Review

Ocular kinematics, vergence,

and orbital mechanics
Strabismus 0927-3972/03/$ 16.00

Strabismus – 2003, Vol. 11, No. 1,

Joseph L. Demer, M.D., Ph.D.
pp. 49–57
© Swets & Zeitlinger 2003 Departments of Ophthalmology and Neurology, and the
Jules Stein Eye Institute, University of California,
Accepted 1 December 2002
Los Angeles, CA
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Abstract Important aspects of ocular kinematics relate to the Correspondence and

geometric configuration of extraocular muscles (EOMs). The orbital reprint requests to:
layer of each rectus EOM inserts on a connective tissue ring called a Prof. Joseph L. Demer, M.D., Ph.D.
pulley that deflects the EOM path. Global layer fibers of each EOM Jules Stein Eye Institute
100 Stein Plaza
pass through the pulley to insert on the sclera. The orbital layer thus
UCLA
controls linear translation of the pulley, regulating the EOM’s pulling
Los Angeles, CA 90095-7002
direction, while the global layer rotates the eye. The active pulley U.S.A.
hypothesis (APH) states that pulleys are actively positioned to regu- Tel.: +1 (310) 825-5931
For personal use only.

late ocular kinematics. The coordinated control postulate of the APH Fax: +1 (310) 206-7826
proposes that during conjugate visually guided eye movements, rectus E-mail: jld@ucla.edu
pulleys move the same anteroposterior distance as their insertions, but
the inferior oblique pulley moves with vertical gaze by half the amount Acknowledgements:
as the inferior rectus insertion. These motions, observable by magnetic The work was supported by National
resonance imaging (MRI), shift the pulling directions of these EOMs Institutes of Health grant EY8313.
by half the ocular angle, mechanically implementing a ‘linear oculo- JLD was the recipient of an
unrestricted grant from Research to
motor plant’ appearing mathematically commutative to the brain and
Prevent Blindness, and is Larraine
consistent with Listing’s Law of ocular torsion.
and David Gerber Professor of
In the non-converged state with the head upright and stationary,
Ophthalmology. Joel M. Miller made
rectus pulleys move little transverse to the EOM axes. During con- insightful suggestions regarding the
vergence and during the static torsional vestibulo-ocular reflex, MRI presentation of the coordinated and
shows that the rectus pulley array rotates around the line of sight. differential control postulates of the
Oblique EOM orbital layers may implement this shift. APH.

Key words Active pulley hypothesis; convergence; extraocular

muscles; magnetic resonance imaging; pulleys; Listing’s law; eye
movements

Introduction The traditional notion of rectus EOM actions was

determined by the geometric relationships between their origins in the
annulus of Zinn, and their scleral insertions. However, quantitative
modeling efforts uncovered consequent anomalies related to absence
of specific constraints on EOM paths,1,2 leading to the supposition that
traditional notions of orbital anatomy might be incorrect.3,4 The result-
ing re-examination of EOM anatomy and physiology has motivated

Ocular kinematics 49
 a paradigm shift5 termed the active pulley hypothesis (APH).6–8 This
paper briefly summarizes the APH, some of its postulates, and evidence
supporting them.

Ocular kinematics as a basic concept Rotations of a three-

dimensional (3-D) object such as the eyeball are not mathematically
commutative, meaning that final eye position depends on the order of
the rotations.9 For similar geometric reasons, angular velocity eye is
not equal to the rate of change of its orientation, but rather is related
to both the time derivative and to instantaneous eye orientation.10,11
A non-commutative peripheral oculomotor apparatus would require
control by a central nervous system burdened with the need to keep
track of the sequence of previous eye movements.
As pointed out by Quaia and Optican,12 a fortunate arrangement of
EOMs and orbital connective tissues makes it appear commutative
to the brain. This occurs if the velocity axis of any ocular rotation
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shifts by half the shift in ocular orientation relative to a primary posi-

tion.12 This ‘half-angle rule’ amounts to one mathematical formulation
of Listing’s Law.11 A more familiar, yet equivalent, formulation of
Listing’s Law states that, with the head upright and stationary, any eye
orientation can be reached from any other by rotation about a single
axis, and that all such possible axes lie in a single plane, Listing’s plane.
It should be noted that Listing’s Law does not apply when the head is
not upright or is moving; the ensuing vestibulo-ocular reflex (VOR)
does not conform to Listing’s Law.
For personal use only.

The APH and commutativity The active pulley hypothesis

(APH) relates ocular kinematics to the relationships between the
EOMs and connective tissue structures in the orbit constraining EOM
paths consistent with Listing’s half-angle rule.6,12,13 The coordinated
control postulate of the APH is illustrated in Figure 1. The upper part
of Figure 1 diagrams a side view of a globe and horizontal rectus EOM.
The EOM’s rotational axis is perpendicular to the segment connecting
its pulley with its scleral insertion, thus vertical in primary gaze. Now
consider the viewing of a horizontally centered target at supraduction
angle a. If the distance from the pulley to globe center D1 is equal to
the distance from the insertion to globe center D2, then (for small
angles typical of the oculomotor range) the rotational axis will tilt pos-
teriorly by a/2 as required by Listing’s Law. This arrangement has been
confirmed quantitatively for all four rectus EOMs by MRI scanning of
people in secondary gaze positions.14
In tertiary (oblique) gaze positions, conformity with Listing’s Law
requires that pulleys translate in the orbit to remain in coordinated
relationship with the EOM’s scleral insertion (Figure 1 bottom).8 This
requirement is for substantial anteroposterior pulley translation for a
significant eye rotation. Shift in the point of EOM path inflection has
been demonstrated by MRI in tertiary gaze positions to correspond
quantitatively to the requirements of the APH,8 and shift of the pulley
connective tissues can also be demonstrated directly by MRI (Figure
2). Under conditions of coordinated control, a rectus pulley moves with
the globe as if rigidly attached to the underlying sclera; however, no

50 J.L. Demer
 Fig. 1. Top: Schematic lateral view of
orbit. Rotational axis for rectus
EOM is perpendicular to segment
connecting its pulley to its insertion.
Looking up by angle f, Listing’s law
is satisfied if distance D1 from pulley
(dark ring) to globe center is equal
to distance D2 from insertion to
globe center. Bottom: superior view
of orbit showing shifts in horizontal
rectus pulley position required to
maintain Listing’s half-angle
relationship in tertiary positions of
adducted elevation and adducted
depression. Pulleys are depicted as
dark rings, and are seen to move
posteriorly with EOM contraction in
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coordination with the globe surface.

Fig. 2. Gadodiamide-enhanced axial

MRI of right orbit in central gaze
and adduction. While the highly
For personal use only.

vascular bellies of the lateral rectus

(LR) and medial rectus (MR)
muscles appear white due to
gadodiamide contrast, the relatively
avascular pulley tissues do not and
so are distinguishable in the anterior
orbit. The MR pulley moves
anteriorly and the LR pulley moves
posteriorly in abduction. Note, in
central gaze, greater gadodiamide
enhancement of the more vascular
orbital layer (OL) than global layer
(GL). There is also marked contrast
enhancement of the highly vascular
choroid. ON = optic nerve.

such direct anatomic attachment exists. The anteroposterior pulley shift

with rectus EOM activation is produced by contraction of the orbital
layer (OL) of the EOM on the pulley itself; only the global layer (GL)
of each EOM passes through the pulley to become continuous with the
scleral insertion.6,15,16
Since all rectus EOMs have pulleys implementing Listing’s half-
angle behavior, the oblique EOMs would appear to be unnecessary
when the head is upright and stationary. In reality, the head is seldom
upright and stationary, necessitating compensatory eye movements by
the VOR, which does not conform to Listing’s law. An ideal VOR

Ocular kinematics 51

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Fig. 3. Lateral schematic of inferior
oblique (IO) and rectus pulleys.
For personal use only.
Left–Lateral rectus (LR) axis
(vertical gray arrow) is perpendicular
to segment from its pulley to its
insertion. Since the IO pulley is
coupled to the IR and LR pulleys,
the IO rotational axis (horizontal
gray arrow) lies perpendicular to
them along the gaze line. Right –
Since distance D1 from the LR
pulley to globe center is equal to
distance D2 from globe center to the
LR insertion, supraduction to angle
b causes the LR axis (short gray
arrow) to tilt by angle b/2.
Relaxation of IR orbital layer allows
IR pulley to move anteriorly by D3,
and partial coupling of IO pulley to
IR pulley moves IO pulley anteriorly
by D3/2. The IO axis continues to be
perpendicular to its segment
between the LR and IR pulleys, so
that the terminal IO path is
perpendicular to the LR path
anterior to its pulley. The IO axis
(long gray arrow) thus remains
perpendicular to LR axis, having
shifted by half the eye orientation
angle b.
52
would have a rotational axis identical to that of the head rotation
evoking it, and so independent of eye position in the orbit. The
observed velocity axis of the VOR rotates from about 25%17 to as little
as 0%18,19 of eye position. Since a 50% rotation of the velocity axis is
the criterion for Listing’s Law, the VOR does not conform even though
it does exhibit a degree of predictability in the behavior of its rotational
axis.At one time it seemed possible that differential shifts in the antero-
posterior locations of rectus pulleys (D1 π D2) might be the mecha-
nism of violations of Listing’s Law during the VOR.6 However,
theoretical analysis has since made clear that anteroposterior shifts of
rectus pulleys alone cannot account for VOR kinematics, which are
better explained by the relative weakness of the torsional component
to the horizontal and vertical components of the VOR.20 The APH has
thus required some modification.
A viable revision of the APH now proposes that the violation of
Listing’s Law during the VOR is mediated by the oblique EOMs, whose
velocity axes are actively maintained orthogonal to the Listing’s veloc-
ity axes of the rectus EOMs (Figure 3). The effect of rectus EOM con-
traction on oblique EOM path appears clearest for the inferior oblique
(IO) muscle, whose pulley is half coupled to that of the inferior rectus
(IR), and whose OL inserts, among other sites, on the LR pulley.21 In
primary gaze (Figure 3 left), this arrangement constrains the terminal
segment of the IO to be perpendicular to the gaze direction, so that the
IO produces a purely torsional action around the gaze line in a Listing’s
coordinate system. (In other coordinate systems, a vertical IO action
would also be observed.) In supraduction (Figure 3 right), the IO pulley
moves anteriorly by half the distance that the IR pulley moves;22 the
IO rotational axis is then no longer perpendicular to the gaze direc-
tion, but it remains perpendicular to the Listing’s velocity axis of the
rectus EOMs. The IO’s action would appear designed to violate
Listing’s law by producing a torsional velocity axis orthogonal to
Listing’s Law. The amount of ocular axis shift during the VOR should
then, as observed,18 be inversely related to torsional VOR gain, and
ideally zero when torsional VOR gain is unity.
The effect of vestibular stimulation on rectus pulley locations is dif-
ficult to study dynamically, for the practical reason that adequate MRI
resolution requires prolonged immobility by the subject. However, as
suggested to the author by B. Hess (personal communication), static
ocular counterrolling is a VOR that can be maintained indefinitely23 by
J.L. Demer
 changing the orientation of the subject’s head relative to gravity in an
MRI scanner. From the supine to ear-down position, normal humans
exhibit idiosyncratic torsional counter-rolling ranging widely in amount
from 3 to 7.5 degrees, and averaging 4.9 degrees.24 When observations
are extended from primary position to secondary and tertiary gazes,
this counter-rolling is associated with a torsional offset in an otherwise
normally-thick Listing’s plane in both monkeys23 and humans.24 When
MRI scanning in humans is repeated in the right ear down vs. left ear
down positions, the result varies quantitatively among subjects, but in
some cases substantial counter-rolling of the rectus pulley array is
observed.25 Extorsion of the pulley array is associated with apparently
contractile thickening of the IO, and apparently relaxational thinning
of the SO. Counter-rolling of the entire rectus pulley array would
produce a torsional offset in Listing’s plane, but leave otherwise
unchanged the kinematics of the rectus pulleys. Pulling directions of
individual EOMs would, of course, be changed for every type of eye
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movement, including saccades. Recordings from burst neurons in

monkeys are compatible with a torsional shift of rectus pulleys in the
direction of ocular counter-roll induced by static head tilt.26 The avail-
able data on pulley behavior during the VOR is obviously very pre-
liminary, and further study will be required to provide quantitative tests
of kinematics.
The superior oblique (SO) muscle, having a rigid pulley in the super-
onasal orbit and a very broad scleral insertion, appears special. Perhaps
the breadth of the anatomical SO insertion allows its functional inser-
For personal use only.

tion at the point of tangency to shift with gaze to maintain a rotational

axis parallel to that of the IO. Additional study of SO kinematics will
be required. However, the foregoing analysis suggests that visually
guided movements with the head upright and stationary can be imple-
mented in conformity to Listing’s Law by rectus EOMs and pulleys
alone, without a need for oblique EOMs. If this concept is accepted,
then the oblique EOMs exist to violate Listing’s Law and so to confer
kinematics appropriate to special situations such as convergence and
to the VOR.
The orthogonality of rectus and oblique actions does not eliminate
mechanical interactions, however. In this volume, Quaia and Optican
point out that even with the geometry described above, the lengths of
the oblique EOMs would passively change during visually guided eye
movements.27 Our observations indicate that human oblique EOMs
have only about one-fourth the number of muscle fibers than rectus
EOMs (Kono and Demer, unpublished observation), but they are nev-
ertheless mechanically significant. Since all EOMs have an elastic resis-
tance to stretch, this implies that oblique EOM forces would passively
change as well, and distort ocular kinematics unless innervational
adjustments were made to compensate.27

Differential control and binocular convergence The

Listing’s planes for the two eyes rotate temporally during convergence
by about twice the vergence angle,28 corresponding to excyclotorsion
in depression and incyclotorsion in elevation.29,30 This is required to
maintain alignment of retinal meridia during near viewing31 and is

Ocular kinematics 53
 greater during stereopsis than with binocular disparity alone. Thus,
during binocular viewing of near and far targets aligned on one eye,
the Listing’s plane for that unmoving eye is nevertheless tilted in asso-
ciation with the vergence movement of the other eye. Orbital MRI in
this situation demonstrates that pulleys correspondingly move in the
aligned eye.32 In craniotopic central gaze, this corresponds to a lateral
shift of the superior rectus (SR), inferior shift of the lateral rectus (LR),
and nasal shift of the inferior rectus (IR), all together amounting to an
excyclorotation of the rectus pulley array in the orbit. These shifts are
appropriate to accomplish the globe extorsion observed in convergence
when gaze is below primary position, which MRI evidence suggests
being slightly above craniotopic central gaze for supine subjects.8 An
opposite intorsional shift of rectus pulleys would be expected for con-
vergence at elevations above Listing’s primary position, but this pre-
diction has yet to be tested experimentally. Van Rijn and Van den Berg
have proposed that a form of Hering’s law of equal innervation exists
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for vergence, such that both eyes receive symmetric version commands
for remote targets, and mirror symmetric vergence commands for near
targets.29 The APH extends this suggestion to propose that symmetric
control may be applied to the pulleys via the oblique OLs and peribul-
bar SM, so that pulleys in both orbits are configured with mirror sym-
metry during convergence regardless of superimposed conjugate gaze.6
Quantitative analysis of MRI images suggests that the SO does not con-
tribute to this reconfiguration for convergence, since its cross-sectional
area is unchanged in the aligned eye, while the IO cross-section
For personal use only.

increases.32 Consistent with recordings of horizontal rectus EOM ten-

sions during the same experiment in monkeys,33 analysis of human
EOM cross-sections did not indicate gross overall co-contraction in
convergence.32

Histological evidence for the APH The orbital connective

tissues have been re-examined by histo- and immunohistochemical
staining of thin, serial sections in humans and monkeys.6,34–36 Rectus and
IO pulleys consist of encircling collagen rings, stiffened by elastin and
in some cases SM. Anterior to the pulley rings, rectus EOMs are
invested by thin collagen slings that are convex toward the orbital walls.
Posterior to the pulley rings, there are relatively thin pulley slings that
are convex toward the globe. The dense pulley rings are connected via
dense collagenous bands to the anterior orbital bones at only two prin-
cipal points called ‘entheses’ (bony attachments).36 The dense bands
suspending the horizontal rectus pulleys to the orbit have been called
‘check ligaments’ in the classical literature,37 based on the idea that they
serve to limit and damp ocular rotation. In the context of the APH, the
term ‘check ligament’ should probably be abandoned as functionally
misleading. Bands from the densely collagenous and elastin-rich medial
suspension extend from the enthesis on the anterior lacrimal crest to
the pulleys of the MR, IR, and SR.36 The medial enthesis also appears
to be the site of insertion of the medial canthal tendon of the lids. From
the lateral enthesis at Whitnall’s tubercle there extend dense collage-
nous bands to the LR, IR, and SR pulleys.36 In order to permit mobil-
ity of the upper and lower lids, there is no direct band from either

54 J.L. Demer
 vertical rectus EOM to the adjacent orbital wall, as is the case for the
MR and LR muscles. The elastin present in pulleys and suspensions has
the property of reversible extensibility, and thus confersa spring-like
property.
Pulley suspensions also contain SM, particularly in a band running
from the MR pulley to the nasal aspect of the IR pulley (Muller’s
peribulbar muscle),34–36 and comprising part of the classical Lockwood’s
ligament.37 This SM receives a rich autonomic innervation: via sympa-
thetic projections employing norepinephrine from the superior cervi-
cal ganglion, cholinergic parasympathetic projections probably from
the ciliary ganglion, and nitroxidergic innervation from the ptery-
gopalatine ganglion.35
Each EOM is histologically confirmed to be bilaminar, consisting of
a GL contiguous with the scleral insertion, and an OL inserting on
pulley tissues. The OLs of the four rectus EOMs contain roughly
similar numbers of fibers, averaging about 55% of the total EOM
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fibers.16 The remaining fibers comprise the GL, varying numerically in

rough proportion to the abundance of connective tissue in each pulley.
For the rectus and IO EOMs, the OL is roughly C-shaped and lies on
the EOM’s orbital surface. The OL fibers are not contiguous with the
scleral insertions, but instead insert on the pulleys, so that OL con-
traction stretches the anteriorly anchored pulley suspensions and trans-
lates the pulleys posteriorly. The IR and IO pulleys are mechanically
coupled in Lockwood’s ligament. The OL of the IL inserts on the IO
pulley, the collagenous sleeve of the IO temporally, and also on the
For personal use only.

LR pulley.21 Contraction of the IO OL thus would translate the IR

pulley nasally and the LR pulley inferiorly, consistent with MRI obser-
vations of pulley motion from infraduction to supraduction.38 In
rabbits, the SO contains EOM fibers that directly insert on the sclera.
In rabbits, the OL and GL both pass through the trochlea. The OL
inserts on the pulley apparatus around the SR, while the GL inserts on
the sclera. In humans and monkeys, the SO OL inserts coaxially pos-
terior to the trochlea on a dense collagenous sheath enveloping its exte-
rior, while slightly more anteriorly the GL becomes contiguous with
the SO tendon. Both the SO sheath and tendon pass through the
trochlea. The SO sheath inserts on the nasal border of the SR pulley,
while the tendon thins and passes inferior to the SR pulley to insert
broadly on the posterior lateral sclera. Contraction of the SO OL thus
would translate the SR pulley nasally, while contraction of the SO GL
rotates the globe.

Implications for further studies The APH amounts to a par-

adigm shift for the oculomotor system. It is now clear that the oculo-
motor system is overdetermined in the mathematical sense: there are
more internal variables than can be ascertained by measurement of the
three angular degrees of freedom of each eye. As demonstrated for
convergence, a single ocular orientation can be attained by more than
one EOM configuration, presumably representing different neural
command sets. It therefore follows that characterization of the normal
and pathological state of the oculomotor system will require more
information than could even theoretically be obtained from external

Ocular kinematics 55
 examination or recording of angular eye movements. It is probable that
separate neural command schemes prevail for the OLs that rotate the
eye, and the GLs that position the pulleys and thus control the direc-
tions of EOM actions. In future oculomotor research it will become
necessary to study EOM pulley behavior as well as eye orientation;
MRI is one way to do this in humans and possibly monkeys. Patho-
logical mechanisms might selectively involve pulleys and the OLs that
act on them.

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Ocular kinematics 57
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