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Original contribution

Dynamic visual acuity while walking in normals and labyrinthine-deficient patients
Edward J. Hillmana , Jacob J. Bloomberg b,∗ , P. Vernon McDonald c and Helen S. Cohen a
Bobby R. Alford Department of Otorhinolaryngology and Communicative Sciences, Baylor College of Medicine, Houston, TX, USA b Life Sciences Research Laboratories, NASA Johnsn Space Center, Houston, TX, USA c Wyle Life Sciences, Houston, TX, USA
Received 29 August 1996 Accepted 20 January 1998
a

We describe a new, objective, easily administered test of dynamic visual acuity (DVA) while walking. Ten normal subjects and five patients with histories of severe bilateral vestibular dysfunction participated in this study. Subjects viewed a visual display of numerals of different font sizes presented on a laptop computer while they stood still and while they walked on a motorized treadmill. Treadmill speed was adapted for 4 of 5 patients. Subjects were asked to identify the numerals as they appeared on the computer screen. Test results were reasonably repeatable in normals. The percent correct responses at each font size dropped slightly while walking in normals and dropped significantly more in patients. Patients performed significantly worse than normals while standing still and while walking. This task may be useful for evaluating post-flight astronauts and vestibularly impaired patients. Keywords: Oscillopsia, walking, human, dynamic visual acuity

1. Introduction The maintenance of functional visual acuity during activities of daily living often demands that gaze be
∗ Reprint address: Jacob J. Bloomberg, PhD, NASA Johnson Space Center, Mail Code: SD3, Houston, TX 77058. Tel.: +281 483 0436; Fax: +281 244 5734; E-mail: jbloombe@ems.jsc.nasa.gov.

stabilized during body motion and/or when the object of visual regard is moving. For example, the act of walking subjects the head to translation and rotation in 6◦ of freedom [1,2]. Moreover, every heelstrike with the ground sends a shockwave through the body to the head [3], causing transient vibrations which, if visual acuity is to be maintained, must be countered. Trying to read the signs for the correct aisle in the grocery store can be a challenge under these conditions. A similar set of perturbations are experienced while driving an automobile, or flying an aircraft: notably, translation through the environment coincides with transient vibrations from the motion of the vehicle on the support surface. These vibrations are transmitted through the seat to the head and can degrade visual acuity. Accurate appraisal of cockpit displays can be very challenging under these conditions. Certain changes in the human system can lead to unsteady or blurred vision during these common activities of daily living. Illusory movement of the visual world with head motion was termed “oscillopsia” by Brickner in 1936 [4]. Labyrinthine-deficient (LD) individuals have commented that oscillopsia impairs the ability to read the instrumentation dials on the dashboard of an automobile while driving [5]. Oscillopsia has been recognized as a symptom of vestibular loss for over 50 years, but has only been described anecdotally in astronauts returning from spaceflight [6]. We have observed that oscillopsia is experienced during active head motion as well as during locomotion during the post-flight recovery period [7]. Several explanations could account for this phenomenon. Post-flight perceptual recalibration along with alterations in head stability and head-trunk coordination during locomotion [7] coupled with changes in energy modulation and transfer associated with heel strike during walking [8,9] could conceivably lead to oscillopsia in crewmembers returning from spaceflight. We reasoned that those individuals who experience oscillopsia would most likely also experience a com-

Journal of Vestibular Research 9 (1999) 49–57 ISSN 0957-4271 / $8.00  1999, IOS Press. All rights reserved

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promise of visual acuity during activities of daily living. A degradation in visual acuity which might lead to an incorrect reading of a cockpit instrument, or a roadside sign, has life threatening implications. The test described in this report was designed as a convenient method of quantifying visual acuity under conditions common to all humans who wish to maintain functional mobility. Dynamic visual acuity (DVA) is the threshold of visual resolution obtained during relative motion of either optotypes or observer [10]. DVA has been measured in patients in several ways including manually moving a display in front of a patient [11], having a patient make active sinusoidal head movements, or having a patient walk in place while attempting to read a visual display [12]. The earliest test of DVA involved moving Snellen letters or Landolt C’s in the horizontal plane while a stationary subject attempted to read or decipher the moving images [13], with more recent investigators using slide projectors and rotating mirrors to project moving images on a screen [14]. Other early DVA studies moved the observer rather than the optotype [15]. Most recently, rotating chairs have been used to move subjects in either the vertical or horizontal plane while they attempted to read a stationary display [16]. Other investigators have tested DVA while subjects made active head motions in the horizontal plane [17,18]. Although these tests accurately assess the vestibular and visual contributions to the maintenance of DVA, they have not addressed the issue of DVA under conditions commonly experienced during activities of daily living. On a daily basis we must all perform tasks that require seeing clearly while moving the head. The treadmill walking task we describe provides a controllable protocol for evaluating visual acuity under the dynamic conditions of walking. Treadmill walking requires the integration of all the systems normally involved in maintaining visual acuity during overground walking, albeit in the absence of the macroscopic horizontal optic flow. The design of this test was intended to satisfy several requirments based on long-term plans for evaluations of functional visual acuity in clinical settings and spaceflight related operational settings. Specifically, the test must be readily implementable at any testing location, be easily administered, last no longer than 10 minutes, provide performance data immediately post-test, not be dependent on a knowledge of the English alphabet (for example, Snellen letters), and avoid stimuli that require spatial orientation skills for interpretation (for example, Landolt C).

The test described in this paper meets all of the above requirements. This report compares the performance of normals and bilateral LD patients undertaking this test during treadmill walking.

2. Methods 2.1. Subjects Ten normal subjects (6 males and 4 females) were recruited from among laboratory personnel at the Johnson Space Center (JSC), mean age 30.8 years, range 26 to 35 yrs. They all denied histories of inner ear, neurological, or musculoskeletal disorders. Six subjects used corrective lenses or contact lenses which were worn during testing. Five patients (3 females and 2 males ) with histories of severe bilateral vestibular dysfunction were recruited from among patients evaluated at the Center for Balance Disorders/Baylor College of Medicine, mean age 40 years, range 24 to 49. Four of the five subjects used corrective lenses, which were worn during testing. All subjects reported corrected static visual acuity close to 20/20. All patients answered questionnaires to document the etiologies of their vestibular dysfunctions, symptoms, past treatments, and current medications. All patients had undergone electronystagmography (ENG) testing in the past as part of their evaluation, and all of them had no response to warm (44◦C), cool (31 ◦ C), and cold (3 ◦ C) water irrigations as well as markedly decreased VOR gains at all frequencies tested (0.0125, 0.05, and 0.2 Hz). No patients had spontaneous nystagmus. Two of the five patients had associated hearing loss. Table 1 summarizes their demographic data, and Table 2 their clinical data. Patients were also screened for cardiac, pulmonary, musculoskeletal, and visual disorders, exercise tolerance, and other conditions which would interfere with walking adequately and safely during testing. Patient 1 had a 10-year history of bilateral vestibular dysfunction as well as a profound, bilateral sensorineural hearing loss for which she had undergone implantation of a cochlear implant in 1994. The etiology of her inner ear disorder was believed to be Cogan’s disease. She had no residual visual disturbances secondary to mild interstitial keratitis that she had experienced early in the course of her disease. Her main complaints at the time of testing were difficulty reading signs while walking and ambulating in poorly lit environments.

E.J. Hillman et al. / Dynamic visual acuity while walking Table 1 Summary of patient demographic and clinical information Patient 1 2 3 4 5 Age (yrs)/Sex 38/F 47/F 42/F 49/M 24/M Etiology Cogan’s syndrome Gentamycin toxicity Idiopathic Possible ototoxicity Idiopathic Chief Complaint Hearing loss, Oscillopsia Oscillopsia Oscillopsia Hearing loss Oscillopsia

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Table 2 Summary of patient VOR data Patient 1 2 3 4 5 1 2 3 4 5 1 2 3 4 5 Test frequency (Hz) .0125 Normal gain range 0.30–0.80 Patient gain right .01 .08 .01 .01 .02 .00 .04 .01 .01 .20 .19 .34 .14 .07 .12 Patient gain left .02 .02 .01 .04 .04 .05 .03 .01 .01 .20 .10 .24 .14 .22 .12

.05

0.35–0.90

.20

0.45–0.90

Patient 2 had a history of right lower limb trauma in 1991 after being struck by a car. She subsequently developed osteomyolitis and was treated with gentamycin. During treatment she began to experience significant oscillopsia from which she currently suffers. She denied any history of hearing loss. She currently has a leglength discrepancy, and her ankle is fused. She is able to ambulate short distances unassisted, but uses a straight cane while walking long distances or on uneven surfaces. Patient 3 had a vestibular disorder of unknown etiology. She began to experience episodic vertigo on three separate occasions in 1975, 1 to 2 weeks apart, each episode lasting 3 to 4 days. These symptoms gradually progressed to constant unsteadiness in the dark and difficulty reading signs while walking. She denied any history of hearing loss. Patient 4 was treated for typhoid fever with unknown medications at the age of 9 in Egypt. Since that time he has complained of bilateral hearing loss, greater on the right. Superimposed on this stable hearing loss, he also reported a history of episodic, temporary deterioration in his hearing associated with bilateral tinnitus. These episodes last about 2 months; the last episode occurred 18 months prior to testing. His only vestibular complaints were mild unsteadiness, primarily in the dark. He denied any vertigo or oscillopsia.

Patient 5 reported a history of episodic mild unsteadiness associated with “bobbing of his eyes” since childhood. These episodes occurred every 3 to 4 months and lasted several minutes to an hour. In 1994 these episodes became more frequent and severe. Since that time he has had constant oscillopsia and difficulty ambulating in the dark. The etiology of these problems is unknown. 2.2. Experimental protocol The test used a Macintosh Apple Powerbook TM 180 and Microsoft Power Point TM slide presentation program. The actual test consisted of presentation of 10 slides appearing on ghe computer screen. Each slide presented a string of white numbers on a black background at one particular font size (Fig. 1). Font sizes ranged from 12-to 20-point font in increments of 2 points. These sizes were chosen because at 2 meters these fonts sizes correspond to a range of visual acuity of 20/16 to 20/27 on a traditional Snellen eye chart (Table 3). This range encompasses most subjects’ static visual acuity. Geneva font was chosen because of its relative simplicity and lack of elaborate number design. One trial consisted of 10 slides, each slide presenting a string of 5 numerals at one font size, visible for 3 seconds. The 5 font sizes were presented pseudorandomly;

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E.J. Hillman et al. / Dynamic visual acuity while walking Table 3 Angle subtended at 2.0 m viewing distance for each font size (Snellen letters for viewing distance of 6.0 m, subtend angle of 5-min Arc Geneva font size 12 14 16 18 20 Pixel height 9 11 13 14 15 Letter height (mm) 2.97 3.63 4.29 4.62 4.95 Angle at 2.0 m (degrees) 0.085 0.103 0.122 0.132 0.141 Angle at 2.0 m (min arc) 5.10 6.23 7.37 7.93 8.50 Snellen ratio 20/ 19.5 18.1 20.4 24.9 27.2

Fig. 1. Laptop computer presenting a string of numbers at one font size.

each font size was presented in 2 slides for a total of 10 numbers per font size per trial. Subjects were given 5 trials, for a total of 250 numerals presented under each condition. Numerals were balanced among integers from 0 to 9 such that each integer was presented an equal number of times. Stimuli were presented with a right-to-left transition, that is, the stimulus slide “slid” onto the screen from the right and “slid” off the screen to the left. Total testing time averaged 10 minutes per subject. The test was administered under two conditions: 1) standing and 2) treadmill walking. Normals and patient 5 walked at 6.4 km/h on the treadmill. This speed was chosen to be consistent with that used in previous and ongoing studies at JSC of head and gaze stability during treadmill locomotion after spaceflight. The other patients were unable to walk at 6.4 km/h unsupported. Patients 1 and 4 were able to walk without touching the

bar on the front of the treadmill but were able to walk safely at a maximum speed of 4.8 km/h. They were tested at that speed. Due to her orthopedic limitation patient 2 needed to support herself with both index fingers on the support bar; she felt safe walking at a maximum speed of 2.4 km/h and was tested at that speed. Patient 3 was able to be tested at 6.4 km/h, but only while touching the safety bar with one index finger. Although use of this design precluded testing all subjects on the same protocol, patient safety was of paramount concern, so the protocol was adapted accordingly. All of the normals were tested at least once at JSC, whereas all of the patients were tested at The Methodist Hospital (TMH). Subjects walked on motorized treadmills (QuintonTM Series Q55 at JSC and Quinton TM Clubtrack at TMH), which provided comparable stimuli. At JSC subjects wore a safety harness; at TMH subjects were spotted by test operators at all times. During

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This process necessitated the use of two statistical models based on different assumptions [19]. A multivariate model was used when all independent variables for an analysis were within-group variables, that is, when normal subject performance was analyzed. The resulting probability values were adjusted for violation of the assumption of sphericity through the GreenhouseGeiser and Huynh-Feldt methods. The appropriate adjusted probability values are reported. A univariate model was used to compare the performance of normals and patients when contrasts involved both withinand between-group independent variables, and the resulting probability values are not adjusted for violation of the assumption of sphericity. A significance level of 0.05 was used throughout.

3. Results
Fig. 2. Subject performing visual acuity test while walking on the treadmill.

3.1. Normal subject performance and test reliability Subject performance was defined as the percentage of correct responses at each font size. Statistical analyses used the mean number correct at each font size as the dependent variable. Figure 3 shows the performance of all 10 normals, both while standing still and while walking at 6.4 km/h. ANOVA indicated no differences in performance with different font sizes while standing still, but while walking, performance decreased significantly (F (1, 9) = 14.04, P = 0.005). This difference was due primarily to a significant decrement in performance at only the smallest font size (F (1, 36) = 47.65, P = 0.0001). No significant differences in performance were seen at any of the larger font sizes. Figure 4 shows the test-retest reliability. Overall test-restest performance at JSC did not differ significantly (F (1, 4) = 0.70, P = 0.45). When broken down by font size, however, subjects performed significantly better on Day 2 at the smallest font size [12] while walking (F (1, 16) = 27.14, P = 0.0001). Figure 5 shows the mean performance of 4 normals tested at JSC and TMH. Overall performance did not differ significantly between the two locations (F (1, 4) = 2.79, P = 0.19). When analyzed by font size, significant performance decrements were found at font sizes 14 (F (1, 12) = 8.73, P = 0.01) and 12 (F (1, 12) = 24.24, P = 0.004) while walking. Subject performance was worse at these font sizes at TMH.

testing, the Powerbook was placed on a tripod at the subject’s eye level at a distance of 2 meters as measured from the screen to the outer canthus of the eye (Fig. 2). The angle between the keyboard and the screen was maintained at 90 ◦ and confirmed with a right angle. The brightness and contrast controls were adjusted for maximum brightness and contrast. Room lighting was held constant during all testing. The protocol was approved by the Baylor College of Medicine Affiliated Review Board for Human Subjects prior to administration of the test. All subjects signed an informed consent form prior to participating. The study involved 4 phases: 1) Ten normal subjects were tested on both conditions at JSC. 2) To assess test-retest reliability, 5 of the original 10 normal subjects were tested at JSC on a second occasion more than one week after the original test, under identical conditions. 3) To assess the effect of location on performance, with slightly different lighting conditions and treadmill models, 4 of the original 10 normals (who had not participated in phase 2) were retested at TMH more than one week after the original test. 4) Five patients were tested at TMH. Since the data consisted of repeated assessment of the performance of two groups of subjects obtained at two conditions, standing and walking, repeated measures analysis of variance (ANOVA) procedures for withinand between group independent variables were used.

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Fig. 3. Performance of 10 normal subjects while (A) standing and (B) walking at 6.4 km/h. Each symbol represents one subject. Some subjects overlap.

Fig. 4. Average performance of 5 normal subjects while (A) standing and (B) walking at 6.4 km/h on two separate testing occasions. Squares represent the first testing session; circles represent the second testing session. Error bars represent ± 1 standard error of the mean.

3.2. Patient performance

4. Discussion The test described here is deceptively simple. It meets all of the complex requirements of a test suitable for easy and flexible clinical and operational implementation, but it still provides a valid and reliable measure of functional visual acuity. Normal subject performance revealed decrements only at the smallest font size, both while standing and while walking. This decrement probably represents the DVA threshold for most subjects and, if smaller font sizes had been used, performance curves similar to those seen in patient testing would probably have been seen, albeit shifted towards the smaller font sizes.

As described above, patients were tested at slightly different conditions when walking. Figure 6 shows the performance of individual patients while standing and walking. Within-subjects analyses indicated that patients showed overall performance that was significantly worse while walking than when standing (F (1, 4) = 105.48, P = 0.0001). When compared to normals, patients showed significantly poorer overall performance while standing (F (1, 4) = 85.03, P = 0.0001) and while walking (F (1, 4) = 394.28, P = 0.0001).

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Fig. 5. Average performance of 4 normal subjects while (A) standing and (B) walking at 6.4 km/h tested at two different locations. Squares represent tests at JSC, and circles represent tests at TMH. Error bars represent ± 1 standard error of the mean.

Fig. 6. Performance of patients (A) while standing and (B) walking. Average performance of 10 normal subjects is included for comparison (bold line).

Reliability of the test was established relative to repeated testing and testing location. The significant differences in performance at the smallest font sizes while walking may have been a result of slight differences in illumination between testing sites, however, the magnitude of the performance difference in absolute terms is relatively small. The differences seen in test-retest assessment suggest a potential training effect on only the most demanding part of the test. Given the small sample size, these significant differences could also represent a statistical phenomenon that might have disappeared given a larger sample. Importantly, from a clinical standpoint, however, overall performance did not differ, and those differences found at the smallest font sizes were small in magnitude compared to the

differences in performance seen among the patients. Therefore, when a patient or crewmember with clinically and functionally significant decreases in visual acuity is tested on two occasions or at two locations, the test will detect the degree of change accurately and reliably. While standing, patients performed significantly worse than normals, although they all reported near normal corrected static visual acuity. In contrast to the normals, patients had significant decreases at all font sizes while standing and while walking. The magnitude of these differences reveals the inability of these patients to compensate for motion and maintain visual acuity while walking. These differences also suggest that this test may be useful in quantifying the severity

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of oscillopsia. However, additional data are needed to verify this suggestion. Although the patients were tested under different dynamic conditions, their performance curves are qualitatively very similar both in absolute values and in shape. Despite these disparities, the patients differed significantly from normals, especially while walking. This difference will allow a physician who is evaluating a post-flight crew member or an LD patient to identify deficits in DVA and possible related functional limitations. The maintenance of visual stability during locomotion is a complex task requiring not only precise interaction between the visual and vestibular systems but also coordination between the head and trunk to maintain head stability during walking. A breakdown in any of these systems can lead to the loss of visual stability. Head-trunk coordination is impaired in patients with vestibular dysfunction, resulting in decreased head stability during locomotion [12,20]. Similarly, after space flight astronauts exhibit comparsble changes in the efficacy of head movement control during locomotion [7]. More recently an abbreviated version of the DVA protocol described here, also using a treadmill walking paradigm, has been used to test crew following several months in space. Preliminary data indicate decreased DVA shortly after landing, as compared to pre-flight tests (Bloomberg and colleagues, unpublished data). The stability of the visual world during movement is important in the successful performance of a number of motion-intense activities, including sports, driving a car, or flying an aircraft [21–23]. Patients with vestibular deficits have difficulties performing these kinds of activities [24]. Given the similarities between this population and astronauts returning from spaceflight, it is possible that astronauts would also experience difficulty performing some of these same activities. An objective, reliable test of DVA while walking might provide a useful predictor of performance on some activities that require good DVA. This test of dynamic visual acuity while walking provides a valid, reliable, and sensitive method of evaluating the functional effects of dynamic visual acuity in patients with bilateral vestibular dysfunction. It can detect signs of vestibular impairment and has the potential to provide a quantitative measure of oscillopsia, which to data has existed as an otherwise unmeasureable subjective symptom.Therefore, it may be useful for following the progress of patients’ oscillopsia as well as for evaluation of post-flight crewmembers.

Acknowledgments The functional visual acuity test used in this report was first conceived by Gary Riccio, Ph.D., Nascent Technologies. We also wish to acknowledge Dr. Riccio’s substantial contributions to improving a prototype version of this test. Dick Calkins, Ph.D., Wyle Life Sciences, assisted with the statistical analyses; members of the Neuroscience Human Movement and Coordination Research Group at JSC assisted with subject testing; and the staff of the Methodist Hospital Cardiac Rehabilitation Laboratory provided the treadmill. Edward Hillman was supported in part by a Visiting Scientist research grant from Universities Space Research Association, Division of Space Life Sciences. Helen Cohen was supported by the Clayton Foundation for Research and NIDCD 5R29DCO2412-02. References
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