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The aim of the EOTA project is to describe the functional 3-dimensional architecture of the extraocular space, distinguishing tissue types (striated muscle, smooth muscle, collagen, elastin, ...) and mechanically cohesive structures (muscle lamina, connective tissue sheets, ...), and abstracting from these data a computationally tractible biomechanical model. We have developed methods for 3D reconstruction from thin histologic slices, and a new technique involving implanted gold bead fiducials in a behaving animal.
A slide presentation describes the rationale, methods, and some results of the project:
Below are 3D reconstructions from stained slices of 3 different human orbits, prepared as described in the slide presentations.
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In the descriptions below, we use standard abreviations for the extraocular muscles: LR = lateral rectus muscle, MR = medial rectus muscle, IR = inferior rectus muscle, SO = superior oblique muscle, and IO = inferior oblique muscle. Tissues are color coded as follows:
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Whole Orbit - Collagen, Smooth Muscle & Elastin (QTVR, 7.9MB). The full orbit showing the distribution of collagen, smooth muscle and elastin. Elastin and collagen are most dense in the anterior orbit between the crossing of the IR and IO, and the MR. |
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Anterior Medial Rectus - Collagen & Smooth Muscle (QTVR, 4.5MB). A heavy band of smooth muscle is seen between the MR and the orbital wall, perhaps serving to control the coupling of the MR to the orbital wall. (A quadrant of collagen has been removed to better visualize the smooth muscle. The MR extends more anteriorly, but becomes tendonous and so is not shown). |
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Anterior Medial Rectus - Smooth Muscle (QTVR, 6.3MB). The heavy smooth muscle band between the MR and orbital wall (shown above) is visualized at a much higher resolution. The globe has been made transparent to illustrate the smooth muscle band wrapping around the MR, a constituent of the MR pulley. |
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Anterior Medial Rectus - Collagen, Smooth Muscle & Elastin (QTVR, 6.8MB). Another sample showing pulley smooth muscle band and elastin bands surrounding the MR. |
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Anterior Lateral Rectus - Collagen (QTVR, 5.5MB). The anterior LR in the region of the globe equator is enveloped in a network of high density collagen bands which extend radially to the orbital wall. |
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Inferior Rectus crossing Inferior Oblique - Collagen & Smooth Muscle (QTVR, 4.1MB). Collagen in the region sometimes called "Lockwood's ligament" is even denser than shown -- it has been decimated and made transparent to visualize tissue relationships. |
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Inferior Rectus crossing Inferior Oblique - Collagen & Smooth Muscle (QTVR, 9.2MB). Smooth muscle density is much higher than in the sample above, and can be seen stretching from the anterior IR muscle, near its global insertion, moving superior and posterior and wrapping around the MR. |
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Inferior Rectus crossing Inferior Oblique - Elastin (QTVR, 5.0MB). Elastin distribution follows a path similar, but generally posterior, to that of the smooth muscle band illustrated above. |
Click for a related study in which we visualize human extraocular nerves, arteries and veins using computer methods.
Miller (1989) first proposed that extraocular connective tissue formed pulleys through which the EOMs passed, and collected MR images of muscle paths before and after transposition surgery to demonstrate their functional existence (Miller, et al, 1993). MRI has recently been used to locate the pulleys as a function of gaze (Clark, et al, 1997; Clark, et al, 2000).
Thus far, pulley locations have only been inferred from muscle path inflections. Except in special cases (eg, where pulley tissues are surrounded by fat) MRI cannot directly discriminate the condensations of connective and smooth muscle tissues that constitute the pulleys.
Collins (1975) demonstrated that the small fibers of an EOMs orbital lamia are active in "off" and primary positions, whereas global fibers become active only in "on" direction eccentric gaze. This suggests that orbital fibers refine primary position alignment. Recently, however, Demer proposed a different role for orbital fibers. According to the "Active Pulley Hypothesis" (APH), global fibers rotate the globe, whereas orbital fibers translate the pulley, through which the global fibers pass, and which determines their functional origin (Demer, 2000). Demers theory explains how EOM pulleys function in tertiary gaze, accounts for the "quarter-angle rule" of VOR, and the temporal tilting of Listings Plane in converged eye positions. It predicts relative shear between orbital and global EOM lamina, and relative movement between global fibers and pulley tissues, but not between orbital fibers and the pulley tissues into which they are proposed to insert.
Strabismologists and modelers have recently constructed explanations involving various other connective tissue structures, including Lockwoods Ligament (Demer and Miller, 1997; Demer and Miller, 1999), the lateral levator aponeurosis (Krzizok and Schroeder, 1999), and the neurofibrovascular bundle (Stager, 1996).
There is a pressing need to develop a general methodology to unambiguously visualize and measure the tissue movements and stretchings proposed by such theories. In monkeys trained to fixate, we plan to implant several dozen small (0.05–0.3mm) gold beads in the extraocular tissues of interest. We will then use dental X-ray equipment to image the beads, as the monkey performs various eye movement tasks.
Below is some pilot data using the gold bead technique. A series of X-ray images (presented as a QuickTime movie) show 8 beads in the region of the lateral rectus muscle (LR), viewed from the side. Even with these free eye movements it is possible to see substantial movements of the beads relative to the skull and to each other. Horizontal patterns of movement and are, no doubt, related to the stretching and contraction of the LR. The absence of overall vertical movement confirms the old finding (Miller, 1989) that muscle paths are stable in the orbit. There are interesting large relative movements of some beads, which must indicate large relative movements of tissues relative to the main, global muscle layer.
Gold Bead Fiducials in RLR (QT, 3MB). 0.3 mm diameter gold beads in right lateral rectus muscle, with free eye movements.
This work was done under consortium grant EY-08313 from the National Eye Institute to Joseph L Demer (UCLA) and Joel M Miller (S-K). Vadims Poukens (UCLA) developed the histologic methods and produced the stained sections. Dmitri S Pavlovski (formerly of S-K) developed and applied the reconstruction methods. Thomas Schiff & Jack N Hadley (UOP Dental School) helped arrange for the X-ray images.
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Extraocular Tissue Architecture (EOTA) Publications from our lab. |
