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1 From the Department of Ophthalmology, Jules Stein Eye Institute, and the 2 Department of Neurology, University of California, Los Angeles; and the 3 Department of Ophthalmology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.
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Abstract |
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METHODS. High-resolution magnetic resonance imaging (MRI) was used to define the anterior paths of rectus EOMs, as influenced by gaze direction in living subjects. Pulley tissues were examined at cadaveric dissections and surgical exposures. Human and monkey orbits were step and serially sectioned for histologic staining to distinguish EOM fiber layers in relationship to pulleys.
RESULTS. MRI consistently demonstrated gaze-related shifts in the anteroposterior locations of human EOM path inflections, as well as shifts in components of the pulleys themselves. Histologic studies of human and monkey orbits confirmed gross examinations and surgical exposures to indicate that the orbital layer of each rectus EOM inserts on its corresponding pulley, rather than on the globe. Only the global layer of the EOM inserts on the sclera. This dual insertion was visualized in vivo by MRI in human horizontal rectus EOMs.
CONCLUSIONS. The authors propose the active-pulley hypothesis: By dual insertions the global layer of each rectus EOM rotates the globe while the orbital layer inserts on its pulley to position it linearly and thus influence the EOM’s rotational axis. Pulley locations may also be altered in convergence. This overall arrangement is parsimoniously suited to account for numerous aspects of ocular dynamics and kinematics, including Listing’s law.
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Introduction |
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Recent anatomic studies of whole orbits confirmed that each rectus EOM passes through a pulley consisting of an encircling ring or sleeve of collagen, located near the globe equator in Tenon’s fascia.6 7 The microscopic structure of pulleys is stereotypic.6 7 8 9 Pulley collagen fibrils are dense and organized in an interdigitating configuration suited to high internal rigidity.10 Pulleys are coupled to the orbital wall, adjacent EOMs, and equatorial Tenon’s fascia by bands containing collagen, elastin, and smooth muscle (SM). Abundant elastic fibers in and around pulleys6 7 provide reversible extensibility essential to these resilient tissues.11 Suspensory bands of the pulleys contain SM6 7 with rich autonomic innervation.7
Pulleys have important implications for EOM action because the functional origin of an EOM is at its pulley.12 It is thus not surprising that coronal plane locations of rectus pulleys, inferred from EOM paths in living subjects, are not only stereotypic in primary gaze, but are also stable in secondary gaze positions.13 Evidence of the mechanical importance of pulleys is the finding that their heterotopy in the coronal plane is associated with predictable patterns of incomitant strabismus.14 Theoretical studies of ocular kinematics suggest that suitable anteroposterior location of pulleys could implement a linear oculomotor plant, one that appears commutative to the brain.15 Lower resolution MRI of rectus paths after surgical transposition of EOM insertions suggests that the anteroposterior location of pulleys is consistent with the foregoing theoretical requirements,5 a finding now confirmed by higher resolution MRI of normal rectus EOM path inflections in secondary gaze positions (Clark and Demer, unpublished data, 2000).
Recent advances in orbital imaging technique have improved earlier orbital MRI resolution by an order of magnitude. Surprisingly, technical limitations in existing orbital anatomic data now make them inadequate for comparison to the increasing quality of modern MRI of living EOMs. A major limitation has resulted from exenteration of orbital tissues before histologic processing. Release of connective tissue tension in a nonphysiologic manner by dissection of individual EOMs from unfixed orbits can distort anatomic relationships. An improved technique involves en bloc exenteration of the orbital soft tissues from their bony supports, followed by fixation.6 7 This method maintains most orbital topology, but not necessarily normal distances. Even so, dissection of the anterior periorbita from the orbital rim damaged the pulley supports. These artifacts limited interpretation of prior anatomic studies of the orbital connective tissues.
It has long been recognized that rectus EOMs of mammals contain two distinct layers.16 17 18 19 20 The global layer contains three types of singly innervated fibers (SIFs) and one type of multiply innervated fiber (MIF); the orbital layer contains one type of SIF and one type of MIF. Classic studies have demonstrated that although the global layer is continuous from the annulus of Zinn to the tendinous insertion on the globe, the orbital layer terminates posterior to the scleral insertion.16 21 Because these studies were performed before appreciation of the existence of pulleys, it is unclear from the literature how the EOM orbital layer may relate to contemporary understanding of pulley anatomy and function.
Technical improvements have made it possible to reconstruct detailed orbital histology without removal from the supporting bones, thus maintaining normal spatial relationships. The present study was thus designed to exploit improvements in MRI in living subjects, as well as histology in cadavers, for study of the precise relationship between EOM layers and the corresponding pulleys. These data were examined in the context of surgical exposures of living tissues and were interpreted in the context of contemporary concepts of the contribution of pulleys to binocular kinematics.
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Methods |
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Tissue Preparation
Five human orbits (aged 44–93 years) were exenterated en bloc at
autopsy through an intracranial approach within 24 hours of death.
These were fixed for at least five days in 10% neutral buffered
formalin with the periorbita intact but separated from bony support.
Three additional human orbits (aged 17 months to 57 years) were
obtained from a tissue bank (IIAM, Scranton, PA), in heads fresh frozen
shortly after death. The frozen heads were slowly thawed in 10%
neutral buffered formalin. Three monkeys, a rhesus (Macaca
mulatta), a fascicularis (Macaca fascicularis), and a
cebus (Cebus apella), were killed in conformity with
recommendations of the American Veterinary Medical Association and ARVO
Statement for the Use of Animals in Ophthalmic and Vision Research and
perfused with fixative through the aorta. The intact, fixed right
orbits of the three humans and three monkeys were then removed in
continuity with the eyelids and orbital bones, the latter being
carefully thinned under magnification by using a high speed-drill.
These fixed right orbits were then decalcified for 24 hours at room
temperature in 0.003 M EDTA and 1.35 N HCl. The left orbit of the cebus
monkey was exenterated after fixation, and longitudinal dissections
were made to remove each rectus EOM in continuity with its adjacent
pulley and underlying sclera.
At autopsy of an adult male human conducted within 8 hours of death, all EOMs were harvested in continuity with their contiguous connective tissues. After atraumatic enucleation of the globes using surgical technique and magnification, EOMs were isolated and excised, with orientation carefully maintained. Representative EOMs and their contiguous pulleys were pinned to cardboard at anatomic length and orientation before fixation in 10% neutral buffered formalin.
Formalin-fixed tissues were dehydrated in graded solutions of alcohol and chloroform, embedded in paraffin, and serially sectioned at 10-µm thickness, as previously described.6 7 Whole orbits were serially sectioned in the coronal plane. Individual human EOMs, as well as EOMs in continuity with the sclera in the cebus monkey, were step sectioned longitudinally in the vicinity of pulleys at intervals of 200 µm, and transversely at intervals of 200 µm posterior to them. All sections were mounted on gelatin-coated glass slides.
Masson’s trichrome stain was used to show muscle and collagen and van
Gieson’s stain to show elastin.23
As previously
described,7
SM was confirmed using monoclonal mouse
antibody to human SM 
-actin (Dako, Copenhagen, Denmark) applied at
4°C overnight at dilutions of 1:100 to 1:500. The antigen–antibody
reaction for human SM -actin was visualized using the ABC kit with
blue chromogen (Alkaline Phosphatase Kit 3; Vector, Burlingame,
CA).24
Orbital dissections were performed in three fresh adult human cadavers to isolate the medial rectus (MR) pulley. Selected tissues were excised and processed histologically to confirm their composition. Findings at these dissections were correlated with findings at routine strabismus surgeries performed by an author (JLD) in which rectus EOMs were exposed and clinical photographs taken.
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Results |
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The insertion of the MR orbital layer into its pulley is illustrated for four representative subjects of various ages in Figure 1A . In dextroversion, the MR path for the abducting right eye is inflected at roughly the point at which the dark band joins the EOM belly. This inflection, more obvious in image planes including the central part of the MR, corresponds to the MR pulley. The insertion of the dark band on the MR’s orbital surface was more anterior in abduction than in adduction (Fig. 1A) . More central image planes (for example, Fig. 1B ) demonstrated a corresponding posterior shift in the MR inflection point with adduction. The dark band was more prominent in older subjects (Fig. 1A) . These findings, supported by histologic evidence below, indicate that the insertion of the MR orbital layer is on the MR pulley that in turn inflects the MR’s path and that the pulley moves posteriorly from abduction to adduction.
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Insertion of the orbital layer of horizontal rectus EOMs into the connective tissues of the peripheral orbit was also consistently appreciated in coronal plane imaging performed in eight subjects. The orbital layer insertion of the MR muscle could be visualized in nearly every orbit as one or more dark bands isodense with EOM extending radially toward the medial orbital wall (Fig. 2) . The MR orbital layer insertion in Figure 2 typifies the most common pattern of three prominent bands. The anteroposterior extent of the orbital layer insertion was focal, so that it was imaged in only one or two adjacent 2-mm-thick coronal planes. As seen in Figure 2 , large horizontal gaze shifts caused a corresponding shift in the anteroposterior location of the MR orbital layer insertion. In 28° adduction, the MR orbital layer insertion was relatively posterior at the level of the globe–optic nerve junction. In primary gaze, the MR orbital layer insertion moved two image planes (4 mm) and another two image planes (4 mm) anteriorly in 28° abduction for a total travel of approximately 8 mm.
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The insertion of rectus orbital layer fibers on their respective pulleys was also confirmed by longitudinal sectioning of rectus EOMs in the cebus monkey orbit and in one human orbit. This is shown for a human LR in Fig. 7 . The lower power view in Fig. 7A confirms that the orbital layer does not extend anteriorly to the LR pulley. The higher power view of the same region shown in Fig. 7B confirms that the orbital layer insertion is through particularly dense, short collagenous tendons that appear as focally dark blue terminations of orbital layer fibers.
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Discussion |
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Before pulleys were known, Listing’s law was presumed to be implemented entirely by complex neural commands to the EOMs. However, experiments have not identified a neural substrate for Listing’s law. In the superior colliculus, saccades are encoded as the two-dimensional (horizontal and vertical) rate of change of eye orientation, implying that any computation of the third dimension, torsion, is accomplished downstream.15 35 Even in the oculomotor nucleus and rostral interstitial nucleus of the medial longitudinal fasciculus, saccadic burst commands are better correlated with rate of change of 3-D eye position than with angular eye velocity.35 36 Nevertheless, Listing’s law is presumed to have a neural basis35 because it is systematically violated by the vestibulo-ocular reflex (VOR)37 and during sleep.38 The VOR is a phylogenetically ancient reflex that stabilizes images of fixed objects on the retina during head motion. An ideal VOR would have an axis of ocular rotation exactly matching that of the head, rather than shifting by half the change in eye orientation. Empirically, the axis of the VOR shifts by one fourth of the shift of eye orientation, so that the VOR follows a quarter-angle rule.37
The pulleys form a natural mechanical substrate for Listing’s law and
several other previously mysterious aspects of ocular
kinematics.15
Figure 9
is a side view of a diagrammatic globe showing a horizontal rectus EOM
in the top panel. The rotational axis of the rectus EOM is
perpendicular to the line connecting its pulley with the scleral
insertion. Thus the rotational axis of the horizontal rectus EOM is
vertical in straight-ahead gaze. Now consider the situation during
visual fixation of a horizontally centered target at an angular
elevation of angle . If the distance from the pulley to the globe
center D1 is equal to the distance from the
insertion to the globe center D2, then the
rotational axis tilts posteriorly by angle /2, precisely the
requirement of Listing’s law. A recent study of EOM path inflections
in secondary gaze positions such as this example has demonstrated that
in straight-ahead gaze the four rectus pulleys are indeed located in
the positions required by the half-angle rule (Clark and Demer,
unpublished data, 2000).
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In tertiary (oblique) gaze positions, pulley behavior can still explain Listing’s law as illustrated in Figure 10a 10b 10c 10d 10e 10f 10g 10h 10i 10j 10k 10l 10m 10n 10o 10p view of a schematic orbit showing the MR and LR muscles. Beginning in primary position in the upper panel, the secondary positions of elevation and depression can be attained in conformity to Listing’s half-angle rule as explained earlier, if the distance from the pulley to the globe center D1 is equal to the distance from the insertion to the globe center D2. Beginning in adduction as diagrammed in the lower panel, the tertiary positions of adducted elevation and adducted depression can be attained in conformity to Listing’s law once again if the distance from the pulley to the globe center D1 is equal to the distance from the insertion to the globe center D2. Distances D1 and D2 are referenced to the globe, not to the orbit. To implement Listing’s law, shifts in the anteroposterior position of the pulleys must occur when beginning in the secondary positions of abduction, elevation, or depression, and moving into tertiary positions. In cats, the most powerful and fatigue-resistant motor units of the LR muscle, comprising of 27% of all units, consist of single neurons innervating fibers in both the orbital and global layers.19 These bilayer motor units would command similar contraction in the two layers, an arrangement convenient to maintain the position of the pulley relative to the EOM insertion in secondary gaze positions as required for the half-angle rule.
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The plausibility of the postulated anteroposterior pulley shifts is supported by MRI images of EOM paths in Figure 1B . Note the similarity of the horizontal rectus paths to the diagram in Figure 10 and the appropriate direction of the shifts in pulley structures denoted with the arrowheads, suggesting that distances D1 and D2 may actually be roughly equal in living subjects. Note that the inflections observed in axial images of the horizontal rectus EOMs in the secondary positions of abduction and adduction may not exactly reflect the points of inflection out of the axial plane in tertiary gaze positions. A quantitative test of the hypothesis illustrated in Figure 10 would require precise measurements of rectus EOM paths in 3-D. However, the qualitative aspects of EOM path evident from these images are consistent with this hypothesis. The orbital layer insertion of each EOM on its corresponding pulley seems ideally suited to implement the necessary pulley repositioning against its elastic and SM suspensions that would, on relaxation of orbital layer fibers, move the pulley forward. For visually guided or volitional eye movements conforming to Listing’s law around primary gaze, global layer fibers would be expected to receive motor commands at roughly the same gain as orbital layer fibers, to maintain the required relationship between the pulley and the scleral insertion.
It has been observed experimentally that Listing’s planes for the two eyes rotate temporally during convergence, corresponding to the relative excyclotorsion in depression and incyclotorsion in elevation41 42 43 necessary to maintain alignment of corresponding retinal meridians during near viewing. Thus, during the binocular viewing of near and far targets aligned on one eye, Listing’s plane for that unmoving eye nevertheless tilts in association with the vergence movement of the other eye.43 This tilting of Listing’s plane has been interpreted as confirmation of the neural nature of Listing’s law but could alternatively be attributed to a symmetrical reconfiguration of rectus pulleys during vergence as illustrated in Figure 11 . Suitable reconfiguration of pulleys could include a nasal displacement of the vertical rectus pulleys due to contraction of the peribulbar SM and due to tension from posterior displacement of the MR pulley by its orbital layer transmitted to the vertical rectus pulleys through fibroelastic intercouplings. The resultant nasal displacement of the vertical rectus pulleys gives the vertical rectus EOMs an extorting action in depression and an intorting action in elevation (Fig. 11) , corresponding to temporal tilting of Listing’s plane in each eye. It has been proposed by van Rijn and van den Berg41 that a form of Hering’s law of equal innervation exists for the vergence system, such that both eyes receive symmetric version commands for remote targets, and mirror symmetric vergence commands for near targets. We extend this suggestion to propose that symmetric control may be applied to the pulleys through the orbital layer rectus fibers and peribulbar SM, so that pulleys in both orbits are configured with mirror symmetry during convergence, regardless of superimposed conjugate gaze. Such a configuration could explain the otherwise perplexing finding in monkeys of mirror units in the abducens40 44 and oculomotor nuclei.40 In these monkeys fixating near and far targets aligned with one eye, identified motoneurons specifically projecting to striated EOMs of the aligned (and nonmoving) eye apparently fired in response to the monocular position of the opposite eye.42 This otherwise astonishing finding could be reconciled if the recorded motoneurons projected to the orbital layer of the aligned eye and were reconfiguring the pulleys of the involved EOMs as vergence changed.
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Implications of the Active-Pulley Hypothesis for Ocular Dynamics
The active-pulley hypothesis has major implications for ocular
dynamics. Raphan45
and Quaia and Optican15
have argued that by implementing a linear plant, pulleys would
effectively permit motor commands to the global layer to consist of the
rate of change of desired eye orientation and its simple mathematical
integral. The pulley system would thus function as an analog computer
to convert rate of change in desired eye orientation into the
kinematically required 3-D eye velocity and would make eye position
commands essentially commutative. This simplifies the otherwise complex
problem of matching the pulse to the step of saccadic
innervation.15
Electromyographic (EMG) recordings in the human LR global layer demonstrate both a phasic pulse and tonic step of activity during saccades, the former necessary to drive the formidable viscous load imposed by the relaxing antagonist EOM and the latter necessary to oppose the lesser elastic load as position is maintained.47 Recordings of tension at the insertions of simian horizontal rectus EOMs confirm the presence of both saccadic pulses and steps.48 In the human orbital layer, however, EMG shows only a step of activity during saccades, whereas the global layer exhibits both pulses and steps.47 Orbital layer fibers have lower recruitment thresholds than global layer fibers,20 47 49 prompting Collins47 to propose that the orbital layer may have a special role in fixation. The insight that the orbital layer inserts on the pulley permits an alternative interpretation. The mechanical load on the orbital layer is likely to be dominated by elasticity of the attached pulley suspension. Collins has pointed out that the main load on an EOM attached to the globe is viscosity arising from the relaxing antagonist EOM. A phasic pulse of force in the orbital layer is unnecessary to achieve brisk pulley motion against a mainly elastic load. However, this elastic loading by passive connective tissue requires that orbital layer fibers maintain active tension throughout the oculomotor range to avoid slack. In contrast, global layer fibers remain under tension, even when relaxed, because of stretching by the antagonist EOM. The active-pulley hypothesis predicts that motor neurons preferentially innervating fibers in the orbital layer should, during saccades, exhibit step but not pulse changes in activity. Many such tonic motor neurons have been found in the abducens and oculomotor nuclei.40
Implications for Muscle Fiber Types
The active-pulley hypothesis may partially account for the complex
variety of fiber types in EOMs, starting from the premise that fiber
characteristics are adapted to their physiologic
demands.50
Approximately 80% of fibers in the orbital
layer of each EOM are fast-twitch–generating SIFs resembling mammalian
skeletal muscle fibers, whereas 20% are MIFs that either do not
conduct action potentials or do so only in their central
portions.16
Orbital SIFs are specialized for intense
oxidative metabolism and fatigue resistance.16
The
vascular supply in the orbital layer is high,21
approximately 50% greater in humans than the well-perfused global
layer.51
The high metabolism, fatigue resistance,
and luxurious blood supply of the numerous orbital SIFs are tailored to
their continuous elastic loading by the pulley suspensions. The
expression of unique myosin isoforms in orbital SIFs may also be
related to the requirements of fast-twitch capability against
continuous loading, because alterations in EOM activity patterns can
change EOM-specific myosin heavy chain gene expression.52
However, the function of the relatively sparse and primitive orbital
MIFs remains unclear.
Approximately 90% of fibers in the global layer are fast-twitch–generating SIFs, whereas 10% are slow, non-twitch MIFs resembling those of amphibians.16 The SIFs are often divided into three types—red, intermediate, and white—distinguished by their density of mitochondria and fatigue resistance.16 The largest and most granular red SIFs, constituting approximately 33% of all global fibers, are very similar to orbital SIFs and are highly fatigue resistant, whereas the intermediate and white SIFs have progressively lower fatigue resistance.16 The predominant static loading of the global layer by the moderate contractile force of antagonist EOM accounts for the global layer’s higher overall recruitment threshold than the orbital layer and the lesser oxidative, vascular, and fatigue-resistant features of orbital SIFs. However, during saccades the high viscous loading of the global layer by the relaxing antagonist EOM requires the high transient force that intermediate and white SIFs are well suited to provide. The function of the small number of global MIFs remains obscure.
Implications for Strabismus
Orbital SIFs are the last EOM fiber type to mature to adult
features and do so after birth during the establishment of binocular
alignment.17
53
Nemestrina monkeys, a macaque species with
a high prevalence of naturally occurring strabismus, show evidence of a
role of orbital layer abnormalities in the pathogenesis of strabismus.
These monkeys transiently exhibit tubular aggregates only in orbital
SIFs during the first 6 months of life, whereas fascicularis monkeys
exhibit neither the tubular aggregates in the orbital layer nor
naturally occurring strabismus.17
Treatment of strabismus probably affects the action of orbital EOM layers on their pulleys. Botulinum toxin treatment of strabismus produces its most lasting effects on orbital SIFs21 and may therefore alter pulley behavior. Strabismus surgery that alters the relationships between EOM insertions and pulleys probably produces unintended effects that should be better understood and perhaps considered in surgical planning. In particular, any pulley manipulation compromising the orderly relationship between eye orientation and the rotational axes of EOMs would compromise neural control of eye movement15 and would be expected to produce at least dynamic binocular misalignments in tertiary gaze positions. Noncommutativity of ocular rotations could also occur in patients who have strabismus with pulley abnormalities.
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Acknowledgements |
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Footnotes |
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Supported by US Public Health Service, National Eye Institute Grant EY-08313 and Core Grant EY-00331. JLD received a Research to Prevent Blindness Lew R. Wasserman merit award and is the Larraine and David Gerber Professor of Ophthalmology.
Submitted for publication September 14, 1999; revised December 9, 1999; accepted December 20, 1999.
Commercial relationships policy: N.
Corresponding author: Joseph L. Demer, Jules Stein Eye Institute, 100 Stein Plaza, UCLA, Los Angeles, CA 90095-7002. jld{at}ucla.edu.
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J. L. Demer Pivotal Role of Orbital Connective Tissues in Binocular Alignment and Strabismus The Friedenwald Lecture Invest. Ophthalmol. Vis. Sci., March 1, 2004; 45(3): 729 - 738. [Full Text] [PDF]
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S. Bicer and P. J. Reiser Myosin Light Chain 1 Isoforms in Slow Fibers from Global and Orbital Layers of Canine Rectus Muscles Invest. Ophthalmol. Vis. Sci., January 1, 2004; 45(1): 138 - 143. [Abstract] [Full Text] [PDF]
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D. M. Dimitrova, M. S. Shall, and S. J. Goldberg Stimulation-Evoked Eye Movements With and Without the Lateral Rectus Muscle Pulley J Neurophysiol, December 1, 2003; 90(6): 3809 - 3815. [Abstract] [Full Text] [PDF]
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D. Straumann, H. Steffen, K. Landau, O. Bergamin, A. V. Mudgil, M. F. Walker, D. L. Guyton, and D. S. Zee Primary Position and Listing's Law in Acquired and Congenital Trochlear Nerve Palsy Invest. Ophthalmol. Vis. Sci., October 1, 2003; 44(10): 4282 - 4292. [Abstract] [Full Text] [PDF]
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E. T. Detorakis, R. E. Engstrom, B. R. Straatsma, and J. L. Demer Functional Anatomy of the Anophthalmic Socket: Insights from Magnetic Resonance Imaging Invest. Ophthalmol. Vis. Sci., October 1, 2003; 44(10): 4307 - 4313. [Abstract] [Full Text] [PDF]
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J. L. Demer, S. Y. Oh, R. A. Clark, and V. Poukens Evidence for a Pulley of the Inferior Oblique Muscle Invest. Ophthalmol. Vis. Sci., September 1, 2003; 44(9): 3856 - 3865. [Abstract] [Full Text] [PDF]
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L. K. McLoon and S. P. Christiansen Increasing Extraocular Muscle Strength with Insulin-like Growth Factor II Invest. Ophthalmol. Vis. Sci., September 1, 2003; 44(9): 3866 - 3872. [Abstract] [Full Text] [PDF]
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D. E. Angelaki Three-Dimensional Ocular Kinematics During Eccentric Rotations: Evidence for Functional Rather Than Mechanical Constraints J Neurophysiol, May 1, 2003; 89(5): 2685 - 2696. [Abstract] [Full Text] [PDF]
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E. M. Klier, H. Wang, and J. D. Crawford Three-Dimensional Eye-Head Coordination Is Implemented Downstream From the Superior Colliculus J Neurophysiol, May 1, 2003; 89(5): 2839 - 2853. [Abstract] [Full Text] [PDF]
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J. L. Demer, R. Kono, and W. Wright Magnetic Resonance Imaging of Human Extraocular Muscles in Convergence J Neurophysiol, April 1, 2003; 89(4): 2072 - 2085. [Abstract] [Full Text] [PDF]
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D. E. Angelaki and J. D. Dickman Premotor Neurons Encode Torsional Eye Velocity during Smooth-Pursuit Eye Movements J. Neurosci., April 1, 2003; 23(7): 2971 - 2979. [Abstract] [Full Text] [PDF]
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R. Kono, V. Poukens, and J. L. Demer Quantitative Analysis of the Structure of the Human Extraocular Muscle Pulley System Invest. Ophthalmol. Vis. Sci., September 1, 2002; 43(9): 2923 - 2932. [Abstract] [Full Text] [PDF]
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S. Y. Oh, R. A. Clark, F. Velez, A. L. Rosenbaum, and J. L. Demer Incomitant Strabismus Associated with Instability of Rectus Pulleys Invest. Ophthalmol. Vis. Sci., July 1, 2002; 43(7): 2169 - 2178. [Abstract] [Full Text] [PDF]
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R. Kono, R. A. Clark, and J. L. Demer Active Pulleys: Magnetic Resonance Imaging of Rectus Muscle Paths in Tertiary Gazes Invest. Ophthalmol. Vis. Sci., July 1, 2002; 43(7): 2179 - 2188. [Abstract] [Full Text] [PDF]
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A. M. F. Wong, J. A. Sharpe, and D. Tweed Adaptive Neural Mechanism for Listing's Law Revealed in Patients with Fourth Nerve Palsy Invest. Ophthalmol. Vis. Sci., June 1, 2002; 43(6): 1796 - 1803. [Abstract] [Full Text] [PDF]
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J. M. Miller, C. J. Bockisch, and D. S. Pavlovski Missing Lateral Rectus Force and Absence of Medial Rectus Co-Contraction in Ocular Convergence J Neurophysiol, May 1, 2002; 87(5): 2421 - 2433. [Abstract] [Full Text] [PDF]
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S. P. Christiansen, D. Peterson, T. To, R. Youle, and L. McLoon Long-term Effects of Ricin-mAb 35 on Extraocular Muscles of Rabbits: Potential Treatment for Strabismus Invest. Ophthalmol. Vis. Sci., March 1, 2002; 43(3): 679 - 685. [Abstract] [Full Text] [PDF]
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A. M. F. Wong, D. Tweed, and J. A. Sharpe Adaptive Neural Mechanism for Listing's Law Revealed in Patients with Sixth Nerve Palsy Invest. Ophthalmol. Vis. Sci., January 1, 2002; 43(1): 112 - 119. [Abstract] [Full Text] [PDF]
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H. Misslisch and D. Tweed Neural and Mechanical Factors in Eye Control J Neurophysiol, October 1, 2001; 86(4): 1877 - 1883. [Abstract] [Full Text] [PDF]
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M. A. Smith and J. D. Crawford Implications of Ocular Kinematics for the Internal Updating of Visual Space J Neurophysiol, October 1, 2001; 86(4): 2112 - 2117. [Abstract] [Full Text] [PDF]
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 M. C. Brodsky and S. P. Donahue Primary Oblique Muscle Overaction: The Brain Throws a Wild Pitch Arch Ophthalmol, September 1, 2001; 119(9): 1307 - 1314. [Abstract] [Full Text] [PDF]
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H. Scherberger, J.-H. Cabungcal, K. Hepp, Y. Suzuki, D. Straumann, and V. Henn Ocular Counterroll Modulates the Preferred Direction of Saccade-Related Pontine Burst Neurons in the Monkey J Neurophysiol, August 1, 2001; 86(2): 935 - 949. [Abstract] [Full Text] [PDF]
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S. Khanna and J. D. Porter Evidence for Rectus Extraocular Muscle Pulleys in Rodents Invest. Ophthalmol. Vis. Sci., August 1, 2001; 42(9): 1986 - 1992. [Abstract] [Full Text] [PDF]
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 C. R. RICHMONDS and H. J. KAMINSKI Nitric oxide synthase expression and effects of nitric oxide modulation on contractility of rat extraocular muscle FASEB J, August 1, 2001; 15(10): 1764 - 1770. [Abstract] [Full Text] [PDF]
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O. Bergamin and D. Straumann Three-Dimensional Binocular Kinematics of Torsional Vestibular Nystagmus During Convergence on Head-Fixed Targets in Humans J Neurophysiol, July 1, 2001; 86(1): 113 - 122. [Abstract] [Full Text] [PDF]
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O. Bergamin, D. S. Zee, D. C. Roberts, K. Landau, A. G. Lasker, and D. Straumann Three-Dimensional Hess Screen Test with Binocular Dual Search Coils in a Three-Field Magnetic System Invest. Ophthalmol. Vis. Sci., March 1, 2001; 42(3): 660 - 667. [Abstract] [Full Text]
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S. Y. Oh, V. Poukens, and J. L. Demer Quantitative Analysis of Rectus Extraocular Muscle Layers in Monkey and Humans Invest. Ophthalmol. Vis. Sci., January 1, 2001; 42(1): 10 - 16. [Abstract] [Full Text]
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S. Y. Oh, V. Poukens, M. S. Cohen, and J. L. Demer Structure-Function Correlation of Laminar Vascularity in Human Rectus Extraocular Muscles Invest. Ophthalmol. Vis. Sci., January 1, 2001; 42(1): 17 - 22. [Abstract] [Full Text]
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R. A. Clark, J. M. Miller, and J. L. Demer Three-dimensional Location of Human Rectus Pulleys by Path Inflections in Secondary Gaze Positions Invest. Ophthalmol. Vis. Sci., November 1, 2000; 41(12): 3787 - 3797. [Abstract] [Full Text]
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M. J. Thurtell, M. Kunin, and T. Raphan Role of Muscle Pulleys in Producing Eye Position-Dependence in the Angular Vestibuloocular Reflex: A Model-Based Study J Neurophysiol, August 1, 2000; 84(2): 639 - 650. [Abstract] [Full Text] [PDF]
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