Given that foveation is so vital, the vestibulo-ocular reflex (VOR) is a fundamental and critically important reflex.  The VOR stabilizes gaze to reduce image motion on the retina during head movement,  for example, when turning one's head to the right, the eyes move to the left in order to compensate for the initial head rotation and to maintain the focus of the image on the fovea. The fovea is also small, meaning that the VOR needs to be very accurate, and also that the VOR needs to be adaptable.

Without an intact VOR, the visual world would slip on the retina with every head movement, resulting in blurred vision. Retinal photoreceptors are slow, cones taking 20 ms or more to respond fully to a change in intensity, so that if the eyes moved passively with the head, the image would be degraded by motion blur. We know from studies on human vision that blurring starts to occur when the image moves across the retina at speeds greater than about 1 degree per second, so compensatory eye movements are essential for clear vision, especially at higher spatial frequencies1.

The superb ability for a very fast (< 10 msec) gaze stabilization response comes about because of a fast transduction process and a direct three-neuron arc pathway. There are only three sets of neurons between the detection of head movement and an eye movement response, and consequently, the VOR is one of the fastest reflexes in the body. Head movements are extremely fast, and the VOR needs to be able to keep up with them. Fortunately, the VOR is effective up to a head rotation speed of 500/second: gaze stabilization in humans is essentially perfect for most behaviours in our environment2

Note that if the system relied on vision for stabilization, its adaptions would be too slow, since visual information normally takes about 100 msec from visual cortex to the ocular motoneurons that move the eyes. However, when the head moves, both vestibular and visual information are available. Vestibular input only takes about 7–15 msec to travel from the vestibular apparatus via the brainstem to the ocular motoneurons2. For example, if one oscillates a piece of paper back and forth horizontally at a rate of about two cycles per second, it becomes apparent that the text is blurred. However, if the page is held still and the head instead oscillates at that same rate, one can still easily read the text clearly3.

The VOR is a highly modifiable reflex: the brain continuously monitors its performance by evaluating the clarity of vision during head movements,with the VOR stabilizing gaze in an earth-fixed frame of reference. This occurs even though there is no direct link with vision: the VOR is purely a connection between vestibular signals and eye muscles, and the VOR acts independently of visually mediated eye movements.  The VOR is therefore an open-loop control system, since the receptors in the labyrinth (from which the input to the reflex is derived) receive no information about eye movements which are the output of the reflex4. Vision therefore can only recalibrate the VOR by short and long term adaptations (VOR adaptation below)4.


 

Video 1. Living without a vestibular apparatus/without a VOR: driving on a bumpy road

 

(vv)Bumpy Roads _ Mongolia.mp4(tt)



The VOR is generated exclusively from circuits which are found in the lower pons/medulla and the cerebellum.  Note that the VOR is intact even when the cerebellum is removed: the cerebellar function is to modulate the VOR in order to reduce image motion during head turning.
Three main structures participate in the generation of the VOR and help with maintaining its accuracy:

To produce the VOR, vestibular neurons must control each of the six pairs of eye muscles in unison through a specific set of connections to the oculomotor nuclei. 

Head movements are made up of both rotations and translations; together, the semicircular canals and the otoliths provide the inputs for the VOR, divided into two forms:
1.  The VOR associated with head rotations is referred to as the rotational VOR (rVOR) or angular VOR: when the head rotates to the right, the rVOR causes the eyes to rotate to the left, such that gaze remains stable in space.

2.  The VOR associated with translations of the head is referred to as the translational VOR (tVOR):  when the head translates to the right, the tVOR rotates the eyes to the left, to compensate for the relative motion of near targets on the retina.

The rVOR is sensed by the semicircular canals, which are sensitive to head rotation, and the canals provide the input for the compensatory slow phases of the rVOR in response to head rotation. The rVOR  must generate ocular rotation equal in magnitude to, but opposite in the direction of head rotation, irrespective of target distance. The slow-phase eye movement produced by the rVOR compensates for horizontal (yaw), vertical (pitch) or torsion (roll) head rotations.  

Figure 3. Horizontal (yaw), vertical (pitch) or torsion (roll) head rotations.

The rVOR is organized in a simple push–pull arrangement using signals from both labyrinths, and this push–pull organization supports the appropriate yoking of the eyes to move in the opposite direction to the head movement6.
   When the head rotates to the left side, the left horizontal semicircular canal afferents increase their firing rates, whereas the right afferents decrease their activity.
   -The excitation is transmitted by excitatory neuron projections via the left vestibular nucleus to the contralateral 6th nerve nucleus.
   -Precisely the converse applies to the right vestibular nucleus: inhibitory signals are transmitted to the ipsilateral 6th nerve nucleus.

Internuclear neurons in the abducens nuclei cross the midline and terminate in the contralateral medial rectus motor neurons. 
Thus, in response to a leftward head movement, motor neurons in the right 6th nerve and left 3rd fire at a higher frequency, whereas those in the left 6th and right 3rd fire at a lower frequency. As a result, the right lateral and left medial recti muscles contract, whereas the right medial and left lateral recti muscles relax, and the eyes rotate rightwards.

Figure 2. Three-neuron arc (for leftward head rotation) of the rotational VOR; image on the right shows additional inputs to oculomotor structures involved in left gaze, which are inhibited.

These three rather simple sensory-motor components constitute the main VOR path, the so-called three neuron arc4,5:
1. Vestibular apparatus to vestibular nucleus (red);  2. Vestibular nucleus to abducens nucleus (green); 3. Abducens nucleus to lateral rectus (blue)
Due to the bilateral symmetry of the premotor circuitry, the decrease in the firing rates of the primary afferents from the right canal during leftward head rotation results in a parallel reduction in the activation of the antagonist muscles (ie, the left lateral rectus and the right medial rectus), as shown in red below in the image on the right:

 

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 the midline when the head stops moving. This pathway is particularly important when the head is moving slowly because here position signals dominate over velocity signals. Circuits in the brainstem are responsible for this position signal and make up the neural integrator.

The normal rVOR is perfectly compensatory in direction and speed during yaw and pitch head rotations. 

For small head rotations, when the compensatory ocular deviation is small, the rVOR is manifested as a deviation in eye position, having a rate of change that should ideally match the velocity of head rotation.
For larger head rotations, the rVOR usually manifests as nystagmus, where slow eye deviations alternate with oppositely directed quick phases (reflexive saccades) that maintain eye position.

Similar to the interaction of saccades and pursuit, ocular nystagmus reflects two different control strategies, in which slow phases reduce the velocity error between eye motion and head motion and fast phases reduce the position error and keep the eyes centered in the orbit. Nystagmus is seen initially physiologically when the head undergoes continuous rotation, but note that this nystagmus dies out over time when the head experiences constant velocity rotation (see video below).  

Figure 7. Quick and slow phase of nystagmus


Video 2. VOR rotating in darkness (with infrared camera). Patient rotated in darkness with camera fixed to the head.

 

(vv)Vestibuloocular Reflex.mp4(tt)

 



VOR Gain
In clinical tests, the VOR is characterized by its gain, which is defined as the amount of eye rotation relative to head rotation. At usual head rotation frequencies (0.5 - 5 Hz), gain is perfect, or nearly so. In the light, gain is slightly better than is the case in darkness, as a result of visual enhancement, which is mediated by the optokinetic, smooth pursuit, or the fixation systems7. The compensatory function of the VOR extends nearly perfectly to high frequencies (up to 25–50 Hz) but at very low frequencies, gain declines. 

When head turns are consistently associated with image motion across the retina, the rVOR undergoes plastic gain changes in the direction which is most appropriate to improving the compensatory ability of the vestibulo-ocular reflex. For example, when the world is viewed through spectacles that magnify or miniaturize the visual scene, rVOR gain increases or decreases accordingly. The reflex behavior can adapt over several minutes, hours, and days. During short-term adaptation, the rVOR gain can be adjusted by exposing the subject to a motion stimulus coupled with an abnormal visual stimulus.  For example, head rotation paired with the rotation of an optokinetic visual stimulus at the same speed but in the opposite direction results in an increase of the rVOR gain. Similarly, rotating the subject and visual surround in tandem can be used to train the rVOR gain toward zero. Modification of the VOR takes place in the cerebellum, with input from the inferior olive.  Note that in patients who habitually wear corrective spectacles, their VOR gains will be adaptively adjusted to their habitual viewing condition, so that during head rotation the VOR can appear hyperactive if the spectacles correct for farsightedness (hyperopia), or hypoactive if the spectacles correct for nearsightedness (myopia)8.

rVOR and velocity storage
The angular/rotational (rVOR) is generally tested with passive whole-body rotation in the dark, while recording conjugate horizontal eye movements.  During the period of acceleration at the beginning of the rotation, the slow phases of eye movement act to stabilize gaze in space by moving the eyes in the opposite direction to the head, whereas the fast phases redirect the gaze with fast reorienting eye movements, typically in the direction of head rotation. These slow and fast intervals constitute VOR nystagmus.  When a subject is submitted to angular rotation with eyes closed, the canal output will accurately signal the direction of rotation when first beginning to move; however, after a period of rotation at constant velocity, the cupula of semicircular canals habituate after 5 seconds9.  However, the associated nystagmus continues for many tens of seconds, as illustrated in Figure 8 below.  This discrepancy, that is, that the rVOR response to a step in head velocity decays slower than would be expected given the properties of the semicircular canals, represents a prolongation or perseveration of the raw vestibular signal indicating head motion, and is likely to reflect a central processing of afferent information referred to as the velocity storage mechanism. 

With ongoing rotation, the subject will report that rotation has stopped, as shown during rotation in Video 2 above. When the sensation of rotation fades at constant velocity, the nystagmus also disappears, as seen in the video. This is predicted from the adaptation of receptors in the semicircular canals at constant velocity, since the canals do not signal a constant velocity stimulus10.  

Sudden cessation of rotation is encoded by the semicircular canals as a step in the opposite direction, eliciting a response typically referred to as postrotatory nystagmus (Video 2), which will be in the direction opposite to the direction of the previous rotation. There will also be a sensation of rotation in the direction opposite to the initial rotation,  and an effect on past-pointing. If a person is asked to point at a target immediately on being stopped after a period of constant velocity rotation, they will consistently point in the direction of the previous rotation. Thus, if the previous rotation was clockwise, they would consistently point to the right of the target.

The sensation of rotation in the opposite direction to the initial rotation will fade with time. This is anticipated given with the discharge properties of receptors in the semicircular canals. When a rotation stops, the discharge frequency of the canal receptors (on the side toward which the head originally rotated) falls below resting levels and below the level of the contralateral canal, just as it would if there were actually a rotation in the opposite direction. Although rotation has ceased, the central nervous system cannot distinguish this signal from the signal that would occur for an opposite rotation and, therefore, it is interpreted as an opposite rotation. This sensation also fades with time because of receptor adaptation8.

 

Figure 8. Nystagmus in response to a step of velocity (platform rotation) in darkness. 
The top traces illustrate horizontal eye position, whereas the bottom traces show slow-phase eye velocity (the large positive and negative spikes reflect the occurrence of fast phases).
The solid red line in the lower trace illustrates the semicircular canal afferent time course, which is much shorter than that of the actual rVOR. 

From: Angelaki, D. E. (2009). Vestibulo-Ocular Reflex. In Encyclopedia of Neuroscience (pp. 139-146). Elsevier Ltd. https://doi.org/10.1016/B978-008045046-9.01107-4

 

 

 

 

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