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The Superior Rectus Is Not Coupled to the Superior Oblique Pulley
Author Response: The Superior Rectus Is Not Coupled to the Superior Oblique Pulley
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Robert S. Jampel
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rjampel{at}comcast.net Robert S. Jampel
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The Active Pulley Hypothesis and the Superior Oblique Muscle According to the APH of Demer and Miller, pulleys cause the tendon pathways of the GLs to shift with gaze and follow the scleral insertions. Thus, the rotational axes of the EOMs are a function of eye position and keep ocular rotations commutative.2,3 (That is, changing the order of the rotational axes involved for any given eye movement does not change its final orientation. The same concept as Donders' Law. All human movements appear commutative.) The evidence for the above is derived entirely from high resolution MRIs and histological preparations. The problem faced by Kono et al. is how to reconcile and integrate the SO, a muscle with a fixed pulley into the APH, which depends upon a mobile pulleys on all the other EOMs. MRI Scans. Review of MRIs of the lateral and medial rectus reveal no tissues resembling pulleys and no antagonists to those pulleys composed of smooth muscle and elastic tissue (Fig. 1). Review of Kono's and Demer's published MRIs of the vertical EOMs reveal no pulleys or orbital wall connections or couplings.2 The MRIs of the SO add no new knowledge concerning that muscle. The SR is sandwiched between the levator and the SO tendon. It cannot possibly be connected by a band of smooth muscle and elastic tissue to the orbital roof. According to the APH, contraction of the GL, which has a fixed pulley, should produce a non-commutative eye movement unless there is a unique independent mechanical mechanism associated with that layer. But, there is no evidence to support this idea. Miller admits that pulleys are not visible on MRI3: Pulleys "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." (Can facts be derived from models without observation or experimentation?) Our conclusion is that MRIs provide evidence against the existence of mobile pulleys on the EOMs. Histochemistry. The SO, according to Kono et al., is divided into two layers, like the other EOMs. Review of their coronal histological sections of the SO shows that the larger muscle fibers are concentrated in the "coaxial periphery" but they are not separated from the rest of the muscle by a distinct cleft or a smooth synovial-like membrane that would allow one layer to slip easily over the other. Also, the SO tendon is not split into two layers. The OL is supposedly attached to the SR pulley by a connective tissue sheath, but the fact that the SR is surrounded by a sheath of connective tissue is no proof that it functions as a pulley. Adjustment of a mobile pulley position of the SR requires both an agonist, the OL of the SO and an antagonist, but no antagonist for the SR pulley is described. The pulleys on the other EOMs are supposedly antagonized by smooth muscle and elastic tissue, but smooth muscle and elastic tissues cannot actively or passively counteract the forces produced by the contraction of striated muscle.4 Histochemistry may suggest but cannot provide definitive evidence for EOM function because chemically fixed orbital tissues may be distorted, fragmented, or thickened. The presence of multifunctional systems in the EOMs was suggested by Dodge in 1903.5 Different motor unit types comprising the EOMs were described beginning in the 1960s.6,7 Whitnall8 described sheaths and denied the existence of pulleys in his comprehensive book on the orbit. An Inconsistency. According to APH, the pulley on the lateral rectus (LR) is pulled back into the orbit by the action of the OL of that muscle and pulled forward by a band composed of smooth muscle and elastic tissue. This pulley movement causes the functional origin of the lateral rectus to vary with the position of the eye insuring commutative behavior. But the LR remains an abductor regardless of the pulley position because the pulley is moving in the same direction as the muscle. In the case where the OL of the SO controls the position of the SR pulley, the SO and SR are acting in opposite directions, because the SO is a depressor and the SR is an elevator. Kono et al. do not consider this possibility. They have not presented convincing histological evidence for the existence of pulleys. Physiology. Kono et al. provide no physiological evidence that "the primate SO has a substantial OL configured to contribute to positioning the superior rectus pulley in the coronal plane." In the 1960s, I experimented on the monkey Macaca mulatta. Sequential faradic stimulation of electrodes implanted in the trochlea, oculomotor nerve and brainstem combined with selective ablations of EOM tendons was performed in terminal experiments. The contractions of the SO, SR and LR were observed in vivo. When the SO contracted it did not "influences the direction of application of rectus EOM forces." Isolated contraction of the SO did not affect the SR. The SO and IO were a reciprocal agonist-antagonist pair as were the SR and IR and the LR and MR.9,10 The EOMs of the monkey were surrounded by connective tissue sheaths that conformed to the contracting muscles.8 There were no discrete connective tissue rings at the equator that could serve as pulley bars and no connective tissue adhesions between the orbital periosteum and the muscle sheaths. The muscle forces were transmitted from each muscle through a single tendon to the globe. Contraction of an isolated SR muscle caused the eye to rotate upward causing the tendon of the SO to rotate passively upward along with it but there were no connective tissue couplings or adhesions between the muscles.9,10 Based on anatomical and mathematical analysis, Helmholtz believed that the axes of the obliques and the vertical recti remained fixed in the orbit during lateral gaze (to and from the mid-orbital sagittal plane).11 Vertical eye movements (towards the brow and towards the chin) occurred around an axis which was the vector sum of the oblique and recti axes. My experiments on the SO demonstrate that Helmholtz was right even though he did not have the technology available today.9 In conclusion, there is no evidence that the superior oblique has a separate layer that controls the pulley on the superior rectus muscle. There is no evidence that a mobile pulley exists on any of EOMs (Fig. 1) (McNeer KW, et al. IOVS 2005;46:ARVO E-Abstract 5721).12 Robert S. Jampel References
1. Kono R, Poukens V, Demer JL. Superior oblique muscle layers in monkeys and humans. Invest Ophthalmol Vis Sci. 2005;46:2790-2799.
Figure 1. The lateral rectus (LR) and the medial rectus (MR) are the two recti closest to the orbital walls and the easiest to visualize with CT and MRI scans. The vertical recti and the inferior oblique (IO) are separated from the orbital walls by intervening tissues and are difficult to visualize. In the contracted state the MR or LR show a straight line course between the annulus of Zinn and the globe. No dense fibroelastic pulleys bands are seen looping around the MR and LR. No demarcation lines splitting the muscles into an OL and GL are visible. There are no smooth muscle and elastic tissue bands connecting the putative pulleys of the MR and LR to the orbital periosteum. No inflections are seen in either muscle. The so-called check ligaments appear attached to the sheaths near the muscle tendons and not to sheaths surrounding the anterior third of the muscle. They are not retracted by horizontal gaze movements. The MR and LR form an agonist-antagonist pair and share a common axis. |
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Joseph L. Demer
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jld{at}ucla.edu Joseph L. Demer
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This is a reply to the letter of Dr. Robert S. Jampel regarding the paper of Kono, Poukens and Demer.1 Dr. Jampel broadly disputed the existence of extraocular muscle (EOM) pulleys, and specifically the connection of the orbital layer of the superior oblique muscle to the pulley of the superior rectus muscle. To keep the matter in context, the statements made in the paper of Kono et al. have been carefully supported by targeted studies on the question in humans and monkeys using modern techniques. The cumulative evidence supporting our claims is now quite extensive, and this letter is not an appropriate vehicle for reviewing all of it. I would refer the interested reviewer to reference #2 cited in Dr. Jampel's letter, and to a recent review.2 In this reply, I will merely address a limited number of Dr. Jampel's statements with which I take issue. 1. In the second paragraph, Dr. Jampel made the parenthetical statement that "all human movements appear commutative." This statement is mathematically absurd, and is demonstrably incorrect even for the oculomotor system. Noncommutativity of the vestibulo-ocular reflex is well described,3 and it is a mathematical truism that rotations of any object are non-commutative.4 2. The figure included by Dr. Jampel with his letter was stated to be a magnetic resonance imaging (MRI) scan, but this figure is in fact an axial computed x-ray tomographic (CT) scan of the orbits! There is no doubt about Dr. Jampel's misidentification of the technique used in his figure, because the CT scan shows high density of the orbital bones, which are invisible on MRI. The fact that an x-ray does not demonstrate soft tissues such as pulleys should surprise no one. The CT scan also fails to demonstrate any of the orbital nerves or blood vessels. These anatomic structures, as well as the pulleys, are invisible if not imaged properly. Figure 1 consists of a high resolution, gadodiamide contrast enhanced axial view of a human left medial rectus pulley, which is demonstrated using this adequate technique. While some early studies could not directly demonstrate the rectus EOM pulleys for reasons such as insufficient resolution (Fig. 1), modern methods do demonstrate them.5 The depiction of the pulley in the MRI may be compared with high quality histology5,6 and with three-dimensional reconstruction of the same region obtained from serial histological sections, which of course shows even more detail than MRI.7
3. Dr. Jampel further stated in his section entitled "MRI Scans" that published MRIs of the vertical EOMs do not reveal pulleys or orbital wall connections or couplings. We have certainly demonstrated the existence of pulleys of the vertical extraocular muscles,5,6,8-10 but have also demonstrated that there is no direct connection between the vertical rectus pulleys and the adjacent orbital walls because this would preclude normal eyelid motion. We have published a detailed structural analysis of the tissue densities in these regions.8 4. Dr. Jampel appeared to state that if the superior oblique muscle had a fixed pulley, it should produce noncommutative eye movement. This issue has been addressed kinematically in my Friedenwald Lecture in 2003, where I argued that the unique path of the superior oblique tendon across the diameter of the globe allows it to have half-angle kinematic behavior.10 5. Dr. Jampel argued that because all features of pulleys cannot be directly imaged in some MRI scans, they must not exist. By this same fallacy, the invisibility of certain structures on x-ray CT would disprove their existence as well. Such reasoning is patently flawed. Absence of evidence obtained using an insensitive technique is not equivalent to evidence of absence. Negative imaging evidence is convincing only if accompanied by the control demonstration of structures comparable in size and composition to the structure in question. In the case of the pulleys, CT cannot satisfy that reasonable criterion. 6. In the section entitled "Histochemistry," Dr. Jampel seemed to argue that the orbital and global layers of the superior oblique muscle are not sufficiently separated to function in a physiologically distinct manner. The orbital and global layers are similarly distinct for the rectus and superior oblique EOMs. There is no reason why the two layers would need to have this greater separation than has been demonstrated. Dr. Jampel was apparently concerned about the absence of a muscular antagonist to the orbital layer of the superior oblique. Like all of the other EOMs, the orbital layer of the superior oblique is antagonized by the passive elastic tension of the orbital connective tissue system.10 7. Dr. Jampel cited a 1932 publication to deny the existence of rectus EOM pulleys. One would hope that the evolution of improved techniques in science might allow us to reconsider and correct erroneous conclusions from the early part of the last century. 8. The section entitled "An Inconsistency" is not at all inconsistent. Dr. Jampel apparently presumed that the only action of the superior oblique muscle is to infraduct the eye in opposition to the superior rectus muscle. The major action of the oblique muscles is to create ocular torsion, as for example during ocular counter-rolling or the extorsional movements associated with convergence.6 There is good evidence that the superior oblique muscle is activated during repositioning of the superior rectus pulley during these two types of physiological eye movements.11 9. The section entitled "Physiology" of his letter refers to Dr. Jampel's terminal experiments in monkeys performed in the 1960s and early 1970s. The reader should be aware that the theoretical concepts in instrumentation techniques necessary for 3-dimensional kinematic analysis of eye movements did not become available until the late 1980s.12 Consequently, the early physiologic studies to which Dr. Jampel refers could not have been guided by any of the concepts that are explained by the active pulley hypothesis, and the studies were preceded by wide ablations of the superior and lateral orbital tissues likely to have obscured pulley function. Furthermore, the most relevant claims made by Dr. Jampel were not published; the references instead are to the reciprocal action of agonist-antagonist EOM pairs. Even here, it is difficult to know how conclusions could be reached using only terminal electrical stimulation experiments. Much better physiologic stimulation13 and recording14 experiments have very recently been performed in behaving primates, and these support the claimed role of pulleys in the regulation of ocular kinematics. There is now good reason to believe that the techniques employed by Dr. Jampel were inaccurate and insensitive, since in his hands they have uniquely failed to demonstrate the existence of ocular counter-rolling,15 a robust vestibulo-ocular reflex readily investigated in numerous modern laboratories.16-24 10. In his section entitled "Physiology," Dr. Jampel made emphatic statements about connective tissue sheaths around the EOMs of monkeys, but denied that these could act as pulleys. Our careful serial histological examinations of these tissues has led to an opposite conclusion.25,26 11. In his penultimate paragraph, Dr. Jampel stated that his experiments confirm the belief of Helmholtz that the axes of the EOMs remained fixed in the orbit during lateral gaze. That historical statement has been conclusively disproven, since MRI of rectus EOMs directly demonstrates that their pulling directions are functions of gaze.10,27 Direct electrical stimulation of the abducens nerve of the behaving monkey demonstrates that the pulling direction of the lateral rectus muscle changes by one-half of the amount of vertical gaze change, precisely as predicted by the active pulley hypothesis.13 Finally, the motor neurons innervating the cyclovertical EOMs do not encode the torsion required by Listing's Law,14 consistent with the proposition of the active pulley hypothesis that this torsion has a mechanical origin in gaze-dependent EOM paths.2,10,28 In summary, a substantial body of evidence obtained using careful, modern techniques contradicts Dr. Jampel's objections. While there certainly remain many questions about the fine structure of the EOMs and their connective tissues, progress in the oculomotor field will not be well served by flatly denying clear and convincing evidence for the existence of fundamental anatomic structures such as the pulleys of Miller.29,30 Joseph L. Demer References 1. Kono R, Poukens V, Demer JL. Superior oblique muscle layers in monkeys and humans. Invest Ophthalmol Vis Sci. 2005;46:2790-2799. |
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