Download SEE++: A Biomechanical Model of the Oculomotor Plant

SEE++: A Biomechanical Model of the
Oculomotor Plant
T. HASLWANTER,a,b M. BUCHBERGER,a T. KALTOFEN,a R. HOERANTNER,c
AND S. PRIGLINGERc
aUpper
Austrian Research, Department for Medical Informatics, Linz, Austria
bDepartment
of Neurology, University Hospital Zurich, Switzerland
cKrankenhaus
der Barmherzigen Brüder, Linz, Austria
ABSTRACT: The consequences of changes in the oculomotor system on the
three-dimensional eye movements are difficult to grasp. Although changes to
the rectus muscles can still be approximately understood with simplified geometric models, this approach no longer works with the oblique muscles. It is
shown how SEE++, a biomechanical model of the oculomotor plant that was
built on the ideas of Miller and Robinson (1984) can improve the understanding of the effects of changes to the oblique eye muscles. By displaying only selected muscles, and by illustrating the relative contribution of these muscles
through color-coding the bulb surface, the functional properties of the oblique
muscles can be presented in a much clearer way. Investigating the effects of a
hyperactive inferior oblique muscle shows that this type of model can help to
clarify the functional cause of a pathology, which can otherwise be unclear,
even for common pathologies.
KEYWORDS: extraocular muscles; oculomotor system; computer simulation;
modeling
INTRODUCTION
Two factors determine the orientation of our eyes: the innervation of the extraocular muscles (EOMs), and the mechanical and physiological properties of the oculomotor plant. For purely horizontal eye movements close to the reference position,
the geometry of the oculomotor plant is fairly simple. As a result, this type of eye
movement has been used to investigate many aspects of the neural control of eye
movements.2 When researchers tried to understand the contributions of the individual extraocular muscles during combined horizontal/vertical eye movements, things
became more complicated.3 Although some have argued that the brain explicitly
controls all three directions of eye rotations,4 others have claimed that the mechanics
of the oculomotor system are such that only commands for the horizontal and vertical eye position need to be controlled explicitly.5,6
Address for correspondence: Dr. T. Haslwanter, UAR—Medical-Informatics, Softwarepark
Hagenberg, Hauptstrasse 99, A-4232 Hagenberg, Austria. Voice: ++43-7236-3343-676.
[email protected]
Ann. N.Y. Acad. Sci. 1039: 9–14 (2005). © 2005 New York Academy of Sciences.
doi: 10.1196/annals.1325.002
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ANNALS NEW YORK ACADEMY OF SCIENCES
Many biomechanical models supporting the more “mechanistic” view are based
on geometrical abstractions. Testing their accuracy is sometimes possible, but then
only for individual parameters.7 Anatomically more accurate models are generally
derived from original ideas by Robinson.8 These ideas were developed further by
Miller,1,15 and integrated into the first visual computer model of the oculomotor
plant, Orbit. Porrill, Warren and Dean wanted to study various aspects of this model,
which required a model that could be run in batch simulations. For this they developed EyeLab, a simplified version of Orbit written in MATLAB.9,10
As we wanted to eliminate some restrictions of Orbit, as well as add more flexibility in the visualizations, we collaborated with Miller and developed a new program, which we called SEE++. A detailed description of the technical details of
SEE++ and of the biomechanical differences between the different models is under
preparation.
METHODS
SEE++ incorporates a wide range of visualization tools, as well as different biomechanical “kernels.” As there are still discussions about the relative contribution of
different parts of the oculomotor plant, the user can choose between different options: a “string mode,” where the extraocular muscles are represented by simple
strings; a “tape mode,” which also includes muscle-stiffness (this makes a significant
difference for the side-slip of the muscle at the insertion on the globe); an “Orbit
mode,” which was made possible by Miller, who gave us full access to the source
code of Orbit; and a full mode, which provides more accurate results for pathological
eyes in eccentric eye positions.
SEE++ also allows the user to adjust the visualization to suit the current requirements. For example, in FIGURE 1 we have removed the face and all muscles but the
superior oblique. Also, we have selected the shading of the globe to reflect the horizontal eye movement contributions of the superior oblique.
RESULTS
As the consequences of changes to the oblique muscles are much more difficult
to understand than changes to the rectus muscles, we concentrate here on the obliques. In FIGURE 1 we show the left and right superior oblique (SO) muscle for a
healthy subject, when looking 30° to the left. It is obvious that a contraction of the
SO muscle of the right eye would lead to a downward movement of that eye, while
on the left eye a SO contraction would mainly induce a torsional eye movement.
For a surgical correction of an oculomotor pathology it can be important to consider all three movement components of a muscle: horizontal, vertical, and torsional.
In FIGURE 1 the horizontal component is color coded on the globes: insertion of the
SO anywhere in the white area elicits no horizontal movement; insertion in the gray
area elicits horizontal movements proportional to the gray level. Thereby horizontal
is defined as ad-/abduction. Looking 30° to the left the SO of the right eye has essentially no horizontal movement component, whereas contraction of the left SO in-
HASLWANTER et al.: SEE++
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FIGURE 1. A top view of the superior oblique muscles, when the subject looks 30° to
the left, nicely visualizes the different contributions for the left and the right eye. The shading of the bulb at the insertion point is proportional to the horizontal movement component
of the superior oblique, so that an insertion anywhere along the white area elicits no horizontal eye movement on contraction.
duces a significant amount of horizontal eye movement (FIG . 1). Without visual
indications, these insights are difficult to obtain.
As a result of the tilted insertions of the oblique muscles, a pathology caused by
hyper- or hypoactivity of an oblique EOM, or by a pathological change in the muscle
geometry of an oblique muscle, is difficult to understand. This can lead to confusion
in the terminology of diseases.
For example, for a hyperactivity of the inferior oblique, which induces predominantly a vertical strabismus, different terminologies are used on the two sides of the
Atlantic: whereas in Europe, especially in the German-speaking countries, both
terms “strabismus sursoadductorius” and “inferior oblique overaction” are used,11,12
the English-speaking literature uses the expression “primary inferior oblique overaction”13 for both vertical motility disorders. Recently, these two expressions have
been used almost synonymously.13,14
A comparison of the definitions for these two types of strabismus shows that the
two are different (TABLE 1), but the etiology is left unclear.
To find out the causal differences between these two pathologies, we tried to simulate them with SEE++.
Strabismus Sursoadductorius
To simulate strabismus sursoadductorius, we started with a lateral displacement
of the functional origin (i.e., the pulley) of the inferior oblique muscle (IO), com-
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TABLE 1. Comparison of German and English nomenclature for pathologies
involving a hyperactivity of the inferior oblique muscle
Strabismus sursoadductorius
Primary inferior oblique overaction
Concomitant vertical deviation, especially
in adduction
Excyclorotation, especially in abduction
Missing hyperdeviation in primary position
Patient indicates no cyclorotation
Positive head-tilt-test (Parks-Bielschowsky
test) in upgaze and downgaze
Negative Parks-Bielschowsky test
Small horizontal incomitance, alphabetpattern
Often alphabet-pattern
High vertical fusion
FIGURE 2. Screen shot of SEE++ for a simulation of strabismus sursoadductorius.
bined with an increase in the muscle force generated by innervation. (For the current
simulations, we doubled the active muscle force.) In addition, we sometimes added
a small lateral displacement of the functional origin of the superior oblique. This
produced the excyclorotation typically observed in patients with strabismus sursoadductorius. The exact choice of the parameters depends on the specific magnitude of
the eye movements of the patient under investigation. An example screenshot of the
resulting SEE++ display is presented in FIGURE 2.
Inferior Oblique Muscle Overaction
We were surprised to find that the eye movement patterns found in patients diagnosed with “IO overaction” could not be simulated solely with an increase in the active force of the IO: an additional medial displacement of the inferior oblique
HASLWANTER et al.: SEE++
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insertion was necessary. To reproduce the observed patterns, we also had to choose
a lateral displacement of the superior oblique muscle insertion. Again, the exact
magnitude of the parameters depends on the individual case.
DISCUSSION
Investigations of the neural control of eye movements, as well as of the mechanical contributions of the oculomotor plant, have concentrated on small horizontal or
vertical eye movements around the primary position. For such movements, an intuitive interpretation of pathologies of the oculomotor plant can often lead to acceptable results. But for arbitrary three-dimensional eye positions, the complexity of the
oculomotor plant is too large for a reliable interpretation of the cause of oculomotor
disorders. As a result, the naming of oculomotor pathologies has been in some cases
purely descriptive and sometimes somewhat arbitrary. We believe that an etiologic
naming of pathologies could facilitate the understanding of pathologies, and could
also reduce intercontinental naming incompatibilities.
In the example presented above, this inconsistency in classification has no negative consequences for the patients. Although strabismus sursoadductorius and inferior oblique muscle overaction are different, they are treated in the same way: in both
cases a recession of the inferior oblique muscle on the affected eye is recommended.
In the future, a systematic application of advanced, realistic computer models to the
investigation of oculomotor pathologies might improve our understanding of diseases, and thus help to optimize the chosen treatments.
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