APRIL 1978 Vol. 17/4 Investigative Ophthalmology & Visual Science A Journal of Clinical and Basic Research Articles Training of voluntary torsion Richard Balliet and Ken Nakayama By means of a visual feedback technique, human subjects were trained to make large conjugate cyclorotary eye movements at will. The range of movement increased with training at a rate of approximately 0.8° per hour of practice, reaching 30° at the end of training. Photographs recorded the ability to make voluntary cyclofixations at any amplitude within the subject's range. Cyclotorsional pursuit was also trained, with ability increasing with greater amounts of visual feedback. In addition, torsional saccadic tracking was trained, showing a magnitude vs. peak velocity relationship similar to that seen for normal saccades. Control experiments indi- cate that all of these movements were voluntary, with no significant visual induction. With extended practice, large torsional movements could be made without any visual stimulation. The emergence of voluntary torsion through training demonstrates that the oculomotor system has more plasticity than has generally been assumed, reopening the issue as to whether other movements could also be trained to alleviate the symptoms of strabismus. Key words: eye movements, torsion, saccades, slow pursuit, fixation, orthoptics, oculomotor plasticity c' yclorotations are defined as rotations the eye can undergo a cyclorotation as it about the visual axis of the eye. These rota- moves from one tertiary position of gaze to tions are considered to be reflexive, with no another, but the amount of this cyclorotation indication of voluntary control. For example, is fixed, being dictated by Listings law.11 In addition, involuntary cyclovergence has been 1 From the Smith-Kettlewell Institute of Visual Science, reported to occur during convergence, and Department of Visual Sciences, University of the reflexive cycloversions have been demon- Pacific, San Francisco, Calif. strated to occur during lateral head tilt.14> 18 This paper is based on a Ph.D. dissertation submitted by Cycloversional movements can also be in- the first author to the Department of Visual Sciences, University of the Pacific, San Francisco, Calif. 94115. duced visually by large field stimuli (25° to The work was supported in part by NEI Grant 50°). These movements include optokinetic EY01582 and the Smith-Kettlewell Eye Research cycloversion,7* 8* 13 fusional cyclovergence,9 Foundation. and tonic cycloversions.8 All of these previ- Submitted for publication July 6, 1977. ously reported cyclorotary eye movements Reprint requests: Dr. Richard Balliet, Smith-Kettlewell Institute, 2232 Webster St., San Francisco, Calif. occur either as a necessary consequence of 94115. other movements or as part of a sensorimotor 0146-0404/78/0417-0303$01.20/0 © Assoc. for Res. in Vis. and Ophthal., Inc. 303 Invest. Ophthalmol. Visual Sci. 304 Balliet and Nakayama April 1978 however, a larger than average torsional response variability in all positions of gaze (S.D. = 0.75°). We reasoned that although small, M. N.'s tor- sional variability was clearly perceptible and perhaps sufficient to extend further by exploratory training procedures. As our first and pilot subject we worked closely with him, up to 5 hr/week over a period of 13 months, testing many methods to develop an apparently optimal approach, Then, having found successful procedures for M. N. (see later), we trained two normal individuals who showed no oculomotor abnormalities. Subjects R. B, (one of the authors, age 30) and C. H. (age 26) were chosen because of their high motivation. These subjects had normal stereopsis and eye movements and normal or corrected nor- mal acuity. Contact lenses were worn by C. H. Both subjects were trained and tested over a period of 2 months. Fig. 1. Photographs showing a tonic voluntary cy- Training and testing procedure. Many different clotorsion of 20°. Bars drawn in across the irises training procedures were used with M. N. We are similar to those used for photographic analysis. report only upon the final method used most suc- Vertical reference marker (present in all photo- cessfully with him and exclusively with C. H. and graphs) is seen at right. R, B. In general, the following procedures were conducted during both training and testing. During visual feedback training, the subject reflex. There are no instances where one sees was seated in a dark room with the left eye purposeful cyclofixations, or smooth and sac- always occluded. Torsional head movement was cadic torsional tracking, phenomena which fixed to within 6' of arc by a full-mouth impres- are common to voluntary horizontal or verti- sion bite plate (see Ditchbum10). Fixating a tar- cal eye rotations. get with the right eye, the subject activated a In this paper we will demonstrate that if an brief vertical electronic flash (11 x 14°), leading adequate sensory feedback loop is created, to the formation of a clear vertical afterimage. providing subjects with a very sensitive indi- By horizontally sliding the base of the bite cator of their own eye position, voluntary cy- plate mechanism, the subject then imaged the clotorsional eye movements can be trained. afterimage parallel to a vertical luminous real- Methodology and results will be presented line of equal visual angle which was viewed at which will substantiate that once this re- 100 om distance in primary position. The real- line was a partially occluded "white" 110 volt lationship is established, large voluntary cy- luminescent panel. It was bisected by a 15' clorotations can be learned and brought circular black fixation point. The subject con- under relatively fine control. trolled the luminance of the real-line over a range of 0.2 to 1.0 log foot-lamberts to prevent Tonic cycloversion visual suppression of the afterimage line by the Methods target line (or vice versa). He also controlled a Subjects. We report the successful training of This rotation angle could be observed by the sub- three subjects. Our first subject, M. N. (age 31) ject directly and/or by a digital voltmeter readout. had unilateral intermittent exotropia, his left eye The meter had an accuracy of ±4'. deviating 30°. Normally he allowed this exotropia The subject was instructed to keep his afterim- to be manifest. Otherwise, he had normal stere- age matched parallel only by cyclorotating his eye opsis, eye movements, and corrected acuity. Ini- to the real-line which he progressively rotated tially both eyes were tested for possible deviations more and more (left or right) from the vertical as from Listing's law. They showed no systematic training progressed. Usually 20' of arc increments deviation, with the mean torsion in each eye being were used. No instructions were given as to what 16 predictable by the direction of gaze We did see, type of eye movement was to be used to arrive at Volume 17 Number 4 Training of voluntary torsion 305 this position, e.g., slow pursuit, saccades, nystag- C.H. mus. Such matches which could be subjectively held for a minimum duration of 5 sec were defined as "cyclofixations." Subjects were encouraged to train equally in both incyclotorsional and excyclo- R.B. torsional directions, training usually at the rate of 1 hr/day. Photographic measurement of eye torsion. Ob- jective measures of cyclofixations were obtained from over 1,500 photographs taken with a 35 mm Nikon F-2 motor-driven camera with lenses and bellows attachments equivalent to a lens with a focal length of 400 mm. Two Vivitar 292 strobe 10 15 20 25 flash units provided illumination. High-resolution HOURS OF TRAINING color photographs on Kodachrome II film were Fig. 2. Training of voluntary tonic cycloversion for taken at 100 cm distance with a first-surface mirror subjects C. H. and R. B. Hours of training at 1 mounted at 30 cm distance in front of the subject hr/day vs. the total range (degrees) of psy- at a 45° angle, so positioned to be 5.0° off the chophysically measured torsion is plotted by the subject's primary visual axis. At this angle sys- small symbols. These are maximum tonic ranges tematic inaccuracies due to perspective distortion which can be held for a 5 sec duration. The three are minimal, not exceeding 3%. (See Appendix of large squares and the one large circle are simulta- Nakayama and Balliet16.) neous measures obtained photographically. The camera was activated by a button which could be pressed by the subject while he simulta- bination of optimal stimulus arrangements as neously held a subjectively determined cyclofixa- well as physical and mental effort. Very small tional match. Fixed to the bite bar was a vertical differences in the brightness of the afterim- photographic reference marker positioned near the outer can thus. Thus each photograph con- age and the real line led to the inhibition of tained all the information necessary to determine the dimmer by the brighter, necessitating eye torsion, eliminating errors due to possible fine control of the intensity of the real-line to camera or film misalignment. During photo- ensure the visibility of both. Attentive con- graphic analysis slides were magnifided 12 times centration was necessary to refrain from mov- in size by a Kodak Carousel projector. The image ing the afterimage with an attempted head was rear-projected onto a horizontal table screen movement. For example, during initial train- made of translucent "white" Mylar. Landmarks ing, two subjects broke bite plates, attempt- used in measurement were two identifiable ing unsuccessfully to rotate the afterimage by limbal-scleral blood vessel junctions which bor- making lateral head movements. dered a diameter of the iris and approximately bisected the pupil. The orientation of a line Slowly, however, the subjects succeeded formed between these two points relative to the in the task, learning to increase their range of stationary vertical marker was used in determining torsional eye movements with greater and objective cyclotorsion.