Vertical Fusional Vergence the Key to Dissociated Vertical Deviation

CLINICAL SCIENCES Vertical Fusional Vergence The Key to Dissociated Vertical Deviation

Edward W. Cheeseman, Jr, MD; David L. Guyton, MD

Objectives: To test the previous findings of Enright that value of torsional shift was 1.15° ± 0.76° in the expected disparity-induced vertical vergence is mediated primar- direction. ily by the oblique muscles, and to relate this normal eye movement pattern to the eye movement pattern seen in Conclusions: Vertical fusional vergences in this study subjects with dissociated vertical deviation. were produced primarily by the oblique extraocular muscles. The eye movement patterns of these vertical Methods: Sixteen normal volunteers underwent 55 mea- vergences in normal subjects are qualitatively similar to surements of the cycloversion associated with prism- those seen in recordings of patients with dissociated induced vertical vergence using an afterimage appara- vertical deviation. Dissociated vertical deviation thus tus. A Vernier scale measured the direction and magnitude seems to be an exaggeration of a normally occurring eye of the torsional shift that occurred with recovery of fu- movement pattern. The cyclovertical component of dis- sion on removal of a 3– or 4–prism diopter prism. sociated vertical deviation may help stabilize the fixing eye by damping vertical nystagmus, while the accompa- Results: Of the 55 trials, the directions of torsional shift nying hypertropia is an incidental and undesirable side were consistent with the oblique muscles being the pri- effect. mary mediators of vertical fusional vergence in 51 (93%) (P = .03 using a binomial distribution). The mean ± SD Arch Ophthalmol. 1999;117:1188-1191

ISSOCIATED vertical devia- noted vertically divergent eye move- tion (DVD) is an enig- ments that were accompanied by a con- matic motility disorder jugate cycloversion. The direction of the that has defied explana- cycloversion implied predominant action since its original de- tion by the oblique muscles and not the Dscription more than a century ago.1 It may vertical rectus muscles. He concluded that occur spontaneously or as a result of cover testing. It may occasionally be found as an See also page 1216 isolated phenomenon, but it generally occurs in association with strabismus, with the bulk of the reflex vertical fusional ver- the most common association being con- gence was due to the superior oblique genital esotropia.2,3 muscle. The role of the inferior oblique The dissociated eye movement of muscle was considered passive and mi- DVD is normally elevation and extorsion nor. van Rijn and Collewijn7 attempted to of the covered eye, accompanied by intor- reproduce Enright’s findings using scleral sion of the fixing eye. It has been docu- search coil recordings. They confirmed his mented, however, that dissociated devia- cycloversion findings in normal subjects tions can be primarily horizontal or accompanying disparity-induced vertical torsional.4 vergences, but refuted his hypothesis that The eye movements of DVD have pre- only the superior oblique muscle was the viously been described as a form of verti- primary mediator of vertical vergence. In cal vergence.2,5 Enright6 reported the in- their study, part of the cycloversion ac- From the Wilmer teresting, and unexpected, finding that companying the disparity-induced verti- Ophthalmological Institute, vertical fusional vergence induced by ver- cal vergence was in the form of torsional The Johns Hopkins University tical disparity in normal subjects is asso- nystagmus. School of Medicine, ciated with binocular torsion. He placed The primary purpose of this study Baltimore, Md. a weak vertical prism in front of 1 eye and was to confirm Enright’s finding that ver-

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©1999 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 SUBJECTS AND METHODS the order of possibilities randomly selected. Initially, a 2–prism diopter (PD) prism was introduced, and this was slowly increased to 4 PD, if possible. Two subjects were Sixteen volunteers, 8 men and 8 women, participated af- only able to fuse a maximum of 3 PD vertically on one of ter giving informed consent. Their ages ranged from 17 to the trials (Table). 53 years. All had a best-corrected visual acuity of at least Once either 3 or 4 PD of vertical disparity were fused, 20/20 OU. None of the volunteers had manifest strabis- the subject was asked to look at a small white dot that was mus or any evidence of amblyopia. painted centrally between the 2 slits on the flash unit. The An apparatus was constructed using an ordinary pho- flash was then fired, and the prism was rapidly removed tographic flash unit that was attached to a standard rotat- from the eye. Gaze was maintained on the white dot until able optical mount (Figure 1). The mount could be ro- the induced vertical diplopia resolved (normally between tated manually for 360°, and the outer edge had an engraved 5 and 10 seconds). The room lights were then turned off, 360° Vernier scale that allowed measurement with a pre- and the subject rotated the entire flash unit until the phos- cision of 0.1°. The flash aperture was masked using black phorescent reference line was parallel to the 2 parallel af- tape such that 2 horizontal slits were created parallel to one terimages that had been created (Figure 2). The magni- another. The 2 slits were separated by 4 mm. Below and tude and direction of any torsional movement occurring, parallel to the 2 slits, a thin line of phosphorescent paint associated with the vertical fusional vergence to recover was applied to the black tape. single binocular vision, were then read from the scale to A near reading card (Bausch & Lomb, Rochester, NY) the nearest 0.1°. Each subject performed 2 to 4 trials in this was then taped to the front surface of the flash unit, with a manner (Table). slot cut in the card to expose the underlying parallel slits To ensure reliability in determining the position of the and phosphorescent line. Lettering (size 20/50) was im- afterimage relative to the reference line, each subject ini- mediately adjacent to the slits. tially performed 2 trials without any prism in place. Sub- The entire apparatus was placed on an optical rail at jects were instructed to look at the central white dot, and a distance of 40 cm from a headrest–chin rest assembly. the flash was fired. The assembly was then rotated 30° from Two cam-type rings were mounted on either side of the the horizontal position, and the lights were turned off. The headrest that, when rotated into place, served to stabilize subject was instructed to rotate the assembly back such that the head and ensure that there were no significant head the phosphorescent reference line was again parallel to the movements. afterimages. If a subject could not perform this task within Each subject was instructed to fixate on the 20/50 size 0.5° of the original horizontal position on each trial, the lettering while progressively stronger vertical prisms were volunteer was not considered reliable. The 16 volunteers placed either base up or base down in front of 1 eye, with selected fulfilled these criteria; 1 volunteer was rejected.

tical fusional vergence is mediated primarily by the oblique muscles. We used a small prism to induce a vertical fusional movement in 16 normal volunteers. We then used a basic afterimage apparatus to measure by subjec- tive means whether a clockwise or counterclockwise torsional movement occurred during recovery of fusion after the prism was removed. A second purpose of the study was to relate the apparently normal eye movement pattern of vertical vergence to the eye movements seen in subjects with DVD.

RESULTS Each subject participated in 2, 3, or 4 trials using the af- Figure 1. Afterimage apparatus. A flash is triggered when the subject verifies terimage device, for a total of 55 trials (Table). In 51 (93%) fusion with the vertical prism, creating an afterimage. of the 55 trials, the direction of the cycloversion that accompanied the vertical vergence required to recover fusion was consistent with the oblique muscles being the tical fusional vergence was classified as “inconsistent.” primary mediators of vertical fusional vergence. That is, Any individual with all observations consistent with ob- in most cases, removal of a base-down prism from the lique muscle mediation was classified as “consistent.” The right eye or a base-up prism from the left eye resulted in criteria for consistent were thus quite strict. The hypoth- a counterclockwise torsional movement (levocyclover- esis of equally likely mediation of the vertical fusional sion) as fusion was regained. Similarly, removal of a vergence response by the oblique muscles or the verti- base-up prism from the right eye or a base-down prism cal rectus muscles was tested by considering each sub- from the left eye resulted in a clockwise torsional move- ject’s consistency or inconsistency as an independent ob- ment (dextrocycloversion) as fusion was regained. servation. A binomial distribution was used with P = .50 Any individual having at least one observation that to describe the chance of observing certain numbers of was not consistent with oblique muscle mediation of ver- subjects with consistent and inconsistent results.

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Prism, Subject No. PD Orientation Eye Degrees Direction 1 4 Base down R 1.8 CCW 4 Base up R 1.5 CW 4 Base down L 1.9 CW 4 Base up L 1.8 CCW 2 4 Base down R 1.2 CCW 4 Base up R 1.0 CW 4 Base down L 2.2 CW 4 Base up L 1.0 CCW 3 4 Base down R 0.8 CCW 4 Base up R 1.8 CW Figure 2. With the prism removed and after recovery of fusion, the subject 4 Base down L 1.4 CW rotates the flash to align the phosphorescent line with the afterimage (with 4 Base up L 0.8 CCW the lights out). 4 4 Base down R 1.8 CCW 4 Base up R 1.0 CW of equally likely control by the oblique muscles or ver- 4 Base down L 1.6 CW tical rectus muscles, and consistent with predominant con- 4 Base up L 1.5 CCW 5 4 Base down R 1.2 CCW trol of vertical vergence by the oblique muscles. Since 4 Base up R 1.3 CW observations within an individual subject are not inde- 4 Base down L 2.2 CW pendent, a mean value of torsional shift was calculated 4 Base up L 1.2 CCW for each subject, and these values were averaged to ob- 6 3 Base down R 2.0 CCW tain an overall mean. A positive value was assigned to 4 Base up R 2.1 CW torsional cycloversions in the expected direction of ob- 4 Base down L 2.4 CW 7 3 Base down R 0.9 CCW lique muscle action and a negative value to those in the 4 Base up R 1.8 CW opposite direction. The mean ± SD value was 1.15° ± 0.76°, 4 Base up L 0.8 CW† with an SEM of ±0.19°. 8 4 Base down R 1.6 CCW 4 Base up R 1.8 CW COMMENT 4 Base down L 1.5 CW 4 Base up L 0.8 CCW The findings in this study strongly support Enright’s po- 9 4 Base down R 1.2 CCW 4 Base down L 1.3 CW sition that the oblique muscles are the primary media- 10 4 Base down R 2.2 CCW tors of vertical fusional vergence. When a vertical dis- 4 Base up R 1.5 CW parity is created using a small prism, a vertical vergence 4 Base down L 1.8 CW is expected. If, for example, a base-up prism is placed be- 11 4 Base down R 1.1 CCW fore the right eye, the right eye should move down with 4 Base up L 2.8 CW† respect to the left eye to regain fusion. When the prism 12 4 Base down R 2.0 CW† 4 Base up R 0.8 CW is removed, the opposite relative movement should oc- 4 Base up L 1.0 CW cur to recover single binocular vision. With each verti- 13 4 Base down R 1.0 CCW cal fusional recovery, there was an associated torsional 4 Base up R 1.5 CW movement that was recorded using the afterimage appa- 4 Base up L 1.0 CW ratus. In separate pilot experiments with a monocular 14 4 Base down R 1.4 CCW afterimage, we had already established that both eyes 4 Base up R 1.2 CW 4 Base down L 0.9 CW cycloduct in the same direction. In other words, the move- 4 Base up L 1.2 CCW ment is a cycloversion. In the example previously cited, 15 4 Base down R 1.9 CCW when the base-up prism was removed from the right eye, 4 Base up R 1.8 CW the right eye moved up and customarily extorted. The 4 Base down L 2.2 CW subject perceived this movement as a clockwise rota- 4 Base up L 1.6 CCW tion of the afterimage. Upward movement of the right 16 4 Base down R 0.9 CCW eye with extorsion can only be mediated by the oblique 4 Base up R 1.5 CCW† 4 Base down L 0.8 CW muscles, with the inferior oblique muscle contracting, 4 Base up L 1.0 CCW and/or the superior oblique muscle relaxing. If a contracting superior rectus muscle had been responsible for *R indicates right; L, left; CCW, counterclockwise; and CW, clockwise. the elevation, an intorsion of the right eye (counterclock- †Direction opposite to expected oblique muscle action. wise movement of the afterimage) should have been measured with the afterimage apparatus. The cycloversion occurring with vertical fusional ver- Of the 16 subjects, 4 had inconsistent results. The gence appears to be an important key to understanding probability of observing a proportion this small, if the DVD. van Rijn and coworkers8 showed with scleral search true probability of an inconsistent result is .50, is .03. The coil recordings that the cyclovertical movements in pa- observed results are thus inconsistent with a hypothesis tients with DVD are remarkably similar to disparity-

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©1999 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 induced vertical vergence in normal subjects. In 3 of their observed clinically, suggests that DVD serves to prefer- 5 patients with DVD, the time course of the vertical di- entially damp this form of nystagmus. vergence and the direction of the cycloversion were comparable with those observed in disparity-induced verti- Accepted for publication April 10, 1999. cal vergence in normal subjects. Although DVD may use This study was supported by core grant EYO1765 from the same eye movement pathways as vertical fusional ver- the National Eye Institute, National Institutes of Health, gence, but in an exaggerated manner, the etiology of DVD Bethesda, Md (Wilmer Biostatistics Center). still remains to be explained. We believe that further clues We thank Susan Vitale, MHS, for assisting in the sta- to understanding DVD come from the strong associa- tistical analysis of data collected. tion of DVD with latent nystagmus. In the setting of the Corresponding author: Edward W. Cheeseman, Jr, MD, cyclovertical latent nystagmus that frequently accompa- 13 Holly View Ct, Olney, MD 20832. nies DVD, Guyton and colleagues9,10 have shown through the use of sensitive search coil recordings that the cycloversion or vertical vergence associated with DVD helps REFERENCES damp this cyclovertical nystagmus. This helps stabilize the fixing eye, but also results in an unavoidable and un- 1. Stevens GT. On double vertical strabismus. Am Oculist Paris. 1895;113:225- desirable elevation of the fellow eye, which we recog- 232. nize as DVD. 2. Helveston EM. Dissociated vertical deviation: a clinical and laboratory study. Trans In summary, the present study demonstrates that the Am Ophthalmol Soc. 1980;78:734-779. vertical vergence that results from a prism-induced ver- 3. Lang J. Congenital convergent strabismus. Int Ophthalmol Clin. 1972;11:88-92. 4. Raab EL. Dissociated vertical deviation. Int Ophthalmol Clin. 1994;25:119-131. tical disparity in normal subjects is mediated primarily 5. Zubcov AA, Goldstein HP, Reinecke RD. Dissociated vertical deviation (DVD): by the oblique muscles, supporting the previous finding the saccadic and slow eye movements. Strabismus. 1994;2:1-11. of Enright.6 The vertical fusional vergence that occurs in 6. Enright JT. Unexpected role of the oblique muscles in the human vertical fu- normal subjects on the introduction of vertical disparity sional reflex. J Physiol. 1992;451:279-293. 7. van Rijn LJ, Collewijn H. Eye torsion associated with disparity induced vertical has been shown to have a time course comparable with vergence in humans. Vision Res. 1994;34:2307-2316. 8 the vertical vergence seen in subjects with DVD. We sug- 8. van Rijn LJ, Simonsz HJ, ten Tussher MPM. Dissociated vertical deviation and gest that DVD is actually an exaggeration of this normal eye torsion: relation to disparity-induced vertical vergence. Strabismus. 1997; vertical vergence pattern, recruited to help compensate 5:13-20. for nystagmus, particularly latent nystagmus, in pa- 9. Guyton DL, Cheeseman EW, Ellis FJ, Strautmann D, Zee DS. Dissociated vertical 9,10 deviation: an exaggerated normal eye movement used to damp cyclovertical la- tients with absent or imperfect binocular function. The tent nystagmus. Trans Am Ophthalmol Soc. 1998;96:390-429. notable prevalence of cyclovertical nystagmus that has 10. Guyton DL. 1998 Costenbader lecture: dissociated vertical deviation: etiology, been reported in conjunction with DVD, and that we have mechanism, and associated phenomena. J AAPOS. In press.

From the Archives of the ARCHIVES

A look at the past...

IDMARK has made a series of experiments with a grating spectroscope in order to determine the sensibility of the retina for ultraviolet rays. He finds the following. The normal human eye perceives only a small portion of Wthe ultraviolet rays. The limit of the visible spectrum varies with different individuals, but usually lies within L-M. The rays are perceived directly, and not through fluorescence. Older persons recognize fewer of the ultraviolet rays than younger. This is especially noticeable in persons over sixty-five. The lens is the chief factor in preventing the visibility of the extreme rays, and after its removal the violet end of the visible spectrum is considerably elongated.

Reference: Arch Ophthalmol. 1898;27:417.

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