Mechanics of the Orbita

Abstract

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 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.

Visuomotor Velocity Transformations for Smooth Pursuit Eye Movements

“…Previous studies have suggested that the brain might not perform explicit visuomotor transformations for eye movements at all, but that the extraocular muscle properties could account for the observed effects through the use of pulleys (Demer 2006(Demer , 2007. In theory, at least part of the visuomotor velocity transformation for eye movements could be implemented mechanically, such as by the half-angle rule (Klier et al 2006).…”

“…The traditional view of how smooth pursuit eye movements are initiated involves computing a two-dimensional (2D) velocitybased motor plan from the retinal slip information, which is then used to drive the 3D ocular plant (Angelaki and Hess 2004;Dicke and Thier 1999;Ghasia et al 2008;Klier et al 2006;Tweed et al 1992). This view proposes that 3D behavioral constraints such as Listing's law, which allows for 2D control of a 3D plant, are implemented through the extraocular muscle-pulley system (Demer 2004(Demer , 2006(Demer , 2007Quaia and Optican 1998). Whether Listing's law is indeed implemented through the extraocular muscle-pulley system or rather is actively controlled by neurons in the brain is still under debate (Dimitrova et al 2003;McClung et al 2006).…”

Compartmentalization of extraocular muscle function

“…1 Pulleys simplify ocular kinematics, the rotational properties of the eyes that would otherwise be unmanageable for the brain. In particular, rectus pulleys are shifted by their corresponding orbital layers to implement mechanically [2][3][4] Listing's Law (LL) of ocular torsion. 3,4 With head upright and stationary, LL specifies ocular cycloposition as that reached by rotation about an axis lying in a unique plane.…”

“…In particular, rectus pulleys are shifted by their corresponding orbital layers to implement mechanically [2][3][4] Listing's Law (LL) of ocular torsion. 3,4 With head upright and stationary, LL specifies ocular cycloposition as that reached by rotation about an axis lying in a unique plane. 5 A formerly attractive belief that the brain explicitly commands LL torsion via the vertical rectus and oblique EOMs 6 was rendered untenable by findings that cyclovertical motor neurons of monkeys do not encode LL torsion during pursuit, 7 and that abducens nerve stimulation in monkeys evokes eye movements conforming to LL.…”

“…5 A formerly attractive belief that the brain explicitly commands LL torsion via the vertical rectus and oblique EOMs 6 was rendered untenable by findings that cyclovertical motor neurons of monkeys do not encode LL torsion during pursuit, 7 and that abducens nerve stimulation in monkeys evokes eye movements conforming to LL. 8 Rather, as systematic changes in rectus EOM pulling directions generate LL torsion, 3 activation of any whole rectus EOM must evoke an eye movement conforming to LL. However, this mechanical constraint engendered a conundrum; while the vestibulo-ocular reflex violates LL so that its velocity axis changes by one-fourth eye position, not half as for LL, 9 motor neurons controlling cyclovertical EOMs do not command the violation.…”