RESEARCH ARTICLE Stroboscopic Vision as a Treatment for Motion Sickness: Strobe Lighting vs. Shutter Glasses Millard F. Reschke, Jeffrey T. Somers, and George Ford RESCHKE MF, SOMERS JT, FORD G. Stroboscopic vision as a treatment for motion sickness: strobe lighting vs. shutter glasses. Aviat Space Environ Med 2006; 77:2–7. Introduction: Countermeasures (e.g., drugs, training, etc.) designed to combat the problem of space motion sickness (SMS) have had only limited successes. A possible solution for SMS and terrestrial motion sickness may rest in preventing retinal slip via stroboscopic vision. Methods: There were 32 subjects who participated in a study to investigate the effect of stroboscopic illumination on motion sickness using either a strobe light or liquid crystal display (LCD) shutter glasses. There were 19 subjects who read text and made ⫾ 20° head movements in the horizontal plane (yaw) at 0.2 Hz while wearing left-right reversing prisms and exposed to 4-Hz stroboscopic or normal room illumination (control condition). Motion sickness was scored using the Miller and Graybiel scale and subjective self-ratings. In a crossover design, testing was repeated using stroboscopic LCD shutter glasses with an additional 13 subjects and 6 subjects from the first condition. Results: During the experiment with a strobe light, motion sickness scores were significantly lower than in the control condition (␹ 0.32 strobe vs. ␹ 3.79 light ⫽ p ⬍ 0.003). Results with the LCD shutter glasses corresponded with those when the environment was strobed in an otherwise dark room (␹ 1.0 glasses vs. ␹ 4.1 light ⫽ p ⬍ 0.001). Conclusions: Stroboscopic illumination reduced the severity of motion sickness symptoms, and shutter glasses with a flash frequency of 4 Hz are as effective as a strobe light. Stroboscopic illumination appears to be an effective countermeasure where retinal slip is a significant factor in eliciting motion sickness due to either self- or surround-motion. Keywords: ocular motility, spaceflight, visual acuity, retinal slip. gree of autonomic discomfort, and symptoms of motion sickness may last 14 d or longer (9). Countermeasures designed to combat the problem of SMS have had only limited success, and those that are being used today are not designed to prevent the first occurrence of SMS. At best, primarily because of their substantial side effects and operational considerations, the available drugs are typically administered only after a crewmember has become ill. Clearly other countermeasures for SMS must be developed. About 25 yr ago, Geoffrey Melvill-Jones first studied adaptation of the vestibulo-ocular reflex (VOR) by having subjects view the surrounding world through leftright prisms to optically reverse their vision during Delivered by Ingenta to: in the horizontal plane (5). His protocol head rotations Johnson Space Centrehorizontal eye movements induced by oscilcompared lation of the head and body under the following conIP : 139.169.159.190 ditions: 1) in the dark; 2) in normal light; 3) with stroThu, 18 May 2006 19:42:30 boscopic illumination to prevent retinal slip; 4) while wearing left-right reversing prisms; and 5) with stroboscopic illumination while wearing left-right reversing prisms. Not surprisingly, most subjects experienced motion sickness while wearing the optically reversing prisms. A serendipitous finding that emerged during this research was that the same subjects did not have motion sickness symptoms when wearing the reversing S THE INTERIOR volume of spacecraft and the prisms under stroboscopic illumination (5). The mechmobility of their inhabitants have increased, the anism by which this effect occurred is not clearly unincidence of space motion sickness (SMS) has increased derstood. However, the observation that no motion as well. Exposure to provocative real or apparent mosickness was ever noted suggested it might be possible tion leads to the progressive cardinal symptoms of terto produce functionally useful adaptation during spacerestrial motion sickness, which typically include pallor, flight without the penalty of disabling motion sickness increased body warmth, cold sweating, dizziness, by using an appropriate stroboscopic environment to drowsiness, nausea, and vomiting. The signs and sympcontrol the rate of adaptation. Melvill-Jones’ hypothetoms of SMS, when considered with the time course of sis, though intriguing, lay dormant partly because imsymptom development and the movements encounplementation of a strobe-lit environment did not seem tered on exposure to microgravity, suggest that sickness feasible for spaceflight. experienced during spaceflight is similar to terrestrial Recently we reported the postflight gaze responses of motion sickness. Both astronauts and cosmonauts have also reported From the Neurosciences Laboratories, NASA Johnson Space Center the development of motion sickness symptoms on re(M. Reschke), and Wyle Laboratories (J. T. Somers, G. Ford), Houston, turning to Earth (2,6). Postflight sickness has become TX. relatively common in the space shuttle program, where This manuscript was received for review in August 2005. It was accepted for publication in October 2005. its incidence is estimated to average between 60 to 70% Address reprint requests to: Dr. Millard Reschke, 2101 NASA Parkacross all flyers (8). The Russian space program estiway (SK272), Houston, TX 77058; millard.f.reschke@nasa.gov. mate for long-duration flyers is even higher. ApproxiReprint & Copyright © by Aerospace Medical Association, Alexandria, VA. mately 92% of their cosmonauts experience some de- A 2 Aviation, Space, and Environmental Medicine • Vol. 77, No. 1 • January 2006 PREVENTION OF MOTION SICKNESS—RESCHKE ET AL. a long-term resident of the Mir space station (10). We cruited 13 additional subjects (8 men, 5 women, ages observed disruption of this astronaut’s steady fixation 26 – 48, mean 36.4 yr). No subjects were taking medicaby frequent, small saccadic intrusions—square-wave tion with effects on the nervous system, and all were jerks (SWJs). Before flight, the frequency of SWJs (conscreened for a history of epilepsy. Subjects either were fined mainly to the horizontal plane) was more than emmetropes or wore their contact lens corrections dur0.45
s⫺1, about 2 times greater than that observed in ing testing. The study protocol was approved in adthe normal population. After landing, SWJ frequency vance by the Johnson Space Center’s Committee for the increased to 0.91
s⫺1, a change of more than 100%. This Protection of Human Subjects, and each subject procrewmember appeared to be unaware of his or her vided written informed consent before participating. SWJs, and when questioned about them during a postflight debrief was surprised that these eye movements Equipment were present. Despite the intrusion of frequent SWJs, During phase 1, the strobe illumination was provided the astronaut’s dynamic visual function (reading ranby a Monarch Instrument strobe light (model Nova domized lines of optotypes while walking) remained Strobe PB, Amherst, NH). The strobe ‘on’ time of 30 ␮s unchanged from the preflight value, unlike that of all (brief enough to prevent retinal slip) and frequency of 4 other astronauts studied after long-duration flights. AlHz were similar to those used by Melvill-Jones and though this astronaut did suffer the common postflight Mandl (5), although the flash duration was of a magnisyndrome of motion sickness symptoms (mal de débartude longer. In phase 2 of testing, a pair of LCD shutter quement), the symptoms abated rapidly and did not glasses developed in house was used to provide the seem to be related to the length of his or her flight. stroboscopic illumination of the visual surround. The The observation that this astronaut’s postflight dyflash rate was again set to 4 Hz, but the flash duration namic visual function was better than that of most was set to 10 ms because of limitations of the liquid long-duration flyers suggested to us that the frequent crystals. During motion sickness testing, subjects wore SWJs may have been beneficial. How could these small, dove, left-right reversing prisms that inverted the vito-and-fro saccades improve this astronaut’s ability to sual scene in the horizontal plane (that is, left and right recognize optotypes while walking on a treadmill? views were reversed). These prisms were also develMost astronauts show some impairment of dynamic oped in house. They were mounted on a headband visual function during treadmill walking after landing. within commercially available chemical safety goggles This has been attributed to changes in the VOR (1). that limited Normally, visual fixation supplements the VOR, butby Ingenta Delivered to:peripheral vision. The visual contributes less during high-frequency head perturbaJohnson Space Centre field that was used to provide the primary source of visual-vestibular conflict was placed 1 m from tions. However, in the wake of a saccade, visual follow: 139.169.159.190 the subjects’ eyes (frontal plane) and centered on the ing mechanisms are enhanced, and it hasIP been sug18 May line 19:42:30 of sight (horizon). The target itself consisted of a gested that this constitutes a fixationThu, mechanism to 2006 short passage from “Treasure Island.” The size of the stabilize gaze immediately after a rapid head motion letters was equivalent to a font (Arial) size of 125 pt, and (3). Such a mechanism might also transiently improve subtended an average visual angle of approximately 1°. gaze stability (reduce retinal slip) during locomotion, A chin rest was used for goggle fitting and adjusting the allowing momentary clear vision of the test optotypes. prisms for different interpupillary differences. We were struck by certain similarities between the improved postflight vision performance of the astronaut who had frequent SWJs, the observation that retProcedures inal slip is known to induce motion sickness (as when Two studies, identified as phase 1 and 2, had identinew eyeglasses that change the gain of the vestibulocal testing protocols except for the source of the stroboocular reflex are worn), and the performance of Melvillscopic environment. Prior to the beginning of the exJones’s subjects under stroboscopic illumination. Thereperimental procedure, the dove prisms were adjusted fore, we have tested the hypothesis that short flash with the subject’s head fixed by the chin rest, such that durations of stroboscopic illumination (flash rates bethe visual target was fused and viewed as a single tween 4 and 8 Hz) provide protection against motion merged object. While wearing the left-right reversing sickness. We have also tested the hypothesis that the prisms, subjects were required to read the passage of same protection against retinal slip and motion sickness text taken from “Treasure Island.” For 30 min, subjects will occur when liquid crystal display (LCD) glasses attempted to read the text presented in front of them constructed to strobe the environment are worn. while moving their head ⫾ 20° in the yaw plane (small pitch head movements were required to read the text METHODS from the top of the chart to the bottom) to a tone modulated at 0.2 Hz. The amplitude of the head moveSubjects ment was closely monitored. Each subject was tested one time under each of the During phase 1 of testing, we studied 19 non-astrotwo experimental conditions, and each test was sepanaut subjects (11 men, 8 women, ages 24 – 46). During rated by a minimum of at least 1 wk to prevent adapphase 2, we retested 6 of the original subjects (4 men tation to the provocative stimulus from carrying over and 2 women, ages 25– 47, mean 35 yr), all of whom from session to session. Subjects were randomly aspresented with symptoms when tested without strobosigned at the beginning of the test to a specific illumiscopic illumination during the phase 1 study, and reAviation, Space, and Environmental Medicine • Vol. 77, No. 1 • January 2006 3 PREVENTION OF MOTION SICKNESS—RESCHKE ET AL. Fig. 1. Comparison of motion sickness scores during phase 1. Motion sickness scores were obtained from subjects wearing left-right reversing prisms and exposed to either normal room illumination or stroboscopic illumination in an otherwise dark room. nation condition: strobe illumination or regular room Data Analysis and Hypothesis Testing illumination. Using a simple crossover design, the sub-by Ingenta to: Delivered All motion sickness test scores were compiled for ject then performed the test under the opposite condi-Space Centre Johnson each test condition. We used the final modified Miller tion on the subsequent test day. and Graybiel score attained, final subjective score atIP : 139.169.159.190 Motion sickness was scored using a modified Miller tained, and time tolerated as our dependent measures. Thu,to18include May 2006 19:42:30 and Graybiel scale (7) that we constructed A non-parametric Friedman two-way ANOVA for resymptoms that might be elicited when reversing prisms peated measures with a significance level of p ⬍ 0.05 are worn. On this scale, a score of 5 to 7 represented was used for all statistical inference. moderate malaise (MIIa) and a score of 8 or above was approaching frank sickness. The subjects were also RESULTS asked to rate their overall subjective feeling on a scale Phase 1: Strobe Illumination from 1 to 20, where typically a score below 10 is taken to indicate minor motion sickness, while 10 and above The results for the condition where stroboscopic illugenerally suggests that the subject is clearly motion mination was used as the independent variable are sick. presented in Fig. 1. Please note that the data in Fig. 1 Before testing began, subjects were given a list of were rank ordered on the motion sickness scores obpossible motion sickness symptoms and a briefing on tained in normal room illumination such that the lowest the development of motion sickness and symptom scores progress to the highest scores. Motion sickness strength during the test. At this time any questions scores recorded using the modified Miller and Graybiel they had about the test or symptoms were answered. scale were significantly lower in the strobe-illuminated Then, before beginning and every 5 min during testenvironment (see Table I for the p-values of each test ing, subjects were asked if they were experiencing performed). With the strobe illumination, 13 out of 19 any of the motion sickness symptoms described. Subsubjects had lower motion sickness scores than with jects were also monitored by the test conductor for normal room illumination, and 5 subjects had no sympthose symptoms for which they were either unable to toms in either test. The remaining subject reported miobserve or unable to establish severity (e.g., pallor, nor symptoms during the stroboscopic treatment and in sweating, reduced head motion, etc). Testing was normal lighting. In normal room lighting, 9 of the 19 limited to 30 min unless the subject wished to stop subjects had a motion sickness score at or above the sooner or the subject’s motion sickness score was MIIa level (i.e., a minimum score of 5) on the motion MIIa or higher, at which time the test was terminated. sickness rating scale. The highest score was 11, and the For Phase 2, the shutter glasses were set to flashing to mean score was 3.79. As illustrated in Fig. 1, when simulate the strobe condition, or were worn but left strobe lighting was employed only four subjects had a turned off (LCDs were clear) to simulate the normal positive score and the highest score recorded was 2 illumination condition. with a mean of 0.32. 4 Aviation, Space, and Environmental Medicine • Vol. 77, No. 1 • January 2006 PREVENTION OF MOTION SICKNESS—RESCHKE ET AL. TABLE I. STATISTICAL COMPARISONS AND ASSOCIATED pVALUES. p-value Test n MG SS TT Strobe vs. No Strobe Goggle Flash vs. No Goggle Flash Strobe vs. Goggle Flash No Strobe vs. No Goggle Flash 19 19 6 6 0.001* 0.020* 0.180 0.414 0.012* 0.012* 0.654 0.102 0.003* ⬍ 0.001* 1.000 0.180 * ⫽ significance values of p ⬍ 0.05. MG ⫽ Miller and Graybiel scoring method; SS ⫽ subjective scoring method; TT ⫽ time to test termination. Scores using the subjective rating scale that was employed by the subjects were consistent with the Miller and Graybiel scale. That is, self-rating showed that the reported motion sickness was significantly lower in the strobe-illuminated environment (see Table I for the pvalues of each test performed). With the strobe illumination, 13 out of 19 subjects had lower motion sickness scores than with normal room illumination, 4 subjects had no symptoms in either test, and 2 subjects had a slightly higher score with the strobe than with normal room illumination. In normal room lighting, the highest score was 15 (two subjects), and the mean score was 5.92. With strobe lighting only 10 subjects had a score above 1, and the highest score was 8 with a mean of 2.34. with the glasses flashing than with the glasses clear. As in presentation of the data for phase 1, the data for phase 2 shown in Fig. 2 were rank ordered on the motion sickness scores obtained in normal room illumination such that the lowest scores progress to the highest scores. With the glasses flashing, 13 out of 19 subjects had lower motion sickness scores than when the glasses were clear, 3 subjects had no symptoms in either test, 1 subject had the same score for both tests, and 2 subjects had slightly higher scores with the glasses flashing than without. With the glasses clear (not strobing), 11 of the 19 subjects had a motion sickness score at or above the MIIa level (minimum score ⫽ 5) on the Miller and Graybiel scale. The highest score was 9, and the mean score was 4.1. With the glasses flashing, nine subjects had a positive score, and the highest score was 4 with a mean of 1.0. When the subjects rated their own sickness level, motion sickness scores were significantly lower with the glasses flashing than with the glasses clear. With the glasses flashing, 13 out of 19 subjects had lower motion sickness scores than with the glasses clear, 3 subjects had no symptoms in either test, and 3 subjects had slightly higher scores with the glasses flashing than without. With the glasses clear, the highest score was 17, and the mean score was 6.58. With the glasses flashing, 10 subjects had a score above 1, and the highest score was 11 with a mean of 2.68. Delivered by Ingenta to: Tolerance Time Johnson Space Centre Results when using the LCD shutter glasses, preThe time that subjects endured the motion sickness IP : 139.169.159.190 sented in Fig. 2, corresponded to those under strobostressor was clearly limited by the criterion restricting Thu,and 18 GrayMay 2006 19:42:30 scopic room illumination. That is, the Miller test duration to 30 min. However, even with this limiPhase 2: LCD Shutter Glasses biel motion sickness scores were significantly lower tation there were significant differences between strob- Fig. 2. Comparison of motion sickness scores during phase 2. Motion sickness scores were obtained from subjects who were wearing left-right reversing prisms and were exposed to either normal room illumination or stroboscopic illumination provided by a set of LCD goggles. Aviation, Space, and Environmental Medicine • Vol. 77, No. 1 • January 2006 5 PREVENTION OF MOTION SICKNESS—RESCHKE ET AL. Fig. 3. Comparison of motion sickness scores across phase 1 and phase 2. Scores were obtained from six subjects who participated in both the phase 1 and phase 2 testing. ing and normal room illumination. Under stroboscopic would have a similar score in phase 2 testing. The same room illumination (phase 1) tolerance times (i.e., time to finding was also true for tolerance times. When the Delivered to:countermeasure was applied, all 6 subjects test termination) were significantly longer than underby Ingenta stroboscopic normal room illumination (see Table I for the p-values were able Johnson Space Centreto go the full 30 min. of each test performed). Out of 19 subjects, 8 tolerated IP : 139.169.159.190 the visual conflict during strobe illumination longer Miller and Graybiel Scores vs. Subjective Rating Scores 18 May than in normal room illumination, andThu, 11 subjects tol- 2006 19:42:30 Although it was not a critical aspect of this investierated both for the full 30 min. Under normal room gation, it was interesting to observe the relationship illumination, the mean tolerance time was 23.9 min. between the motion sickness scores derived by the With strobe lighting, all 19 subjects went the full 30 min. Miller and Graybiel method (7) and the scores reported When the stroboscopic environment was provided with when the subjects rated their own well-being. While the LCD glasses (phase 2), similar tolerance times were related [r (2) ⫽ 0.68], the two scales are not a linear observed when compared with stroboscopic room illumifunction. Instead, there appeared to be an exponential nation. Out of 19 subjects, 11 tolerated the visual conflict relationship where the self-rating tended to accelerate with the glasses flashing longer than with the glasses relative to the Miller and Graybiel scoring method. That clear, and 8 subjects tolerated both for the full 30 min. is, once the subjective scores reached a value of approxWith the glasses clear, the mean tolerance time was 23.9 imately 10 on the subjective scale, symptoms would min. With strobe lighting, all 19 subjects went the full 30 accumulate at an increased rate, whereas the Miller and min. Statistically, there was no difference between phase 1 Graybiel scale remained linear, as it was designed to do. and phase 2 in terms of tolerance times. Phase 1 and Phase 2 with Repeat Subjects DISCUSSION By using a small repeat subject population (six subjects) in both the phase 1 and phase 2 testing, it was possible to determine that there was no difference between the stroboscopic conditions when significance was tested across the subjects that participated in both phases of the investigation. Random assignment to the original start group in either phase 1 or phase 2 (strobe, glasses, or normal room illumination), in addition to the delay imposed between testing, controlled for adaptation across treatment. The data showing individual scores for each subject in each condition are presented in Fig. 3. It can be seen in Fig. 3 that if a subject had motion sickness symptoms in phase 1, that same subject The results of this study clearly showed that motion sickness evoked under conditions of visual-vestibular conflict is mitigated through the use of a stroboscopic countermeasure. These results compare nicely with those obtained by Melvill-Jones and Mandl (5), who observed no motion sickness under stroboscopic room illumination when their subjects wore left-right reversing prisms and made low-frequency head movements. However, unlike the initial studies of Gonshor and Melvill-Jones (4), which reported no motion sickness under stroboscopic illumination, our data suggest that stroboscopic illumination during image reversal does allow for the development of some minor symptoms. 6 Aviation, Space, and Environmental Medicine • Vol. 77, No. 1 • January 2006 PREVENTION OF MOTION SICKNESS—RESCHKE ET AL. Differences in protocols between the earlier studies and visual-vestibular conflict as it is associated with motion sickness. ours could account for this disparity. First, the differThere is no evidence that stroboscopic presentation of ence may be attributable to how the symptoms of mothe visual surround will have any effect on motion sicktion sickness were reported. There is no indication that ness that is associated with canal-otolith cross coupling, Gonshor and Melvill-Jones (4) nor Melvill-Jones and nor have the glasses been evaluated in gravitational enviMandl (5) systematically tracked or recorded subsets of ronments different than what is typically available on specific symptoms during their investigations. In these Earth. Future plans include testing the stroboscopic two early papers, nausea was the primary symptom glasses during the microgravity phase of parabolic flight reported when subjects were exposed to reversed vision and on rotating platforms with the ultimate goal of using without stroboscopic illumination. Since our study was these glasses as a protection against some forms of terresdesigned to look specifically at motion sickness (rather trial and space motion sickness. Some success with car than a post hoc evaluation), we tracked even minor (approximately 12 individuals with 100% efficacy) and symptoms that may have been overlooked in the earlier seasickness (1 person) have already been anecdotally reinvestigations. Second, a contributing factor to this difported. Formal testing at sea is currently being scheduled ference in the reporting symptoms may have been as a part of on-the-surface activity associated with driven by the duration of exposure to the reversing NASA’s Extreme Environment Mission Operations prisms. The earlier investigations typically exposed project. It is also our intention to test the viability of the subjects to either hours or days of vision reversal rather stroboscopic glasses on select patient populations. In parthan the 30 min used in this study. Symptoms leading ticular, it is believed that a stroboscopic presentation of the up to nausea were likely not recorded when a definitive environment may be particularly effective in those paend point like nausea was available. Thus, the lack of tients who have difficulty with visual streaming during nausea during vision reversal under stroboscopic illuhead turns and locomotion. mination in the earlier studies would have indicated no motion sickness. ACKNOWLEDGMENTS Of particular importance in the current investigation We thank Drs. Jane Krauhs and Scott Wood for their technical is the observation that there was no significant differediting assistance, and Dr. Deborah Harm for her assistance with the ence between whole room stroboscopic illumination statistical analysis of our results. We would also like to acknowledge and the LCD goggles. For the prevention of motion the published work of Professor Melvill-Jones as inspiration for developing a technique for the treatment of space motion sickness. This sickness induced as a result of visual-vestibular conflict, research wasto: supported by a grant from the Johnson Space Center’s the important parameter appears to be Delivered stroboscopicby Ingenta Director’s Discretionary Fund, and NASA Grant 111–10 –10 –73A. Johnson Space Centre illumination. While it is not feasible to stroboscopically illuminate the entire environment outside ofIP controlled : 139.169.159.190 REFERENCES conditions, it is possible to use glasses that act as elec1. Bloomberg JJ, Mulavara AP. Changes in walking strategies after Thu, 18 May 2006 19:42:30 tronic shutters to provide the appropriate stroboscopic spaceflight. IEEE Eng Med Biol Mag 2003; 22:58 – 62. illumination of the visual surround. 2. Bryanov IL, Gorgiladze GI, Kornilova LN. Vestibular function. In: Gazenko OG, ed. 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