AMERICAN JOURNAL O F OPHTHALMOLOGY
MARCH, 1967
I S DIVERGENCE ACTIVE? AN ELECTROMYOGRAPHIC STUDY EDWARD TAMLER,M.D.,
AND
.ARTHURJAMPOLSKY, M.D.
San Francisco, California
Many authors have made the statement rectus muscles may resemble that of an eye that divergence is active. It is the purpose engaged with its fellow eye in the binocular of this paper to review the electromyo- act of divergence. In the top trace of Figure 1, for example, graphic evidence upon which this is based and to present electromyographic data from we have an abducting right eye during a our laboratory which, we believe, more con- version movement of both eyes to the right. clusively supports the concept of an active Notice the increase in recorded activity of the right lateral rectus and decrease of acdivergence mechanism. tivity in the right medial rectus. I n the middle trace of Figure 1 we again have an abDEFINITIONS ducting right eye but this time during a Evaluation of evidence depends upon recession of convergence. Again, there is an one's definitions. We define the active func- increase in the right lateral-rectus activity tion or mechanism of divergence as a binoc- and a decrease in right medial-rectus activiular simultaneous increase in innervation to ty. I n the bottom trace of Figure 1 we again both lateral rectus muscles as (1) the eye or have an abducting right eye but now occureyes move outward to fuse from the fusion- ring after a break of convergence when the free position or (2) during the maintenance near-point of convergence has been exceedof fusion against odds, that is, increasing ed. Again, note the increase in right lateralbase-in prism. Abduction is defined as an rectus activity and decrease in right medialeye moving temporalward from the primary rectus activity. position. The fusion-free position is defined Similarly, in the top electromyogram of as that position of relative convergence or Figure 2 we have an abducting left eye in a divergence assumed by the eyes when fusion patient with exophoria following occlusion is broken. (first arrow) of the recorded left eye. Here This matter of definition must be made again, the lateral rectus shows increased acclear for it is the crux of the discussion re- tivity while the medial rectus shows a simulgarding active divergence. One eye moving taneous decrease in activity. In the bottom outward is not divergence in a functional trace of Figure 2, we have an abducting sense of the word. One eye moving tempo- right eye following a break of fusion (near ralward is termed abduction but the electro- the beginning of the trace) in a patient with myographic trace of the medial and lateral intermittent exotropia. Again there is increase in lateral-rectus activity and decrease . From the Institute of Visual Sciences, Institute of Medical Sciences, Presbyterian Medical Cen- in medial-rectus activity. ter. This work was supported by funds from the Finally, in Figure 3, we have an abductOffice of Naval Research contract 3009(00) and ing right eye in a patient with esophoria th,e National Institutes of Health grant NB consequent to a refusion movement follow02633.
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Fig. 1 (Tamler and Jampolsky). (Top) Abducting right eye during version movement of both eyes to the right. (Middle) Abducting right eye during recession of convergence. (Bottom) Abducting right eye after break of convergence.
ing removal of occlusion from the recorded right eye. Once again there is an increase in lateral-rectus activity. The decrease in medial-rectus activity is difficult to see. I n all of these examples, the common factor to each is that the recorded eye was seen to abduct, that is, to turn outward. I n all of these examples the electromyograms are of the same type, that is, increasing lateral-rectus activity and reciprocal diminishing activity of the medial rectus of the moving eye. This was the case regardless of whether the abduction recorded was part of a vergence or version, a break of fusion or a refusion movement. It is, therefore, apparent that monocular electromyograms recorded from a single abducting eye show the same electromyographic pattern and therefore tell us
very little about the binocular function of divergence. All that these electromyograms tell us is that horizontal rectus muscles are involved in moving the eye outward. When an eye abducts, it is the lateral rectus that pulls it out while the medial rectus is reciprocally inhibited. As we shall see later, such electromyograms showing abduction of one eye have been cited by other investigators as evidence for active divergence, but these monocular electromyograms cannot be employed as the sole criterion in studying the divergence function or mechanism. What we prefer to call active divergence function refers to the simultaneous increase in activity of both lateral rectus muscles while performing a movement, such as re-
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Fig. 2 (Tarnler and Jampolsky). (Top) Abducting left eye in patient with exophoria following occlusion (first arrow) of recorded left eye. (Bottom) Abducting right eye following break of fusion (near beginning of trace) in patient with intermittent exophoria.
AMERICAN JOURNAL O F OPHTHALMOLOGY
MARCH, 1967
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Fig. 3 (Tamler and Jampolsky). Abducting right eye in patient with esophoria consequent to a refusion movement following removal of occlusion from the recorded right eye.
covery of fusion, or maintenance of fusion during the presentation of increasing amounts of base-in prism before the eyes. It would not include the movement of symmetrically converged eyes back to the comfortable, natural, primary position in normal individuals, or movements of the eye to the fusion-free position in heterophoria or heterotropia. What we mean by active divergence is specifically exemplified in electromyography by either of the following two situations : 1. Divergence beyond the fusion-free position, as in response to base-in prisms while maintaining fusion, with both lateral rectus muscles showing simultaneous increase in electrical activity. 2. Recovery of fusion by an esophore or an intermittent esotrope from the fusionfree position with both lateral rectus muscles showing simultaneous increase in electrical activity. I n these instances the divergence function is working either to maintain fusion against odds or to restore fusion. BACKGROUND With this definition in mind, let us review the electromyographic evidence given in the literature for active divergence. I n 1953, Adlerl showed an increase in the frequency and amplitude of a lateral rectus muscle as the eyes moved outward from the near-point of convergence. H e cites this as evidence for the existence of an active divergence mechanism. Breininj2 in 1955, found that, when the deviating eye of an intermittent exotrope swung outward, the electrical activity of its
lateral rectus muscle increased. H e stated that this conclusively demonstrated that divergence is definitely associated with active innervation of the lateral rectus muscles. Blodi and Van Allen,3 in 1957, reported active contraction of the external rectus at the break-point of convergence in the eye which abducts. They cautiously stated that this '(could be" proof of an active divergence mechanism. I n another paper on the nature of vergence, in 1957, Breinin4 stated that fusional amplitudes measured from the dissociated position show that a true active divergence does occur which cannot be construed as a relaxation of convergence. Miller,5 in 1959, also reported active divergence on the basis of increased electrical activity in one lateral rectus muscle in an abducting eye.
Pursuant to our definition of active divergence, we recorded increases in both lateral rectus muscles as a subject maintained fustion beyond his f usion-f ree position while base-in prisms were placed before his eyes (figs. 4 and 5). Our technique of electromyography has been previously d e ~ r i b e d .I~n Figure 4 we are recording both lateral rectus muscles of a subject fusing a near target before base-in prisms are added before both eyes with Risley prisms. The subject had an exophoria of six prism diopters as measured by dissociating prisms at this distance, but could maintain fusion with basein prisms up to 18 prism diopters, beyond which fusion was disrupted. Figure 5 shows the increased activity of both lateral rectus
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Fig. 4 (Tamler and Jampolsky). Top trace is right lateral rectus. Bottom trace is left lateral rectus. (Before base-in prism added bilaterally.)
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muscles, as compared to Figure 4, when the subject was still fusing just before the break-point of divergence. W e have also tested intermittent esotropes and esophores with deviations greater than 15 prism diopters and recorded increases in activity of both lateral rectus muscles during a recovery of fusion movement. I n Figure 6, the arrow indicates the uncovering of the left eye of a patient with 17 prism diopters of intermittent alternating esotropia. The left lateral rectus of the moving eye and the right lateral rectus of the stationary eye show simultaneous increased activity with the clinically observed fusional
Fig. 5 (Tamler and Jampolsky). Same as Figure
4 after 18 prism diopters were added bilaterally while fusion was maintained. Note increased electrical activity of both lateral rectus muscles as compared to Figure 4.
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divergence movement. The vertical height of the integrated trace reflects the increasing activity of the right lateral rectus. Figure 7 shows the same phenomenon. Here, on two occasions (arrows), the occluded inturned left eye is uncovered and a fusional divergence movement takes place with both lateral rectus muscles showing simultaneous increase in activity.
W e believe that some of the earlier electromyographic evidence for active divergence is equivocal.
MARCH, 1967
Fig. 6 (Tamler and Jampolsky). Uncovering (arrow) left eye of patient with 17 prism diopters of intermittent alternating esotropia. Note increased activity of both lateral rectus muscles as the left eye makes a fusional divergent movement.
If one considers a descriptive definition of divergence as both eyes moving away from each other, then Adler's conclusion1 is acceptable. On the other hand, according to our functional definition, the active contraction of one or both lateral rectus muscles during symmetrical relaxation of convergence is not considered to be active divergence since the lateral rectus muscles are merely returning the eyes toward a relative position of rest. Nor is active contraction of the lateral rectus of the deviating eye of an intermittent exotrope as it swings outward2 an ex-
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Fig. 7 (Tamler and Jampolsky). Uncovering (arrows) of occlude'd inturned left eye followed by fusional divergence movement. Note increased activity of both lateral rectus muscles each time as the left eye makes a fusional divergent movement.
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+R.Lat. R. +-R.Med.R. <- L.Med.R. +-LaL a t. R. Fig. 8 (Tamler and Jampolsky). Covering (arrow) left eye of patient with 25 prism diopters of intermittent exotropia. Followed by break of fusion and manifest exotropia. Note decrease in activity of right lateral rectus.
ample of active divergence. W e have repeatedly seen, in such instances, that, when all four horizontal rectus muscles are recorded simultaneously, the lateral rectus of the stationary eye does not change, or decreases in electrical activity, while the other eye moves temporalward. I n Figure 8, the arrow indicates the covering of the left eye of an intermittent exotrope of 25 prism diopters. The occlusion is followed by a break of fusion and manifest exotropia. As the left eye goes out, the left lateral rectus activity increases and the left medial rectus activity decreases, as expected. But observe that the
right lateral rectus decreases in activity at the same time. Incidentally the right medial rectus muscle also decreases in activity, indicating a simultaneous decrease in the activity of the horizontal rectus muscles of the stationary eye in a break of fusion movement or movement toward the fusion-free position. Similarly, active contraction of the lateral rectus after the break-point of convergence in the eye which abducts3 is not evidence for active divergence. Again, when all four horizontal rectus muscles are recorded simultaneously around the break-point of conver-
Fig. 9 (Tamler and Jampolsky). (Top and bottom) Arrow represents break-point of convergence followed by abduction of left eye. Note decrease in activity of right lateral rectus as left eye abducts.
AMERICAN JOURNAL O F OPHTHALMOLOGY
MARCH, 1967
Fig. 10 (Tamler and Jampolsky). Arrow indicates start of fusional convergent movement of left eye in an intermittent exotrope. Note increase in activity of right lateral rectus during convergent movement of other eye.
gence, it will be seen that the lateral rectus muscle of the stationary eye decreases in activity as the other eye abducts. I n both electromyograms of Figure 9 the arrow represents the break-point of convergence. In each, the left eye abducts when fusion is lost and the horizontal rectus muscles of the moving left eye show the expected reciprocal innervation. But note that, in each subject, the activity of the lateral rectus of the stationary right eye decreases after the break of convergence. I t is important to stress again that one cannot draw conclusions about an active divergence mechanism from monocular electromyograms. For example, in Figure 10, the arrow indicates the start of a fusional convergent movement of the left eye of an intermittent exotrope. As the left eye converges to fuse, the left medial rectus increases in activity and the lateral rectus decreases in activity, as expected. At the same time, the lateral rectus (as well as the medial rectus) of the stationary right eye increases in activity. If one recorded only the right lateral rectus in this instance, one could mistakenly call this an active divergent movement, whereas, actually we are dealing with a convergent movement from the binocular point of view. On the other hand, we believe we have demonstrated true active divergence in the examples given (figs. 4-7). Here both later-
al rectus muscles increase their activity simultaneously while the eyes maintained fusion beyond the fusion-free position as base-in prism is added or when an esotropic eye makes a fusion movement from its "comfortable" dissociated position. We have found it to be a general rule that a fusional movement leads to simultaneous increased activity or co-contraction of the horizontal rectus muscle of the stationary eye, whereas, a break of fusion movement is associated with a simultaneous decrease in the activity of the horizontal rectus muscles of the fixing or stationary eye. This is illustrated in Figures 8-10, and suggests that fusional movements are active movements in the binocular sense, whereas, break of fusion movements are relaxation movements in the same sense. Active divergence, therefore, is present in fusional divergent movements as indicated in our electromyographic data.
SUMMARY AND CONCLUSIONS Electromyographically, active divergence is defined here as the simultaneous increase in electrical activity of both lateral rectus muscles as the eyes perform a fusional divergent movement or maintain fusion beyond the fusion-free position as base-in prisms are added. The existence of active divergence is best demonstrated by simultaneously recording both eyes of an intermittent esotrope mak-
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ing a fusional divergence movement and of a subject maintaining fusion beyond the fusion-free position as base-in prism is added. I n such cases, one can record increased activity of both lateral rectus muscles. Multiple-channel simultaneous recordings of all four horizontal rectus muscles suggest the general rule that horizontal fusional movements of an eye are accompanied by increased activity or co-contraction of the horizontal rectus muscles of the stationary eye, whereas, a break of fusion is associated with a simultaneous decrease in activity of the horizontal rectus muscles of the fixing stationary eye. Clay and Webster Streets (94115)
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ACKNOWLEDGMENT We are indebted to Elwin Marg, Ph.D., School of Optometry, University of California, Berkeley, for his help in the early phase of this study.
1. Adler, F. H. : Pathologic physiology of strabismus. Arch. Ophth. 50:19, 1953. 2. Breinin, G. M. and Moldaver, J. : Electromyography of the human extraocular muscles. Arch. Ophth. 54 :200,1955. 3. Blodi, F. C. and Van Allen, M. W. : Electromyography of extraocular muscles in fusional movement. Am. J. Ophth. 44 :I36 (Oct. Pt. 11) 1957. 4. Breinin, G. M.: The nature of vergence revealed by electromyography. Arch. Ophth. 58 :623, 1957. 5. Miller, J. E.: The electromyography of vergence movement. Arch. Ophth. 62 :790, 1959. 6. Marg E., Jampolsky, A. and Tamler, E.: Elements of human extraocular electromyography. Arch. Ophth. 61:258, 1959.
