Neuroscience Letters 566 (2014) 326–330
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Is there a relationship between odors and motion sickness? A.C. Paillard a,b,c , M. Lamôré a,b,c , O. Etard c,d , J.-L. Millot e , L. Jacquot e , P. Denise a,b,c,d , G. Quarck a,b,c,∗ a
UNICAEN, COMETE, 14032 Caen, France INSERM, U1075, 14032 Caen, France Normandie Univ, Caen, France d CHU de Caen, Service des Explorations Fonctionnelles, 14000 Caen, France e Université de Franche-Comté, Laboratoire de Neurosciences, 25000 Besanc¸on, France b c
h i g h l i g h t s • We evaluate the relationship between olfaction and motion sickness. • Our study highlighted the lack of influence of odors in motion-induced sickness. • Our results showed an impact of a nauseogenic test on olfactory perception.
a r t i c l e
i n f o
Article history: Received 11 June 2013 Received in revised form 18 February 2014 Accepted 22 February 2014 Keywords: Motion sickness OVAR Odor Perception
a b s t r a c t The aim of this study was to evaluate the relationship between olfaction and motion sickness. A sample of 18 participants was recruited and submitted to three sessions of nauseogenic stimulations: off vertical axis rotation (OVAR), performed under conditions of olfactory stimulation with limonene (pleasant odor), petrol (unpleasant odor) or distilled water (as a control). Motion sickness was assessed before, during and after each OVAR session. In addition, participants were asked to evaluate the intensity and hedonic valence of four odors (geraniol, limonene, butanol, petrol) as well as distilled water (as a control) before and after each OVAR session. Our analysis showed that OVAR has consistently increased the inducedmotion sickness. However the addition of an odor that is pleasant or unpleasant during the rotation did not affect the occurrence of motion sickness symptoms compared to the control condition. Our results also showed that intensity of odors was significantly increased after OVAR and the intensity was significantly higher for unpleasant odors than for pleasant one. For the hedonicity, OVAR made unpleasant odors more unpleasant (p < 0.0001) while it made limonene odor slightly more pleasant (p < 0.05). The present study highlighted the lack of influence of odors in motion-induced sickness but an impact of a nauseogenic test on olfactory perception. © 2014 Elsevier Ireland Ltd. All rights reserved.
Introduction Technological evolution of modern transports, such as cars or trains, significantly increases motion sickness symptoms occurrence. Motion sickness (MS) is defined by a set of four main symptoms that regularly appear: facial pallor, cold sweats, nausea and vomiting. Other additional signs such as dizziness, headache, fatigue, postural instability, which are more variable in their appearance and duration, can be also observed [9]. One of the most established theories to explain in which circumstances
∗ Corresponding author at: UMR UCBN INSERM U1075 COMETE, 14032 Caen, France. Tel.: +33 2 31 56 72 63. E-mail address: [email protected] (G. Quarck). http://dx.doi.org/10.1016/j.neulet.2014.02.049 0304-3940/© 2014 Elsevier Ireland Ltd. All rights reserved.
motion sickness arises is the “sensory conflict” theory [21]. This theory postulates that motion sickness originates from a sensory mismatch between actual versus expected invariant patterns of vestibular, visual and somatosensory inputs [21]. It has been accepted that the vestibular system influences individual motion sickness susceptibility (MSS) since patients with bilateral vestibular deficit have greatly reduced susceptibility or do not become motion sick at all [15,25]. This sensory mismatch leads to an activation of vestibuloautonomic pathways, which have been shown to be also involved in producing nausea and vomiting during motion sickness and those that generate illness after ingestion of toxins [25]. Among factors that may contribute to motion sickness, such as alcohol or hunger, the presence of strong smells is very often reported by individuals who are sensitive to motion sickness.
A.C. Paillard et al. / Neuroscience Letters 566 (2014) 326–330
Similarly, there are a variety of companies claiming that the inhalation of some essential oils can alleviate motion sickness symptoms. Besides, an interesting parallel between motion sickness and the olfactory system may be underlined. On one hand, it is granted that women are more sensitive to motion sickness than men [7,18,19]; in particular, it has been shown that the MSS fluctuates across menstrual cycle [10,11] as a consequence of hormonal variation [2]. On the other hand, women demonstrate better olfactory abilities than men [1]. But, surprisingly, the link between olfaction and MSS has been poorly investigated by the research community. Sharma and Aparna [22] showed that participants with high-MSS were more sensitive to unpleasant odors. Fessler and Arguello [6], who asked participants to report on a 5-point scale how sensitive they were to unpleasant odors, highlighted a positive correlation between sensitivity to unpleasant odors and MSS in women. Similarly, Paillard et al. [18] reported pilot data demonstrating that high-MSS participants perceived the odors of petrol and leather as more unpleasant than participants who were not sensitive to motion sickness. The aim of the present study is to delve further into these initial findings and to assess the relationship between odors and motion sickness. We can question the influence of odors on motion-induced sickness (i.e. can pleasant or unpleasant odors have an influence on MS symptoms occurrence?) as well as the influence of motioninduced sickness on the perceived quality of an odor (i.e. can a nauseogenic test influence odors intensity and hedonicity?). The study focuses specifically on these two dimensions because they have long been recognized as the most important features of odors [12,26]. Previous study showed that high-MSS participants are more sensitive to unpleasant odors [22] and also perceived the odors of petrol and leather as more unpleasant than participants who were not sensitive to motion sickness [18]. Moreover, Herz et al. [13] supported the statement that hedonic judgment of familiar odors is deteriorated in an unpleasant context. Besides, it has been shown that the perceived intensity depends, at least in part, on experience-dependent factors [5]. Thus, our hypotheses are that (i) the motion sickness occurrence may be influenced by unpleasant odors such as petrol or leather during a nauseogenic test; (ii) pleasant odors smelt by participants during a nauseogenic test are perceived as less pleasant after the test and unpleasant odors are perceived as more unpleasant and (iii) perceived intensity of odors is increased after a nauseogenic test.
Material and methods Participants A sample of 18 volunteer participants (mean age 23.8 years old, range 19–40 years old, 11 women and 7 men) was recruited in this experiment. In order to assess the MSS, participants were required to complete the motion sickness susceptibility questionnaire (MSSQ) [8]. According to Paillard et al. [18], who found that high-MSS subjects judged odors related to transports as more unpleasant than low-MSS subjects, our participants were divided in two groups: 10 subjects represent low MSS individuals (MSSQ scores from 0 to 10.75; 6 women and 4 men) and 8 subjects represent high MSS individuals (MSSQ scores from 17.63 to 44; 5 women and 3 men). All participants were non-smokers and reported normal smell sensitivity. None of them had a history of nasal/sinus disease or extensive exposure to chemical with potential olfactory toxicity. Participants with past or present otologic or neurological disorders were not included in the study. Women were not tested during their menses period. All participants provided informed written consent.
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This study was conducted in accordance with the Declaration of Helsinki (1964). Motion sickness induction and symptoms ratings The off vertical axis rotation (OVAR) test is ideal for our purpose, as it has been established that it is highly effective in evoking MS. On the basis of a previous study performed in the laboratory [4], the stimulation parameters (70◦ s−1 , 15◦ tilt, in total darkness) were chosen to make the examination moderately nauseogenic. Subjects were comfortably seated and secured into a rotating chair driven by a torque. They were restrained by means of a seat belt. The center of their head was also positioned and maintained at the center of the rotation by means of a concave headrest and a helmet fixed to the chair. The degree of motion sickness during OVAR test (i.e. motion sickness rating, MSR) has been used to define the end-point of the OVAR test. MSR was rated every minute; (1): no symptom; (2): initial symptoms but no nausea; (3): mild nausea; (4): moderate nausea. The MSR score is defined as the time (in minutes) to reach MSR-level 3, which was defined as the end-point of each OVAR test. Motion sickness symptoms were also assessed before and after motion with the simulator sickness questionnaire (SSQ) [17] that probes polysymptomatic responses to motion and yields a score between 0 (no symptoms) and 51 (maximum symptoms). Odorants For the test of olfactory perception, four specific odorants were used: two pleasant odors (geraniol and limonene, corresponding to rose- and orange-like smells, respectively) and two unpleasant odors (n-butanol and petrol). Pleasantness scores of each odor were obtained from preliminary self-report ratings. We also used distilled water as a control condition. The dilutions used in our study have been determined according to a pretest carried out on 10 participants: three dilution series (100%, 50%, 25%) were prepared for each odorant and participants were required to rate from 0 (weak) to 10 (strong) the perceived intensity of odors. The dilutions that reach a similar moderate perceived intensity have been chosen for the tests. Specifically, geraniol and limonene were used without dilution (100% of the stock solution), while petrol and butanol were diluted at 25% in odorless mineral oil. Four milliliters of each odorant solution was placed into glass tubes (6.5 cm high, 1 cm at the opening). For the OVAR session, 10 L of pure limonene or 25% petrol or distilled water was placed on a piece of cotton attached to participant facemask. The concentrations for each odorant were determined during pretesting such as they were both of equal perceived intensity. Before and after the nauseogenic test, participants were asked to rate the perceived intensity and hedonic valence of the four odors as well as the control odor on analogic scales ranging from 0 (weak/unpleasant) to 10 (strong/pleasant). Procedure The experiment consisted of three OVAR sessions. In order to avoid habituation, there was at least one week between each session. Before each OVAR session the test of olfactory perception of the four odors (geraniol, limonene, butanol and petrol) and the distilled water was carried out in a separate room. Odor presentation order was randomized for each participant. At the beginning of each OVAR session, participants were informed on how to recognize symptoms of motion sickness as they developed and how to report them. Then the first SSQ was administered. The participant seated on the OVAR chair and was equipped with a facemask soaked with limonene, petrol or distilled water. The participants performed these three sessions in a random order (balanced for order design) and the OVAR stimulation always started immediately after
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the facemask application. During stimulation, the participant was requested to verbally report every minute his/her degree of motion sickness (MSR). The stimulation was stopped at MSR-level 3 or after 16 min whichever came first. Immediately following cessation of motion, the second SSQ was administered. Then, after a 10-min break, the four odors (geraniol, limonene, butanol and petrol) as well as the distilled water were once again randomly tested in a separate room. Statistical analysis A mixed-model analysis of variance and covariance followed by contrasts analysis when necessary were performed using linear mixed effects models and the R package nmle (R Core Team) [23]. In the first part of the analysis, independent variables studied were SSQ scores. We tested the following factors as fixed effects in the model: OVAR with 2 levels (before and after); odors-during-OVAR with three levels (pleasant, unpleasant and control); MSS of subject with two levels (low and high). Subject factor is used as random effects. In the second part of the analysis, independent variables studied were the intensity variations and the hedonicity variations of the odors tested after-OVAR sessions in comparison with the pre-OVAR test. In order to determine if the motion sickness susceptibility of the subjects and the odors perceived during OVAR have an effect on the olfactory perception test realized after OVAR, two factors were added in the model: MSS of subjects (high or low MSS) and type of odors during OVAR (pleasant, unpleasant, control). Moreover, subject factor was used as random effects. Subject factor is used as random effects. The fitted values calculated by the model were used for Fig. 2. In all cases, normality and homogeneity of the model’s error were checked by inspections of plots of residuals against fitted values. Results Odor during OVAR and motion sickness occurrence Fig. 1 shows the SSQ values before and after OVAR and the MSR for pleasant (limonene), unpleasant (petrol) and control (water) odors tested during the rotation. OVAR has consistently increased
the SSQ score, confirming the ability of the test to induce motion sickness (F(1,85) = 115.7, p < 0.0001). However, the addition of a smell that is pleasant or unpleasant during the rotation did not affect the occurrence of motion sickness symptoms compared to the control condition. The type of subject (low or high MSS) had a significant effect on the model (F(1,16) = 7.6, p = 0.01), since the SSQ scores before OVAR were similar in the two subgroups, SSQ values after OVAR were higher in the two subgroups (low or high MSS) but it has to be noticed that after OVAR the high MSS group presented higher scores than the low MSS group (they were more motion sick) (Fig. 1). However the analysis of MSS groups demonstrated that subjects with high MSS were not more sensitive to the smell added during rotation than during the control test (p > 05).
Olfactory perception variation after OVAR Despite the pretest carried out to define a concentration, for each odorant that reaches a moderate intensity perception, our results showed (i) that the perceived intensity (F(4) = 124.0, p < 0.0001) and perceived hedonicity (F(4) = 88.5, p < 0.0001) was different from one odor to the other and (ii) that the amplitude of variation depends on the levels of pre-OVAR intensity (F(1,247) = 56.4, p < 0.0001) (or pre-OVAR hedonicity (F(1,247) = 112.4, p < 0.0001). On the basis of these results, an analysis of covariance was used with the pre-OVAR intensity or pre-OVAR hedonicity as continuous variable in order to test the three factors: OVAR, odors-during-OVAR and MSS; Fig. 2 shows the estimated parameters explaining the perceived intensity and hedonicity of odors observed after-OVAR in comparison to the control condition and ignoring the pre-OVAR intensity value. Intensity of odors was significantly increased afterOVAR and this increase in intensity was significantly higher for unpleasant odors than for pleasant one (F(4,247) = 19.9, p < 0.0001). However, no effect was found for odors-during-OVAR factor or for MSS levels. For the hedonicity, OVAR test made unpleasant odors more unpleasant while it made limonene odor slightly more pleasant (F(4,247) = 9.5, p < 0.001). As for intensity variation, no effect was found for odors-during-OVAR factor or for MSS levels.
Fig. 1. SSQ scores before (in black) and after (in gray). OVAR for the whole group (left panel), the low MSS group (middle panel) and for the high MSS group (right panel). OVAR sessions were performed using different odors.
A.C. Paillard et al. / Neuroscience Letters 566 (2014) 326–330
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Fig. 2. Fitted variations of the perception observed after OVAR in comparison to the control condition.
Discussion The aim of the present study was to assess the relationship between olfaction and motion sickness susceptibility (MSS). Firstly, our results showed higher motion sickness scores after OVAR sessions. Our results confirmed the nauseogenic effect of OVAR test, as shown by Denise et al. [4] and Quarck et al. [20]. The present study also demonstrated that subjects who have a higher MSS score have a higher motion sickness score after OVAR test. Furthermore, our analysis showed that the addition of an odor that is a pleasant or unpleasant odor (limonene or petrol, respectively) during the rotation did not affect the occurrence of motion sickness symptoms compared to the control condition (distilled water), whatever the type of subject (low or high MSS). Whereas we showed the efficiency of the OVAR test as a nauseogenic test, the present study suggested that the hedonic valence of an odor does not influence motion sickness symptoms occurrence. Our first hypothesis was that unpleasant odors, such as petrol, could induce motion sickness more rapidly. This hypothesis is not supported by our results. As mean MSSQ score of our high-MSS individuals is not that high (from 17.63 to 44), it might be necessary to delve further into our first findings with MSS participants with higher MSS scores. However, the protocol used in our study might be too nauseogenic and uncomfortable for high-MSS participants. In fact, the stimulation parameters were chosen to make the examination moderately nauseogenic; but the association of smells and a nauseogenic test might be too uncomfortable for high-MSS participants. In addition, our results showed an effect of motion-induced sickness on olfactory perception. Indeed, intensity of odors significantly increased after OVAR sessions: odors were perceived are more intense after the nauseogenic test; hedonicity changed significantly after OVAR: unpleasant odors were perceived as more unpleasant and pleasant odor such as limonene was perceived as more pleasant. The subjects’ motion sickness susceptibility scores did not affect the olfactory perception alteration. This post-OVAR olfactory variation seems to affect more importantly unpleasant odors than pleasant ones. In fact, post-OVAR intensity modification was significantly higher for unpleasant odors than for pleasant one. Moreover, only the limonene (pleasant odor smelt during OVAR session) perception was modified whereas the hedonicity of both unpleasant odors was affected by OVAR. Herz et al. [13] highlighted that olfactory hedonic responses could be modified in accord with the emotional valence of the associated experience. The OVAR used in our study is well known for its nauseogenic effect and there is little doubt that participants consider this test as a negative experience. Based on Herz’s work, we hypothesized that the hedonicity of pleasant odors smelt by participants during our OVAR stimulation could be perceived as less pleasant after the test. Our results did not
support this hypothesis. Actually, the OVAR test seems to accentuate the perceived quality of odors: odors are perceived as more intense after the nauseogenic test, unpleasant odors are perceived as more unpleasant, pleasant odors are perceived as more pleasant. In other words, subjects exposed to an odor during the OVAR test showed apparent sensitization or cross-sensitization, i.e. an increase in rated intensity, compared to subjects that were not exposed to an odor during the test. Considering the 10 min delay between the end of odor exposure and the odor intensity test, this effect probably occurs via a cognitive process. Indeed, it has been shown that cognitive factors influencing the situational context and the perceiver’s expectations could have an effect on odor perceived intensity [3]. In the present study, the cognitive “bias” could be the negative experience of OVAR test under conditions of olfactory stimulation. The effect of odor exposure during the OVAR test on the increased odor unpleasantness (for unpleasant odors) and pleasantness (for the pleasant odors) could be related to the increased intensity rating. Even though intensity has a rather complex relationship to pleasantness, it could be expected that a pleasant or unpleasant odor perceived as stronger would be evaluated, respectively, as more pleasant or more unpleasant. Conclusions The present study highlighted the lack of influence of odors in motion-induced sickness but showed an impact of a nauseogenic test on the dimensions of odors, i.e. its intensity valence and hedonic valence changed in a nauseogenic context, such as travel in modern transports. Our work is of importance because it emphasizes the necessity to control the smells in modern transports so that the travel experience does not become more uncomfortable. Acknowledgments The authors would like to thank the participants involved in this study for their sympathy. The authors are grateful to Claire Paris for her help and assistance. References [1] G. Brand, J.L. Millot, Sex differences in human olfaction: between evidence and enigma, Quart. J. Exp. Psychol. 54 (2001) 259–270. [2] S.A. Clemes, P.A. Howarth, The menstrual cycle and susceptibility to virtual simulation sickness, J. Biol. Rhythms 20 (2005) 71–82. [3] P. Dalton, Odor perception and beliefs about risk, Chem. Senses 21 (1996) 447–458. [4] P. Denise, O. Etard, L. Zupan, C. Darlot, Motion sickness during off-vertical axis rotation: prediction by a model of sensory interactions and correlation with other forms of motion sickness, Neurosci. Lett. 203 (1996) 183–186.
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[5] H. Distel, S. Ayabe-Kanamura, M. Martínez-Gómez, I. Schicker, T. Kobayakawa, S. Saito, R. Hudson, Perception of everyday odors—correlation between intensity, familiarity and strength of hedonic judgement, Chem. Senses 24 (1999) 191–199. [6] D.M.T. Fessler, A. Arguello, The relationship between susceptibility to nausea and vomiting and the possession of conditioned food aversions, Appetite 43 (2004) 331–334. [7] J.F. Golding, Motion sickness susceptibility, Auton. Neurosci. 129 (2006) 67–76. [8] J.F. Golding, Predicting individual differences in motion sickness susceptibility by questionnaire, Pers. Individ. Dif. 41 (2006) 237–248. [9] J.F. Golding, M. Gresty, Motion sickness, Curr. Opin. Neurol. 18 (2005) 1. [10] J.F. Golding, P. Kadzere, M.A. Gresty, Motion sickness susceptibility fluctuates through the menstrual cycle, Aviat. Space Environ. Med. 76 (2005) 970–973. [11] E.A. Grunfeld, C. Price, P.J. Goadsby, M.A. Gresty., Motion sickness, migraine, and menstruation in mariners, Lancet 351 (1998) 9109. [12] R.S. Herz, C. McCall, L. Cahill, Hemispheric lateralization in the processing of odor pleasantness versus odor names, Chem. Senses 24 (1999) 691–695. [13] R.S. Herz, Odor-associative learning and emotion: effets on perception and behavior, Chem Senses 30 (Suppl 1) (2005) 250–251. [15] W.H. Johnson, F.A. Sunahara, J.P. Landolt, Importance of the vestibular system in visually induced nausea and self-vection, J. Vestib. Res. 9 (1999) 83–87.
[17] R.S. Kennedy, F. JE, K.S. Berbaum, M.G. Lilienthal, Use of a motion sickness history questionnaire for prediction of simulator sickness, Aviat. Space Environ. Med. 63 (1992) 588–593. [18] A. Paillard, L. Jacquot, J.L. Millot, Olfactory perception and motion sickness, Chem. Senses 36 (2011) E35. [19] A.H. Park, S. Hu, Gender differences in motion sickness history and susceptibility to optokinetic rotation-induced motion sickness, Aviat. Space Environ. Med. 70 (1999) 1077–1080. [20] G. Quarck, O. Etard, M. Oreel, P. Denise, Motion sickness occurrence does not correlate with nystagmus characteristics, Neurosci. Lett. 287 (2000) 49–52. [21] J.T. Reason, J.J. Brand, Motion Sickness, Academic Press, London, 1975. [22] K. Sharma, Aparna, Prevalence and correlates of susceptibility to motion sickness, Acta Genet. Med. Gemellol. 46 (1997) 105–121. [23] R.C. Team, in: R.F.f.S. Computing (Ed.), R. A Language and Environment for Statistical Computing, R.F.f.S. Computing, Vienna, Austria, 2013, http://www.Rproject.org/. [25] B.J. Yates, A.D. Miller, J.B. Lucot, Physiological basis and pharmacology of motion sickness: an update, Brain Res. Bull. 47 (1998) 395–406. [26] D.H. Zald, J.V. Pardo, Functional neuroimaging of the olfactory system in humans, Int. J. Psychophysiol. 36 (2000) 165–811.
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Is there a relationship between odors and motion sickness? A.C. Paillard a,b,c , M. Lamôré a,b,c , O. Etard c,d , J.-L. Millot e , L. Jacquot e , P. Denise a,b,c,d , G. Quarck a,b,c,∗ a
UNICAEN, COMETE, 14032 Caen, France INSERM, U1075, 14032 Caen, France Normandie Univ, Caen, France d CHU de Caen, Service des Explorations Fonctionnelles, 14000 Caen, France e Université de Franche-Comté, Laboratoire de Neurosciences, 25000 Besanc¸on, France b c
h i g h l i g h t s • We evaluate the relationship between olfaction and motion sickness. • Our study highlighted the lack of influence of odors in motion-induced sickness. • Our results showed an impact of a nauseogenic test on olfactory perception.
a r t i c l e
i n f o
Article history: Received 11 June 2013 Received in revised form 18 February 2014 Accepted 22 February 2014 Keywords: Motion sickness OVAR Odor Perception
a b s t r a c t The aim of this study was to evaluate the relationship between olfaction and motion sickness. A sample of 18 participants was recruited and submitted to three sessions of nauseogenic stimulations: off vertical axis rotation (OVAR), performed under conditions of olfactory stimulation with limonene (pleasant odor), petrol (unpleasant odor) or distilled water (as a control). Motion sickness was assessed before, during and after each OVAR session. In addition, participants were asked to evaluate the intensity and hedonic valence of four odors (geraniol, limonene, butanol, petrol) as well as distilled water (as a control) before and after each OVAR session. Our analysis showed that OVAR has consistently increased the inducedmotion sickness. However the addition of an odor that is pleasant or unpleasant during the rotation did not affect the occurrence of motion sickness symptoms compared to the control condition. Our results also showed that intensity of odors was significantly increased after OVAR and the intensity was significantly higher for unpleasant odors than for pleasant one. For the hedonicity, OVAR made unpleasant odors more unpleasant (p < 0.0001) while it made limonene odor slightly more pleasant (p < 0.05). The present study highlighted the lack of influence of odors in motion-induced sickness but an impact of a nauseogenic test on olfactory perception. © 2014 Elsevier Ireland Ltd. All rights reserved.
Introduction Technological evolution of modern transports, such as cars or trains, significantly increases motion sickness symptoms occurrence. Motion sickness (MS) is defined by a set of four main symptoms that regularly appear: facial pallor, cold sweats, nausea and vomiting. Other additional signs such as dizziness, headache, fatigue, postural instability, which are more variable in their appearance and duration, can be also observed [9]. One of the most established theories to explain in which circumstances
∗ Corresponding author at: UMR UCBN INSERM U1075 COMETE, 14032 Caen, France. Tel.: +33 2 31 56 72 63. E-mail address: [email protected] (G. Quarck). http://dx.doi.org/10.1016/j.neulet.2014.02.049 0304-3940/© 2014 Elsevier Ireland Ltd. All rights reserved.
motion sickness arises is the “sensory conflict” theory [21]. This theory postulates that motion sickness originates from a sensory mismatch between actual versus expected invariant patterns of vestibular, visual and somatosensory inputs [21]. It has been accepted that the vestibular system influences individual motion sickness susceptibility (MSS) since patients with bilateral vestibular deficit have greatly reduced susceptibility or do not become motion sick at all [15,25]. This sensory mismatch leads to an activation of vestibuloautonomic pathways, which have been shown to be also involved in producing nausea and vomiting during motion sickness and those that generate illness after ingestion of toxins [25]. Among factors that may contribute to motion sickness, such as alcohol or hunger, the presence of strong smells is very often reported by individuals who are sensitive to motion sickness.
A.C. Paillard et al. / Neuroscience Letters 566 (2014) 326–330
Similarly, there are a variety of companies claiming that the inhalation of some essential oils can alleviate motion sickness symptoms. Besides, an interesting parallel between motion sickness and the olfactory system may be underlined. On one hand, it is granted that women are more sensitive to motion sickness than men [7,18,19]; in particular, it has been shown that the MSS fluctuates across menstrual cycle [10,11] as a consequence of hormonal variation [2]. On the other hand, women demonstrate better olfactory abilities than men [1]. But, surprisingly, the link between olfaction and MSS has been poorly investigated by the research community. Sharma and Aparna [22] showed that participants with high-MSS were more sensitive to unpleasant odors. Fessler and Arguello [6], who asked participants to report on a 5-point scale how sensitive they were to unpleasant odors, highlighted a positive correlation between sensitivity to unpleasant odors and MSS in women. Similarly, Paillard et al. [18] reported pilot data demonstrating that high-MSS participants perceived the odors of petrol and leather as more unpleasant than participants who were not sensitive to motion sickness. The aim of the present study is to delve further into these initial findings and to assess the relationship between odors and motion sickness. We can question the influence of odors on motion-induced sickness (i.e. can pleasant or unpleasant odors have an influence on MS symptoms occurrence?) as well as the influence of motioninduced sickness on the perceived quality of an odor (i.e. can a nauseogenic test influence odors intensity and hedonicity?). The study focuses specifically on these two dimensions because they have long been recognized as the most important features of odors [12,26]. Previous study showed that high-MSS participants are more sensitive to unpleasant odors [22] and also perceived the odors of petrol and leather as more unpleasant than participants who were not sensitive to motion sickness [18]. Moreover, Herz et al. [13] supported the statement that hedonic judgment of familiar odors is deteriorated in an unpleasant context. Besides, it has been shown that the perceived intensity depends, at least in part, on experience-dependent factors [5]. Thus, our hypotheses are that (i) the motion sickness occurrence may be influenced by unpleasant odors such as petrol or leather during a nauseogenic test; (ii) pleasant odors smelt by participants during a nauseogenic test are perceived as less pleasant after the test and unpleasant odors are perceived as more unpleasant and (iii) perceived intensity of odors is increased after a nauseogenic test.
Material and methods Participants A sample of 18 volunteer participants (mean age 23.8 years old, range 19–40 years old, 11 women and 7 men) was recruited in this experiment. In order to assess the MSS, participants were required to complete the motion sickness susceptibility questionnaire (MSSQ) [8]. According to Paillard et al. [18], who found that high-MSS subjects judged odors related to transports as more unpleasant than low-MSS subjects, our participants were divided in two groups: 10 subjects represent low MSS individuals (MSSQ scores from 0 to 10.75; 6 women and 4 men) and 8 subjects represent high MSS individuals (MSSQ scores from 17.63 to 44; 5 women and 3 men). All participants were non-smokers and reported normal smell sensitivity. None of them had a history of nasal/sinus disease or extensive exposure to chemical with potential olfactory toxicity. Participants with past or present otologic or neurological disorders were not included in the study. Women were not tested during their menses period. All participants provided informed written consent.
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This study was conducted in accordance with the Declaration of Helsinki (1964). Motion sickness induction and symptoms ratings The off vertical axis rotation (OVAR) test is ideal for our purpose, as it has been established that it is highly effective in evoking MS. On the basis of a previous study performed in the laboratory [4], the stimulation parameters (70◦ s−1 , 15◦ tilt, in total darkness) were chosen to make the examination moderately nauseogenic. Subjects were comfortably seated and secured into a rotating chair driven by a torque. They were restrained by means of a seat belt. The center of their head was also positioned and maintained at the center of the rotation by means of a concave headrest and a helmet fixed to the chair. The degree of motion sickness during OVAR test (i.e. motion sickness rating, MSR) has been used to define the end-point of the OVAR test. MSR was rated every minute; (1): no symptom; (2): initial symptoms but no nausea; (3): mild nausea; (4): moderate nausea. The MSR score is defined as the time (in minutes) to reach MSR-level 3, which was defined as the end-point of each OVAR test. Motion sickness symptoms were also assessed before and after motion with the simulator sickness questionnaire (SSQ) [17] that probes polysymptomatic responses to motion and yields a score between 0 (no symptoms) and 51 (maximum symptoms). Odorants For the test of olfactory perception, four specific odorants were used: two pleasant odors (geraniol and limonene, corresponding to rose- and orange-like smells, respectively) and two unpleasant odors (n-butanol and petrol). Pleasantness scores of each odor were obtained from preliminary self-report ratings. We also used distilled water as a control condition. The dilutions used in our study have been determined according to a pretest carried out on 10 participants: three dilution series (100%, 50%, 25%) were prepared for each odorant and participants were required to rate from 0 (weak) to 10 (strong) the perceived intensity of odors. The dilutions that reach a similar moderate perceived intensity have been chosen for the tests. Specifically, geraniol and limonene were used without dilution (100% of the stock solution), while petrol and butanol were diluted at 25% in odorless mineral oil. Four milliliters of each odorant solution was placed into glass tubes (6.5 cm high, 1 cm at the opening). For the OVAR session, 10 L of pure limonene or 25% petrol or distilled water was placed on a piece of cotton attached to participant facemask. The concentrations for each odorant were determined during pretesting such as they were both of equal perceived intensity. Before and after the nauseogenic test, participants were asked to rate the perceived intensity and hedonic valence of the four odors as well as the control odor on analogic scales ranging from 0 (weak/unpleasant) to 10 (strong/pleasant). Procedure The experiment consisted of three OVAR sessions. In order to avoid habituation, there was at least one week between each session. Before each OVAR session the test of olfactory perception of the four odors (geraniol, limonene, butanol and petrol) and the distilled water was carried out in a separate room. Odor presentation order was randomized for each participant. At the beginning of each OVAR session, participants were informed on how to recognize symptoms of motion sickness as they developed and how to report them. Then the first SSQ was administered. The participant seated on the OVAR chair and was equipped with a facemask soaked with limonene, petrol or distilled water. The participants performed these three sessions in a random order (balanced for order design) and the OVAR stimulation always started immediately after
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the facemask application. During stimulation, the participant was requested to verbally report every minute his/her degree of motion sickness (MSR). The stimulation was stopped at MSR-level 3 or after 16 min whichever came first. Immediately following cessation of motion, the second SSQ was administered. Then, after a 10-min break, the four odors (geraniol, limonene, butanol and petrol) as well as the distilled water were once again randomly tested in a separate room. Statistical analysis A mixed-model analysis of variance and covariance followed by contrasts analysis when necessary were performed using linear mixed effects models and the R package nmle (R Core Team) [23]. In the first part of the analysis, independent variables studied were SSQ scores. We tested the following factors as fixed effects in the model: OVAR with 2 levels (before and after); odors-during-OVAR with three levels (pleasant, unpleasant and control); MSS of subject with two levels (low and high). Subject factor is used as random effects. In the second part of the analysis, independent variables studied were the intensity variations and the hedonicity variations of the odors tested after-OVAR sessions in comparison with the pre-OVAR test. In order to determine if the motion sickness susceptibility of the subjects and the odors perceived during OVAR have an effect on the olfactory perception test realized after OVAR, two factors were added in the model: MSS of subjects (high or low MSS) and type of odors during OVAR (pleasant, unpleasant, control). Moreover, subject factor was used as random effects. Subject factor is used as random effects. The fitted values calculated by the model were used for Fig. 2. In all cases, normality and homogeneity of the model’s error were checked by inspections of plots of residuals against fitted values. Results Odor during OVAR and motion sickness occurrence Fig. 1 shows the SSQ values before and after OVAR and the MSR for pleasant (limonene), unpleasant (petrol) and control (water) odors tested during the rotation. OVAR has consistently increased
the SSQ score, confirming the ability of the test to induce motion sickness (F(1,85) = 115.7, p < 0.0001). However, the addition of a smell that is pleasant or unpleasant during the rotation did not affect the occurrence of motion sickness symptoms compared to the control condition. The type of subject (low or high MSS) had a significant effect on the model (F(1,16) = 7.6, p = 0.01), since the SSQ scores before OVAR were similar in the two subgroups, SSQ values after OVAR were higher in the two subgroups (low or high MSS) but it has to be noticed that after OVAR the high MSS group presented higher scores than the low MSS group (they were more motion sick) (Fig. 1). However the analysis of MSS groups demonstrated that subjects with high MSS were not more sensitive to the smell added during rotation than during the control test (p > 05).
Olfactory perception variation after OVAR Despite the pretest carried out to define a concentration, for each odorant that reaches a moderate intensity perception, our results showed (i) that the perceived intensity (F(4) = 124.0, p < 0.0001) and perceived hedonicity (F(4) = 88.5, p < 0.0001) was different from one odor to the other and (ii) that the amplitude of variation depends on the levels of pre-OVAR intensity (F(1,247) = 56.4, p < 0.0001) (or pre-OVAR hedonicity (F(1,247) = 112.4, p < 0.0001). On the basis of these results, an analysis of covariance was used with the pre-OVAR intensity or pre-OVAR hedonicity as continuous variable in order to test the three factors: OVAR, odors-during-OVAR and MSS; Fig. 2 shows the estimated parameters explaining the perceived intensity and hedonicity of odors observed after-OVAR in comparison to the control condition and ignoring the pre-OVAR intensity value. Intensity of odors was significantly increased afterOVAR and this increase in intensity was significantly higher for unpleasant odors than for pleasant one (F(4,247) = 19.9, p < 0.0001). However, no effect was found for odors-during-OVAR factor or for MSS levels. For the hedonicity, OVAR test made unpleasant odors more unpleasant while it made limonene odor slightly more pleasant (F(4,247) = 9.5, p < 0.001). As for intensity variation, no effect was found for odors-during-OVAR factor or for MSS levels.
Fig. 1. SSQ scores before (in black) and after (in gray). OVAR for the whole group (left panel), the low MSS group (middle panel) and for the high MSS group (right panel). OVAR sessions were performed using different odors.
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Fig. 2. Fitted variations of the perception observed after OVAR in comparison to the control condition.
Discussion The aim of the present study was to assess the relationship between olfaction and motion sickness susceptibility (MSS). Firstly, our results showed higher motion sickness scores after OVAR sessions. Our results confirmed the nauseogenic effect of OVAR test, as shown by Denise et al. [4] and Quarck et al. [20]. The present study also demonstrated that subjects who have a higher MSS score have a higher motion sickness score after OVAR test. Furthermore, our analysis showed that the addition of an odor that is a pleasant or unpleasant odor (limonene or petrol, respectively) during the rotation did not affect the occurrence of motion sickness symptoms compared to the control condition (distilled water), whatever the type of subject (low or high MSS). Whereas we showed the efficiency of the OVAR test as a nauseogenic test, the present study suggested that the hedonic valence of an odor does not influence motion sickness symptoms occurrence. Our first hypothesis was that unpleasant odors, such as petrol, could induce motion sickness more rapidly. This hypothesis is not supported by our results. As mean MSSQ score of our high-MSS individuals is not that high (from 17.63 to 44), it might be necessary to delve further into our first findings with MSS participants with higher MSS scores. However, the protocol used in our study might be too nauseogenic and uncomfortable for high-MSS participants. In fact, the stimulation parameters were chosen to make the examination moderately nauseogenic; but the association of smells and a nauseogenic test might be too uncomfortable for high-MSS participants. In addition, our results showed an effect of motion-induced sickness on olfactory perception. Indeed, intensity of odors significantly increased after OVAR sessions: odors were perceived are more intense after the nauseogenic test; hedonicity changed significantly after OVAR: unpleasant odors were perceived as more unpleasant and pleasant odor such as limonene was perceived as more pleasant. The subjects’ motion sickness susceptibility scores did not affect the olfactory perception alteration. This post-OVAR olfactory variation seems to affect more importantly unpleasant odors than pleasant ones. In fact, post-OVAR intensity modification was significantly higher for unpleasant odors than for pleasant one. Moreover, only the limonene (pleasant odor smelt during OVAR session) perception was modified whereas the hedonicity of both unpleasant odors was affected by OVAR. Herz et al. [13] highlighted that olfactory hedonic responses could be modified in accord with the emotional valence of the associated experience. The OVAR used in our study is well known for its nauseogenic effect and there is little doubt that participants consider this test as a negative experience. Based on Herz’s work, we hypothesized that the hedonicity of pleasant odors smelt by participants during our OVAR stimulation could be perceived as less pleasant after the test. Our results did not
support this hypothesis. Actually, the OVAR test seems to accentuate the perceived quality of odors: odors are perceived as more intense after the nauseogenic test, unpleasant odors are perceived as more unpleasant, pleasant odors are perceived as more pleasant. In other words, subjects exposed to an odor during the OVAR test showed apparent sensitization or cross-sensitization, i.e. an increase in rated intensity, compared to subjects that were not exposed to an odor during the test. Considering the 10 min delay between the end of odor exposure and the odor intensity test, this effect probably occurs via a cognitive process. Indeed, it has been shown that cognitive factors influencing the situational context and the perceiver’s expectations could have an effect on odor perceived intensity [3]. In the present study, the cognitive “bias” could be the negative experience of OVAR test under conditions of olfactory stimulation. The effect of odor exposure during the OVAR test on the increased odor unpleasantness (for unpleasant odors) and pleasantness (for the pleasant odors) could be related to the increased intensity rating. Even though intensity has a rather complex relationship to pleasantness, it could be expected that a pleasant or unpleasant odor perceived as stronger would be evaluated, respectively, as more pleasant or more unpleasant. Conclusions The present study highlighted the lack of influence of odors in motion-induced sickness but showed an impact of a nauseogenic test on the dimensions of odors, i.e. its intensity valence and hedonic valence changed in a nauseogenic context, such as travel in modern transports. Our work is of importance because it emphasizes the necessity to control the smells in modern transports so that the travel experience does not become more uncomfortable. Acknowledgments The authors would like to thank the participants involved in this study for their sympathy. The authors are grateful to Claire Paris for her help and assistance. References [1] G. Brand, J.L. Millot, Sex differences in human olfaction: between evidence and enigma, Quart. J. Exp. Psychol. 54 (2001) 259–270. [2] S.A. Clemes, P.A. Howarth, The menstrual cycle and susceptibility to virtual simulation sickness, J. Biol. Rhythms 20 (2005) 71–82. [3] P. Dalton, Odor perception and beliefs about risk, Chem. Senses 21 (1996) 447–458. [4] P. Denise, O. Etard, L. Zupan, C. Darlot, Motion sickness during off-vertical axis rotation: prediction by a model of sensory interactions and correlation with other forms of motion sickness, Neurosci. Lett. 203 (1996) 183–186.
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