration associated with the sinusoidal stimulus increases in proportion to the frequency of the stimulus, canal afferents respond much better to high-frequency rotations than to low-frequency rotations. Furthermore, canal afferents respond in phase with the velocity of the sinusoidal stimulus (90 phase advance with respect to stimulus position) over the physiological range of head rotation frequencies. In contrast, otolith afferents have little gain increase with increasing stimulus frequency, and respond in phase with stimulus position. Systems Neurobiology Page 9 February 13, 2015
10 Central Nervous System Connections of Vestibular Afferents Although some vestibular afferents project directly to the cerebellum, most terminate in one of 4 brainstem nuclei, which are collectively called the vestibular nuclei. The 4 vestibular nuclei are distinguished on the basis of cytoarchitecture, and are located near the dorsal surface of the brainstem. They are the superior, lateral (also called Deiters' nucleus), medial, and inferior (or descending) nuclei. The vestibular nuclei extend rostro-caudally throughout much of the medulla and pons. The diagram to the left shows the locations of the vestibular nuclei on the surface of the brainstem (perspective is looking down on the brainstem with the cerebellum removed). Projections of the Vestibular Nuclei and their Function 1. The vestibular nuclei on the two sides have extensive interconnections. These connections are not surprising, since the nervous system needs to analyze inputs from the two labyrinths to determine body position in space. 2. The vestibular nuclei have extensive connections with the cerebellum. Cerebellar inputs to the vestibular nuclei come from the medial cerebellum (cortex + fastigial nucleus) and from the vestibulocerebellum (flocculus). These connections will be explored in detail later in the course. 3. The vestibular nuclei have extensive connections with cranial nerve nuclei III, IV, and VI, which contain motoneurons that innervate eye muscles. The beststudied of the vestibulo-ocular reflexes is that elicited by horizontal rotation of the head. This reflex acts to stabilize a target on the fovea during head movements. The circuitry associated with the horizontal vestibulo-ocular reflex is diagramed to the left. 4. The vestibular nuclei have extensive effects on spinal motoneurons. The vestibulospinal tracts mainly affect motoneurons indirectly via connections with interneurons. The reticulospinal system also carries vestibular information to the spinal cord. These connections will be discussed in detail later in the course. 5. The vestibular nuclei also have effects on neurons in cerebral cortex. Although no one area of cortex exclusively processes vestibular signals, several regions contain cells that receive convergent vestibular and other inputs. The cortical areas receiving vestibular inputs include somatosensory cortex (both SI and SII). The inputs to somatosensory cortex involve a relay through the VPL thalamic nucleus. Systems Neurobiology Page 10 February 13, 2015
11 6. The vestibular nuclei also make direct and indirect connections with brainstem monoaminergic neurons, and thus vestibular signals participate in the global "modulatory" functions of the monoaminergic systems. Vestibular inputs have been demonstrated to locus coeruleus and subcoeruleus, as well as to the medullary raphe nuclei. 7. It has recently been shown that the vestibular system has influences on regions of the brainstem that control respiration and circulation. Vestibular effects on the respiratory and circulatory systems are important in making adjustments in breathing and circulation that are necessary during movement and changes in posture. Non-Vestibular Inputs to the Vestibular Nuclei The vestibular nuclei also receive other sensory inputs. Amongst these are inputs from proprioceptors, including muscle spindles in neck muscles. It is important that the vestibular system differentiates between whole body movements and head movements. Head movements involve contraction/stretching of muscles in the neck, which results in inputs from neck muscle spindles. Neck muscles have a particularly high density of muscle spindles, so neck movements provide tremendous sensory feedback to the nervous system. Many (but not all) neurons in the vestibular nuclei have complementary inputs from neck and vestibular receptors, such that the two inputs cancel each other out during head movements. These neurons fire only when the vestibular system alone is stimulated (as when we lose our balance and begin to fall over), and not when the head is moved. Example: Left Side Down Tilt of Body (Vestibular receptors stimulated) Cell Firing Increases Left Side Down Tilt of the Neck (Head fixed in space, and body rotated) (Neck Muscle Spindles Stimulated) Cell Firing Decreases Left Side Down Head Movement No Change in Cell's Firing (Neck and Vestibular Receptors Stimulated Together) Systems Neurobiology Page 11 February 13, 2015
12 Convergence of Vestibular Inputs in the Vestibular Nuclei By and large, vestibular nucleus neurons have similar response properties as vestibular afferents. An exception is that many vestibular nucleus neurons receive convergent inputs from semicircular canals and otolith organs. In general, the otolith and canal inputs to a neuron are spatially aligned, so that the neuron's preferred direction of rotation is similar at both low and high frequencies. A few neurons, however, have canal and otolith inputs that are not aligned spatially. This misalignment produces unusual response properties. In particular, the preferred direction of rotation changes with stimulus frequency. At frequencies that produce comparable activation of canals and otoliths, there is no preferred direction. Systems Neurobiology Page 12 February 13, 2015
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