Extraocular connective tissue architecture.

Extraocular muscle pulleys, now well known to be kinematically significant extraocular structures, have been noted in passing and described in fragments several times over the past two centuries. They were late to be fully appreciated because biomechanical modeling of the orbit was not available to derive their kinematic consequences, and because pulleys are distributed condensations of collagen, elastin and smooth muscle (SM) that are not sharply delineated. Might other mechanically significant distributed extraocular structures still be awaiting description?An imaging approach is useful for describing distributed structures, but does not seem suitable for assessing mechanical properties. However, an image that distinguished types and densities of constituent tissues could give strong hints about mechanical properties. Thus, we have developed methods for producing three dimensional (3D) images of extraocular tissues based on thin histochemically processed slices, which distinguish collagen, elastin, striated muscle and SM. Overall tissue distortions caused by embedding for sectioning, and individual-slice distortions caused by thin sectioning and subsequent histologic processing were corrected by ordered image warping with intrinsic fiducials. We describe an extraocular structure, partly included in Lockwood's ligament, which contains dense elastin and SM bands, and which might refine horizontal eye alignment as a function of vertical gaze, and torsion in down-gaze. This active structure might therefore be a factor in strabismus and a target of therapeutic intervention.

Missing lateral rectus force and absence of medial rectus co-contraction in ocular convergence.

For a given position of the eye in the orbit, most abducens motoneurons (LRMNs) fire at higher rates in converged gaze than when convergence is relaxed, implying that lateral rectus (LR) muscle force will be higher for a given eye position in convergence. If medial rectus (MR) muscle force balances LR force, it too would be higher in convergence, that is, LRMN recording studies predict horizontal rectus co-contraction in convergence. Three trained rhesus monkeys with binocular eye coils and custom muscle force transducers (MFTs) on LR and MR of one eye alternately fixated near (approximately 7 cm) and far (200 cm) targets with vergence movements of 20-30 degrees. Tonic muscle forces were also measured during conjugate fixation of far targets over a 30 x 30 degrees field. MFT characteristics and effects on oculomotility were assessed. Contrary to predictions, we found small (<1 g) decreases in both LR and MR forces in convergence, for those gaze positions that were used in the brain stem recording studies. This missing LR force paradox (higher LRMN firing rates in convergence but lower LR forces) suggests that motoneurons or muscle fibers contribute differently to oculorotary forces in converged and unconverged states, violating the final common path hypothesis. The absence of MR co-contraction is consistent with, and supports, the missing LR force finding. Resolution of the missing LR force paradox might involve nonlinear interactions among muscle fibers, mechanical specialization of muscle fibers and other articulations of the peripheral oculomotor apparatus, or extranuclear contributions to muscle innervation.