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Pulley and Global Stability
Author Response: Pulley and Global Stability
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Robert S. Jampel
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rjampel{at}comcast.net Robert S. Jampel
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This paper1 is part of a series of papers presenting Dr. Demer's validations and justifications for his Active Pulley Hypothesis (APH). The APH states that there is a mechanical system in the orbit that is independent of the CNS control and that the EOMs consist of two distinct, independently functioning muscle layers. An orbital layer, OL, inserts on a mobile pulley that loops around an underlying global layer, GL. By sliding back and forth over the GL, the pulley determines the functional origin of the GL. The reciprocal back-and-forth movement of the pulley is provided by striated muscle attached at its inner side and by smooth muscle and elastic tissue attached to its outer side. The purpose of this mechanical mechanism is to assist the brain in maintaining commutative eye movements by determining the positions of the axes of rotation for each direction of gaze. The proof of pulley existence, according to Dr. Demer, rests with MRI interpretations and chemically-fixed histological preparations. No physiological experiments have been performed to support the APH.2 The purpose of the current paper1 is to demonstrate that recessions and resections of horizontal EOMs have minimal effect on pulley positions. Because the pulley remains stationary, a recession places the insertion closer to the pulley. The authors predict that the change in the relationship between the insertion and the pulley will cause "vertical and torsional actions" in tertiary gaze positions. Also, dissection of connective tissue "or other factors" associated with medial rectus recession or resection may destabilize the vertical position of the globe. The authors are apparently capable of performing a selective recession of the GL while leaving the OL intact and in the same location. This is an extraordinary surgical feat. My surgical experience and in vivo observations of a contracting superior rectus and superior oblique muscles in a Macaque revealed that these muscles insert on a tendon directly attached to the globe and that there are no pulleys.3 Histological studies have confirmed these surgical and experimental observations.4 Horizontal strabismus surgery, in my experience, does not in itself cause abnormal vertical and torsional abnormalities in tertiary gaze positions or global instability. For example, intermittent exotropia improves with bilateral lateral rectus recessions, and post-operative prism measurements reveal no disturbances in "vertical and torsional actions." Also, there have been strabismus cases in which horizontal surgery alone has partially or completely corrected associated vertical muscle abnormalities. I interpreted the MRIs published by the author2 and my own CT scans as showing no connective tissues bands between the orbital walls and the muscle parenchyma, no connective tissues near the posterior globe dense enough to be functional pulleys, and no clearly demarcated EOM layers. Recent histological preparations reveal that the lateral rectus inserts on a single tendon.4 The idea that a mechanical mechanism exists in the orbit to maintain commutativity that is independent of CNS control requires physiological proof. Smooth muscle and elastic tissue cannot oppose the contraction of striated muscle. No such independent mechanism is known to exist in any other striated muscle system. Ablating the superior cervical ganglion in a monkey or cat should have an effect on eye movements. My guess is that there would be no effect. Robert S. Jampel Kresge Eye Institute, Detroit, MI References 1. Clark RA, Demer JL. Magnetic resonance imaging of the effects of horizontal rectus extraocular muscle surgery on pulley and globe positions and stability. Invest Ophthalmol Vis Sci. 2006;47:188-194. |
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Joseph L. Demer
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jld{at}ucla.edu Joseph L. Demer
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Ocular Motility in a Time of Revolutionary Paradigm Shift This Letter from Dr. Jampel is another letter from him1 criticizing the active pulley hypothesis (APH) of ocular kinematics,2 directed toward our recent related publication in IOVS.3 Jampel's letter largely restates prior criticisms made in his Letter to the Editor regarding the APH. Jampel evidently prefers traditional concepts dating back to the 19th century that presume that extraocular muscles (EOMs) follow shortest paths over the globe without any other constraints and that the rotational behavior of the globe is specified explicitly by neural commands as perhaps modified by EOM length or stiffness changes. He does not accept the notion that EOM pulling directions are important or are actively controlled by connective tissue pulleys. Jampel claimed that proof of the existence of pulleys arises only from functional magnetic resonance imaging (MRI) and histological examinations. From my viewpoint, functional MRI constitutes simultaneous anatomic and physical evidence,4-18 and in context of our modern three-dimensional computer assisted reconstructions of serial histo- and immunohistochemistry of whole human19-21 and monkey20,21 orbits represents a level of rigor never previously achieved for the oculomotor system. In this sense, data supporting the APH are superior to that supporting Jampel's traditional notions of EOM function. Jampel's letter incorrectly asserted that no physiological evidence exists supporting the APH. Decisive physiological experiments have been done in behaving monkeys. Ghasia et al.22 have recorded single motor unit activity in neurons innervating all of the cyclovertical muscles; their finding that these neurons do not encode the torsional behavior underlying Listing's Law (LL) confirms the APH proposition that LL is not explicitly specified by the brain. Complementing this, Klier et al.23 have demonstrated by direct electrical stimulation of the abducens nerve in alert monkeys that the evoked eye movements conform to the kinematics expected under the APH and not as predicted if LL were directly specified neurally. There is no longer any evidentiary basis for controversy concerning this issue.24 Beyond this, human ocular motor behavioral experiments exploring the short time frame interactions between vestibulo-ocular reflexes and saccades seemingly too fast for neural computations, yet consistent with the APH.25 The aforementioned evidence supporting the APH is strong and consistent and excludes the traditional explanation that ocular torsion underlying LL is explicitly encoded by neural commands.24 The APH is quantitative, and its major quantitative prediction has been confirmed by functional MRI.4 It therefore may be paradoxical to readers that Jampel and others persist in denying this powerful and eminently useful new concept, even as the alternative traditional hypothesis has apparently become untenable. To understand this situation, one must appreciate that the APH is a "revolution" in the scientific sense.26,27 The work of Thomas Kuhn on the philosophy of science provides good insight into the current situation.28 Kuhn has examined in detail the circumstances of "scientific revolutions," fundamental shifts in the paradigms used to conduct science. Examples of such paradigm shifts include the revolution in astronomy when the notion of a heliocentric solar system supplanted the ancient idea that all celestial bodies rotate about a flat earth. Other such revolutions are the atomic theory and the neuron theory of the brain. In each case, practitioners of the older paradigm found it impossible to accept new paradigms and the observations underlying these paradigms. Entrenched practitioners of older paradigms found it difficult even to communicate scientifically with followers of the new paradigm because, among other reasons, even the nosology of the older paradigms carried mechanistic implications. I have elsewhere emphasized how traditional terminology in ocular motility can strongly bias our thinking in ocular motility.29 For these and other reasons, adherents to older paradigms have typically been unwilling to consider new observations as valid scientific evidence at all. I contend that the same phenomenon underlies Jampel's denial that evidence supports the APH. The historical studies of Thomas Kuhn demonstrate that competing scientific paradigms cannot co-exist in harmony and that new scientific paradigms supplant old ones for various reasons.28 Kuhn considers this process of change a "scientific revolution." Historically, the most common reason for the ascendance of a new scientific paradigm is that it better predicts new phenomena than the old paradigm does. I foresee this as the reason for ultimate widespread acceptance of the APH, since it quantitatively explains numerous fundamental and clinical phenomena in ocular motility inexplicable under the traditional paradigm. For example, the APH correctly predicted phenomena such as those recently confirmed by Klier et al.23 and Ghasia et al.22 that are impossible with the traditional paradigm. To paraphrase Kuhn, "There is nothing more practical than a good theory." 28 The notions of pulleys and their physiologic behavior allow previously mysterious causes of strabismus to be diagnosed9,18,30,31 and effective surgeries to be performed.32 This practical value includes the emerging range of surgical treatments of disorders of pulleys that could never have been contemplated under the traditional paradigm that fails to recognize the existence of these structures upon which modern strabismus surgeons now operate. The analogy of the flat earth paradigm is instructive. The distinction between flat and spherical earth paradigms is of no practical importance for navigating the streets within a city, so members of the Flat Earth Society do not become lost as a result of that paradigm. Flat earth navigational theory results in appreciable errors for aircraft flying from state to state, but flat earth theory is of no navigational value at all for space travel. Consequently, while the Flat Earth Society lists a wide range of evidence for their minority view, most travelers have abandoned the flat earth paradigm. Like navigating within a city using a flat earth paradigm, traditional views of EOM action give practically acceptable results for a limited range of clinical situations. The traditional paradigm simply cannot account for many contemporary scientific findings and provides no reliable guidance in complex clinical situations. Returning to his specific comments, Jampel expressed surprise that it was possible to selectively recess the global layer while leaving the orbital layer of an EOM intact. Our paper described the functional anatomic effects of conventional strabismus surgery repositioning EOM tendons. The orbital layer is too far posterior to be directly manipulated in conventional strabismus surgery.2 Jampel cited anecdotal clinical experience to contend that horizontal strabismus surgery does not cause abnormal vertical and torsional abnormalities in tertiary gaze positions. This is contrary to the findings of Kushner,33 who has cautioned that clinical diagnostic maneuvers, such as the Bielschowsky 3-step test, can be misleading following strabismus surgery. Furthermore, the kinematic effects to which we were referred would seldom be apparent on clinical prism and cover testing. Adequate three-dimensional quantitative recordings will be required to compare APH predictions with behavioral observations and are underway in my laboratory. Jampel concluded by demanding physiologic proof that a mechanical mechanism exists in the orbit to implement commutative ocular rotations. As noted, the Ghasia et al.22 and Klier et al.23 experiments should already satisfy that demand. We have not proposed that this behavior is instantaneously implemented by smooth muscle,34,35 although smooth muscle may contribute in a long-term way to optimization of pulley positions and connective tissue mechanical properties. It might indeed be useful to perform experiments in which the activity of sympathetic innervation to smooth muscle in the orbit is physiologically altered. The expected effect of such manipulations could not possibly be predicted without the detailed theoretical framework provided by the APH. At least for those open to the possibility of a superior paradigm for understanding ocular motility, there now exists a substantial body of anatomic, functional imaging and physiologic evidence supporting the APH. Interested reviewers may consult contemporary reviews and chapters on this subject.15,24,36,37 Joseph L. Demer References 1. Jampel RS. The superior rectus is not coupled to the superior oblique pulley (letter). Invest Ophthalmol Vis Sci [serial online]. Available at http://www.iovs.org/cgi/eletters/46/8/2790#2802006. Accessed on April 14, 2006. |
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