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Coriolis effects and motion sickness modelling
Brain Research Bulletin, Vol. 47, No. 5, pp. 543–549, 1998 Copyright © 1999 Elsevier Science Inc. Printed in the USA. All rights reserved 0361-9230/99/$–see front matter
PII S0361-9230(98)00017-3
Coriolis effects and motion sickness modelling Willem Bles* TNO Human Factors Research Institute, Soesterberg, The Netherlands [Received 10 January 1998; Accepted 28 April 1998] ABSTRACT: Coriolis effects are notorious in relation to disorientation and motion sickness in aircrew. A review is provided of experimental data on these Coriolis effects, including the modulatory effects of adding visual or somatosensory rotatory motion information. A vector analysis of the consequences of head movements during somatosensory, visual and/or vestibular rotatory motion stimulation revealed that the more the sensed angular velocity vector after the head movements is aligned with the gravitoinertial force vector, the less nauseating effects are experienced. It is demonstrated that this is a special case of the subjective vertical conflict theory on motion sickness that assumes that motion sickness may be provoked if a discrepancy is detected between the subjective vertical and the sensed vertical as determined on the basis of incoming sensory information. © 1999 Elsevier Science Inc.
an immersion easily provokes motion sickness symptoms [27]. One reason is that the visual and proprioceptive motion information is necessarily incongruent because of inevitable time delays for computing the appropriate visual stimuli during fast head movements. But it is also feasible that in particular applications the subject is confronted with inappropriate proprioceptive motion information, which may contribute to the induction of motion sickness as well. For instance, to look around and to displace oneself in VE, the subject may move his or her head, turn and walk around on a little area, which keeps the incoming sensory information from the visual, the vestibular and the somatosensory system in agreement with each other (apart from the mentioned time delays in case of abrupt movements). If, however, larger displacements are required than the head position tracker system allows, a space mouse may be used by the subject to move through the visual surroundings. In that case, the proprioceptive motion information does not match the visual motion information anymore, because the subject is not moving his or her legs and the vestibular system does not sense motion. Consequently, during immersion in VE the visual and proprioceptive motion information is intermittently in conflict with one another. It is not obvious that the system can handle that situation without any problems, certainly not when head movements are involved as well. In VE experiments it is difficult to isolate the contribution of this particular aspect to the provoked motion sickness, but from other laboratory experiments it is known that somatosensory angular motion information interacts with vestibular and visual angular motion information during standing or walking around. The somatosensory angular motion information often determines not only the magnitude of the final motion percept but also the direction [6,8, 18]. If we define the Coriolis effect as the disorienting and nauseating feelings associated with head tilt during constant velocity rotation, the strength of these Coriolis effects is also considerably enhanced or diminished in a systematic way due to these interactions. This is true both for visual-vestibular interactions [7] and for somatosensory-vestibular interactions [1]. A motion sickness theory has been proposed hypothesizing that there is virtually only one conflict that provokes motion sickness, the conflict concerning the subjective vertical [5]. It is worthwhile to analyse the abovementioned interactions in the Coriolis effects in more detail to determine whether the hypothesis of only one single sensory conflict underlying motion sickness can be maintained or not. If the hypothesis can be maintained, a more quantitative approach on the motion sickness problems is possible. This
KEY WORDS: Locomotion, Motion sickness, Coriolis effects, Modelling, Subjective vertical.
INTRODUCTION When humans and animals walk around in their normal habitat, motion sickness does not occur. If we define locomotion as the natural way to move around (for humans this means primarily walking), then the somatoreceptors dealing with locomotion are important contributors to the equilibrium system to maintain a proper spatial orientation, just as vision and the vestibular system [21,28]. It has been argued that these sensory systems are complementary to each other to guarantee optimal motion and position information over the whole frequency range of the natural movements. However, in the daily life of humans today, locomotion is not the only way to move around. Many transport means are available, often causing stimulation of the sensory systems out of their normal stimulus range, which may lead to incongruent motion information between the different senses. There are various examples of transport means where the somatosensory motion information is not congruent with either the visual or the vestibular motion information. For instance, the equilibrium system of people standing on an escalator or walking on a rolling carpet is confronted with differences in somatosensory motion information about the walking speed and optokinetic surround velocity. Interestingly, these discrepancies do not seem to bother people in terms of spatial orientation or motion sickness, but it is true of course that the time spent on these devices is only short. Incongruent somatosensory and visual motion information is also present during immersion in a virtual environment (VE). Such
* Address for correspondence: Dr. Willem Bles, TNO Human Factors Research Institute, P.O. Box 23, 3769 ZG Soesterberg, The Netherlands. Fax: (31)346 353 977; E-mail: [email protected]
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FIG. 1. Central vestibular angular velocity responses for different stimulus conditions. (A) Response vector due to stimulation of the semicircular yaw-canal, optokinetic and/or somatosensory yaw motion stimulation. (B) Response vectors immediately after a 30° head tilt during constant velocity rotation in darkness, the Coriolis effect. (C) Response vector immediately after a 30° head tilt after a sudden stop from constant velocity rotation, the Purkinje effect.
would be a favorable situation in view of the growing role of VE applications and other simulators in every day life. In the following paragraphs, therefore, some basic experiments on angular self-motion and Coriolis effects are analysed. These experiments are based on paradigms frequently used in research on visual-vestibular and somatosensory-vestibular interactions, which are well documented in the literature. A subsequent vector analysis reveals the common underlying mechanism, which is shown to fit the proposed model on motion sickness. In the Discussion, the consequences of this approach are elaborated, and an approach is suggested to analyse VE conditions on their provocativeness of motion sickness. EXPERIMENTAL DATA AND VECTOR PRESENTATION Angular Motion Perception An angular motion percept, rotation around the z-axis, may be induced by stimulation of the appropriate sensory systems, apart or in combination. Examples of stimuli are acceleration of a rotating chair in darkness (stimulation of the semicircular canals; e.g. [15]), rotation of the visual surroundings (optokinetic stimulation; [9]) and stepping around on a counterrotating platform in darkness (somatosensory stimulation; [1]). The development of the percept in time depends on the applied stimulus and the transfer characteristics of the sensory systems involved. For instance, if a subject is sitting on a chair in total darkness, which is rotated with a trapezoidal velocity profile around the z-axis (yaw-axis rotation; angular acceleration and deceleration 1 rad/s2, maximum velocity v1 5 1 rad/s), the subject will experience an increasing angular velocity during the acceleration phase. This percept fades away after the chair has reached the constant velocity plateau. Constant velocity rotation as such is not sensed by the vestibular system. In the deceleration phase, the subject experiences an increasing angular velocity in the opposite direction, which fades out after the chair has come to a stop. This is a consequence of the second-order system dynamics of the semicircular canals [10]. For the vector in Fig. 1A, it means that the magnitude and the direction may vary, depending on the stimulus characteristics. But the vector is always parallel to the gravity vector. Optokinetically induced sensation of rotation, the so-called
circular vection, has different characteristics [9]. Rotation of the visual surroundings with the same trapezoidal velocity profile will only after a few seconds lead to a sensation of self-rotation with increasing velocity in the opposite direction. After a few more seconds, the induced speed saturates and a constant velocity selfmotion percept remains, whereas the stimulus is perceived as stationary. When the light is switched off, the angular motion percept fades away. Similar observations have been made for somatosensory stimulation, like the apparent stepping in circles in darkness on a counterrotating platform [1]. Neurophysiologic studies in animals showed that second-order neurons in the vestibular nuclei exhibit a direction specific modulation of resting discharge evoked either by body acceleration, optokinetic stimulation [32] or somatosensory stimulation [30]. Combination of the different sensory cues reduces the shortcomings of each transfer characteristic alone (i.e., the poor vestibular response at low frequencies and the poor visual and somatosensory performance at high frequencies). So congruent visual, vestibular and somatosensory stimulation results in a function that accurately transfers velocity information over the whole frequency range of interest for normal every-day motion (up to 1 Hz). The point of interest here is that the different sensory systems all contribute to create in the central vestibular system only one neural discharge pattern, which is the equivalent of an angular velocity vector. Coriolis and Purkinje Effects It is obvious that head tilt on the shoulder over an angle fx of 30° during constant velocity rotation at 1 rad/s in the dark has consequences for the stimulation of the semicircular canals. If we assume that we are dealing with an idealised canal system, a “yaw” canal lying in the head-fixed xy-plane, a “pitch” canal in the xz-plane and a “roll” canal in the yz-plane, sensing rotation about the z-, y- and x-axis, respectively, nothing special happens to the roll-canal other than rotation over the tilt angle fx. Because this is a shortlasting high-frequency stimulus, the response follows the stimulus adequately and at the end of the tilt manoeuver there is no aftereffect, the roll-canal signals no rotation anymore. However, the yaw-canal loses angular momentum and the pitch-canal gains angular momentum proportional to cosf21 (5 20.13) and sin f (5 0.5) respectively [see for details 15,16]. The resulting response vector, together with the angular velocity vectors signalled by the contributing semicircular canals after completion of the head tilt, are depicted in Fig. 1B. The subject indeed experiences a sensation of pitch rotation, in agreement with the resultant vector, but this percept is also often accompanied by signs of nausea [15]. This kind of vestibular stimulation, together with its perceptual and nauseating consequences, is referred to as the Coriolis effect [29]. Guedry explains the Coriolis effect as the consequence of the conflict between the head tilt indicated by the otolith and neck receptors and the direction of the angular velocity vector as sensed by the canals. If a subject rotating in darkness at constant velocity is brought to a sudden stop and immediately thereafter tilts his or her head, he or she will experience a Coriolis-like effect, be it of less intensity. This effect was named Purkinje effect, because Purkinje first described this sort of experiment [26]. The resulting angular velocity response vector after the head tilt is different from the Coriolis effect: Only the head-fixed response vector of the yawcanal due to the stop remains (see Fig. 1C) [15]. Guedry and Benson [16] showed that it was possible to modulate the magnitude of the vestibular Coriolis effect by applying different accelerative stimuli to the horizontal semicircular canals before the head tilt. They had their subjects tilt the head always
CORIOLIS EFFECTS
FIG. 2. (A) The experimental setup for studying somatosensory-vestibular interactions (Dichgans and Brandt had for their studies on visual-vestibular interactions the bar replaced by a rotating chair). (B and C) Effects of head tilt on the magnitude of the nauseating Coriolis effect as determined for visual-vestibular [7] and for somatosensory-vestibular and somatosensoryvisual-vestibular interactions [1]. The arrows in the conditions represent the magnitude of the angular velocities of the chair and the drum in condition B and of the bar and the drum in condition C.
when the chair had a specific angular velocity. If the head was tilted during the acceleration phase (so when a motion percept was present that corresponded to the actual motion stimulus before the head tilt), the Coriolis effect was significantly diminished. However, it was significantly enhanced when before the head tilt a deceleration took place from a twice as large angular rotation velocity (in that case the velocity percept was of equal magnitude but in the opposite direction before the head tilt). In summarizing the relevant results of this section, one should notice that the Coriolis and Purkinje effects are qualitatively the same and that the magnitude of the Coriolis effect can be influenced by additional stimulation of the semicircular canals before the head tilt. Pseudo-Coriolis Effects The studies from Dichgans and Brandt [9] on visual-vestibular interactions and those from Bles [1] on somatosensory-vestibular interactions were both performed with the same instrument, a concentric rotating chair and drum combination (To¨nnies, Freiburg im Breisgau). This device is described in more detail to facilitate understanding of the experimental paradigm. The drum has a cylindrical shape with a diameter of 1.5 m and the inner walls are painted with vertical black and white stripes. The chair and the drum can be rotated separately or simultaneously at any desirable speed in both directions. The subject is sitting with the head exactly in the axis of rotation. The vestibular stimulus is determined by the movements of the chair, the optokinetic stimulus by the difference of the angular velocity of the drum and the chair. For the somatosensory-vestibular experiments from Bles, the chair was replaced by a bar construction as shown in Fig. 2A. The subject is then walking, and instructed to remain behind the bar held with his or her hands. This means that the vestibular stimulus is determined by the rotation of the bar. The somatosensory stimulation, the stepping velocity, is determined by the difference in angular velocity of the bar and the drum. If in this setup the light in the drum is switched on, the optokinetic stimulus is always congruent to the somatosensory stimulus, because the floor is coupled to the cylinder walls. 1
545 In Fig. 2, B and C, the main results are summarized of those studies on intersensory interactions that are relevant in the present context. By means of a magnitude estimation technique, Brandt et al. [7] determined the nauseogenic power of the Coriolis effect for different visuovestibular stimulus combinations in which the pure vestibular Coriolis effect served as a standard nauseogenic stimulus with a magnitude of 5; “nothing particular” was scored as 0. It is seen that congruent visuovestibular stimulation diminished the severity of the Coriolis effect considerably, whereas incongruent visuovestibular stimulation enhanced the effect (Fig. 2B).1 Similar differences were obtained with somatosensory-vestibular interactions. Here too, the effects were much smaller during congruent stimulation than during incongruent stimulation (Fig. 2C, closed circles). If the light in the drum was on in this last set of experiments, the differences were even more pronounced, illustrating that the natural condition with all sensory systems delivering congruent information caused almost no problem at all (Fig. 2C, open circles). Of particular interest is also that pure optokinetic stimulation (subject sitting in the stationary chair while the drum rotates and the light is on) or pure somatosensory stimulation (subject stepping “sur place” on the rotating floor of the drum behind the earthstationary bar in total darkness) results in a sensation of selfrotation, without any signs of motion sickness. However, head tilt in these stimulus conditions provoked Coriolis-like effects, which were called the optokinetic pseudo-Coriolis effect [7] and the somatosensory pseudo-Coriolis effect [1]. Most subjects experience these pseudo-Coriolis effects as less nauseating than the vestibular Coriolis effect. The observation that in the large To¨nnies drums motion sickness was absent in all the studies on pure optokinetic or somatosensory stimulation as performed in Freiburg or Amsterdam is an interesting finding in view of the reports in the literature that motion sickness can be elicited by pure optokinetic stimulation [see e.g. 17,31]. These differences need to be elaborated. As indicated already, Guedry [15] explained the Coriolis effect as the consequence of the conflict between the head tilt indicated by the otolith and neck receptors and the direction of the angular velocity vector as sensed by the canals. He had preferred that the optokinetic pseudo-Coriolis effect would have been called the pseudo-Purkinje effect instead, because the pseudo-Coriolis effect resembles more the Purkinje than the Coriolis effect: The optokinetically induced central vestibular angular velocity vector is head fixed and rotates together with the head during the head tilt (mimics Fig. 1C). This is true indeed, but care should be taken in what we mean with a Purkinje effect, because Purkinje [26] performed his experiments not with a rotating chair but by stepping around with the eyes open. In that case we are dealing with optokinetic and somatosensory aftereffects, which certainly play an important role [7,8,18]. We summarize the most relevant findings from this section as follows: ●
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The strength of the pure vestibular Coriolis effect may be modified by varying the canal response vector just before the head movement. If that vector mimics the physical motion, the nauseating effect due to the head movement is smallest. Pure optokinetic and pure somatosensory rotatory stimulation induces a sensation of self-rotation and is not accompanied with motion sickness symptoms. Head tilt during pure optokinetic and pure somatosensory rotatory stimulation results in an optokinetic, respectively, a somato-
The term incongruent visual-vestibular stimulation refers to the situation where the visual stimulus is not an earth-stationary surround.
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FIG. 3. Angular velocity response vectors. The response due to head tilt over 30°, after constant velocity rotation in the dark (A); immediately after angular acceleration up to that angular velocity (B); and at that velocity but immediately after an angular deceleration from twice that velocity (C). The central angular velocity response vector for the optokinetic or somatosensory pseudo-Coriolis effect is shown in D, the response vector after head tilt during constant velocity rotation with congruent visual or somatosensory motion information is shown in E, with incongruent motion information in F.
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sensory pseudo-Coriolis effect, which is qualitatively the same as the vestibular Coriolis effect. The strength of the vestibular Coriolis effect may be reduced by providing congruent optokinetic or somatosensory motion information and may be enforced by adding incongruent optokinetic or somatosensory motion information. Somatosensory-vestibular interactions show the same characteristics as visual-vestibular interactions. MODELLING OF CORIOLIS EFFECTS
Vector Analysis Guedry and Benson [16] provided a clear analysis of the stimulus consequences for the vestibular system in case of head tilt during rotation. In Fig. 3A, the response of the semicircular canals is shown again for the case of the pure vestibular Coriolis effect, immediately after a head tilt of 30°, just as in Fig. 1B. It is seen that the resulting angular velocity vector is about perpendicular to gravity. In Fig. 3B it is shown what happens if before the head tilt an angular velocity vector is already present (e.g., a canal response due to a just-started angular acceleration). Because this vector is head fixed, it adds to the angular velocity vectors from the vestibular Coriolis effect, and immediately after the head tilt the resultant vector is parallel to the gravity vector if the magnitude of the 2
vector equals the stimulus velocity, independent of f. Test subjects did not report any nausea in this condition. If the subject decelerated from a twice as large constant angular velocity just before the head tilt, there is again an angular velocity response vector present, indicating, however, a rotation into the opposite direction (cf. Fig. 1C). Adding this vector to the vector from Fig. 3A results in a large vector as depicted in Fig. 3C, definitely not aligned with gravity. In this condition the test subjects reported severe nausea from only one head movement. Based on this analysis, Guedry and Benson [16] argued that the magnitude of the Coriolis effect depends on the alignment of the resulting angular velocity response vector and the gravitoinertial force: the more they are aligned, the smaller the (nauseating) effect. The central angular velocity vector as present during pure optokinetic or pure somatosensory yaw-stimulation is, of course, aligned with gravity (cf. Fig. 1A). According to Guedry and Benson, the motion sickness incidence in this condition should be zero, in line with the experimental experience from Brandt (personal communication) and our own studies. Head tilt during pure optokinetic or somatosensory stimulation, however, rotates this vector over the tilt angle as shown in Fig. 3D, because the vector is head fixed (cf. the Purkinje effect in Fig. 1C). Consequently, the angular velocity vector and the gravitoinertial force are not aligned anymore, so motion sickness may be provoked by this manoever according to Guedry and Benson, as is the case indeed [1,7].2 If a subject is submitted to constant velocity rotation with full sight on the surroundings, the canals will not respond to the stimulus after a while, but in the central vestibular system an angular velocity vector will remain present as indicated above, evoked by the optokinetic stimulation. That implies that subsequent head tilt adds to this head-fixed vector the angular velocity vectors due to canal stimulation as a result of the head tilt (cf. the pure vestibular Coriolis effect; Fig. 1B). The result is a vector aligned with gravity as shown in Fig. 3E (cf. also Fig. 3B). Motion sickness should be minimal because the resulting angular velocity vector is aligned with gravity, which is true indeed according to the data as shown in Fig. 2. An angular velocity vector before the head tilt indicating rotation into the opposite direction (the drum rotates in the same direction as the chair but with twice the velocity) will result after the head tilt in an angular velocity vector as shown in Fig. 3F (cf. Fig. 3C). Because the vector is large and not at all aligned with gravity, motion sickness should be easily provoked in this condition, which is true indeed (cf. Fig. 2). A similar vector analysis holds for the somatosensory-vestibular interactions (Fig. 2), because those interactions mimic the visuovestibular interactions quite well [1,30]. The main conclusion from this vector analysis is that the statement of Guedry and Benson [16] is correct indeed: The more the gravitoinertial force vector is aligned with the resulting central vestibular angular velocity response vector after a head tilt during rotation, the smaller the nauseating effect. Furthermore, it is shown that this statement holds for all head tilts during all kinds of visual, somatosensory and vestibular rotatory stimulation about the z-axis (yaw). The Subjective Vertical Conflict Theory The findings as described above fit into the more generalized motion sickness model as proposed by Bles et al. [5]. They proposed a model that claims that motion sickness is only pro-
The angular response vector after the head tilt during optokinetic stimulation will soon align itself again with the axis of rotation, because the optokinetic stimulation continues around the vertical axis. Bringing the head back in the original upright position therefore does not reduce the nauseogenic effect caused by the head tilt but induces a new pseudo-Coriolis effect.
CORIOLIS EFFECTS
FIG. 4. Schematic model to construct the sensed vertical vsens, sensed translations tsens and sensed rotations rsens. It assumes that the low-pass filtered gravitoinertial acceleration signals, stemming from integration (INT) of the signals from otoliths (OTO) and the somatoreceptors (SOM), determine vsens. Semicircular canal information (SCC), integrated with additional visual and somatosensory rotatory motion information, helps to compensate for the high-frequency otolith stimuli during head tilt by a transformation (T) and inverse transformation (T 21 ). Visual frame information about horizontal and vertical structures in the surroundings also helps to establish vsens. Sensed translations are in principle the result of the interactions between the optokinetic (VIS) and somatosensory (SOM) linear motion information, the gravitoinertial force information and the output of T 21 .
voked if the subjective vertical, vsubj, as determined on previous experience differs from the sensed vertical, vsens, as determined on the basis of the incoming sensory information. The computation of vsens is proposed to take place according to the model as depicted in Fig. 4 [2]. It is assumed that low-pass filtering of the gravitoinertial force vector could preserve gravity, provided that angular motion information compensated for the consequences of head tilt [see also 12, 19, 20]. The angular motion information in this schematic model is the resulting information from the visual-vestibular-somatosensory interactions regarding angular motion detection as described in the previous sections. Similar multisensory interactions are also known for linear motion detection and are depicted in the model as well. How vsens depends on the visual frame remains to be determined in more detail, but for the moment we assume that the interaction takes place after the low-pass (LP) filter operation. In the present context this is of no particular concern, however. In a similar approach as propagated by Oman [22], Bles et al. [5] proposed an internal model with the same computational rules as described above to calculate the expected vertical, vexp. The difference between these vectors vsens and vexp serves to adjust vexp, which is then the actual subjective vertical, vsubj. It is this difference vector between vsens and vsubj that they proposed to be the input to the motion sickness generator [cf. 22]. For a detailed discussion on the similarities and differences between the subjective vertical (SV)-conflict model and the classic motion sickness models, reference is made to Bles et al. [5]. So the question is whether the SV-conflict motion sickness model also accounts for the data as described above. Internal Model Predictions Let us consider the consequences for vexp in the previous experiments. Basically, there are two possibilities.
547 1. If the subject perceives no motion, the internal model should predict that head tilt changes the components of the gravitoinertial force vector along the subject’s z- and y-axis. It should also expect a roll-canal response due to the head tilt (and a neck response as well) indicating, after integration, a roll-angle of equal magnitude as the tilt angle. The consequence of the transformation T is that the input signals to the LP filter are not altered. The output of the LP filter is then inversely transformed over the roll angle, keeping vexp aligned with gravity all the time during the head tilt. In other words, the internal model would predict that during a head tilt the expected vertical would remain aligned with gravity. 2. If the subject perceives the self-rotation correctly, the internal model assumes the presence of an angular velocity vector pointing along the z-axis, aligned with gravity. According to the model, this vector as such does not affect the direction of vexp (!). Subsequent head tilt would develop in a similar way to what has been described under 1. However, it would also expect a response of the yaw and pitch canals, resulting in an angular velocity response vector aligned with gravity, similar to what is depicted in Fig. 3B. This vector does not affect the direction or magnitude of the expected vertical according to the model of Fig. 4. So here too the foreseen angular velocity response vector would remain aligned with gravity during head tilt, and therefore no change of the expected vertical with respect to gravity is predicted. Therefore, the internal model would always compute the expected vertical to remain aligned with gravity during and after a head tilt, whether stationarity or rotation is assumed by the internal model. Sensory-Based Determination of the Vertical On the sensory side, the situation may be different. In those stimulus conditions described in the previous sections where the angular velocity vector after the head tilt is not aligned with gravity, the sensed vertical vsens will be affected. Because of the transformation T, which does not match the change of the otolith signals, the input signals of the LP filter change too rapidly to pass unperturbed, which means that the inverse transformation T 21 after the LP filter disturbs the alignment of vsens with gravity. Because vexp remains aligned with gravity according to the internal model, there is a difference between vsens and vexp, which triggers motion sickness according to the SV-conflict theory on motion sickness. This SV-conflict model would also predict that the difference vector between vexp and vsens is larger when the angle between the sensed angular velocity vector and the gravity increases. So this SV-conflict theory on motion sickness is in agreement with the experimental data as described above as well (cf. Figs. 2 and 3). The advantage over the claim from Guedry and Benson is that the SV-conflict theory also describes the occurrence of motion sickness in situations where no angular motion is present [5]. DISCUSSION AND CONCLUSION The previous analyses have shown that the conclusion from Guedry and Benson that motion sickness decreases the more the resulting angular velocity response vector is aligned with the gravitoinertial force vector is in agreement with the SV-conflict theory. This is based on the analysis that showed that the internal model always expects the subjective vertical to be aligned with the gravity vector during head movements, whether one assumes that one rotates or that one is stationary. It is also obvious from the previous analysis that one should not
548 neglect the contribution of somatosensory motion and position information in determining spatial orientation and computing the chance on, and the severity of, motion sickness. There is ample evidence for a substantial contribution of the somatosensory system in enhancing or suppressing motion sickness. Moreover, it is shown that the somatosensory system contributes in a controlled way. The contributions are not merely disturbing and misleading, as stated by the early investigators in this field [11,26]. However, they should be dealt with in a logical manner. In some VE applications with standing subjects [e.g. 27], the somatosensory information of the feet is twofold: For displacements over a small distance, the information counts, and for larger displacements, it does not. This creates problems for the internal model that could be alleviated if a transport medium would be defined and made visible to the subject. Further research on this topic is recommended. Especially for this approach, the SV-conflict model on motion sickness may be a useful tool, because VE applications involve mostly also linear motion, which can be dealt with appropriately. In the vector analysis as shown in the previous sections, much depends on the transfer characteristics of the sensory systems. For instance, if the yaw-response vector due to vestibular, somatosensory or optokinetic stimulation has not the appropriate magnitude, the resulting angular velocity response vector after the head tilt may not be aligned exactly with gravity, and some Coriolis effect might be noticed. It is also known that the vectors as induced by the various sensory modalities have different weight factors, which may also affect the result of the vector addition [25]. Moreover, one should take into account that weight factors can be adapted by training to obtain the best strategies to meet specific stimulus conditions (as observed in e.g. ballet dancers or fighter pilots) or to compensate for malfunctioning of one of the contributing sensory systems [3,13,23]. Inappropriate weighting is also possible: the individual responses of motion sickness-susceptible student pilots on the so-called Intersensory Coriolis Stress Test, a test series of Coriolis effects in different combinations of sensory motion information, related to the severity of motion sickness experienced during elementary flight training [4]. During excentric rotation, additional problems arise because the equilibrium system is willing to accept the gravitoinertial force vector as gravity, resulting in a tilt sensation when the centripetal force is directed along the subject’s y-axis in a centrifuge with a fixed gondola [14]. In a centrifuge with a free-swinging gondola, the subject experiences the gondola oriented horizontally during a constant G-load. This is in accordance with the model of Fig. 4. If the centrifuge is brought to a stop, however, many people experience tumbling sensations and nausea, much more as encountered at the start of the ride. It is not unlikely that the new subjective vertical is part of these problems, because the problems are less if the subject is provided with a visual stimulus with information about his or her actual attitude. The fact that in motor races the motorcyclists keep their head upright aligned with gravity, even when the motor is almost horizontal during a turn, must have an advantage. Apparently it is easier in that case to use the visual information to keep a correct spatial orientation about what is horizontal and to suppress the horizontal vestibular nystagmus by visual fixation (horizontal nystagmus is more easily suppressed than vertical nystagmus). In view of the scheme of Fig. 4, this would be the most elegant solution, because aftereffects from the semicircular canals are restricted to the yaw-canals that do not affect the direction of the sensed vertical. The observation that fighter pilots also tend to align their head to gravity during a turn is probably based on the same strategy [24]. Further research about the exact influence of visual horizontal and vertical structures upon the vestibular signal processing in determining the subjective
BLES vertical (see Fig. 4) is required, certainly in view of the requirements for the design of centrifuge based flight simulators. In conclusion, it has been shown that the SV-conflict theory on motion sickness is able to explain when head movements during vestibular, visual and/or somatosensory rotatory motion stimulation are nauseating and when not. For VE applications and other simulators, this means that it is possible to analyse the conditions to be simulated at forehand and restrict the simulation to those conditions where mismatches in the determination of the subjective vertical are avoided. This will lower the incidence of simulator sickness.
REFERENCES 1. Bles, W. Stepping around: circular vection and coriolis effects. In: Long, J.; Baddeley, A., eds. Attention and performance IX. Hillsdale, NJ: Lawrence Erlbaum Assoc.; 1981. 2. Bles, W.; Bos, J. E. Een ruimtelijk orientatie model. TNO report 1994 A-58. TNO Human Factors Research Institute, Soesterberg, The Netherlands; 1994. 3. Bles, W.; De Jong, J. M. B. V.; Wit, G. Somatosensory compensation for loss of labyrinthine function. Acta Otolaryngol. Stockh. 97:213– 221; 1984. 4. Bles, W.; De Graaf, B.; Bos, J. E. Vestibular examination in pilots susceptible to motion sickness. AGARD Conference Proceedings: the clinical basis for aeromedical decision making. CP-553:15/1–15/8; 1994. 5. Bles, W.; Bos, J. E.; De Graaf, B.; Groen, E.; Wertheim, A. H. Motion sickness: Only one provocative conflict? Brain Res. Bull. 47:481– 487; 1999. 6. Brandt, Th.; Bu¨chele, W.; Arnold, F. Arthrokinetic nystagmus and ego-motion sensation. Exp. Brain Res. 30:331–338; 1977. 7. Brandt, Th.; Wist, E.; Dichgans, J. Optisch induzierte PseudocoriolisEffekten und Circularvektion. Arch. Psych. Nervenkrank. 214:365– 389; 1971. 8. Correia, M. J.; Nelson, J. B.; Guedry, F. E. Antisomatogyral illusion. Aviat. Space Environm. Med. 48:859 – 862; 1977. 9. Dichgans, J.; Brandt, Th. Visual-vestibular interaction: effects on self-motion perception and postural control. In: Held, R.; Leibowitz, H. W.; Teuber, H. L. eds. Handbook of sensory physiology. Vol. VIII. Berlin: Springer-Verlag; 1978. 10. van Egmond, A. A. J.; Groen, J. J.; Jongkees, L. B. W. The mechanics of the semicircular canals. J. Physiol. Lond. 110:1–17; 1949. 11. Fischer, M. H.; Wodak, E. Beitra¨ge zur Physiologie des menslichen Vestibularapparatus. I. Die vestibula¨ren Ko¨rperreflexe und die Fallreaktion. Pflu¨gers Arch. Physiol. 202:523–552; 1924. 12. Glasauer, S. Das Zusammenspiel von Otolithen und Bogenga¨ngen im Wirkungsgefu¨ge der subjektiven Vertikale. Ph.D. Thesis Technische Universita¨t Mu¨nchen, Germany; 1992. 13. De Graaf, B.; Bos, J. E.; Bles, W. Longitudinal investigation for vestibular adaptation by aviators: interim report (in Dutch). Report TM-97-A017, TNO Human Factors Research Institute, Soesterberg, The Netherlands; 1997. 14. Graybiel, A. Measurement of otolith function in man. In: Kornhuber, H. H., ed. Handbook of sensory physiology. VI/2. New York: Springer; 1974:233–266. 15. Guedry, F. E. Psychophysics of vestibular sensation. In: Kornhuber, H. H., ed. Handbook of sensory physiology. Vol. VI/2. Berlin: Springer-Verlag; 1974:3–154. 16. Guedry, F. E.; Benson, A. J. Coriolis cross-coupling effects: disorienting and nauseogenic or not? Aviat. Space Environ. Med. 49:29 –35; 1978. 17. Hu, S.; Stern, R. M.; Vasey, M. W.; Koch, K. L. Motion sickness and gastric myoelectric activity as a function of speed of rotation of a circular vection drum. Aviat. Space Environ. Med. 60:411– 414; 1989. 18. Kapteyn, T. S.; Bles, W. Circular vection and human posture. III. Relation between the reactions to different stimuli. Agressologie 18: 335–339; 1977. 19. Mayne, R. A systems concept of the vestibular organs. In: Kornhuber,
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20. 21. 22. 23.
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H. H., ed. Handbook of sensory physiology. VI/2. New York: Springer-Verlag; 1974:493–580. Merfeld, D. M.; Young, L.; Oman, C.; Shelhamer, M. A multidimensional model of the effect of gravity on the spatial orientation of the monkey. J. Vest. Res. 3:141–161; 1993. Mittelstaedt, H. Kybernetische Analyse von Orientierungsleistungen. In: Hauske, G.; Butenandt, E., eds. Kybernetik 1977. Mu¨nchen: R. Oldenbourg Verlag; 1978:144 –195. Oman, C. M. A heuristic mathematical model for the dynamics of sensory conflict and motion sickness. Acta. Oto laryngol. Suppl. 392; 1982. Parker, D. E.; Reschke, M. F.; Arrott, A. P.; Homick, J. L.; Lichtenberg, B. K. Otolith tilt-translation reinterpretation following prolonged weightlessness: implications for preflight training. Aviat. Space Environ. Med. 56:601– 606; 1985. Patterson, F. R. Aviation spatial orientation in relationship to head position and attitude interpretation. Ph.D. Thesis, Wright State University; 1995. Probst, Th.; Straube, A.; Bles, W. Differential effects of ambivalent visual-vestibular-somatosensory stimulation on the perception of selfmotion. Behav. Brain Res. 16:71–79; 1985.
549 26. Purkinje, J. E. Beitra¨ge zur na¨heren Kenntnis des Schwindels aus heautognostischen Daten. Med. Jb. (Oesterreich) 6:79 –125; 1820. 27. Regan, E. C.; Price, K. R. The frequency of occurrence and severity of side-effects of immersion virtual reality. Aviat. Space Environ. Med. 65:527–530; 1994. 28. Scho¨ne, H. Orientierung im Raum. Stuttgart: Wissenschaftliche Verlagsgesellschaft; 1980. 29. Schubert, G. Die Physiologischen Auswirkungen der Coriolisbeschleunigungen bei Flugzeugsteuerung. Arch. Ohr., Nas., Kehlk. Heilk. 30, 595– 604; 1932. 30. Solomon, D.; Cohen, B. Stabilization of gaze during circular locomotion in darkness. II. Contribution of velocity storage to compensatory eye and head nystagmus in the running monkey. J. Neurophysiol. 67:1158 –1170; 1992. 31. Stern, R. M.; Hu, S.; Anderson, R. B.; Leibowitz, H. W.; Koch, K. L. The effects of fixation and restricted visual field on vection-induced motion sickness. Aviat. Space Environ. Med. 61:712–715; 1990. 32. Waespe, W.; Henn, V. Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation. Exp. Brain Res. 27:523–538; 1977.
PII S0361-9230(98)00017-3
Coriolis effects and motion sickness modelling Willem Bles* TNO Human Factors Research Institute, Soesterberg, The Netherlands [Received 10 January 1998; Accepted 28 April 1998] ABSTRACT: Coriolis effects are notorious in relation to disorientation and motion sickness in aircrew. A review is provided of experimental data on these Coriolis effects, including the modulatory effects of adding visual or somatosensory rotatory motion information. A vector analysis of the consequences of head movements during somatosensory, visual and/or vestibular rotatory motion stimulation revealed that the more the sensed angular velocity vector after the head movements is aligned with the gravitoinertial force vector, the less nauseating effects are experienced. It is demonstrated that this is a special case of the subjective vertical conflict theory on motion sickness that assumes that motion sickness may be provoked if a discrepancy is detected between the subjective vertical and the sensed vertical as determined on the basis of incoming sensory information. © 1999 Elsevier Science Inc.
an immersion easily provokes motion sickness symptoms [27]. One reason is that the visual and proprioceptive motion information is necessarily incongruent because of inevitable time delays for computing the appropriate visual stimuli during fast head movements. But it is also feasible that in particular applications the subject is confronted with inappropriate proprioceptive motion information, which may contribute to the induction of motion sickness as well. For instance, to look around and to displace oneself in VE, the subject may move his or her head, turn and walk around on a little area, which keeps the incoming sensory information from the visual, the vestibular and the somatosensory system in agreement with each other (apart from the mentioned time delays in case of abrupt movements). If, however, larger displacements are required than the head position tracker system allows, a space mouse may be used by the subject to move through the visual surroundings. In that case, the proprioceptive motion information does not match the visual motion information anymore, because the subject is not moving his or her legs and the vestibular system does not sense motion. Consequently, during immersion in VE the visual and proprioceptive motion information is intermittently in conflict with one another. It is not obvious that the system can handle that situation without any problems, certainly not when head movements are involved as well. In VE experiments it is difficult to isolate the contribution of this particular aspect to the provoked motion sickness, but from other laboratory experiments it is known that somatosensory angular motion information interacts with vestibular and visual angular motion information during standing or walking around. The somatosensory angular motion information often determines not only the magnitude of the final motion percept but also the direction [6,8, 18]. If we define the Coriolis effect as the disorienting and nauseating feelings associated with head tilt during constant velocity rotation, the strength of these Coriolis effects is also considerably enhanced or diminished in a systematic way due to these interactions. This is true both for visual-vestibular interactions [7] and for somatosensory-vestibular interactions [1]. A motion sickness theory has been proposed hypothesizing that there is virtually only one conflict that provokes motion sickness, the conflict concerning the subjective vertical [5]. It is worthwhile to analyse the abovementioned interactions in the Coriolis effects in more detail to determine whether the hypothesis of only one single sensory conflict underlying motion sickness can be maintained or not. If the hypothesis can be maintained, a more quantitative approach on the motion sickness problems is possible. This
KEY WORDS: Locomotion, Motion sickness, Coriolis effects, Modelling, Subjective vertical.
INTRODUCTION When humans and animals walk around in their normal habitat, motion sickness does not occur. If we define locomotion as the natural way to move around (for humans this means primarily walking), then the somatoreceptors dealing with locomotion are important contributors to the equilibrium system to maintain a proper spatial orientation, just as vision and the vestibular system [21,28]. It has been argued that these sensory systems are complementary to each other to guarantee optimal motion and position information over the whole frequency range of the natural movements. However, in the daily life of humans today, locomotion is not the only way to move around. Many transport means are available, often causing stimulation of the sensory systems out of their normal stimulus range, which may lead to incongruent motion information between the different senses. There are various examples of transport means where the somatosensory motion information is not congruent with either the visual or the vestibular motion information. For instance, the equilibrium system of people standing on an escalator or walking on a rolling carpet is confronted with differences in somatosensory motion information about the walking speed and optokinetic surround velocity. Interestingly, these discrepancies do not seem to bother people in terms of spatial orientation or motion sickness, but it is true of course that the time spent on these devices is only short. Incongruent somatosensory and visual motion information is also present during immersion in a virtual environment (VE). Such
* Address for correspondence: Dr. Willem Bles, TNO Human Factors Research Institute, P.O. Box 23, 3769 ZG Soesterberg, The Netherlands. Fax: (31)346 353 977; E-mail: [email protected]
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FIG. 1. Central vestibular angular velocity responses for different stimulus conditions. (A) Response vector due to stimulation of the semicircular yaw-canal, optokinetic and/or somatosensory yaw motion stimulation. (B) Response vectors immediately after a 30° head tilt during constant velocity rotation in darkness, the Coriolis effect. (C) Response vector immediately after a 30° head tilt after a sudden stop from constant velocity rotation, the Purkinje effect.
would be a favorable situation in view of the growing role of VE applications and other simulators in every day life. In the following paragraphs, therefore, some basic experiments on angular self-motion and Coriolis effects are analysed. These experiments are based on paradigms frequently used in research on visual-vestibular and somatosensory-vestibular interactions, which are well documented in the literature. A subsequent vector analysis reveals the common underlying mechanism, which is shown to fit the proposed model on motion sickness. In the Discussion, the consequences of this approach are elaborated, and an approach is suggested to analyse VE conditions on their provocativeness of motion sickness. EXPERIMENTAL DATA AND VECTOR PRESENTATION Angular Motion Perception An angular motion percept, rotation around the z-axis, may be induced by stimulation of the appropriate sensory systems, apart or in combination. Examples of stimuli are acceleration of a rotating chair in darkness (stimulation of the semicircular canals; e.g. [15]), rotation of the visual surroundings (optokinetic stimulation; [9]) and stepping around on a counterrotating platform in darkness (somatosensory stimulation; [1]). The development of the percept in time depends on the applied stimulus and the transfer characteristics of the sensory systems involved. For instance, if a subject is sitting on a chair in total darkness, which is rotated with a trapezoidal velocity profile around the z-axis (yaw-axis rotation; angular acceleration and deceleration 1 rad/s2, maximum velocity v1 5 1 rad/s), the subject will experience an increasing angular velocity during the acceleration phase. This percept fades away after the chair has reached the constant velocity plateau. Constant velocity rotation as such is not sensed by the vestibular system. In the deceleration phase, the subject experiences an increasing angular velocity in the opposite direction, which fades out after the chair has come to a stop. This is a consequence of the second-order system dynamics of the semicircular canals [10]. For the vector in Fig. 1A, it means that the magnitude and the direction may vary, depending on the stimulus characteristics. But the vector is always parallel to the gravity vector. Optokinetically induced sensation of rotation, the so-called
circular vection, has different characteristics [9]. Rotation of the visual surroundings with the same trapezoidal velocity profile will only after a few seconds lead to a sensation of self-rotation with increasing velocity in the opposite direction. After a few more seconds, the induced speed saturates and a constant velocity selfmotion percept remains, whereas the stimulus is perceived as stationary. When the light is switched off, the angular motion percept fades away. Similar observations have been made for somatosensory stimulation, like the apparent stepping in circles in darkness on a counterrotating platform [1]. Neurophysiologic studies in animals showed that second-order neurons in the vestibular nuclei exhibit a direction specific modulation of resting discharge evoked either by body acceleration, optokinetic stimulation [32] or somatosensory stimulation [30]. Combination of the different sensory cues reduces the shortcomings of each transfer characteristic alone (i.e., the poor vestibular response at low frequencies and the poor visual and somatosensory performance at high frequencies). So congruent visual, vestibular and somatosensory stimulation results in a function that accurately transfers velocity information over the whole frequency range of interest for normal every-day motion (up to 1 Hz). The point of interest here is that the different sensory systems all contribute to create in the central vestibular system only one neural discharge pattern, which is the equivalent of an angular velocity vector. Coriolis and Purkinje Effects It is obvious that head tilt on the shoulder over an angle fx of 30° during constant velocity rotation at 1 rad/s in the dark has consequences for the stimulation of the semicircular canals. If we assume that we are dealing with an idealised canal system, a “yaw” canal lying in the head-fixed xy-plane, a “pitch” canal in the xz-plane and a “roll” canal in the yz-plane, sensing rotation about the z-, y- and x-axis, respectively, nothing special happens to the roll-canal other than rotation over the tilt angle fx. Because this is a shortlasting high-frequency stimulus, the response follows the stimulus adequately and at the end of the tilt manoeuver there is no aftereffect, the roll-canal signals no rotation anymore. However, the yaw-canal loses angular momentum and the pitch-canal gains angular momentum proportional to cosf21 (5 20.13) and sin f (5 0.5) respectively [see for details 15,16]. The resulting response vector, together with the angular velocity vectors signalled by the contributing semicircular canals after completion of the head tilt, are depicted in Fig. 1B. The subject indeed experiences a sensation of pitch rotation, in agreement with the resultant vector, but this percept is also often accompanied by signs of nausea [15]. This kind of vestibular stimulation, together with its perceptual and nauseating consequences, is referred to as the Coriolis effect [29]. Guedry explains the Coriolis effect as the consequence of the conflict between the head tilt indicated by the otolith and neck receptors and the direction of the angular velocity vector as sensed by the canals. If a subject rotating in darkness at constant velocity is brought to a sudden stop and immediately thereafter tilts his or her head, he or she will experience a Coriolis-like effect, be it of less intensity. This effect was named Purkinje effect, because Purkinje first described this sort of experiment [26]. The resulting angular velocity response vector after the head tilt is different from the Coriolis effect: Only the head-fixed response vector of the yawcanal due to the stop remains (see Fig. 1C) [15]. Guedry and Benson [16] showed that it was possible to modulate the magnitude of the vestibular Coriolis effect by applying different accelerative stimuli to the horizontal semicircular canals before the head tilt. They had their subjects tilt the head always
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FIG. 2. (A) The experimental setup for studying somatosensory-vestibular interactions (Dichgans and Brandt had for their studies on visual-vestibular interactions the bar replaced by a rotating chair). (B and C) Effects of head tilt on the magnitude of the nauseating Coriolis effect as determined for visual-vestibular [7] and for somatosensory-vestibular and somatosensoryvisual-vestibular interactions [1]. The arrows in the conditions represent the magnitude of the angular velocities of the chair and the drum in condition B and of the bar and the drum in condition C.
when the chair had a specific angular velocity. If the head was tilted during the acceleration phase (so when a motion percept was present that corresponded to the actual motion stimulus before the head tilt), the Coriolis effect was significantly diminished. However, it was significantly enhanced when before the head tilt a deceleration took place from a twice as large angular rotation velocity (in that case the velocity percept was of equal magnitude but in the opposite direction before the head tilt). In summarizing the relevant results of this section, one should notice that the Coriolis and Purkinje effects are qualitatively the same and that the magnitude of the Coriolis effect can be influenced by additional stimulation of the semicircular canals before the head tilt. Pseudo-Coriolis Effects The studies from Dichgans and Brandt [9] on visual-vestibular interactions and those from Bles [1] on somatosensory-vestibular interactions were both performed with the same instrument, a concentric rotating chair and drum combination (To¨nnies, Freiburg im Breisgau). This device is described in more detail to facilitate understanding of the experimental paradigm. The drum has a cylindrical shape with a diameter of 1.5 m and the inner walls are painted with vertical black and white stripes. The chair and the drum can be rotated separately or simultaneously at any desirable speed in both directions. The subject is sitting with the head exactly in the axis of rotation. The vestibular stimulus is determined by the movements of the chair, the optokinetic stimulus by the difference of the angular velocity of the drum and the chair. For the somatosensory-vestibular experiments from Bles, the chair was replaced by a bar construction as shown in Fig. 2A. The subject is then walking, and instructed to remain behind the bar held with his or her hands. This means that the vestibular stimulus is determined by the rotation of the bar. The somatosensory stimulation, the stepping velocity, is determined by the difference in angular velocity of the bar and the drum. If in this setup the light in the drum is switched on, the optokinetic stimulus is always congruent to the somatosensory stimulus, because the floor is coupled to the cylinder walls. 1
545 In Fig. 2, B and C, the main results are summarized of those studies on intersensory interactions that are relevant in the present context. By means of a magnitude estimation technique, Brandt et al. [7] determined the nauseogenic power of the Coriolis effect for different visuovestibular stimulus combinations in which the pure vestibular Coriolis effect served as a standard nauseogenic stimulus with a magnitude of 5; “nothing particular” was scored as 0. It is seen that congruent visuovestibular stimulation diminished the severity of the Coriolis effect considerably, whereas incongruent visuovestibular stimulation enhanced the effect (Fig. 2B).1 Similar differences were obtained with somatosensory-vestibular interactions. Here too, the effects were much smaller during congruent stimulation than during incongruent stimulation (Fig. 2C, closed circles). If the light in the drum was on in this last set of experiments, the differences were even more pronounced, illustrating that the natural condition with all sensory systems delivering congruent information caused almost no problem at all (Fig. 2C, open circles). Of particular interest is also that pure optokinetic stimulation (subject sitting in the stationary chair while the drum rotates and the light is on) or pure somatosensory stimulation (subject stepping “sur place” on the rotating floor of the drum behind the earthstationary bar in total darkness) results in a sensation of selfrotation, without any signs of motion sickness. However, head tilt in these stimulus conditions provoked Coriolis-like effects, which were called the optokinetic pseudo-Coriolis effect [7] and the somatosensory pseudo-Coriolis effect [1]. Most subjects experience these pseudo-Coriolis effects as less nauseating than the vestibular Coriolis effect. The observation that in the large To¨nnies drums motion sickness was absent in all the studies on pure optokinetic or somatosensory stimulation as performed in Freiburg or Amsterdam is an interesting finding in view of the reports in the literature that motion sickness can be elicited by pure optokinetic stimulation [see e.g. 17,31]. These differences need to be elaborated. As indicated already, Guedry [15] explained the Coriolis effect as the consequence of the conflict between the head tilt indicated by the otolith and neck receptors and the direction of the angular velocity vector as sensed by the canals. He had preferred that the optokinetic pseudo-Coriolis effect would have been called the pseudo-Purkinje effect instead, because the pseudo-Coriolis effect resembles more the Purkinje than the Coriolis effect: The optokinetically induced central vestibular angular velocity vector is head fixed and rotates together with the head during the head tilt (mimics Fig. 1C). This is true indeed, but care should be taken in what we mean with a Purkinje effect, because Purkinje [26] performed his experiments not with a rotating chair but by stepping around with the eyes open. In that case we are dealing with optokinetic and somatosensory aftereffects, which certainly play an important role [7,8,18]. We summarize the most relevant findings from this section as follows: ●
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The strength of the pure vestibular Coriolis effect may be modified by varying the canal response vector just before the head movement. If that vector mimics the physical motion, the nauseating effect due to the head movement is smallest. Pure optokinetic and pure somatosensory rotatory stimulation induces a sensation of self-rotation and is not accompanied with motion sickness symptoms. Head tilt during pure optokinetic and pure somatosensory rotatory stimulation results in an optokinetic, respectively, a somato-
The term incongruent visual-vestibular stimulation refers to the situation where the visual stimulus is not an earth-stationary surround.
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FIG. 3. Angular velocity response vectors. The response due to head tilt over 30°, after constant velocity rotation in the dark (A); immediately after angular acceleration up to that angular velocity (B); and at that velocity but immediately after an angular deceleration from twice that velocity (C). The central angular velocity response vector for the optokinetic or somatosensory pseudo-Coriolis effect is shown in D, the response vector after head tilt during constant velocity rotation with congruent visual or somatosensory motion information is shown in E, with incongruent motion information in F.
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sensory pseudo-Coriolis effect, which is qualitatively the same as the vestibular Coriolis effect. The strength of the vestibular Coriolis effect may be reduced by providing congruent optokinetic or somatosensory motion information and may be enforced by adding incongruent optokinetic or somatosensory motion information. Somatosensory-vestibular interactions show the same characteristics as visual-vestibular interactions. MODELLING OF CORIOLIS EFFECTS
Vector Analysis Guedry and Benson [16] provided a clear analysis of the stimulus consequences for the vestibular system in case of head tilt during rotation. In Fig. 3A, the response of the semicircular canals is shown again for the case of the pure vestibular Coriolis effect, immediately after a head tilt of 30°, just as in Fig. 1B. It is seen that the resulting angular velocity vector is about perpendicular to gravity. In Fig. 3B it is shown what happens if before the head tilt an angular velocity vector is already present (e.g., a canal response due to a just-started angular acceleration). Because this vector is head fixed, it adds to the angular velocity vectors from the vestibular Coriolis effect, and immediately after the head tilt the resultant vector is parallel to the gravity vector if the magnitude of the 2
vector equals the stimulus velocity, independent of f. Test subjects did not report any nausea in this condition. If the subject decelerated from a twice as large constant angular velocity just before the head tilt, there is again an angular velocity response vector present, indicating, however, a rotation into the opposite direction (cf. Fig. 1C). Adding this vector to the vector from Fig. 3A results in a large vector as depicted in Fig. 3C, definitely not aligned with gravity. In this condition the test subjects reported severe nausea from only one head movement. Based on this analysis, Guedry and Benson [16] argued that the magnitude of the Coriolis effect depends on the alignment of the resulting angular velocity response vector and the gravitoinertial force: the more they are aligned, the smaller the (nauseating) effect. The central angular velocity vector as present during pure optokinetic or pure somatosensory yaw-stimulation is, of course, aligned with gravity (cf. Fig. 1A). According to Guedry and Benson, the motion sickness incidence in this condition should be zero, in line with the experimental experience from Brandt (personal communication) and our own studies. Head tilt during pure optokinetic or somatosensory stimulation, however, rotates this vector over the tilt angle as shown in Fig. 3D, because the vector is head fixed (cf. the Purkinje effect in Fig. 1C). Consequently, the angular velocity vector and the gravitoinertial force are not aligned anymore, so motion sickness may be provoked by this manoever according to Guedry and Benson, as is the case indeed [1,7].2 If a subject is submitted to constant velocity rotation with full sight on the surroundings, the canals will not respond to the stimulus after a while, but in the central vestibular system an angular velocity vector will remain present as indicated above, evoked by the optokinetic stimulation. That implies that subsequent head tilt adds to this head-fixed vector the angular velocity vectors due to canal stimulation as a result of the head tilt (cf. the pure vestibular Coriolis effect; Fig. 1B). The result is a vector aligned with gravity as shown in Fig. 3E (cf. also Fig. 3B). Motion sickness should be minimal because the resulting angular velocity vector is aligned with gravity, which is true indeed according to the data as shown in Fig. 2. An angular velocity vector before the head tilt indicating rotation into the opposite direction (the drum rotates in the same direction as the chair but with twice the velocity) will result after the head tilt in an angular velocity vector as shown in Fig. 3F (cf. Fig. 3C). Because the vector is large and not at all aligned with gravity, motion sickness should be easily provoked in this condition, which is true indeed (cf. Fig. 2). A similar vector analysis holds for the somatosensory-vestibular interactions (Fig. 2), because those interactions mimic the visuovestibular interactions quite well [1,30]. The main conclusion from this vector analysis is that the statement of Guedry and Benson [16] is correct indeed: The more the gravitoinertial force vector is aligned with the resulting central vestibular angular velocity response vector after a head tilt during rotation, the smaller the nauseating effect. Furthermore, it is shown that this statement holds for all head tilts during all kinds of visual, somatosensory and vestibular rotatory stimulation about the z-axis (yaw). The Subjective Vertical Conflict Theory The findings as described above fit into the more generalized motion sickness model as proposed by Bles et al. [5]. They proposed a model that claims that motion sickness is only pro-
The angular response vector after the head tilt during optokinetic stimulation will soon align itself again with the axis of rotation, because the optokinetic stimulation continues around the vertical axis. Bringing the head back in the original upright position therefore does not reduce the nauseogenic effect caused by the head tilt but induces a new pseudo-Coriolis effect.
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FIG. 4. Schematic model to construct the sensed vertical vsens, sensed translations tsens and sensed rotations rsens. It assumes that the low-pass filtered gravitoinertial acceleration signals, stemming from integration (INT) of the signals from otoliths (OTO) and the somatoreceptors (SOM), determine vsens. Semicircular canal information (SCC), integrated with additional visual and somatosensory rotatory motion information, helps to compensate for the high-frequency otolith stimuli during head tilt by a transformation (T) and inverse transformation (T 21 ). Visual frame information about horizontal and vertical structures in the surroundings also helps to establish vsens. Sensed translations are in principle the result of the interactions between the optokinetic (VIS) and somatosensory (SOM) linear motion information, the gravitoinertial force information and the output of T 21 .
voked if the subjective vertical, vsubj, as determined on previous experience differs from the sensed vertical, vsens, as determined on the basis of the incoming sensory information. The computation of vsens is proposed to take place according to the model as depicted in Fig. 4 [2]. It is assumed that low-pass filtering of the gravitoinertial force vector could preserve gravity, provided that angular motion information compensated for the consequences of head tilt [see also 12, 19, 20]. The angular motion information in this schematic model is the resulting information from the visual-vestibular-somatosensory interactions regarding angular motion detection as described in the previous sections. Similar multisensory interactions are also known for linear motion detection and are depicted in the model as well. How vsens depends on the visual frame remains to be determined in more detail, but for the moment we assume that the interaction takes place after the low-pass (LP) filter operation. In the present context this is of no particular concern, however. In a similar approach as propagated by Oman [22], Bles et al. [5] proposed an internal model with the same computational rules as described above to calculate the expected vertical, vexp. The difference between these vectors vsens and vexp serves to adjust vexp, which is then the actual subjective vertical, vsubj. It is this difference vector between vsens and vsubj that they proposed to be the input to the motion sickness generator [cf. 22]. For a detailed discussion on the similarities and differences between the subjective vertical (SV)-conflict model and the classic motion sickness models, reference is made to Bles et al. [5]. So the question is whether the SV-conflict motion sickness model also accounts for the data as described above. Internal Model Predictions Let us consider the consequences for vexp in the previous experiments. Basically, there are two possibilities.
547 1. If the subject perceives no motion, the internal model should predict that head tilt changes the components of the gravitoinertial force vector along the subject’s z- and y-axis. It should also expect a roll-canal response due to the head tilt (and a neck response as well) indicating, after integration, a roll-angle of equal magnitude as the tilt angle. The consequence of the transformation T is that the input signals to the LP filter are not altered. The output of the LP filter is then inversely transformed over the roll angle, keeping vexp aligned with gravity all the time during the head tilt. In other words, the internal model would predict that during a head tilt the expected vertical would remain aligned with gravity. 2. If the subject perceives the self-rotation correctly, the internal model assumes the presence of an angular velocity vector pointing along the z-axis, aligned with gravity. According to the model, this vector as such does not affect the direction of vexp (!). Subsequent head tilt would develop in a similar way to what has been described under 1. However, it would also expect a response of the yaw and pitch canals, resulting in an angular velocity response vector aligned with gravity, similar to what is depicted in Fig. 3B. This vector does not affect the direction or magnitude of the expected vertical according to the model of Fig. 4. So here too the foreseen angular velocity response vector would remain aligned with gravity during head tilt, and therefore no change of the expected vertical with respect to gravity is predicted. Therefore, the internal model would always compute the expected vertical to remain aligned with gravity during and after a head tilt, whether stationarity or rotation is assumed by the internal model. Sensory-Based Determination of the Vertical On the sensory side, the situation may be different. In those stimulus conditions described in the previous sections where the angular velocity vector after the head tilt is not aligned with gravity, the sensed vertical vsens will be affected. Because of the transformation T, which does not match the change of the otolith signals, the input signals of the LP filter change too rapidly to pass unperturbed, which means that the inverse transformation T 21 after the LP filter disturbs the alignment of vsens with gravity. Because vexp remains aligned with gravity according to the internal model, there is a difference between vsens and vexp, which triggers motion sickness according to the SV-conflict theory on motion sickness. This SV-conflict model would also predict that the difference vector between vexp and vsens is larger when the angle between the sensed angular velocity vector and the gravity increases. So this SV-conflict theory on motion sickness is in agreement with the experimental data as described above as well (cf. Figs. 2 and 3). The advantage over the claim from Guedry and Benson is that the SV-conflict theory also describes the occurrence of motion sickness in situations where no angular motion is present [5]. DISCUSSION AND CONCLUSION The previous analyses have shown that the conclusion from Guedry and Benson that motion sickness decreases the more the resulting angular velocity response vector is aligned with the gravitoinertial force vector is in agreement with the SV-conflict theory. This is based on the analysis that showed that the internal model always expects the subjective vertical to be aligned with the gravity vector during head movements, whether one assumes that one rotates or that one is stationary. It is also obvious from the previous analysis that one should not
548 neglect the contribution of somatosensory motion and position information in determining spatial orientation and computing the chance on, and the severity of, motion sickness. There is ample evidence for a substantial contribution of the somatosensory system in enhancing or suppressing motion sickness. Moreover, it is shown that the somatosensory system contributes in a controlled way. The contributions are not merely disturbing and misleading, as stated by the early investigators in this field [11,26]. However, they should be dealt with in a logical manner. In some VE applications with standing subjects [e.g. 27], the somatosensory information of the feet is twofold: For displacements over a small distance, the information counts, and for larger displacements, it does not. This creates problems for the internal model that could be alleviated if a transport medium would be defined and made visible to the subject. Further research on this topic is recommended. Especially for this approach, the SV-conflict model on motion sickness may be a useful tool, because VE applications involve mostly also linear motion, which can be dealt with appropriately. In the vector analysis as shown in the previous sections, much depends on the transfer characteristics of the sensory systems. For instance, if the yaw-response vector due to vestibular, somatosensory or optokinetic stimulation has not the appropriate magnitude, the resulting angular velocity response vector after the head tilt may not be aligned exactly with gravity, and some Coriolis effect might be noticed. It is also known that the vectors as induced by the various sensory modalities have different weight factors, which may also affect the result of the vector addition [25]. Moreover, one should take into account that weight factors can be adapted by training to obtain the best strategies to meet specific stimulus conditions (as observed in e.g. ballet dancers or fighter pilots) or to compensate for malfunctioning of one of the contributing sensory systems [3,13,23]. Inappropriate weighting is also possible: the individual responses of motion sickness-susceptible student pilots on the so-called Intersensory Coriolis Stress Test, a test series of Coriolis effects in different combinations of sensory motion information, related to the severity of motion sickness experienced during elementary flight training [4]. During excentric rotation, additional problems arise because the equilibrium system is willing to accept the gravitoinertial force vector as gravity, resulting in a tilt sensation when the centripetal force is directed along the subject’s y-axis in a centrifuge with a fixed gondola [14]. In a centrifuge with a free-swinging gondola, the subject experiences the gondola oriented horizontally during a constant G-load. This is in accordance with the model of Fig. 4. If the centrifuge is brought to a stop, however, many people experience tumbling sensations and nausea, much more as encountered at the start of the ride. It is not unlikely that the new subjective vertical is part of these problems, because the problems are less if the subject is provided with a visual stimulus with information about his or her actual attitude. The fact that in motor races the motorcyclists keep their head upright aligned with gravity, even when the motor is almost horizontal during a turn, must have an advantage. Apparently it is easier in that case to use the visual information to keep a correct spatial orientation about what is horizontal and to suppress the horizontal vestibular nystagmus by visual fixation (horizontal nystagmus is more easily suppressed than vertical nystagmus). In view of the scheme of Fig. 4, this would be the most elegant solution, because aftereffects from the semicircular canals are restricted to the yaw-canals that do not affect the direction of the sensed vertical. The observation that fighter pilots also tend to align their head to gravity during a turn is probably based on the same strategy [24]. Further research about the exact influence of visual horizontal and vertical structures upon the vestibular signal processing in determining the subjective
BLES vertical (see Fig. 4) is required, certainly in view of the requirements for the design of centrifuge based flight simulators. In conclusion, it has been shown that the SV-conflict theory on motion sickness is able to explain when head movements during vestibular, visual and/or somatosensory rotatory motion stimulation are nauseating and when not. For VE applications and other simulators, this means that it is possible to analyse the conditions to be simulated at forehand and restrict the simulation to those conditions where mismatches in the determination of the subjective vertical are avoided. This will lower the incidence of simulator sickness.
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