35
Journal of Vestibular Research 25 (2015) 35–39 DOI 10.3233/VES-150542 IOS Press
Susceptibility to motion sickness is not increased following spinal cord injury Vaughan G. Macefielda,b,∗ and Darren K. Waltonc a
School of Medicine, University of Western Sydney, Sydney, Australia Neuroscience Research Australia, Sydney, Australia c Health Promotion Agency, Wellington, New Zealand b
Received 19 February 2014 Accepted 27 August 2014
Abstract. BACKGROUND: There are two leading theories on the origin of motion sickness. One, the sensory conflict theory, states that sensory information provided by one sensory channel does not match the expected input from another channel; commonly, these two inputs originate in the vestibular system and the eyes. The second theory – the postural instability theory – states that motion sickness comes about not through sensory conflict, but through an inability to control one’s posture. OBJECTIVE: Given that people with a motor-complete spinal cord injury cannot control their muscles below the level of the spinal lesion, we predicted that susceptibility to motion sickness would be higher in individuals who have suffered a spinal cord injury. METHODS: Twenty-one people living with chronic spinal cord injury (9 quadriplegics, 12 paraplegics) completed the Motion Sickness Susceptibility Questionnaire (MSSQ), via an online survey, to compare susceptibility to motion sickness before and after injury. RESULTS: Spinal cord injury, regardless of level, did not produce an increase in susceptibility to motion sickness. CONCLUSION: We have tested the general validity of the postural-instability theory by assessing susceptibility to motion sickness in individuals with spinal cord injury. Despite the loss of postural control, there was no increase in motion sickness susceptibility. Keywords: Motion sickness, spinal cord injury, vestibular
1. Introduction Motion sickness is a common disorder that is highest in childhood and, in most people, usually decreases in adulthood [1,10,13]. There are two leading theories as to how motion sickness comes about [11]. One, the sensory conflict theory, states that sensory information provided by one sensory channel does not match the expected input from another channel. Commonly, ∗ Corresponding author: Vaughan G. Macefield, Vaughan Macefield, School of Medicine, University of Western Sydney, Locked Bag 1797, Penrith NSW 2751, Australia. Tel.: +61 2 4620 3779; Fax: +61 2 4620 3880; E-mail: [email protected].
these two inputs originate in the vestibular system – the otoliths and semicircular canals – that detect changes in head position in space (or with respect to gravity) and the eyes. A common example is a child becoming sick in a car whilst reading; here, the vestibular system is telling the child’s brain that he or she is moving forwards, yet the visual input registers no such motion. A similar experience may occur on a boat in a heavy swell: the vestibular system is registering motion (in multiple axes) while the eyes may not register motion unless the gaze is fixed on the horizon. Visually-induced motion sickness, such as that produced by playing video games (cybersickness) – in which visual inputs are changing but vestibular inputs
c 2015 – IOS Press and the authors. All rights reserved ISSN 0957-4271/15/$35.00
36
V.G. Macefield and D.K. Walton / Susceptibility to motion sickness following spinal injury
are stable – can be explained similarly. Of course, it should be pointed out that blind people can experience motion sickness [6], and visual input is not necessary for motion sickness – one can suffer motion sickness in the dark. The second theory – the postural instability theory – states that motion sickness comes about not through sensory conflict, but through an inability to control one’s posture [15–19]: in the boat analogy, a person will become sick because he or she is unable to maintain an adequate posture. Recent support for this theory comes from the observation that people with a higher degree of postural sway at rest are more likely to experience sea sickness [20], but it could be argued that the increase in sensory feedback associated with the increase in sway presents as a conflict with the intended movement. Both theories have been criticized, with the sensoryconflict theory in particular being criticised for being untestable [10,17]. However, this criticism ignores the extensive data that relates coding of the spatial vertical and body angle by the vestibular system and the processing of eye velocity through velocity storage [2,3]. Moreover, the postural-instability theory, while framed in terms of motor control, could still be regarded as a form of sensory conflict, given that postural instability may be a reflection of disturbed proprioceptive information originating in the muscles and skin. Irrespective of the physiological foundations of the latter theory, there is one approach that could test the general validity of the postural instability theory. Given that people with a motor-complete spinal cord injury cannot control their muscles below the level of the spinal lesion, one would predict that susceptibility to motion sickness would be higher in individuals who have suffered a spinal cord injury. Moreover, given that more muscles are paralysed in quadriplegic people, who have sustained an injury in the cervical cord, one would predict that susceptibility to motion sickness would be elevated in these individuals compared to before the spinal injury. Likewise, paraplegics, in whom only the trunk and legs are paralysed from a thoracic or lumbar lesion, would also be expected to have an elevated susceptibility to motion sickness, though not as high as the quadriplegics. The purpose of the current study was to test the hypothesis that susceptibility to motion sickness, as assessed by administration of the Motion Sickness Susceptibility Questionaire (MSSQ) via an online survey, is higher following a spinal cord injury than before the injury. A secondary aim was to test the hypothesis that susceptibility to motion sickness is higher in quadriplegics than paraplegics.
2. Methods The study was conducted as an online survey by invitation to people with spinal cord injury who had registered their interest to participate through the Australian and New Zealand Spinal Cord Injury Network (ANZSCIN). The study was approved by the Human Research Ethics Committee of the University of Western Sydney. Participants volunteered and were not provided with any compensation for their time, as the survey was conducted at their own leisure. Standard questions from the Motion Sickness Susceptibility Questionnaire (MSSQ) [4,5] were presented online to registered participants, who provided their gender, age, whether they were quadriplegic or paraplegic, and the age at which they sustained their injury. Participants were asked to answer standard questions from the MSSQ, dealing with their susceptibility to sickness for various forms of transport as (i) a child < 12 years, (ii) as an adult prior to the spinal cord injury, and (iii) as an adult following the injury. All statistical analyses were performed using Prism 6 (GraphPad Software, USA); differences were considered significant at P < 0.05.
3. Results The MSSQ survey was completed by 23 participants, but data from two were excluded because their injuries did not result in complete paralysis below lesion. The mean (± SE) age of the included participants was 46 years ± 2 years; the mean age at which the injury was sustained was 33 years ± 3 years. Nine of the subjects (5 male, 4 female) were defined as quadriplegic, 12 (7 male, 5 female) as paraplegic. Composite MSSQ scores are shown for all participants in Fig. 1(a). Repeated measures analysis of variance (RMANOVA), coupled with Friedman’s test for multiple comparisons, revealed no significant differences in susceptibility to motion sickness between childhood, adulthood and following spinal cord injury. However, if we simply compared mean MSSQ scores in childhood and adulthood, we could see that – as expected – susceptibility to motion sickness was highest in childhood (p = 0.0423, paired t-test). A similar restricted analysis, in which mean scores were compared in adulthood before and after spinal cord injury, revealed that these scores tended to be lower following spinal cord injury, although this difference was not statistically significant (p = 0.2242, Wilcoxon matchedpairs test). There was no difference when the partic-
V.G. Macefield and D.K. Walton / Susceptibility to motion sickness following spinal injury
37
an increase in susceptibility to motion sickness, at least as reflected in the mean MSSQ scores. In addition to the standard MSSQ, subjects were asked to respond to specific questions regarding motion sickness. Only three participants considered themselves to be strongly susceptible to motion sickness, selecting “very much so”, while two considered themselves to be “moderately susceptible” and seven “slightly susceptible”; nine did not consider themselves to be prone to motion sickness. Just over half (12/21; 57%) did not consider themselves to be more susceptible to motion sickness following their spinal injury, though seven participants did report that they felt more susceptible and two had selected “maybe”. However, only four participants indicated that they avoided certain modes of transport because of motion sickness.
4. Discussion
Fig. 1. Composite scores from the Motion Sickness Symptoms Questionaire (MSSQ) survey, conducted on 21 people with chronic spinal cord injury; pooled data are shown in (a), with data from subjects with quadriplegia and paraplegia being shown in (b) and (c), respectively. There were no significant differences in MSSQ scores when the participants were asked to rate their sensitivity as a child, as an adult prior to the spinal cord injury and as an adult following the injury.
ipants were divided according to lesion level: mean scores for the quadriplegics and paraplegics are shown in Figs 1(b) and (c), respectively. We can conclude that spinal cord injury, regardless of level, did not produce
We have shown that susceptibility to motion sickness is not increased following a spinal cord injury, either in individuals with cervical lesions and hence paralysis of the arms, trunk and legs, or those with thoracic or lumbar lesions and hence paralysis of the trunk and/or lower limb muscles. Accordingly, we reject the two hypotheses we set out to test. We know that subjects with a high cervical spinal lesion have essentially normal thresholds for detecting acceleration of the body, indicating that somatosensory inputs below the lesion are not as important as sensory receptors in the head (i.e. within the vestibular apparatus) in providing information on motion in the absence of visual cues [9,21]. Moreover, movement detection thresholds are ∼ 10x higher in individuals with bilateral damage to the vestibular organs [21]. There is no doubt that excitation of vestibular inputs can induce motion sickness, and selective stimulation of the vestibular nerves, through sinusoidal galvanic vestibular stimulation at frequencies 0.2 Hz, can precipitate nausea in certain individuals [7,8]. Because the vestibular system is intact in people with spinal cord injuries, any changes in head position will be faithfully encoded by afferents within the semicircular canals (sensitive to rotational acceleration) and the utricular and saccular components of the otolithic organs, sensitive to linear acceleration in the horizontal and vertical planes, respectively. This means that reflexly-generated increases in motor output to the postural muscles still occur in people with spinal cord in-
38
V.G. Macefield and D.K. Walton / Susceptibility to motion sickness following spinal injury
jury during changes in position of the head with respect to gravity, or during rotational or linear acceleration of the body in space; vestibulospinal output still occurs, but is ineffective owing to paralysis of the trunk and limb muscles. In addition to appropriate motor signals being generated during automatic reactions to movements of the head and/or body in individuals with spinal injury, motor commands will still be generated during volitional responses to postural changes – despite the paralysis of muscles below the lesion. What is different, of course, is that any postural reactions are ineffective in spinal cord injury. So, according to the postural-instability theory, the loss of postural control posited to underlie motion sickness [15], would be greatly exaggerated, and so would motion sickness. Given that the central tenet of this theory is that “motion sickness results from prolonged instability in the control of posture” [15] it would appear that the current results lend no support to this theory. It is also worth pointing out that a complete spinal lesion will prevent proprioceptive feedback from the paralysed muscles and skin from reaching the brain; accordingly, any volitional motor commands, or motor output generated in response to a postural disturbance, will occur in the absence of sensory input. As such, this lack of afferent input can be seen as a sensory conflict between the expected proprioceptive input and the sensory input conveyed by the vestibular and visual systems; whether this of itself promotes motion sickness is a matter of speculation.
5. Limitations This was a survey that was open to anyone with a spinal cord injury, so it could be argued that those who chose to participate had an interest in motion sickness and hence the sample may be biased. The means by which the survey was promoted was through an online monthly newsletter put out by the Australia and New Zealand Spinal Cord Injury Network, which provides subscribers to information about available research projects. Because this was an online survey that did not take long to complete, and requested no personally identifying information, we are confident that the current results reflect an adequate sample of responses from individuals living with chronic spinal cord injury. Nine of the participants identified as quadriplegic, twelve as paraplegic, with slightly more male (n = 12) than female (n = 9) participants. While more males than females suffer spinal cord injuries, owing to the
higher risk-taking amongst young adult males, the current gender distribution no doubt reflects the willingness of older people to participate in research surveys such as this; most of the participants were 40–60 years of age. The MSSQ is a reliable instrument validated in clinical settings [4,5]. However, we should point out that the MSSQ was not designed for use within the current study. The assumption of the MSSQ is that there is equal opportunity to engage with or avoid typical sources of motion sickness such as driving, trains, buses, or roller coasters. When this is untrue because of changing patterns of behavior through aging, experience or injury, then the results might be somewhat conservative. It is typical to find adult scores are significantly lower than those of children, and this was confirmed in the present study. What is clear from the design of the MSSQ is that people have a good ability to report their sensitivity, and changes to that sensitivity. The increases in overall sensitivity to motion sickness that are reported for some of participants signals a need for further investigation to determine the reason behind such changes. Finally, this study was an online survey that asked subjects to compare their current susceptibility to motion sickness while living with spinal cord injury with their recollections of their susceptibility prior to the injury. Our original aim was to recruit a sufficient number of individuals with spinal cord injury, seated on a motorized platform, and expose them to lowfrequency sinusoidal linear acceleration. We have used this method previously to study vestibulo-sympathetic reflexes in able-bodied subjects [9], but it proved too difficult to recruit suitable participants for a laboratorybased study – hence the current study design. Nevertheless, as noted above, the current data do indicate that further studies on susceptibility to motion sickness in individuals with spinal cord injury are warranted.
6. Conclusions We have tested the general validity of the posturalinstability theory by assessing susceptibility to motion sickness in individuals who are living with chronic spinal cord injury. We predicted that sensitivity to motion sickness would be increased in spinal individuals, owing to the loss of postural control, but this was not borne out.
V.G. Macefield and D.K. Walton / Susceptibility to motion sickness following spinal injury
References [1] [2]
[3]
[4]
[5]
[6] [7]
[8]
[9]
A.J. Benson, Motion Sickness, New York: Wiley and Sons, 1984. M. Dai, T. Raphan and B. Cohen, Labyrinthine lesions and motion sickness susceptibility, Experimental Brain Research 178 (2007), 477–487. M. Dai, S. Sofroniou, M. Kunin, T. Raphan and B. Cohen, Motion sickness induced by off-vertical axis rotation (OVAR), Experimental Brain Research 204 (2010), 207–222. J.F. Golding, Motion sickness susceptibility questionnaire revised and its relationship to other forms of sickness, Brain Research Bulletin 47 (1998), 507–516. J.F. Golding, Predicting individual differences in motion sickness susceptibility by questionnaire, Personality and Individual Differences 41 (2006), 237–248. A. Graybriel, Susceptibility to acute motion sickness in blind persons, Aerospace Medicine 41 (1970), 650–653. T. Grewal, C. James and V.G. Macefield, Frequencydependent modulation of muscle sympathetic nerve activity by sinusoidal galvanic vestibular stimulation in human subjects, Experimental Brain Research 197 (2009), 379–386. E. Hammam, T. Dawood and V.G. Macefield, Low-frequency galvanic vestibular stimulation evokes two peaks of modulation in skin sympathetic nerve activity, Experimental Brain Research 219 (2012), 441–446. E. Hammam, C.L.V. Hau, K.-S. Wong, K. Kwok and V.G. Macefield, Vestibular modulation of muscle sympathetic nerve activity by the utricle during sub-perceptual sinusoidal linear acceleration in humans, Experimental Brain Research (2014), in press.
[10]
39
K.E. Money, Motion sickness, Psychological Reviews 50 (1970), 1–39. [11] T.H. Probst and U. Schmidt, The sensory conflict concept for the generation of nausea, Journal of Psychophysiology 12 (1998), 34–49. [12] J.T. Reason, Motion sickness adaptation: A neural mismatch model, Journal of the Royal Society of Medicine 1(7) (1978), 819–829. [13] J.T. Reason and J.J. Brand, Motion sickness, (1975) London: Academic Press. [14] J.T. Reason, Relations between motion sickness susceptibility, the spiral after-effect and loudness estimation, British Journal of Psychology 59 (1968), 385–393. [15] G.E. Riccio and T.A. Stoffregen, An ecological theory of motion sickness and postural instability, Ecological Psychology 3 (1991), 195–240. [16] T.A. Stoffregen and G.E. Riccio, An ecological theory of orientation of the vestibular system, Psychological Review 95 (1988), 3–14. [17] T.A. Stoffregen and G.E. Riccio, An ecological critique of the sensory conflict theory of motion sickness, Ecological Psychology 3 (1991), 159–194. [18] T.A. Stoffregen and L.J. Smart, Postural instability preceded motion sickness, Brain Research Bulletin 47 (1998), 437–448. [19] T.A. Stoffregen, K. Yoshida, S. Villard, L. Scibora and B. Bardy, Stance width influences postural stability and motion sickness, Ecological Psychology 22 (2010), 169–191. [20] T.A. Stoffregen, F.C. Chen, M. Varlet, C. Alcantara and B.G. Bardy, Getting your sea legs, PLoS One 8 (2013), e66949. [21] E. Walsh, Role of the vestibular apparatus in the perception of motion on a parallel swing, Journal of Physiology 155 (1961), 506–513.
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Journal of Vestibular Research 25 (2015) 35–39 DOI 10.3233/VES-150542 IOS Press
Susceptibility to motion sickness is not increased following spinal cord injury Vaughan G. Macefielda,b,∗ and Darren K. Waltonc a
School of Medicine, University of Western Sydney, Sydney, Australia Neuroscience Research Australia, Sydney, Australia c Health Promotion Agency, Wellington, New Zealand b
Received 19 February 2014 Accepted 27 August 2014
Abstract. BACKGROUND: There are two leading theories on the origin of motion sickness. One, the sensory conflict theory, states that sensory information provided by one sensory channel does not match the expected input from another channel; commonly, these two inputs originate in the vestibular system and the eyes. The second theory – the postural instability theory – states that motion sickness comes about not through sensory conflict, but through an inability to control one’s posture. OBJECTIVE: Given that people with a motor-complete spinal cord injury cannot control their muscles below the level of the spinal lesion, we predicted that susceptibility to motion sickness would be higher in individuals who have suffered a spinal cord injury. METHODS: Twenty-one people living with chronic spinal cord injury (9 quadriplegics, 12 paraplegics) completed the Motion Sickness Susceptibility Questionnaire (MSSQ), via an online survey, to compare susceptibility to motion sickness before and after injury. RESULTS: Spinal cord injury, regardless of level, did not produce an increase in susceptibility to motion sickness. CONCLUSION: We have tested the general validity of the postural-instability theory by assessing susceptibility to motion sickness in individuals with spinal cord injury. Despite the loss of postural control, there was no increase in motion sickness susceptibility. Keywords: Motion sickness, spinal cord injury, vestibular
1. Introduction Motion sickness is a common disorder that is highest in childhood and, in most people, usually decreases in adulthood [1,10,13]. There are two leading theories as to how motion sickness comes about [11]. One, the sensory conflict theory, states that sensory information provided by one sensory channel does not match the expected input from another channel. Commonly, ∗ Corresponding author: Vaughan G. Macefield, Vaughan Macefield, School of Medicine, University of Western Sydney, Locked Bag 1797, Penrith NSW 2751, Australia. Tel.: +61 2 4620 3779; Fax: +61 2 4620 3880; E-mail: [email protected].
these two inputs originate in the vestibular system – the otoliths and semicircular canals – that detect changes in head position in space (or with respect to gravity) and the eyes. A common example is a child becoming sick in a car whilst reading; here, the vestibular system is telling the child’s brain that he or she is moving forwards, yet the visual input registers no such motion. A similar experience may occur on a boat in a heavy swell: the vestibular system is registering motion (in multiple axes) while the eyes may not register motion unless the gaze is fixed on the horizon. Visually-induced motion sickness, such as that produced by playing video games (cybersickness) – in which visual inputs are changing but vestibular inputs
c 2015 – IOS Press and the authors. All rights reserved ISSN 0957-4271/15/$35.00
36
V.G. Macefield and D.K. Walton / Susceptibility to motion sickness following spinal injury
are stable – can be explained similarly. Of course, it should be pointed out that blind people can experience motion sickness [6], and visual input is not necessary for motion sickness – one can suffer motion sickness in the dark. The second theory – the postural instability theory – states that motion sickness comes about not through sensory conflict, but through an inability to control one’s posture [15–19]: in the boat analogy, a person will become sick because he or she is unable to maintain an adequate posture. Recent support for this theory comes from the observation that people with a higher degree of postural sway at rest are more likely to experience sea sickness [20], but it could be argued that the increase in sensory feedback associated with the increase in sway presents as a conflict with the intended movement. Both theories have been criticized, with the sensoryconflict theory in particular being criticised for being untestable [10,17]. However, this criticism ignores the extensive data that relates coding of the spatial vertical and body angle by the vestibular system and the processing of eye velocity through velocity storage [2,3]. Moreover, the postural-instability theory, while framed in terms of motor control, could still be regarded as a form of sensory conflict, given that postural instability may be a reflection of disturbed proprioceptive information originating in the muscles and skin. Irrespective of the physiological foundations of the latter theory, there is one approach that could test the general validity of the postural instability theory. Given that people with a motor-complete spinal cord injury cannot control their muscles below the level of the spinal lesion, one would predict that susceptibility to motion sickness would be higher in individuals who have suffered a spinal cord injury. Moreover, given that more muscles are paralysed in quadriplegic people, who have sustained an injury in the cervical cord, one would predict that susceptibility to motion sickness would be elevated in these individuals compared to before the spinal injury. Likewise, paraplegics, in whom only the trunk and legs are paralysed from a thoracic or lumbar lesion, would also be expected to have an elevated susceptibility to motion sickness, though not as high as the quadriplegics. The purpose of the current study was to test the hypothesis that susceptibility to motion sickness, as assessed by administration of the Motion Sickness Susceptibility Questionaire (MSSQ) via an online survey, is higher following a spinal cord injury than before the injury. A secondary aim was to test the hypothesis that susceptibility to motion sickness is higher in quadriplegics than paraplegics.
2. Methods The study was conducted as an online survey by invitation to people with spinal cord injury who had registered their interest to participate through the Australian and New Zealand Spinal Cord Injury Network (ANZSCIN). The study was approved by the Human Research Ethics Committee of the University of Western Sydney. Participants volunteered and were not provided with any compensation for their time, as the survey was conducted at their own leisure. Standard questions from the Motion Sickness Susceptibility Questionnaire (MSSQ) [4,5] were presented online to registered participants, who provided their gender, age, whether they were quadriplegic or paraplegic, and the age at which they sustained their injury. Participants were asked to answer standard questions from the MSSQ, dealing with their susceptibility to sickness for various forms of transport as (i) a child < 12 years, (ii) as an adult prior to the spinal cord injury, and (iii) as an adult following the injury. All statistical analyses were performed using Prism 6 (GraphPad Software, USA); differences were considered significant at P < 0.05.
3. Results The MSSQ survey was completed by 23 participants, but data from two were excluded because their injuries did not result in complete paralysis below lesion. The mean (± SE) age of the included participants was 46 years ± 2 years; the mean age at which the injury was sustained was 33 years ± 3 years. Nine of the subjects (5 male, 4 female) were defined as quadriplegic, 12 (7 male, 5 female) as paraplegic. Composite MSSQ scores are shown for all participants in Fig. 1(a). Repeated measures analysis of variance (RMANOVA), coupled with Friedman’s test for multiple comparisons, revealed no significant differences in susceptibility to motion sickness between childhood, adulthood and following spinal cord injury. However, if we simply compared mean MSSQ scores in childhood and adulthood, we could see that – as expected – susceptibility to motion sickness was highest in childhood (p = 0.0423, paired t-test). A similar restricted analysis, in which mean scores were compared in adulthood before and after spinal cord injury, revealed that these scores tended to be lower following spinal cord injury, although this difference was not statistically significant (p = 0.2242, Wilcoxon matchedpairs test). There was no difference when the partic-
V.G. Macefield and D.K. Walton / Susceptibility to motion sickness following spinal injury
37
an increase in susceptibility to motion sickness, at least as reflected in the mean MSSQ scores. In addition to the standard MSSQ, subjects were asked to respond to specific questions regarding motion sickness. Only three participants considered themselves to be strongly susceptible to motion sickness, selecting “very much so”, while two considered themselves to be “moderately susceptible” and seven “slightly susceptible”; nine did not consider themselves to be prone to motion sickness. Just over half (12/21; 57%) did not consider themselves to be more susceptible to motion sickness following their spinal injury, though seven participants did report that they felt more susceptible and two had selected “maybe”. However, only four participants indicated that they avoided certain modes of transport because of motion sickness.
4. Discussion
Fig. 1. Composite scores from the Motion Sickness Symptoms Questionaire (MSSQ) survey, conducted on 21 people with chronic spinal cord injury; pooled data are shown in (a), with data from subjects with quadriplegia and paraplegia being shown in (b) and (c), respectively. There were no significant differences in MSSQ scores when the participants were asked to rate their sensitivity as a child, as an adult prior to the spinal cord injury and as an adult following the injury.
ipants were divided according to lesion level: mean scores for the quadriplegics and paraplegics are shown in Figs 1(b) and (c), respectively. We can conclude that spinal cord injury, regardless of level, did not produce
We have shown that susceptibility to motion sickness is not increased following a spinal cord injury, either in individuals with cervical lesions and hence paralysis of the arms, trunk and legs, or those with thoracic or lumbar lesions and hence paralysis of the trunk and/or lower limb muscles. Accordingly, we reject the two hypotheses we set out to test. We know that subjects with a high cervical spinal lesion have essentially normal thresholds for detecting acceleration of the body, indicating that somatosensory inputs below the lesion are not as important as sensory receptors in the head (i.e. within the vestibular apparatus) in providing information on motion in the absence of visual cues [9,21]. Moreover, movement detection thresholds are ∼ 10x higher in individuals with bilateral damage to the vestibular organs [21]. There is no doubt that excitation of vestibular inputs can induce motion sickness, and selective stimulation of the vestibular nerves, through sinusoidal galvanic vestibular stimulation at frequencies 0.2 Hz, can precipitate nausea in certain individuals [7,8]. Because the vestibular system is intact in people with spinal cord injuries, any changes in head position will be faithfully encoded by afferents within the semicircular canals (sensitive to rotational acceleration) and the utricular and saccular components of the otolithic organs, sensitive to linear acceleration in the horizontal and vertical planes, respectively. This means that reflexly-generated increases in motor output to the postural muscles still occur in people with spinal cord in-
38
V.G. Macefield and D.K. Walton / Susceptibility to motion sickness following spinal injury
jury during changes in position of the head with respect to gravity, or during rotational or linear acceleration of the body in space; vestibulospinal output still occurs, but is ineffective owing to paralysis of the trunk and limb muscles. In addition to appropriate motor signals being generated during automatic reactions to movements of the head and/or body in individuals with spinal injury, motor commands will still be generated during volitional responses to postural changes – despite the paralysis of muscles below the lesion. What is different, of course, is that any postural reactions are ineffective in spinal cord injury. So, according to the postural-instability theory, the loss of postural control posited to underlie motion sickness [15], would be greatly exaggerated, and so would motion sickness. Given that the central tenet of this theory is that “motion sickness results from prolonged instability in the control of posture” [15] it would appear that the current results lend no support to this theory. It is also worth pointing out that a complete spinal lesion will prevent proprioceptive feedback from the paralysed muscles and skin from reaching the brain; accordingly, any volitional motor commands, or motor output generated in response to a postural disturbance, will occur in the absence of sensory input. As such, this lack of afferent input can be seen as a sensory conflict between the expected proprioceptive input and the sensory input conveyed by the vestibular and visual systems; whether this of itself promotes motion sickness is a matter of speculation.
5. Limitations This was a survey that was open to anyone with a spinal cord injury, so it could be argued that those who chose to participate had an interest in motion sickness and hence the sample may be biased. The means by which the survey was promoted was through an online monthly newsletter put out by the Australia and New Zealand Spinal Cord Injury Network, which provides subscribers to information about available research projects. Because this was an online survey that did not take long to complete, and requested no personally identifying information, we are confident that the current results reflect an adequate sample of responses from individuals living with chronic spinal cord injury. Nine of the participants identified as quadriplegic, twelve as paraplegic, with slightly more male (n = 12) than female (n = 9) participants. While more males than females suffer spinal cord injuries, owing to the
higher risk-taking amongst young adult males, the current gender distribution no doubt reflects the willingness of older people to participate in research surveys such as this; most of the participants were 40–60 years of age. The MSSQ is a reliable instrument validated in clinical settings [4,5]. However, we should point out that the MSSQ was not designed for use within the current study. The assumption of the MSSQ is that there is equal opportunity to engage with or avoid typical sources of motion sickness such as driving, trains, buses, or roller coasters. When this is untrue because of changing patterns of behavior through aging, experience or injury, then the results might be somewhat conservative. It is typical to find adult scores are significantly lower than those of children, and this was confirmed in the present study. What is clear from the design of the MSSQ is that people have a good ability to report their sensitivity, and changes to that sensitivity. The increases in overall sensitivity to motion sickness that are reported for some of participants signals a need for further investigation to determine the reason behind such changes. Finally, this study was an online survey that asked subjects to compare their current susceptibility to motion sickness while living with spinal cord injury with their recollections of their susceptibility prior to the injury. Our original aim was to recruit a sufficient number of individuals with spinal cord injury, seated on a motorized platform, and expose them to lowfrequency sinusoidal linear acceleration. We have used this method previously to study vestibulo-sympathetic reflexes in able-bodied subjects [9], but it proved too difficult to recruit suitable participants for a laboratorybased study – hence the current study design. Nevertheless, as noted above, the current data do indicate that further studies on susceptibility to motion sickness in individuals with spinal cord injury are warranted.
6. Conclusions We have tested the general validity of the posturalinstability theory by assessing susceptibility to motion sickness in individuals who are living with chronic spinal cord injury. We predicted that sensitivity to motion sickness would be increased in spinal individuals, owing to the loss of postural control, but this was not borne out.
V.G. Macefield and D.K. Walton / Susceptibility to motion sickness following spinal injury
References [1] [2]
[3]
[4]
[5]
[6] [7]
[8]
[9]
A.J. Benson, Motion Sickness, New York: Wiley and Sons, 1984. M. Dai, T. Raphan and B. Cohen, Labyrinthine lesions and motion sickness susceptibility, Experimental Brain Research 178 (2007), 477–487. M. Dai, S. Sofroniou, M. Kunin, T. Raphan and B. Cohen, Motion sickness induced by off-vertical axis rotation (OVAR), Experimental Brain Research 204 (2010), 207–222. J.F. Golding, Motion sickness susceptibility questionnaire revised and its relationship to other forms of sickness, Brain Research Bulletin 47 (1998), 507–516. J.F. Golding, Predicting individual differences in motion sickness susceptibility by questionnaire, Personality and Individual Differences 41 (2006), 237–248. A. Graybriel, Susceptibility to acute motion sickness in blind persons, Aerospace Medicine 41 (1970), 650–653. T. Grewal, C. James and V.G. Macefield, Frequencydependent modulation of muscle sympathetic nerve activity by sinusoidal galvanic vestibular stimulation in human subjects, Experimental Brain Research 197 (2009), 379–386. E. Hammam, T. Dawood and V.G. Macefield, Low-frequency galvanic vestibular stimulation evokes two peaks of modulation in skin sympathetic nerve activity, Experimental Brain Research 219 (2012), 441–446. E. Hammam, C.L.V. Hau, K.-S. Wong, K. Kwok and V.G. Macefield, Vestibular modulation of muscle sympathetic nerve activity by the utricle during sub-perceptual sinusoidal linear acceleration in humans, Experimental Brain Research (2014), in press.
[10]
39
K.E. Money, Motion sickness, Psychological Reviews 50 (1970), 1–39. [11] T.H. Probst and U. Schmidt, The sensory conflict concept for the generation of nausea, Journal of Psychophysiology 12 (1998), 34–49. [12] J.T. Reason, Motion sickness adaptation: A neural mismatch model, Journal of the Royal Society of Medicine 1(7) (1978), 819–829. [13] J.T. Reason and J.J. Brand, Motion sickness, (1975) London: Academic Press. [14] J.T. Reason, Relations between motion sickness susceptibility, the spiral after-effect and loudness estimation, British Journal of Psychology 59 (1968), 385–393. [15] G.E. Riccio and T.A. Stoffregen, An ecological theory of motion sickness and postural instability, Ecological Psychology 3 (1991), 195–240. [16] T.A. Stoffregen and G.E. Riccio, An ecological theory of orientation of the vestibular system, Psychological Review 95 (1988), 3–14. [17] T.A. Stoffregen and G.E. Riccio, An ecological critique of the sensory conflict theory of motion sickness, Ecological Psychology 3 (1991), 159–194. [18] T.A. Stoffregen and L.J. Smart, Postural instability preceded motion sickness, Brain Research Bulletin 47 (1998), 437–448. [19] T.A. Stoffregen, K. Yoshida, S. Villard, L. Scibora and B. Bardy, Stance width influences postural stability and motion sickness, Ecological Psychology 22 (2010), 169–191. [20] T.A. Stoffregen, F.C. Chen, M. Varlet, C. Alcantara and B.G. Bardy, Getting your sea legs, PLoS One 8 (2013), e66949. [21] E. Walsh, Role of the vestibular apparatus in the perception of motion on a parallel swing, Journal of Physiology 155 (1961), 506–513.
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