Incomitant strabismus associated with instability of rectus pulleys

PURPOSE: Connective tissue pulleys serve as functional mechanical origins of the extraocular muscles (EOMs) and are normally stable relative to the orbit during gaze shifts. This study evaluated pulley stability in incomitant strabismus. METHODS: Contiguous 2- or 3-mm thick magnetic resonance images (MRIs) perpendicular to the orbital axis spanned the anteroposterior extents of 12 orbits of six patients with incomitant strabismus. Imaging was performed in central gaze, supraduction, infraduction, abduction, and adduction. Rectus EOM paths were defined by their area centroids and plotted in a normalized, oculocentric coordinate system. Paths of EOMs ran toward the pulleys. Sharp EOM path inflections in secondary gaze indicated pulley locations in three dimensions. RESULTS: MRI revealed substantial inferior shift of the lateral rectus (LR) pulley of up to 1 mm during vertical gaze shifts in patients with axial high myopia and a posterior shift from abduction to adduction in simulated Brown syndrome. There was substantial LR pulley shift opposite the direction of vertical gaze in a subject with X-pattern exotropia who had undergone repeated LR surgery. The medial rectus (MR) pulley shifted inferiorly with gaze elevation in Marfan syndrome. Pulley instability was associated with significantly increased globe translation during gaze shifts. CONCLUSIONS: Pulley instability, resulting in EOM sideslip during ductions, occurs in some cases of incomitant strabismus. Resultant patterns of strabismus may depend on static pulley positions, pulley instability, and coexisting globe translation that alters pulley locations relative to the globe. Translational instability of pulleys and the globe could produce abnormalities in actions of otherwise normal EOMs, and connective tissue disorders causing these instabilities should be considered as potential causes of strabismus.     

Rectus extraocular muscle pulley displacement after surgical transposition and posterior fixation for treatment of paralytic strabismus.

PURPOSE: To determine the effect of rectus extraocular muscle (EOM) transposition with posterior fixation (PF), we employed magnetic resonance imaging (MRI) to demonstrate pulley inflections in EOM paths before and after surgery in patients with paralytic strabismus. DESIGN: Consecutive interventional case series. METHODS: Five consecutive patients (three males and two females with a mean age 52 years, range 33 to 77 years) with paralytic strabismus were studied prospectively before and more than 6 weeks after EOM transposition and PF by means of contiguous cross-sectional MRI obtained in planes perpendicular to the long axis of the orbit. Muscle paths were determined in three dimensions (3-D) for each EOM by analysis of cross-sectional area centroids in normalized, oculocentric coordinate systems. RESULTS: Four patients underwent full tendon transposition with PF of the vertical rectus EOMs. One other patient underwent full tendon transposition without PF of the horizontal rectus EOMs superiorly. For transpositions with PF, there was a large displacement of EOM path in central (straight ahead) gaze beginning in the posterior orbit. After surgical transposition, clear inflections representing pulley locations of the superior, medial, and lateral rectus paths occurred in central gaze. There was no clear path inflection for the inferior rectus in central gaze, but there was a small inflection in adduction. After all transpositions, the globe center shifted away from the transposed insertions. CONCLUSIONS: Rectus EOM transpositions with PF shift EOM pulleys posteriorly and in the directions of the transposed EOM tendons, while translating the globe center. These changes may explain the superior effectiveness of PF in increasing duction towards the transposition.     

Three-dimensional location of human rectus pulleys by path inflections in secondary gaze positions

PURPOSE: Connective tissue pulleys serve as the functional mechanical origins of the extraocular muscles (EOMs). Anterior to these pulleys, EOM paths shift with gaze to follow the scleral insertions, whereas posterior EOM paths are stable in the orbit. Inflections in EOM paths produced by gaze shifts can be used to define the functional location of pulleys in three dimensions (3-D). METHODS: Contiguous magnetic resonance images in planes perpendicular to the orbital axis spanned the anteroposterior extents of 22 orbits of 11 normal adults with the eyes in central gaze, elevation, depression, abduction, and adduction. Mean EOM cross-sectional area centroids represented in a normalized, oculocentric coordinate system were plotted over the length of each EOM to determine paths. Path inflections were identified to define pulley locations in 3-D. RESULTS: All rectus EOM paths exhibited in secondary gaze positions distinct inflections 3 to 9 mm posterior to globe center, which were consistent across subjects. The globe center and the lateral rectus pulley translated systematically in the orbit with lateral gaze, whereas other pulleys remained stable relative to the orbit. CONCLUSIONS: Distinct inflections in rectus EOM paths in secondary gaze positions confirm the existence of pulleys and define their locations in 3-D. The globe and lateral rectus pulley translate systematically with gaze position. The EOM pulleys may simplify neural control of eye movements by implementing a commutative ocular motor plant in which commands for 3-D eye velocity are effectively independent of eye position.     

Effect of aging on human rectus extraocular muscle paths demonstrated by magnetic resonance imaging

PURPOSE: To compare normal functional anatomy of rectus extraocular muscles (EOMs) and pulleys in normal older humans with previously reported findings in younger subjects. DESIGN: Experimental study of the orbits of normal healthy older volunteers by magnetic resonance imaging (MRI). METHODS: In planes perpendicular to the orbital axis, contiguous MRI images spanned the anteroposterior extents of 22 orbits in 12 older adults with an average age of 65.2 years (range, 56-74). Images were obtained in central gaze in all subjects and repeated in supraduction, infraduction, abduction, and adduction in some subjects. Mean EOM cross-sectional area centroids were normalized to an oculocentric coordinate system and plotted over the length of each EOM to determine paths. RESULTS: Compared with images obtained using identical technique in 12 younger subjects (average age, 28.5 years, range 21-33), the horizontal rectus EOMs in the 12 older subjects were significantly displaced inferiorly throughout the anteroposterior extent of the orbit. The vertical rectus EOM was positioned identically to those of younger subjects. Inflections in EOM paths produced by the connective tissue pulleys could not be determined in most older subjects, because of difficulties in maintaining extreme eccentric gaze. For one subject who was able to do this, the anteroposterior location of the medial rectus pulley inferred from path inflection was similar to that of younger subjects. CONCLUSIONS: The horizontal rectus EOMs are displaced inferiorly in the elderly relative to the globe center. This displacement presumably reflects an inferior location of the corresponding pulleys, partially converting horizontal rectus EOM force to depression. This may contribute to the observed impairment of elevation in older people and predispose them to a characteristic pattern of incomitant strabismus.     

Active pulleys: magnetic resonance imaging of rectus muscle paths in tertiary gazes

PURPOSE: The orbital layer of each rectus extraocular muscle (EOM) inserts on connective tissue, and the global layer inserts on the eyeball. The active-pulley hypothesis (APH) proposes that a condensation of this connective tissue constitutes a pulley serving as the functional origin of the rectus EOM, and that this pulley makes coordinated, gaze-related translations along the EOM axis to implement a linear ocular motor plant. This study was designed to measure gaze-related shifts in EOM pulley locations. METHODS: Magnetic resonance imaging (MRI) was performed in eight normal volunteers in 2-mm thickness coronal planes perpendicular to the orbital axis for nine cardinal gaze directions. Intravenous gadodiamide contrast was administered to define EOM tendons anterior to the globe equator. Paths of EOMs, defined by their area centroids, were transformed into an oculocentric coordinate system. Sharp inflections in EOM paths in secondary and tertiary gaze positions defined pulley locations which were then correlated with gaze direction and compared with theoretical predictions. RESULTS: Rectus pulley positions were consistent with a central primary position. In tertiary gaze positions, each of the four rectus pulleys translated posteriorly with EOM contraction and anteriorly with EOM relaxation by a significant (P < 0.02) amount predicted by the APH, but more than 100 times greater than the translation predicted by a passive pulley model. CONCLUSIONS: The APH prediction of coordinated anteroposterior shifting of EOM pulleys with gaze is quantitatively supported by changes in EOM path inflections among tertiary-gaze positions. Human rectus pulleys move to shift the ocular rotational axis to attain commutative behavior of the ocular motor plant.     

Evidence for active control of rectus extraocular muscle pulleys

PURPOSE: Connective tissue structures constrain paths of the rectus extraocular muscles (EOMs), acting as pulleys and serving as functional EOM origins. This study was conducted to investigate the relationship of orbital and global EOM layers to pulleys and kinematic implications of this anatomy. 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.     

Ocular kinematics,vergence, and orbital mechanics

Important aspects of ocular kinematics relate to the geometric configuration of extraocular muscles (EOMs). The orbital layer of each rectus EOM inserts on a connective tissue ring called a pulley that deflects the EOM path. Global layer fibers of each EOM pass through the pulley to insert on the sclera. The orbital layer thus controls linear translation of the pulley, regulating the EOM's pulling direction, while the global layer rotates the eye. The active pulley hypothesis (APH) states that pulleys are actively positioned to regulate ocular kinematics. The coordinated control postulate of the APH proposes that during conjugate visually guided eye movements, rectus pulleys move the same anteroposterior distance as their insertions, but the inferior oblique pulley moves with vertical gaze by half the amount as the inferior rectus insertion. These motions, observable by magnetic resonance imaging (MRI), shift the pulling directions of these EOMs by half the ocular angle, mechanically implementing a 'linear oculomotor plant' appearing mathematically commutative to the brain and consistent with Listing's Law of ocular torsion. In the non-converged state with the head upright and stationary, rectus pulleys move little transverse to the EOM axes. During convergence and during the static torsional vestibulo-ocular reflex, MRI shows that the rectus pulley array rotates around the line of sight. Oblique EOM orbital layers may implement this shift.     

Ocular kinematics,vergence, and orbital mechanics

Important aspects of ocular kinematics relate to the geometric configuration of extraocular muscles (EOMs). The orbital layer of each rectus EOM inserts on a connective tissue ring called a pulley that deflects the EOM path. Global layer fibers of each EOM pass through the pulley to insert on the sclera. The orbital layer thus controls linear translation of the pulley, regulating the EOM’s pulling direction, while the global layer rotates the eye. The active pulley hypothesis (APH) states that pulleys are actively positioned to regulate ocular kinematics. The coordinated control postulate of the APH proposes that during conjugate visually guided eye movements, rectus pulleys move the same anteroposterior distance as their insertions, but the inferior oblique pulley moves with vertical gaze by half the amount as the inferior rectus insertion. These motions, observable by magnetic resonance imaging (MRI), shift the pulling directions of these EOMs by half the ocular angle, mechanically implementing a ‘linear oculomotor plant’ appearing mathematically commutative to the brain and consistent with Listing’s Law of ocular torsion. In the non-converged state with the head upright and stationary, rectus pulleys move little transverse to the EOM axes. During convergence and during the static torsional vestibulo-ocular reflex, MRI shows that the rectus pulley array rotates around the line of sight. Oblique EOM orbital layers may implement this shift.     

正常人眼球直肌Pulley功能位置的动态磁共振成像研究

目的研究正常人眼球运动动态磁共振成像（MRI）4条直肌Pulley（滑车）的功能性位置。方法采用西门子公司Sonata1.5T超导型MRI扫描仪,应用眼球运动动态MRI技术,获取20名正常人（20个眼眶）眼球原在位及上转、下转、内转、外转20度时垂直于眶轴的眼眶冠状位MRI图像。以眼球中心为原点建立三维坐标系,应用ScionImage医学图像测量软件分别测量各层面眼球垂直转动时水平直肌、眼球水平转动时垂直直肌的横截面质心。根据各层面直肌横截面质心的坐标值建立直线回归方程,分别求得眼球垂直转动时内、外直肌径路及眼球水平转动时上、下直肌径路直线回归曲线斜率变化最大的一点,即为该直肌Pulley的功能性位置。对4条直肌Pulley相对于眼球中心的坐标值（X、Y）进行统计。结果内直肌Pulley位于眼球中心后4mm,内14.7mm,下0.3mm;外直肌Pulley位于眼球中心后8mm,外9.8mm,下0.3mm;上直肌Pulley位于眼球中心后6mm,内1.6mm,上11.5mm;下直肌Pulley位于眼球中心后6mm,内4.4mm,下12.7mm。结论应用眼球运动动态MRI技术,分析眼球转动时直肌径路的变化,可证实4条直肌Pulley的存在并确定其功能位置。     

Quantitative analysis of the structure of the human extraocular muscle pulley system

PURPOSE: Extraocular muscle (EOM) paths are constrained by connective tissue pulleys serving as functional origins. The quantitative structural features of pulleys and their intercouplings and orbital suspensions remain undetermined. This study was designed to quantify the composition of EOM pulleys and suspensory tissues. METHODS: Five human orbits, ages 33 weeks gestation to 93 years, were imaged intact by magnetic resonance (MRI), serially sectioned at 10 micro m thickness, and stained for collagen, elastin, and smooth muscle (SM). With MRI used as a reference, digital images of sections were geometrically corrected for shrinkage and processing deformations, and normalized to standard normal adult globe diameter. EOM pulleys, interconnections, suspensory tissues, and entheses were quantitatively analyzed for collagen, elastin, and SM thickness and density. RESULTS: Rectus and inferior oblique pulleys had uniform structural features in all specimens, comprising a dense EOM encirclement by collagen 1 to 2 mm thick. Elastin distribution varied, but was greatest in the orbital suspension of the medial rectus pulley and in a band from it to the inferior rectus pulley. This region corresponded to maximum SM density. Structural features of pulleys, intercouplings, and entheses were similar among specimens. The major mechanical couplings to the osseous orbit were near the medial and lateral rectus pulleys. CONCLUSIONS: Quantitative analysis of structure and composition of EOM pulleys and their suspensions is consistent with in vivo MRI observations showing discrete inflections in EOM paths that shift predictably with gaze. Focal SM distributions in the suspensions suggest distinct roles in stiffening as well as shifting rectus pulleys.     

轴性高度近视眼直肌PULLEY功能位置的动态磁共振成像研究

目的用MRI研究轴性高度近视眼4条直肌pulley的功能位置,探讨轴性高度近视继发性眼球运动障碍的病因。方法轴性高度近视12例(22眼)根据眼屈光度、眼轴长度以及有无眼球运动受限分为A、B两组。A组无眼球运动受限;B组有眼球运动受限。应用动态MRI技术,获取眼球原在位及上转、下转、内转、外转位时的冠状位MRI图象。应用计算机图像处理软件测量各层面MRI图像眼球垂直方向转动时水平直肌、眼球水平方向转动时垂直直肌的横截面质心,根据其坐标值建立直线回归方程,统计求得眼球垂直转动时内、外直肌径路及眼球水平转动时上、下直肌径路直线回归曲线斜率变化最大的一点(直肌pulley的位点),将A组、B组、正常对照组进行比较。结果A组与正常对照组4条直肌pulley的位点比较无显著差异(P>0.05);B组与正常对照组内直肌、上直肌、下直肌pulley的位点比较无显著性差异(P>0.05);B组外直肌pulley的位点较正常对照组向颞下移位(P<0.01);A组与B组内直肌、上直肌、下直肌pulley的位点比较无显著性差异(P>0.05);B组较A组外直肌pulley位点向颞下移位(P<0.05)。结论外直肌pulley的位点向颞下移位可能是引起轴性高度近视眼继发性眼球运动障碍的主要病因之一。     

Magnetic resonance imaging of the extraocular muscle path before and after strabismus surgery for a large degree of cyclotorsion induced by macular translocation surgery

Purpose  To evaluate the changes in the location of the extraocular muscles (EOMs) following strabismus surgery to treat a large degree of torsional diplopia induced by macular translocation surgery. Methods  Six consecutive patients who underwent macular translocation surgery with 360° of retinotomy and subsequent strabismus surgery were studied. Magnetic resonance imaging (MRI) was performed before and after the surgery. The angle made by the line connecting the center of the orbit and the center of each rectus muscle and the horizontal was measured. The changes in these angles before and after strabismus surgery were studied. Results  The average rotation of the globe after strabismus surgery was 28° (SD = 7.21; range, 17°–39°). The average measured EOM shift was −0.3° (SD = 8.04; range, −20.4° to 20.2°). Conclusions  Despite large torsional rotation of the globe, there was no corresponding torsional repositioning of the deep paths of the rectus muscles. The paths of the operated muscles were essentially unchanged.     

Horizontal rectus muscle anatomy in naturally and artificially strabismic monkeys

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 quasi-coronal 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 quasi-coronal 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.     

Measurement of recti eye muscle paths by magnetic resonance imaging in highly myopic and normal subjects.

PURPOSE: To analyze the path of extraocular muscles (EOMs) quantitatively in highly myopic subjects with and without restricted eye motility versus control. To elucidate the cause of the acquired motility disorder in patients with high myopia. METHODS: Thirty-three orbits were imaged using a Magnetom or Siemens Vision (Siemens, Erlangen, Germany; both 1.5 Tesla) MRI (magnetic resonance imaging) scanner. Coronal T1-weighted, spin-echo images were obtained with repetition time of 550 msec and echo time of 15 msec. Subjects had to fixate in different positions of gaze. Orbits of three patient groups were analyzed: group 1 (n = 14), patients with high axial myopia and restricted eye motility (average axial length, 31.4 mm; refractive error more than -15 D); group 2 (n = 8), subjects with high axial myopia and normal eye motility (average axial length, 29.2 mm); control group (n = 11), emmetropic subjects with normal eye motility (average axial length, 23.6 mm). RESULTS: Highly myopic patients showed significant displacements of recti EOMs in comparison with control subjects. Mean displacements, measured in the plane 3 mm anterior to the globeoptic nerve junction in primary gaze, were in group 1, lateral rectus (LR) 2.9 mm (2.5 downward, 1.4 medial), medial rectus (MR) 1.3 mm downward and in group 2, LR 1.4 mm (1.3 downward, 0.6 medial) and MR 1.2 mm downward. In groups 1 and 2 the inferior rectus (IR) was displaced 1.3 mm medially and upward. In both groups of myopic patients the superior rectus (SR) was displaced 1.5 mm medially and downward. CONCLUSIONS: In patients with high axial myopia, displacements of all recti EOMs can be detected by MRI. Displacements of SR, MR, and IR were very similar in groups 1 and 2 versus control. LR displacement into the lateral and inferior quadrant of the orbit was greatest in patients with restricted eye motility. Thus, LR displacement is probably the major pathophysiological factor for the restrictive motility disorder in high myopia. EOM dislocations can be explained by myopia-associated alterations in the orbital connective tissues confining EOM positions in relation to the orbital wall.     

Magnetic resonance imaging evidence for widespread orbital dysinnervation in dominant Duane's retraction syndrome linked to the DURS2 locus

PURPOSE: High-resolution, multipositional magnetic resonance imaging (MRI) was used to demonstrate extraocular muscles (EOMs) and associated motor nerves in Duane retraction syndrome (DRS) linked to the DURS2 locus on chromosome 2. METHODS: Five male and three female affected members of two autosomal dominant DURS2 pedigrees were enrolled in the study. Coronal T(1)-weighted MRI of the orbits was obtained in multiple gaze positions, as well as with heavy T(2) weighting in the plane of the cranial nerves. MRI findings were correlated with motility. RESULTS: All subjects had unilateral or bilateral limitation of abduction, or of both abduction and adduction, with palpebral fissure narrowing and globe retraction in adduction. Orbital motor nerves were typically small, with the abducens nerve (cranial nerve [CN]6) often nondetectable. Lateral rectus (LR) muscles were structurally abnormal in seven subjects, with structural and motility evidence of oculomotor nerve (CN3) innervation from vertical rectus EOMs leading to A or V patterns of strabismus in three cases. Four cases had superior oblique, two cases superior rectus, and one case levator EOM hypoplasia. Only the medial and inferior rectus and inferior oblique EOMs were spared. Two cases had small CN3s. CONCLUSIONS: DRS linked to the DURS2 locus is associated with bilateral abnormalities of many orbital motor nerves, and structural abnormalities of all EOMs except those innervated by the inferior division of CN3. The LR may be coinnervated by CN3 branches normally destined for any other rectus EOMs. Therefore, DURS2-linked DRS is a diffuse congenital cranial dysinnervation disorder involving but not limited to CN6.     

Quantification of recti eye muscle paths in high myopia

PURPOSE To elucidate the etiology of an acquired, restrictive motility disorder in patients with high myopia. METHODS Thirty-three orbits were imaged using a Siemens Magnetom or Siemens Vision (both 1.5 Tesla) MRI (magnetic resonance imaging) scanner, applying a head coil. Coronal T1-weighted, spin-echo images were obtained. Orbits of three different patient groups were analyzed. Group 1 (n = 14): patients with high axial myopia and restricted eye motility (average axial length = 31.4mm; refractive error more than –15D). Group 2 (n = 8): subjects with high axial myopia and normal eye motility (average axial length = 29.2mm). Controls (n = 11): emmetropic subjects with normal eye motility. RESULTS Highly myopic patients showed significant displacements of recti EOMs in comparison to the controls. Mean displacements as measured in the plane 3mm anterior to the globe-optic nerve junction in primary gaze were, in group 1: lateral rectus (LR) 2.9mm (2.5 downward, 1.4 medial), medial rectus (MR) 1.3mm downward. In group 2: LR 1.4mm (1.3 downward, 0.6 medial) and MR 1.2mm downward. In both groups 1 and 2, the inferior rectus (IR) was displaced 1.3mm medially and upwards. In both groups of myopic patients the superior rectus (SR) was displaced 1.5mm medially and downwards. CONCLUSIONS In patients with high axial myopia, displacements of all recti EOMs can be detected by MRI. However, displacement of the LR into the lateral and inferior quadrant of the orbit is significantly greatest. We therefore assume LR displacement to be a major pathophysiological factor for the restrictive motility disorder in high myopia. EOM dislocations can be explained by myopia-associated alterations in the orbital connective tissues confining EOM positions in relation to the orbital wall.     

Extraocular muscle forces in alert monkey.

We describe an extraocular muscle (EOM) force transducer that provides low-noise signals from an alert animal for several months, is implanted without disinserting the muscle, and is well-tolerated by the body, and present results obtained with the device. The transducer can be used to study orbital statics and dynamics, and oculomotor control signals undiminished by orbital low-pass filtering and antagonistic pairing of muscles. It may provide an index of effective EOM innervation, useful in studies of orbital tissue healing and plasticity, and oculomotor (OM) signal adaptation. During horizontal saccades transducers implanted in the lateral rectus (LR) and medial rectus (MR) of a monkey trained to fixate revealed an agonist muscle tension waveform corresponding to the "pulse-slide-step" pattern of saccadic innervation, and an antagonist waveform that was similar within a scale factor. We never observed transient increases in antagonist force at the ends of saccades (active braking) or at the beginnings. Onset of saccadic force in LR preceded that in MR by 1.6 msec for abducting saccades, and lagged that in MR by 1.1 msec for adducting saccades. During vertical saccades, transient force changes were found in LR and MR, which were likely due, at least in part, to globe translation. LR and MR forces during fixation tended to be largest with the eye about 10 degrees in elevation, and smallest in depression, indicating that effective total innervation was a function of vertical gaze, or that there was variation in the elastic component of muscle force related to orbital geometry, with LR and MR innervation independent of vertical gaze. An exponential decrease in fixation force, having a time constant of about 10 days, was observed after implantation. This may have reflected adaptive muscle lengthening or post-surgical healing.     

Finite Element Model of Ocular Adduction by Active Extraocular Muscle Contraction

PurposeIn order to clarify the role of the optic nerve (ON) as a load on ocular rotation, we developed a finite element model (FEM) of incremental adduction induced by active contractility of extraocular muscles (EOMs), with and without tethering by the ON.MethodsThree-dimensional (3-D) horizontal rectus EOM geometries were obtained from magnetic resonance imaging of five healthy adults, and measured constitutive tissue properties were used. Active and passive strain energies of EOMs were defined using ABAQUS (Dassault Systemes) software. All deformations were assumed to be caused by EOM twitch activation that rotated the eye about a fixed center. The medial rectus (MR) muscle was commanded to additionally contract starting from 26 degrees adducted position, and the lateral rectus (LR) to relax, further adducting the eye either with or without loading by the ON. Tridimensional heat maps were generated to represent the stress and strain distributions.ResultsTensions in the EOMs were physiologically plausible during incremental adduction. Force in the MR increased from 10 gm at 26 degrees adduction to approximately 28 gm at 32 degrees adduction. Under identical MR contraction, adduction with ON loading reached 32 degrees but 36 degrees without it. Maximum and minimum principal strains within the MR were 16% and 22%, respectively, but when ON loading was included, resulting stress and strain were concentrated at the optic disc.ConclusionsThis physiologically plausible method of simulating EOM activation can provide realistic input to model biomechanical behavior of active and passive tissues in the orbit to clarify biomechanical consequences of ON traction during adduction.     

Compartmentalization of extraocular muscle function

Ocular motor diversity exceeds capabilities of only six extraocular muscles (EOMs), but this deficiency is overcome by the plethora of fibers within individual EOMs surpassing requirements of homogeneous actuators. This paper reviews emerging evidence that regions of individual EOMs can be differentially innervated to exert independent oculorotary torques, broadening the oculomotor repertoire, and potentially explaining diverse strabismus pathophysiology. Parallel structure characterizes EOM and tendon fibers, with little transverse coupling of experimentally imposed or actively generated tension. This arrangement enables arbitrary groupings of tendon and muscle fibers to act relatively independently. Coordinated force generation among EOM fibers occurs only upon potentially mutable coordination of innervational commands, whose central basis is suggested by preliminary findings of apparent compartmental segregation of abducens motor neuron pools. Humans, monkeys, and other mammals demonstrate separate, nonoverlapping intramuscular nerve arborizations in the superior vs inferior compartments of the medial rectus (MR) and lateral rectus (LR) EOMs that could apply force at the superior vs inferior portions of scleral insertions, and in the medial vs lateral compartments of the superior oblique that act at the equatorial vs posterior scleral insertions that might preferentially implement incycloduction vs infraduction. Magnetic resonance imaging of the MR during several physiological ocular motor behaviors indicates differential compartmental function. Differential compartmental pathology can influence clinical strabismus. Partial abducens palsy commonly affects the superior LR compartment more than the inferior, inducing vertical strabismus that might erroneously be attributed to cyclovertical EOM pathology. Surgery may selectively manipulate EOM compartments.