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Conflicting Sensory Orientation Cues as a Factor in Motion Sicknessl FRED E. GUEDRY, JR. Naval Aerospace Medical Institute SUMMARY Evidence is adduced to support the hypothesis that conflicting sensory data relating In spatial orientation from among visual, vestibular, and somatosensory systems can induce motion sickness in the absence of any strong, long, or periodic stimulus to the semicircular canals or otolith system. During a number of years of conducting spin- ning, oscillating, and tilting experiments, I have never purposely conducted a motion-sickness experiment. However, in the course of various experiments, some stimulus conditions seemed much more conducive to motion sickness than others, and some individuals were much more susceptible to motion sickness than others. One of the primary aims of the present paper is to point out that a vestibular stimulus of moderate magnitude, repeated several times but not with any particular periodicity, can produce a high incidence of the signs and symptoms of motion sickness. This stimulus, which has been vari- ously named the Coriolis vestibular stimulus or the angular Coriolis stimulus, involves contradic- tory sensory input from within the labyrinth itself. The kind of stimulus to which I refer is de- picted in figure 1. The subject is rotating on a device about an Earth-vertical axis that has an angular velocity o>i, and his head tilt is made about a second axis, the ovaxis, which is orthog- onal to the axis of the turntable. During the head movement there are two angular acceleration components: (1) Angular accelerations about the 1 I should like lo acknowledge very helpful communica- tions with K. E. Money and with J. T. Reason who have conducted independent reviews of motion-sickness literature and have provided me with their prepublication manuscripts. from starting and stopping the head move- ment, which would occur during any natural head movement even if the table were not rotating. These accelerations leave no residual effects. (2) The second component is constituted by angu- lar accelerations about a third orthogonal axis, the cuio>2-axis, shown in figure 1. During the head movement, this stimulus changes in magni- tude and direction relative to the canal system so that a complex pattern of stimulation of the canals is produced during the movement. The o>io>2 acceleration would cause the canals to signal approximate angular velocity about the subject's y-axis, whereas the change in position relative to gravity signaled by the otolith organs during the movement would be about the sub- ject's jr-axis. The cti|0>2 stimulus shifts during the head movement but when averaged over time, the (aio>> stimulus is alined with the sub- ject's y-axis. When the movement is completed, the cupulae deflections would signal rotation which should be accompanied by change in orien- tation relative to gravity (if such rotation were really taking place), but the otoliths would signal constant position; i.e., no change in orientation relative to gravity. These patterns of sensory input from the canals and otoliths are clearly con- flicting. This is in contrast to the normal synergy between canals and otoliths depicted schemat- ically in the lower right portion of figure 1, where
46 THE ROLE OF THE VESTIBULAR ORGANS IN SPACE EXPLORATION the axis of change in orientation signaled by the otoliths and the axis of angular velocity sig- naled by the canals are one and the same; viz, the subject's *-axis. In the past few years we have observed more than 500 student pilots while they made six 45Â° head tilts with their eyes closed during rotation at 15 rpm (refs. 1 and 2). These head move- ments were approximately 30 seconds apart, but there was no strict periodicity maintained. After six such head movements, only 5 percent of the student pilots were adjudged by observers to have been unaffected by the head movements. By the students' own ratings, about 50 percent indicated some feelings of nausea and only 11 percent indicated no effect at all. The magni- tude of the stimulus to the semicircular canals produced by each head movement can be dupli- cated by a simple angular acceleration to 11.5 rpm. Simple angular impulses of this magni- tude seldom produce nausea in the absence of conflicting visual data. Moreover, during the initial angular acceleration to 15 rpm while the head was fixed relative to the turntable, there AXIS OF CHANGE IN ORIENTATION SIGNALED IY OTOLITHS x ----- MEAN AXIS OF ANGULAR VELOCITY SIGNALED BY CANALS HEAD TILT ON ROTATING TABLE ANGULAR VELOCITY SIGNAL FROM CANALS POSITION SIGNAL FROM OTOLITHS RESIDUAL EFFECTS FROM HEAD TILT ON ROTATING TABLE AXIS OF CHANGE IN ORIENTATION SIGNALED rY OTOLITHS AXIS OF ANGULAR VELOCITY SIGNALED IY CANALS NATURAL HEAD TILT FIGURE 1. âIllustrating the directional conflict of sensory inputs from canals and otoliths during head tilt on a rotating table and the concordant sensory input during natural head tilt without concomitant whole-body rotation.
CONFLICTING SENSORY ORIENTATION CUES IN MOTION SICKNESS 47 were no signs from these subjects of displeasure or surprise; yet, with the first head movement that actually produced a lesser angular impulse to the canal system, many subjects indicated dis- pleasure and many exhibited pallor and sweat- ing. All of those subjects who were adjudged to have been severely affected by the head- movement stimulus later dropped out of the flight program. To illustrate the magnitude of this Coriolis vestibular stimulus, the situation shown in figure 2 was used. The configuration shown in A was selected because the residual stimulus as the head movement is completed is to the lateral canals that yield an easily recorded nystagmus. Subjects were positioned so as to locate the plane of the horizontal canals 30Â° from the axis of the turntable. The rotation device was set into rota- tion at 10 rpm (o>r = 10 rpm). After 2 minutes of constant rotation at 10 rpm, the head was dorso- flexed through 60Â° in 3 seconds from the initial position to the final position. In this particular head movement, it is primarily the lateral canals that are stimulated, and though there is some stimulation of the vertical canals, the net residual effect of the stimulus to the vertical canals is zero when the movement is complete. It can be shown that, under this particular condition as the head movement is just completed (A of fig. 2), the angular impulse delivered to the lateral canals by the head movement is equivalent in magnitude to the angular impulse delivered by angular acceleration to 10 rpm with the head fixed as shown in B. Subjects placed in situations A and B of figure 2 produced results graphed in figure 3. The nystagmus produced by the head tilts (A) was usually of lower intensity, and it clearly declined more quickly than that produced by simple angular acceleration (B). A. HEAD TILT DURING ROTATION 6. SIMPLE ANGULAK ACCELERATION FIGURE 2. â Stimulus used to produce horizontal nystagmus (A) by head movement during 60 Â°/sec angular velocity and (B) Ay simple angular acceleration to 60Â°/sec with head in fixed relation to the axis of rotation.
48 THE ROLE OF THE VESTIBULAR ORGANS IN SPACE EXPLORATION STOPPING SIMPLE ANGULAR ACCELERATION ABOUT VERTICAL AXIS Io *â¢â¢ HMD MOVEMFNT CORIOUS STIMULUS H -f'i STOPPING SIMPLE ANGULAR ACCELERATION ABOUT VERTICAL AXIS ) 5Â° 40 3O LU If) > u Â£ Â» rÂ«-9 10 20 30 I0 JO JO K> SO 301 FIGURE 3.âIllustating different decay rates (TT I k) of nystagmus slow-phase velocity following different stimuli of equal magnitude to the lateral canals. Upper left panel is the average result from the individual responses (G through S) displayed in the five lower panels. The rapid decline of nystagmus produced by the head movement is a sign of conflict between the canals, which signal rotation about an axis not alined with gravity, and the otolith and somatosensory systems, which signal a constant orientation relative to gravity. This situation as the head movement is completed is closely analogous to the nystagmus and sensation pro- duced by cessation of rotation about an Earth- horizontal axis; in the latter situation as well, the canals signal rotation while the other sys- tems signal no rotation. As shown in the upper right graphs, the nystagmus decline following rotation about a horizontal axis is more rapid than the decline of nystagmus produced by simple angular acceleration about a vertical axis even though the angular impulses are equal in the two situations (ref. 3). From considerations of the mechanics of the stimulus as well as the magnitude of the nystag- mus responses, the stimulus in situation A is no greater in magnitude than that in situation B. Yet simple angular acceleration of the magnitude and duration used in B may be repeatedly ad- ministered without producing any of the signs of motion sickness, whereas head movements during rotation produce signs of motion sickness. For example, I conducted one experiment in which more than 100 men received 176 simple angular accelerations to 10 rpm within a 4-hour interval. There was not a single indication of motion sickness from these subjects. In an- other series of experiments (refs. 4 and 5) in which a total of 50 men made 45Â° head tilts dur- ing rotation at 7.5 rpm, approximately 70 percent of the subjects showed some sign of motion sick-
CONFLICTING SENSORY ORIENTATION CUES IN MOTION SICKNESS 49 ness. Typically, signs of motion sickness ap- peared within the first 40 head movements. The angular impulses produced by the head move- ments were of less magnitude than the simple angular accelerations to 10 rpm, yet the head movements produced signs of sickness, whereas the stronger simple angular accelerations did not produce these signs. When a person is permitted to move around within a rotating room, there is much more than an intralabyrinthine conflict. During body move- ment within the room, information fed back from the muscles and joints signal curvilinear motion relative to the Earth, while visual estimates that gage the intended movement do not register the curvilinear path. Movement in a straight line relative to the floor of the room is actually move- ment in a curved path relative to the Earth. Even in the absence of vision, the somatosensory system would feed back information indicating curvilinear movement of the hand or foot when the intended movement of the hand or foot is in a straight line. Coupled with these incongruities (between intended movements, somatosensory feedback, and visual feedback) is the intralaby- rinthine conflict as described above. The rearranged sensory input that occurs within the slow rotation room (SRR) is analogous to what happens in experiments in which lenses have been used to rearrange the visual input as subjects attempted to move about (ref. 6). The results within the rotating room have characteris- tics in common with other sensory rearrange- ments. At first, subjects experience difficulty in walking and in other voluntary motor activities, and most subjects experience nausea. With prolonged exposure, the psychomotor skills im- prove, while nausea, nystagmus, and illusions diminish. After adaptation to this situation, return to a natural environment reinstates many of these responses, including nausea (refs. 7 to 9). These new reactions in a natural environ- ment offer inferential support for the "pattern copy" hypothesis proposed by Groen (ref. 10). It may be significant that individuals without labyrinthine function, when exposed to this rotating-room environment, have all of the visual and somatosensory rearrangement encountered by normal subjects, yet they have not been made sick (ref. 7 and A. Graybiel et al., "Compara- tive Effects of 12 Days' Rotation at 10 RPM on Four Normal Subjects and Four Persons With Bilateral Labyrinthine Defects," in preparation). The fact that these subjects showed psycho- motor disturbance upon return to a normal stationary environment indicates that a central- nervous-system adjustment to sensory rearrange- ment had occurred, but no sickness was pro- duced. This could be interpreted to indicate that the intralabyrinthine conflict is crucial to the motion sickness in this situation. However, other interpretations are clearly possible, and this is a debatable issue. Many authors have pointed out experiments (refs. 11 to 17) that show that visual-sensed mo- tion without concomitant vestibular stimulation can produce motion sickness. Especially inter- esting observations were made by Miller and Goodson (ref. 18) in connection with a helicopter simulator. The subject's control stick manipu- lated the motion of the visual field as though the subject had moved, but he actually remained sta- tionary relative to the Earth. Experienced heli- copter flight instructors were reported to be more susceptible to sickness in this situation than were inexperienced students. There is in progress a closely related study by Sinacori (J. B. Sinacori, Northrup Norair Division, Hawthorne, Calif., personal communication), who is using a simulator similar to that used by Miller and Goodson. Some visual distortion present in the earlier device has been reduced, but even so, experienced helicopter pilots have become nause- ated and have found the device difficult to control, whereas inexperienced personnel were less dis- turbed by nausea. The most interesting new development reported by Sinacori is that a motion base has been incorporated into the simulator which gives a vestibular signal as the visual simu- lation is commenced. These vestibular signals are limited by restricted angular displacement of about 10Â° in pitch, roll, and yaw; but the results indicate that when the signals are "washed out" gradually, i.e., by using a time constant of 2 sec- onds or longer in returning the subject to initial upright position, there is a greatly improved con- trol of the simulator and a reduction in nausea among experienced pilots. This improvement
50 THE ROLE OF THE VESTIBULAR ORGANS IN SPACE EXPLORATION with the motion base has been present irrespec- tive of whether the pilots have been exposed first to the motion-base or to the fixed-base condition. Recently, an inexperienced person was exposed to the motion base but with unfavorable washout characteristics, and he did not have nausea. He was then given a training session with favor- able motion characteristics during which his per- formance became very good and nausea was absent. In a third session, he was reexposed to the unfavorable motion characteristics and he became sick and performed poorly, even though initially the same exposure did not produce nausea. The results imply that at least part of the nausea and lack of control with the fixed- base simulator used by Miller and Goodson and later by Sinacori was attributable to the absence of correlated vestibular input. These studies imply that conflicting data from the visual, ves- tibular, and somatosensory systems may be the important aspect of the stimulus relative to pro- ducing motion-sickness symptoms in these situa- tions, and these situations certainly did not in- volve intense or periodic stimuli to either the otolith or semicircular canal systems. The re- sults also stress the fact that training in a motion device sets up expected correlations between motor commands and expected patterns of sen- sory input pertaining to spatial orientation and motion. When these expected patterns do not match the incoming patterns, the probability of sickness is increased. Several authors (refs. 19 to 22; ref. 23, p. 99) have emphasized intralabyrinthine conflict as an especially important factor in production of mo- tion sickness. The invariant correlation be- tween information from otoliths and canals in natural head movements leads me to speculate that unnatural stimuli that yield conflicting inputs from these two kinds of labyrinthine sense organs are especially potent in the production of motion sickness. The vestibular receptors work on an inertial principle and provide quantitative velocity and position data relative to an external fixed reference system which perceptually is the Earth. In a natural environment, the adequacy of reflex actions and perceptions depends upon the magnitude and direction of angular velocities and displacements signaled. Inherent in ves- tibular sensations are both magnitude and direc- tion. If an unnatural stimulus situation produces a magnitude mismatch or a directional mismatch in the sensory signals from the otoliths and canals, the individual's reflex actions and per- ceptions are inadequate to cope with his state of motion unless the central nervous system either disregards part of the vestibular input or develops new compensatory reflexes appropriate to the situation. In some individuals, motion sickness is a byproduct of the adjustment to such situations. While I have been emphasizing the importance of intralabyrinthine conflict in the production of motion sickness, I should not discard the idea of "overstimulation" of the canals or otoliths completely. Motion sickness has been en- countered in several experiments involving pro- longed simple angular acceleration about a ver- tical axis (ref. 24, and personal observation). Angular impulses from a 40-rpm change in angu- lar velocity produce pronounced dissociation be- tween nystagmus and sensation in many subjects and strong secondary effects that interact with the effects of immediately following stimuli. There is reason to believe that these interactions increase the incidence of motion sickness that oc- curs with these particular stimuli (ref. 24, and personal observation), but the intensity of the in- teraction is partially determined by the length and strength of the preceding canal stimulus. Motion sickness has also been encountered occasionally in prolonged sinusoidal variation of angular accel- eration, and it has been encountered frequently in sinusoidal variation of vertical linear accel- eration (ref. 25). In some of these experiments, periodicity and intensity of stimulation both ap- pear to be important to the motion sickness that occurs, and it is possible to raise arguments that intermodality conflicts were also present. Whether one chooses to call these situations cases of conflicting sensory inputs, unfavorable periodicity, or overstimulation appears some- what arbitrary. In summary, it has been my purpose to point out that conflicting sensory data relating to spatial orientation from among visual, vestibular, and somatosensory systems can produce a high incidence of motion sickness in the absence of
CONFLICTING SENSORY ORIENTATION CUES IN MOTION SICKNESS 51 any strong, long, or periodic stimulus to the semicircular canals or otolith system. An argument has been presented for the proposition that intralabyrinthine conflict is especially potent in the production of motion sickness, perhaps more potent than intermodality conflicts between the visual, vestibular, and somatosensory sys- tems. It is possible that a functional vestibular system is necessary to the motion sickness that occurs when motion is sensed directly only by the visual system. It has not been my purpose to imply that the idea of overstimulation of the canals or of the otoliths should be discarded as a factor in motion sickness. There are several forms of vestibular stimulation that produce motion sickness without obvious intralabyrinthine conflict or intermodality conflict. REFERENCES 1. AMBLER, R. K.; AND GUEDRY, F. E.: The Validity of a Brief Vestibular Disorientation Test in Screening Pilot Trainees. Aerospace Med., vol. 37, 1966, pp. 124-126. 2. AMBLER, R. K.; AND GUEDRY, F. E.: Cross-Validation of a Brief Vestibular Disorientation Test Administered by a Variety of Personnel. Aerospace Med., vol. 39, 1968, pp. 603-605. 3. BENSON, A. J.; AND BODIN, M. A.: Effect of Orientation to the Gravitational Vertical on Nystagmus Following Rotation About a Horizontal Axis. IAM Rept. no. 338. RAF Institute of Aviation Medicine, Farnborough, England, 1965. 4. GUEDRY, F. E.; COLLINS, W. E.; AND GRAYBIEL, A.: Vestibular Habituation During Repetitive Complex Stimulation: A Study of Transfer Effects. J. Appl. Physiol., vol. 19, 1964, pp. 1005-1115. 5. GUEDRY, F. E.: Visual Control of Habituation to Complex Vestibular Stimulation in Man. Acta Oto-Laryngol., vol. 58. 1964. pp. 377-389. 6. HELD, R.: Exposure History as a Factor in Maintaining Stability of Perception and Coordination. J. Nerv. Ment. Dis., vol. 132, 1961, pp. 26-39. 7. GRAYBIEL, A.; CLARK, B.; AND ZARRIELLO, J. J.: Observa- tions on Human Subjects Living in a "Slow Rotation Room" for Periods of Two Days. Arch. Neurol., vol. 3, 1960, pp. 55-73. 8. GUEDRY, F. E.; AND GRAYBIEL, A.: Compensatory Nystagmus Conditioned During Adaptation to Living in a Rotating Room. J. Appl. Physiol., vol. 17, 1962, pp. 398-404. 9. GUEDRY, F. E.: Habituation to Complex Vestibular Stimulation in Man: Transfer and Retention of Effects From Twelve Days of Rotation at 10 RPM. Percept. Mot. Skills, vol. 21, monograph suppl. 1-V21, 1965, pp. 459-481. 10. GROEN, J. J.: Problems of the Semicircular Canal From a Mechanico-physiological Point of View. Acta Oto-Laryngol., suppl. 163, 1960, pp. 59-66. 11. CLAREMONT, C. A.: The Psychology of Sea-Sickness. Psyche, vol. 11. 1930, pp. 86-90. 12. CRAMPTON, G. H.; AND YOUNG, F. A.: The Differential Effect of a Rotary Visual Field on Susceptibles and Non-susceptibles to Motion Sickness. J. Comp. Physiol. Psychol., vol. 45, 1953, pp. 451-453. 13. GILLINGHAM, K. K.: A Primer of Vestibular Function, Spatial Disorientation and Motion Sickness. Review 4-66. USAF School of Aerospace Medicine, Brooks Air Force Base, Tex. 1966. 14. STEELE, JACK E.: Motion Sickness and Spatial Percep- tion. A Theoretical Study. ASD TR 61-530. Aero- nautical Systems Division, Aerospace Medical Labora- tory, Wright-Patterson Air Force Base, Ohio, 1961. 15. McEACHERN, D.; MORTON, G.; AND LEHMAN, P.: Sea- sickness and Other Forms of Motion Sickness. 1. A General Review of the Literature. War Med., 1942, pp. 410-428. 16. BENFARI, R. C.: Perceptual Vertigo: A Dimensional Study. Percept. Mot. Skills, vol. 18, 1964, pp. 633- 639. 17. REASON, JAMES T.: Motion Sickness: Some Theoretical Considerations. Intern. J. Man Machine Studies, vol. 1. 1969. pp. 21-38. 18. MILLER, J. W.; AND GOODSON, J. E.: A Note Concerning "Motion Sickness" in the 2-FH-2 Hoover Trainer. NSAM-519. Naval School of Aviation Medicine, Pensacola, Fla., 1958. 19. LANSBERG, M. P.: A Primer of Space Medicine. Elsevier, Amsterdam, 1960. 20. LANSBERG, M. P.: Canal Sickness: Fact or Fiction? Industr. Med. Surg., vol. 32,1963, pp. 21-24. 21. ARSLAN, M.: Les Accelerations de Coriolis dans la Stimulation Vestibulaire (Recherches Electronys- tagmographiques). Confin. Neurol., vol. 21, 1961, pp. 403-411. 22. GUEDRY, F. E.; AND MONTAGUE, E. K.: Quantitative Evaluation of the Vestibular Coriolis Reaction. Aero- space Med., vol. 32, 1961, pp. 487-500. 23. GUEDRY, F. E.: Psychophysiological Studies of Vestibular Function. Contributions to Sensory Physiology, W. D. Neff, ed., Academic Press, 1965, pp. 63-135. 24. BROWN, J. H.: Interacting Vestibular Stimuli and Nystagmic Habituation. Acta Oto-I.aryngol., vol. 62. 1966. pp. 341-350. 25. ALEXANDER, S. J.; COTZIN, M.; kin.. J. G.; AND WENDT, G. R.: Studies of Motion Sickness: XVI. The Effects upon Sickness Rates of Waves of Various Frequencies but Identical Acceleration. J. Exptl. Psychol., vol. 37, 1947, pp. 440-448.