2
Anatomy and Physiology
of Eye Movements
Kenneth W. Wright
OCULAR POSITION
Within the orbit, the eye is suspended by six extraocular muscles
(four rectus muscles and two oblique muscles), suspensory ligaments, and surrounding orbital fat (Fig. 2-1). A tug-of-war exists
between the rectus and oblique muscles. The four rectus
muscles insert anterior to the equator, and pull the eye posteriorly, while the two oblique muscles insert posterior to the
equator providing anterior counterforces. Posterior orbital fat
also pushes the eye forward. If rectus muscle tension increases,
the eye will be pulled back causing enophthalmos and lid fissure
narrowing. Simultaneous cocontraction of the horizontal rectus
muscles in Duane’s syndrome, for example, can cause significant lid fissure narrowing and enophthalmos. In contrast,
decreased rectus muscle tone causes proptosis and lid fissure
widening. Conditions such as muscle palsies or a detached
rectus muscle allow the eye to move forward and result in lid
fissure widening. Rectus muscle tightening procedures such as
resections tend to cause lid fissure narrowing whereas loosening procedures such as rectus recessions induce lid fissure
widening. When the eye is looking straight ahead with the visual
axis parallel to the sagittal plane of the head, the eye is in
primary position. The vertical rectus muscles follow the orbits
and diverge from the central sagittal plane of the head by 23°.
Thus, the visual axis in primary position is 23° nasal to the
muscle axis of the vertical rectus muscles (Fig. 2-2). This discrepancy between the vertical rectus muscle axis and the visual
axis of the eye explains the secondary and tertiary functions of
the vertical rectus muscles (see muscle functions, following).
24
Whitnall's lig.
Superior oblique m.
Levator palpebrae
Müller's m.
Superior rectus m.
Intraconal fat
Lateral rectus m.
Inferior rectus m.
Lockwood's lig.
Extraconal fat
Inferior oblique m.
FIGURE 2-1. Side view of extraocular muscles. Note that the rectus
muscles pull the eye posteriorly while the oblique muscles pull the eye
anteriorly.
FIGURE 2-2. Diagram shows visual axis versus muscle/orbital axis. Note
that the visual axes parallel the central sagittal plane, while the orbital
axis of each eye diverges 23° from the visual axis.
25
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handbook of pediatric strabismus and amblyopia
The term position of rest refers to the position of the eyes when
all the extraocular muscles are relaxed or paralyzed. Normally,
the position of rest is divergent (i.e., exotropic), with the visual
axis in line with the orbital axis. The eyes of a patient under
general anesthesia are usually deviated in a divergent position.
OCULAR MOVEMENTS
Ductions
The term ductions is used to describe monocular eye movements without regard for the movement of the fellow eye (Fig.
2-3). Ductions result from an extraocular muscle contraction
A
B
E
C
F
D
G
FIGURE 2-3A–G. Diagram of ductions, which are monocular eye
movements.
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chapter 2: anatomy and physiology of eye movements
TABLE 2-1. Extraocular Muscles.
Muscle
Medial
rectus
Lateral
rectus
Superior
rectus
Approximate
muscle
length
(mm)
Origin
40
40
40
Annulus
of Zinn
Annulus
of Zinn
Annulus
of Zinn
Anatomic
insertion
(mm)
Tendon Arc of
length contact
(mm)
(mm)
Action
from
primary
position
5.5
4
6
Adduction
7.0
8
10
Abduction
8.0
6
6.5
6.5
7
7
26
12
1
15
Inferior
rectus
40
Annulus
of Zinn
Superior
oblique
32
Inferior
oblique
37
Orbit apex From
above
temporal
annulus
pole of
of Zinn
superior
rectus to
within
6.5 mm
of optic
nerve
Lacrimal
Macular
fossa
area
Elevation
Adduction
Intorsion
Depression
Adduction
Extorsion
Intorsion
Depression
Abduction
Extorsion
Elevation
Abduction
that pulls the scleral insertion site toward the muscle’s origin
while the opposing extraocular muscle simultaneously relaxes.
The contracting muscle is referred to as the agonist and the
relaxing muscle as the antagonist. An upward movement of an
eye is referred to as supraduction or sursumduction, a downward movement is termed infraduction or dorsumduction, a
nasal-ward movement is termed adduction, and a temporal
movement is termed abduction. Torsional rotations (twisting
movements) are known as cycloductions, with incycloduction
(intorsion) referring to a nasal rotation of the 12 o’clock position
of the cornea and excycloduction (extorsion) referring to a temporal rotation of the 12 o’clock position.
Muscle Action Versus Field of Action
The terms “muscle action” and the “field of action” are often
confused. Muscle action refers to the effect of muscle contraction on the rotation of the eye when the eye starts in primary
position. Table 2-1 lists the muscle actions of each extraocular
muscle. Horizontal rectus muscles have but one action: horizontal rotation of the eye. Vertical rectus and oblique muscles,
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handbook of pediatric strabismus and amblyopia
however, have three actions: vertical, horizontal, and torsional.
The most robust action is termed the primary action, followed
by the less obvious secondary and tertiary actions. It is important to remember the classic descriptions of primary, secondary
and tertiary muscle actions as they relate to the eye when it is
in primary position.
In contrast, the field of action of a muscle is the position of
gaze when an individual muscle is the primary mover of the eye.
Granted, virtually all eye movements are the result of combined
contraction and relaxation of multiple muscles, but there are
eight positions of gaze where one muscle provides the dominant
force (Fig. 2-4). For example, when one looks up, the brain
recruits both the superior rectus and the inferior oblique
muscles. Looking up and nasal, however, is the primary function of the inferior oblique muscle, so this is the field of action
of the inferior oblique muscle. A muscle’s function is best evaluated by having the patient look into the field of action of the
FIGURE 2-4. Diagram of the field of action of the extraocular muscles.
Arrows point to the quadrant where the specified muscle is the major
mover of the eye. SR, superior rectus; IR, inferior oblique; MR, medial
rectus; SO, superior oblique; IO, inferior oblique; IR, inferior rectus; LR,
lateral rectus.
chapter 2: anatomy and physiology of eye movements
29
muscle. Thus, even though the secondary action of the inferior
oblique muscle is abduction, evaluate inferior oblique function
by having the patient look “up and nasal.” A patient with an
inferior oblique palsy will show limitation of eye movement up
and nasal. Note, for straight upgaze, the superior rectus muscle
is the major elevator, and for straight down-gaze the inferior
rectus is the major depressor, with the oblique muscles contributing little.
Smooth Pursuit Versus Saccadic Eye Movements
There are two basic forms of eye movements: smooth pursuit
and saccadic. Smooth pursuit eye movements are generated in
the occipital parietal temporal cortex, with the right cortex controlling movements to the right and the left cortex controlling
movements to the left. In humans, smooth pursuit first occurs
at 4 to 6 weeks of age. These are slow accurate eye movements
requiring visual feedback from central foveal fixation. Smooth
pursuit eye movements can follow visual targets moving at
velocities up to 30° per second (30°/s). Clinically, accurate
smooth pursuit indicates central fixation and in preverbal children is an indication of good vision.
Saccadic movements are rapid eye movements with velocities usually ranging from 200° to 700°/s, but saccades have been
recorded up to 1000°/s. The peak velocity increases as the amplitude of the movement increases, and this relationship is termed
the main sequence. Saccades are movements used to keep up
with targets moving too fast for smooth pursuit and for quick
refixation from one target to another. Saccadic eye movements
develop before smooth pursuits, occurring as early as 1 week of
age. Saccadic eye movements are generated in the frontal lobes
and are under contralateral control; that is, right frontal lobe
stimulation will result in a saccadic eye movement to the left.
Saccadic movements can be voluntarily initiated, but they are
not voluntarily controlled, and there is no significant visual
feedback to adjust the amount of movement. It is thought that
the amplitude of a saccadic movement is preprogrammed based
on the degree of retinal eccentricity of the target; this is why
saccadic movements are termed ballistic, analogous to the ballistic trajectory of a cannon ball. The neuronal signal that initiates a saccade consists of a burst of high-frequency discharge or
pulse to the agonist and inhibition of the antagonist. Because all
neurons available are activated for eye movements greater than
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handbook of pediatric strabismus and amblyopia
5°, the magnitude of a saccade is determined by the duration of
the pulse. At the end of a saccade, tonic neuronal firing of the
agonist and antagonist muscles occurs to hold the eye position
referred to as the step. Vision during a saccadic eye movement
is suspended or suppressed. Some have used the term saccadic
omission for the process of cortical suppression.1 A tremendous
force is required to produce a saccadic eye movement; therefore,
the presence of saccadic eye movements indicates “good” muscle
function. Only rectus muscles generate saccadic eye movements. When evaluating a patient with limited ductions, look for
the presence of a normal saccadic eye movement into the field
of limited ductions. If there is a brisk saccade in the direction of
the limitation, this indicates good muscle function and suggests
the limited movement is caused by restriction, not a muscle
paresis.
Optokinetic nystagmus (OKN) can be generated by a slowly
rotating drum with stripes and used to evaluate smooth pursuit
and saccadic eye movements. As the drum rotates toward the
patient’s right, there is a smooth pursuit eye movement to the
right to follow the stripe. As the end of the stripe passes, there
is a fast saccadic movement to the left to refixate on the next
stripe. At target velocities less than 30°/s, smooth pursuit keeps
pace with the target. At velocities between 30° and 100°/s,
smooth pursuit movements progressively lag behind the target.
At velocities greater than 100°/s, OKN is not evoked. OKN can
be used to evaluate saccadic and smooth pursuit eye movements. Look at the fast phase of OKN to evaluate saccadic movements and the slow phase to evaluate smooth pursuit.
ANATOMY OF THE EYE MUSCLES
Rectus Muscles
The four rectus muscles originate at the orbital apex at the
annulus of Zinn and course anteriorly to insert on the anterior
aspect of the globe. The “straight” course of the rectus muscles
gives rise to the term rectus. The rectus muscle insertions form
a progressive spiral termed the spiral of Tillaux around the
corneal limbus. The medial rectus muscle is the closest to the
limbus (5.5 mm), then the inferior rectus (at 6.5 mm), the lateral
rectus (at 7.0 mm), and the superior rectus is the furthest from
the limbus (8.0 mm). The muscle–scleral insertion line has
chapter 2: anatomy and physiology of eye movements
31
FIGURE 2-5. Diagram of distance of the rectus muscle insertions from
the limbus (in millimeters, mm). Note that the medial rectus muscle
inserts closest to the limbus and the distances increase, going counterclockwise from the medial rectus toward the superior rectus, which
inserts furthest from the limbus.
a horseshoe configuration with the rounded apex pointing
toward the cornea (Fig. 2-5). One can remember this as the horseshoes are always galloping toward the cornea. The scleral thickness behind the rectus insertions is the thinnest of the eye, being
only 0.3 mm thick. Hooking a rectus muscle requires passing
the hook several millimeters behind the central muscle insertion to clear the posterior aspect of the horseshoe insertion. The
widths of the insertions are all approximately 10 mm, and the
distance between insertions or intermuscle spacing is only 6 to
8 mm. Because of the proximity of the rectus muscle insertions,
it is easier than you might think to hook the wrong muscle
during strabismus surgery. An important number to remember
is the rectus muscle length, which is 40 mm for all rectus
muscles and is also the length of the orbit. Rectus muscles are
innervated from the intraconal side of the muscle belly at the
junction of the anterior two-thirds and posterior one-third of the
muscle.
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handbook of pediatric strabismus and amblyopia
HORIZONTAL RECTUS MUSCLES
The horizontal rectus muscles consist of the medial and lateral
rectus muscles. In primary position, each muscle has one action:
the medial rectus is an adductor and the lateral rectus is an
abductor (Fig. 2-6). When the eye elevates or depresses away
from primary position, however, the horizontal rectus muscles
take on secondary vertical functions. When the eye is “up,” the
horizontal rectus muscles take on a secondary action of supraduction, and when the eye is “down,” the secondary action is
infraduction (Fig. 2-7). In addition, if one surgically transposes a
horizontal rectus muscle insertion up, the muscle becomes an
elevator in addition to the horizontal function. Supraplacing
the horizontal rectus insertions during strabismus surgery will
induce a hyperdeviation whereas infraplacement induces a
hypodeviation. Vertically displacing the medial and lateral
rectus muscle insertion is an excellent way to correct small vertical deviations when performing a recession/resection procedure. In Duane’s syndrome, the common finding of upshoot
and downshoot is probably caused by the secondary elevator
and depressor actions of the cocontracting horizontal rectus
FIGURE 2-6. Diagram of simple function of the medial rectus (MR) and
lateral rectus (LR) muscle with the eye in primary position.
chapter 2: anatomy and physiology of eye movements
33
A
B
C
FIGURE 2-7A–C. Diagram of secondary actions of the medial rectus
when the eye rotates up or down. These secondary actions also relate to
the lateral rectus. (A) Globe rotated superiorly; now the medial rectus acts
as an elevator in addition to its adduction or horizontal function. (B) In
the center part of the figure, the medial rectus is a pure adductor. (C)
Globe rotated down; in this position, the medial rectus acts as a depressor and an adductor.
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handbook of pediatric strabismus and amblyopia
muscles. Remember, the secondary vertical functions of the
horizontal rectus muscles occur only when the eye is rotated
vertically off primary position.
MEDIAL RECTUS MUSCLE
The medial rectus muscle is innervated by the lower division of
the oculomotor nerve (third cranial nerve) and, in primary position, is a pure adductor. The medial rectus is uniquely diminutive. It has the shortest arc of scleral contact (6 mm) and the
shortest tendon length of the rectus muscles (4 mm). The inferior oblique muscle actually has the shortest tendon (1 mm)
of the extraocular muscles, but it is not a rectus muscle. (Be
careful; this could be the basis of a trick question.) Of the
extraocular muscles, the medial rectus inserts closest to the
limbus and is therefore susceptible to insult during anterior
segment surgical procedures. Inadvertent removal of the medial
rectus muscle is a well-known complication of pterygium
removal. The medial rectus is also unique, as it is the only rectus
muscle without fascial connections to an adjacent oblique
muscle. This lack of oblique muscle connection makes the
medial rectus the most difficult to surgically retrieve if lost.
Once disinserted, the medial rectus is free to retract completely
off the globe into the orbital fat, making retrieval extremely difficult and, in some cases, almost impossible.
LATERAL RECTUS MUSCLE
The lateral rectus muscle is innervated by the sixth cranial nerve
and is a pure abductor. In direct contrast to the medial rectus
muscle, the lateral rectus has the longest tendon (8 mm) and the
longest arc of scleral contact (10 mm) of the rectus muscles. Be
careful, the “longest” cited above refers to only rectus muscles,
as the superior oblique tendon has the longest arc of contact and
tendon length of all the extraocular muscles. (This could be the
source of another trick question.) The long arc of contact occurs
because the lateral rectus muscle initially has a divergent course
following the lateral wall of the orbit. Then, in the anterior orbit,
it turns nasally, wrapping around the globe to its scleral insertion point (see Fig. 2-6). This temporal to nasal wrap around the
globe accounts for the long arc of contact. The inferior border of
the lateral rectus muscle courses above the inferior oblique
insertion, and there are connective tissue bands connecting the
lateral rectus muscle to the inferior oblique muscle.13 This is an
important anatomic relationship, because a lost lateral rectus
chapter 2: anatomy and physiology of eye movements
35
muscle will come to rest at the insertion of the inferior oblique
muscle. The surgeon can often find a lost lateral rectus muscle
by tracing the inferior oblique muscle back to its insertion.
VERTICAL RECTUS MUSCLES
EA
XIS
VISUAL AXIS
The superior and inferior rectus muscles are the vertical rectus
muscles and are the major elevators and depressors of the eye,
respectively. The vertical rectus muscles have secondary and
tertiary actions because, in primary position, the muscle axis
is 23° temporal to the visual axis of the eye (Figs. 2-2, 2-8A).
MU
SC
L
23°
TEMPORAL
VI
MUSUA
SC L &
LE
A
XIS
NASAL
MU
SC
LE
AX
IS
A
B
VISUAL AXIS
C
FIGURE 2-8A–C. Functions of the vertical rectus muscles with the eye
in various positions of gaze. (A) The eye is in primary position with the
visual axis 23° nasal to the muscle axis. (B) The eye is abducted 23° from
the primary position, and the visual axis is in line with the muscle axis.
(C) The eye is abducted more than 23° from the primary position, and the
visual axis is now temporal to the muscle axis.
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handbook of pediatric strabismus and amblyopia
Their secondary action is adduction, and it occurs because the
vertical rectus muscles pull the front of the eye nasal to the
visual axis. Tertiary actions are torsional, consisting of intorsion for the superior rectus muscle and extorsion for the
inferior rectus muscle. These secondary and tertiary muscle
actions are dependent on eye position. If the eye is abducted
23°, for example, the muscle and visual axes will be in line, and
the vertical rectus muscles lose their secondary and tertiary
actions, leaving only their vertical actions (Fig. 2-8B). In this
position of 23° abduction, the superior rectus acts purely as an
elevator, and the inferior rectus purely as a depressor. With
further abduction past 23°, the secondary and tertiary actions
of the vertical rectus muscles return, but they are different.
The secondary action for both vertical rectus muscles becomes
abduction, and the tertiary functions reverse, becoming extorsion for the superior rectus and intorsion for the inferior rectus
muscle (Fig. 2-8C).
SUPERIOR RECTUS MUSCLE
The upper division of the oculomotor nerve innervates the
superior rectus muscle. It is the major elevator of the eye,
and its actions include supraduction (primary), adduction
(secondary), and intorsion (tertiary). The superior rectus
muscle overlies the superior oblique tendon and has connective tissue connections to the superior oblique tendon below
and the levator palpebrae muscle above (Fig. 2-9). This anatomic relationship to the levator palpebrae is important because
a large superior rectus recession can cause upper lid retraction and lid fissure widening. On the other hand, a superior
rectus resection pulls the upper lid down, resulting in lid fissure
narrowing. Lid fissure changes associated with superior rectus
surgery can be minimized by surgically removing the fascial
connections between the levator and the superior rectus
muscles.
INFERIOR RECTUS MUSCLE
The inferior rectus muscle is innervated by the lower division
of the oculomotor nerve and is the principal depressor of the
eye. Actions of the inferior rectus muscle include infraduction
(primary), adduction (secondary), and extorsion (tertiary). The
inferior rectus is sandwiched between the inferior oblique below
chapter 2: anatomy and physiology of eye movements
37
FIGURE 2-9. Diagram of the eye and orbit from a top view looking down
on the superior rectus (SR) muscle. Note that the superior rectus muscle
overlies the superior oblique (SO). T, temporal; N, nasal.
and the sclera above (Fig. 2-10). The fascial connection between
the inferior rectus muscle, the inferior oblique muscle, and the
lower lid retractors (capsulopalpebral fascia) is termed Lockwood’s ligament (Fig. 2-11).17 These fascial connections are
responsible for the eyelid changes that often occur after inferior
rectus surgery. An inferior rectus recession results in lower lid
retraction with lid fissure widening, and a resection causes lid
advancement with lid fissure narrowing. If the inferior rectus is
inadvertently disinserted or lost during surgery, these connections will hold the inferior rectus to the inferior oblique and
keep it from retracting posteriorly. The surgeon who is in search
of a lost inferior rectus muscle can usually find it lying between
the inferior oblique and sclera.
FIGURE 2-10. Diagram of the eye and orbit viewed from below. Note
that the inferior oblique (IO) underlies the inferior rectus (IR) muscle.
Conjunctiva
Tarsus
Fornix
Tenon's capsule
Orbicularis m.
Inf. rectus m.
ITM
CPF
Orbital septum
CPH
Lockwood's lig.
Inf. oblique m.
38
chapter 2: anatomy and physiology of eye movements
39
FIGURE 2-12. Diagram of the superior oblique (SO) muscle and tendon.
The functional muscle axis extends from the trochlea to the superior
oblique insertion. The muscle axis is 54° nasal to the visual axis.
OBLIQUE MUSCLES
Like the vertical rectus muscles, the oblique muscles have
primary, secondary and tertiary actions. In the case of the
oblique muscles, this is because the functional muscle axis is
approximately 50° nasal to the visual axis, and the insertion
extends posterior to the equator of the eye (Figs. 2-12, 2-13). By
FIGURE 2-11. Diagram of the relationship between the inferior rectus,
inferior oblique, lower lid retractors, and Lockwood’s ligament. The inferior tarsal muscle (ITM) courses from the posterior border of the tarsus
toward the inferior oblique muscle. It then passes between the inferior
oblique muscle and the inferior rectus muscle to insert at the capsulopalpebral head (CPH). The CPH extends posteriorly to connect the inferior oblique to the inferior rectus muscle. The capsulopalpebral fascia
(CPF) is the anterior extension of the CPH and courses from the inferior
oblique anteriorly to the tarsus along with the ITM. “Lockwood’s ligament” (Lockwood’s lig.) consists of these fascial attachments that connect the lower lid, inferior rectus, and inferior oblique muscles.
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handbook of pediatric strabismus and amblyopia
FIGURE 2-13. Diagram of the inferior oblique (IO) from a view from
below. The inferior oblique muscle axis is 51° nasal to the visual axis.
comparing Figures 2-12 and 2-13, one can see that the oblique
muscles have an almost identical functional course with both
muscle axes at approximately 50°. The posterior muscle–scleral
insertion gives the oblique muscles their seemingly paradoxical
vertical functions, with the superior oblique being a depressor
and the inferior oblique an elevator. The oblique muscles have
no anterior ciliary blood supply, and they do not contribute to
the anterior segment circulation. Remember that the “oblique
muscles always course below the corresponding vertical rectus
muscle” (Fig. 2-14).
SUPERIOR OBLIQUE MUSCLE
The primary action of the superior oblique muscle is intorsion,
but it also acts as a depressor (secondary) and an abductor
(tertiary). Depression and abduction occur as the back of the eye
is pulled up and in toward the trochlea. The superior oblique
chapter 2: anatomy and physiology of eye movements
41
muscle originates at the orbital apex just above the annulus of
Zinn and gradually becomes tendon at the trochlea (see Fig.
2-12). After passing through the trochlea, the superior oblique
tendon reverses course and turns in a posterior temporal direction to pass under the superior rectus muscle to insert on sclera
along the temporal border of the superior rectus muscle (Fig.
2-14). Even though the anatomic origin is at the apex of the orbit,
the functional origin of the superior oblique is at the trochlea.
This tendon is the longest tendon of the extraocular muscles,
26 mm in length. The tendon insertion fans out broadly under
the superior rectus muscle, extending from the temporal pole
of the superior rectus muscle to 6.5 mm from the optic nerve.13
Fascial attachments connect the superior oblique tendon to the
superior rectus muscle above and to the sclera below.13 The
tendon insertion can be functionally divided into two basic
parts: the anterior one-third and the posterior two-thirds.
Posterior fibers are responsible for depression and abduction
whereas tendon fibers anterior to the equator are devoted to
intorsion. This distinction between anterior and posterior
superior oblique tendon fibers is important because one can
FIGURE 2-14. Diagram of posterior anatomy of the eye and muscles.
Note the proximity of the inferior oblique to the macula and vortex veins
(vv). The posterior aspect of the superior oblique insertion is in proximity to the superior temporal vortex vein and is approximately 6 to 8 mm
from the optic nerve.
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handbook of pediatric strabismus and amblyopia
manipulate these functions surgically to correct specific motility disorders. The Harada–Ito procedure, for example, involves
tightening the anterior fibers of the superior oblique tendon.
Because the anterior tendon fibers intort the eye, the Harada–Ito
procedure can be used to treat extorsion associated with superior oblique palsy.
The trochlear nerve innervates the superior oblique muscle
at its midpoint from outside the muscle cone. The superior
oblique muscle is, in fact, the only eye muscle innervated on the
outer surface of the muscle belly. This unique innervation
explains why a retrobulbar anesthetic block results in akinesia
of all the eye muscles except the superior oblique muscle.
TROCHLEA
The trochlea (Latin for pulley) is a cartilaginous U-shaped structure attached to the periosteum that overlies the trochlear fossa
of the frontal bone in the superior nasal quadrant of the orbit. It
has been taught that the superior oblique tendon moves through
the trochlea much like a rope through a pulley. Anatomic
studies have shown, however, that tendon movement is not that
simple. Within the trochlea is a connective tissue capsule with
connective tissue bands that unite the superior oblique tendon
to the surrounding trochlea (Fig. 2-15).46 Some of the tendon
slackening distal to the trochlea may come from a telescoping
elongation of the central tendon (Fig. 2-16).19 This telescoping
elongation of the tendon appears to be caused by movement of
the central tendon fibers that have scant interfiber connections.
Thus, the mechanism for tendon movement is complex, with
at least two mechanisms: (1) tendon movement through
the trochlea (pulley and a rope) and (2) tendon elongation
(telescoping).
INFERIOR OBLIQUE MUSCLE
It is the principal extortor of the eye; however, other actions
include elevation (secondary) and abduction (tertiary). The inferior oblique muscle originates at the lacrimal fossa located at
the anterior aspect of the inferior nasal quadrant of the orbit (see
Fig. 2-13). Starting at the lacrimal fossa, the inferior oblique
muscle courses posteriorly and temporally underneath the inferior rectus muscle to its scleral insertion, which is adjacent to
the inferior border of the lateral rectus muscle (see Fig. 2-14).
The inferior oblique muscle has fascial connections to the lower
chapter 2: anatomy and physiology of eye movements
43
A
B
FIGURE 2-15A–B. Histology of the trochlea. (A) Low-magnification cross
section of midtrochlea. H&E stain. Note horseshoe shape of cartilaginous
tissue and the fibrous connective tissue ring that surrounds the superior
oblique muscle. At this cross section, the superior oblique is two-thirds
muscle and one-third tendon. (B) High-magnification cross section of
superior oblique muscle in midtrochlea shows fibrous connective tissue
ring connecting to muscle via fine fascial septae.
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handbook of pediatric strabismus and amblyopia
C
D
FIGURE 2-15C–D. (C) Low-magnification cross section of superior
oblique tendon exiting the trochlea. Note small area of cartilage and larger
ring of fibrous connective tissue that surrounds the superior oblique
tendon as the tendon capsule. At this section, the superior oblique is onethird muscle and two-thirds tendon. (D) High magnification of the superior oblique tendon exiting the trochlea. Note the superior oblique tendon
capsule consists of circumferential onionskin layers of fibrous connective
tissue. The tendon capsule is attached to the superior oblique tendon
capsule by circumferential connective tissue fibers. (From Wright et al.,
Ref. 46, with permission.)
chapter 2: anatomy and physiology of eye movements
45
FIGURE 2-16. Diagram of anatomy of the trochlea. Note the central
fibers of the tendon expand and retract more than the peripheral tendon
fibers. (From Ref. 19, with permission.)
border of the lateral rectus muscle and to the overlying inferior
rectus muscle via Lockwood’s ligament (see Fig. 2-11). When the
inferior oblique muscle contracts, it pulls the back of the eye
down and in toward the insertion at the lacrimal fossa. This
action produces elevation, abduction, and extorsion (Fig. 2-14).
Important structures near the inferior oblique insertion include
the macula and inferior temporal vortex vein (Fig. 2-14).
The inferior oblique muscle has only 1 mm of tendon at its
insertion.
The inferior oblique muscle is innervated by the inferior
branch of the third nerve at a point just lateral to the inferior
rectus muscle. Innervation occurs at the posterior aspect of the
inferior oblique muscle belly, and the nerve is accompanied by
blood vessels forming a neurovascular bundle. This neurovascular bundle is surrounded by an inelastic capsule of collagen
tissue that protects the inferior oblique nerve from damage
caused by stretching.39 The neurovascular bundle with its insertion into the posterior aspect of the muscle is an important
structure in regard to inferior oblique surgery. Anterior transposition of the inferior oblique muscle is an effective surgical
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handbook of pediatric strabismus and amblyopia
procedure used to treat inferior oblique muscle overaction;
however, the complication of postoperative limited elevation
has been reported.5,25,26,47 This complication is caused by anteriorizing the posterior muscle fibers at, or anterior to, the inferior
rectus muscle insertion, because this tightens the inelastic neurovascular bundle.38 The tight neurovascular bundle acts as the
functional origin of the inferior oblique muscle and changes
the action of the inferior oblique muscle from an elevator to
a depressor (Fig. 2-17A).16 This author has coined the term
J-deformity for this acute bend of the anteriorized inferior
oblique.47 When the patient looks up, the inferior oblique muscle
contracts along with the superior rectus muscle, but the anteri-
Inferior oblique
muscle
Neurofibrovascular
bundle
Maxillary bone
Inferior rectus
muscle
FIGURE 2-17A,B. (A) Diagram of inferior oblique muscle anteriorization
with “J-deformity.” The J-deformity is caused by anterior placement of
the posterior inferior oblique muscle fibers to the level of the inferior
rectus muscle insertion. Because the neurovascular bundle of the inferior
oblique muscle inserts in the posterior muscle belly, anteriorization of
the posterior muscle fibers produces a tight neurovascular bundle; this
causes limited elevation of the eye as active contraction of the anteriorized inferior oblique muscle pulls against the tight neurovascular
bundle.16
chapter 2: anatomy and physiology of eye movements
47
Vortex
vein
Inferior oblique
muscle
Inferior rectus
muscle
FIGURE 2-17A,B. (B) Diagram of the “graded anteriorization” technique
described by Guemes and Wright that is effective in reducing inferior
oblique overaction but avoids the postoperative complication of limited
elevation.16 The new inferior oblique muscle insertion is shown being
placed 1 mm behind the inferior rectus muscle insertion, and the posterior muscle fibers are placed an additional 4 to 5 mm further posterior,
and parallel to the inferior rectus muscle axis. Note that the posterior
placement of the posterior muscle fibers avoids the J-deformity. By
keeping the posterior muscle fibers posterior to the anterior fibers and
avoiding the J-deformity, the neurovascular bundle remains loose, preventing postoperative limitation of elevation.
orized inferior oblique muscle now depresses the eye and limits
elevation; this is an active leash caused by inferior oblique contraction, and forced ductions on patients with this complication
of limited elevation often show only slight restriction to supraduction. The complication of limited elevation can be avoided
while maintaining excellent results by anterior transposition of
the anterior muscle fibers at, or a millimeter or two behind, the
inferior rectus insertion. Be sure to keep the posterior fibers
back, behind the anterior fibers. Placing the posterior muscle
fibers several millimeters posterior to the inferior rectus insertion and in line with the inferior rectus muscle prevents the
J-deformity (Fig. 2-17B).16,47
48
handbook of pediatric strabismus and amblyopia
EXTRAOCULAR MUSCLE HISTOLOGY
As are other skeletal muscles, extraocular muscles are made up
of striated fibers that, on electron microscopy, show the typical
banding pattern of sarcomeres with overlapping threads of actin
and myosin. Also resembling other muscles, the strength of an
extraocular muscle contraction is dependent on the number of
motor units activated (recruitment) and the frequency of muscle
fiber stimulation. Extraocular muscles, however, do show some
interesting anatomic and physiological differences from other
skeletal muscles. The fibers are variable in size, are considerably
smaller, and contract more than 10 times faster than other
skeletal muscle. Extraocular muscle fibers are innervated at a
high nerve fiber to muscle fiber ratio (almost 1:1), whereas other
skeletal muscle can have up to 100 muscle fibers for every nerve
fiber. This rich innervation, teamed with a fast muscle reaction
time, contributes to the precision, accuracy, and control of eye
movements.
Another distinction of extraocular muscles is the presence
of two distinct muscle fiber types: fast muscle fibers and slow
muscle fibers. The fast, or twitch, fibers are single innervated
fibers (SIF), innervated by a large motor neuron with “en plaque”
neuromuscular junctions and are typical of mammalian skeletal muscle. The SIF can be classified into three types: red,
intermediate, and white. Red SIF have the highest density of
mitochondria and are the most fatigue resistant, while the white
SIF have fewer mitochondria and are less resistant to fatigue.
Intermediate and white fibers provide the high transient force
needed for the extremely fast saccadic eye movements.
Slow, or tonic muscle fibers, are multiple innervated fibers
(MIF) innervated by small-diameter motor nerves with “en
grappe” neuromuscular endings characteristic of avian and
amphibian muscles. MIF are thought to participate in smooth
pursuit movements and static muscle tone to hold and maintain
eye position, and SIF probably also play a supportive role in tonic
control of eye position and pursuit eye movements. The exact
functions of the variety of specific muscle fiber types are
unknown, and it is likely that various fibers have overlapping
functions.28
Within extraocular muscle tissue are neuromuscular
spindles that are concentrated at the muscle–tendon junction.
Neuromuscular spindles are thought to be sensory organs providing information on muscle tone to the brain.9 The exact role
chapter 2: anatomy and physiology of eye movements
49
of the muscle spindles is unknown, but they may provide proprioceptive feedback to motor centers in the brain regarding
muscle tone and eye position. Muscle spindles may explain why
many adult patients experience transient spatial disorientation
after strabismus surgery on the dominant eye.
ARCHITECTURE OF THE EXTRAOCULAR
MUSCLES AND PULLEYS
Extraocular muscles have two distinct muscle layers seen on
transverse sections (cross section). There is a peripheral layer
closest to the orbital wall called the orbital layer (OL) and an
inner layer closest to the eye globe called the global layer
(GL).33,37 OL muscle fibers contain small-diameter fibers with
many mitochondria and abundant vessels, staining dark red by
Masson’s trichrome. The GL, in contrast, contains larger fibers
with variable numbers of mitochondria and fewer vessels; it
stains bright red by Masson’s trichrome. Approximately 90% of
GL muscle fibers are fast-twitch SIF, with one-third of the SIF
being fatigue-resistant red SIF; 80% of OL muscle fibers are
twitch-generating SIF and 20% are MIF.33 In humans, OL muscle
fibers do not appear to run the entire course of the muscle and
do not insert in sclera, as there is a gradual decline in the OL in
the anterior aspect of the muscle.11,28
Elastic fibers connect the OL to a fibromuscular pulley
sleeve that surrounds each extraocular muscle close to the
muscle insertion (see Muscle Pulleys, following) (Fig. 2-18).11
There are also muscle-to-muscle-fiber junctions (myomyous
junctions) within the OL. GL fibers, on the other hand, are continuous from their origin in the orbital apex to their insertion
by tendon into sclera.28 Most GL fibers act in saccadic eye movements and function only in the field of action of the muscle
whereas OL fibers are active throughout the oculomotor range,
providing continuous muscle tone to the pulley system.7 Collins
hypothesized that OL muscle fibers might have a role in
maintaining fixation whereas GL muscle fibers participate in
dynamic eye movements.7 An alternative hypothesis proposed
by Demer is that OL muscle fibers actively control pulley position, thereby influencing the rotational force vectors during eye
movements.11,28
A
FIGURE 2-18A–C. Masson’s trichrome stain of 10-␮m-thick transverse
section of medial rectus at the level of the pulley ring of a 17-month-old
human. (A) Low power shows the overall architecture of the pulley (P)
that surrounds the medial rectus muscle. Fibers in the orbital layer (OL)
(arrowheads) insert in the pulley, shown at high power in (B). The OL
muscle layer takes the form of a C-shape and is on the left, delineated by
the large arrows; the global layer (GL) fibers are to the right. OL on the
left is shown on the bottom.
50
chapter 2: anatomy and physiology of eye movements
51
B
C
FIGURE 2-18A–C. (B) High-power magnification shows the insertion of
the OL into the pulley (taken from the upper left box on A). (C) Highpower magnification of the GL and pulley relationship. The GL does not
insert into the surrounding pulley (taken from the middle right box on
A).11,28
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handbook of pediatric strabismus and amblyopia
EXTRAOCULAR MUSCLE FASCIA
A smooth white connective tissue, Tenon’s capsule, underlies
the conjunctiva and envelops the globe and extraocular muscles.
This delicate membrane partitions the orbital contents, isolating the globe and extraocular muscles from the surrounding
orbital fat. Another fascial structure interconnected with
Tenon’s capsule is the muscle sleeve or extraocular muscle
pulley, which suspends the extraocular muscles.
Muscle Pulley (Muscle Sleeve)
Each of the rectus muscles passes through a pulley system consisting of a sleeve or ring of collagen, elastic, and smooth muscle
fibers. Previously, this structure was termed muscle sleeve. The
medial rectus muscle pulley has the most fibroelastic tissue and
smooth muscle. Muscle pulleys connect to the orbital layer (OL)
of the rectus muscle, to the orbital wall, to adjacent extraocular
muscles, and to Tenon’s capsule.10 The pulley or sleeve extends
for approximately 10 mm from the equator of the globe anteriorly to approximately 6 mm from the muscle insertion. During
strabismus surgery, one can see these bands as they connect the
surrounding muscle sleeve or pulley to the OL of the rectus
muscle. Similar to the trochlea and superior oblique tendon, the
pulleys guide the rectus muscles to their insertion point. In contrast to the superior oblique muscle, which changes direction
after passing through the trochlea, rectus muscle pulleys keep
the muscle in line with their anatomic origin. Demer has suggested that in secondary gaze positions the extraocular muscle
path is “discretely inflected by the pulley.”6 Demer et al. also
hypothesized that OL muscle fibers insert into the pulley
system and actively influence pulley position and the mechanics of ocular rotation.11,28
Tenon’s Capsule
Tenon’s capsule is a collagen-elastic tissue that is a continuous
membrane surrounding the eye and extraocular muscles.22 This
membrane separates surrounding orbital fat from the globe and
extraocular muscles. The elastic nature of Tenon’s capsule
allows free rotation of the globe and unrestricted muscle relaxation and contraction. For clinical and surgical purposes, it is
useful to subdivide it into the following categories:
chapter 2: anatomy and physiology of eye movements
53
1. Intermuscular septum
2. Anterior Tenon’s capsule
3. Posterior Tenon’s capsule
4. Check ligaments
5. Muscle sleeve (see Pulley System, earlier)
INTERMUSCULAR SEPTUM
This thin tissue lies sandwiched between the conjunctiva
and sclera, spanning between the rectus muscles (Fig. 2-19).30,40
During strabismus surgery, intermuscular septum can be identified as the white membrane on each side of the rectus muscles.
When elevated with muscle hooks, the intermuscular septum
takes on the appearance of the wings of a manta ray (Fig. 2-20).45
The intermuscular septum can be safely incised during strabismus surgery, as it is not a barrier to orbital fat.
ANTERIOR TENON’S CAPSULE
This tissue is the subconjunctival membrane anterior to the
muscle insertions. It proceeds forward with the intermuscular
septum and fuses with the conjunctiva at 2 to 3 mm posterior
to the corneal limbus (Figs. 2-18, 2-20). When suturing a muscle
during strabismus surgery, it is important to dissect anterior
Tenon’s capsule off the tendon insertion to avoid the complica-
Reflected
conjunctiva
SR
IMS
IMS
MR
LR
Anterior
Tenon's Capsule
FIGURE 2-19. Anterior ocular fascia. Intermuscular septum (IMS) is the
connective tissue that spans between the rectus muscles underneath the
conjunctiva. Anterior Tenon’s is that tissue anterior to the rectus muscle
insertions; it fuses with the conjunctiva 3 mm posterior to the limbus.
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handbook of pediatric strabismus and amblyopia
A
B
FIGURE 2-20A,B. (A) Lateral rectus muscle with intermuscular septum and
check ligaments. Check ligaments overlie the rectus muscle and connect
the muscle to the overlying conjunctiva. Intermuscular septum is seen on
either side of the lateral rectus muscle, spanning between the superior and
inferior rectus muscles. (B) Photograph shows the Jameson hook under the
lateral rectus muscle and Desmarres retractor pulling the conjunctiva
posteriorly. (Figure published with permission of J.B. Lippincott Co. from
Wright KW. Color Atlas of Ophthalmic Surgery: Strabismus. Philadelphia:
Lippincott, 1991.)
chapter 2: anatomy and physiology of eye movements
55
Anterior Tenon's
capsule
Medial rectus
Anterior ciliary
muscle
artery
FIGURE 2-21. Anterior Tenon’s capsule is the white tissue retracted
anteriorly with a small Steven’s hook (bottom left hook). During strabismus surgery, it is important to remove the anterior Tenon’s capsule to
visualize the muscle tendon for suturing. Note the anterior ciliary vessels
on the tendon insertion.
tion of a slipped muscle (Fig. 2-21). If anterior Tenon’s capsule
is left on the tendon, the surgeon may inadvertently suture
and secure anterior Tenon’s capsule, missing all or part of the
tendon. The unsuspecting surgeon then disinserts the unsutured
tendon and allows the muscle to slip posteriorly while anterior
Tenon’s capsule is placed at the intended recession site.31 A
slipped muscle is a frequent cause of unexpected overcorrection
after recession procedures, as it often goes unrecognized at the
time of surgery. Remember that some slipped muscles involve
only part of the muscle and can present as a mild overcorrection
with relatively good muscle function.48
POSTERIOR TENON’S CAPSULE
This tissue lines the posterior globe and functions to separate
orbital fat from the sclera (Fig. 2-22). Just anterior to the equator
of the eye, the four rectus muscles penetrate Tenon’s capsule and
become surrounded by intra- and extraconal orbital fat. At this
juncture, Tenon’s capsule unites with the capsule of the rectus
muscle to form a muscle pulley or muscle sleeve (see Muscle
Pulley, earlier). The muscle sleeve is an important surgical
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handbook of pediatric strabismus and amblyopia
Posterior
Tenon's capsule
Extraconal fat
Anterior Tenon's
capsule
Muscle sleeve
(pulley)
Conjunctiva
Fused anterior
Tenon's and
conjunctiva
Intraconal
fat
Medial rectus
muscle
FIGURE 2-22. Drawing of a rectus muscle showing fascial relationships.
Note that the muscle penetrates posterior Tenon’s capsule; the capsule at
this point forms a muscle sleeve or muscle pulley. Intraconal and extraconal fat are isolated from the globe by Tenon’s capsule.
landmark when looking for a slipped or lost rectus muscle. A lost
muscle is a rectus muscle that has become completely detached
from the globe because of trauma or a surgical mistake.32,48 Once
lost, the muscle will slip posteriorly within the muscle sleeve
to be surrounded by intra- and extraorbital fat. To find a lost
muscle, first find the muscle sleeve located between the intraand extraconal fat; then, carefully follow the sleeve to retrieve
the muscle. When looking for a lost medial rectus muscle, avoid
the tendency to follow the sclera posteriorly, as this leads to the
optic nerve. An important complication of attempted retrieval
of a lost medial rectus muscle is inadvertent transection of the
optic nerve that is enshrouded in postoperative scar tissue.
Together, posterior Tenon’s capsule, anterior Tenon’s
capsule, and the muscle sleeve are very important structures as
they are the barrier that keeps orbital fat from the globe and
extraocular muscles. If posterior Tenon’s capsule or muscle
sleeve is traumatically or surgically violated, fat adherence can
occur because orbital fat prolapses through the torn Tenon’s
capsule and scars to the sclera or an extraocular muscle (Fig.
2-23). The scarring of orbital fat produces a restrictive scar,
which extends from the periosteum to the eyeball. As the scar
chapter 2: anatomy and physiology of eye movements
57
contracts over weeks to several months, the scar pulls the eye,
producing a restrictive strabismus associated with limitation of
eye movements. Fat adherence can occur as a complication of
almost any extraocular surgery (e.g., strabismus surgery, retina
surgery) or periocular trauma.31,49 Extreme care must be taken
when operating in the area of orbital fat, which starts 10 mm
posterior to the limbus. Once fat adherence occurs, it is almost
impossible to correct. Surgically induced fat adherence can
usually be avoided if the surgeon carefully dissects close to
muscle belly or sclera, thus preserving the integrity of the overlying posterior Tenon’s capsule and muscle sleeve.
CHECK LIGAMENTS
These are fine falciform webs that overlie the rectus muscles
and join the muscle capsule with overlying bulbar conjunctiva
A
B
FIGURE 2-23A,B. Diagram modified after Parks and published in Ophthalmology by Wright (1986)49 shows the pathophysiology of the fat
adherence syndrome. (A) Normal anatomy with orbital bone, periorbita,
extraconal fat, muscle, and intermuscular septum. Note that the fat is
isolated from muscle and sclera by intact Tenon’s capsule and intermuscular septum. (B) Violation of Tenon’s capsule with fat adherence to the
globe and muscle (to right).
58
handbook of pediatric strabismus and amblyopia
at the muscle tendon (see Fig. 2-20). More posteriorly, check ligaments are probably the bands that connect the OL muscle fibers
to the surrounding muscle sleeve (muscle pulley). In the case of
the superior and inferior rectus muscles, check ligaments also
connect to the levator muscle and lower lid retractors, respectively. A recession or resection of vertical rectus muscles requires
removal of these ligaments to avoid lid fissure changes after
surgery.
VASCULAR SUPPLY TO
THE ANTERIOR SEGMENT
The anterior segment and iris are supplied by the anterior ciliary
arteries, conjunctival vessel, and the long posterior ciliary
arteries (Fig. 2-24). Approximately 50% of the anterior segment
circulation comes from the long posterior ciliary arteries and
FIGURE 2-24. Diagram of circulation of the anterior segment with the
rectus muscle supplying the anterior ciliary arteries (aa); the deep long
posterior arteries are also shown. (Figure published with permission of
J.B. Lippincott Co. from Wright KW. Color Atlas of Ophthalmic Surgery:
Strabismus. Philadelphia: Lippincott, 1991.47)
chapter 2: anatomy and physiology of eye movements
44
59
50% from the anterior ciliary arteries. The conjunctival vessels
also contribute to anterior segment circulation.14 Anterior
ciliary arteries and the conjunctival vessels merge at the limbus
to form the episcleral limbal plexus.27 These vessels in turn
connect with the major arterial circle of the iris, which is also
fed by the two long posterior ciliary arteries. The superior rectus,
inferior rectus, and medial rectus muscles have at least two anterior ciliary arteries and are major contributors to the anterior
segment circulation.18 The lateral rectus has a single anterior
ciliary artery and, of the four recti muscles, the lateral rectus
probably provides the least in the way of anterior segment circulation.20,41 The oblique muscles do not have anterior ciliary
arteries, and they do not contribute to the anterior segment
circulation.
Iris angiograms can be used to assess anterior segment
circulation in blue-eyed patients. Removal of a vertical rectus
muscle will cause hypoperfusion in that area that relates to the
vascular input.18 It is interesting that this hypoperfusion lasts
only 1 to 2 months because its collateral circulation and vasodilatation will replenish the hypoperfused area.45 Additionally,
infants and children do not typically show hypoperfusion even
when multiple rectus muscles are removed. Removal of a rectus
muscle during strabismus surgery will permanently interfere
with vascular supply of the anterior ciliary arteries unless the
surgery is performed specifically to maintain anterior segment
circulation. Surgeries have been devised that attempt to maintain anterior segment circulation despite manipulations of the
muscle position.24,45 Iris angiograms can be used to document
anterior segment blood flow from the anterior ciliary arteries in
nonhuman primates. A muscle-to-sclera plication developed by
this author (Wright plication) is designed to tighten a rectus
muscle but spare the anterior ciliary arteries. Instead of resecting the muscle, as is done in the standard muscle tightening procedure, the Wright plication folds the muscle, suturing muscle
to sclera without disrupting the anterior ciliary vessels. Figure
2-25 shows an iris angiogram after inferior rectus muscle plication and surgical removal of the other three rectus muscles in a
nonhuman primate. The iris angiogram demonstrates intact perfusion from the inferior rectus muscle and hypoperfusion superiorly because the arteries of the other three rectus muscles had
been sacrificed on surgical removal.
Anterior segment ischemia can be a consequence of
strabismus surgery, most often after a three- or four-muscle
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handbook of pediatric strabismus and amblyopia
FIGURE 2-25. Monkey fluorescein iris angiogram, early phase after
Wright plication of the inferior rectus muscle and removal of the other
three rectus muscles. Note the hypoperfusion superiorly (black area of
iris) as the medial, lateral, and superior rectus muscles have been
removed. The perfusion from the inferior rectus remains intact after the
Wright plication because fluorescence is seen inferiorly (white vessels on
iris).46
transposition procedure.35,42 This is a rare occurrence, as collateral circulation from the long posterior ciliary arteries can
usually maintain adequate perfusion to the anterior segment
even when three or four rectus muscles have been removed.36
Factors that predispose to anterior segment ischemia include
arteriosclerosis, hyperviscosity of the blood, and scleral encircling elements such as 360° retinal buckles posteriorly, all of
which can compromise the long posterior ciliary arteries. Older
patients have a higher likelihood for developing anterior
segment ischemia, whereas infants and children are generally
protected from this condition.15 Anterior segment ischemia has
even been reported after removing as few as two rectus muscles
in high-risk patients.12,15 It is important to remember, however,
that disruption of anterior ciliary arteries associated with strabismus surgery is permanent, and anterior segment ischemia
can occur years or decades later, as the collateral circulation
diminishes with age.34
chapter 2: anatomy and physiology of eye movements
61
PHYSIOLOGY OF OCULAR ROTATIONS
Donder’s and Listing’s Laws
Ocular movements are a result of contraction and relaxation of
multiple muscle groups that act to rotate the eye around a fixed
center of rotation. There are three axes that pass through the
center of rotation, termed the axes of Fick (Fig. 2-26). The axes
of Fick include the Z axis (vertical orientation) for horizontal
rotation, the X axis (horizontal orientation) for vertical rotation,
and the Y axis (oriented with the visual axis) for torsional rotation. Listing’s plane is a vertical plane that includes the X, Z,
and oblique axes that pass through the center of the eye (Fig.
2-26). Listing’s law states that virtually all positions of gaze can
be achieved by rotations around axes that lie on Listing’s plane.
Donder’s law is related to Listing’s law and states that there is
a specific orientation of the retina and cornea for every position
of gaze. This corneal orientation is specific for each position of
gaze regardless of the path the eye took to achieve that position
of gaze. Figure 2-27 demonstrates Listing’s and Donder’s laws,
showing the specific corneal orientations for ocular rotations
around various axes on Listing’s plane. Note that when rotations
B
A
C
FIGURE 2-26A–C. The three axes of Fick allow horizontal rotation. (A)
Vertical axis (Z axis): horizontal rotations. (B) Horizontal axis (X axis):
vertical rotations. (C) Visual axis (Y axis): torsional rotations.
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handbook of pediatric strabismus and amblyopia
FIGURE 2-27. Listing’s plane is shown in the center diagram, which
includes the Z and X axes of Fick. Diagram shows that the eye can reach
all positions of gaze by rotations around axes that are on Listing’s plane.
In the center diagram, the O axes represent oblique axes that are on
Listing’s plane and are oriented between the Z and X axes of Fick. Note
that the oblique axes of rotation seen on the four corners of the diagram
allow the eye to rotate obliquely, up and in, up and out, down and in, and
down and out. Also, observe the pseudotorsion of the cornea when the
eye rotates around the oblique axis.
are directly around the X axis (pure vertical movement) or
directly around the Z axis (pure horizontal movement) there is
no associated torsional rotation of the cornea. In contrast,
oblique ocular rotations cause a torsional shift in the corneal orientation relative to the planar coordinates of Listing’s plane.
This torsional shift relative to Listing’s plane is not due to true
rotation around the Y axis and is therefore referred to as pseudotorsion. Active, or true, torsional rotations around the Y axis
(cycloduction) are created by contraction of vertical and oblique
muscles. True torsional movements normally occur to keep the
eyes aligned during head tilting23 or occur pathologically when
a vertical or an oblique muscle over- or underacts.21
chapter 2: anatomy and physiology of eye movements
63
TABLE 2-2. Agonist–Antagonist Muscle Pairs.
Medial rectus—Lateral rectus
Superior rectus—Inferior rectus
Superior oblique—Inferior oblique
Sherrington’s Law: Agonist and
Antagonist Muscles
As described in this chapter previously, ductions are monocular
rotations and are clinically examined with one eye occluded to
force fixation to the eye being tested. Table 2-2 lists agonist–
antagonist pairs for the primary function of the muscles. This
relationship between agonist (contracting muscle) and antagonist (relaxing muscle) muscles is referred to as Sherrington’s
law of reciprocal innervation.
Sherrington’s law can be demonstrated by using electromyography (EMG). The EMG measures electrical potential
changes within a muscle as the muscle fibers contract and indicates the degree of overall neuromuscular activity. The EMG is
performed by placing a needle electrode in the muscle (extracellularly) and then recording the amplified electrical activity
from the muscle. Figure 2-28 shows results of EMG for agonist
and antagonist muscles that demonstrates Sherrington’s law.
The needle electrode is placed in the medial and lateral rectus
muscles. At the beginning of the EMG tracing, there is lowamplitude tonic activity that maintains the eye position in
FIGURE 2-28. Sherrington’s Law: Electromyographic (EMG) tracing from
the lateral rectus muscle (LR) and medial rectus muscle (MR). Note that
when the eye adducts, the medial rectus muscle increases EMG activity
as the muscle contracts. EMG activity from the lateral rectus muscle
diminishes as the antagonist lateral relaxes.
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handbook of pediatric strabismus and amblyopia
primary position. As the eye is adducted, the medial rectus contracts, resulting in increasing EMG activity, while the lateral
rectus muscle simultaneously relaxes and EMG activity is inhibited. At the end of the tracing, both muscles show tonic activity to maintain eye position. In patients with motor neuron
misdirection syndromes such as Duane’s retraction syndrome,
Sherrington’s law is violated. In Duane’s syndrome, the lateral
rectus muscle is innervated by a branch of the third nerve that
also supplies the medial rectus muscle. When the patient
adducts the eye, instead of the medial rectus contracting and the
lateral rectus relaxing, both the medial and lateral rectus
muscles contract simultaneously. It should be remembered that
Sherrington’s law of reciprocal innervation refers strictly to
monocular eye movements, as does the term ductions. A trick
to remember this, is the S in Sherrington stands for Single eye.
Synergist
The term synergist is used for muscles of the same eye that act
to move the eye in the same direction. In other words, synergist
muscles have common actions. For example, the superior
oblique and the inferior rectus muscles both act as depressors;
therefore, they are synergists for infraduction. These muscles are
not, however, synergists for horizontal or torsional rotations, as
the inferior rectus muscle is an adductor and extortor whereas
the superior oblique muscle is an abductor and intortor. Table
2-3 lists synergist muscles for various duction movements. Note
that synergist muscles relate to monocular rotations, not to be
confused with yoke muscles involved with binocular eye movements (see Hering’s Law of Yoke Muscles, below). Like the S
trick in Sherrington’s law, remember the S in Synergist stands
for Single eye.
TABLE 2-3. Synergist Muscles.
Duction
Primary mover
Secondary mover
Supraduction
Infraduction
Adduction
Abduction
Extorsion
Intorsion
Superior rectus
Inferior rectus
Medial rectus
Lateral rectus
Inferior oblique
Superior oblique
Inferior oblique
Superior oblique
Superior rectus/inferior rectus
Superior oblique/inferior oblique
Inferior rectus
Superior rectus
chapter 2: anatomy and physiology of eye movements
65
Oculomotor Reflexes
Two important oculomotor reflexes are the vestibulo-ocular
reflex (VOR) and optokinetic nystagmus (OKN). The vestibuloocular reflex functions to keep the eyes steady when the head
moves. Vestibular stimulation, induced by turning the head,
results in a compensatory movement of the eyes to maintain the
position of gaze. If the head is rapidly turned to the left, the eyes
move to the right with the same velocity. A similar reflex, the
orthostatic reflex, is responsible for keeping the eyes torsionally
aligned when the head is tilted. This reflex is the basis of the
Bielschowsky head tilt test for vertical muscle palsies. Optokinetic nystagmus is a visually mediated reflex consisting of
smooth pursuit alternating with saccadic refixation as a series
of objects cross the visual field. The eyes follow a moving object
with smooth pursuit, then use a saccadic movement in the opposite direction to refixate on the next approaching target. The
stimulus most commonly used to produce OKN is a pattern of
black and white stripes presented on a rotating drum or moving
tape. The best OKN stimulus fills the visual field so there are
no stationary objects for the subject to fixate.
Hering’s Law of Yoke Muscles
Normally, our two eyes move together in the same direction;
this is termed a version movement. Coordinated binocular eye
movements require symmetrical innervation of each eye. For
example, when one looks to the left, the left lateral rectus and
right medial rectus muscles simultaneously contract as the left
medial and right lateral rectus muscles relax (Fig. 2-29). The
paired agonist muscles from each eye are referred to as yoke
muscles. In Figure 2-29, the left lateral and right medial rectus
muscles are yoke agonist muscles whereas the left medial and
right lateral are yoke antagonists. Hering’s law states that yoke
muscles receive equal innervation. Remember, Hering’s law
relates to yoke muscles and binocular eye movements (versions),
whereas Sherrington’s law explains agonist–antagonist relationships and monocular eye movements (ductions). Figure 2-30
shows the yoke agonist muscles responsible for various fields of
gaze. In most situations, the term yoke muscles refers to yoke
agonist muscles.
FIGURE 2-29. Hering’s Law: Diagram of version movements to the left.
As the left lateral rectus (LR) contracts (), the contralateral medial
rectus (MR) simultaneously contracts (). Also note that the left
medial rectus relaxes () and the right lateral rectus also relaxes
().
FIGURE 2-30. Yoke muscles are shown for specific field of gaze. Top: gaze
up and to the side with yoke muscles being the superior rectus (SR) and
inferior oblique (IO) muscles. Middle: straight sidegaze with the yoke
muscles being lateral rectus (LR) and medial rectus (MR). Bottom: gaze
down and to the side with yoke muscles being the inferior rectus (IR) and
superior oblique (SO).
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chapter 2: anatomy and physiology of eye movements
67
Versions
Versions can be classified as follows: dextroversion for rightgaze,
levoversion for leftgaze, supraversion for upgaze, and infraversion for downgaze. In contrast to ductions, versions are performed with both eyes open and compare how well the eyes
move together in synchrony. Versions will identify a subtle
restriction or paresis and muscle overaction that results in asymmetrical eye movements.
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