RESEARCH ARTICLE
Visual Blur and Motion Sickness in an Optokinetic Drum Frederick Bonato; Andrea Bubka; William Thornton
BACKGROUND:
METHODS:
RESULTS:
CONCLUSIONS:
KEYWORDS:
The most commonly cited hypotheses for motion sickness (MS) focus on inconsistent sensory inputs. Visual/vestibular conflicts may lead to MS, but visual input from retinal regions/neural pathways that are sensitive to motion might bear more weight in MS etiology. We hypothesized in an optokinetic drum would attenuate the Delivered by Ingentathat to:inducing Simon blurred Fraservision University influence of foveal (parvocellular) input, butOn: not peripheral (magnocellular) input that is sensitive to motion. Increased IP: 185.71.3.84 Fri, 29 Jul 2016 20:31:14 Copyright: Aerospace Medical Association relative influence of peripheral visual input was predicted to subsequently lead to more visual/vestibular conflict and subsequently more severe MS symptoms. Through goggles that were either clear or frosted, 15 subjects (5 men, 10 women, mean age 5 24.9 yr, range 5 18-49) viewed the interior of a rotating (60° · s21) optokinetic drum for 10 min. Subjects completed the Simulator Sickness Questionnaire (SSQ) before and after viewing. Overall subjective sickness ratings (0-10) and visually induced self-motion perception (vection) ratings (0-10) were also recorded. Postexposure SSQ scores obtained in the blur condition (total - 52.9, oculomotor - 38.9, disorientation - 69.6) were significantly higher than those obtained in the control condition (total - 30.4, oculomotor - 21.7, disorientation - 37.8). Overall sickness ratings and vection ratings were also significantly higher in the blur condition. These results suggest that visual blur can exacerbate MS, perhaps because of differential influences of visual pathways. Although these results were obtained with an optokinetic drum, possible effects of visual blurring in motion provocative environments such aircraft, watercraft, spacecraft, and land vehicles should be considered. sensory conflict, vision, vestibular, vection. Bonato F, Bubka A, Thornton W. Visual blur and motion sickness in an optokinetic drum. Aerosp Med Hum Perform. 2015; 86(5):440–444.
T
he best known theories of motion sickness (MS) are based on sensory conflict.17 These theories assert that when afferent signals regarding self-motion are not consistent, MS can result. Such inconsistencies often involve the visual and vestibular systems. Hence, the navigator of an aircraft, who looks mostly at instruments, may be more susceptible to MS than the pilot who often receives consistent visual and vestibular inputs regarding self-motion. Sensory conflict does not require actual self-motion relative to Earth. Visual input alone such as that which can occur in a flight simulator can lead to compelling self-motion perception that is entirely visually induced. This phenomenon, known as vection,3,23 is associated with simulator sickness.8 Even if one accepts sensory conflict as a possible cause of MS, the explanation is incomplete. The question about “why” sensory conflict should lead to MS needs to be addressed. Some investigators and theorists have proposed that MS is part of our genetic endowment and the product of evolution.6,13,14 A large survey study of monozygotic and dizygotic twins yielded 440
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results suggesting a strong and significant genetic contribution to MS susceptibility.18 One set of theories asserts that sensory conflict can ‘trick’ the brain into reacting as if poisoning has occurred.15,22 Such theories treat MS as a mistakenly engaged mechanism aimed at eliminating toxins from the body. Another explanation for MS is that sensory conflict both within a sense (vestibular) and between senses (visual/vestibular) can falsely trigger a protective mechanism aimed at inhibiting mobility during
From Montclair State University, Montclair, NJ; Saint Peter’s University, Jersey City, NJ; and Houston, TX. This manuscript was received for review in July 2014. It was accepted for publication in February 2015. Peer review and editorial oversight for this article were conducted by Sarah A. Nunneley, M.D., M.S., former Editor of this journal. Address correspondence to: Frederick Bonato, Ph.D., Montclair State University, 1 Normal Ave., Montclair, NJ 07043; [email protected]. Reprint & Copyright © by the Aerospace Medical Association, Alexandria, VA. DOI: 10.3357/AMHP.4105.2015
May 2015
VISUAL BLUR & MS SYMPTOMS—Bonato et al.
a time when vestibular damage or malfunction has occurred.21 2 h before each trial. The Saint Peter’s University InstituSuch a protective mechanism would offer a survival advantage tional Review Board approved the study in advance. Each subfor our ancient ancestors in that a low level of activity would be ject provided written informed consent before participating in less likely to attract predators during a time when the ability to the study. spatially orient is compromised by vestibular malfunction. Equipment and Materials The human visual system has also evolved in ways that may The optokinetic drum consisted of a synthetic composite cylhave helped enhance our ancestors’ survivability. Central, or foveal, vision largely involves a visual pathway from retina to inder 122 cm in height and 107 cm in diameter. The cylinder was mounted in a sturdy wooden frame, yielding a drum that brain that is high resolution in nature. Packed with some six million cones, visual acuity is sharpest for images that fall on or close was completely rigid. The drum was suspended from a motor to the fovea. This parvocellular pathway is also color sensitive attached to a beam directly above the drum with four steel and, hence, when we want to identify something in our environ- cables. Given the mass of the drum, and the position of the ment we naturally look directly at it, using color and visual details cables supporting it, this method of suspending the drum resulted in a smooth and steady rotation, free of any wobble or to aid identification.11,12 Peripheral vision facilitated by rods is color-blind and is not able to process fine details. Hence, periph- sway after approximately 2 s of rotation. Head position was eral vision that is facilitated by the magnocellular pathway is not maintained throughout the experiment by means of an optical as useful for identifying objects. This pathway, however, is sensi- chin rest in which the subject’s chin rested in a stationary contive to motion that is detected by shifting patterns of light on the cave depression while the subject’s forehead rested against a curved metal bar. Viewing took place with the subject’s head retina. It is good for detecting moving objects—that for our centered at the axis of rotation. This resulted in a viewing disancient ancestors may have been predator or prey—but also bythrough Ingentathe to: Simon tanceFraser of 48.5 University cm when the subject’s line of sight was perpenhelps to provide information aboutDelivered self-motion IP: 185.71.3.84 On: Fri, 29 Jul 4,5 dicular2016 to the20:31:14 drum’s surface. Horizontally positioned baffles environment via optical flow patterns on the retina. It is imporCopyright: Aerospace Medical Association attached to the top and bottom of the chin rest restricted the tant to note that several investigators have reported results that suggest visually induced self-motion perception, or vection, is subject’s view so that the only surface seen through the baffles was the drum’s interior. Illumination was provided by two largely mediated by peripheral stimulation. Vection is also some32-W florescent bulbs positioned directly behind a translutimes accompanied by MS symptoms.8 It has been claimed that visual acuity is correlated with MS cent plastic diffuser panel and 102 cm directly above the top in an optokinetic drum.24,25 It has been suggested that this cor- of the drum. The stimulus pattern that lined the interior of the drum consisted of a black and a white checkerboard patrelation is possibly due to eye movements that, in turn, influtern. Each patch was 9° wide and 30° wide. The black and ence motion sickness, or the detection of foveal image slip which somehow influences MS. Webb reported24 that present- white stripes had luminance values of 1.6 and 36.0 cd · m22, respectively. ing blurred stripes in an optokinetic drum also exacerbated MS Viewing took place through a pair of goggles with a transcompared to sharply printed ones. For the current study, we artificially blurred the visual field using a frosted optical filter. parent plastic front. The front of the goggles was either left clear and unobstructed (control condition) or a frosted aceSuch a manipulation creates a degraded image that leads to less meaningful input to the parvocellular pathway. It could be pre- tate filter was adhered to the surface, creating a “blurred” view dicted that blurring the image would not adversely affect the of the drum’s interior (blur condition). The filter used (Rosculux #114: Hamburg Frost) was obtained from Roscolux Labomotion sensitive magnocellular system. The brain receiving inputs from these two pathways could weight them differently ratories (Stamford, CT). Digital photographs of the drums because of blurring—the motion sensitive magnocellular input interior taken with and without the frosted filter are shown in being given more weight compared to the parvocellular input Fig. 1. Motion sickness symptoms were assessed using the Simulathat is differentially affected by visual ‘noise.’ In light of this pretor Sickness Questionnaire (SSQ).10 The SSQ is a well-accepted dicted differential weighting of neural inputs, it was hypotheassessment instrument that has been used for various forms of sized that artificially blurring the scene would lead to more MS, including MS that is visually induced. When scored accordsevere MS symptoms in addition to more salient vection. ing to published guidelines,9 the SSQ yields four scores: a total SSQ score and three subscores corresponding to nausea, oculomotor effects, and disorientation. There are 16 items on the METHODS questionnaire (general discomfort, fatigue, headache, eye strain, difficulty focusing, increased salivation, sweating, nausea, diffiSubjects Voluntarily participating in the experiment were 15 Saint Peter’s culty concentrating, fullness of the head, blurred vision, dizziness University undergraduate students and staff members (5 men, with eyes open, dizziness with eyes closed, vertigo, stomach awareness, and burping) that contribute to the SSQ scores. Sub10 women). The mean age of subjects was 29.9 yr and ranged jects indicate the level at which each symptom is experienced from 18 to 49. Persons reporting any visual, vestibular, neurological, gastrointestinal abnormality, or any other health prob- both pre-treatment and post-treatment by circling one of four choices (none, slight, moderate, or severe). lem were not allowed to participate. Subjects fasted for at least AEROSPACE MEDICINE AND HUMAN PERFORMANCE Vol. 86, No. 5
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weighting factors outlined in Kennedy et al.9: a total SSQ score and three subscores for nausea, oculomotor symptoms, and disorientation (see Fig. 2). No main effects of Order were revealed. A two-way ANOVA revealed a significant main effect of condition for total SSQ scores [F(1,13) 5 5.18, P 5 0.040] and significantly higher subscores for oculomotor symptoms [F(1, 13) 5 5.77, P 5 0.032] and disorientation Fig. 1. Optokinetic drum interior viewed with A) clear lenses and B) through a frosted acetate filter (Rosculux #114: [F(1, 13) 5 4.76, P 5 0.048] in Hamburg Frost). the Blur condition. Mean (0-10) Overall Sickness ratings obtained Procedure and Design The subject was given instructions regarding the SSQ before in the Blur condition (3.9) were also significantly higher [F(1, 13) 5 5.17, P 5 0.041] than those obtained in the Control proceeding to fill out the pre-treatment page of the SSQ form. The subject was then positioned inside the optokinetic drum, condition (2.9). No interaction effects between Order and Condition were revealed. Three subjects reported ‘slight’ nausea and fitted with the goggles, and asked to keep his or her head staby instructed Ingenta to: Simon Fraser‘moderate University one reported ’ nausea in the control condition. In tionary by using an optical chin rest. ThDelivered e subject was IP: 185.71.3.84 On: Fri, 29 Jul 2016 20:31:14 to close his/her eyes until the experimenter gave instructions the Blur condition, two subjects reported slight nausea and Copyright: Aerospace Medical Association to open them, marking the beginning of the trial. The subject four reported moderate nausea. Mean (0-10) Overall Vection ratings obtained in the Blur condition (8.4) were signifiwas also told to keep his/her head still while watching the cantly higher [F(1,13) 5 4.77, P 5 0.049] than those obtained interior surface of the rotating (60° · s21) drum. After 10 min of viewing, the subject was instructed to close his/her eyes, the in the Control condition (6.9). drum was raised, and the subject was immediately given the post-treatment portion of the SSQ form to complete. After DISCUSSION completing the SSQ a 0-10 Overall Sickness rating was obtained for the entire trial (0 5 I feel fine, 10 5 I feel like I am Collectively, these results suggest that blurring the visual field about vomit). An overall 0-10 Vection rating was also recorded (0 5 I felt I was completely stationary, 10 5 I felt that I was hastens the onset of MS symptoms in an optokinetic drum. The mean SSQ Total score obtained in the Blur condition was rotating and the drum was completely stationary). The 0-10 74% higher than the mean score obtained in the control Overall Sickness scale and the 0-10 Vection scale did not contain any subdivisions apart from the two extreme anchor points. Each subject served in both the Control and Blur conditions. Participation was nearly completely counterbalanced (there was an odd number of subjects) to control for any possible order effects, including adaptation. At the conclusion of each trial, the subject rested until the severity of symptoms subsided before leaving the laboratory. The interval between conditions was 48-72 h. Statistical Analysis
SSQ scores, overall sickness ratings, and vection ratings were all analyzed using two-way ANOVAs. The between-subjects factor was Order (first or second) and the within-subjects factor was Vision (control or blur). Tests yielding a P-value of 0.05 or less were considered to be statistically significant. All data were analyzed using the statistical computational web-based tests available at VassarStats.net. RESULTS All 15 subjects completed the full 10 min of each trial. Four SSQ scores were calculated for each subject using methods and 442
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Fig. 2. Mean overall SSQ scores and subscores for nausea, oculomotor symptoms, and disorientation. Error bars represent 6 1 SEM.
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VISUAL BLUR & MS SYMPTOMS—Bonato et al.
condition. Also, oculomotor and disorientation subscores were, using strobe lighting26 and shutter glasses19 that ‘freeze’ subserespectively, 79% and 84% higher in the Blur condition, sug- quent images on the retina for brief periods of time and prevent gesting that the effect of visual blur was the largest for disorien- retinal drift. When retinal slippage and blurring is reduced tation. Given that the conditions were exactly the same except using these techniques, MS is also reduced.19,26 for the frosted filter used in the Blur condition it seems likely An alternative explanation for the current results is based on that visual blur alone led to these results. The authors recognize the ‘poison hypothesis.’ It has been proposed14,22 that sensory that significantly different SSQ scores do not necessarily indi- conflict may result in afferent signals that are similar to those cate significant differences in “sickness,” or even that individu- that might occur when some types of neurotoxins enter the als felt sick at all. body. According to this hypothesis MS may be a genetically Current study results differ from those obtained by Webb,24 programmed response that has evolved to rid the body of poiwho presented a blurred striped pattern that was printed and son, but that is mistakenly engaged. Of course not all poisons mounted to an optokinetic drum’s interior and found no sig- are the same. It has been shown that nicotine hastens the onset nificant difference in accumulated sickness ratings between the of MS symptoms7—a finding that supports the poison hypothcontrol and blur conditions. Post-exposure symptoms were dif- esis in that it shows the combination of a real poison with senferent in the Webb experiment and the author concluded that sory inputs that mimic poison have an additive effect. However, the blurred drum was only partially effective in producing more scopolamine, a toxin derived from the nightshade (Solanaceae) MS. There are differences, however, between the Webb study family of plants, has been shown to be an effective treatment for and the current one. The speed of rotation was twice as fast in MS.16,20 Collectively, such findings suggest sensory conflict the current study (60° · s21 as opposed to 30° · s21). In addition, may mimic cholinergic poison effects (e.g., nicotine) but not anticholinergic effects (scopolamine). the filter used in the current experiment also blurred the entire Delivered by Ingenta to: Simon Fraser University Blurred vision is a symptom of many poisons. Hence, the scene, whereas in Webb’s study some sharp edges may have IP: 185.71.3.84 On: Fri, 29 Jul 2016 20:31:14 hypothesis that adding a symptom of poisoning (in this case been visible. We also note that the results of the current study Copyright: Aerospace Medical Association are consistent with the reported correlation between visual acu- blurring) to a sensory conflict situation can exacerbate MS seems to be supported by the obtained results. However, there ity and MS—those with lower visual acuity report more severe are several issues that warrant mention here that call this MS. In the authors’ opinion, the frosted filter used in the curhypothesis into question. First off, the poison hypothesis does rent study created a realistic simulation of visual acuity degranot assert, and does not make any predictions about, vection. dation caused by myopia. In accordance with our hypothesis, the current results sup- In the current study, subjects rated vection to be significantly port our assertion that differences in the relative strength of stronger in the Blur condition. Although it has been suggested retinal inputs to the brain can affect both self-motion percept that vection and MS symptoms can be correlated,8 the authors (in this case vection) and MS. It is fairly well accepted that the can think of no reason why a simulated poisoning symptom, in visual system uses different channels or pathways.11,12 The parthis case, blurred vision, should produce more vection. vocellular pathway is much involved in the processing of inforAnother problem for the poison hypothesis, both for this mation that comes in from the central portion of the visual experiment and in general, is that one of the most effective field. Details of what are being looked at, falling on the fovea, treatments for MS is scopolamine, a drug derived from the are primarily processed via the parvocellular pathway. It is Nightshade family of plants and most definitely a poison. important to note that the parvocellular pathway does not have Attempts to argue out of this paradox run into trouble even if a primary role in processing motion signals, but the magnocel- one tries to differentiate between different types of poisons. lular pathway does. Hence, in the current experiment blurring One hypothesis regarding the differential effects of poisons is the stimulus served to degrade input for the parvocellular path- that the symptoms or conditions that mimic cholinergic poiway but not the magnocellular. The current results may be soning lead to MS. This hypothesis would be in agreement with rooted in a differential weighting of these two pathways. When reported findings that nicotine can exacerbate MS symptoms.7 the stimulus is blurred, visual acuity is compromised and hence It is also in agreement with research on scopolamine16,20 that the parvocelluar pathway may play a lesser role. However, the supports the hypothesis that this anticholinergic poison is an magnocellular pathway that is sensitive to motion is less effective countermeasure against MS. The catch here is that affected by blurring. blurred vision is not just a symptom of some cholinergic poiA similar explanation was provided for previous results that sons, it is also a possible symptom of scopolamine. suggested vection1 and MS2 are both increased when chromatic There are several limitations of this study. The MS symptoms stimuli are viewed as opposed to achromatic. Under the current in the current study were visually induced and hence may apply experimental conditions blurring may have then added to the more for simulator sickness given that optokinetic drum net influence of afferent magnocellular signals, leading to an conditions are similar to those occurring in some vehicle simulaincrease in: 1) vection; 2) the salience of sensory conflict; and 3) tors (fixed-base) in that the self-motion that is experienced is creMS symptoms. ated by visual input. Subsequent testing should be conducted on The authors acknowledge that blurring the visual scene the effects of visual blurring under more typical MS-producing could also serve to exacerbate retinal slippage, a factor that in conditions. If a blurred visual field does lead to a faster onset turn could lead to more MS. This possibility has been tested of MS in vehicles, it would lead to practical but simple AEROSPACE MEDICINE AND HUMAN PERFORMANCE Vol. 86, No. 5
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8. Hettinger LJ, Berbaum KS, Kennedy RS, Dunlap WP, Nolan MD. Vection countermeasures such as not removing optical correcting and simulator sickness. Mil Psychol. 1990; 2(3):171–181. lenses under motion provocative conditions. However, the 9. Kennedy RS, Drexler JM, Compton DE, Stanney KM, Lanham DS, scope of the current study does not allow us to address that et al. Configural scoring of simulator sickness, cybersickness, and space question directly, only to suggest additional research. Another adaptation syndrome: similarities and differences. In: Hettinger LJ, related limitation is the artificial nature of the conditions in our Hass MW, editors. Virtual and adaptive environments: applications, implications, and human performance issues. Mahwah (NJ): Lawrence lab. These conditions allow for a high degree of control, allowing Erlbaum Associates; 2003:247–278. us to isolate the effects of the independent variable, in this case 10. Kennedy RS, Lane NE, Berbaum KS, Lilienthal MG. Simulator sickness visual blur. Unfortunately, more control often means that the questionnaire: an enhanced method for quantifying simulator sickness. testing environment is less like the environments that we want to Int J Aviat Psychol. 1993; 3(3):203–220. know about. Those environments are most often the interiors of 11. Livingstone MS, Hubel DH. Psychophysical evidence for separate channels for the perception of form, color, movement, and depth. J moving vehicles. Neurosci. 1987; 7(11):3416–3468. In conclusion, blurring the visual field in an optokinetic 12. Livingstone M, Hubel D. Segregation of form, color, movement, and drum can exacerbate MS symptoms and enhance vection. Blurdepth: anatomy, physiology, and perception. Science. 1988; 240(4853): ring the visual field, however, may lend more influence to the 740–749. magnocellular visual pathway by weakening the role played by 13. Money KE. Motion sickness. Physiol Rev. 1970; 50(1):1–39. 14. Money KE. Motion sickness and evolution. In: Crampton GH, editor. the parvocellular pathway. Such a differential influence of these Motion and space sickness, Chapter 1. Boca Raton (FL): CRC Press; pathways would serve to explain both the vection and MS 1990. results obtained in the current study. It is difficult to account 15. Money KE, Cheung BS. Another function of the inner ear: facilitation for these results in the context of the poison hypothesis that of the emetic response to poisons. Aviat Space Environ Med. 1983; asserts MS is the result of a mistakenly engaged mechanism 54(3):208-211. Delivered Fraser University 16. Price NM, Schmitt LG, McGuire J, Shaw JE, Trobough G. Transdermal that evolved to rid the body of dangerous toxins. by Ingenta to: Simon IP: 185.71.3.84 On: Fri, 29 Jul 2016 20:31:14 scopolamine in the prevention of motion sickness at sea. Clin Pharmacol Copyright: Aerospace Medical Association Ther. 1981 ; 29(3):414–419.
ACKNOWLEDGMENTS Authors and affiliations: Frederick Bonato, Ph.D., Montclair State University, Montclair, NJ; Andrea Bubka, Ph.D., Saint Peter's University, Jersey City, NJ; and William Thornton, M.D., Houston, TX.
REFERENCES 1. Bonato F, Bubka A. Chromaticity, spatial complexity, and the perception of self-motion. Perception. 2006; 35(1):53–64. 2. Bonato F, Bubka A, Alfieri L. Display color affects motion sickness onset in an optokinetic drum. Aviat Space Environ Med. 2004; 75(4):306–311. 3. Fischer MH, Kornmüller AE. Optokinetisch ausgelöste Bewegungswahrnehmung und optokinetischer Nystagmus. [Optokinetically induced motion perception and optokinetic nystagmus.] Journal für Psychologie und Neurologie (Liepzig). 1930; 41:273–308. 4. Gibson JJ. The perception of the visual world. Boston (MA): Houghton Mifflin; 1950. 5. Gibson JJ. The senses considered as perceptual systems. Boston (MA): Houghton Mifflin; 1966. 6. Knox GW. Motion sickness: an evolutionary and genetic basis for the negative reinforcement model. Aviat Space Environ Med. 2014; 85(1):46–49. 7. Golding JF, Prosyanikova O, Flynn M, Gresty MA. The effect of smoking nicotine tobacco versus smoking deprivation on motion sickness. Auton Neurosci. 2011; 160(1-2):53–58.
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17. Reason J, Brand J. Motion sickness. London (UK): Academic Press; 1975:103–128. 18. Reavley CM, Golding JF, Cherkas LF, Spector TD, MacGregor AJ. Genetic influences on motion sickness susceptibility in adult women: a classical twin study. Aviat Space Environ Med. 2006; 77(11):1148–1152. 19. 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(1):2–7. 20. Simmons RG, Phillips JB, Lojewski RA, Wang Z, Boyd JL, Putcha L. The efficacy of low-dose intranasal scopolamine for motion sickness. Aviat Space Environ Med. 2010; 81(4):405–412. 21. Thornton WE, Bonato F. Space motion sickness and motion sickness: symptoms and etiology. Aviat Space Environ Med. 2013; 84(7):716– 721. 22. Treisman M. Motion sickness: an evolutionary hypothesis. Science. 1977; 197(4302):493–495. 23. Tschermak A. Optischer raumsinn. In: Bethe A, Bergnann G, Emden G, Ellinger A, editors. Handbuch der normalen und pathologischen physiologie. Berlin (Germany): Springer-Verlag; 1931. 24. Webb NA. Visual acuity, eye movements, the illusion of motion and motion sickness with optokinetic stimuli. [Ph.D. thesis; 1995.] [Accessed 16 July 2013.] Available from http://www.motion-sickness.co.uk. 25. Webb NA, Griffin MJ. Optokinetic stimuli: motion sickness, visual acuity, and eye movements. Aviat Space Environ Med. 2002; 73(4):351– 358. 26. Webb CM, Estrada A, Athy JR. Motion sickness prevention by an 8-Hz stroboscopic environment during air transport. Aviat Space Environ Med. 2013; 84(3):177–183.
May 2015
Visual Blur and Motion Sickness in an Optokinetic Drum Frederick Bonato; Andrea Bubka; William Thornton
BACKGROUND:
METHODS:
RESULTS:
CONCLUSIONS:
KEYWORDS:
The most commonly cited hypotheses for motion sickness (MS) focus on inconsistent sensory inputs. Visual/vestibular conflicts may lead to MS, but visual input from retinal regions/neural pathways that are sensitive to motion might bear more weight in MS etiology. We hypothesized in an optokinetic drum would attenuate the Delivered by Ingentathat to:inducing Simon blurred Fraservision University influence of foveal (parvocellular) input, butOn: not peripheral (magnocellular) input that is sensitive to motion. Increased IP: 185.71.3.84 Fri, 29 Jul 2016 20:31:14 Copyright: Aerospace Medical Association relative influence of peripheral visual input was predicted to subsequently lead to more visual/vestibular conflict and subsequently more severe MS symptoms. Through goggles that were either clear or frosted, 15 subjects (5 men, 10 women, mean age 5 24.9 yr, range 5 18-49) viewed the interior of a rotating (60° · s21) optokinetic drum for 10 min. Subjects completed the Simulator Sickness Questionnaire (SSQ) before and after viewing. Overall subjective sickness ratings (0-10) and visually induced self-motion perception (vection) ratings (0-10) were also recorded. Postexposure SSQ scores obtained in the blur condition (total - 52.9, oculomotor - 38.9, disorientation - 69.6) were significantly higher than those obtained in the control condition (total - 30.4, oculomotor - 21.7, disorientation - 37.8). Overall sickness ratings and vection ratings were also significantly higher in the blur condition. These results suggest that visual blur can exacerbate MS, perhaps because of differential influences of visual pathways. Although these results were obtained with an optokinetic drum, possible effects of visual blurring in motion provocative environments such aircraft, watercraft, spacecraft, and land vehicles should be considered. sensory conflict, vision, vestibular, vection. Bonato F, Bubka A, Thornton W. Visual blur and motion sickness in an optokinetic drum. Aerosp Med Hum Perform. 2015; 86(5):440–444.
T
he best known theories of motion sickness (MS) are based on sensory conflict.17 These theories assert that when afferent signals regarding self-motion are not consistent, MS can result. Such inconsistencies often involve the visual and vestibular systems. Hence, the navigator of an aircraft, who looks mostly at instruments, may be more susceptible to MS than the pilot who often receives consistent visual and vestibular inputs regarding self-motion. Sensory conflict does not require actual self-motion relative to Earth. Visual input alone such as that which can occur in a flight simulator can lead to compelling self-motion perception that is entirely visually induced. This phenomenon, known as vection,3,23 is associated with simulator sickness.8 Even if one accepts sensory conflict as a possible cause of MS, the explanation is incomplete. The question about “why” sensory conflict should lead to MS needs to be addressed. Some investigators and theorists have proposed that MS is part of our genetic endowment and the product of evolution.6,13,14 A large survey study of monozygotic and dizygotic twins yielded 440
AEROSPACE MEDICINE AND HUMAN PERFORMANCE Vol. 86, No. 5
results suggesting a strong and significant genetic contribution to MS susceptibility.18 One set of theories asserts that sensory conflict can ‘trick’ the brain into reacting as if poisoning has occurred.15,22 Such theories treat MS as a mistakenly engaged mechanism aimed at eliminating toxins from the body. Another explanation for MS is that sensory conflict both within a sense (vestibular) and between senses (visual/vestibular) can falsely trigger a protective mechanism aimed at inhibiting mobility during
From Montclair State University, Montclair, NJ; Saint Peter’s University, Jersey City, NJ; and Houston, TX. This manuscript was received for review in July 2014. It was accepted for publication in February 2015. Peer review and editorial oversight for this article were conducted by Sarah A. Nunneley, M.D., M.S., former Editor of this journal. Address correspondence to: Frederick Bonato, Ph.D., Montclair State University, 1 Normal Ave., Montclair, NJ 07043; [email protected]. Reprint & Copyright © by the Aerospace Medical Association, Alexandria, VA. DOI: 10.3357/AMHP.4105.2015
May 2015
VISUAL BLUR & MS SYMPTOMS—Bonato et al.
a time when vestibular damage or malfunction has occurred.21 2 h before each trial. The Saint Peter’s University InstituSuch a protective mechanism would offer a survival advantage tional Review Board approved the study in advance. Each subfor our ancient ancestors in that a low level of activity would be ject provided written informed consent before participating in less likely to attract predators during a time when the ability to the study. spatially orient is compromised by vestibular malfunction. Equipment and Materials The human visual system has also evolved in ways that may The optokinetic drum consisted of a synthetic composite cylhave helped enhance our ancestors’ survivability. Central, or foveal, vision largely involves a visual pathway from retina to inder 122 cm in height and 107 cm in diameter. The cylinder was mounted in a sturdy wooden frame, yielding a drum that brain that is high resolution in nature. Packed with some six million cones, visual acuity is sharpest for images that fall on or close was completely rigid. The drum was suspended from a motor to the fovea. This parvocellular pathway is also color sensitive attached to a beam directly above the drum with four steel and, hence, when we want to identify something in our environ- cables. Given the mass of the drum, and the position of the ment we naturally look directly at it, using color and visual details cables supporting it, this method of suspending the drum resulted in a smooth and steady rotation, free of any wobble or to aid identification.11,12 Peripheral vision facilitated by rods is color-blind and is not able to process fine details. Hence, periph- sway after approximately 2 s of rotation. Head position was eral vision that is facilitated by the magnocellular pathway is not maintained throughout the experiment by means of an optical as useful for identifying objects. This pathway, however, is sensi- chin rest in which the subject’s chin rested in a stationary contive to motion that is detected by shifting patterns of light on the cave depression while the subject’s forehead rested against a curved metal bar. Viewing took place with the subject’s head retina. It is good for detecting moving objects—that for our centered at the axis of rotation. This resulted in a viewing disancient ancestors may have been predator or prey—but also bythrough Ingentathe to: Simon tanceFraser of 48.5 University cm when the subject’s line of sight was perpenhelps to provide information aboutDelivered self-motion IP: 185.71.3.84 On: Fri, 29 Jul 4,5 dicular2016 to the20:31:14 drum’s surface. Horizontally positioned baffles environment via optical flow patterns on the retina. It is imporCopyright: Aerospace Medical Association attached to the top and bottom of the chin rest restricted the tant to note that several investigators have reported results that suggest visually induced self-motion perception, or vection, is subject’s view so that the only surface seen through the baffles was the drum’s interior. Illumination was provided by two largely mediated by peripheral stimulation. Vection is also some32-W florescent bulbs positioned directly behind a translutimes accompanied by MS symptoms.8 It has been claimed that visual acuity is correlated with MS cent plastic diffuser panel and 102 cm directly above the top in an optokinetic drum.24,25 It has been suggested that this cor- of the drum. The stimulus pattern that lined the interior of the drum consisted of a black and a white checkerboard patrelation is possibly due to eye movements that, in turn, influtern. Each patch was 9° wide and 30° wide. The black and ence motion sickness, or the detection of foveal image slip which somehow influences MS. Webb reported24 that present- white stripes had luminance values of 1.6 and 36.0 cd · m22, respectively. ing blurred stripes in an optokinetic drum also exacerbated MS Viewing took place through a pair of goggles with a transcompared to sharply printed ones. For the current study, we artificially blurred the visual field using a frosted optical filter. parent plastic front. The front of the goggles was either left clear and unobstructed (control condition) or a frosted aceSuch a manipulation creates a degraded image that leads to less meaningful input to the parvocellular pathway. It could be pre- tate filter was adhered to the surface, creating a “blurred” view dicted that blurring the image would not adversely affect the of the drum’s interior (blur condition). The filter used (Rosculux #114: Hamburg Frost) was obtained from Roscolux Labomotion sensitive magnocellular system. The brain receiving inputs from these two pathways could weight them differently ratories (Stamford, CT). Digital photographs of the drums because of blurring—the motion sensitive magnocellular input interior taken with and without the frosted filter are shown in being given more weight compared to the parvocellular input Fig. 1. Motion sickness symptoms were assessed using the Simulathat is differentially affected by visual ‘noise.’ In light of this pretor Sickness Questionnaire (SSQ).10 The SSQ is a well-accepted dicted differential weighting of neural inputs, it was hypotheassessment instrument that has been used for various forms of sized that artificially blurring the scene would lead to more MS, including MS that is visually induced. When scored accordsevere MS symptoms in addition to more salient vection. ing to published guidelines,9 the SSQ yields four scores: a total SSQ score and three subscores corresponding to nausea, oculomotor effects, and disorientation. There are 16 items on the METHODS questionnaire (general discomfort, fatigue, headache, eye strain, difficulty focusing, increased salivation, sweating, nausea, diffiSubjects Voluntarily participating in the experiment were 15 Saint Peter’s culty concentrating, fullness of the head, blurred vision, dizziness University undergraduate students and staff members (5 men, with eyes open, dizziness with eyes closed, vertigo, stomach awareness, and burping) that contribute to the SSQ scores. Sub10 women). The mean age of subjects was 29.9 yr and ranged jects indicate the level at which each symptom is experienced from 18 to 49. Persons reporting any visual, vestibular, neurological, gastrointestinal abnormality, or any other health prob- both pre-treatment and post-treatment by circling one of four choices (none, slight, moderate, or severe). lem were not allowed to participate. Subjects fasted for at least AEROSPACE MEDICINE AND HUMAN PERFORMANCE Vol. 86, No. 5
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weighting factors outlined in Kennedy et al.9: a total SSQ score and three subscores for nausea, oculomotor symptoms, and disorientation (see Fig. 2). No main effects of Order were revealed. A two-way ANOVA revealed a significant main effect of condition for total SSQ scores [F(1,13) 5 5.18, P 5 0.040] and significantly higher subscores for oculomotor symptoms [F(1, 13) 5 5.77, P 5 0.032] and disorientation Fig. 1. Optokinetic drum interior viewed with A) clear lenses and B) through a frosted acetate filter (Rosculux #114: [F(1, 13) 5 4.76, P 5 0.048] in Hamburg Frost). the Blur condition. Mean (0-10) Overall Sickness ratings obtained Procedure and Design The subject was given instructions regarding the SSQ before in the Blur condition (3.9) were also significantly higher [F(1, 13) 5 5.17, P 5 0.041] than those obtained in the Control proceeding to fill out the pre-treatment page of the SSQ form. The subject was then positioned inside the optokinetic drum, condition (2.9). No interaction effects between Order and Condition were revealed. Three subjects reported ‘slight’ nausea and fitted with the goggles, and asked to keep his or her head staby instructed Ingenta to: Simon Fraser‘moderate University one reported ’ nausea in the control condition. In tionary by using an optical chin rest. ThDelivered e subject was IP: 185.71.3.84 On: Fri, 29 Jul 2016 20:31:14 to close his/her eyes until the experimenter gave instructions the Blur condition, two subjects reported slight nausea and Copyright: Aerospace Medical Association to open them, marking the beginning of the trial. The subject four reported moderate nausea. Mean (0-10) Overall Vection ratings obtained in the Blur condition (8.4) were signifiwas also told to keep his/her head still while watching the cantly higher [F(1,13) 5 4.77, P 5 0.049] than those obtained interior surface of the rotating (60° · s21) drum. After 10 min of viewing, the subject was instructed to close his/her eyes, the in the Control condition (6.9). drum was raised, and the subject was immediately given the post-treatment portion of the SSQ form to complete. After DISCUSSION completing the SSQ a 0-10 Overall Sickness rating was obtained for the entire trial (0 5 I feel fine, 10 5 I feel like I am Collectively, these results suggest that blurring the visual field about vomit). An overall 0-10 Vection rating was also recorded (0 5 I felt I was completely stationary, 10 5 I felt that I was hastens the onset of MS symptoms in an optokinetic drum. The mean SSQ Total score obtained in the Blur condition was rotating and the drum was completely stationary). The 0-10 74% higher than the mean score obtained in the control Overall Sickness scale and the 0-10 Vection scale did not contain any subdivisions apart from the two extreme anchor points. Each subject served in both the Control and Blur conditions. Participation was nearly completely counterbalanced (there was an odd number of subjects) to control for any possible order effects, including adaptation. At the conclusion of each trial, the subject rested until the severity of symptoms subsided before leaving the laboratory. The interval between conditions was 48-72 h. Statistical Analysis
SSQ scores, overall sickness ratings, and vection ratings were all analyzed using two-way ANOVAs. The between-subjects factor was Order (first or second) and the within-subjects factor was Vision (control or blur). Tests yielding a P-value of 0.05 or less were considered to be statistically significant. All data were analyzed using the statistical computational web-based tests available at VassarStats.net. RESULTS All 15 subjects completed the full 10 min of each trial. Four SSQ scores were calculated for each subject using methods and 442
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Fig. 2. Mean overall SSQ scores and subscores for nausea, oculomotor symptoms, and disorientation. Error bars represent 6 1 SEM.
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condition. Also, oculomotor and disorientation subscores were, using strobe lighting26 and shutter glasses19 that ‘freeze’ subserespectively, 79% and 84% higher in the Blur condition, sug- quent images on the retina for brief periods of time and prevent gesting that the effect of visual blur was the largest for disorien- retinal drift. When retinal slippage and blurring is reduced tation. Given that the conditions were exactly the same except using these techniques, MS is also reduced.19,26 for the frosted filter used in the Blur condition it seems likely An alternative explanation for the current results is based on that visual blur alone led to these results. The authors recognize the ‘poison hypothesis.’ It has been proposed14,22 that sensory that significantly different SSQ scores do not necessarily indi- conflict may result in afferent signals that are similar to those cate significant differences in “sickness,” or even that individu- that might occur when some types of neurotoxins enter the als felt sick at all. body. According to this hypothesis MS may be a genetically Current study results differ from those obtained by Webb,24 programmed response that has evolved to rid the body of poiwho presented a blurred striped pattern that was printed and son, but that is mistakenly engaged. Of course not all poisons mounted to an optokinetic drum’s interior and found no sig- are the same. It has been shown that nicotine hastens the onset nificant difference in accumulated sickness ratings between the of MS symptoms7—a finding that supports the poison hypothcontrol and blur conditions. Post-exposure symptoms were dif- esis in that it shows the combination of a real poison with senferent in the Webb experiment and the author concluded that sory inputs that mimic poison have an additive effect. However, the blurred drum was only partially effective in producing more scopolamine, a toxin derived from the nightshade (Solanaceae) MS. There are differences, however, between the Webb study family of plants, has been shown to be an effective treatment for and the current one. The speed of rotation was twice as fast in MS.16,20 Collectively, such findings suggest sensory conflict the current study (60° · s21 as opposed to 30° · s21). In addition, may mimic cholinergic poison effects (e.g., nicotine) but not anticholinergic effects (scopolamine). the filter used in the current experiment also blurred the entire Delivered by Ingenta to: Simon Fraser University Blurred vision is a symptom of many poisons. Hence, the scene, whereas in Webb’s study some sharp edges may have IP: 185.71.3.84 On: Fri, 29 Jul 2016 20:31:14 hypothesis that adding a symptom of poisoning (in this case been visible. We also note that the results of the current study Copyright: Aerospace Medical Association are consistent with the reported correlation between visual acu- blurring) to a sensory conflict situation can exacerbate MS seems to be supported by the obtained results. However, there ity and MS—those with lower visual acuity report more severe are several issues that warrant mention here that call this MS. In the authors’ opinion, the frosted filter used in the curhypothesis into question. First off, the poison hypothesis does rent study created a realistic simulation of visual acuity degranot assert, and does not make any predictions about, vection. dation caused by myopia. In accordance with our hypothesis, the current results sup- In the current study, subjects rated vection to be significantly port our assertion that differences in the relative strength of stronger in the Blur condition. Although it has been suggested retinal inputs to the brain can affect both self-motion percept that vection and MS symptoms can be correlated,8 the authors (in this case vection) and MS. It is fairly well accepted that the can think of no reason why a simulated poisoning symptom, in visual system uses different channels or pathways.11,12 The parthis case, blurred vision, should produce more vection. vocellular pathway is much involved in the processing of inforAnother problem for the poison hypothesis, both for this mation that comes in from the central portion of the visual experiment and in general, is that one of the most effective field. Details of what are being looked at, falling on the fovea, treatments for MS is scopolamine, a drug derived from the are primarily processed via the parvocellular pathway. It is Nightshade family of plants and most definitely a poison. important to note that the parvocellular pathway does not have Attempts to argue out of this paradox run into trouble even if a primary role in processing motion signals, but the magnocel- one tries to differentiate between different types of poisons. lular pathway does. Hence, in the current experiment blurring One hypothesis regarding the differential effects of poisons is the stimulus served to degrade input for the parvocellular path- that the symptoms or conditions that mimic cholinergic poiway but not the magnocellular. The current results may be soning lead to MS. This hypothesis would be in agreement with rooted in a differential weighting of these two pathways. When reported findings that nicotine can exacerbate MS symptoms.7 the stimulus is blurred, visual acuity is compromised and hence It is also in agreement with research on scopolamine16,20 that the parvocelluar pathway may play a lesser role. However, the supports the hypothesis that this anticholinergic poison is an magnocellular pathway that is sensitive to motion is less effective countermeasure against MS. The catch here is that affected by blurring. blurred vision is not just a symptom of some cholinergic poiA similar explanation was provided for previous results that sons, it is also a possible symptom of scopolamine. suggested vection1 and MS2 are both increased when chromatic There are several limitations of this study. The MS symptoms stimuli are viewed as opposed to achromatic. Under the current in the current study were visually induced and hence may apply experimental conditions blurring may have then added to the more for simulator sickness given that optokinetic drum net influence of afferent magnocellular signals, leading to an conditions are similar to those occurring in some vehicle simulaincrease in: 1) vection; 2) the salience of sensory conflict; and 3) tors (fixed-base) in that the self-motion that is experienced is creMS symptoms. ated by visual input. Subsequent testing should be conducted on The authors acknowledge that blurring the visual scene the effects of visual blurring under more typical MS-producing could also serve to exacerbate retinal slippage, a factor that in conditions. If a blurred visual field does lead to a faster onset turn could lead to more MS. This possibility has been tested of MS in vehicles, it would lead to practical but simple AEROSPACE MEDICINE AND HUMAN PERFORMANCE Vol. 86, No. 5
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8. Hettinger LJ, Berbaum KS, Kennedy RS, Dunlap WP, Nolan MD. Vection countermeasures such as not removing optical correcting and simulator sickness. Mil Psychol. 1990; 2(3):171–181. lenses under motion provocative conditions. However, the 9. Kennedy RS, Drexler JM, Compton DE, Stanney KM, Lanham DS, scope of the current study does not allow us to address that et al. Configural scoring of simulator sickness, cybersickness, and space question directly, only to suggest additional research. Another adaptation syndrome: similarities and differences. In: Hettinger LJ, related limitation is the artificial nature of the conditions in our Hass MW, editors. Virtual and adaptive environments: applications, implications, and human performance issues. Mahwah (NJ): Lawrence lab. These conditions allow for a high degree of control, allowing Erlbaum Associates; 2003:247–278. us to isolate the effects of the independent variable, in this case 10. Kennedy RS, Lane NE, Berbaum KS, Lilienthal MG. Simulator sickness visual blur. Unfortunately, more control often means that the questionnaire: an enhanced method for quantifying simulator sickness. testing environment is less like the environments that we want to Int J Aviat Psychol. 1993; 3(3):203–220. know about. Those environments are most often the interiors of 11. Livingstone MS, Hubel DH. Psychophysical evidence for separate channels for the perception of form, color, movement, and depth. J moving vehicles. Neurosci. 1987; 7(11):3416–3468. In conclusion, blurring the visual field in an optokinetic 12. Livingstone M, Hubel D. Segregation of form, color, movement, and drum can exacerbate MS symptoms and enhance vection. Blurdepth: anatomy, physiology, and perception. Science. 1988; 240(4853): ring the visual field, however, may lend more influence to the 740–749. magnocellular visual pathway by weakening the role played by 13. Money KE. Motion sickness. Physiol Rev. 1970; 50(1):1–39. 14. Money KE. Motion sickness and evolution. In: Crampton GH, editor. the parvocellular pathway. Such a differential influence of these Motion and space sickness, Chapter 1. Boca Raton (FL): CRC Press; pathways would serve to explain both the vection and MS 1990. results obtained in the current study. It is difficult to account 15. Money KE, Cheung BS. Another function of the inner ear: facilitation for these results in the context of the poison hypothesis that of the emetic response to poisons. Aviat Space Environ Med. 1983; asserts MS is the result of a mistakenly engaged mechanism 54(3):208-211. Delivered Fraser University 16. Price NM, Schmitt LG, McGuire J, Shaw JE, Trobough G. Transdermal that evolved to rid the body of dangerous toxins. by Ingenta to: Simon IP: 185.71.3.84 On: Fri, 29 Jul 2016 20:31:14 scopolamine in the prevention of motion sickness at sea. Clin Pharmacol Copyright: Aerospace Medical Association Ther. 1981 ; 29(3):414–419.
ACKNOWLEDGMENTS Authors and affiliations: Frederick Bonato, Ph.D., Montclair State University, Montclair, NJ; Andrea Bubka, Ph.D., Saint Peter's University, Jersey City, NJ; and William Thornton, M.D., Houston, TX.
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