Vestibulo–ocular reflex

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The vestibulo-ocular reflex. A rotation of the head is detected, which triggers an inhibitory signal to the extraocular muscles on one side and an excitatory signal to the muscles on the other side. The result is a compensatory movement of the eyes. Simple vestibulo-ocular reflex.PNG
The vestibulo-ocular reflex. A rotation of the head is detected, which triggers an inhibitory signal to the extraocular muscles on one side and an excitatory signal to the muscles on the other side. The result is a compensatory movement of the eyes.

The vestibulo-ocular reflex (VOR) is a reflex that acts to stabilize gaze during head movement, with eye movement due to activation of the vestibular system, it is also known as the Cervico-ocular reflex. The reflex acts to stabilize images on the retinas of the eye during head movement. Gaze is held steadily on a location by producing eye movements in the direction opposite that of head movement. For example, when the head moves to the right, the eyes move to the left, meaning the image a person sees stays the same even though the head has turned. Since slight head movement is present all the time, VOR is necessary for stabilizing vision: people with an impaired reflex find it difficult to read using print, because the eyes do not stabilise during small head tremors, and also because damage to reflex can cause nystagmus. [1]

Contents

The VOR does not depend on what is seen. It can also be activated by hot or cold stimulation of the inner ear, where the vestibular system sits, and works even in total darkness or when the eyes are closed. However, in the presence of light, the fixation reflex is also added to the movement. [2] Most features of VOR are present in kittens raised in complete darkness. [3]

In lower animals, the organs that coordinate balance and movement are not independent from eye movement. A fish, for instance, moves its eyes by reflex when its tail is moved. Humans have semicircular canals, neck muscle "stretch" receptors, and the utricle (gravity organ). Though the semicircular canals cause most of the reflexes which are responsive to acceleration, the maintaining of balance is mediated by the stretch of neck muscles and the pull of gravity on the utricle (otolith organ) of the inner ear. [2]

The VOR has both rotational and translational aspects. When the head rotates about any axis (horizontal, vertical, or torsional) distant visual images are stabilized by rotating the eyes about the same axis, but in the opposite direction. [4] When the head translates, for example during walking, the visual fixation point is maintained by rotating gaze direction in the opposite direction, [5] by an amount that depends on distance. [6]

Function

Vestibulo-ocular reflex EN.svg

The vestibulo-ocular reflex is driven by signals arising from the vestibular system of the inner ear. The semicircular canals detect head rotation and provide the rotational component, whereas the otoliths detect head translation and drive the translational component. The signal for the horizontal rotational component travels via the vestibular nerve through the vestibular ganglion and end in the vestibular nuclei in the brainstem. From these nuclei, fibers cross to the abducens nucleus of the opposite side of the brain. Here, fibres synapse with 2 additional pathways. One pathway projects directly to the lateral rectus muscle of the eye via the abducens nerve. Another nerve tract projects from the abducens nucleus by the medial longitudinal fasciculus to the oculomotor nucleus of the opposite side, which contains motor neurons that drive eye muscle activity, specifically activating the medial rectus muscle of the eye through the oculomotor nerve.

Another pathway (not in picture) directly projects from the vestibular nucleus through the ascending tract of Deiter's to the medial rectus muscle motor neuron of the same side. In addition there are inhibitory vestibular pathways to the ipsilateral abducens nucleus. However no direct vestibular neuron to medial rectus motoneuron pathway exists. [7]

Similar pathways exist for the vertical and torsional components of the VOR.

Oculomotor integrator

In addition to these direct pathways, which drive the velocity of eye rotation, there is an indirect pathway that builds up the position signal needed to prevent the eye from rolling back to center when the head stops moving. This pathway is particularly important when the head is moving slowly because here position signals dominate over velocity signals. David A. Robinson discovered that the eye muscles require this dual velocity-position drive, and also proposed that it must arise in the brain by mathematically integrating the velocity signal and then sending the resulting position signal to the motoneurons. Robinson was correct: the 'neural integrator' for horizontal eye position was found in the nucleus prepositus hypoglossi [8] in the medulla, and the neural integrator for vertical and torsional eye positions was found in the interstitial nucleus of Cajal [9] in the midbrain. The same neural integrators also generate eye position for other conjugate eye movements such as saccades and smooth pursuit.

The integrator is leaky, with a characteristic leaking time of 20 s. For example, when the subject is sitting still and focusing on an object, and suddenly the light is turned off, the eyes would return to their neutral position in around 40 seconds even as the subject is attempting to keep the focus. [10] [11]

Example

For instance, if the head is turned clockwise as seen from above, then excitatory impulses are sent from the semicircular canal on the right side via the vestibular nerve through Scarpa's ganglion and end in the right vestibular nuclei in the brainstem. From this nuclei excitatory fibres cross to the left abducens nucleus. There they project and stimulate the lateral rectus of the left eye via the abducens nerve. In addition, by the medial longitudinal fasciculus and oculomotor nuclei, they activate the medial rectus muscles on the right eye. As a result, both eyes will turn counter-clockwise.

Furthermore, some neurons from the right vestibular nucleus directly stimulate the right medial rectus motor neurons, and inhibits the right abducens nucleus.

Integrated neural control

The VOR is controlled by a neural integrator. The neuron from each horizontal semicircular canal fires at a rate of , where is the sensed horizontal angular velocity of the semicircular canal. The motoneuron commanding the horizontal eye muscles fires at a rate of , where is the horizontal turning angle, and is its horizontal angular speed. The two terms account for the elasticity and viscosity of ocular tissue. [12]

The rotational moment of inertia of the eye is negligible, as individuals wearing weighted contact lens that increases the rotational moment of inertia almost 100-fold still has the same VOR (p. 94 [13] ).

Speed

The vestibulo-ocular reflex needs to be fast: for clear vision, head movement must be compensated almost immediately; otherwise, vision corresponds to a photograph taken with a shaky hand. Signals are sent from the semicircular canals using only three neurons, called the three neuron arc. This results in eye movements that lag head movement by less than 10 ms. [14] The vestibulo-ocular reflex is one of the fastest reflexes in the human body.

VOR suppression

When a person tracks the movement of something with both their eyes and head together, the VOR is counterproductive to the goal of keeping the gaze and head angle aligned. Research indicates that there exists mechanisms in the brain to suppress the VOR using the active visual (retinal) feedback obtained by watching the object in motion. [15] In the absence of visual feedback, such as when the object passes behind an opaque barrier, humans can continue to visually track the apparent position of the object using anticipatory (extra-retinal) systems within the brain, and the VOR is also suppressed during this activity. The VOR can even be cognitively suppressed, such as when following an imagined target with the eyes and head together, although the effect tends to be less dramatic than with visual feedback. [16]

Gain

The "gain" of the VOR is defined as the change in the eye angle divided by the change in the head angle during the head turn. Ideally the gain of the rotational VOR is 1.0. The gain of the horizontal and vertical VOR is usually close to 1.0, but the gain of the torsional VOR (rotation around the line of sight) is generally low. [4] The gain of the translational VOR has to be adjusted for distance, because of the geometry of motion parallax. When the head translates, the angular direction of near targets changes faster than the angular direction of far targets. [6]

If the gain of the VOR is wrong (different from 1)—for example, if eye muscles are weak, or if a person puts on a new pair of eyeglasses—then head movement results in image motion on the retina, resulting in blurred vision. Under such conditions, motor learning adjusts the gain of the VOR to produce more accurate eye motion. This is what is referred to as VOR adaptation.

Nearsighted people who habitually wear negative spectacles have lower VOR gain. Farsighted people or aphakes who habitually wear positive spectacle have higher VOR gain. People who habitually wear contact lens show no change in VOR gain. Monocular, disconjugate adaptation of the VOR is possible, for example, after extraocular muscle palsy. (p. 27 [17] )

The phase of the VOR can also adapt. [18]

Leak

The oculomotor integrator is a leaky integrator, with a characteristic leaking time of ~20 s. If the leaking time is too low, some form of adaptation occurs to "patch the leak" to raise the leaking time. It is hypothesized that the leaking integrator is constructed by a feedback circuit with a gain of slightly below 1, and adaptation occurs by adjusting the gain of the feedback circuit. The hypothesis is tested by using an specially patterned optokinetic drum that simulates the visual effect of having a very leaky oculomotor integrator. After 1 hour of viewing, the integrator becomes "anti-leaky", meaning that its value grows exponentially even in the absence of input. The eye motion becomes positive-feedback, meaning that if it is slightly to the left of a fixation target, it would drift even further to the left, and similarly for the right. It is also accompanied by nausea. [19] (p. 84 [13] )

Disruption by ethanol

Orientation of three semicircular canals in the head. Semicircular Canals.png
Orientation of three semicircular canals in the head.

Ethanol consumption can disrupt the VOR, reducing dynamic visual acuity. [20] In normal conditions, the cupula and the endolymph are equal in density (both are ). After ingesting ethanol, the ethanol diffuses into the cupula before it diffuses into the endolymph, because it is closer to blood capillaries. This makes the cupula temporarily lighter. In this state, if a person lies down with right cheek touching the ground, then the cupula in the left ear would float towards the left, creating an illusory sense of slow left-to-right head rotation. To compensate for this, the VOR moves the eyes towards the left slowly until it reaches the limit, and the eyes pull to the right rapidly (nystagmus). This is the positional alcohol nystagmus, phase I (PAN I). The unusual vestibular stimulation also caused motion sickness symptoms: illusions of bodily rotations, dizziness, and nausea. These symptoms subside in a few seconds after assuming an upright posture. [21]

After some time, the density of cupula and endolymph equalizes, removing the nystagmus effect. After ethanol is fully metabolized, the cupula returns to normal density first, creating nystagmus in the opposite direction (PAN II) during the hangover. [21]

As predicted, heavy water (1.1 density of water) consumption has the exact opposite nystagmus effect compared to ethanol consumption. Consuming a mixture of heavy water () and ethanol () largely cancels out the effect. [21] Macroglobulinaemia, or consuming glycerol (1.26 density of water), have similar effects as heavy water. [22] [23] [24]


Clinical significance

Testing

This reflex can be tested by the rapid head impulse test or Halmagyi–Curthoys test, in which the head is rapidly moved to the side with force, and is controlled if the eyes succeed to remain to look in the same direction. When the function of the right balance system is reduced, by a disease or by an accident, a quick head movement to the right cannot be sensed properly anymore. As a consequence, no compensatory eye movement is generated, and the patient cannot fixate a point in space during this rapid head movement.

The head impulse test can be done at the bed side and used as a screening tool for problems with a person's vestibular system. [25] It can also be diagnostically tested by doing a video-head impulse test (VHIT). In this diagnostic test, a person wears highly sensitive goggles that detect rapid changes in eye movement. This test can provide site-specific information on vestibular system and its function. [26]

Another way of testing the VOR response is a caloric reflex test, which is an attempt to induce nystagmus (compensatory eye movement in the absence of head motion) by pouring cold or warm water into the ear. Also available is bi-thermal air caloric irrigations, in which warm and cool air is administered into the ear. [27]

The vestibulo-ocular reflex can be tested by the aforementioned caloric reflex test; this plays an important part in confirming diagnosis of brainstem death. A code of practice must be followed in this process, namely that of the Academy of Medical Royal Colleges. [28]

Cervico-ocular reflex

Summary: Cervico-ocular reflex, also known by its acronym COR, involves the achievement of stabilization of a visual target, [29] and image on the retina, through adjustments of gaze impacted by neck and, or head movements or rotations. The process works in conjunction with the vestibulo-ocular reflex (VOR). [30] It is conspicuous in certain animals that cannot move their eyes much, such as owls. [31]

See also

Related Research Articles

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<span class="mw-page-title-main">Sense of balance</span> Physiological sense regarding posture

The sense of balance or equilibrioception is the perception of balance and spatial orientation. It helps prevent humans and nonhuman animals from falling over when standing or moving. Equilibrioception is the result of a number of sensory systems working together; the eyes, the inner ears, and the body's sense of where it is in space (proprioception) ideally need to be intact.

<span class="mw-page-title-main">Abducens nerve</span> Cranial nerve VI, for eye movements

The abducens nerve or abducent nerve, also known as the sixth cranial nerve, cranial nerve VI, or simply CN VI, is a cranial nerve in humans and various other animals that controls the movement of the lateral rectus muscle, one of the extraocular muscles responsible for outward gaze. It is a somatic efferent nerve.

<span class="mw-page-title-main">Vestibular system</span> Sensory system that facilitates body balance

The vestibular system, in vertebrates, is a sensory system that creates the sense of balance and spatial orientation for the purpose of coordinating movement with balance. Together with the cochlea, a part of the auditory system, it constitutes the labyrinth of the inner ear in most mammals.

<span class="mw-page-title-main">Medial longitudinal fasciculus</span> Nerve tracts in the brainstem

The medial longitudinal fasciculus (MLF) is an area of crossed over tracts, on each side of the brainstem. These bundles of axons are situated near the midline of the brainstem. They are made up of both ascending and descending fibers that arise from a number of sources and terminate in different areas, including the superior colliculus, the vestibular nuclei, and the cerebellum. It contains the interstitial nucleus of Cajal, responsible for oculomotor control, head posture, and vertical eye movement.

<span class="mw-page-title-main">Accommodation reflex</span> Reflex action of the human eye

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<span class="mw-page-title-main">Eye movement</span> Movement of the eyes

Eye movement includes the voluntary or involuntary movement of the eyes. Eye movements are used by a number of organisms to fixate, inspect and track visual objects of interests. A special type of eye movement, rapid eye movement, occurs during REM sleep.

<span class="mw-page-title-main">Extraocular muscles</span> Seven extrinsic muscles of the eye

The extraocular muscles, or extrinsic ocular muscles, are the seven extrinsic muscles of the eye in humans and other animals. Six of the extraocular muscles, the four recti muscles, and the superior and inferior oblique muscles, control movement of the eye. The other muscle, the levator palpebrae superioris, controls eyelid elevation. The actions of the six muscles responsible for eye movement depend on the position of the eye at the time of muscle contraction.

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<span class="mw-page-title-main">Abducens nucleus</span>

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<span class="mw-page-title-main">Electronystagmography</span>

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<span class="mw-page-title-main">Caloric reflex test</span> Test of the vestibulo-ocular reflex

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<span class="mw-page-title-main">Vestibulospinal tract</span> Neural tract in the central nervous system

The vestibulospinal tract is a neural tract in the central nervous system. Specifically, it is a component of the extrapyramidal system and is classified as a component of the medial pathway. Like other descending motor pathways, the vestibulospinal fibers of the tract relay information from nuclei to motor neurons. The vestibular nuclei receive information through the vestibulocochlear nerve about changes in the orientation of the head. The nuclei relay motor commands through the vestibulospinal tract. The function of these motor commands is to alter muscle tone, extend, and change the position of the limbs and head with the goal of supporting posture and maintaining balance of the body and head.

<span class="mw-page-title-main">Optokinetic response</span>

The optokinetic reflex (OKR), also referred to as the optokinetic response, or optokinetic nystagmus (OKN), is a compensatory reflex that supports visual image stabilization. The purpose of OKR is to prevent image blur on the retina that would otherwise occur when an animal moves its head or navigates through its environment. This is achieved by the reflexive movement of the eyes in the same direction as image motion, so as to minimize the relative motion of the visual scene on the eye. OKR is best evoked by slow, rotational motion, and operates in coordination with several complementary reflexes that also support image stabilization, including the vestibulo-ocular reflex (VOR).

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<span class="mw-page-title-main">Vestibulocerebellar syndrome</span> Medical condition

Vestibulocerebellar syndrome, also known as vestibulocerebellar ataxia, is a progressive neurological disorder that causes a variety of medical problems. Initially symptoms present as periodic attacks of abnormal eye movements but may intensify to longer-lasting motor incapacity. The disorder has been localized to the vestibulocerebellum, specifically the flocculonodular lobe. Symptoms of vestibulocerebellar syndrome may appear in early childhood but the full onset of neurological symptoms including nystagmus, ataxia, and tinnitus does not occur until early adulthood. To date, vestibulocerebellar syndrome has only been identified in three families but has affected multiple generations within them. Based on the familial pedigrees it has been characterized as an autosomal dominant disorder, although the exact genetic locus has not been identified. It has been found to be genetically distinct from other seemingly similar forms of neurological syndromes such as episodic ataxia types 1 and 2. Due to its rarity, however, little is known about specific details of the pathology or long-term treatment options. There is currently no cure for vestibulocerebellar syndrome, although some drug therapies have been effective in alleviating particular symptoms of the disorder.

The righting reflex, also known as the labyrinthine righting reflex, or the Cervico-collic reflex; is a reflex that corrects the orientation of the body when it is taken out of its normal upright position. It is initiated by the vestibular system, which detects that the body is not erect and causes the head to move back into position as the rest of the body follows. The perception of head movement involves the body sensing linear acceleration or the force of gravity through the otoliths, and angular acceleration through the semicircular canals. The reflex uses a combination of visual system inputs, vestibular inputs, and somatosensory inputs to make postural adjustments when the body becomes displaced from its normal vertical position. These inputs are used to create what is called an efference copy. This means that the brain makes comparisons in the cerebellum between expected posture and perceived posture, and corrects for the difference. The reflex takes 6 or 7 weeks to perfect, but can be affected by various types of balance disorders.

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