Motion sickness and perception: a reappraisal of the sensory conflict approach.

British JournaI of PsychoIogy (1992), 83, 449-471 Printed in Great Britain

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0 1992 The British Psychological Society

Motion sickness and perception : A reappraisal of the sensory conflict approach Lucy Yardley* Medical Research ,Council Human Movement and Balance Unit, Section of Neuro-otology, National Hospital, Queen Square, London W C l N 3BG, UK

This review examines the role of activity and perceptual learning in motion sickness by means of a survey of the two kinds of recent research relevant to this topic. The first is a body of literature concerned not with motion sickness as such, but with perception of orientation and self-motion under the conditions of ‘sensory conflict ’ which are thought to provoke motion sickness. The second consists of investigations into the prediction and prevention of motion sickness itself. A major weakness is identified in the methodologies employed in both types of research: namely, a neglect of the way in which responses to unusual and disorienting environments, whether nauseogenic or not, may be affected by the activities, skills and strategies of the perceiver. New directions are outlined for future research into immediate reactions and longer-term adaptation to such environments.

‘Motion sickness ’ is the blanket term commonly given to the syndrome provoked by many forms of travel, by fairground rides, and by various unusual forms of motion which have been developed in the laboratory. Two partly independent classes of symptom can be distinguished. The first group consists of the direct consequences of disruption to perceptual and sensorimotor activities involving the vestibular system, such as disorientation, disequilibrium, and inappropriate vestibulo-ocular or vestibulo-spinal reflexes. The second group embraces a constellation of mainly autonomic symptoms (commonly including pallor, drowsiness, salivation, sweating, nausea and vomiting) which also appear to have a perceptual origin, since they are triggered by the same unusual motions or disorienting perceptual conditions. Almost all individuals eventually adapt to motions or situations which initially provoke sickness ; continued exposure to a particular nauseogenic environment leads to a gradual reduction in the disorientation and associated symptomatology, usually culminating in recovery of both sensorimotor control and well-being. However, the speed and pattern of adaptation can vary widely between individuals and in differing environments. Since susceptibility and adaptation to motion sickness are intimately linked to the perception of orientation and self-motion, hypotheses concerning the onset and cessation of motion sickness also serve as a useful testing-ground for the predictions derived from more general theories of perception and perceptual learning. Some fundamental theoretical issues are thus addressed in this review through a critique of *

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the ideas and research associated with the ‘sensory conflict’ theory of motion sickness. In particular, this paper seeks to explain and give structure to the, hitherto unstated, change in emphasis in research into orientation which has been occurring gradually over the past decade. The motivation for this shift, from a preoccupation with psychophysical quantification of responses to sensory stimuli towards a growing interest in sensorimotor activities and capabilities, can be traced to the investigative findings and frustrations described below. Since the mid-l970s, perception of ‘sensory conflict ’ induced by exposure to unusual combinations of visual and vestibular stimuli has widely been regarded as the cause of motion sickness. The first part of this paper therefore outlines the sensory conflict theory of motion sickness, and then critically examines the methodology and outcome of investigations into perception under conditions of sensory conflict (referred to below as the ‘perception’ studies). The second part of the paper integrates the more atheoretical and pragmatic work on the prediction and prevention of motion sickness (the ‘sickness ’ literature). The processes which may contribute to susceptibility and adaptation to nauseogenic environments are considered, drawing on the understanding of perception in disorienting conditions gained from the review of the perception studies.

The sensory conflict theory bf motion sickness Until the latter half of this century it was generally believed that motion sickness was caused by overstimulation of the vestibular system. This was a natural supposition, as many of the situations which provoke sickness involve turbulent motion or unusual force environments, and motion sickness bears a remarkable resemblance to the symptoms induced by vestibular malfunction (Benson, .1984; Brandt & Daroff, 1979). Moreover, although there is a great deal of variability in the susceptibility and syniptomatology displayed by different individuals, the only group of people who are completely resistant to the syndrome under all circumstances are those who have no functioning vestibular system (Money, 1990). However, the ‘vestibular overstimulation’ hypothesis was discredited when it was noted that motion sickness could be induced in a variety of situations where the sufferer experienced hardly any physical movement or active stimulation at all; for example; in cineramas, or in fixedbase aircraft simulators.’ In the mid-1970s a theory developed by James Reason (Reason, 1978; Reason & Brand, 1975) identified ‘sensory conflict’ as the factor common to all the situations provoking motion sickness. He proposed that the syndrome was triggered when the pattern of dovariance between the incoming signals from the vestibular system and the other sensory systems monitoring self-motion did not accord with the pattern of signals expected on the basis of previous motion experience. Thus, sickness in This statement is open to dispute, firstly, because the constellation’of symptoms provoked by visual field motion (and also weightlessness) differs somewhat from that provoked by vestibular stimulation, and, secondly, because it has been argued that discrepant visual input actually causes an intra-vestibular conflict via central vestibular pathways (see Crampton, 1990). However, symptoms.provoked by visual conditions and weightlessness are generally regarded as manifestations of motion sickness, and so these qualifications do not contradict the basic contention that motion sickness is triggered by perceptual disorientation rather than simple sensory over-stimulation. The peculiarly nauseogenic effect of ‘vestibular stimulation’ in the form of low frequency vertical oscillation (for example, at sea) can also be explained in perceptual terms, since the otoliths register repetitive changes in the gravity vector, yet neither the canals nor the somatosensory system indicate any head movement.

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simulators could be attributed to the unexpected absence of vestibular signals to accompany the visual field motion (a visual-vestibular conflict), whilst canal-otolith conflict was held responsible for the sickness provoked, even in the blind or blindfolded, by the unusual force environments encountered during air and space travel.’ Reason derived his description of the perceptual processes mediating detection of and adaptation to conditions of sensory conflict from von Hoist's (1954) ‘reafference principle’, and modifications of this concept developed by Held (1961, 1965). Following Held, he proposed that every active movement was accompanied by both a command signal (efference), and a resultant pattern of input from the orientation senses (reafference). Traces of these patterns of covarying efference and reafference were retained in a neural store, and during active movement the efference-copy enabled rapid retrieval of the reafferent trace combinations previously associated with it. Reason hypothesized that under unusual sensory conditions a discrepancy between the current and previous patterns of reafference would be detected, and a ‘mismatch signal ’ generated which would trigger the mechanisms mediating. the motion sickness syndrome. Subsequent adaptation to the nauseogenic conditions could be explained by exactly the same principles. With continued exposure to these unusual sensory conditions, new patterns of covarying efference and reafference would gradually be established. Consequently, the discrepancy between the incoming and previous patterns of reafference would be steadily reduced, and eventually motion sickness would no longer be triggered. While there is little theoretical or empirical cause to doubt the perceptual basis of motion sickness, various difficulties are associated with Reason’s characterization of the precise processes by which the individual detects and adapts to unusual perceptual conditions. Some of these problems originate from weaknesses in the theories from which his was derived. In particular, the idea that movements can be described in terms of fixed patterns of efference and reafference has been called into question (Lackner, 1981). Bernstein (1967) pointed out that the relationship between efferent activity and the physical movement and reafference resulting from it must vary constantly. This is because the actual effect of any particular motor command is constrained by the context created by such factors as the position and state of the limb to be moved. As early as 1932 Bartlett had also observed that no movement is ever duplicated exactly, and further noted that this posed considerable storage problems for theories which postulated a bank of neural traces corresponding to each motion (see Bootsma, 1988). Some theorists have therefore proposed a more flexible basis for sensorimotor coordination, based on skills adapted to the constraints of the environment and human abilities, rather than simple neural traces (e.g. Lackner, 1981, 1985; Whiting, 1980). The most recent reformulation of the sensory conflict theory, a ‘heuristic mathematical model’ developed by Oman (1982), avoids the problem of a lack of invariance between motor commands and their effect. This model characterizes the

* The sensory conflict theory seeks to explain how, but not, of course, why the precise symptoms of motion sickness are triggered. Triesman (1977) has suggested that motion sickness is an accidental manifestation of an originally adaptive response to ingesting poisons which disrupt coordination and perception through their effects on the nervous system; vomiting would expel the poison, nausea would cause aversion to it, and the general malaise would limit activity while dangerously uncoordinated. 19-2

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central nervous system as an information processing system which can produce continuously corrected predictions of sensory feedback using estimates of the current state of the ‘control system’ based on efferent and afferent information as well as inbuilt knowledge about the characteristics of that system. ‘Sensory conflict ’ is then signalled by a discrepancy between predicted and actual feedback. The predictive utility of such a model, in terms of its ability to identify the degree of sensory conflict (and, therefore, motion sickness) that will be experienced in a given situation, depends ultimately on its ability to represeot all the relevant internal and external sources of information employed by the control system concerned - the human individual. The way in which this information is integrated to determine orientation and self-motion must also be accurately modelled. The experiments reviewed in the following section attempted to define these parameters by systematically documenting the ‘normal ’ sensory response to various combinations of visual and vestibular stimuli. By employing a variety of unusual physical and visual field motions the ‘perception ’ studies artificially created conditions of sensory conflict, although the dependent variable upon which they focused was the perceptual response to these conditions, rather than the actual provocation of sicknes~.~ Since Oman (1982) explicitly stated that his model was intended to combine Reason’s qualitative sensory conflict theory of motion sickness with the mathematical approach to characterizing orientation adopted by the perception research, these studies should have furnished the empirical data required in order to implement (and validate) his model. The purpose of the critique of these studies presented below is not to deny the value of a detailed knowledge of the dynamics, constraints and biases of the sensory systems which contribute to orientation, but to question whether it is appropriate, or indeed possible, to characterize perception in unusual motion environments solely in terms of normative sensory responses to visual and vestibular stimuli. A reappraisal of the perception studies suggests that integral aspects of the human control system, such as purposive behaviour and acquired knowledge and skills, have tended to be ignored or excluded in the interests of experimental control and the measurement of a ‘pure’ sensory response. Consequently, the description of perception of orientation and self-motion derived from these investigations is, at best, incomplete. Moreover, it is evident that the wealth and complexity of information available to the perceiver, together with the flexible way in which this information may be selected and utilized, militate against the development of a set of universal ‘rules’ for the prediction of responses to the unusual perceptual environments which provoke motion sickness.

The ‘perception’ research Table 1 summarizes a representative, though by no means exhaustive, sample of investigations conducted in an effort to determine the precise sensory conditions under which the sensations of motion generated by the visual channel would In many of these studies frank sickness would not actually have been provoked, owing to the limited extent and duration of exposure to disorienting conditions; however, visual-vestibular conflict of this kind is also used to study susceptibility and adaptation to motion sickness itself (e.g. Dobie & May, 1990; Matsnev, Kuzimin & Zakharova, 1986).


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dominate, sum with, or be overshadowed by the signals for motion arising from the vestibular channel. During these experiments either the subjects, the visual field they are viewing, or both, undergo a variety of different physical motions. The perception resulting from each combination of visual field and self-motion is assessed by one of several techniques which seem to be treated as essentially equivalent. These include monitoring either the subject’s psychophysical estimation of motion or the compensatory motion the subject judges necessary to ‘null ’ the motion experienced, and measurement of compensatory eye-movements or postural adjustments.

Table 1. A representative sample of the ‘perception’ studies Authors

Motions employed

Huang & Young (1981) Keller & Henn (1984) Melcher & Henn (1981) Probst, Straube & Bles (1985) Wong & Frost (1981) Young, Dichgans, Murphy & Brandt (1973) Zacharias & Young (1981) Brandt, Dichgans & Koenig (1973) Held, Dichgans & Bauer (1975) Reason, Mayes & Dewhurst (1982) Young, Oman & Dichgans (1975) Berthoz, Pavard & Young (1975) Huang & Young (1987) Lestienne, Soechting & Berthoz (1977) Pavard & Berthoz (1977) Huang & Young (1988) Lessard & Wong (1987)

Subject rotated about an earth-vertical axis : stationary visual field.

Subject stationary, visual field rotated about various axes.

Subject linearly translated, with moving or stationary field.

Other combinations of subject and/or visual field motion.

Some consistent patterns of results have emerged from these studies. Visual field movement tends to be more effective in inducing illusory self-motion (vection) when presented to peripheral vision, and the vection tends to become more pronounced as the area and velocity of the visual field motion is increased (Brandt, Dichgans & Koenig, 1973; Dichgans & Brandt, 1978; Held, Dichgans & Bauer, 1975). Visual field motion also seems to have a more compelling influence on self-motion perception at constant velocities and low accelerations, which the vestibular system cannot reliably detect (Dichgans & Brandt, 1978; Melcher & Henn, 1981). However, these broad principles simply provide indications of evolutionary, physiological and developmental constraints or biases in the way that information from the visual and vestibular systems is commonly utilized. Many of the perception studies attempted to go beyond such generalities and establish precise psychophysical laws or mathematical models of the form of sensory integration and resultant perception induced by the various combinations of visual

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and vestibular stimulation. Yet very different models have often been derived under perceptual conditions which appear extremely similar in terms of their physical characteristics. For example, Zacharias & Young (1981) exposed subjects to a visual surround rotating at a constant velocity, and then superimposed physical yaw motion (rotation about an earth-vertical axis). They found that the vestibular signal generated by the physical motion dominated perception of self-motion at all accelerations above 0.2-1 .0°/s2, and when the vestibular signal was not in agreement with the sensation of movement induced by the rotating surround this sensation was abruptly cancelled. However, when Probst, Straube & Bles (1985) conducted a very similar experiment, they found that the visual input predominated over a contradictory vestibular input of up to 250/s2 in determining the perceived direction of self-rotation. Probst attributes the discrepancy between his results and those of Young to differences in the area of the moving visual field presented in the two experiments, since both the total area and the extent of peripheral visual field motion employed were less in Young's experiment. If the precise characteristics of the visual field have such a pronounced influence on perception, it follows that the exact effect of these factors, in isolation and in combination, must in turn be determined. Unfortunately, attempts to tie the relative.weight attached to the visual channel to specific physical parameters of the visual field have themselves encountered difficulties. For example, the stronger influence of peripheral compared with central field motion noted by Brandt and his colleagues has not always been replicated (Paulus, Straube & Brandt, 1984). It can be removed or reversed simply by dividing the visual field into several sectors (Held e t al., 1975). In addition, lamellar optic flow has been shown to have much the same effect on postural control whether presented to central or to peripheral vision (Stoffregen, 1985, 1986). It has also proved difficult to determine whether perceived velocity is principally influenced by the total area of the moving visual field (Held e t al., 1975), its spatial frequency (Diener, Wist, Dichgans & Brandt, 1976), or the total boundary length of the elements within it (Reason e t al., 1982). Even the three broad principles cited above were contravened by an optical display created by Andersen & Braunstein (1985). They induced both linear vection and motion sickness by presenting an expanding pattern of dots, subtending less than 30" of visual angle, to central vision ; moreover, increasing the area of the display did not increase the illusion of self-motion, while increasing the speed of the display sometimes led to a reduction in vection. Besides these changes in perception resulting from slightly differing combinations of visual and vestibular stimuli, even when sensory conditions are held constant, large unexplained inter- and intra-individual. differences are commonly observed. Marked variability in response to linear motion of the visual field has been attributed (post hoc) to learning effects (Berthoz, Pavard & Young, 1975), mental activities and unknown individual differences (Lestienne, Soechting & Beahoz, 1977). Moreover, the true extent and importance of individual differences in perception is often masked by selective sampling, Fdr example, Huang & Young (1987) based their mathematical model of linear self-motion perception on the responses of just five out of an original sample of 11 normal subjects, since the remaining six were quite unable to judge their self-motion under the unusual perceptual conditions employed in their experiment.


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Similarly, to derive their description of the combined effects of vestibular and visual stimuli on the vestibulo-ocular reflex, Koenig, Allum & Dichgans (1978) preselected just four subjects (from an initial group of 40) whose reflexes they considered suitably stable. The purpose of focusing on the anomalous results of these attempts to document perceptual ‘rules’ €or the integration of visual and vestibular stimuli is not simply to highlight the enormous difficulty and complexity of such a task. In fact, these difficulties, and some of the explanations offered for them, suggest that the investigators, in their quantification of the physical characteristics of the motions and displays employed, have failed to describe adequately the parameters actually effective in influencing perception in these studies. Individual differences, learning effects and complex interactions between various features of the visual field and physical motions do indeed have a fundamental impact upon perception, and must consequently be given formal and explicit consideration. Some preliminary indications of the role played by such factors are described below. Relational perceptual structures The notable, but not absolute, influence on perception of crude physical parameters such as the area, velocity and retinal eccentricity of a moving visual display suggests that these features of the visual field might be indirectly influencing perception, through their mediating impact upon a related property of the visual environment. A clue to the possible identity of one such higher-order variable is provided by Brandt’s own observation that a moving visual surround is less able to induce an illusion of self-motion if a stable structure can be seen beyond it (Brandt, Wist & Dichgans, 1975). Thus, it is the motion of the perceived background which appears to dominate the perception of self-motion. Movement of a small area of optic structure in the centre of the visual field is likely to be associated with object movement, but motion of large areas of the visual field, particularly in the retinal periphery, is normally concomitant with self-motion (Gibson, 1966). Therefore, it seems reasonable to suggest that such parameters as the area or retinal eccentricity of visual field movement may influence the extent to which such motion is perceived as pertaining to the foreground or background, and it is this which then determines whether the motion is perceived as consistent with object or self-motion. Two experiments by Ohmi & Howard (1988; Ohmi, Howard & Landolt, 1987) provide compelling support for this interpretation. They presented subjects with various combinations of stationary and moving displays and found that vection was always controlled by whichever display was perceived as the background. Moreover, the perception of a display as background did not appear to be tied to any specific ‘depth cues ’, and background stationary displays were shown to suppress vection by about the same amount whatever their size and eccentricity. Ohmi & Howard’s demonstration of the intimate relationship between the perception of background and self-motion carries profound implications for the way in which motion perception must be characterized and studied. The perception of ‘background motion’ cannot be an automatic response to a particular sensory stimulus. An integration of many kinds of information contributes to this perception,

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and, as Ohmi’s studies have shown, no one source of information is necessarily either indispensable or absolutely compelling. Consequently, the factors ‘controlling ’ perception, at least under the unusual perceptual conditions considered here, cannot be described solely in terms of the physical characteristics of the environment, but must also take into account the way in which the perceiver attends to, structures and utilizes these characteristics.

Activity and perceptual exploration Although in studies of visual-vestibular conflict a variety of responses have been measured, from psychophysical judgements to postural adjustments, these often appear to be regarded as interchangeable. Little attention has been paid to the likelihood that quite different aspects or modes of perception may be involved (and thus assessed) in each form of response. For example, a visual surround which rotates about the line of sight can provoke subjective reports of what Brandt termed a ‘paradoxical perception ’ of continuous bodily rotation combined with a fairly steady apparent tilt of the vertical. When subjects were asked to set a line to the vertical under these conditions, the maximum average value of the tilt of the perceived vertical was 15 degrees (Dichgans, Held, Young & Brandt, 1972). However, postural compensation for this apparent tilt, using exactly the same apparatus and visual field motion, seldom exceeded 3 degrees (ClCment, Jacquin & Berthoz, 1985). Clearly, the activities of making judgements of the gravitational vertical and controlling posture are quite Merent, and evoke different uses of the available perceptual information. In the perception research very little attention has been paid to the role of voluntary activity, which has generally been kept to a minimum. Activity emphasizes information from the somatosensory system, the influence of which has been largely neglected. Even during passive motion, Lackner & Graybiel (1978) found that the perception of self-motion, and compensatory eye-movements, of blindfolded, recumbent subjects rotated about the Z (long body) axis were more consistent with the patterns of touch and pressure along the body surface than with the otolithic signals (at rotational velocities above 12 rev/min). Active, voluntary movements have a much more pronounced impact on perception. Indeed, the sensation of rotation and postural adjustments which follow active turning are opposite in direction to those induced by passive rotation, and serve to cancel out the vestibularinduced illusory after-effects of constant velocity rotation (Bles, De Jong & De Wit, 1984a; Probst et al., 1985). Voluntary movement can be used to gain additional information about orientation. For example, the vestibular information produced by continuous head movements can delay and attenuate both the illusory self-motion and the motion sickness induced by a rotating display (Lackner & Teixeira, 1977). Activity also helps to direct attention and shape the selection of perceptual information. The interdependent effects of attention, activity and somatosensory information have been documented by extensive work on adaptation to distorting prisms (see Welch, 1986 for a review of the relevant literature). For example, Welch, Widawski, Harrington & Warren (1979) demonstrated that subjects who watched their own arm movements while wearing displacing prisms were less susceptible to the illusion that their arm position had changed if they made active, rather than passive, movements. Movement affectedadaptation as well as immediate perception ;


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following active arm movements a shift in the perceived direction of gaze could be measured, while passive movements produced only a shift in the felt position of the arm. Various other effects on perceptual adaptation have been linked to factors such as the instructions, activities and opportunities for detecting relevant information incorporated into the experimental situation (Canon, 1970; Uhlarik, 1973;Warren & Schmitt, 1978; Welch, 1978), and the variety of perceptual environments explored (Redding, 1981). Given the evident importance of activity and perceptual exploration for perception, the validity of investigations into visual-vestibular conflict in which these are virtually precluded must be questioned. Although many of the prism studies referred to above were concerned more with adapted than immediate perception, in practice it can prove extremely difficult to draw a dividing line between the two (which Welch and his colleagues have, in any case, shown to be intimately related). For example, Berthoz e t al. (1975) note that a marked change in perception occurred during the course of their experiment on (initially) nalve perceptions of linear self-motion. During the course of only 10 trials subjects apparently learned to attend to some undefined feature of the experimental situation which helped them to detect their true self-motion with ever increasing accuracy, despite the presence of visual field movement which had initially caused severe disruption to such judgements. Individual differences and perceptual learning

In the perception literature, marked individual differences in response are typically ignored, and models of perception are based on averages derived from very widely varying perceptual judgements. Yet, by glossing over this large unexplained intersubject variability in perception, valuable insights into the process of perception may be lost. Drawing again on studies of adaptation to distorting prisms, it can be seen that the amount of attention paid to a particular source of information can be determined by an individual’s long-term perceptual skills or biases (McDonnell & Duffetti, 1972; Melamed, Beckett & Halay, 1979). For example, Warren & Platt (1975) were able to relate inter-subject differences in amount and type of adaptation to prisms to pre-test measures of visual and manual abilities. Such variations in the use of perceptual information may in turn result from an individual’s history of sensorimotor experience. In a study of the effect of diving experience on perception underwater, O’Reilly (1975) found that over a 24-minute period experienced divers adapted to performing manual tasks underwater by a shift in the interpretation of the visual information, whereas novice divers developed only a localized shift in the felt position of the arm used to perform the task. Summary and implications for research

This review of the perception research indicates that perception in unusual environments does not consist of an automatic response to specific physical parameters of that environment, but is influenced by the individual’s selective utilization of the available perceptual information, which is in turn shaped by his or her activities, and sensorimotor skills and biases. It therefore seems inappropriate to employ a methodology which analyses the environment solely in terms of simple

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physical stimuli, prevents voluntary activity and perceptual exploration, and averages important individual differences. Even though the situations which provoke motion sickness normally involve passive modes of transportation, in these naturalistic situations the sources of information from which one can select are actually quite rich, and some exploratory movements can be made in an attempt to determine one’s orientation or motion. Often the act of controlling some necessary activity, such as maintaining balance or guiding a vehicle, can itself provide rapid feedback to the perceiver about the accuracy and relevance of the various types of information. For example, Kruk & Regan (1983) and Owen (1986) have identified subtle but highly effective alterations in the selection of optic information by pilots for the differing purposes of monitoring var’ious kinds of self-motion, or successfully tracking or aiming at external targets. Martin, Riccio & Stoffregen (1988) have also shown that the activity of maintaining balance itself constitutes a source of information about the effective ‘vertical ’ which is quite independent of optic, vestibular and somatosensory information. Future research into responses to novel perceptual environments should therefore examine the selection of information from those environments in relation to the various activities undertaken. The way in which perceivers bring their knowledge and perceptual skills to bear upon the available information is also relevant. Many skills and strategies are likely to prove virtually universal. However, it is probable that, as in the studies of adaptation to distorting prisms, some perceptual biases may prove specific to identifiable groups of people, and may thus be able to account for some of the wide, hitherto unexplained inter-subject variability observed in responses to various forms of sensory conflict. A series of experiments initiated by Lackner has already furnished some preliminary explorations of the impact of such perceptual processes (e.g. DiZio & Lackner, 1986; Lackner, 1985). His findings suggest that when subjects are confronted with apparently contradictory information they utilize their previous experience of the regularities and constraints which exist in the environments normally encountered to arrive at a plausible, albeit sometimes idiosyncratic, interpretation of the ambiguous situation. The various solutions devised by his subjects generally represent a compromise between the ‘evidence ’ of their senses, and their knowledge of what is possible or probable. In the following sections the insights into perception in novel environments derived from this review of the perception literature are used to integrate and interpret the results of investigations into susceptibility and adaptation to nauseogenic conditions. The ‘sickness’ research

Much of the research on motion sickness has consisted of diverse pragmatic, and largely atheoretical, attempts to discover ways of predicting who is most likely to become sick in the various nauseogenic situations encountered. Unfortunately, due to this lack of theoretical integration several fundamental issues pertaining to the reliability and validity of measures of susceptibility have not yet been resolved. The issue of validity is closely related to questions concerning the factors which are generally presumed relevant to the study and understanding of motion sickness. It is also necessary to determine whether a person’s susceptibility is dominated by their


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immediate response to a novel motion environment, or by the ability to adapt to this environment over time. In addition, the reliability with which susceptibility can be predicted in different situations will depend upon the degree to which susceptibility constitutes a global trait, rather than a local response to a particular set of perceptual conditions.

Reliabilio and validio Two main techniques are commonly employed for the practical purpose of predicting susceptibility to motion sickness. The first is to administer a motion sickness questionnaire (MSQ), which simply gathers inforniation about previous responses to various types of travel, while the second consists of exposing the individuals concerned to some laboratory-based nauseogenic motion. Future susceptibility to motion sickness is then predicted on the basis of the degree of malaise induced in the laboratory, or the score on the MSQ, which represents some weighted summation of the individual’s reported history of reactions to motion. Some authors report finding a significant relationship between observed susceptibility to air or seasickness and scores on MSQs or provocative tests (Hixson, Guedry & Lentz, 1984; Keinan, Friedland, Yitzhaky & Moran, 1981). However, Lentz (1984) concluded a lengthy development and evaluation of five laboratory tests of motion sickness susceptibility by commenting that ‘all of these tests have had typically low correlations with field conditions ’ (pp. 29-7). Reschke, Homick, Ryan & Moseley (1984) used a battery of provocative tests, MSQs and measures of vestibular function to predict sickness during parabolic flight. No single test correlated reliably with the response to parabolic flight, and the level of prediction obtained using a linear equation derived from these data was only a little better than chance. A subsequent logistic model developed from scores on a similar range of tests could only correctly classify 65 per cent of a new sample of subjects into the categories ‘sick’ or ‘nonsick’ (Lin & Reschke, 1987). The limited predictive value of the commonly used tests of susceptibility does not appear to be due to a lack of reliability in the techniques used to measure sickness. Individual physiological measures such as gastric motility (Stern e t al., 1985) or electrodermal activity (Isu, Koo & Takahasi, 1987; Warwick-Evans e t al., 1987) show only moderate covariance with subjective symptoms, and therefore self- or observer ratings of multiple symptoms are generally employed to assess tolerance of a provocative motion. These rating systems usually show fair inter-rater agreement (Lentz, 1984), and Calkins, Reschke, Kennedy & Dunlop (1987) have established a relatively high test-retest reliability for symptom points scored on two tests involving cross-coupled angular acceleration, and one consisting of exposure to parabolic flight (between 0.70 and 0.88 for normalized data). The test-retest reliability of MSQs is also good; Lentz & Collins (1977) report a coefficient of 34, while Reason (1968) obtained a coefficient of .89, with an inter-test interval of six months. Since the reliability of existing measures of motion sickness susceptibility is evidently fairly good, it seems probable that the inability of laboratory tests to predict sickness under ‘field conditions ’ is due to more fundamental problems concerning

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their validity. The two aspects considered below are temporal and perceptual characteristics.

Consisteny of susceptibilig across situations and over time Laboratory tests differ from most field conditions in that they generally consist of a fairly brief exposure to a highly nauseogenic motion, and thus measure immediate susceptibility. The target situations, in contrast, typically involve longer-term exposure to milder motions, and so may require an ability to adapt quite quickly to the new sensory conditions, rather than an immediate resistance to them. The importance of distinguishing between initial susceptibility and ability to adapt has, in fact, been stressed by Reason, who found rate of adaptation rather than immediate response to be the principal correlate of both MSQ scores and persistence of symptoms during prolonged exposure to laboratory tests (Reason & Graybiel, 1972). Evaluating a programme designed to prevent in-flight sickness in susceptible airmen, Graybiel & Kiepton (1978) noted that an individual’s rate, retention and transfer of adaptation to provocative motions were much better predictors of a successful return to flying than was his initial reaction. Similar conclusions were reached by Graybiel & Lackner ( 1 9 8 0 ~ who ) ~ exposed subjects to a ‘vestibulovisual’ test on four occasions, separated by a few days. They drew the general conclusion that, although tolerance of the test on the first trial was not a good predictor of adaptation to it, tolerance remained fairly consistent from the second trial onwards. Graybiel & Lackner performed no statistical analysis on the results of the study reported above, but my own post hoc analysis of their published data not only confirms their conclusions, it also suggests a second possible cause of invalidity in laboratory tests of susceptibility. The vestibulovisual test consisted of a series of sudden stops from constant velocity rotation, first with eyes closed and then with eyes open; however, half the subjects failed to reach the ‘eyes open’ stage of the test on the first trial, although all subjects were exposed to this condition during the later trials. For the purposes of my analysis these subjects were allocated to two groups, according to whether or not they had reached the ‘eyes open ’ stage of the test on the first trial, and the Spearman’s rank order correlations between the scores obtained on each trial were calculated for each group independently. The intercorrelations between scores on the second, third and fourth trials ranged from .75 to .97 for both groups. For those subjects who completed the whole test on the first trial the range of correlations between the first and later trials was .49-.68, confirming that the initial response to the test was a relatively poor indicator of later reactions. However, for those subjects who did not reach the ‘eyes open’ on the first trial, the correlation between the first and subsequent trials ranged from only .19 to .24. This suggests that the initial susceptibility with eyes closed may have been a particularly inadequate predictor of the level of adaptation finally achieved, with the aid of visual information. The results of this reanalysis can be readily understood in the light of the conclusions derived from the review of the perception literature, which indicated that wide variations in responses to novel conditions are to be expected if the availability and utility of the perceptual information differs in the situations compared. Further support for this contention is provided by the failure of attempts


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to predict space sickness on the Spacelab 1 mission (von Baumgarten, 1986; Oman, Litchenber, Money & McCoy, 1986; Young, Shelhamer & Modestino, 1986). Predictions were based on the responses of the four astronauts to six tests, including four types of constant velocity rotation. During the constant velocity tests no informative visual cues were available, signals from the semicircular canals were misleading, and so otolithic and somatosensory signals provided the most accurate guide to self-motion. However, the utilization of information required for orientation in space is almost opposite to that needed for accurate perception of self-motion on these rotation tests ; weightlessness alters the otolithic and somatosensory information, necessitating a greater reliance on vision for orientation. The rank ordering of susceptibility to the rotation tests was highly consistent, but the rank order of severity of symptoms in space proved to be the exact reverse of that predicted from these tests. The evidence regarding the degree to which motion sickness susceptibility is situation-specific is at present inconclusive. Lentz & Guedry (1978) and Stott & Bagshaw (1984) have both observed subject-motion interactions in the susceptibility of chronically motion sick individuals. However, whereas the inter-test correlations obtained by Reschke e t al. (1984) were mainly non-significant, Lentz & Guedry (1978) found that the inter-test correlations of normal subjects on three tests of susceptibility ranged from .38 to .70, and were all significant. Moreover, the ability to adapt to nauseogenic environments over time appears to be less situation-specific than the initial susceptibility. Graybiel & Lackner (1983) have presented evidence of a qualitative consistency in the rate and retention of adaptation in 14 subjects exposed to a series of vestibulovisual tests and parabolic flights, despite differing initial susceptibilities to the two conditions. A definite relationship between sea, car and air sickness has also been reported by Pethybridge (1982) ; as this conclusion was drawn from a questionnaire survey, scores were presumably based on the persistent reactions of the individuals concerned over a period of time. Summary and implicationsfor research

The preceding overview of measures of motion sickness susceptibility suggests that many of the existing tests, while reasonably reliable, fail to predict sickness in specific situations owing to problems of validity. Some of these problems may be due to a lack of correspondence between the perceptual conditions used to test susceptibility and those that exist in the situations actually provoking sickness; immediate responses to potentially nauseogenic environments certainly appear to exhibit some situational specificity. The difficulty in generalizing from one set of perceptual conditions to another that emerges from this review of the sickness literature closely parallels the high degree of situational specificity that was found to characterize the models derived from the perception studies. Moreover, as in the perception studies, the lack of correspondence between ‘field’ and test conditions may also have been aggravated by the prevention of any natural exploratory physical and perceptual activities during most tests of motion sickness susceptibility. The review of the perception literature concluded that perception in, and adaptation to, unusual perceptual environments was significantly affected by the activities, perceptual biases and strategies adopted by the perceiver. Clearly, the

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effectiveness of such strategies must vary as a function of the conditions pertaining to any particular situation. An individual’s response to a potentially nauseogenic environment might therefore also be expected to depend to some extent on the availability, accuracy and utility of various sources of information in that environment, defined in relation to the activities undertaken by the individual. The impact of such factors must consequently be taken into consideration when attempting to predict susceptibility, and could usefully be explored further. However, the ability to adapt to provocative motions, rather than immediate reactions to them, appears to be the most important factor determining motion sickness susceptibility in the long term (unless, of course, the individual experiences no initial sickness, in which case adaptation is unnecessary). Moreover, subjects seem to display more cross-situational consistency in their ability to adapt to motion than in their initial susceptibility. It was noted in the section on perception research that immediate perception and adaptation are intimately linked, and may both be affected by sensorimotor activity, experience, skills and strategies. Since it is evident that the processes subserving adaptation should be the main focus for investigations into resistance to motion sickness, the next section is devoted to a discussion of these processes. Adaptability and adaptation The question of why and how some people adapt more easily than others to potentially nauseogenic conditions is, of course, intimately linked to questions regarding the processes which mediate the response to unusual perceptual environments, and the nature of the changes subserving adaptation. In this section three possible explanations for individual differences in resistance and adaptation to motion sickness are considered, based on differences in either low-level responses, central processes, or perceptual learning and sensorimotor skills. Basic processes Resistance to motion sickness might plausibly be thought to be mediated by a simple reduction in the autonomic responsivity which subserves the secondary symptomatology associated with the syndrome. Adaptation and susceptibility have been linked to patterns of physiological responses, including heart rate, galvanic skin response, respiration rate and blood volume pulse (Cowings, Naifeh & Toscano, 1990; Cowings & Toscano, 1982). However, the precise pattern of autonomic response associated with reactions to nauseogenic motions remains a matter for debate (Cowings, Suter, Toscano, Kamiya & Naifeh, 1986; Graybiel & Lackner, 1980b). It is also unclear whether the patterning of autonomic responses should be regarded as a cause or a mere symptom of susceptibility; the close association between symptoms of sickness and perceptual illusions observed by Reason & Graybiel (1972) certainly suggests that the autonomic reaction is not independent of the perceptual response to motion. A great deal of research into individual differences in resistance to motion has been devoted to an unsuccessful search for variations in sensory sensitivity, or low-level sensory integration and reflex control. In view of the central role in the development of motion sickness played by the vestibular system, an obvious candidate was


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vestibular sensitivity. However, investigations into possible links between susceptibility and vestibular sensitivity eventually concluded that no such relationship existed (Clark & Stewart, 1973; Dobie, 1969). In view of the evidence that motion sickness susceptibility seems to be dominated by a general ability to adapt to unusual perceptual circumstances, rather than by immediate responses to particular sensory conditions, it is hardly surprising that individual differences in resistance to motion sickness are apparently not reducible to simple variations in basic sensory processing. The visual-vestibular integration believed to subserve vestibulo-ocular reflex (VOR) control has also received considerable attention. Here again, while some researchers claim to have found associations between susceptibility and various slight abnormalities of VOR control (Matsnev e t al., 1986; Shirabe, Soda, Kawano & Shiraishi, 1986), others have failed to observe any systematic differences between the reflexes of normal and sick or susceptible subjects (Lentz, 1976; Peterka & Black, 1986; Peterka, Black & Schoenhoff, 1987). Most recently, DiZio & Lackner (1991) have reported a significant correlation between motion sickness susceptibility and the effect of head movements on the post-rotatory VOR. However, the status of the VOR as an indicator of the processes subserving motion sickness is again unclear. Compensatory eye movements are not the product of a totally reflexive integration of visual-vestibular stimuli. Instead, like most other responses to motion, they can be influenced by auditory and somatosensory information, and by attention and mental strategies (Guedry & Benson, 1983; Melville-Jones, Berthoz & Segal, 1984; Moller, White & Odkvist, 1990). Thus, there is no reason to suppose that minor variations in the VOR are either the fundamental cause of motion sickness, or even a privileged indicator of visual-vestibular integration. Rather, VORs constitute just one of the many facets of sensorimotor control in unusual environments which may be used to assess the underlying perceptual and motor coordination or disorientation in that environment.

Central processes and neural traces Since it appears unlikely that resistance to motion sickness can be attributed to basic autonomic or sensory processes, a reasonable alternative hypothesis is that this resistance is mediated by more complex, central processing. This approach was adopted by Reason, who proposed that adaptation proceeded through the gradual laying down of neural traces corresponding to the precise patterns of covarying efference and reafference that obtained under the novel sensory conditions provoking sickness. Once the pattern of neural traces pertaining to the new sensory conditions was sufficiently consolidated a mismatch between the expected and actual sensory inputs would no longer exist, and so motion sickness would not be triggered. The idea that perception is such a stereotyped process of sensory integration that the perception of a particular motion in a particular environment can be represented by one fixed set of neural traces seems somewhat incompatible with the indications which emerged from the perception studies, that perception involves an active, flexible and sometimes idiosyncratic selection from many potential sources of information. The theoretical objections to the concept of a store of neural representations of the efference and afference corresponding to every movement have been discussed above. Moreover, Reason’s theory of adaptation should virtually

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preclude the possibility of transfer of protective adaptation acquired under a particular set of conditions to another provocative environment. However, a review of the empirical evidence on this point (presented below) suggests that some form of transfer of adaptation may, in fact, occur. A further consequence of Reason’s characterization of adaptation concerns the processes hypothesized to mediate ‘adaptability ’. Since adaptation is presumed to consist of a relatively automatic updating of neural traces, Reason could only speculate that individual differences in adaptability must be due to internal variations in the ability to acquire, store or retrieve these traces (Reason & Brand, 1975). This view of adaptability unfortunately led to an apparent investigative dead-end. While inter-subject differences in the rate and retention of adaptation could certainly be documented, no other observable correlates of the hypothetical underlying neural processes were suggested. Thus, although Reason himself concluded that ‘perceptual adaptation is brought about by something very akin to learning’ (Reason & Brand, 1975, p. 165), his characterization of this learning was both inflexible and circular. If, however, the learning mediating resistance to motion sickness could be shown to involve the acquisition of sensorimotor skills and abilities, then a whole new range of possibilities for the investigation of these processes presents itself.

Cross-situational transfer of adaptation and sensorimotor strategies The conditions under which adaptation to nauseogenic motions will transfer from one situation to another has received little systematic exploration. This may be because such transfer is not predicted by Reason’s model of adaptation, although Reason himself recorded several instances of a long-term, but limited, generalization of resistance to nauseogenic motion (Reason & Brand, 1975, ch. 6). Yet a degree of generalization of adaptation has been documented by several other investigators (e.g. Dobie & May, 1990; Graybiel & Knepton, 1978; Kennedy, Berbaum, Williams, Brannan & Welch, 1987). A generalized resistance to potentially nauseogenic vestibular stimulation is also observed in various groups of people whose occupations involve repeated exposure to unusual motion, such as seamen, pilots and athletes (Collins, 1974; Dowd & Cramer, 1971 ;Hood, 1984). Dancers and skaters, who must learn to orient accurately during and after pirouettes, seem able to suppress most of the compensatory eyemovements, and virtually all the feelings of rotation, imbalance or nausea that are normally induced by rotatory and caloric tests (Dix & Hood, 1969; McCabe, 1960; Osterhammel, Terkildsen & Zilstorff, 1968). Yet such tests are very different, in terms of physical activity and sensory input, from making self-induced spinning movements about an earth-vertical axis. This resistance to the effects of motion is not congenital, but acquired ;McCabe was actually able to chart the gradual development of suppression of rotatory and caloric responses in a group of young skaters as they were taught to spin over a five-month period. Reason’s ‘neural trace ’ account of adaptation has difficulty in accommodating the phenomenon of cross-situational transfer. However, the description of perception and adaptation in novel environments emerging from the review of the perception literature not only allows for such phenomena, but indeed provides a framework for investigation into the processes which may be involved. If adaptation to potentially


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nauseogenic conditions involves the same processes as were shown to mediate responses to ‘visual-vestibular conflict ’, then the response to a nauseogenic situation will depend on the availability and utilization of various sources of information about orientation and self-motion, defined in relation to the activities undertaken by the individual. Following from this approach, a plausible explanation of the phenomenon of cross-situational transfer of adaptation is that some perceptual strategies or modes of functioning developed in a particular nauseogenic environment will prove specific to a restricted set of perceptual conditions, while others may prove useful in a wide range of environments, or for several different activities. For example, post-flight patterns of susceptibility in astronauts suggest both situation-specific and nonspecific components of adaptation (Oman e t a/., 1986). A short-term, relatively environment-specific adaptation - perhaps the reinterpretation of otolithic information (Parker, Reschke, Arrott, Homick & Lichtenberg, 1985) - provides protection against certain nauseogenic motions (e.g. Coriolis head movements) but temporarily increases susceptibility to others (e.g. seasickness). In addition, a longerlasting slight general reduction in motion sickness susceptibility is observed. Variations in exploratory activity, and perceptual experience and skills, were also shown to influence perception of, and adaptation to, the various unusual perceptual conditions studied in the laboratory. There has been, to date, very little research into the possible links between susceptibility to motion sickness and variations in individuals’ activities or uses of perceptual information, but a few promising examples can be found. One of these is a rare study of natural postural responses to passive transportation by Fukuda (1975), who observed that bus drivers lean in the opposite direction to passengers when the bus navigates a bend. It is well known that individuals are much more resistant to motion sickness while driving a vehicle than when they are passengers ; perhaps this resistance is associated with such postural strategies. In addition, there is accumulating evidence to suggest that the ability to select the appropriate source of information for orientation when some cues are misleading may prove a useful index of the multisensory coordination required to provide resistance to motion sickness. Several studies have demonstrated an association between motion sickness susceptibility and the utilization of vision for orientation even when vision is misleading (Bles, De Jong & Oosterveld, 1984b; Frank & Casali, 1986; Yardley, 1990; Yardley, Lerwill, Hall & Gresty, 1992), whereas dancers are apparently less influenced than most by vision-distorting prisms (Kahane & Auerbach, 1973). Sgmmay

Individual differences in resistance to motion have not yet been reliably linked to any particular mode of low-level sensory or autonomic responding. Moreover, it is debatable whether any variation in such basic processes as might be found could justifiably be regarded as a cause, rather than a symptom, of motion sickness susceptibility. Thus, Reason may have been correct in regarding the perceptual learning which apparently subserves adaptation to motion sickness as the principal factor influencing resistance to a nauseogenic motion. However, his characterization of this learning consists of a somewhat circular definition in terms of hypothesized

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central processes, and is incompatible with evidence of a degree of transfer of adaptation from one set of voluntary motions and perceptual conditions to another. The alternative conceptualization of adaptation derived from the review of the perception studies suggests a potentially more fruitful analytic approach, involving examination of the way in which the experience and sensorimotor skills of individuals may influence both their susceptibility, and their motor and perceptual activities and strategies in potentially nauseogenic environments.

Conclusions The sensory conflict theory of motion sickness inspired a substantial body of research into responses to various conditions of visual-vestibular conflict (the perception literature), and also had a more remote and dilute influence on the diverse pragmatic investigations into susceptibility and resistance to motion sickness (the sickness studies). However, the review of both these literatures presented above reveals that neither has yielded any decisive and comprehensive principles. The results of the perception experiments have tended to be highly specific to the very artificial situations in which they were obtained, while the sickness studies have so far failed to develop any reliable methods of predicting or preventing the syndrome in most of the target individuals and environments with which they have been concerned. In this paper, the inconclusive results of both types of research into motion sickness are traced to a common neglect of the role played by active perceptual strategies, exploration and voluntary movement in reactions to unusual perceptual environments. Despite the emphasis placed on activity and perceptual learning by Held, from whose ideas the sensory conflict theory was derived, the perception and sickness studies have tended to adopt a methodology which precluded any examination of the impact of either of these factors. Yet it is clear from this review that an individual's response to a novel environment can be strongly influenced by the way in which the information available in that environment is selected and utilized. This, in turn, depends on the activities, experience, biases and skills of the individual in question. Thus, by utilizing unrepresentative perceptual conditions, and controlling or ignoring the voluntary activities and perceptual strategies employed by their subjects, the studies of motion sickness reviewed in this paper have excluded the very factors most likely to influence responses to nauseogenic conditions encountered in everyday life. In conclusion, it is apparent that research into susceptibility and resistance to environments provoking sickness must adopt a fresh approach. For several decades it has been generally accepted that motion sickness is caused by an alteration in the perceptual environment which disrupts the way in which information from the senses is normally utilized to perceive, and control, orientation and self-motion. Nevertheless, despite this widespread recognition of the perceptual basis for the syndrome, principles derived from general models of perception and perceptual learning have seldom been systematically applied to the problem of motion sickness. In fact, not since Reason's attempt, over 15 years ago, to apply the ideas of von Holst and Held to motion sickness has an explanation of motion sickness been grounded on more general theories of perception and adaptation. In view of the considerable theoretical advances that have since been made in relevant disciplines (e.g. Flach,


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1990; Runeson, 1988; Stoffregen & Riccio, 1988) a complete re-evaluation of the problem of motion sickness seems overdue. This review has sought to provide a first step in this direction, and some preliminary recommendations : future research should be concerned, not with various parameters of the environment defined from a physicalist perspective, and their effects upon a passive individual, but rather with informative structures, which can only be defined in relation to the skills and activities of the perceiver.

Acknowledgements The first draft of this paper was completed at Southampton University; I would like to thank Dr Alan Costal1 for his invaluable comments and advice, and Professor Anthony Gale, Dr Michael Griffin and D r Michael Gresty for their support and encouragement.

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Received 27 March 1991; revised version received 6 January 1992

Motion sickness: a synthesis and evaluation of the sensory conflict theory.

Postural behaviour and motion sickness.

Pathophysiology and treatment of motion sickness.

Brainstem processing of vestibular sensory exafference: implications for motion sickness etiology.

Vection is the main contributor to motion sickness induced by visual yaw rotation: Implications for conflict and eye movement theories.

Motion sickness adaptation: a neural mismatch model.

The Machine behind the Stage: A Neurobiological Approach toward Theoretical Issues of Sensory Perception.

Electrocortical therapy for motion sickness.

The temporal range of motion sensing and motion perception.

Motion perception and aging.

The Perception of Auditory Motion.

The perception of visual motion.

Motion sickness: more than nausea and vomiting.

Occlusion and the perception of coherent motion.

Is there a relationship between odors and motion sickness?

Vestibular and postural findings in the motion sickness syndrome.

Motion sickness, nausea and thermoregulation: The "toxic" hypothesis.

Conflict Engagement: A Relational Approach.

Why is the driver rarely motion sick? The role of controllability in motion sickness.

Effects of ginger on motion sickness susceptibility and gastric function.

Reversed rotary motion perception.

Influence of Visual Motion, Suggestion, and Illusory Motion on Self-Motion Perception in the Horizontal Plane.

Attention-based motion perception.

The perception of shrinking in apparent motion.