Information about the position and movement of the body with respect to the external environment is vital for normal bodily function. It allows us, for example, to walk and run upright without falling over, and at the same time to maintain steady fixation on an object that may itself be moving. The speed and precision with which the mammalian brain can gather and use this information is evident in the supreme body control displayed by predators such as cats. When a cat falls from a tree or ledge, it can sense the orientation of its body relative to the ground and maneouvre itself to land feet-first, even when falling from an inverted position.
Physiology of the Vestibular System
The neural system responsible for such beautifully executed movements, the vestibular system, is a prime example of exquisite biological engineering. It employs receptors that are sensitive to the forces of gravity and acceleration acting on the head. The two organs housing these receptors lie buried in deep openings on either side of the skull known as vestibules. Consequently they are called the ‘vestibular organs’.
This figure shows the position of the vestibular organs in the head. Each organ consists of a complex set of interconnected canals, known as the vestibular labyrinth. Another organ, the cochlea, is connected to each vestibular organ, and shares its afferent nerve, the eighth cranial nerve. The cochlea is a complex spiral-shaped canal that mediates hearing. In both the vestibular organ and the cochlea sensory reception is based on minute displacements of hair cells, caused by the movement of fluid inside the organ. In the case of the vestibular system, fluid movement is caused by accelerations of the head, or by gravity. In the case of the cochlea, fluid movement is caused by air pressure waves transmitted through each ear.
Vestibular Receptors
The figure (from Purves et al., 2001) depicts a group of vestibular hair cells on a patch of sensory epithelium. Notice that each hair cell gives rise to a single tall, thick hair known as a kinocilium, and a number of smaller, narrower hairs (stereocilia) grouped together on one side of the kinocilium. The stereocilia decrease in size with distance away from the kinocilium, and thin filaments connect the tip of each cilium to the side of its taller neighbour. This arrangement is crucial to the sensory properties of hair cells.
Hair cells do not have axons, and do not generate action potentials. Instead, pre- synaptic active zones around the base of each hair cell make synaptic connections with afferent nerve cells forming part of the VIIIth cranial nerve. Stimulation of a hair cell increases its receptor potential and causes the release of chemical neurotransmitter from its pre-synaptic zones. This transmitter influences the pattern of action potentials generated by the sensory neuron. Movement of the stereocilia towards the kinocilium depolarizes the hair cell and results in increases in sensory nerve activity. Movement of the stereocilia away from the kinocilium hyperpolarizes the cell, reducing sensory nerve activity. In the patch of sensory epithelium shown in the Figure all the hair cells are aligned so that deflection to the left causes excitation, and deflection to the right causes inhibition. Resting potentials in hair cells generate a high level of spontaneous neural activity in sensory nerves (about 110 spikes per second), so the firing rate of vestibular nerve fibres can faithfully reflect the change in receptor potential, increasing or decreasing in accordance with the movement of the cilia. The significance of this biphasic response is that it allows nerve fibres to signal the direction of displacement of the hairs, which depends directly on the direction of tilt or acceleration of the head, as we shall see.
The Vestibular Labyrinth The labyrinth consists of two chambers (otolith organs), the utricle and the saccule, and three semicircular canals. All of these membranous structures are inter-connected and filled with fluid (endolymph). In each structure there is a small area of sensory epithelium containing hair cells. Displacement of these hair cells provides the stimulus for vestibular responses. In the saccule, the sensory epithelium is oriented vertically, and in the utricle it is oriented horizontally. The three semicircular canals are oriented at right-angles to each other. The two vestibular organs on either side of the body are mirror images of each other. The significance of this arrangement becomes apparent when one considers the physics of head movement and the vertical direction of gravitational force. Head movements can be defined in terms of three principle planes and three axes passing through the head, as illustrated below.
The median plane passes vertically through the head from front to back. The frontal plane passes vertically through the head from side to side. Finally, the transverse plane passes through the head horizontally. The x-axis runs from front to back, the y- axis runs from side to side, and the z-axis runs vertically. Within this framework, there are six possible ways that the head can move, usually called six degrees of freedom, also shown in the figure. There are three possible linear (translatory) movements, corresponding to translation along one of the three axes (backward and forward along the x-axis; sideways along the y-axis; up and down along the z-axis). There are also three possible rotational movements corresponding to rotation in one of the three planes. Rotation in the median plane, as in a ‘yes’ nod, is called ‘pitch’. Rotation in the transverse plane, as in a ‘no’ shake, is known as ‘yaw’. Rotation in the frontal plane, as in a side-ways tilt of the head, is known as ‘roll’. Each of these six different possible movements can occur independently of the others. Complex natural movements of the head can be considered to contain a combination of two or more of these movement components. For example, as you bend down to tie a shoe lace, your head might move in a way that combines linear downward motion in the median plane and rotational movement about the y-axis as the head tilts forward. A turn of the head to one side during this movement would add a second rotational component about the z-axis.
The otolith organs and semicircular canals are shaped and positioned very precisely so that their responses during natural three-dimensional head and body movements effectively decompose complex movements into their translatory and rotational components. This decomposition is crucially important for proper control of body and eye position. For example the presence of a translatory component of body movement may indicate a need to adjust one’s balance, while the presence of rotational component may require compensating eye movement to maintain steady fixation on an object. The vestibular labyrinth is beautifully designed to achieve this decomposition. The otolith organs provide information about linear movement components, and the semicircular canals provide information about rotational components. Precisely how they achieve this decomposition is explained in the following paragraphs.
Otolith Organs The patch of hair cells in each otolith organ is called the macula. It is covered in a gelatinous layer, which in turn is covered by a heavy fibrous carpet (otolithic membrane) containing calcium carbonate crystals (otoconia; see Figure above, from Purves et al., 2001). Linear acceleration of the head causes a shifting or shearing motion between the layer of hair cells and the otolithic membrane above them (similar to the movement of a loosely-fitting hat placed on the head when the head is moved or tilted). The shearing motion displaces the hair cells and results in a sensory response, as shown in the Figure (right). Recall from the previous section that individual hair cells are directional in the sense that deflections toward the kinocilium are excitatory and deflections away from the kinocilium are inhibitory. Close examination of the arrangement of hair cells in the saccule and utricle reveals that the macula in each is split down the middle. All hair cells on one side of the division are excited by deflection in one direction but inhibited by deflection in the opposite direction, whereas hair cells on the other side of the division show the opposite pattern of response. This arrangement allows the organs to distinguish between opposite directions of shear on the basis of the pattern of excitation. Since the macula of the utricle is approximately horizontal, and the macula of the saccule is roughly vertical, the two organs together can signal linear acceleration along any axis, since one or the other or both will always be activated. The otolith organs respond to acceleration rather than to movement at a constant velocity, because displacement of their hair cells is due to the initial inertia of the otolithic membrane. Once a steady speed of bodily motion is reached, the otolithic membrane catches up with the macula, so the hair cells return to their resting position. It is important to note that the otolith organs provide static information about gravitational vertical as well as dynamic information about linear acceleration. This property arises from Einstein’s equivalence principle, according to which a gravitational force field is equivalent to an artificial force field resulting from linear acceleration (the effect of gravity can, of course, be described in terms of acceleration toward the ground at a specific rate). Consequently, as illustrated in the Figure above, the shearing motion of the otolithic membrane produced by horizontal acceleration is identical to that produced by a static tilt of the head at an angle of 15 deg. This equivalence has important consequences for perception.
Semicircular Canals In each semicircular canal the bundle of hairs cells (known as the crista) stretches across the canal inside a gelatinous mass (the cupula) that blocks the flow of fluid around the canal. Rotational acceleration of the head causes a flow of fluid around the canal, due to the inertia of the fluid. The cupula is distorted by the force of these currents, displacing the hair cells by a very small amount (about 10 millimicrons for a relatively slow head movement), as shown in the Figure above (bottom). The curved shape of the semicircular canals allows them to signal rotational acceleration of the head, because this movement will set up strong current flows around the canals. Since there are three degrees of freedom in rotational movement, three canals in each labyrinth are sufficient to detect any combination of the components. The canals are roughly at right-angles because this is the optimal arrangement to signal movement about the three possible axes, which are also at right- angles. Unlike hair cells in the utricle and saccule, hair cells in each canal are arranged with their kinocilium pointing in the same direction, so all cells within a particular canal will be excited or inhibited together by movement of fluid in a particular direction through the canal. It is important to note that each canal works in partnership with its mirror-image canal on the other side of the head, whose hair cells point in the opposite direction. Rotation of the head about any axis will set up strong current flows in the canals on each side of the head, but the resulting responses from canals on opposite sides will be in opposition. For example, a leftward head turn will cause an increase in firing rate in the left vestibular nerve, connected to the left horizontal canal, but a decrease in firing rate in the right vestibular nerve. Rightward rotation reverses the pattern of firing. This arrangement also applies to the other two pairs of canals (left anterior and right posterior, left posterior and right anterior), which respond well to rotation in the x- and z- axes. The semicircular canals respond only to angular acceleration, not to a constant angular velocity of rotation. As in the case of the otolith organs, this property arises because of the initial inertia of the endolymph fluid at the start of the rotation. Once a steady rotational velocity has been reached, the fluid catches up with the canal movement, and the cupula returns to its rest position.
Central Vestibular Pathways
Hair cell responses are transmitted along the vestibular branch of the VIIIth cranial nerve. There are about 20,000 fibres on each side of the head, most of which terminate in several large groups of neurons in the brainstem called the vestibular nuclei. The remainder project directly to the cerebellum (see below). Projections from the vestibular nuclei can be grouped into four systems, two ascending ( cerebellar and thalamic), and two descending (spinal and ocular).
The vestibulo-cerebellar system projects to the cerebellum, and regulates the movements that control posture and bodily equilibrium.
The vestibulo-thalamic system's cortical projections may mediate perception of balance.
The vestibulo-spinal system is thought to be involved in reflexive control of body posture and head position in space.
The vestibulo-ocular system mediates reflexive eye movements (vestibulo-ocular reflex) that compensate for head movement and stabilize the visual image.
Vestibular Perception
As we have seen above, the sensory information supplied by the vestibular system is used largely to control reflexive movements of the eyes and limbs. Its cortical representation is small relative to the representation of the other senses. In addition, information about the body’s position and movement in the environment is available from vision as well as from the vestibular system. For example, contour orientation and texture gradients offer cues about the orientation of the ground plane relative to the body, and large-scale patterns of movement in the image (‘optic flow’) offer reliable information on bodily movement. Vestibular responses tend to intrude on conscious experience only when there is a discrepancy between visual information and vestibular information. The resulting sensations of ‘motion sickness’ can, however, be very powerful, often inducing confusion, disorientation and nausea. The situations giving rise to such discrepancies typically involve subjecting the body to movements outside the range normally experienced.
Perceptual effects attributable to vestibular responses
The oculogyral illusion and Coriolis effects Everyone has experienced the dizziness that results from rotating the body about the z (vertical) axis very rapidly. Just as the spin stops there is a strong illusory sense of bodily movement, and loss of body equilibrium, accompanied by apparent visual movement in stationary objects and reflexive movements of the eyes ( the ‘oculogyral illusion’). These effects can be attributed to responses in the semicircular canals. During initial acceleration into the spin, ‘backward’ deflection of the cupula due to its inertia leads to appropriate vestibular signals concerning angular acceleration. During sustained rotation the cupula returns to its resting position. During and after deceleration as the spin stops, momentum in the fluid deflects the cupula ‘forwards’ in the direction normally associated with a spin in the opposite direction. The resulting erroneous signals lead to disorientation and dizziness. The illusory impression of turning can persist for up to 30 or 40 seconds after stopping, during which time the vestibular system recovers to its resting state.
Coriolis effects are experienced when the head is moved during a spin. Head movements modify the effect that the spin has on the semicircular canals. If the head rotates about the same axis as the spin, there is a momentary increase or decrease in the total angular acceleration of the head. If the head rotates about a different axis, then the angular accelerations produced by the spin and by the head rotation interact in a complex way, under forces known as Coriolis forces (similar to the forces that act on a spinning wheel if you try to turn its axis at right angles to itself). For example, if you are spinning in a leftward direction, and incline your head forward during the spin, the resultant stimulation of the canals produces a sensation that the head is being tilted sideways toward the left shoulder (see Howard, 1982, for more details). The mismatch with information supplied by the otolith organs and by vision induces dizziness and nausea.
The oculogravic illusion Illusory tilt that is perceived during linear acceleration is known as the oculogravic illusion. For example, a seated individual undergoing horizontal linear acceleration will experience a strong sensation of backwards tilt, and a corresponding apparent elevation of visible points positioned at eye level. The illusion can be attributed to responses in the otolith organs. As discussed earlier, the macula cannot distinguish between displacements due to horizontal acceleration and displacements due to static head tilt. As a result, a displacement of the macula during acceleration may be attributed, at least partially, to head tilt. This illusion can have potentially disastrous consequences in modern transportation.
Vection Wood in 1895 described a visit to a fairground attraction called the ‘Haunted Swing’ at the San Francisco Midwinter Fair. Visitors entered a large cubical room containing various items of furniture, and sat on a large swing that hung in the centre of the room. The swing was set in motion, eventually turning a complete revolution. Participants experienced a compelling sensation of bodily movement, but in reality the swing was stationary, and the room moved (the furniture was fastened to the floor). Wood reports that “many persons were actually made sick by the illusion…[and could] …scarcely walk out of the building from dizziness and nausea”. This kind of illusory motion is sometimes known as vection (Howard, 1982). Lishman and Lee (1973) constructed a moveable room similar to that used in the Haunted Swing to study one form of vection, apparent translation or ‘linearvection’. The subject stood on a stationary platform inside the room, the walls and ceiling of which swung back and forth slowly. Adults experienced a sensation of body sway, and tended to sway in synchrony with the room to compensate for the apparent movement of the body. Infants who had recently learned to walk fell over as soon as the room began to move. Illusions of rotary movement of the body (‘circularvection’) can be induced by placing the subject inside a large textured cylinder, and setting the cylinder to rotate around the subject very slowly. One could argue that vection is not truly a consequence of vestibular responses, because the subject is stationary, and the illusion is induced by movement of the scene surrounding her. However, visually induced sensations of body motion (involving no direct stimulation of the vestibular organs) are indistinguishable from sensations induced by actual body motion. For example, if a person tilts his head while experiencing visually induced rotation of the body, he experiences the same Coriolis effect that would be induced by real rotation.
Readings
Howard I (1982) Human Visual Orientation. Wiley, New York.
Lishman J, Lee D (1973) The autonomy of visual kinaesthesis. Perception 2, 287-294.
Purves D, Augustine G, Fitzpatrick D, Katz L, LaMantia A, McNamara J, Williams S (2001) Eds. Neuroscience 2nd Ed. Sinauer, Sunderland Mass.