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1.  Differential Lateral Rectus Compartmental Contraction during Ocular Counter-Rolling 
Purpose.
The lateral rectus (LR) and medial rectus (MR) extraocular muscles (EOMs) have largely nonoverlapping superior and inferior innervation territories, suggesting functional compartmental specialization. We used magnetic resonance imaging (MRI) in humans to investigate differential compartmental activity in the rectus EOMs during head tilt, which evokes ocular counter-rolling, a torsional vestibulo-ocular reflex (VOR).
Methods.
MRI in quasi-coronal planes was analyzed during target-controlled central gaze in 90° right and left head tilts in 12 normal adults. Cross sections and posterior partial volumes of the transverse portions of the four rectus EOMs were compared in contiguous image planes 2 mm thick spanning the orbit from origins to globe equator, and used as indicators of contractility.
Results.
Horizontal rectus EOMs had significantly greater posterior volumes and maximum cross sections in their inferior compartments (P < 10−8). In orbit tilt up (extorted) compared with orbit tilt down (intorted) head tilts, contractile changes in LR maximum cross section (P < 0.0001) and posterior partial volume (P < 0.05) were significantly greater in the inferior but not in the superior compartment. These changes were not explainable by horizontal or vertical eye position changes. A weaker compartmental effect was suggested for MR. The vertical rectus EOMs did not exhibit significant compartmental contractile changes during head tilt. Mechanical modeling suggests that differential LR contraction may contribute to physiological cyclovertical effects.
Conclusions.
Selective activation of the two LR, and possibly MR, compartments correlates with newly recognized segregation of intramuscular innervation into distinct compartments, and probably contributes to noncommutative torsion during the VOR.
Magnetic resonance imaging of extraocular muscles during ocular counter-rolling demonstrates selective activation of the lateral rectus inferior but not superior compartment. This is novel functional evidence that differential rectus compartmental activation contributes to a vestibulo-ocular reflex.
doi:10.1167/iovs.11-7929
PMCID: PMC3367472  PMID: 22427572
2.  Mechanics of the Orbita 
Developments in ophthalmology  2007;40:132-157.
The oculomotor periphery was formerly regarded as a simple mechanism executing complex behaviors explicitly specified by innervation. It is now recognized that several fundamental aspects of ocular motility are properties of the extraocular muscles (EOMs) and their associated connective tissue pulleys. The Active Pulley Hypothesis proposes that rectus and inferior oblique EOMs have connective tissue soft pulleys that are actively controlled by the direction action of the EOMs’ orbital layers. Functional imaging and histology have suggested that the rectus pulley array constitutes an inner mechanism, similar to a gimbal, that is rotated torsionally around the orbital axis by an outer mechanism driven by the oblique EOMs. This arrangement may mechanically account for several commutative aspects of ocular motor control, including Listing’s law, yet permits implementation of noncommutative motility as during the vestibulo-ocular reflex. Recent human behavioral studies, as well neurophysiology in monkeys, are consistent with mechanical rather than central neural implementation of Listing’s law. Pathology of the pulley system is associated with predictable patterns of strabismus that are surgically treatable when the pathologic anatomy is characterized by imaging. This mechanical determination may imply limited possibilities for neural adaptation to some ocular motor pathologies, but indicates greater potential for surgical treatments.
doi:10.1159/0000100353
PMCID: PMC2268111  PMID: 17314483
3.  Functional Imaging of Human Extraocular Muscles In Head Tilt Dependent Hypertropia 
High-resolution MRI shows heterogeneous extraocular muscle features in strabismus, typical of superior oblique palsy. Rectus pulley counterrotations in response to head tilt may be paradoxical and depend on the presence of superior oblique atrophy, which is detected in half of patients.
Purpose.
Although alteration in hypertropia induced by head tilt is considered a clinical criterion for diagnosis of superior oblique (SO) palsy, the mechanism of this head-tilt–dependent hypertropia (HTDHT) is unclear. In this study, magnetic resonance imaging (MRI) was used to study extraocular muscle (EOM) responses to head tilt in HTDHT.
Methods.
Orbital MRI was used to study 16 normal subjects and 22 subjects with HTDT, of whom 12 had unilateral SO atrophy and 10 had “masquerading” SO palsy with normal SO size. Sizes and paths of all EOMs were compared in 90° roll tilts.
Results.
Normal subjects exhibited the expected 3° to 7° physiologic extorsion of all four rectus pulleys in the orbit up-versus-down roll positions, corresponding to ocular counterrolling. In orbits with SO atrophy, the lateral (LR) and inferior rectus (IR) pulleys paradoxically intorted by approximately 2°. Subjects with HTDHT but normal SO size exhibited reduced or reversed extorsion of the medial, superior, and LR pulleys, whereas pulley shift was normal in nonhypertropic fellow orbits in HTDHT. In normal subjects and in SO atrophy, the inferior oblique (IO) muscle contracted in the orbit up-versus-down roll position, but paradoxically relaxed in HTDHT without SO atrophy.
Conclusions.
The ipsilesional IR and LR pulleys shift abnormally during head tilt in HTDHT with SO atrophy. In HTDHT without SO atrophy, the ipsilesional MR, SO, and LR pulleys shift abnormally, and the IO relaxes paradoxically during head tilt. These widespread alterations in EOM pulling directions suggest that complex neural adjustments to the otolith–ocular reflexes mediate HTDHT.
doi:10.1167/iovs.10-6596
PMCID: PMC3109014  PMID: 21282574
4.  Intramuscular Innervation of Primate Extraocular Muscles: Unique Compartmentalization in Horizontal Recti 
Segregation of intramuscular motor nerves indicates distinct superior and inferior zones within the horizontal but not vertical rectus extraocular muscles in humans and monkeys, supporting a potential functional role for differential innervation that might mediate oculorotary actions.
Purpose.
It has been proposed that the lateral rectus (LR), like many skeletal and craniofacial muscles, comprises multiple neuromuscular compartments subserving different physiological functions. To explore the anatomic potential of compartmentalization in all four rectus extraocular muscles (EOMs), evidence was sought of possible regional selectivity in intramuscular innervation of all rectus EOMs.
Methods.
Whole orbits of two humans and one macaque monkey were serially sectioned at 10 μm thickness and stained with Masson's trichrome. Three-dimensional reconstruction was performed of the intramuscular courses of motor nerves from the deep orbit to the anterior extents of their arborizations within all four rectus EOMs in each orbit.
Results.
Findings concorded in monkey and human orbits. Externally to the global surface of the lateral (LR) and medial rectus (MR) EOMs, motor nerve trunks bifurcated into approximately equal-sized branches before entering the global layer and observing a segregation of subsequent arborization into superior zones that exhibited minimal overlap along the length of the LR and only modest overlap for MR. In contrast, intramuscular branches of the superior and the nasal portion of the inferior rectus were highly mixed.
Conclusions.
Consistent segregation of intramuscular motor nerve arborization suggests functionally distinct superior and inferior zones within the horizontal rectus EOMs in both humans and monkeys. Reduced or absent compartmentalization in vertical rectus EOMs supports a potential functional role for differential innervation in horizontal rectus zones that could mediate previously unrecognized vertical oculorotary actions.
doi:10.1167/iovs.10-6651
PMCID: PMC3088565  PMID: 21220556
5.  Fascicular Specialization in Human and Monkey Rectus Muscles: Evidence for Anatomic Independence of Global and Orbital Layers 
Purpose
Connective tissue pulleys inflect the extraocular muscles (EOMs) and receive insertions from some fibers. The authors investigated insertions and anatomic relationships of fiber fascicles within rectus EOMs to clarify the relationship to their pulleys.
Methods
Two human and two monkey orbits were removed intact, serially sectioned in the coronal plane, histologically stained, and digitally photographed. The authors traced representative fascicles in the human medial rectus (MR) and inferior rectus and monkey lateral rectus and superior rectus muscles. In the human MR, the authors computed average collagen fractions in the orbital layer (OL) and the global layer (GL).
Results
In human and monkey, OL fascicles remained distinct from each other and from the GL throughout. Most OL fascicles were inserted into the pulley through short tendons. Most GL fascicles bypassed the pulley without insertion. Collagen content in the human MR OL increased from 29% ± 5% (SD) in midorbit to 65% ± 9% in the anterior orbit but slightly decreased from 26% ± 6% to 23% ± 1% in the GL. Tracing of every fiber in a human MR OL fascicle demonstrated terminations on pulley tendons without myomyous junctions.
Conclusions
Fibers in the primate rectus OL lack myomyous or GL junctions, but nearly all insert on the pulley through a broad distribution of short tendons and dense intercalated collagen. Fibers in the GL generally do not insert on pulley tissues and are associated with less collagen. These features support the distinct role of the OL in anteroposterior positioning of connective tissues proposed in the active pulley hypothesis and substantial mechanical independence of the OL and GL.
doi:10.1167/iovs.06-0692
PMCID: PMC1978188  PMID: 17591878
6.  Current concepts of mechanical and neural factors in ocular motility 
Current opinion in neurology  2006;19(1):4-13.
Purpose of review
The oculomotor periphery was classically regarded as a simple mechanism executing complex behaviors specified explicitly by neural commands. A competing view has emerged that many important aspects of ocular motility are properties of the extraocular muscles and their associated connective tissue pulleys. This review considers current concepts regarding aspects of ocular motility that are mechanically determined versus those that are specified explicitly as innervation.
Recent findings
While it was established several years ago that the rectus extraocular muscles have connective tissue pulleys, recent functional imaging and histology has suggested that the rectus pulley array constitutes an inner mechanism, analogous to a gimbal, that is rotated torsionally around the orbital axis by an outer mechanism driven by the oblique extraocular muscles. This arrangement may account mechanically for several commutative aspects of ocular motor control, including Listing’s Law, yet permits implementation of non-commutative motility. Recent human behavioral studies, as well as neurophysiology in monkeys, are consistent with implementation of Listing’s Law in the oculomotor periphery, rather than centrally.
Summary
Varied evidence now strongly supports the conclusion that Listing’s Law and other important ocular kinematics are mechanically determined. This finding implies more limited possibilities for neural adaptation to some ocular motor pathologies, but indicates possibilities for surgical treatments.
PMCID: PMC1847330  PMID: 16415671
connective tissue; extraocular muscles; eye movements; Listing’s Law; ocular counter-rolling; pulleys; saccades; vestibulo-ocular reflex
7.  Nonclassical Innervation Patterns In Mammalian Extraocular Muscles 
Current eye research  2012;37(9):761-769.
Purpose
The abducens (CN6) and oculomotor (CN3) nerves (nn) enter target extraocular muscles (EOMs) via their global surfaces; the trochlear (CN4) nerve enters the superior oblique (SO) muscle on its orbital surface. Motor nn are classically described as entering the EOMs in their middle thirds. We investigated EOM innervation that does not follow the classic pattern.
Methods
Intact, whole orbits of two humans and one each monkey, cow, and rabbit were paraffin embedded, serially sectioned in coronal plane, and prepared with Masson’s trichrome and by choline acetyltransferase (ChAT) immunohistochemistry. Nerves innervating EOMs were traced from the orbital apex toward the scleral insertion, and some were reconstructed in three dimensions.
Results
Classical motor nn positive for ChAT entered rectus and SO EOMs and coursed anteriorly, without usually exhibiting recurrent branches. In every orbit, nonclassical (NC) nn entered each EOM well posterior to classical motor nn. These NC nn entered and arborized in the posterior EOMs, mainly within the orbital layer (OL), but often traveled into the global layer or entered an adjacent EOM. Other NC nn originated in the orbital apex and entered each EOM through its orbital surface, ultimately anastomosing with classical motor nn. Mixed sensory and motor nn interconnected EOM spindles.
Conclusions
EOMs exhibit a previously undescribed pattern of NC innervation originating in the proximal orbit that partially joins branches of the classical motor nn. This NC innervation appears preferential for the OL, and may have mixed supplemental motor and/or proprioceptive functions, perhaps depending upon species. The origin of the NC innervation is currently unknown.
doi:10.3109/02713683.2012.676699
PMCID: PMC3608520  PMID: 22559851
cranial nerve; eye movement; extra-ocular muscle; spindle
8.  Compartmentalized Innervation of Primate Lateral Rectus Muscle 
Innervation to monkey and human lateral rectus muscles is segregated into well-defined superior and inferior zones, so that the lateral rectus may function as two parallel muscles under separate control. Differential activation of the two lateral rectus zones could impart previously unrecognized torsional and vertical actions to this nominally “horizontal” rectus muscle, potentially resolving an important paradox in ocular kinematics.
Purpose.
Skeletal and craniofacial muscles are frequently composed of multiple neuromuscular compartments that serve different physiological functions. Evidence of possible regional selectivity in LR intramuscular innervation was sought in a study of the anatomic potential of lateral rectus (LR) muscle compartmentalization.
Methods.
Whole orbits of two humans and five macaque monkeys were serially sectioned at 10-μm thickness and stained with Masson trichrome. The abducens nerve (CN6) was traced anteriorly from the deep orbit as it branched to enter the LR and arborized among extraocular muscle (EOM) fibers. Three-dimensional reconstruction was performed in human and monkey orbits.
Results.
Findings were in concordance in the monkey and human orbits. External to the LR global surface, CN6 bifurcated into approximately equal-sized trunks before entering the global layer. Subsequent arborization showed a systematic topography, entering a well-defined inferior zone 0.4 to 2.5 mm more posteriorly than branches entering the largely nonoverlapping superior zone. Zonal innervation remained segregated anteriorly and laterally within the LR.
Conclusions.
Consistent segregation of intramuscular CN6 arborization in humans and monkeys suggests functionally distinct superior and inferior zones for the LR. Since the LR is shaped as a broad vertical strap, segregated control of the two zones could activate them separately, potentially mediating previously unappreciated but substantial torsional and vertical oculorotary LR actions.
doi:10.1167/iovs.10-5330
PMCID: PMC2941164  PMID: 20435590
9.  Increased Extraocular Muscle Strength with Direct Injection of Insulin-like Growth Factor-I 
Purpose
Previous work has demonstrated the effectiveness of insulin-like growth factor (IGF)-II in increasing force generation in extraocular muscle (EOM). Studies in the literature have suggested that IGF-I would be even more effective than IGF-II. This study was performed to assess the effects on muscle mass and force generation of IGF-I injection in adult rabbit superior rectus muscle.
Methods
Adult rabbits received a single injection of IGF-I at one of several doses into one superior rectus muscle. One week after treatment, the rabbits were euthanatized, and the superior rectus muscle from each orbit was removed. Force generation was measured using an in vitro apparatus, and injected muscles were compared with the contralateral control. A second group of animals were injected similarly, and the muscles were examined at 1 week for changes in cross-sectional area of individual myofibers.
Results
EOMs demonstrate significant numbers of cells expressing the IGF receptor. After the EOMs were injected with IGF-I, there were significant increases both in muscle force generation and cross-sectional area at all doses tested in this study. Doses of 10 and 25 μg IGF-I were most effective.
Conclusions
Direct muscular injection of IGF-I effectively increases EOM force generation without the potential biomechanical hazards of surgery such as permanently altered muscle length or insertional position on the globe.
doi:10.1167/iovs.05-1416
PMCID: PMC3039316  PMID: 16723457
10.  Physically-based Modeling and Simulation of Extraocular Muscles 
Dynamic simulation of human eye movements, with realistic physical models of extraocular muscles (EOMs), may greatly advance our understanding of the complexities of the oculomotor system and aid in treatment of visuomotor disorders. In this paper we describe the first three dimensional (3D) biomechanical model which can simulate the dynamics of ocular motility at interactive rates. We represent EOMs using “strands”, which are physical primitives that can model an EOM's complex nonlinear anatomical and physiological properties. Contact between the EOMs, the globe, and orbital structures can be explicitly modeled.
Several studies were performed to assess the validity and utility of the model. EOM deformation during smooth pursuit was simulated and compared with published experimental data; the model reproduces qualitative features of the observed non-uniformity. The model is able to reproduce realistic saccadic trajectories when the lateral rectus muscle was driven by published measurements of abducens neuron discharge. Finally, acute superior oblique palsy, a pathological condition, was simulated to further evaluate the system behavior; the predicted deviation patterns agree qualitatively with experimental observations. This example also demonstrates potential clinical applications of such a model.
doi:10.1016/j.pbiomolbio.2010.09.002
PMCID: PMC3003910  PMID: 20868704
physically-based modeling; extraocular muscle; interactive simulation; soft tissue motion; eye movement; biomechanics
11.  Functional Morphometry of Horizontal Rectus Extraocular Muscles during Horizontal Ocular Duction 
Purpose.
We explored multiple quantitative measures of horizontal rectus extraocular muscle (EOM) morphology to determine the magnetic resonance imaging (MRI) measure best correlating with duction and thus contractility.
Methods.
Surface coil coronal MRI was obtained in target-controlled central gaze and multiple positions of adduction and abduction in 26 orbits of 15 normal volunteers. Duction angles were determined by position changes of the globe-optic nerve junction. Cross-sectional areas, partial volumes, and location of peak cross-sections of the horizontal rectus EOMs were computed in contiguous image planes 2-mm thick spanning the EOM origins to the globe equator.
Results.
All measures correlated significantly with duction angle (P < 0.0001). The best measures obtainable in single image planes were the maximum change in the cross-sectional area between equivalent image planes, with coefficients of determination R2 = 0.92 for medial rectus (MR) and 0.91 for lateral rectus (LR), and percentage change in maximum cross-section with R2 = 0.79 for MR and 0.78 for LR. The best partial volume measure of contractility was the change in partial volumes in four contiguous posterior planes (R2 = 0.86 MR and for 0.89 LR), particularly when combined with the corresponding change in partial volume for the antagonist EOM (R2 = 0.95 for MR and LR).
Conclusions.
EOM morphologic changes are highly correlated with degrees of duction and thus contractility. Both changes in single-plane maximum cross-sectional areas and posterior partial volumes provide accurate, quantitative measures of EOM contractility.
Magnetic resonance morphometry of horizontal rectus extraocular muscles is highly correlated with duction angle in normal subjects, suggesting that local volume and cross-section muscle features reflect contractile state.
doi:10.1167/iovs.12-9730
PMCID: PMC3481603  PMID: 22997285
12.  Functional Anatomy of the Extraocular Muscles During Vergence 
Progress in brain research  2008;171:21-28.
Magnetic resonance imaging (MRI) now enables precise visualization of the mechanical state of the living human orbit, enabling inferences about the effects of mechanical factors on ocular kinematics. We used 3-dimensional magnetic search coil recordings and MRI to investigate the mechanical state of the orbit during vergence in humans. Horizontal convergence of 23° from a remote to a near target aligned on one eye was geometrically ideal, and was associated with lens thickening and extorsion of the rectus pulley array of the aligned eye with superior oblique muscle relaxation and inferior oblique muscle contraction. There was no rectus muscle cocontraction. Subjective fusion through a 1° vertical prism caused a clockwise (CW) torsion in both eyes, as well as variable vertical and horizontal vergences that seldom corresponded to prism amount or direction. MRI under these conditions did not show consistent torsion of the rectus pulley array, but a complex pattern of changes in rectus extraocular muscle (EOM) crossections, consistent with co-contraction. Binocular fusion during vergence is accomplished by complex, 3D eye rotations seldom achieving binocular retinal correspondence. Vergence eye movements are sometimes associated with changes in rectus EOM pulling directions, and may sometimes be associated with co-contraction. Thus, extraretinal information about eye position would appear necessary to interpret binocular correspondence, and to avoid diplopia.
doi:10.1016/S0079-6123(08)00604-3
PMCID: PMC2881303  PMID: 18718278
active pulley hypothesis; extraocular muscles; magnetic resonance imaging; pulleys; vergence
13.  Absence of Relationship between Oblique Muscle Size and Bielschowsky Head Tilt Phenomenon in Clinically Diagnosed Superior Oblique Palsy 
Purpose
To study whether the variation in maximum oblique muscle size accounts for individual variation in the Bielschowsky head tilt phenomenon (BHTP) in clinically diagnosed superior oblique (SO) palsy.
Methods
Seventeen subjects with clinically diagnosed early-onset or idiopathic SO palsy and 14 normal subjects were enrolled in the study. Magnetic resonance imaging (MRI) in coronal and sagittal planes was used for quantitative morphometry of inferior oblique (IO) and SO muscles. Maximum cross-sectional area of the SO and IO cross section at the mid-inferior rectus crossing were determined in central gaze and compared with paretic eye hypertropia on ipsilesional versus contralesional head tilt.
Results
Mean (±SD) maximum SO cross section was 18.1 ± 3.2 mm2 in normal subjects, 14.2 ± 6.8 mm2 ipsilesional to SO palsy, and 19.2 ± 4.5 mm2 contralesional to SO palsy. The ipsilesional SO cross section was significantly smaller than the contralesional (P = 0.004) and normal (P = 0.01) ones. The mean IO cross section was 18.3 ± 3.5 mm2 in normal subjects, 21.3 ± 7.9 mm2 ipsilesional to SO palsy (P = 0.43), and 22.0 ± 6.7 mm2 contralesional to SO palsy (P = 0.26). Hyperdeviation varied with head tilt by 20.1 ± 5.5° in subjects with SO atrophy, and 10.3 ± 5.6° in subjects without SO atrophy (P = 0.003). Although oblique muscle cross sections did not correlate with BHTP, subjects with clinically diagnosed SO palsy segregated into groups exhibiting normal versus atrophic SO size.
Conclusions
SO size does not account for the variation in BHTP in clinically diagnosed SO palsy, supporting the proposition that the BHTP is nonspecific for SO function.
doi:10.1167/iovs.08-2393
PMCID: PMC2839068  PMID: 18791177
14.  Clinico-Radiologic Findings of Entrapped Inferior Oblique Muscle in a Fracture of the Orbital Floor 
A 51-year old man presented with vertical and torsional diplopia after reduction of a blowout fracture at another hospital one year ago. He had no anormalies of head position and 14 prism diopters (PD) right hypertropia (RHT) in the primary position. In upgaze no vertical deviation was found, and hyperdeviation on downgaze was 35PD. Bielschowsky head tilt test showed a negative response. Distinct superior oblique (SO) and inferior rectus (IR) underaction of the right eye was noted but IO overaction was mild on the ocular version test. Double Maddox rod test (DMRT) revealed 10-degree extorsion, but fundus extorsion was minimal in the right eye.
Thin-section coronal CT scan showed that there was no fracture line on the anterior orbital floor, but a fracture remained on the posterior orbital floor. Also, the anterior part of the right inferior oblique muscle was vertically reoriented and the medial portion of the inferior oblique muscle was not traced on the coronal CT scan. The patient underwent 14 mm right IO recession and 3 mm right IR resection. One month after the surgery, his vertical and torsional diplopia were eliminated in the primary position.
doi:10.3341/kjo.2009.23.3.224
PMCID: PMC2739963  PMID: 19794954
Blow-out Fracture; Restrictive Strabismus
15.  Effects of Hyperthyroidism on the Rectus Muscles in Mice 
Background: Structural details of vertebrate extraocular muscles (EOMs) have shown an anatomically and functionally distinct laminar organization into an outer orbital (OL) and an inner global layer (GL). Since hyperthyroidism alters tissue oxidative metabolism through mitochondrial enzymes, it is expected that structural/mitochondrial changes may be seen in hyperthyroid EOMs. We investigated the alterations in the laminar organization and mitochondrial changes in hyperthyroid mouse EOMs. Methods: Hyperthyroidism was induced in C57BL/6 mice and fresh rectus muscles were obtained to identify functional mitochondria using MitoTracker® Green and confocal microscopy; frozen sections from rectus muscles were stained with anti-rabbit Troponin T (selectively present in the OL) to demonstrate changes in the OL and GL of the EOMs. Ultrastructural features of EOMs were studied using transmission electron microscopy (TEM). Results: Of all four rectus EOMs studied, the maximum change was seen in the inferior rectus muscle (IR) followed by medial rectus (MR). Myofiber cross-sectional area measurements and Troponin T staining in the control IR EOMs demonstrated a smaller OL (113.2 ± 3.66 μm2) and higher density staining with Troponin T (90%) and a larger GL (411 ± 13.84 μm2) with low intensity staining (10%), while hyperthyroidism resulted in an increased OL (205.9 ± 5.3 μm2) and decreased GL (271.7 ± 7.5 μm2) p = 0.001. Confocal microscopy demonstrated an intense staining especially in the outer rims in the hyperthyroid IR which was confirmed by TEM showing structural alterations in the mitochondria and a subsarcolemmal migration. Conclusions: The outer, thinner, OL of the mouse EOM contains smaller diameter myofibers and fewer mitochondria while the inner, larger GL contains larger diameter myofibers and larger density of mitochondria. Hyperthyroidism results in a significant alteration in the laminar organization and mitochondrial alterations of mouse EOMs.
doi:10.3389/fneur.2010.00143
PMCID: PMC3015165  PMID: 21212842
hyperthyroid mice; orbital layer; global layer; extraocular muscles; inferior rectus; Troponin T; mitochondria
16.  High-resolution magnetic resonance imaging demonstrates reduced inferior oblique muscle size in isolated inferior oblique palsy 
PURPOSE
The diagnosis of isolated inferior oblique muscle palsy is controversial for 2 reasons: first, clinical findings seem inconsistent with our current understanding of oculomotor neuro-anatomy and, second, similar findings can occur with other causes. Because denervated extraocular muscles atrophy, we used high-resolution magnetic resonance imaging (MRI) to assess inferior oblique muscle size in patients with clinically suspected inferior oblique muscle palsy.
METHODS
A diagnosis of inferior oblique muscle palsy in 6 patients (4 unilateral, 2 bilateral) was made clinically. High-resolution coronal and sagittal orbital MRI were obtained in subjects with clinical inferior oblique muscle palsy and in 30 age-matched control subjects. Cross sections of the inferior oblique, inferior rectus (IR), and medial rectus muscles were determined together because each is innervated by the common inferior division of the oculomotor nerve. No subject had pupillary abnormalities or other extraocular muscle weakness or restriction.
RESULTS
Mean cross-sectional area of the affected inferior oblique muscle (n = 8) at the midpoint of the inferior rectus muscle was 10.2 ± 1.05 mm2, which was significantly smaller than the value of 18.8 ± 3.6 mm2 for control subjects (n = 58, p < 0.00001). Unilaterally affected inferior oblique muscles were significantly smaller than unaffected inferior oblique muscles (p < 0.05). Mean medial rectus muscle cross section (n = 8) ipsilateral to the affected inferior oblique muscle was 36.8 ± 2.4 mm2, which was not significantly different from the 35.1 ± 3.7 mm2 value for the medial rectus muscles of control subjects (n = 61, p > 0.1). Mean inferior rectus muscle cross section (n = 8) ipsilateral to the affected inferior oblique muscle was 32.5 ± 2.3 mm2, which was significantly greater than the 29.9 ± 3.3 mm2 measurement for the control subjects (n = 61, p < 0.01).
CONCLUSIONS
We used MRI to demonstrate reduced inferior oblique muscle size in patients with clinically diagnosed inferior oblique muscle palsy, supporting the concept of isolated inferior oblique muscle weakness.
doi:10.1016/j.jaapos.2008.06.012
PMCID: PMC2882439  PMID: 18835733
17.  Magnetic Resonance Imaging of the Effects of Horizontal Rectus Extraocular Muscle Surgery on Pulley and Globe Positions and Stability 
Purpose
Magnetic resonance imaging (MRI) was used to determine the effect of recessions and resections on horizontal extraocular muscle (EOM) paths and globe position.
Methods
Four adults with horizontal strabismus underwent contrast-enhanced, surface-coil MRI in central, secondary, and tertiary gazes, before and after horizontal EOM recessions and/or resections. EOM paths were determined from 2-mm thickness, quasicoronal MRI by analysis of cross-sectional area centroids in a normalized, oculocentric coordinate system. Globe displacement was determined by measuring the apparent shift of the bony orbit in eccentric gaze.
Results
In all subjects, the anteroposterior positions of the horizontal rectus pulleys shifted by less than 2 mm after surgery, indistinguishable from zero within measurement precision. In three subjects who underwent medial rectus (MR) recession or resection, postoperative globe position was similar in central gaze, but globe translation during vertical gaze shift changed markedly. There was no effect on globe translation in the subject who underwent only lateral rectus (LR) resection.
Conclusions
Recessions and resections of horizontal EOMs have minimal effect on anteroposterior EOM pulley positions. Because the pulley does not shift appreciably despite large alterations in the EOM insertion, the proximity of a recessed EOM to its pulley would be expected to introduce torsional and vertical actions in tertiary gazes. Connective tissue dissection during MR surgery may destabilize the globe’s vertical translational stability within the orbit, potentially changing the effective pulling directions of the rectus EOMs in vertical gazes. These changes may mimic oblique muscle dysfunction. LR surgery may avoid globe destabilization.
doi:10.1167/iovs.05-0498
PMCID: PMC1850672  PMID: 16384961
18.  Effects of Recession versus Tenotomy Surgery without Recession in Adult Rabbit Extraocular Muscle 
The EOMs are particularly adaptive to changes induced by recession and tenotomy surgery, responding with modulations in fiber remodeling and myosin expression and also with changes in antagonist and contralateral muscles. These results suggest the possibility that these processes are manipulated immediately after surgery to improve surgical success rates.
Purpose.
Surgical recession of an extraocular muscle (EOM) posterior to its original insertion is a common form of strabismus surgery, weakening the rotational force exerted by the muscle on the globe and improving eye alignment. The purpose of this study was to assess myosin heavy chain (MyHC) isoform expression and satellite cell activity as defined by Pax7 expression in recessed EOMs of adult rabbits compared with that in muscles tenotomized but not recessed and with that in normal control muscles.
Methods.
The scleral insertion of the superior rectus muscle was detached and sutured either 7 mm posterior to its original insertion site (recession surgery) or at the same site (tenotomy). One day before euthanatization, the rabbits received bromodeoxyuridine (BrdU) injections. After 7 and 14 days, selected EOMs from both orbits were examined for changes in fast, slow, neonatal, and developmental MyHC isoform expression, Pax7 expression, and BrdU incorporation.
Results.
Recession and tenotomy surgery resulted in similar changes in the surgical EOMs. These included a decreased proportion of fast MyHC myofibers, an increased proportion of slow MyHC myofibers, and increased BrdU-positive satellite cells. Similar changes were seen in the non-operated contralateral superior rectus muscles. The ipsilateral inferior rectus showed reciprocal changes to the surgical superior rectus muscles.
Conclusions.
The EOMs are extremely adaptive to changes induced by recession and tenotomy surgery, responding with modulations in fiber remodeling and myosin expression. These adaptive responses could be manipulated to improve surgical success rates.
doi:10.1167/iovs.10-5523
PMCID: PMC3061502  PMID: 20538996
19.  Microdissection of guinea pig extraocular muscles 
The guinea pig, a widely used experimental animal, has been used in myopia research in recent years. The structure of the extraocular muscles is important in research on eyeball movement, regulation of movement, binocular vision and surgical intervention. In this study, the anatomy and the structure of the extraocular muscles of guinea pigs were investigated. Five guinea pig eyes were dissected under a surgical microscope immediately after sacrifice, and an additional five were fixed in 10% formaldehyde solution and dissected under a surgical microscope 1 week after sacrifice. The guinea pig eye has seven extraocular muscles: two medial rectus muscles, one superior rectus muscle, one inferior rectus muscle, one superior oblique muscle and one inferior oblique muscle. The retractor bulbi muscle fibers surround the optic nerve longitudinally and insert circumferentially into the posterior pole of the eyeball. The lateral rectus was not found. Our results showed that there is a disparity between the structure of guinea pig extraocular muscles and that of humans.
doi:10.3892/etm.2011.341
PMCID: PMC3440814  PMID: 22977641
extraocular muscles; guinea pig; microdissection
20.  Enhanced Vertical Rectus Contractility by Magnetic Resonance Imaging in Superior Oblique Palsy 
Archives of Ophthalmology  2011;129(7):904-908.
Objective
To seek evidence for causative secondary changes in extraocular muscle volume, cross-sectional area, and contractility in superior oblique (SO) palsy using magnetic resonance imaging, given that vertical deviations in SO palsy greatly exceed those explained by loss of SO vertical action alone.
Methods
High-resolution, quasi-coronal orbital magnetic resonance images in target-controlled central gaze, supraduction, and infraduction were obtained in 12 patients with chronic unilateral SO palsy and 36 age-matched healthy volunteers using an 8-cm field of view and 2-mm slice thickness. Digital image analysis was used to quantify rectus extraocular muscle and SO cross-sectional areas and volumes. Measurements were compared with those of controls in central gaze to detect hypertrophy or atrophy and during vertical gaze changes to detect excess contractility.
Results
In central gaze, the paretic SO was significantly atrophic (P<.001) and the contralesional superior rectus (SR) was significantly hypertrophic (P=.02). Across the range of vertical duction from supraduction to infraduction, both the contralesional SR (P=.04) and inferior rectus (P=.001) exhibited significantly supernormal contractile changes in maximum cross-sectional area. Contractile changes in the ipsilesional SR and inferior rectus exhibited a similar but insignificant trend (.08
Conclusions
Central gaze hypertrophy of the contralesional SR may be secondary to chronic excess innervation to compensate for relative hypotropia of this eye. Supernormal contralesional SR and inferior rectus contractility suggests that dynamic patterns of abnormal innervation to vertical rectus extraocular muscles may contribute to large hypertropias often observed in SO palsy.
doi:10.1001/archophthalmol.2011.152
PMCID: PMC3286651  PMID: 21746981
The extraocular muscles (EOM), the effector arm of the ocular motor system, have a unique embryological origin and phenotype. The naked mole-rat (NMR) is a subterranean rodent with an underdeveloped visual system. It has not been established if their ocular motor system is also less developed. The NMR is an ideal model to examine the potential codependence of oculomotor and visual system development and evolution. Our goal was to compare the structural features of NMR EOMs to those of the mouse, a similar sized rodent with a fully developed visual system. Perfusion-fixed whole orbits and EOMs were dissected from adult NMR and C57BL mice and examined by light and electron microscopy. NMR orbital anatomy showed smaller EOMs in roughly the same distribution around the eye as in mouse and surrounded by a very small Harderian gland. The NMR EOMs did not appear to have the two-layer fiber distribution seen in mouse EOMs; fibers were also significantly smaller (112.3 ± 46.2 vs. 550.7 ± 226sq μm in mouse EOMs, *P<0.05). Myofibrillar density was less in NMR EOMs, and triad and other membranous structures were rudimentary. Finally, mitochondrial volume density was significantly less in NMR EOMs than in mouse EOM (4.5%± 1.9 vs. 21.2%± 11.6 respectively, *P<0.05). These results demonstrate that NMR EOMs are smaller and less organized than those in the mouse. The “simpler” EOM organization and structure in NMR may be explained by the poor visual ability of these rodents, initially demonstrated by their primitive visual system.
doi:10.1002/ar.21107
PMCID: PMC3086521  PMID: 20186962
extraocular muscle; Heterocephalus glaber; naked mole-rat; mitochondria
Traditional evaluation of strabismus has included cover test measurements, evaluation of the range of ocular rotations, and an array of subjective sensory tests. These studies could not always differentiate paresis of an extraocular muscle from restrictions and from various neuro-ophthalmic motility disorders. The measurement of horizontal and vertical saccadic movements can provide an objective test of rectus muscle function. Using EOG, saccades can be recorded easily, inexpensively, and repeatably at any age. In ocular muscle paresis or paralysis, saccadic speed is reduced mildly to markedly and can be used to monitor recovery. Assessment of saccadic velocity does not appear useful in evaluating superior oblique palsy, although it is valuable in sixth nerve palsy, Duane's syndrome, and third nerve palsy. When restrictions are the major cause of limited rotation, as in thyroid ophthalmopathy and orbital floor fracture, saccadic speed is unaffected. The induction of OKN or vestibular nystagmus is helpful in the study of children too young to perform voluntary saccadic movements. In patients with limitation of elevation or depression, this technique can separate innervational from mechanical causes of diminished rotation. The specific saccadic velocity pattern in myasthenia gravis, progressive external ophthalmoplegia, internuclear ophthalmoplegia, and Möbius' syndrome is helpful in differentiating these disorders from other neuroophthalmic motility problems. Transposition surgery of the rectus muscle is effective because of an increase in force, seen as an improvement in saccadic velocity and resulting from the change of insertion of the muscles. Saccadic velocities can also be of assistance in diagnosing a lost or disinserted muscle following surgery for strabismus. Although analysis of saccadic velocity is not required for the proper evaluation of all problems in strabismus and motility, it can be of inestimable value in the diagnosis of many complex and confusing disorders. Together with forced duction testing, a clinical profile can be obtained concerning muscle force and muscle and orbital restrictions, which are required information for appropriate surgical planning.
Images
PMCID: PMC1312465  PMID: 6676980
Purpose
Structural abnormalities of extraocular muscles (EOMs) or their pulleys are associated with some forms of human strabismus. This experiment was conducted to investigate whether such abnormalities are associated with artificial or naturally occurring strabismus in monkeys.
Methods
Binocular alignment and grating visual acuities were determined in 10 monkeys representing various species using search coil recording and direct observations. Four animals were orthotropic, two had naturally occurring “A”-pattern esotropia, two had concomitant and one had “V”-pattern esotropia artificially induced by alternating or unilateral occlusion in infancy, and one had “A”-pattern exotropia artificially induced by prism wear. After euthanasia, 16 orbits were examined by high-resolution magnetic resonance imaging (MRI) in the quasicoronal plane. Paths and sizes of horizontal rectus EOMs were analyzed quantitatively in a standardized coordinate system. Whole orbits were then serially sectioned en bloc in the quasicoronal plane, stained for connective tissue, and compared with MRI. Nerve and EOM features were analyzed quantitatively.
Results
Quantitative analysis of MRI revealed no significant differences in horizontal rectus EOM sizes or paths among orthotropic or naturally or artificially strabismic monkeys. Histologic examination demonstrated no differences in EOM size, structure, or innervation among the three groups, and no differences in connective tissues in the pulley system. The accessory lateral rectus (ALR) EOM was present in all specimens, but was small, inconsistently located, and sparsely innervated. Characteristics of the ALR did not correlate with strabismus.
Conclusions
Major structural abnormalities of horizontal rectus EOMs and associated pulleys are unrelated to natural or artificial horizontal strabismus in the monkeys studied. The ALR is unlikely to contribute to horizontal strabismus in primates. However, these findings do not exclude a possible role of pulley abnormalities in disorders such as cyclovertical strabismus.
doi:10.1167/iovs.06-0662
PMCID: PMC1975407  PMID: 17525187
Purpose
A common treatment for motility disorders of the extraocular muscles (EOMs) is a resection procedure in which there is surgical shortening of the muscle. This procedure results in rotation of the globe toward the resected muscle, increased resting tension across the agonist–antagonist pair, and stretching of the elastic components of the muscles. In the rabbit, due to orbital constraints and limited rotation, resection results in more significant stretch of the surgically treated muscle than the antagonist. This surgical preparation allows for the examination of the effects of surgical shortening of one rectus muscle and passive stretch of its ipsilateral antagonist.
Methods
The insertional 6 mm of the superior rectus muscles of adult rabbits were resected and reattached to the original insertion site. After 7 and 14 days, the animals were injected intraperitoneally with bromodeoxyuridine (BrdU) every 2 hours for 12 hours, followed by a 24-hour BrdU-free period. All superior and inferior rectus muscles from both globes were examined for BrdU incorporation, MyoD expression, neonatal and developmental myosin heavy chain (MyHC) isoform expression, and myofiber cross-sectional area alterations.
Results
In the resected muscle and in the passively stretched antagonist muscle, there was a dramatic increase in the number of myofibers positive for neonatal MyHC and in the number of BrdU- and MyoD-positive satellite cells. The addition of BrdU-positive myonuclei increased from 1 per 1000 myofibers in cross sections of control muscles to 2 to 3 per 100 myofibers in the resected muscles. Single myofiber reconstructions showed that multiple BrdU-positive myonuclei were added to individual myofibers. Addition of new myonuclei occurred in random locations along the myofiber length of single fibers. There was no correlation between myofibers with BrdU-positive myonuclei and neonatal MyHC isoform expression.
Conclusions
Both active and passive stretch of the rectus muscles produced by strabismus surgery dramatically upregulated the processes of satellite cell activation, integration of new myonuclei into existing myofibers, and concomitant up-regulation of immature myosin heavy chain isoforms. Understanding the effects of strabismus surgery on muscle cell biological reactions and myofiber remodeling may suggest new approaches for improving surgical outcomes.
doi:10.1167/iovs.05-1069
PMCID: PMC1780261  PMID: 16431957
American journal of ophthalmology  2006;143(2):280-287.
Purpose
The etiology of third nerve palsy is usually diagnosed by history, motility examination, and presence of lid and pupil involvement, as well as cranial and vascular imaging. We used high-resolution magnetic resonance imaging (hrMRI) of the oculomotor nerve and affected extraocular muscles (EOMs) to investigate oculomotor palsy.
Design
Prospective, noncomparative, observational case series in an academic referral setting.
Methods
Twelve patients with non-aneurysmal oculomotor palsy of duration 0.75 to 252 months were studied. In the orbit and along the intracranial oculomotor nerve, hrMRI at 1–2mm thickness was performed. Coronal plane images of each orbit were obtained in multiple, controlled gaze positions. Structural abnormalities of the oculomotor nerve and associated changes in EOM volume and contractility were evaluated.
Results
Cases were categorized as tumor-related, congenital, diabetic, traumatic, and idiopathic according to clinical characteristics and hrMRI findings. Reduction of volume and contractility of affected EOMs were noted in six patients; however, there was no significant EOMs atrophy in two cases with diabetic oculomotor palsy, and four cases with aberrant regeneration. hrMRI demonstrated the oculomotor nerve at the midbrain and at EOMs in all cases, and in two case with previous normal neuroimaging elsewhere demonstrated contrast-enhancing tumors on the oculomotor nerve. One patient with apparently unilateral congenital inferior division oculomotor palsy had no detectable ipsilateral and a hypoplastic contralateral oculomotor nerve exiting the midbrain.
Conclusions
hrMRI provides valuable information in patients with oculomotor palsy, such as structural abnormalities of the orbit and oculomotor nerve, and atrophy and diminished contractility of innervated EOMs. This information could be helpful in diagnosis and management of oculomotor palsy.
doi:10.1016/j.ajo.2006.10.035
PMCID: PMC1850712  PMID: 17173848

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