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Effect of Sustained Cyclovergence on Eye Alignment: Rapid Torsional Phoria Adaptation

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Effect of Sustained Cyclovergence on Eye Alignment: Rapid Torsional Phoria Adaptation Matthew J. Taylor,1 Dale C. Roberts,1,2 and David S. Zee1,2 PURPOSE. To describe adaptive changes in torsional alignment that follow sustained cyclovergence in healthy humans. METHODS. Eye movements were recorded binocularly from four healthy subjects using dual-coil scleral annuli. Cyclovergence movements were evoked over periods of 30 to 150 seconds using a stereoscopic display, presenting gratings of lines arranged horizontally, vertically, or at 45°, subtending angles of up to 48°. In- and excyclodisparities of 5° were introduced and removed in a single-step fashion. After stimulation, the time course and magnitude of the decay in cyclovergence was compared with the subject either in darkness or viewing a baseline stimulus of zero cyclodis- parity. RESULTS. As reported previously, the cyclovergence response to incyclodisparities was greater than to excyclodisparities. After sustained excyclovergence, however, in all subjects and in response to all orientations of the gratings, the decay in darkness was incomplete, implying an adaptive change in torsional alignment. In response to the horizontal gratings, for incyclovergence there was also an incomplete decay in darkness but to a lesser degree than in response to excyclovergence, and in only three of four subjects. The incyclovergence evoked by the oblique and vertical gratings was of small magnitude, and its decay was unaffected by the presence or absence of a visual stimulus. CONCLUSIONS. After sustained cyclovergence, its decay in the absence of a visual stimulus may be incomplete. The residual component may be interpreted, by analogy with horizontal and vertical vergence, as reflecting so-called phoria adaptation for torsional alignment. (Invest Ophthalmol Vis Sci. 2000;41:1076–1083) he torsional orientation of the eye is usually determined similar to vertical vergence, is much slower than horizontal solely by the position of the eye in its horizontal and vergence8–9 and usually10 is not under voluntary control. Tvertical dimensions: Listing’s law constrains the degrees Horizontal vergence can be elicited by horizontal disparity of freedom of movement of the eyes to two. Exclusively tor- between the images on the retinas. If this retinal disparity sional movements, however, can be elicited in certain circum- signal is removed, either by occluding one eye11 or by placing stances. In 1861, Nagel1 first proposed that disjunctive tor- the subject in darkness,8 the eyes return to their initial, resting sional movement around the visual axis, cyclovergence, takes horizontal position. The time taken for this decay is greater 8,11 place when horizontal lines, observed in the stereoscope, are than the rise time in response to a disparity, and if horizon- rotated in opposite directions. There was much controversy tal disparity vergence is maintained for periods of hours, then about the existence of these movements because subjective the decay on removal of retinal disparity is incomplete for 12 methods, none of which was entirely satisfactory,2 had to be several hours or until binocular fixation is reinstated. The used to imply the presence of cyclovergence. It was not until portion of the vergence response that is sustained after re- 1975 that Crone and Everhard–Halm3 demonstrated the exis- moval of the disparity stimulus has been attributed to the tence of cyclovergence objectively using a photographic tech- output of a slow fusional vergence response that leads to 13 nique. Since then, cyclovergence has been well characterized so-called prism or phoria adaptation. It can be observed after (see Howard and Rogers2 for a recent review). Many of its exposure to disparities for periods as brief as 30 seconds. A similar phenomenon may be observed after exposure to verti- dynamic characteristics are qualitatively similar to those of 14–16 horizontal and vertical vergence4–7 although cyclovergence, cal disparity. Investigation of the behavior of the cyclovergence sys- tem, by using subjective methods of estimating cyclover- gence, suggests that, as is the case for the horizontal ver- 1 2 From the Departments of Neurology and Ophthalmology, The gence system, the return to the initial alignment occurs Johns Hopkins University School of Medicine, Baltimore, Maryland. Supported by National Institutes of Health Grant EY-01849 and the more slowly in the dark than if a zero disparity stimulus is Kass Foundation. provided. In contrast to the horizontal system, the decay of Submitted for publication April 20, 1999; revised September 22 torsion to its initial alignment is reportedly almost complete, and November 2, 1999; accepted November 30, 1999. even after prolonged (tens of minutes17) exposure. Van Rijn Commercial relationships policy: N. 18 Corresponding author: David S. Zee, Pathology 2-210, Johns Hop- et al. reported a systematic difference in cyclovergence, kins Hospital, 600 North Wolfe Street, Baltimore, MD 21287. measured using an objective technique, while a subject [email protected] fixed on a dot with or without a structured background. This Investigative Ophthalmology & Visual Science, April 2000, Vol. 41, No. 5 1076 Copyright © Association for Research in Vision and Ophthalmology Downloaded from iovs.arvojournals.org on 09/24/2021 IOVS, April 2000, Vol. 41, No. 5 Cyclophoria Adaptation 1077 difference implies cyclophoria in the absence of disparity Eye Movements cues. Adaptation of cyclophoria, related to head roll, has Horizontal, vertical, and torsional eye movements were re- been described recently in abstract form.19 corded using the magnetic field search coil technique with In the present study, using an objective technique to dual-coil annuli.20 The field coil system consisted of a cubic measure the torsional position of the eye, the time course of coil frame of welded aluminum that produced three orthogo- decay of cyclovergence after a sustained exposure to cyclodis- nal magnetic fields with frequencies of 55.5, 83.3, and 42.6 parity is described. The present study also provides an objec- kHz and intensities of 0.088 Gauss. The side length of the coil tive demonstration of rapid phoria adaptation in the cyclover- frame was 1.02 m. Amplitude-modulated signals were ex- gence system. tracted by synchronous detection. The bandwidth of the sys- tem was 0 to 90 Hz. Maximum levels of peak-to-peak noise signals, measured behaviorally for a period of 5 seconds of METHODS steady fixation, were approximately 0.05° for horizontal eye position, 0.08° for vertical eye position, and 0.1° for torsional Subjects eye position. The voltage offsets of the system were zeroed by Four normal subjects (ages 22–54) who had no disorders of placing the dual search coils in the center of a metal tube that ocular motility and had normal stereopsis, indicated by identi- shielded the coils from the magnetic fields. Thereafter, the fying all elevated circles on the Randot test, participated in this relative gains of the three magnetic fields were determined study. Informed consent was obtained according to a protocol with the search coils on a gimbal system placed in the center conforming to the Declaration of Helsinki and approved by the of the coil frame. Further details of the calibration procedure Johns Hopkins Joint Committee on Clinical Investigation. No are as described previously.7,21 The positions of the eyes were spectacles were worn during testing. calculated in rotation vectors, but eye movement data are expressed here in a Fick coordinate reference frame, so that Display torsion reflects rotation of the eye around its line of sight. For Subjects were seated in the dark, their heads stabilized by a bite practical purposes, because the eyes were kept near the bar. Stimuli were presented dichoptically using a virtual-reality straight-ahead position, the choice of coordinate frame does display mounted on the head (ProView 60; Kaiser Electro- not affect the results. optics, Carlsbad, CA), with a display brightness of 25 foot lamberts and display area of 36° (V) ϫ 48° (H), composed of Possible Coil Artifacts 480 ϫ 640 pixels, the boundary of which was visible during It has been suggested that long-term drifts (Ͼ20 seconds) of display. This display was calibrated using a small video camera torsional coil signals are mainly due to torsional slippage of the mounted on a calibrated gimbal to determine the angle sub- annulus around the line of sight.18,21 Short-term torsional changes tended between lines forming a grid of known pixel spacing. (in the range 10–20 seconds), however, more closely reflect The virtual-reality display was shown in preliminary experi- actual torsional eye position.22 This is supported by photographic ments not to confound the measures of eye position. Recorded recordings of eye position.23 Accordingly, most analysis of eye position was unaffected by whether the video display was changes in eye position restricted comparisons to within short on or off, and translation of the headset over many centimeters periods (see description later). Another type of artifact in torsional caused a variation in recorded eye position of, at most, Ϯ0.16°. eye position occurs when the coil abruptly slips during large In the experiments, any headset movement was minimized by saccades and blinks. We could usually identify these changes and supports for the eyepieces that were fixed to the bite bar, and ensure the data were interpreted appropriately. the head itself was stabilized with the bite bar. Three kinds of stimuli were used, all light-on-dark gratings Protocol rendered with antialiasing (3D Studio, Autodesk, San Rafael, In each trial, the subject was initially presented with a stimulus CA). Horizontal gratings were used in all subjects: subtending at zero cyclodisparity. After a period of 10 seconds, the stim- 48° horizontally and 36° vertically, composed of eight equidis- ulus was stepped to a 5° cyclodisparity, either in- or ex-, which tant horizontal, parallel lines, each subtending 0.4°, and a was maintained for 30 seconds.
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