Exp Brain Res DOI 10.1007/s00221-014-3950-9

Research Article

Enhanced perceptions of control and predictability reduce motion‑induced nausea and gastric dysrhythmia Max E. Levine · Robert M. Stern · Kenneth L. Koch 

Received: 13 February 2014 / Accepted: 3 April 2014 © Springer-Verlag Berlin Heidelberg 2014

Abstract  Nausea is a debilitating condition that is typically accompanied by gastric dysrhythmia. The enhancement of perceived control and predictability has generally been found to attenuate the physiological stress response. The aim of the present study was to test the effect of these psychosocial variables in the context of nausea, motion sickness, and gastric dysrhythmia. A 2x2, independentgroups, factorial design was employed in which perceived control and predictability were each provided at high or low levels to 80 participants before exposure to a rotating optokinetic drum. Ratings of nausea were obtained throughout a 6-min baseline period and a 16-min drum rotation period. Noninvasive recordings of the electrical activity of the stomach called electrogastrograms were also obtained throughout the study. Nausea scores were significantly lower among participants with high control than among those with low control, and were significantly lower among participants with high predictability than among those with low predictability. Estimates of gastric dysrhythmia obtained from the EGG during drum rotation were significantly lower among participants with high predictability than among those with low predictability. A significant interaction effect of control and predictability on M. E. Levine (*)  Department of Psychology, Siena College, Loudonville, NY 12211, USA e-mail: [email protected] R. M. Stern  Department of Psychology, The Pennsylvania State University, University Park, PA, USA K. L. Koch  Department of Internal Medicine, Section of Gastroenterology, Wake Forest University School of Medicine, Winston‑Salem, NC, USA

gastric dysrhythmia was also observed, such that high control was only effective for arresting the development of gastric dysrhythmia when high predictability was also available. Stronger perceptions of control and predictability may temper the development of nausea and gastric dysrhythmia during exposure to provocative motion. Psychosocial interventions in a variety of nausea contexts may represent an alternative means of symptom control. Keywords Control · Predictability · Nausea · Motion sickness · Gastric dysrhythmia

Introduction Nausea is a highly aversive subjective experience that is not managed well by standard medical interventions. Susceptibility to the experience of nausea varies dramatically between individuals, as some appear to be much more able than others to tolerate exposure to nauseogenic stimulation such as provocative motion (Stern 2002; Stern and Koch 1996), chemotherapy agents (Roscoe et al. 2000), pregnancy (Einarson et al. 2013), and anesthetization (Janicki et al. 2011). Differential susceptibility is likely attributable to a multitude of sensory, physiological, and demographic factors, but to the extent that nausea represents a distinct subjective and physiological response to stressful environmental circumstances, psychosocial factors such as the perception of control and predictability may also play an important role. Reports of nausea have been demonstrated to be accompanied by gastric dysrhythmias, sympathetic activation, and vagal withdrawal (Gianaros et al. 2001; Koch 2003; Levine 2005; Levine et al. 2004); the physiological response profile associated with nausea, therefore, is consistent with the typical autonomic stress response.

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The aim of the present study was to determine whether factors that have been successful for reducing stress might also diminish the incidence and severity of nausea and gastric dysrhythmia. In order to study both the subjective experience of nausea and the associated physiological changes in a controlled environment, useful methods of modeling nausea in the laboratory with motion sickness have been developed. Rotating optokinetic drums have been employed to effectively induce nausea and motion sickness in susceptible participants (Bos and Bles 2004; Stern et al. 1985). Observing the motion of the vertical stripes that line the inside surface of the drum while seated on a stationary stool induces the sensation of illusory self-motion, or vection. The visual-vestibular sensory mismatch that results is sufficient for susceptible individuals to develop nausea and other symptoms of motion sickness (Golding 2006; Stern and Koch 1991). The primary symptoms of motion sickness other than nausea include dizziness and drowsiness (Kennedy et al. 2010); there also appears to be a high prevalence of headache, excessive warmth, sweating, pallor, stomach awareness, and stomach discomfort (Hu et al. 1989). The perception of control may be conceived of as the belief that one has the power to dictate the outcome of a situation; for example, the driver of a car is likely to perceive control over the vehicle since turning the steering wheel unequivocally causes it to move in the corresponding direction. Perceived control over a potentially aversive situation has been repeatedly demonstrated to have a significant favorable impact on an individual’s subjective and physiological response to stress (e.g., Abelson et al. 2008; Gerin et al. 1992; Glass and Singer 1972; Lundberg and Frankenhaeuser 1978; Peters et al. 1998; Ranchor et al. 2010; Seligman 1991; Weiss 1977). Even under conditions in which the belief that one has control is not warranted, or when the opportunity to exercise control is not actually utilized, the extent to which an individual responds negatively to a stressor is mitigated by the mere perception of control (Geer et al. 1970; Houston 1972; Visintainer et al. 1982). It is not entirely clear how perceptions of control minimize stress, but most theorists advocate the position that maintaining a belief that the outcomes one experiences are contingent upon one’s actions allows the person to more effectively cope with and hence reduce the unpleasantness of stress. There are, of course, exceptions to the rule that seeking and gaining control over a stressful situation will invariably be stressreducing (Burger 1989; Shapiro et al. 1996), but for the most part, perceptions of control are viewed as beneficial and powerfully influential. Predictability is the capacity to accurately anticipate future events. Students with predictability, for instance,

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know when the next examination is scheduled to take place in a class they are taking; in courses where pop quizzes are occasionally administered, predictability would accordingly be lacking. Many studies have demonstrated the availability of predictive information to diminish the subjective and physiological response to stress as well (e.g., Abbott et al. 1984; Davis and Levine 1982; Oka et al. 2010; Schaap et al. 2013; Seligman 1975; Seligman and Meyer 1970; Staub et al. 1971; Weiss 1972). The ability to foresee how a stressful situation will develop can be advantageous for generating an adaptive coping response; knowing when, and for how long, a stressful period will last allows people to prepare themselves to cope more effectively with the stressor. Perhaps more importantly, a sense of predictability allows a person to take comfort in the awareness of when it is no longer necessary to engage a coping response and relax given the absence of a stressor (Sapolsky 1998). One feature of the perception of control that might allow it to be effective for reducing stress is its relationship with being able to predict and anticipate the development of a challenging situation. An individual who knows he or she can dictate future events related to a potentially aversive interaction can, by definition, predict the course of those events (Geer and Maisel 1972). For instance, if a participant can terminate a noxious stimulus, then the participant can also predict its duration. The beneficial effect of perceived or actual control on responses to various forms of stress may therefore, in varying degrees, be attributed to the predictability that it provides. The present study explored the extent to which perceptions of control and predictability could both individually and collectively affect the development of nausea, motion sickness, and gastric dysrhythmia during exposure to a motion sickness stimulus. Perceived control was manipulated in the present study by providing some participants with the means to start and, more importantly, stop their exposure to a rotating optokinetic drum at their discretion. For ethical reasons, other participants were also told that they may terminate the session if their symptoms became intolerable, but to do so, they needed to request the drum’s rotation to be stopped by an experimenter from an adjacent room. Given that perceptions of control, whether veridical or not and whether exercised or not, have been repeatedly demonstrated to have a positive influence on one’s ability to effectively manage a stressful situation, it was reasoned that providing participants with control over stimulation that was capable of inducing nausea and motion sickness would be helpful for preventing the development of such symptoms. It was hypothesized that participants with control on the onset and offset of the drum’s rotation would experience less severe symptoms of nausea and motion sickness than participants without direct control.

Exp Brain Res Table 1  Demographic characteristics of study participants in each experimental group Experimental group

n

Sex

Age (years)

Ethnicity

Male Female Range Mean European-American African-American Asian-American Hispanic High Control/High Predictability 20 9 High Control/Low Predictability 20 11 Low Control/High Predictability 20 7

11 9 13

18–2520.0 18–2420.3 18–3620.6

16 15 14

2 1 4

1 2 2

1 2 0

Low Control/Low Predictability 20 10

10

19–2620.2

16

2

2

0

Separating the effects of control from the effects of predictability on an individual’s response to a stressful situation is complicated (Levine 2000). Whereas predictability can exist conceptually with or without control, control cannot be completely disentangled from predictability. Providing control over the delivery or cessation of an aversive stimulus makes the stimulus more predictable to a certain extent. This makes the evaluation of the relative influence of control and predictability difficult to achieve, even in a controlled experimental setting. One can, however, determine whether predictability alone can exert a protective effect, and control can be provided along with varying levels of predictability in order to examine an interaction effect between the two variables. In this way, it is possible to examine control and predictability as distinct psychological factors. In the present study, predictability was provided with and without control of the motion sickness stimulus. Some participants were informed of the duration of their exposure to the rotating drum and were also given regular updates regarding how much time remained. Although the provision of control of the drum made the situation somewhat more predictable, the availability of temporal information made the experience considerably more predictable for some participants. In order to examine the effects of perceived control and predictability on the development of nausea and motion sickness symptoms, a 2x2, independent-groups, factorial design was employed. Manipulation of perceived control and predictability at high and low levels produced four independent groups, to which participants were randomly assigned. It was hypo thesized that significant main effects of both perceived control and predictability on the development of nausea, motion sickness symptoms, and gastric dysrhythmia would be observed. Given the notion that control and predictability are independent modulators of the stress response, the interaction effect of perceived control and predictability was not expected to be significant. The effects of these variables were anticipated to be additive, such that having both control and predictability would lead to the most favorable outcome, but that the effect of one variable would not depend on the level of the other.

Methods Participants Eighty healthy college students were randomly assigned to one of four groups of 20. None of the participants had previous experience with a rotating optokinetic drum. A breakdown of the sex, age, and ethnicity of participants in each group is provided in Table 1. Differences between the sex, age, and ethnicity distributions of each group were not statistically significant. Each participant’s history of motion sickness was assessed by the Motion Sickness Questionnaire (Hu et al. 1996); differences in mean susceptibility of each group were not statistically significant. All participants were at least 4 h fasted when they arrived at the laboratory, and none reported histories of neurological, cardiovascular, uncorrected visual, respiratory, or gastrointestinal disorders. None had taken any medication, consumed alcohol or caffeine, used recreational drugs, or smoked cigarettes within the previous 24 h, and none had exercised within the previous 3 h. The Institutional Review Board approved the use of human participants, and participants provided written informed consent of their willingness to participate before beginning the experimental session. Apparatus The rotating optokinetic drum employed in the present study was a metal cylindrical chamber 91.5 cm in height and 76.0 cm in diameter (Fig. 1). On the inside surface of the drum were alternating black and white vertical stripes; the black stripes were 3.8 cm wide (7° visual angle), and the white stripes were 6.2 cm wide (11°). The light source inside the drum was a 40-W light bulb mounted in a rectangular lamp near the bottom of the drum. Participants sat on a stool inside the drum with their heads positioned approximately in the center of the cylinder. The viewing distance was roughly 35 cm. The drum was rotated at a constant speed of 60°/s (10 rpm) in the clockwise direction (left to right for the viewer). Some participants were given a handheld switch-box (B&B Motor & Control Corp., Long Island City, NY, USA) while seated in the drum that started and stopped the rotation of the drum. A

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Fig. 1  The rotating optokinetic drum used to elicit symptoms of nausea and motion sickness in healthy participants

Sony camera mounted inside the drum was used to ensure that participants kept their eyes open and directed straight ahead at the movement of the drum throughout the experiment. An intercom system allowed for two-way communication between the experimenter and the participant inside the drum to be maintained from an adjacent room. Subjective measures Nausea was rated by participants over an intercom system once before and every 2 min during exposure to the rotating drum along a scale from 0 to 10, with 0 representing “not at all” and 10 representing “extremely.” Mean nausea ratings were taken as an index of the severity of nausea experienced. The Subjective Symptoms of Motion Sickness (SSMS) questionnaire was also used to assess the severity of participants’ nausea and motion sickness symptoms during exposure to the rotating drum (Graybiel et al. 1968). Common symptoms of motion sickness were assessed only once, immediately before exposure to the rotating drum was discontinued. For questions pertaining to the severity of dizziness, headache, warmth, sweating, drowsiness, and salivation, scores of 0, 1, 2, and 3 were assigned for responses of none, slight, moderate, and severe, respectively. For the question pertaining to stomach awareness, scores of 0, 1, 2, 3, and 4 were assigned for responses of none, stomach discomfort (without nausea), slight nausea, moderate nausea, and severe nausea, respectively.

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SSMS scores were calculated as the total number of points assigned for all of the symptoms in the questionnaire. The range of possible SSMS scores was therefore 0–22. In order to examine the extent to which the experimental manipulations had the desired effects, a subset of participants was asked to complete two manipulation check items. One question was meant to gauge differences in perceived control between participants in groups given control of the drum’s rotation and participants who were not. “How much control did you feel you had over the operation of the rotating drum?” was presented with possible responses ranging along a scale of 0–10. Zero was presented as representing “no control,” five was anchored by “moderate control,” and 10 represented “complete control.” The other question referred to participants’ perceptions of predictability. “How well did you feel you could predict the duration of the drum rotation period?” was followed by a range of possible answers along another scale from 0 to 10. Zero was said to represent “not at all predictable,” five represented “moderately predictable,” and ten represented “completely predictable.” Participants were free to terminate their exposure to the rotating drum if their symptoms became intolerable, either by requesting that the experimenter stop the drum’s rotation, or by stopping it themselves if applicable. Therefore, another index of the subjective experience associated with exposure to the rotating drum was the stimulus duration before early termination was requested (if ever). Longer periods of time in the rotating drum were taken to represent better toleration of the drum’s stimulation, and hence, less severe nausea and motion sickness. In addition, the proportion of participants who requested early termination of the drum’s rotation was determined for each experimental group. Electrogastrography Electrogastrograms (EGGs) were recorded throughout the experiment in a manner identical to that described by Levine et al. (2000) from three electrodes placed on the surface of the abdomen over the stomach. The electrodes detect signals that reflect gastric myoelectrical activity. The EGG data were analyzed using running spectral analysis software (EZEM, Lake Success, NY, USA). Spectral analyses were performed on the 6-min baseline period, and the entire duration of the drum rotation period. The first 4 min of each period comprised the first epoch to be analyzed. The last 75 % (minutes 2, 3, and 4) of the first epoch was combined with the first new minute (minute 5) to comprise the second epoch, and so on. Therefore, three epochs were analyzed for the baseline period (minutes 1–4, 2–5, and 3–6) and then averaged for the entire period as many epochs allowable by the number of minutes of data that were obtained

Exp Brain Res

during the drum rotation period were analyzed and averaged for the entire period. The 75 % overlap in each epoch provides stable spectral estimates. The epochs were analyzed via fast Fourier transform (FFT) to obtain spectral estimates for each 240-s epoch. Estimates of the percentage of EGG power within the gastric tachyarrhythmia frequency bandwidth (4.00–9.75 cpm) were obtained for each experimental period based on the method of Uijtdehaage et al. (1992). Movement artifacts in the EGG were detected by visual inspection of the record as they occurred; minutes containing such artifacts were excluded from the analysis.

impression of the study to determine whether they had had any suspicions or other ideas concerning the true nature of the experiment. None of the participants expressed any suspicion. A subset of participants also completed the manipulation check questionnaire. Participants were then fully debriefed about the true nature of the experiment. It was explained that the withholding of information regarding the entire purpose of the study was necessary for the design of the experiment and that the work was important for the improvement of our understanding of the nature of nausea. Statistical analysis

Procedure Participants were informed that the general purpose of the experiment was to examine the effects of the illusion of self-motion on bodily symptoms. All participants were reassured that if they ever felt too uncomfortable to continue, they were free to terminate the experiment at any point without penalty. Participants assigned to groups receiving “high control” were responsible for starting and stopping the rotation of the drum by flipping a power switch on a handheld control box. They were instructed via intercom when to turn the drum on at the beginning of the drum rotation period and to turn the drum off when the drum rotation period had ended. They also were told that they were free to turn the drum off themselves at their discretion if at any time they felt too uncomfortable to continue for any reason. Participants assigned to groups receiving “low control” were told that the drum would be turned on and off by an experimenter from an adjacent room. Participants assigned to groups receiving “high predictability” were told that the duration of the drum rotation period would be a maximum of 16 min and that they would receive updates every 2 min via intercom about how much time had expired and how much time was remaining in the 16-min period. The experimenter reassured the participants that the provision of regular time updates was not meant to suggest that they must endure the entire 16-min period; it was merely for the purpose of informing them of how much time could remain should they elect to continue to the end of the experiment. Participants assigned to groups receiving “low predictability” were not provided with any information about the duration of the drum rotation period. They did not receive regular updates about how much time had passed and how much time remained. Before the beginning of the drum rotation period, participants were seated quietly in the motionless drum for 6 min while their EGG data were collected. Following the baseline period, participants were asked to rate their nausea, and the drum rotation period began, and then continued for a maximum of 16 min. Following the conclusion of the drum rotation period, participants were asked of their

Main effect means and other descriptive statistics were calculated for nausea ratings, SSMS scores, and stimulus duration estimates. Two-factor analyses of variances (ANOVAs) were performed with control and predictability as independent variables in order to detect significant main and interaction effects of control and predictability. Responses to the perceived control and predictability questions on the manipulation check questionnaire were analyzed with ANOVAs as well. Main effect means and descriptive statistics were also calculated for the percentage of EGG power in the gastric tachyarrhythmia frequency bandwidth during the baseline and drum rotation periods. Two-factor analyses of covariances (ANCOVAs) were performed with control and predictability as independent variables, and with baseline values as the covariate. ANCOVAs were completed in order to detect main and interaction effects of control and predictability on percent gastric tachyarrhythmia during the drum rotation period. Tests of null hypotheses resulting in p values of .05 or less were considered statistically significant, and p values between .05 and .10 were considered marginally significant.

Results One participant failed to comply with repeated instructions to fixate on the drum’s stripes as they passed through her field of view. This participant continuously kept her eyes closed or directed at the floor. Her data were therefore excluded from statistical analyses. Five participants’ EGG records were corrupted by movement artifacts; the EGG records of these participants were removed from the analyses. A significant main effect of perceived control on ratings of nausea during exposure to the rotating drum was observed, F(1,75) = 5.46, p = .022, d = 0.82. Nausea ratings were significantly lower among participants with high control than among participants with low control. The main effect of predictability on ratings of nausea was also significant, F(1,75) = 3.75, p = .044, d = 0.28. Nausea ratings

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Exp Brain Res Table 2  Nausea ratings, Subjective Symptoms of Motion Sickness (SSMS) scores, and percent gastric tachyarrhythmia during drum rotation as a function of control and predictability level Predictability

Perceived control High control

Fig. 2  Nausea ratings as a function of the manipulation of perceived control and predictability. Nausea ratings were significantly lower among participants with high control (p 

Enhanced perceptions of control and predictability reduce motion-induced nausea and gastric dysrhythmia.

Nausea is a debilitating condition that is typically accompanied by gastric dysrhythmia. The enhancement of perceived control and predictability has g...
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