Abstract
Dynamic visual acuity is an important clinical tool for assessment of the rotational vestibulo-ocular reflex (rVOR). It is based on the fact that the normal rVOR stabilizes vision and maintains visual acuity during head rotation. The translational VOR (tVOR) generates eye movements during linear head motion. Studies in humans have shown that gaze stabilization during translation is incomplete and that there is a strong effect of the visual environment: eye velocity is much greater in the light than in the dark. In this study, we measured visual acuity during vertical translation in 11 subjects and asked whether a more complex visual background would enhance the response and improve acuity. During 2 Hz whole-body translation, tumbling-E optotypes (0.0–0.9 logMAR in steps of 0.1 logMAR, six trials of each size randomly ordered) were flashed on a screen that was 30 cm in front of the subject’s eyes. The subject reported the optotype’s orientation with a joystick. Based on a threshold of 75% trials correctly identified, the group dynamic acuity was 0.72 logMAR, compared to a static acuity of 0.0 logMAR. When the background was enhanced with a stationary dot pattern, dynamic acuity improved to 0.42 logMAR. Our findings show that vertical head translation degrades vision more than head rotation. This may limit the use of dynamic acuity as a clinical measure of otolith function.
Introduction
Assessment of vestibular function is important in the diagnosis of dizziness and balance disorders. Dynamic visual acuity (DVA) has emerged as a valuable tool that is not only a surrogate measure of the integrity of the vestibulo-ocular reflex (VOR) but also a functional test of the effect of vestibular impairment on vision. Rotational DVA (rDVA) has a high sensitivity and specificity for the detection of impaired semicircular canal function and is commonly used in clinical diagnosis and assessment of response to rehabilitation [2–5, 25]. Based on these studies, individuals with normal vestibular function typically lose from less than 0.1 logMAR of acuity (one line on the Snellen chart) at lower head speeds and frequencies [5] up to nearly 0.4 logMAR during abrupt, rapid head rotations [25]. For each of these stimulus types, patients with deficient vestibular function have sufficiently more loss of dynamic acuity that they can be distinguished from normal subjects. The amount of DVA loss depends on several factors, including age [5, 7], motion speed/acceleration [2, 24], predictability [4, 25], whether vestibular loss is unilateral or bilateral [5, 25], and the degree of compensation [4, 17].
In contrast to head rotation, gaze stabilization is less complete during head translation, even in the absence of vestibular disease. The translational VOR (tVOR) compensates for linear head motion based on inputs from the otolith organs. It is a more complex reflex than the rVOR, depending highly on viewing distance [9, 22], on the visual environment [9, 23] and on the predictability of head motion [20, 26]. In particular, the tVOR in humans is much more robust in the light than in the dark, even at a frequency (2 Hz) for which visual tracking is expected to contribute little [9].
The present study examines visual acuity during vertical translation. Prior studies have shown that the vertical tVOR in humans is under-compensatory, even in the light; tVOR gains are much lower than what would be required to stabilize the fovea on the object of regard [9, 26]. More studies have investigated the response to interaural translation and have reported a wide range of tVOR gains [1, 23]. It is not possible to combine these varied results meaningfully, because of marked differences in the dynamics of the motion stimuli (e.g., abrupt steps vs. sinusoidal translation), stimulus frequency, viewing condition (dark vs. light), target distance (15–440 cm), and the method by which gain was calculated. In some cases, response measures other than gain were reported. The most robust tVOR occurs with near viewing; for studies in which the viewing distance was ≤30 cm, interaural tVOR gains ranged from <0.1 for some subjects during whole-body translations in the dark [1] to 0.63 for abrupt head translations with viewing of a continuous target [16].
Clinical application of rDVA is well established [3], but data supporting the use of DVA in the assessment of the tVOR and otolith function are more limited. Lempert, et al., reported an increase in errors reading numbers of a single size during interaural translation at 1.5 Hz but not at 1 Hz [6]. Schmäl, et al., found only a small decrease in DVA in normal subjects during 1.5 Hz interaural translation [19] and no decrease during vertical translation [18], but both were tested with far viewing (440 cm) and optotypes were visible at the time of zero velocity. Finally, near viewing during treadmill walking, which elicits combined head translation and rotation [15], results in greater decrease in acuity compared to distance viewing [14].
The present study had two main objectives. First, we investigated tDVA during pure vertical translation to confirm that head translation substantially degrades vision during near viewing. Second, we asked whether a more complex visual background would enhance retinal image stability and improve tDVA, similar to the enhancement, albeit incomplete, of the tVOR by vision.
Methods
Subjects
Eleven healthy adult participants (5 M, 6 F) participated in this study. Participants were interviewed to rule out any neurological, otologic, or ocular disorders, other than refractive error. Subjects who required corrective lenses wore them during the experimental session. All subjects gave informed, written consent in accordance with the Declaration of Helsinki, under a protocol approved by the Institutional Review Board of the Cleveland Veterans Affairs Medical Center.
Apparatus
Subjects were seated on a chair mounted to a Moog 6DOF2000E electric motion platform (Moog, East Aurora, NY), and secured with safety belts around the torso. An adjustable, chair-mounted skateboard helmet was used to stabilize the head relative to the platform. For safety, an investigator with an emergency stop button was present to monitor the platform throughout the duration of the experiment. Platform and head positions were tracked with an infrared motion capture system (Vicon Motion Systems, Los Angeles, CA), utilizing four reflective markers on the helmet and one over the temporal process of each zygomatic bone. Optotypes for the acuity test were presented on a 4th generation iPod Touch (Apple, Cupertino, CA), at a viewing distance of 30 cm. At this distance, the display’s specifications allowed for minimum resolvable detail corresponding to –0.05 logMAR. The iPod was linked to a host computer via a dedicated 802.11 g wireless connection and operated as a remote virtual display (iDisplay, Shape Services, Brookline MA). User responses were recorded using a joystick with a 4-way thumb switch. Images for the visual acuity test and user responses were handled by a custom program running in MATLAB (The MathWorks, Natick MA) on the host computer.
Visual acuity testing
The tVOR stimulus chosen for this study was a 4-cycle, 2 Hz sinusoidal vertical translation (peak acceleration 0.38 g, peak velocity 30 cm/s, and peak displacement 2.39 cm). The tumbling-E optotype was chosen for the visual acuity test, as there was not sufficient screen resolution at this viewing distance to present the smallest Landolt C optotypes. The tumbling-E was presented at 10 sizes between 0.0 and 0.9 logMAR inclusive, at steps of 0.1 logMAR. Optotypes were white, presented on a black background, and testing took place in a darkened room. Each trial consisted of a tVOR stimulus associated with a single optotype presentation for a 100 ms segment of the penultimate half-cycle of the tVOR stimulus, around the time of peak velocity. In the periods between optotype presentations, a small crosshair was presented on the screen at the location of the optotype in order to provide a fixation reference for the subject. For each condition, a complete test set contained 60 trials, 6 at each of the 10 possible acuity levels, in pseudo-random order. A forced choice paradigm was used, with subjects instructed to provide a response for every trial, indicating with the thumb switch toward which direction the E was pointed.
Three different testing conditions were used in this study: static, dynamic enhanced (DE), and dynamic non-enhanced (DN). In the static condition, subjects were seated in the testing apparatus and the visual acuity test was performed as described above, but the platform remained stationary. For the dynamic conditions (DE and DN), the acuity stimulus was presented during translation. In the DE condition, a fixed random dot pattern surrounded the fixation cross-hair (Fig. 1), based on the hypothesis that a more complex visual stimulus would enhance the tVOR, aiding gaze stabilization, and thereby would improve dynamic acuity. Conversely, in the DN condition, the fixation cross-hair was made to flash (on for 100 ms, off for 900 ms) and there was otherwise no background, minimizing retinal slip. For each trial in the DN condition, the cross-hair flashed once a second five times, followed by the presentation of the optotype.
Data analysis
We quantified static and dynamic acuity for each subject in two ways. First, we determined an acuity threshold for each condition by fitting a sigmoidal curve to the fraction of correct responses for each logMAR. The fit was performed using a least-squares optimization method (nlinfit in MATLAB). Data were fit to the following function:
For both methods, a one-tailed Wilcoxon signed-rank test was used for paired comparisons of acuity measurements across conditions, testing the hypotheses that dynamic acuity is less than static acuity and that acuity for DE is greater than acuity for DN.
Measurement of the translational vestibulo-ocular reflex (tVOR)
Eye movements were not recorded in this study. Five of our 11 subjects, however, underwent measurement of the tVOR during 2-Hz vertical translation as a part of other experiments. In those experiments, the fixation distance was closer (∼15 cm) than was possible for this DVA experiment (30 cm); a prior study, however, showed that for this 2 Hz sinusoidal head motion, the tVOR gain varies little with fixation distance [9]. As in this prior study, a fully compensatory ideal eye movement was calculated from recorded head position, calibrated to viewing distance, and the tVOR gain was determined as the ratio of the amplitude of the actual eye movement to this ideal eye movement.
Results
Figure 2 shows tDVA results from one subject (left panel) and for the group (right panel). Note that for both the individual subject and for the group as a whole, there were more errors during motion than in the static condition. For the smaller optotypes, the error rate was higher in the visually impoverished (DN) than in the visually enhanced condition (DE).
Fits for determination of acuity thresholds are shown in Fig. 3 for one subject. In each case, the location on the curve corresponding to fcorr= 0.75 is shown by an open circle. Note that this threshold is close to zero for the static condition, corresponding to an equivalent Snellen acuity of 20/20, whereas the threshold is much greater during translation and highest for DN. The median acuity thresholds were 0.0 logMAR (20/20) for the static condition, 0.42 logMAR (20/53) for the DE condition, and 0.72 logMAR (20/105) for the DN condition. This represents a loss of roughly four lines of acuity for DE and 6 lines for DN.
Figure 4 shows group data for all subjects for each of the two acuity measures. For both threshold and AUC, the median tDVA was significantly lower than static acuity, and DE acuity was better than DN acuity.
For the five subjects with tVOR measurements, the tVOR gain was 0.55 + – 0.14 (mean + – 95% C.I.), similar to what has been previously reported for this stimulus [9]. For this small sample, however, there was no direct correlation between tVOR gain and tDVA, whether measured by threshold or by AUC (p > 0.6).
Discussion
Our results confirm that vertical translational motion decreases visual acuity substantially at near viewing distances. This functional measure agrees with direct assessment of the tVOR at the same frequency. In normal subjects, including those in this study in whom the tVOR was measured, the vertical tVOR at 2 Hz has an average gain of about 0.4–0.6, thus compensating for only about half of the translational head movement [9, 26]; in response to abrupt head translations, the gain is even lower [16]. An additional finding of our study is that a more complex visual background aids gaze stability during translation and improves dynamic acuity, possibly via a supplementary optokinetic reflex.
An under-compensatory tVOR could impair tDVA by two primary mechanisms. First, the less than unity gain results in a retinal slip velocity that may be quite large. For our particular stimulus (30 cm/s peak velocity) and viewing distance (30 cm), a tVOR gain of 0.6 would create a peak retinal slip of about 26°/s and a root-mean square slip velocity of 18°/s, assuming a phase lag of 15° [9]. Retinal slip of 18°/s corresponds approximately to a DVA of 0.5 logMAR [2], similar to what was found in this study for the DE condition (0.42 logMAR).
Second, an under-compensatory tVOR fails to maintain gaze position on the target. Displacement of the optotype’s image away from the fovea could reduce acuity independent of the effect of retinal image motion. For this particular stimulus, assuming that eye position remains centered about the target, an average tVOR gain of 0.6 would imply a root-mean-square retinal position error of about 1.4°.
Why the tVOR is consistently under-compensatory, even with an explicit visual acuity task, remains elusive. Such a deficient tVOR cannot be simply attributed to exceeding the response dynamics of the reflex, but rather it appears that the gain is deliberately set to be low, even if this sacrifices visual acuity. For example, moving the target closer will increase eye velocity dramatically, but the gain will remain about the same [9]. Eye velocity also increases if viewing distance is kept constant, but image magnification is increased optically; again the gain remains about 0.5 [8]. Thus, although visual input contributes substantially to eye velocity during translation, and it improves DVA, as we have shown here, it still does not lead to foveal image stabilization; considerable retinal slip is maintained. Such behavior is very different from the rVOR, for which maximizing gaze stimulation is the primary goal. One alternative that has been suggested is that the tVOR may be optimized to assist depth perception based on motion parallax that occurs when moving through an environment containing objects at different distances [10], but this hypothesis has not been directly tested. Even if this were the case, it remains curious that during a visual acuity task, such a strategy cannot be or is not altered, in favor of foveal stabilization. Further experiments will be required to elucidate more clearly these mechanisms.
In conclusion, DVA is considerably reduced during vertical head translation in normal subjects, although less so when visual cues are added to assist gaze stabilization. This confirms that the low gain of the tVOR, which causes retinal slip and loss of foveation, has a substantial impact on visual function. Further studies will be required to determine if there is a set of stimulus conditions that will nonetheless be able to detect impaired vestibular function based on tDVA.
Disclaimer
The contents do not represent the views of the U.S. Department of Veterans Affairs or the United States Government.
Footnotes
Acknowledgments
The authors thank Dr. R. John Leigh for critically reading this manuscript and Dr. Ke Liao for technical assistance. This material is the result of work supported with resources and the use of facilities at the Louis Stokes Cleveland Department of Veterans Affairs Medical Center.