Monocular eye movements are called ductions. Binocular eye movements in the same direction are called versions or gaze movements. Normal eyes maintain the same relative alignment in various positions of gaze: comitance. When the eyes move unequally because of muscle weakness or restrictions, incomitance results. Eye movements in contrary directions are called vergences. A tropia is a manifest deviation of the visual axes. A tendency to deviation of the visual axes held in check by the fusion mechanism is a phoria. See Figure 2 for these and additional terms.

In agonist-antagonist relationships, the muscles pull in opposite directions, for instance, medial rectus versus lateral rectus. To a substantial degree, vestibular gaze and control of oculomotor function are arranged around these muscles as pairs that control rotation in horizontal, vertical, and torsional directions.

Synergists are agonist muscles pulling in the same direction. Muscles often are synergists for one direction, such as the superior rectus and inferior oblique for supraduction, while at the same time acting as antagonists for their horizontal and torsional vectors.

The eye is a sphere rotating around three orbital axes: vertical rotation around the horizontal (x) axis, cyclorotation around the anterior-posterior (AP) or y, axis, and horizontal rotation around the vertical (z) axis. The eye has a similar set of axes, which rotate with the eye (Fig. 3). The study by Howard and Templeton provides further description of axis systems.¹ The eye and its center of rotation can also be translated by small amounts in other directions: medial to lateral, up to down, and inward to outward.

The global axes can be compared with the orbital axes in various gaze positions by marking a cross on the front of the cornea to tell how the eye is oriented (Fig. 4).

Donders found that for any gaze position, there is a predictable amount of torsion, and that this is independent of how the eye travels to that gaze position.² The amount of torsion increases with increased movement of gaze from the primary position. For an oblique position of 10 degrees vertical and 10 degrees horizontal, there is 1 degree of torsion, for 20 degrees vertical and horizontal, 3 degrees of torsion, for 30 degrees, 8 degrees; for 40 degrees, 15. Listing proposed (and Von Helmholtz formulated and verified) a clever way to consider the torsions that Donders described.³ The image is that of a vertical plane cutting the eye into front and back halves going right through the center of rotation at the equator (see Fig. 3). Next imagine a rod attached to the center of this equatorial plane (called Listing’s plane) so that it can spin around like a hand on a clock. This rod is the axis of rotation for the eye. For an eye position straight upward, this axis is placed horizontally from the 3- to the 9-o’clock positions. For a rotation obliquely, this axis is placed at an oblique axis, say 10:30 to 4:30 positions. The advantage is that only two data are needed to describe the eye position instead of three: one, the orientation of the rotation axis, and two, how far the eye rotated in that direction. The torsion that is required to be added in a triaxial system turns out to be automatically corrected using Listing’s system. Listing’s law has been tested under a variety of circumstances and shown to be correct for vertical and horizontal movements in the frontal plane with the head erect. Listing’s law does cease to be demonstrable in abnormal innervations causing restrictions to movement and also for normal convergence positions; there is about 1 degree of excyclophoria for each 4 degrees of convergence.

The triaxial system is no problem for modern computers; all serious modeling of eye movements is currently performed using the triaxial scheme. Clinicians think in terms of horizontal, vertical, and cyclotorsional effects of the muscles in a system of three axes. Moreover, the vestibular system driving many eye movements is also organized into vertical, horizontal, and torsional subsystems.

But Listing’s concept is more than a clever way to think about normal eye rotations and turns out to have some basis in anatomy. Nakayama conceived of Listing’s plane as an elastic membrane with the eye suspended in it (Fig. 5).⁴ If the eye is pulled in any direction, it obeys Listing’s law. Anatomically, there is a matrix of fatty fibromuscular tissue suspending the eye and the anterior third of the muscles in the orbit and attached to the orbit walls. This is very like the eye suspended in a foam rubber layer several millimeters in thickness that acts like the membrane of Nakayama. The eye is thus somewhat mechanically constrained. During normal large saccadic movements accompanied by strong head rotation, transient torsional deviations up to 25 degrees have been found,⁵ showing that this mechanical restraint is only partial. In addition, the eye muscles are programmed to have a certain particular set of pulls for each gaze position. Large deviations from Listing’s law occur with non-paralytic brainstem lesions altering the innervation program. So Donders’ law is also confirmed by eye muscle innervations.

The eye positions of orthophoric, normal individuals under deep anesthesia with curare paralysis are probably the closest approximation to a true position of rest. De Groot and coworkers found an exotropia of 2.25 degrees for each eye in young adults, which increased with age.⁶ This is in accord with the estimate of most clinicians. In newborns whose eyes are straight when awake, the visual axes are commonly divergent up to 35 degrees in deep sleep, which become progressively straighter within only a few weeks.⁷ The position of the eyes under anesthesia in strabismus cases helps to show anatomic vertical, horizontal, or torsional factors underlying the alignment disorder. Differences in waking eye position from those while asleep indicate innervational factors. In general, esotropic cases are less esotropic, showing that innervational factors are dominant, and exotropia cases are about the same, showing that anatomic position is the major factor. Difference between the position of the two eyes shows the effect of unequal anatomic factors; rotation of the fundus structures indicate torsional factors.

Cross-sectional areas of the extraocular muscles in square millimeters from Volkmann and Nakagawa’s measurements appear in Table 1.^8,9

The extraocular muscles are from 32 to 40 mm in length (see Table 1). Inasmuch as each 1.0 mm on the surface of the eye corresponds to 4.5 to 5 degrees of rotation, the normal amplitude of eye rotation of 45 to 50 degrees each way from the primary position requires 10 mm change of length of the muscle in each direction. This represents a contraction of 25% to 30% and an extension of 25% to 30% from the normal resting length of the muscle, nearly optimal excursions for linear performance. Sacrifice of muscle length during eye muscle operations can reduce the amplitude of eye rotation. Muscle length is not proportional to eye size, so that large myopic eyes rotate less and small microphthalmic eyes rotate farther than normal.

Muscle attachments and directions of pull (Fig. 6) are defined as follows:

Muscle plane. The origin, functional insertion, and center of rotation establish an imaginary plane through which the muscle pulls to move the globe (see Fig. 6).

Muscle axis of rotation is perpendicular to the muscle plane. The individual muscle pulling on the eye rotates the globe around this axis through the center of rotation. For the horizontal recti, it coincides with the vertical axis of the globe when the eye is in the primary position. For other muscles, it is oriented at various angles established by their coordinates of origin and insertion (see Table 1, Fig. 7).

The forces of muscle contraction and relaxation pull on the eye according to the muscle plane established by the origin, functional insertion, and center of rotation. Clinical strabismus patterns due to anatomic variation of this anatomy, which can be shown on CT or MRI scans, are not rare. For more detailed measurements of arc of contact, exact point of origin, and so forth, see Tables 1 and 2.

One scheme is to assign rotation around each of the axes as a major or minor function of muscles:

Another helpful concept of how each muscle acts from the primary position is to show what would happen if you plotted the direction of your fovea on a wall while each muscle individually pulled the eye in its muscle plane (Fig. 8).

When the eye moves to new positions, the orbit axes stay fixed and do not move. The eye carries its axes and the muscle insertions along to the new position with it. The action of each muscle on the eye changes because the eye axes are now in different positions.

Figure 9 shows the effect that each muscle pair would have if it were the only one pulling. This graph is like that in Figure 8 but involves other gaze positions in addition to the primary position. The horizontal recti are considered as starting from various positions of vertical gaze. There is a minimal change of effect; they remain as horizontal movers. The effect of the oblique and rectus muscles is considered starting from various positions in the horizontal plane. The vertical rectus muscles have a nearly pure vertical effect when the eye is in abduction, but increasing torsional and horizontal effect as the eye moves into adduction. For the obliques, there is almost purely vertical action in extreme adduction and almost purely torsional effect in extreme abduction. The superior and inferior rectus muscles are quite symmetric, whereas the superior and inferior oblique are not quite symmetric, as a result of the long arc of contact of the inferior oblique.

The anatomic muscle insertions on the globe are carried along by rotation of the eye to new positions. What about the functional origins and insertions: are they moved to the same degree as the anatomic insertions? For example, in the classic geometric analyses in Figures 8 and 9, the muscles are supposed to behave as if they were a single string connecting the origin and center of insertion and as if the muscles could slip sideways over the globe.^15,16 Four factors alter this: (1) first is the width and geometry of the insertion (Fig. 10). The extraocular muscle insertions are all convex at their insertional end; (2) they are all approximately 9 to 10 mm wide; (3) the muscle almost bisects the center of rotation of the globe on its way to the insertion; and (4) these insertions are all approximately 5 to 6 mm in front of the center of rotation (inferior oblique excepted).

The practical effect of this on, for instance, the medial rectus, is to slack off the upper fibers during upward gaze and transfer the effective tension generated by the muscle from the center of the muscle to the lower fibers. Similarly, in downward gaze, muscle tension is transferred to the upper fibers, and the lower border of the muscle is slack (Fig. 11A). Were this not true, the situation would be as shown in Figure 11B: the medial rectus would become an elevator in upward gaze and a depressor in downward gaze. Similar figures show the stabilizing effect of a wide insertion on the line of pull of oblique and vertical rectus muscles. Von Helmholtz first described this attribute of the width of the extraocular muscles tending to hold the direction of pull of the muscle stable in the orbit, regardless of eye position.

The trochlea (pulley) of the superior oblique constrains the tendon and changes its direction of pull so that a new origin is created. Less dramatic accumulations of fibrous orbital tissue surround the rectus muscles just behind the equator and extend to the orbit holding it to some degree to the orbit wall (Fig. 12). These tissues also act to limit sideslip in the rectus muscle and to limit the surgical effect of rectus muscle transposition operations in which the insertion is moved laterally. They bias the origin as the trochlea does, but to a much lesser degree, thus acting as “soft pulley” (Fig. 13). such displacement occurs in strabismus disorders, but it is not always clear whether the displaced muscle is taking the pulley with it or vice versa. These tissues have long been known to contain smooth muscle fibers.¹⁷ Innervation to these structures and their functional significance is a current topic of investigation.

Imagine that the medial rectus consisted only of two stiff chains. Then, when the eye rotated upward, the smallest bit of slack created by relaxation at the upper border of the medial and lateral muscle totally relaxes tension and transfers it to the lower border. Clearly, this jerkiness would be unsatisfactory, and the smooth compliant nature of the extraocular muscle and its convex anterior insertion are factors that combine to transfer this force easily and smoothly from one side of the muscle to the other. On the contrary, if the muscle were extremely flexible, like a wide elastic band, then relaxation on one side would have very little effect on the transfer of tension along the muscle insertion. In fact, the stiffness of the muscle, about 0.25 to 0.5 g per degree, seems exactly adapted. In awake patients, when the upper part of the medial rectus insertion is cut away from the globe except for 2 mm at the lower end of the insertion, the cut muscle retracts, making an angle of about 45 degrees with the original insertion. When the patient rotates his eye superiorly, the cut superior fibers fall back almost exactly onto the insertion, an indication that the inferior fibers are taking almost the entire strain. Thus, as the eye carries the medial rectus insertion up, the force moves down, keeping its pull horizontal on the globe and horizontal in the orbit.

The intermuscular membrane stabilizes the anterior portion of the rectus muscles from the equator forward, preventing each muscle from slipping sideways. In Figure 14, the path of the lateral rectus in gaze nasally and upward is indicated, assuming the muscle took the shortest path from origin to center of insertion. This extreme upward path is not taken, but a course nearly over the lateral meridian of the eye is maintained by the intermuscular membrane. If the intermuscular membrane is cut away at the time of surgery, the horizontal muscle slips about 2 mm vertically during vertical movements. A second factor holding the rectus muscle from slipping sideways is the adhesion or “foot plate” that attaches the global surface of the muscle to the sclera and extends some 4 to 5 mm posterior to the insertion. Abnormal vertical eye movements from such sideslip of horizontal can occur in strabismus disorders in which high forces gradually tear and obliterate the intermuscular membrane (Duane’s syndrome), and in high myopia in which expansion of the globe, usually in the upper temporal area, stretches the intermuscular membrane and pushes the lateral rectus downward. These disorders can be treated by fixing the muscle to the sclera at the equator to prevent sideslip.^18,19 The superior oblique tendon has a very short length and arc of contact, and here sideslip is not a significant factor. The inferior oblique has a very long arc of contact. Indeed, the necessary length of muscle to allow extension and contraction is provided by the coiling of the inferior oblique muscle around the globe for a long distance. The ligament of Lockwood, at the crossing of the inferior oblique and inferior rectus muscles, acts to prevent A-P slip of the inferior oblique, just as the intermuscular membrane acts in terms of the rectus muscle (Fig. 15). Eye muscles imaged on MRI scans had only small sideslip when subjects fixated in various directions.²⁰

The belly of the muscle is readily split longitudinally because it contains little transverse fascial tissue, but the anterior muscle is cohesive within itself to prevent separation because otherwise, the fibers of the lateral rectus muscle would splay out almost 18 mm wide in extreme gaze into elevation and adduction. Thus, the anterior muscles, their surrounding Tenon’s fascia, and the intermuscular membranes form a continuous stabilizing band or cap around the globe extending from the muscle insertions anteriorly back to the equator. The muscle “pulley” tissue anchoring the muscles to the orbit adds to this.

Even though all these muscles have some effect on the eye in every gaze position, each pulls preferentially in a specific direction, called its field of action. Torsion is not usually considered, only horizontal and vertical actions. The field of action is established by two considerations: geometry and innervation.

We have seen in our analysis that the lateral rectus pulls toward abduction almost exclusively. That is its field of action. The medial rectus pulls toward adduction almost exclusively. That is its field of action.

For vertical gaze such a simple arrangement is not present, for a combination of muscle actions exists. In 23 degrees of abduction, the superior rectus is a pure rotator around the horizontal axis of the adducted eye. This is its field of vertical action for clinical testing. If the eye rotates well vertically in this position, it must be due to a normal superior rectus. Here, the inferior oblique muscle contributes little vertical movement. In adduction, the oblique becomes an increasing elevator, but the superior rectus remains a substantial elevator even in adduction because of its angle of insertion and its greater cross-sectional area. Thus, elevation in adduction is a combination of inferior oblique and superior rectus activity. Nevertheless, vertical contribution of the oblique can be assessed clinically by comparing elevation in abduction, in which it has virtually no effect on elevation, with elevation in adduction in which it contributed 45% to 50% of elevation (Fig. 16). The superior oblique and the inferior rectus muscles have the same relationship in infraduction. The inferior rectus is virtually the sole infraductor in the abducted gaze positions, and both the superior oblique and the inferior rectus contribute as gaze is moved toward adduction.

In addition to the mechanics, changes in the innervation to the muscles in various gaze directions establish what they do; this might be thought of as field of activation. For abduction, innervation progressively increases to the lateral rectus as the eye abducts from the primary position. This is true whether it starts from the primary position, or whether the eye starts from a position of slight elevation or depression: the program of innervation of the lateral rectus appears to be the same. Similarly, the medial rectus increases activity with all attempts to adduct the eye, whether the eye starts in the primary position, in moderate supraduction, or moderate infraduction.

The elevators of the eye, the superior rectus and the inferior oblique muscles, probably receive equal innervation increments during supraduction attempts, and this is true whether the eye is straight ahead, abducted, or adducted. That is, if one establishes a horizontal line 30 degrees above the primary position, whether the eye looked at the adduction end, the middle of the line, or the abduction end, any individual vertical muscle has the same innervation. The same applies for infraduction involving the superior oblique and the inferior rectus. Thus, it must follow that the oblique muscles and the rectus muscles establish their field of vertical action primarily on the basis of mechanics, and they do not separate themselves one from another on the basis of differences in innervation reaching them in adduction versus abduction.

We occasionally find a motor unit within, say, the inferior rectus that changes its innervation in the downgaze plane slightly, increasing slightly in abduction, but decreasing with adduction. However, just the reverse of this may be seen in another patient. Consequently, minor variations from the general rule occur. Perhaps these variations act to correct differences in anatomy from one person to another. We know oblique muscle planes are at 30 degrees to the visual axis in one person and 50 degrees in another; perhaps these variations represent individual innervational adjustments that develop during infancy and visual development to achieve concomitance. These variations may have been the basis of the anecdotal reports of difference in vertical muscle innervation in abduction vs abduction.²¹ Data on the innervational change of vertically acting eye muscles with gaze are few and a careful systematic study remains to be done. For vertical fusion movements, evidence from the torsional position of the eye indicates that the oblique muscles are the primary movers, not the vertical rectus muscles,^22,23 although electromyographic (EMG) studies remain to be done. Vertical supraduction during forced blinking (Bell’s phenomenon) appears to be carried out primarily by the oblique muscles.

In normal children, the eye can rotate from the primary position about 45 to 50 degrees horizontally and downward and about 40 to 45 degrees upward. This 45 to 50 degrees of movement requires about 10 mm of contraction and 10 mm of relaxation from the primary position (4.8 degrees of rotation equals 1 mm of distance on the sclera). Supraduction diminishes with age. It is reduced a bit even by age 25 and averages only 16 degrees of supraduction at age 80. Other directions of gaze persist better. Exercise helps.²⁴ Donders pointed out that the eyes of myopic people rotate less than this.² The center of rotation is more posterior in myopic people, effectively increasing the radius of the eye as it rotates and thus giving less rotation for each millimeter of muscle shortening. On the contrary, microphthalmic eyes can often turn more—up to 70 degrees abduction!

Almost all investigators find that the extraocular muscles of mammals are divided into two layers to some extent: a global or central layer, next to the eye, and a superficial or orbital layer confined to the posterior two thirds of the rectus muscles and less evident in oblique muscles. This layering is much less obvious in humans than lower species (Fig. 17). The orbital layer has a high capillary density and generally contains small fibers. Scott and Collins confirmed that, in humans, fibers that are active constantly for fixation near the primary position are predominantly in this layer.²⁶ By the classification of Alvarado and Van Horn in cat, the orbital layer contains two fiber types.²⁷ Both are relatively small, rich in mitochondria, and contain some lipid vacuoles. About 60% to 70% of the cells are singly innervated with good sarcoplasmic reticulum content, which allows rapid calcium ion changes with each contraction, and about 30% to 40% are multiply innervated slower fibers.

The global layer contains one type of multiply innervated fiber and three types of single innervated fibers of varying size, mitochondrial supply, and sarcoplasmic reticulum content. Type 1 is a large, pale, relatively mitochondria-free type rich in endoplasmic reticulum. This should be a very fast but readily fatigued fiber, good for saccades and for short periods of extreme gaze. These fibers constitute about 30% to 40% of the total number, but they occupy about 60% of the core area and thus contribute importantly in terms of strong but temporary force production. Types 2 and 3 are progressively smaller and contain increasing amounts of mitochondria and probably decreasing amounts of endoplasmic reticulum. These would be more fatigue resistant and slower in response than those that contain a great deal of cytoplasmic reticulum.

The muscle fibers are mostly parallel, but some side-to-side and end-to-side junctions of muscle fibers exist, creating a network within the global layer. Many fibers thus terminate before the end of the muscle; a cross section at the center shows more fibers than cross sections near either end. Oh and Demer have recently counted the fibers in the rectus muscles of monkeys and humans and confirm this restriction of the orbital layer to the posterior two thirds of the muscle.²⁸ Surprising was the finding of insertion of some of these orbital fibers onto the fibromuscular tissue (“pulley”) in Tenon’s fascia near the anterior one third of the muscle.

The endomysium surrounding these fibers contains substantial elastic tissue. The perimysium surrounding groups of muscle fibers contains more collagen fibers. Within this area run the small vessels and nerves to the muscle. These collagen fibers run along the length of the muscle; thus, their shortening by inflammation, scar or lack of being stretched by antagonist contraction (e.g., in paralysis) results in stiffening and restriction of eye movement, a common clinical problem.

In Figure 18, the muscle is diagrammatically dissected into its components. The heavy filaments are myosin; the thin filaments, a double helix of actin with additional proteins, tropomyosin, and troponin. The sliding of these filaments past one another provides length change, especially apparent in Figure 19. As thick and thin filaments of the muscle fiber slide past one another, the bridges between these filaments maintain the strength of the muscle. If there were many crossbridges, there would be more force, and if there were fewer crossbridges, there would be less force, as seen in isometric testing. In Figure 20, one can see that as the muscle is normally stretched, the number of cross bridges being effectively used maximumizes and then gradually diminishes as further stretching occurs. Unlike many muscles that work over a large range, extraocular muscles work almost entirely in the region from 1 to 2.2; that is, the rather linear slope to the left of the peak of tension. To work within this range, sarcomeres of muscles cannot be greatly stretched or compressed from their normal length of about 2.3 μm. When muscles are maintained at a stretched or shortened length for weeks or months, they respond by adding or removing sarcomeres to regain this length of 2.3 μm. Muscles so shortened become stiff also and cannot be distinguished mechanically from fascial or fibrotic contraction.²⁹

Both singly and multiply innervated types of eye muscle fibers are composed of thick and thin filaments of about the same length. Thus, it is not surprising that they give about the same total force for each cross-sectional area.³⁰

How can a wave of depolarization sweep through an eye muscle and cause a twitch in 2 msec? Invaginations of the muscle membrane, the sarcolemma, extend into the muscle fiber in a direction transverse (t) to the axis of the fibrils, carrying the wave of polarization into the muscle itself. The sarcoplasmic reticulum that stores calcium necessary for activation is associated directly with these transverse tubules. Much T-system and sarcoplasmic reticulum is present in eye muscles to allow very rapid contraction frequencies up to 400 Hz.

Mitochondria provide power to the muscle by oxidative phosphorylation. Because muscle contraction is powered by dephosphorylation of adenosine triphosphate, mitochondria are one source of energy. Thus, the more mitochondria present, the more power and stamina are provided. The extraocular muscles have an extremely high content of oxidative enzymes associated with the mitochondria.

In certain eye muscle fibers, the filaments are separated into bundles. Obvious under light microscopy, this fibrillar pattern (Fibrillenstruktur) is generally associated with rapid, twitch-type contraction. A horizontal view of such a fiber (Fig. 21) reveals the extensive mitochondrial involvement and the differentiation into small bundles. Most of these fibers have single nerve innervation by only one motor endplate. Such a fiber is adapted for rapid, short-term use. In other fibers, the fibrils are not divided much into separate bundles, giving a rather uniform field of distribution (Felderstruktur). Some of these muscle fibers contract only in local areas of the muscle by local innervation around multiple nerve endings along the fiber, without an overall depolarization and twitch. In Figure 22, such a fiber is seen in cross section, again emphasizing the lack of separation into myofibrils. Such fibers would be less capable of high frequence contraction but more capable of slow, steady, stamina-oriented tasks.

Blood flow in the extraocular muscles must be exceedingly high to account for the rapid metabolism. Indeed, average blood flow per gram of extraocular muscles proportionally to that of other skeletal muscles and was second only to myocardium.³¹ Eye muscles are very resistant to fatigue under laboratory conditions. Extreme gaze to one side for several minutes, however, gives rise to unstable fixation in humans (end-gaze nystagmus). This is unequal in the two eyes, so it appears to be a fatigue of the muscles or motor units rather than of gaze function.

Miller found alterations in staining characteristics, occasionally degenerating nerve fibers, and disturbance of the orderly fiber alignment and direction of human muscles after age 30.³² With age, the collagen fibers within the muscle itself increased. As motor nerve fibers drop out with neuron death, the remaining nerve fibers send sprouts to form new neuromuscular endings on the denervated muscle fibers. This process preserves muscle strength with aging. A similar sprouting in partial nerve damage leads to prolonged recovery with large motor units. The different types of muscle fiber are probably susceptible to diseases at varying rates. For example, muscular dystrophies associated with mitochondrial abnormalities should especially involve extraocular muscles. Cogan and colleagues have proposed a susceptibility difference seen also in myasthenia gravis.³³

Except for those virtually eyeless animals, all vertebrates possess the standard six extraocular muscles, whether lateral or frontal eyed, developed for roles as predator or prey.⁴² They all make reflexive, compensatory eye movements in response to a movement of the head. All three sorts of natural head movement are more or less compensated: head rotation activates the angular VOR (AVOR); head translation activates the linear VOR (LVOR); and head tilt in a coronal plane activates the torsional VOR (TVOR). Associated eye movements are compensatory because, for example, to a rightward head movement, the eyes move reflexively leftward in an attempt to steady the visual image on the retina.

There are numerous variations on this theme. Usually, VOR performance is better when combined with visual cues. This reflex response is referred to as visually enhanced VOR (VVOR). When the result of a deliberate head movement, the VOR is called active, or passive when the result of external forces moving the head. Active and passive VORs may differ given that the former can be influenced simultaneously by the cervico-ocular reflex and perhaps by internal command signals (efference copy), but the effect of either in normals appears small and is not usually considered.^43,44 Active or passive head movement can be either transient, that is, the head moves from one steady position (or velocity) to another as, for example, one might orient toward something far to one side, or oscillatory as, for example, one might track an insect flying nearby. Additionally, the head (and body) can be passively rotated. Such continuous rotation in one direction is unnatural for humans but not necessarily so for fish swimming in tight circles or being carried by swirling currents.

Optokinetic eye movements, by definition, are driven by movement in the visual scene. Thus, all oculomotor subsystems except the VOR come into play when tracking a visual target with the head stationary. One of these subsystems, the optokinetic system (OKS) evolved early in vertebrate history in fish⁵⁵ and supplements the VOR by eliciting compensatory eye movements in response to large-field retinal stimulation, the rationale perhaps being that whenever the images of most everything visible move within a “stationary” world, then most likely the eyes moved in space rather than the other way around. To a suddenly presented stimulus such as a full visual field of horizontally translating vertical stripes, the optokinetic response is the rapid onset of optokinetic nystagmus (OKN) with slow phases in the direction of stripe motion (Fig. 26C). In humans, peak slow phase eye velocity is reached during the first slow phase.⁵⁶ As long as the stimulation continues, OKN continues unabated. The ratio of slow phase velocity to stimulus velocity defines OKN gain, which is close to unity for stimulus velocity up to 60 to 90 degrees/sec. Instructing subjects to pick out and follow stripes (look mode) results in large amplitude, low frequency (more than 40 degrees at about 1 Hz) nystagmus while instructing subjects to stare straight ahead results in small amplitude, high frequency (less than 20 degrees at about 2 Hz) nystagmus.⁵⁷ Without instruction, most subjects naturally adopt the stare mode. If all lights are extinguished during OKN, nystagmus, in most subjects, does not stop entirely but continues as optokinetic after-nystagmus (OKAN) with an attenuated slow phase velocity that slowly decays away in about 1 minute (see Fig. 26C). The initial OKAN slow phase velocity depends not just on the OKN stimulus velocity but also on the OKN stimulus duration; longer duration OKN stimulation (up to 1 minute) leads to higher velocity slow phases during OKAN. The latter property has been called velocity storage.⁵⁶ Two integrated signal pathways have been postulated to explain OKN and OKAN. The so-called “direct” signal pathway produces the nearly instantaneous, rapid rise of eye velocity at stimulus onset. The so-called “indirect” signal pathway slowly charges the velocity storage element during OKN and discharges the “stored velocity” during OKAN.⁵⁸ If OKN stimulation is prolonged, OKAN, which beats in the same direction as the OKN, is followed in some subjects by optokinetic after-after nystagmus (OKAAN), which beats in the opposite direction (Fig. 26C). (There is no agreed upon terminology of optokinetic after-nystagmus. Other terms for OKAN include primary OKAN and OKAN I and other terms for OKAAN include secondary OKAN, reversed OKAN, and OKAN II.) OKAAN is thought to reflect OKS habituation.⁵⁹ Interestingly, labrynthine disease abolishes OKAN when the optokinetic stimulus produced OKN with fast phases toward the affected ear.⁶⁰ A particularly curious observation is the sensation perceived during full-field optokinetic stimulation. At stimulus onset human subjects report that only the drum is moving but after a short while most subjects report the sensation of slow self rotation in a direction opposite to the drum’s rotation, a phenomenon called circular vection. Circular vection builds until the subject is convinced that the drum is stationary and it is the subject who is rotating exclusively. Nothing in the OKN record, however, reflects the development of circular vection.

The saccadic system generates all reorienting eye movements. When these eye movements are used to acquire novel visual targets or correct for positioning inaccuracies and drift they are referred to as saccades. The French word saccade means jerk and appropriately describes the eye’s behavior. When these movements reset the eye during nystagmus, the resulting phenomena are called quick phases. Physiologically, saccades and naturally induced quick phases are not known to be different.⁶¹ Saccades are often called fast or rapid eye movements but this seems poor terminology because the vestibular system can generate “slow” phases of comparable velocity.⁴⁹

When using eye movements only, a normal subject tracks a small moving target with a mixture of smooth pursuit, saccadic, and vergence eye movements. The overall strategy is to maximize acuity by keeping the target close to the fovea while reducing retinal image slip. For a particular subject, the relative mix of smooth and saccadic eye movement to track a target moving on a uniform background depends primarily on target velocity and regularity. The smooth pursuit subsystem (SPS) creates the conjugate smooth pursuit component. SPS gain, the ratio of eye velocity to target velocity, seldom is unity so that as the eye drifts away from the target saccades are triggered to reduce the accumulated error.⁹¹ SPS gain decreases with increasing target velocity, increasing target eccentricity with respect to the fovea, decreasing target movement predictability and decreasing attention. SPS gain is also lower when the moving target is viewed against a stationary structured background.⁹⁰ With an alert subject, as SPS gain decreases for whatever reason, the frequency of catch-up saccades increases, thus keeping the target close to the fovea.

Higher SPS gain when tracking predictably as opposed to randomly moving targets hints at a fundamentally complicated system: a simpler control system would depend only on the target’s instantaneous kinematics. Further along this same line, the observation that the SPS can be, to some extent and with practice, driven by perception in lieu of retinal image motion along the pursuit direction^92,93 has not yet been explored beyond psychophysics and is too often ignored. Reliance on an internal model of target motion probably stems from the somewhat longer time needed by the visual system to process motion cues. Generally, though, voluntary smooth pursuit requires some motion cues, either visual, proprioceptive, or auditory. Nevertheless, target image slip on the retina is considered the primary input to the SPS but constant retinal error can be an adequate stimulus as well.^94,95