Vestibular Dysfunction and Dynamic Visual Acuity during Treadmill Locomotion

49

Original contribution

Dynamic visual acuity while walking innormals and labyrinthine-deficient patients

Edward J. Hillmana, Jacob J. Bloombergb,∗,P. Vernon McDonaldc and Helen S. Cohena

aBobby R. Alford Department of Otorhinolaryngologyand Communicative Sciences, Baylor College ofMedicine, Houston, TX, USAbLife Sciences Research Laboratories, NASA JohnsnSpace Center, Houston, TX, USAcWyle Life Sciences, Houston, TX, USA

Received 29 August 1996

Accepted 20 January 1998

We describe a new, objective, easily administered test ofdynamic visual acuity (DVA) while walking. Ten normalsubjects and five patients with histories of severe bilateralvestibular dysfunction participated in this study. Subjectsviewed a visual display of numerals of different font sizespresented on a laptop computer while they stood still andwhile they walked on a motorized treadmill. Treadmill speedwas adapted for 4 of 5 patients. Subjects were asked to iden-tify the numerals as they appeared on the computer screen.Test results were reasonably repeatable in normals. The per-cent correct responses at each font size dropped slightly whilewalking in normals and dropped significantly more in pa-tients. Patients performed significantly worse than normalswhile standing still and while walking. This task may beuseful for evaluating post-flight astronauts and vestibularlyimpaired patients.

Keywords: Oscillopsia, walking, human, dynamic visual acu-ity

1. Introduction

The maintenance of functional visual acuity duringactivities of daily living often demands that gaze be

∗Reprint address: Jacob J. Bloomberg, PhD, NASA JohnsonSpace Center, Mail Code: SD3, Houston, TX 77058. Tel.: +281 4830436; Fax: +281 244 5734; E-mail: [email protected].

stabilized during body motion and/or when the objectof visual regard is moving. For example, the act ofwalking subjects the head to translation and rotation in6◦ of freedom [1,2]. Moreover, every heelstrike withthe ground sends a shockwave through the body to thehead [3], causing transient vibrations which, if visualacuity is to be maintained, must be countered. Tryingto read the signs for the correct aisle in the grocery storecan be a challenge under these conditions. A similarset of perturbations are experienced while driving anautomobile, or flying an aircraft: notably, translationthrough the environment coincides with transient vi-brations from the motion of the vehicle on the supportsurface. These vibrations are transmitted through theseat to the head and can degrade visual acuity. Accurateappraisal of cockpit displays can be very challengingunder these conditions.

Certain changes in the human system can lead to un-steady or blurred vision during these common activi-ties of daily living. Illusory movement of the visualworld with head motion was termed “oscillopsia” byBrickner in 1936 [4]. Labyrinthine-deficient (LD) in-dividuals have commented that oscillopsia impairs theability to read the instrumentation dials on the dash-board of an automobile while driving [5]. Oscillopsiahas been recognized as a symptom of vestibular lossfor over 50 years, but has only been described anecdo-tally in astronauts returning from spaceflight [6]. Wehave observed that oscillopsia is experienced duringactive head motion as well as during locomotion duringthe post-flight recovery period [7]. Several explana-tions could account for this phenomenon. Post-flightperceptual recalibration along with alterations in headstability and head-trunk coordination during locomo-tion [7] coupled with changes in energy modulation andtransfer associated with heel strike during walking [8,9]could conceivably lead to oscillopsia in crewmembersreturning from spaceflight.

We reasoned that those individuals who experienceoscillopsia would most likely also experience a com-

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

50 E.J. Hillman et al. / Dynamic visual acuity while walking

promise of visual acuity during activities of daily liv-ing. A degradation in visual acuity which might lead toan incorrect reading of a cockpit instrument, or a road-side sign, has life threatening implications. The testdescribed in this report was designed as a convenientmethod of quantifying visual acuity under conditionscommon to all humans who wish to maintain functionalmobility.

Dynamic visual acuity (DVA) is the threshold of vi-sual resolution obtained during relative motion of eitheroptotypes or observer [10]. DVA has been measuredin patients in several ways including manually movinga display in front of a patient [11], having a patientmake active sinusoidal head movements, or having apatient walk in place while attempting to read a visualdisplay [12]. The earliest test of DVA involved movingSnellen letters or Landolt C’s in the horizontal planewhile a stationary subject attempted to read or decipherthe moving images [13], with more recent investigatorsusing slide projectors and rotating mirrors to projectmoving images on a screen [14]. Other early DVA stud-ies moved the observer rather than the optotype [15].Most recently, rotating chairs have been used to movesubjects in either the vertical or horizontal plane whilethey attempted to read a stationary display [16]. Otherinvestigators have tested DVA while subjects made ac-tive head motions in the horizontal plane [17,18].

Although these tests accurately assess the vestibularand visual contributions to the maintenance of DVA,they have not addressed the issue of DVA under condi-tions commonly experienced during activities of dailyliving. On a daily basis we must all perform tasksthat require seeing clearly while moving the head. Thetreadmill walking task we describe provides a control-lable protocol for evaluating visual acuity under thedynamic conditions of walking. Treadmill walking re-quires the integration of all the systems normally in-volved in maintaining visual acuity during overgroundwalking, albeit in the absence of the macroscopic hor-izontal optic flow.

The design of this test was intended to satisfy severalrequirments based on long-term plans for evaluations offunctional visual acuity in clinical settings and space-flight related operational settings. Specifically, the testmust be readily implementable at any testing location,be easily administered, last no longer than 10 minutes,provide performance data immediately post-test, not bedependent on a knowledge of the English alphabet (forexample, Snellen letters), and avoid stimuli that requirespatial orientation skills for interpretation (for example,Landolt C).

The test described in this paper meets all of the aboverequirements. This report compares the performanceof normals and bilateral LD patients undertaking thistest during treadmill walking.

2. Methods

2.1. Subjects

Ten normal subjects (6 males and 4 females) wererecruited from among laboratory personnel at the John-son Space Center (JSC), mean age 30.8 years, range 26to 35 yrs. They all denied histories of inner ear, neuro-logical, or musculoskeletal disorders. Six subjects usedcorrective lenses or contact lenses which were wornduring testing.

Five patients (3 females and 2 males ) with histo-ries of severe bilateral vestibular dysfunction were re-cruited from among patients evaluated at the Center forBalance Disorders/Baylor College of Medicine, meanage 40 years, range 24 to 49. Four of the five sub-jects used corrective lenses, which were worn duringtesting. All subjects reported corrected static visualacuity close to 20/20. All patients answered question-naires to document the etiologies of their vestibulardysfunctions, symptoms, past treatments, and currentmedications. All patients had undergone electronys-tagmography (ENG) testing in the past as part of theirevaluation, and all of them had no response to warm(44◦C), cool (31◦C), and cold (3◦C) water irrigationsas well as markedly decreased VOR gains at all fre-quencies tested (0.0125, 0.05, and 0.2 Hz). No patientshad spontaneous nystagmus. Two of the five patientshad associated hearing loss. Table 1 summarizes theirdemographic data, and Table 2 their clinical data. Pa-tients were also screened for cardiac, pulmonary, mus-culoskeletal, and visual disorders, exercise tolerance,and other conditions which would interfere with walk-ing adequately and safely during testing.

Patient 1 had a 10-year history of bilateral vestibulardysfunction as well as a profound, bilateral sensorineu-ral hearing loss for which she had undergone implanta-tion of a cochlear implant in 1994. The etiology of herinner ear disorder was believed to be Cogan’s disease.She had no residual visual disturbances secondary tomild interstitial keratitis that she had experienced earlyin the course of her disease. Her main complaints atthe time of testing were difficulty reading signs whilewalking and ambulating in poorly lit environments.

E.J. Hillman et al. / Dynamic visual acuity while walking 51

Table 1Summary of patient demographic and clinical information

Patient Age (yrs)/Sex Etiology Chief Complaint

1 38/F Cogan’s syndrome Hearing loss, Oscillopsia2 47/F Gentamycin toxicity Oscillopsia3 42/F Idiopathic Oscillopsia4 49/M Possible ototoxicity Hearing loss5 24/M Idiopathic Oscillopsia

Table 2Summary of patient VOR data

Patient Test frequency (Hz) Normal gain range Patient gain right Patient gain left

1 .0125 0.30–0.80 .01 .022 .08 .023 .01 .014 .01 .045 .02 .04

1 .05 0.35–0.90 .00 .052 .04 .033 .01 .014 .01 .015 .20 .20

1 .20 0.45–0.90 .19 .102 .34 .243 .14 .144 .07 .225 .12 .12

Patient 2 had a history of right lower limb traumain 1991 after being struck by a car. She subsequentlydeveloped osteomyolitis and was treated with gen-tamycin. During treatment she began to experience sig-nificant oscillopsia from which she currently suffers.She denied any history of hearing loss. She currentlyhas a leglength discrepancy, and her ankle is fused.She is able to ambulate short distances unassisted, butuses a straight cane while walking long distances or onuneven surfaces.

Patient 3 had a vestibular disorder of unknown etiol-ogy. She began to experience episodic vertigo on threeseparate occasions in 1975, 1 to 2 weeks apart, eachepisode lasting 3 to 4 days. These symptoms gradu-ally progressed to constant unsteadiness in the dark anddifficulty reading signs while walking. She denied anyhistory of hearing loss.

Patient 4 was treated for typhoid fever with unknownmedications at the age of 9 in Egypt. Since that time hehas complained of bilateral hearing loss, greater on theright. Superimposed on this stable hearing loss, he alsoreported a history of episodic, temporary deteriorationin his hearing associated with bilateral tinnitus. Theseepisodes last about 2 months; the last episode occurred18 months prior to testing. His only vestibular com-plaints were mild unsteadiness, primarily in the dark.He denied any vertigo or oscillopsia.

Patient 5 reported a history of episodic mild unsteadi-ness associated with “bobbing of his eyes” since child-hood. These episodes occurred every 3 to 4 monthsand lasted several minutes to an hour. In 1994 theseepisodes became more frequent and severe. Since thattime he has had constant oscillopsia and difficulty am-bulating in the dark. The etiology of these problems isunknown.

2.2. Experimental protocol

The test used a Macintosh Apple PowerbookTM 180and Microsoft Power PointTM slide presentation pro-gram. The actual test consisted of presentation of10 slides appearing on ghe computer screen. Eachslide presented a string of white numbers on a blackbackground at one particular font size (Fig. 1). Fontsizes ranged from 12-to 20-point font in increments of2 points. These sizes were chosen because at 2 metersthese fonts sizes correspond to a range of visual acuityof 20/16 to 20/27 on a traditional Snellen eye chart (Ta-ble 3). This range encompasses most subjects’ staticvisual acuity. Geneva font was chosen because of itsrelative simplicity and lack of elaborate number design.

One trial consisted of 10 slides, each slide presentinga string of 5 numerals at one font size, visible for 3 sec-onds. The 5 font sizes were presented pseudorandomly;


Table 3Angle subtended at 2.0 m viewing distance for each font size (Snellen letters for viewingdistance of 6.0 m, subtend angle of 5-min Arc

Geneva Pixel Letter height Angle at 2.0 m Angle at 2.0 m Snellen ratiofont size height (mm) (degrees) (min arc) 20/

12 9 2.97 0.085 5.10 19.514 11 3.63 0.103 6.23 18.116 13 4.29 0.122 7.37 20.418 14 4.62 0.132 7.93 24.920 15 4.95 0.141 8.50 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 of10 numbers per font size per trial. Subjects were given5 trials, for a total of 250 numerals presented undereach condition. Numerals were balanced among inte-gers from 0 to 9 such that each integer was presented anequal number of times. Stimuli were presented with aright-to-left transition, that is, the stimulus slide “slid”onto the screen from the right and “slid” off the screento the left. Total testing time averaged 10 minutes persubject.

The test was administered under two conditions: 1)standing and 2) treadmill walking. Normals and patient5 walked at 6.4 km/h on the treadmill. This speed waschosen to be consistent with that used in previous andongoing studies at JSC of head and gaze stability dur-ing treadmill locomotion after spaceflight. The otherpatients 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 walksafely at a maximum speed of 4.8 km/h. They weretested at that speed. Due to her orthopedic limitationpatient 2 needed to support herself with both index fin-gers on the support bar; she felt safe walking at a max-imum 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 onlywhile touching the safety bar with one index finger. Al-though use of this design precluded testing all subjectson the same protocol, patient safety was of paramountconcern, 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 MethodistHospital (TMH). Subjects walked on motorized tread-mills (QuintonTM Series Q55 at JSC and QuintonTM

Clubtrack at TMH), which provided comparable stim-uli. At JSC subjects wore a safety harness; at TMH sub-jects were spotted by test operators at all times. During


Fig. 2. Subject performing visual acuity test while walking on thetreadmill.

testing, the Powerbook was placed on a tripod at thesubject’s eye level at a distance of 2 meters as measuredfrom the screen to the outer canthus of the eye (Fig. 2).The angle between the keyboard and the screen wasmaintained at 90◦ and confirmed with a right angle.The brightness and contrast controls were adjusted formaximum brightness and contrast. Room lighting washeld constant during all testing.

The protocol was approved by the Baylor College ofMedicine Affiliated Review Board for Human Subjectsprior to administration of the test. All subjects signedan informed consent form prior to participating.

The study involved 4 phases: 1) Ten normal sub-jects were tested on both conditions at JSC. 2) To as-sess test-retest reliability, 5 of the original 10 normalsubjects were tested at JSC on a second occasion morethan one week after the original test, under identicalconditions. 3) To assess the effect of location on perfor-mance, with slightly different lighting conditions andtreadmill models, 4 of the original 10 normals (who hadnot participated in phase 2) were retested at TMH morethan one week after the original test. 4) Five patientswere tested at TMH.

Since the data consisted of repeated assessment of theperformance of two groups of subjects obtained at twoconditions, standing and walking, repeated measuresanalysis of variance (ANOVA) procedures for within-and between group independent variables were used.

This process necessitated the use of two statistical mod-els based on different assumptions [19]. A multivari-ate model was used when all independent variables foran analysis were within-group variables, that is, whennormal subject performance was analyzed. The result-ing probability values were adjusted for violation ofthe assumption of sphericity through the Greenhouse-Geiser and Huynh-Feldt methods. The appropriate ad-justed probability values are reported. A univariatemodel was used to compare the performance of nor-mals and patients when contrasts involved both within-and between-group independent variables, and the re-sulting probability values are not adjusted for violationof the assumption of sphericity. A significance level of0.05 was used throughout.

3. Results

3.1. Normal subject performance and test reliability

Subject performance was defined as the percentageof correct responses at each font size. Statistical anal-yses used the mean number correct at each font sizeas the dependent variable. Figure 3 shows the per-formance of all 10 normals, both while standing stilland while walking at 6.4 km/h. ANOVA indicatedno differences in performance with different font sizeswhile standing still, but while walking, performancedecreased significantly (F (1, 9) = 14.04, P = 0.005).This difference was due primarily to a significant decre-ment in performance at only the smallest font size(F (1, 36) = 47.65, P = 0.0001). No significant dif-ferences in performance were seen at any of the largerfont sizes.

Figure 4 shows the test-retest reliability. Overalltest-restest performance at JSC did not differ signif-icantly (F (1, 4) = 0.70, P = 0.45). When brokendown by font size, however, subjects performed signif-icantly 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 nor-mals tested at JSC and TMH. Overall performancedid not differ significantly between the two locations(F (1, 4) = 2.79, P = 0.19). When analyzed by fontsize, significant performance decrements were foundat font sizes 14 (F (1, 12) = 8.73, P = 0.01) and 12(F (1, 12) = 24.24, P = 0.004) while walking. Sub-ject performance was worse at these font sizes at TMH.


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

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

3.2. Patient performance

As described above, patients were tested at slightlydifferent conditions when walking. Figure 6 showsthe performance of individual patients while stand-ing and walking. Within-subjects analyses indicatedthat patients showed overall performance that was sig-nificantly worse while walking than when standing(F (1, 4) = 105.48, P = 0.0001).

When compared to normals, patients showed sig-nificantly poorer overall performance while standing(F (1, 4) = 85.03, P = 0.0001) and while walking(F (1, 4) = 394.28, P = 0.0001).

4. Discussion

The test described here is deceptively simple. Itmeets all of the complex requirements of a test suit-able for easy and flexible clinical and operational im-plementation, but it still provides a valid and reliablemeasure of functional visual acuity.

Normal subject performance revealed decrementsonly at the smallest font size, both while standing andwhile walking. This decrement probably representsthe DVA threshold for most subjects and, if smallerfont sizes had been used, performance curves similar tothose seen in patient testing would probably have beenseen, albeit shifted towards the smaller font sizes.


Fig. 5. Average performance of 4 normal subjects while (A) standing and (B) walking at 6.4 km/h tested at two different locations. Squaresrepresent 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 re-peated testing and testing location. The significant dif-ferences in performance at the smallest font sizes whilewalking may have been a result of slight differences inillumination between testing sites, however, the mag-nitude of the performance difference in absolute termsis relatively small. The differences seen in test-retestassessment suggest a potential training effect on onlythe most demanding part of the test. Given the smallsample size, these significant differences could alsorepresent a statistical phenomenon that might have dis-appeared given a larger sample. Importantly, from aclinical standpoint, however, overall performance didnot differ, and those differences found at the smallestfont sizes were small in magnitude compared to the

differences in performance seen among the patients.Therefore, when a patient or crewmember with clin-ically and functionally significant decreases in visualacuity is tested on two occasions or at two locations,the test will detect the degree of change accurately andreliably.

While standing, patients performed significantlyworse than normals, although they all reported nearnormal corrected static visual acuity. In contrast to thenormals, patients had significant decreases at all fontsizes while standing and while walking. The magni-tude of these differences reveals the inability of thesepatients to compensate for motion and maintain visualacuity while walking. These differences also suggestthat this test may be useful in quantifying the severity


of oscillopsia. However, additional data are needed toverify this suggestion.

Although the patients were tested under different dy-namic conditions, their performance curves are qual-itatively very similar both in absolute values and inshape. Despite these disparities, the patients differedsignificantly from normals, especially while walking.This difference will allow a physician who is evalu-ating a post-flight crew member or an LD patient toidentify deficits in DVA and possible related functionallimitations.

The maintenance of visual stability during locomo-tion is a complex task requiring not only precise inter-action between the visual and vestibular systems butalso coordination between the head and trunk to main-tain head stability during walking. A breakdown in anyof these systems can lead to the loss of visual stability.Head-trunk coordination is impaired in patients withvestibular dysfunction, resulting in decreased head sta-bility during locomotion [12,20]. Similarly, after spaceflight astronauts exhibit comparsble changes in the effi-cacy of head movement control during locomotion [7].More recently an abbreviated version of the DVA pro-tocol described here, also using a treadmill walkingparadigm, has been used to test crew following severalmonths in space. Preliminary data indicate decreasedDVA shortly after landing, as compared to pre-flighttests (Bloomberg and colleagues, unpublished data).

The stability of the visual world during movement isimportant in the successful performance of a numberof motion-intense activities, including sports, driving acar, or flying an aircraft [21–23]. Patients with vestibu-lar deficits have difficulties performing these kinds ofactivities [24]. Given the similarities between this pop-ulation and astronauts returning from spaceflight, it ispossible that astronauts would also experience diffi-culty performing some of these same activities. An ob-jective, reliable test of DVA while walking might pro-vide a useful predictor of performance on some activi-ties that require good DVA.

This test of dynamic visual acuity while walking pro-vides a valid, reliable, and sensitive method of eval-uating the functional effects of dynamic visual acuityin patients with bilateral vestibular dysfunction. It candetect signs of vestibular impairment and has the po-tential to provide a quantitative measure of oscillopsia,which to data has existed as an otherwise unmeasure-able subjective symptom.Therefore, it may be usefulfor following the progress of patients’ oscillopsia aswell as for evaluation of post-flight crewmembers.

Acknowledgments

The functional visual acuity test used in this reportwas first conceived by Gary Riccio, Ph.D., NascentTechnologies. We also wish to acknowledge Dr. Ric-cio’s substantial contributions to improving a prototypeversion of this test. Dick Calkins, Ph.D., Wyle LifeSciences, assisted with the statistical analyses; mem-bers of the Neuroscience Human Movement and Coor-dination Research Group at JSC assisted with subjecttesting; and the staff of the Methodist Hospital CardiacRehabilitation Laboratory provided the treadmill. Ed-ward Hillman was supported in part by a Visiting Sci-entist research grant from Universities Space ResearchAssociation, Division of Space Life Sciences. HelenCohen was supported by the Clayton Foundation forResearch and NIDCD 5R29DCO2412-02.

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Vestibular Dysfunction and Dynamic Visual Acuity during Treadmill Locomotion

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