Video 1. Introduction:Oculomotor and Vestibular Systems. Professor M Strupp, University of Munich

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Video 2. Performing a Standard Eye Examination:                                 This video covers the following topics:

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Symptoms

Patients with ocular motor disturbances usually report the following symptoms in isolation or in combination1:

 


 

Video 3. Normal eye movement evaluation, including checking smooth pursuit and saccades, both vertical and horizontal

 

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NORMAL EYE MOVEMENTS

Primary eye movements can be divided into those that produce gaze shifts which bring an object of interest onto the fovea, and those that promote gaze stabilisation.  The strategy can be summed as: saccade and fixate.

Distinct oculomotor mechanisms provide for the achievement of foveation across a variety of visual circumstances.  The fovea is the portion of the retina with the highest visual acuity, hence maintaining image focus upon this structure promotes image processing and visual fixation.  The various types of eye movements serve to keep the visual target on the fovea stable and thus avoid illusory movements (oscillopsia) and blurred vision under a variety of visual conditions.
The control circuits associated with gaze stabilizing and gaze shifting movements all must activate the same set of pculomotor neurons, and all of these circuits must produce signals which regulate both the velocity and position of the eyes in a manner appropriate for that type of eye movement1.

The six physiological forms of eye movement are2:

INFORMATION GATHERING/ Gaze SHIFTING: these eye movements shift the fovea to align with objects of interest in the visual world

1. Saccades are fast eye movements that mediate rapid shifts of gaze to a new fixation target.  The saccadic system, including the frontal eye field and the superior colliculus, needs to provide the oculomotor neurons with the amplitude and direction of the required change in the line of sight1.
Quick phases of nystagmus are the evolutionary forerunners of saccades, and provide a resetting mechanism for the eyes during sustained vestibular or optokinetic stimulation (discussed further below)3.

2. Smooth pursuit eye movements allow foveation while tracking a slowly moving target.  Signals carrying information about target motion are extracted by motion processing areas in the visual cortex and then passed to the dorsolateral pontine nucleus of the brainstem, which encode the direction and velocity of pursuit eye movements, in combination with cerebellar input1.  The smooth eye movements which characterize pursuit will match the velocity of a moving visual stimulus and require use of prediction and adjustment processes to stabilize the visual target. 
Pursuit responds slowly to unexpected changes, which is why the faster acting vestibulo-ocular reflex (VOR) is necessary in order to provide stabilization of the eyes with head movement4.

3. Vergence movements represent an evolutionary adaptation for frontal vision with binocularity.  When a target moves towards or away from the viewer, vergence results in eye movements in opposite directions for simultaneous foveation. For all other movements the two eyes receive identical movement commands (Hering's law of equal innervation).

4. Gaze holding is the ability to keep the eyes in an eccentric position.

REFLEXIVE/ Gaze STABILISING: gaze is held almost stationary by eye movements which rotate the line-of-sight to compensate for head and body movements, stabilising the visual world on the retina
Blurring starts to occur when an image moves across the retina at speeds greater than about 1 degree per second, so compensatory eye movements are essential for clear vision.
Two distinct mechanisms evolved to stabilize images on the retina during head movement, driven by the vestibular and visual systems:
-Vestibular: the Vestibulo-ocular reflex (VOR)
-Visual: visually mediated reflexes (optokinetic and smooth- pursuit tracking), which depend on the ability of the brain to determine the speed of image drift on the retina. 

5. Visual fixation Fixation is critical both at rest, when the head is stationary, and during head movements, when visual fixation upon still objects is achieved through the recruitment of vestibular mechanisms that move the eyes in an equal and opposite direction to the head movement in order to maintain foveation.  The goal of both pursuit and fixation is to retain a visual image on the fovea and hence these are often considered to be supported by the same system.

Fixation at rest: The degradation of image quality that would result if the eye was completely still is countered by microsaccadic reɹxation movements. These are continuous, very small amplitude square waves.( The term square waves derives from the appearance of eye movement tracings, in which eye movements of equal amplitude and speed to the left and right have a brief intersaccadic interval that produces tracings in the shape of square waves). The to-and-fro movements are small enough that the image is maintained within the field of the fovea but large enough to provide a constantly changing image to photoreceptors, thereby enhancing perceptual quality. As is true for most saccadic movements, there is a slight pause (180–200 milliseconds) between movements, known as an intersaccadic interval. The anatomic pathways that control ocular fixation include the dorsolateral prefrontal cortex, the supplementary eye ɹeld, the parietal eye field, regions V5 and V5a, the basal ganglia, and the superior colliculi.

Fixation during head movements: This is achieved through the vestibulo-ocular reflex (VOR); brief head movements generate a vestibular response triggering compensatory eye movements, which keep the image of the visual surroundings stable on the retina during head movement.Sustained head rotation stimulates the VOR to generate slow-phase ocular movements that are opposite to the direction of head rotation, however this attenuates after about 30 seconds:
6. With sustained head rotation or environmental movement with the head steady, the resultant wide-field image velocity signals are detected by retinal ganglion cells and are fed back to the eye muscles in order to null out any residual slip of the image across the retina.  This results in optokinetic nystagmus, which combines slow pursuit eye movements punctuated by saccadic refixations, to bring about the re-establishment of image focus. This is essentially a reflex which is triggered by moving visual targets; in nature, almost the only situation in which a large visual scene moves as a single whole is when the animal itself is moving and its VOR is not compensating perfectly. The optokinetic reflex response acts as a visual backup for the angular VOR in order to generate compensatory eye movements4.  The smooth-pursuit system and the optokinetic system are similar but distinct. The smooth-pursuit system is voluntarily activated; its function is to place the image of a small moving object onto the fovea. In contrast, the optokinetic system is involuntary and is reflexively activated when a large visual image sweeps across a large area of retina.

At low speeds of head rotation, the optokinetic system obtains information about the rate at which the whole visual field slides across the retina, information which accurately encodes the velocity of head rotation. As the velocity of head rotation increases, head velocity is underestimated. Thus, although either the vestibulo-ocular or optokinetic system working alone are unable to fully compensate for all movements of the head and body, working together these two systems can provide an accurate estimate of head velocity that can be used by the oculomotor control circuitry to counterrotate the eyes in the head across a broad range of head speeds1.

The interrelationship of vestibular slow phases, saccades and nystagmus

Most head movements are brief, requiring only small compensatory eye movements.  However, any sustained head rotation would cause the eyes to lodge at the corners of the orbits in extreme contraversive deviation, where they no longer could make appropriate movements.An example would be as a swimming fish makes a turn, the eyes would become trapped at the limit of their range in the orbit, and a mechanism is needed to return them to a central point in the orbit. The gaze stabilization systems respond to this challenge by very quickly moving the eyes in the opposite direction; this gives rise to a repetitive pattern of quick reset movements and slow stabilization phases usually called nystagmus. These resetting movements are found in very primitive organisms, and are the basis for the evolutionary development of the saccadic and pursuit systems. In humans, extreme deviation of the eyes  is not observed, except in certain pathologic states such as congenital ocular motor apraxia, again due to corrective quick saccades. These rapid eye movements, the evolutionary forerunners of voluntary saccades, have been likened to a resetting mechanism for the eye. In fact, they do more than this since, during head rotation, quick phases move the eyes in the orbit in the same anticompensatory direction as that of head rotation and thus enable perusal of the oncoming visual scene. Quick phases of nystagmus are rapid, with maximal velocities as high as 500 /sec, repositioning the eye in the shortest time possible. The anatomic substrate of these rapid eye movements is in the paramedian reticular formation of the pons and mesencephalon, the same as that for saccades.

 

 

EXAMINATION OF EYE MOVEMENTS 

 

Ocular motility examination should include bedside evaluation and laboratory recording of2:

1. Ocular Misalignment confirmed with a cover test in primary gaze, during both near and distant fixation. 

2. Range of eye motion and gaze holding function : typically 10–20for vertical gaze (Note that a moderate restriction of upward gaze is common in elderly individuals); it is frequently useful to provide a target for the patient to fixate on.

3. Involuntary eye movements: nystagmus or inappropriate saccades 

4. Saccades both horizontal and vertical, should be assessed for latency, velocity, accuracy, and conjugacy.

5. Smooth Pursuit (SP) may be evaluated by asking the patient to track a small target moving slowly in the horizontal or vertical direction with the head still.  If the pursuit movement does not match the target velocity, corrective catch-up or back-up saccades would occur. Since many neural structures are involved in the generation of SP, and many factors affect it, impaired pursuit generally does not have a localizing value.

6. Vestibulo-ocular reflex (VOR):  may be evaluated bedside using head impulse tests (HIT), visual enhancement of the VOR, and visual cancellation of the VOR.

7. Optokinetic Nystagmus (OKN):  induction of OKN may be useful in some patients who have difficulty initiating voluntary saccades.

8. Vergence Eye Movements:  tested by having the patients look back and forth between a distant and a near target.

9. Tests of peripheral vestibular function: 

10. Inspection of head/body posture

 

 

 

References

  1. Glimcher, P. W. (2001). Eye Movement, Control of (Oculomotor Control). In International Encyclopedia of the Social & Behavioral Sciences (pp. 5205–5208). Elsevier. https://doi.org/10.1016/b0-08-043076-7/03542-7
  2. Strupp M, Kremmyda O, Adamczyk C, et al. Central ocular motor disorders, including gaze palsy and nystagmus. J Neurol. 2014;261 Suppl 2:S542-58
  3. Chen AL, Riley DE, King SA, et al. The disturbance of gaze in progressive supranuclear palsy: implications for pathogenesis. Front Neurol. 2010;1:147. Published 2010 Dec 3. doi:10.3389/fneur.2010.00147
  4. Wong, A. M. (2008). Eye movement disorders. Oxford: Oxford University Press.
  5. Frohman EM, Solomon D, Zee DS. Vestibular Dysfunction and Nystagmus in Multiple Sclerosis. Int MSJ 1995 3(3):87-99.