Chapter 2
Eye Movements and Positions
MARSHALL M. PARKS
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MOVEMENT
POSITION
REFERENCES

An eye may be moved or displaced in the orbit without rotating about its center of rotation. Such a change in eye position unaccompanied by movement about its center of rotation is a translatory movement. The translatory movement may be in the equatorial plane, with the eye being displaced horizontally, vertically, or obliquely; the movement may also occur in the sagittal (anteroposterior) axis, resulting in exophthalmos or proptosis and enophthalmos. Translatory eye movements are passive and may be produced by the examiner displacing the eye while palpating the orbital region. Both an expanding lesion in the orbit and a defect in the orbital bones may cause translatory eye movements.
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MOVEMENT

Duction

The term duction refers to the movement of one eye. A prefix is attached to this word to indicate the direction in which the eye is moved (Fig. 1). Duction is accomplished by simultaneous and equally graded contraction and relaxation of antagonistic muscles, in accord with Sherrington's law of reciprocal innervation.

Fig 1. Ductions. Horizontal ductions (adduction and abduction) are produced by contractions of the medial rectus (MR) and lateral rectus (LR) muscles. Vertical ductions and cycloductions result from combined contractions of the vertical rectus and oblique muscles. Combined contractions of the superior rectus (SR) and inferior oblique (I0) muscles produce supraduction; combined contractions of the inferior rectus (IR) and superior oblique (SO) muscles produce infraduction. Incy-cloduction is caused by combined SO and SR contractions, and excycloduction is caused by combined IO and IR contractions. In abduction the vertical rectus muscles are the prime vertical movers, and the obliques are the prime torsional movers; in adduction this is reversed.

Adduction

Adduction is a horizontal movement directed medially from the vertical axis. It is primarily accomplished by contraction of the medial rectus muscle and relaxation of the lateral rectus muscle.

Recessing the insertion does not reduce the adduction significantly until the recession exceeds 6 mm. In the primary position the muscle contacts the globe 6 mm as it arcs around the nasal sclera to insert. The medial rectus is a tight muscle; a maximum resection of 6 mm is possible without also producing resistance to abduction and slight retraction of the eye into the orbit (enophthalmos), with a reduction of the vertical dimension of the palpebral fissure.

A small amount of secondary adduction is accomplished by contraction of the vertical rectus muscles: in upgaze by the superior rectus muscle, in downgaze by the inferior rectus muscle, and in the primary position by their combined contraction.

Abduction

Abduction is a horizontal movement directed laterally from the vertical axis. It is accomplished by contraction of the lateral rectus muscle and relaxation of the medial rectus muscle.

Recessing the insertion does not reduce the abduction significantly until the recession exceeds 7 to 8 mm. In the primary position the muscle contacts the globe approximately 8 mm as it arcs around the temporal sclera to insert. The lateral rectus is not a tight muscle like the medial rectus, so excessive resection is less inclined to result in retraction of the eye into the orbit. However, resection of more than 8 mm does offer clinically detectable resistance to adduction.

A small amount of secondary abduction is accomplished by contraction of the oblique muscles: in upgaze by the inferior oblique muscle, in downgaze by the superior oblique muscle, and in the primary position by their combined contraction.

Supraduction

Supraduction (sursumduction) is a vertical movement (elevation) directed superiorly from the horizontal axis of the eye. It is the result of the combined contraction of the superior rectus and inferior oblique muscles and the combined relaxation of the inferior rectus and superior oblique muscles. However, as the eye moves into an abducted position, the superior rectus becomes the prime elevator muscle, and as the eye moves into adduction, the inferior oblique is the principal elevator muscle.

Since the superior rectus muscle courses forward from the orbital apex at an angle of 23° temporal to the medial wall of the orbit and inserts anterior to the center of rotation of the globe, the movement of the eye produced by the contraction of the muscle varies according to its horizontal starting position (Fig. 2). Starting from a position of 23° of abduction, the only movement is elevation. Starting from a position of 67° of adduction, the only movement is intorsion. Starting from the primary position, the movement is combined elevation and intorsion plus slight adduction; the adduction results from the midline of the muscle being medial to the center of rotation of the globe when the eye is in the primary position.

Fig 2. Superior rectus muscle. The superior rectus muscle courses at an angle of 23° to the medial wall of the orbit, giving elevation principally in abduction (C) and intorsion in adduction (A). In the primary position (B) the main thrust of the pulling power is medial to the center of rotation, causing slight adduction action in addition to the cyclovertical action. (Parks MM, Parker JE: Atlas of Strabismus Surgery. Philadelphia, Harper & Row [in press]. Courtesy of John E. Parker)

Recessing the superior rectus muscle decreases all its functions; resecting the muscle enhances all primary position functions plus offers resistance to the relaxation of its functions. Recessions and resections of the superior rectus muscle in excess of 4 mm reduce the normal full vertical excursion of the eye in abduction; those in excess of 6 mm produce a detectable change from the preoperative primary position relationship between the superior limbus and the position of the upper eyelid. Postoperatively, the vertical dimension of the palpebral fissure remains unchanged from the preoperative value but the level of the eye is vertically changed; this causes the sclera to present above the limbus following excessive recession and causes the superior pupillary border to be tangential with the upper eyelid following excessive resection.

Nasal transposition of the superior rectus muscle by one-half width enhances the adduction function, while temporal transposition of the same amount eliminates the secondary adduction, the effect being most conspicuous in midline upgaze.

Infraduction

Infraduction (deorsumduction) is a vertical movement (depression) directed inferiorly from the horizontal axis. It is the result of the combined contraction of the inferior rectus and superior oblique muscles. However, as the eye moves into an abducted position, the inferior rectus becomes the prime depressor muscle, and in adduction, the superior oblique is the principal depressor muscle.

Since the inferior rectus muscle courses forward from the orbital apex at an angle of 23° temporal to the medial wall of the orbit and inserts anterior to the center of rotation of the globe, the movement of the eye produced by the contraction of the muscle varies according to its horizontal starting position (Fig. 3). Starting from a position of 23° of abduction, the only movement is depression. Starting from a position of 67° of adduction, the only movement is extorsion. Starting from the primary position, the movement is combined depression and extorsion plus slight adduction; the adduction results from the midline of the muscle being medial to the center of rotation of the globe when the eye is in the primary position.

Fig 3. Inferior rectus muscle. The inferior rectus muscle courses at an angle of 23° to the medial wall of the orbit, giving depression principally in abduction (C) and extorsion in adduction (A). In the primary position (B) the main thrust of the pulling power is medial to the center of rotation, causing slight adduction action in addition to the cyclovertical action. (Parks MM, Parker JE: Atlas of Strabismus Surgery. Philadelphia, Harper & Row [in press]. Courtesy of John E. Parker)

Recessing the inferior rectus muscle decreases all its functions; resecting the muscle enhances all primary position functions plus offers resistance to the relaxation of its functions. Unless the inelastic cords extending between the external capsular surface of the inferior rectus muscle and lower eyelid tarsus skin and the inferior orbital septum are completely severed, any quantity of recession or resection will lower or raise the lower eyelid, causing either an increase or a decrease in the vertical dimension of the palpebral fissure. Recession of the inferior rectus muscle in excess of 4 mm reduces the total excursion of downgaze in abduction; however, as much as a 10-mm resection only minimally reduces the expected total excursion of upgaze.

Nasal transposition of the inferior rectus muscle by one-half tendon width enhances the adduction function, while temporal transposition of the same amount eliminates the secondary adduction, the effect being most conspicuous in midline downgaze.

Incycloduction

Incycloduction (intorsion) is a torsional movement of the eye about the anteroposterior axis that displaces the superior pole of the eye medially. Intorsion is the result of the combined contraction of the superior oblique and superior rectus muscles and the combined relaxation of the inferior oblique and inferior rectus muscles. However, as the eye moves into an abducted position, the superior oblique muscle becomes the prime intortor, and in adduction, the superior rectus muscle is the principal intortor.

Since the reflected tendon of the superior oblique muscle delivers the direction of the pulling power to the scleral surface when the muscle contracts, the movement of the eye varies according to its horizontal starting position (Fig. 4). Starting from a position of 39° of abduction, the only movement is intorsion. Starting from a position of 51° of adduction, the only movement is depression. Starting from the primary position, the movement is combined intorsion and depression plus slight abduction; the abduction results from the tendon being posterior to the rotation center of the globe when the eye is in the primary position.

Fig 4. Superior oblique muscle. The reflected tendon of the superior oblique muscle courses at an angle of 51° to the medial wall of the orbit, giving a cyclovertical action in the primary position (B) that becomes principally intorsion in abduction (C) and depression in adduction (A). Slight abduction action is also produced, because the pulling power is exerted along a line posterior to the center of rotation. (Parks MM, Parker JE: Atlas of Strabismus Surgery. Philadelphia, Harper & Row [in press]. Courtesy of John E. Parker)

Unlike the tendons of the rectus muscles, the superior oblique tendon does not lend itself well to recession or resection. Tenotomy and tucking of the tendon are the usual weakening and strengthening procedures performed on the superior oblique muscle. Tenotomy is performed medial to the superior rectus muscle on the cord portion of the tendon; the tuck may be performed on the tendon either medial or lateral to the superior rectus muscle. A tenotomy does not completely eliminate all function of the superior oblique, because some pull power persists when the muscle contracts through the connections of the tendon to the Tenon's capsule and the intermuscular septum. Tucking the tendon causes a relative decrease in the elevation excursion of the adducted globe; the severity is directly proportional to the quantity of the tuck.

The anterior half of the reflected tendon of the superior oblique muscle has a greater intorsion function, and the posterior half has a greater depressor function, according to Fink.1 Emanating from the thesis is an operative procedure described by Harada and Ito that either advances or anteroplaces the anterior half of the tendon to enhance the intorsion function.2

The secondary abduction function of the superior oblique muscle is apparent in midline downgaze by hyperfunctioning (overaction), causing excess abduction, and hypofunctioning (palsy), causing deficient abduction. The midline downgaze abduction abnormality associated with either overaction or palsy is eliminated by tenotomy or tucking of the tendon, respectively.

Excycloduction

Excycloduction (extorsion) is a torsional movement of the eye about the anteroposterior axis that displaces the superior pole of the eye laterally. Extorsion is the result of the combined contraction of the inferior oblique and inferior rectus muscles and the combined relaxation of the superior oblique and superior rectus muscles. However, as the eye moves into an abducted position, the inferior oblique muscle becomes the prime extortor, and in adduction, the inferior rectus muscle is the principal extortor.

When the inferior oblique muscle contracts, the resulting movement of the eye varies according to its horizontal starting position (Fig. 5). Thus, starting from a position of 39° of abduction, the only movement is extorsion. Starting from a position of 51° of adduction, the only movement is elevation. Starting from the primary position, the movement is combined extorsion and elevation plus slight abduction; the abduction results from the muscle being posterior to the center of rotation of the globe when the eye is in the primary position.

Fig 5. Inferior oblique muscle. The inferior oblique muscle courses at an angle of 51° to the medial wall of the orbit, giving a cyclovertical action in the primary position (B) that becomes principally extorsion in abduction (C) and elevation in adduction (A). Slight abduction action is also produced, because the pulling power is exerted along a line posterior to the center of rotation. (Parks MM, Parker JE: Atlas of Strabismus Surgery. Philadelphia, Harper & Row [in press]. Courtesy of John E. Parker)

Weakening the inferior oblique muscle is accomplished by recession, myotomy, myectomy, or denervation plus extirpation. Recession can be graded according to the severity of the hyperfunction, ranging between 6 and 14 mm. Disinsertion without suturing the end of the muscle to the sclera is of little value, because the muscle reattaches near the original insertion site, nullifying an initially satisfactory result. The same fate is shared by denervation, since reinnervation occurs within a matter of months. Myotomy anywhere along the course of the muscle is followed by subsequent reunion of the cut ends, which also occurs in minimal myectomies. Myectomies of several millimeters are more effective but do not permit a graded quantity of surgery. The most complete elimination of the overaction is accomplished by extirpating all muscle tissue between the inferior oblique's penetration of Tenon's capsule and insertion. Denervation of the muscle is required in performing the extirpation, and this procedure is justified only in the case of the most severe overaction of the inferior oblique muscle. Strengthening procedures, such as resections and advancements, for an underacting inferior oblique are difficult and have proved rather useless.

The secondary abduction function of the inferior oblique muscle is apparent in midline upgaze by hyperfunctioning, causing excess abduction. The excessive upgaze abduction associated with the overaction is eliminated by weakening the muscle.

Jampel does not agree with the foregoing classic teaching regarding the vertical and torsional movements of the eyes.3, 4 He has challenged the concept of oblique muscle action. Based on mathematical considerations, studies of models of the eye, experimental studies on monkeys, and limited clinical observations, he proposes the following: (1) Elevation and depression, even in adduction, are mainly a function of the superior and inferior rectus muscles. (2) The torsional component of the oblique muscles is the same throughout the range of horizontal eye movement. (3) The abducting component of the oblique muscles does not decrease on adduction but actually increases.

Version

Version refers to simultaneous movement of both eyes in the same direction; a prefix indicates the direction of the conjugate movement. The muscles in each eye that are the prime movers undergo equally graded contractions in accord with Hering's law of innervation, and for each contracting muscle there is an opposite and equally graded antagonist (Sherringtons law). The complete range of versions, indicating only the contracting muscles, is shown in Figure 6.

Fig 6. Versions. Horizontal versions (dextroversion and levoversion) are produced by contractions of yoked medial rectus (MR) and lateral rectus (LR) muscles. Vertical versions result from combined contractions. Combined contractions of the superior rectus (SR) and inferior oblique (I0) muscles cause supraversion, and combined contractions of the inferior rectus (IR) and superior oblique (SO) muscles cause infraversion. Torsional versions are produced by combined contractions of intortors of one eye (SO and SR) and extortors of the other (IO and IR); dextrocyloversion results from right eye extortors and left eye intortors contracting, and le-vocycloversion results from right eye intortors and left eye extortors contracting.

Horizontal versions are dextroversion and levoversion. Dextroversion is accomplished by contraction of the right lateral rectus and left medial rectus muscles and relaxation of the right medial rectus and left lateral rectus muscles. Levoversion is accomplished by contraction of the left lateral rectus and right medial rectus muscles and relaxation of the left medial rectus and right lateral rectus muscles.

Vertical versions are supraversion (sursumversion) and infraversion (deorsumversion). Supraversion is accomplished by bilateral contraction of the elevator muscles (the superior rectus and inferior oblique muscles) with simultaneous relaxation of the depressor muscles (the inferior recti and the superior obliques). As the eyes move into dextroversion, the right superior rectus and left inferior oblique muscles are the prime elevators; in levoversion, the left superior rectus and right inferior oblique muscles are the prime elevators. Infraversion is accomplished by an increase of innervation to the four depressor muscles with an equal decrease of innervation to the four elevator muscles. In dextroversion the prime depressors are the right inferior rectus and left superior oblique muscles; in levoversion, the left inferior rectus and right superior oblique muscles are the prime depressors.

Cycloversion is the simultaneous and equal tilting of the corneal superior poles either to the right or to the left (either dextrocycloversion or levocycloversion). Dextrocycloversion is accomplished by contraction of the extortors of the right eye (i.e., the inferior rectus and inferior oblique) and of the intortors of the left eye (i.e., the superior rectus and superior oblique) and by relaxation of the intortors of the right eye (i.e., the superior rectus and superior oblique muscles) and of the extortors of the left eye (i.e., the inferior rectus and inferior oblique muscles). In dextroversion the most effective dextrocycloverters are the right inferior oblique and left superior rectus muscles. In levoversion the most effective dextrocycloverters are the left superior oblique and right inferior rectus muscles. Levocy-cloversion is accomplished by an increase of innervation to the extortors of the left eye and the intortors of the right eye with a simultaneous decrease of innervation to the intortors of the left eye and the extortors of the right eye. In dextroversion the primary levocycloverters are the left inferior rectus and right superior oblique muscles; in levoversion the left inferior oblique and right superior rectus muscles are the prime levocycloverters.

Vergence

Vergence is the simultaneous and equal movement of the eyes in opposite directions; a prefix attached to “vergence” indicates the direction of the disjugate movement. The muscles that are the prime movers undergo equally graded contractions in accord with Hering's law of innervation, and for each contracting muscle there is an opposite and equally graded relaxing antagonist (Sherrington's law). All possible vergence movements are shown in Figure 7, which indicates only the contracting muscles.

Fig 7. Vergences. Horizontal vergences are produced by simultaneous contractions of the medial rectus (MR) muscles of each eye (convergence) or the lateral rectus (LR) muscles of each eye (divergence). The vertical vergences are caused by combined superior rectus (SR ) and inferior oblique (IO) muscle contractions in one eye and inferior rectus (IR) and superior oblique (SO) muscle contractions in the other; the right eye elevators and the left eye depressors simultaneously contract to produce positive vertical vergence, and the right eye depressors and the left eye elevators simultaneously contract to produce negative vertical vergence. The torsional vergences result from simultaneous combined contractions of either the two intortors (SO and SR) of both eyes, producing incyclovergence, or the two extortors (IO and IR) of both eyes, producing excyclovergence.

Horizontal vergences are convergence and divergence. Convergence is accomplished by contraction of the medial rectus muscles and relaxation of the lateral rectus muscles. Divergence is accomplished by contraction of the lateral rectus muscles and relaxation of the medial rectus muscles.

Vertical vergences are designated as positive and negative. Positive vertical vergence is elevation of the right eye with simultaneous depression of the left; negative vertical vergence is depression of the right eye with simultaneous elevation of the left. Each is accomplished by elevators contracting in one eye and depressors contracting in the other with equal and simultaneous relaxation of their antagonistic muscles.

Cyclovergence is equal and simultaneous tilting of the corneal superior poles either inward or outward (either incyclovergence or excyclovergence). Incyclovergence is accomplished by simultaneous contraction of all intortors (superior recti and superior obliques) and relaxation of all extortors (inferior recti and inferior obliques). Excyclovergence is accomplished by an increase of innervation to the extortors and an equal decrease of innervation to the intortors.

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POSITION
The primary position is the position the eyes assume when fixating an infinitely distant object straight ahead. Because of the difficulty in meeting the requirement that the fixation point be at an infinite distance and because of the little practical difference in the horizontal alignment of the eyes between fixating at infinity and fixating at 6 meters, fixating at 6 meters is considered primary position. The primary position can be maintained with the head erect or with the head tilted to either shoulder. By comparing the eye alignment in the primary position in the various tilted positions of the head, the physician can evaluate the muscles that have a combined torsional and vertical action. Levocycloversion is stimulated with the head tilted to the right; dextrocycloversion is stimulated with the head tilted to the left. A weak cyclovertical muscle produces both a torsional and a vertical deviation that changes as the head is tilted, although the eyes never move out of the primary position.

Secondary positions are any variation of eye position other than primary and include near fixation positions, cardinal positions, and midline vertical positions.

Near fixation position is fixating straight ahead at a point at some arbitrary distance less than 6 meters. Distances for near fixation usually range from 0.25 to 1 meter, with most near testing of the eye alignment performed at 0.33 meter.

Comparison of the near fixation and primary position alignments provides information about the reflex involving convergence and accommodation.

Cardinal positions are the six gaze positions that compare the horizontal and vertical eye alignments produced by the six extraocular muscles. One muscle of each eye is the prime mover to achieve the six positions. The primary position and the six cardinal positions are illustrated in Figure 8, which also indicates the prime movers of each eye (yoke muscles) that achieve these positions. Three of the cardinal positions are in dextroversion; the other three are in levoversion. In each levoversion and dextroversion, elevation and depression are compared in addition to straight right and straight left gaze.

Fig 8. Primary position and cardinal positions. The pulling power of each of the six extraocular muscles compared to its yoke is assessed by studying the movements of the eyes from the primary position into the cardinal positions. Illustration is arranged as if the patient is facing the examiner. RSR, right superior rectus; LIO, left inferior oblique; RLR, right lateral rectus; LMR, left medial rectus; RIR, right inferior rectus; LSO, left superior oblique; LSR, left superior rectus; RIO, right inferior oblique; LLR, left lateral rectus; RMR, right medial rectus; LIR, left inferior rectus; RSO, right superior oblique.

Midline positions are straight up and down from the primary position. They are of value in comparing the elevating and depressing capabilities of each eye, but they do not allow a discreet comparison of isolated muscles of each eye, as the cardinal positions do. This is because each eye has two elevator and two depressor muscles, and both effectively move the eye in a vertical plane away from the primary position. The midline position is all-important for assessing horizontal alignment change as the eyes move in the vertical plane; this change consists of the A and V patterns.

Eye position relative to the position of the upper lid is of interest. Normally, the upper lid follows the vertical eye movements, the eye maintaining approximately the same relative position to the superior limbus during movement. However, during sleep the levator muscle becomes atonic, permitting the lid to cover the eye; the eyes are usually elevated and diverged (Bell's phenomenon), and this movement is simulated by forced closure of the eyelids. Prying the eyelids apart as the patient attempts to forcibly close them reveals the eyes to be markedly elevated.

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REFERENCES

1. Fink WH: Surgery of Oblique Muscles, p 296. Springfield, IL, Charles C Thomas, 1951

2. Harada M, Ito Y: Surgical correction of cyclotropia. Jpn J Ophthalmol 8:24, 1964

3. Jampel RS: The action of the superior oblique muscle. Arch Ophthalmol 75:535, 1966

4. Jampel RS: The fundamental principle of the action of the oblique ocular muscles. Am J Ophthalmol 69:623, 1970

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