Eye Movements

Eye Movement Axes

All movements of each eye are produced by (3) pairs of extraocular muscles, which operate antagonistically.  Referring to the figure below, their principal actions are:

• Medial Rectus (adduction) versus Lateral Rectus (abduction)
• Superior Rectus (elevation) versus Inferior Rectus (depression)
• Superior Oblique (depression) versus Inferior Oblique (elevation)

The medial and lateral recti perform abduction/adduction nearly exclusively. The other pairs effect elevation/depression as primary actions, but secondarily exert various amounts and types of cyclotorsion, as shown diagramatically below.

Innervation of the Extraocular Muscles

• Medial, Inferior & Superior Rectus; Inferior Oblique:   Oculomotor nerve (III)
• Superior Oblique: Trochlear nerve (IV)  N.B.:  tendon of superior oblique passes through the trochlea
• Lateral Rectus: Abducens nerve (VI)  N.B.:  action of lateral rectus is abduction (abducens)

A Brief Taxonomy of Eye Movements

Much of the time the two eyes move as a unit, through equal angles in the same direction.  Such eye movements constitute conjugate, or version eye displacements.  Other eye movements involve coordinated, but unequal, degrees of movement of the eyes, and are variously referred to as non-conjugate, vergence, or disjunctive eye movements.

Vergence movements result in pupils which move together or apart:

• Interpupillary distance decreases:  congergence
• Interpupillary distance increases:  divergence

Holding:  For stationary retinal images the quality of vision depends almost entirely upon spatial factors, such as the size and shape of the pupil, the quality of the optics, the spectral composition of the stimulus, and the spatial positions and sizes of the retinal sampling elements.  Once image motion across the retina is allowed, however, temporal factors become paramount.  The electrical response of photoreceptors lasts for a finite period of time, on the order of tens of milliseconds:  light flickering faster than approximately 75 Hz appears steady.  Image displacement blurs the neural image in time: the photoreceptor is unable to conclude its response to stimulus A before it is forced to produce a second response to stimulus B.  The result is a response in which information concerning the two stimuli is "blurred" together.  This is called motion blur.  An example of motion blur is shown in the figures below. 

It is remarkable that image motion as slow even as 1^o/sec (note: at this rate a target would take nearly 3 minutes to traverse the entire visual field) can, in conjunction with a stationary eye, produce a deterioration of spatial resolution (acuity) equivalent to 3 diopters of optical defocus.  The first type of eye movements believed to have evolved are therefore those designed, seemingly paradoxically, not to move the eye at all, but to hold it still with respect to the external environment.  The animal must somehow sense the movement of the eye with respect to the environment, and move the eyes in an equal and opposite direction to compensate.   Since eyes can rotate, but cannot translate, "holding" eye movements are effective in counteracting rotations, but not linear translations, of the head/body, as shown in the figure below.

In animals with laterally-located eyes, like the pigeon, the solution is to stabilize the entire head, including the eyes. The peculiar bobbing gait of these birds appears to be a specialization to accomplish this feat (see figure below). The body walks on, while the head (and eyes) are temporarily left behind, and are jerked forward rapidly. The benefit from this strategy is that the head (and eyes) are maximally immobile during locomotion.

Catching:  There is great variety in the visual panoramas afforded to different species.  As shown in the figure below, the horse can see nearly completely in a 360^o arc around his head.   It might seem unnecessary for the horse to possess any other than "holding" eye movements. This would be inappropriate, however, for the vast majority of creatures whose monocular visual fields do not adjoin, thus leaving conspicuous gaps in their visual worlds.  A second, more fundamental problem, even for the horse, is that most eyes cannot see equally well at all locations in the visual field.  High-quality vision is limited to a rather small region of the retina, called the area centralis (the horse's equivalent of the human fovea); visual acuity falls off rapidly with increasing distance from this area.  In humans, acuity at 1^o eccentricity is roughly three times lower than that for the fovea.  The fovea is tiny: only 1/10,000^th of the full visual field is sampled with foveal fidelity.  That we are not, under most normal circumstances, greatly aware of our "blindness" in this regard is a tribute to the importance and efficiency of eye movements, which cast this narrow tunnel of high-quality vision from location to location at whim.  These eye movements, produced reflexively by visual or auditory alerting stimuli, or purely voluntarily, are the "catching" movements of the eye, whereby new objects of interest are seized by the fovea, and thereafter held there by the previously discussed "holding" movements.  Another glance at the Taxonomic table above reveals that, since vision is poor during slippage of the image across the photoreceptor array, these "catching" movements are fast.  Some are reflexive, some are voluntarily produced; yet unlike "holding" movements, all are of the conjugate (version) variety.

Sustaining:  Compared with either the "holding" or "catching" movements discussed above, the defining characteristic of "sustaining" eye movements is their amplitude:  they are extremely small.  As illustrated by inspecting the figure below, normal observers generally make, even while fixating a stationary object, small eye movements of which they are unaware, which are a few minutes of arc in extent.  Foveal cones are spaced approximately 0.5 minutes apart, so that these eye movements impose a temporal pattern on the photoreceptor's output.  Indeed, it turns out that vision is entirely dependent upon the small-scale irregular motion of the retinal image which is produced by these movements.  Hence, they actually "sustain" visual perception. 

Vestibular Nystagmus Eye Movements

Static:  Static vestibular reflexes consist of torsional (rotational) movements to compensate for head/body tilt about the anterior-posterior axis.  The counterrolling movements are small, maximally about 7^o, and as can be seen, are hardly compensatory in humans and other animals with front-facing eyes.  The static vestibular reflex is considerably stronger in lateral-eyed species, such as the rabbit.  If the head is tilted, the eyes tend to move in such a manner as to preserve their former orientation with respect to the environment, both for static tilt about the anterior-posterior and medial-lateral axes.

Dynamic:  In humans, movements of the eyes occur much more readily in response to rotations of the head than to linear accelerations.  The semicircular canals signal angular velocity of the head, and the dynamic vestibulo-ocular reflex strives to match the head's instantaneous velocity with a compensatory eye movement, so as to keep the retinal image stationary.  Since the eye can rotate only through a finite extent within the orbit the eye's smooth counterrotation (slow phase) is punctuated, during prolonged rotations of the head, at intervals by fast flicks (fast phase) in the same direction as the rotation.  Thus the eye continues to match the velocity of eye movement, while having reset position relative to the image (see figure below). 

The relationship between vestibular nystagmus (eye movements) and optokinetic nystagnus (described below) can be witnessed for yourself:  hold your forefinger at arm's length from your eyes and rapidly move it from side-to-side through several inches.  Allow your eyes move to track the finger's movement.  Now, compare the quality of that image with what you see when, instead of moving your finger, you hold your finger stationary and rotate your head with the same frequency through the same angle:  the difference is striking.  Vestibulo-ocular eye movements are a reflex velocity-matching mechanism for middle to high temporal frequencies.  Second, the low-frequency falloff in vestibulo-ocular reflex eye movements is adaptive in the context of normal (not laboratory-induced sinusoidal rotations) head movements, which are usually made for the purpose of shifting gaze.  The change in fixation implies that for at least some time the eye must move with respect to the environment.  The visual system is best able to supply information if the time that the image moves relative to the retina is minimized.  That is best accomplished by "holding" the eyes steady while the (high-inertia) head turns through some portion of its arc, then superimposing a fast position change using the (low-inertia) eyes themselves, then "holding" the eyes steady on the new target as the head completes its turn (see figure below).

Tracking Eye Movements: Optokinetic Nystagmus and Smooth Pursuit

Tracking eye movements are those which are made under visual guidance for the purpose of holding an object of regard and/or following it when it moves.  They are rather less reflexive than vestibulo-ocular movements, for they are capable of being modified by acts of will.  However, few subjects can generate them in the absence of an appropriate stimulus, and so they are rather less voluntary than saccades or vergence eye movements.

Optokinetic Nystagmus (OKN):  Easiest to demonstrate by viewing a rotating, striped drum that fills a substantial portion of the visual field.  For moderate rotational velocities, the subject's eyes will follow a particular stripe as it moves (slow phase).  As the gaze is carried further from the primary position, a quick anticompensatory flick is made to bring the point of fixation back onto some new feature of the drum (fast phase).

OKN depends upon subject's attitude, and instructions: "looking" and "gazing" at a rotating striped drum produce different kinds of OKN.  "Looking" instructions produce less frequent movements of larger amplitude; "gazing" instructions produce more frequent, lower amplitude eye movements (see figure below).  The slow phase of OKN can follow stimulus velocities up to approximately 100^o/sec, beyond which the system breaks down, and inappropriate eye movements, or none at all, are made to moving targets. 

Smooth Pursuit:  Voluntary smooth eye movements which track the location of objects of interest.  Although voluntary, smooth pursuit requires a stimulus to track; they cannot be executed in the absence of some environmental stimulus (try it with a partner if you don't believe me).

Saccadic Eye Movements

Saccades are the voluntary movements of the eyes which serve to bring a new part of the visual field into the foveal region.  While essentially voluntary, they share many characteristics with the quick phases of vestibular and optokinetic nystagmus and microsaccades. Saccades are stereotyped movements.  They are so fast that there is little time for visual guidance: saccadic eye movements are therefore said to be ballistic.   The figure below illustrates a number of saccades of different amplitudes.  A notable feature of such records is the velocities attained by the eye during large amplitude saccades:  in excess of 400^o/sec.

To execute a saccade, the visual system must convert retinal distance (for example, between current position, and a desired new position) into signals controlling the extraocular muscles.   The complexity of these calculations is reflected in the rather long latencies associated with the initiation of saccadic eye movements.  A typical stimulus arrangement is for the subject to fixate a small light.  This light is extinguished while another light, at a variable distance from the first, is turned on:  the saccade the subject makes to the new light typically does not begin before 200 ms. 

During saccades, visual sensitivity is suppressed (see figure below), though it is easily demonstrated that it is not completely eliminated.  In general, however, one cannot "see" ones own saccadic eye movements in a mirror. 

Saccadic eye movements can reveal global aspects of perception, such as the scan patterns and fixation locations of subjects inspecting human faces (see figure below).

Vergence Eye Movements

Vergence eye movements are principally restricted to primates, although cats have been shown to produce convergence eye movements upon occasion.  Vergence eye movements thus are thought to be those most recently evolved, and disorders of vergence systems are among the most common clinical ophthalmological symptoms (e.g., strabismus, amblyopia consequent to strabismus, diplopia).  These are the first type eye movements to suffer from fatigue and drugs (principally alcohol).  There is enormous individual variation in the degree of voluntariness of vergence movements.  There are two types of vergence.

Disparity vergence:  Binocular disparity alone is a sufficient stimulus for vergence eye movements.  A prism which changes the retinal position of a fixation point in the left eye relative to the right (i.e., introduces disparity in the two retinal images) will induce a vergence eye movement.

Accommodative vergence:  The deformation of the eye's lens (accommodation) is itself sufficient to elicit vergence eye movements.  If one eye is covered while the other fixates a target, an a negative lens is placed before the seeing eye (which forces accommodation), the companion eye converges. 

Miniature Eye Movements

In humans there are three different types of miniature eye movements:  tremor, drift, and microsaccades.  The effect of these miniature movements is to move the retinal image about, over the fovea, in a pattern considerably larger than a foveal cone photoreceptor (see figure below).

Tremor:  The amplitude of tremor is smallest, about 5-10 seconds of arc. Binocular measures of tremor show that it is uncorrelated between the two eyes, suggesting a peripheral origin.

Drift:  Drift movements are relatively large and slow, possessing velocities of 1 min/sec, and median amplitudes of around 2-5 minutes.  Each drift movement is terminated by a microsaccade, and drift movements appear to be uncorrelated between the eyes.

Microsaccades:  Microsaccades serve the same function as their larger cousins, ordinary gross saccades, which is to bring a visual target into register with the fovea.   They probably share the same control mechanism as saccades.  Microsaccades are primarily corrective in nature.

The Stability of Perception with Eye Movements

Inflow Theory:  Extraocular muscles have length receptors (muscle spindles).  These provide continuous information to the perceptual system regarding the position and movement of the eyes.  This can be shown to be false, however, since mechanically moving your eyeball produces large perceptual instability, whereas it should not alter outflow from extraocular muscle length receptors.

Outflow (Efference Copy) Theory:  The brain nuclei which control the extraocular muscles (and hence eye movements) send a "carbon copy" to the perceptual centers of the brain.

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Copyright © 1997 [Mark E. McCourt]. All rights reserved.
Revised: September 22, 2001.