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Journal of Neurophysiology logoLink to Journal of Neurophysiology
. 2016 Mar 23;115(6):3045–3051. doi: 10.1152/jn.00065.2016

Decreased otolith-mediated vestibular response in 25 astronauts induced by long-duration spaceflight

Emma Hallgren 1, Ludmila Kornilova 2, Erik Fransen 3, Dmitrii Glukhikh 2, Steven T Moore 4, Gilles Clément 5, Angelique Van Ombergen 1, Hamish MacDougall 6, Ivan Naumov 2, Floris L Wuyts 1,✉
PMCID: PMC4922620  PMID: 27009158

Long-duration spaceflight causes a significant decrease in otolith-mediated ocular counterrolling (OCR) response.

Keywords: otolith function, ocular counterrolling, spaceflight, centrifugation, artificial gravity

Abstract

The information coming from the vestibular otolith organs is important for the brain when reflexively making appropriate visual and spinal corrections to maintain balance. Symptoms related to failed balance control and navigation are commonly observed in astronauts returning from space. To investigate the effect of microgravity exposure on the otoliths, we studied the otolith-mediated responses elicited by centrifugation in a group of 25 astronauts before and after 6 mo of spaceflight. Ocular counterrolling (OCR) is an otolith-driven reflex that is sensitive to head tilt with regard to gravity and tilts of the gravito-inertial acceleration vector during centrifugation. When comparing pre- and postflight OCR, we found a statistically significant decrease of the OCR response upon return. Nine days after return, the OCR was back at preflight level, indicating a full recovery. Our large study sample allows for more general physiological conclusions about the effect of prolonged microgravity on the otolith system. A deconditioned otolith system is thought to be the cause of several of the negative effects seen in returning astronauts, such as spatial disorientation and orthostatic intolerance. This knowledge should be taken into account for future long-term space missions.

NEW & NOTEWORTHY

Long-duration spaceflight causes a significant decrease in otolith-mediated ocular counterrolling (OCR) response.

to coordinate movements, ensure balance, and maintain stable gaze, humans depend on the peripheral vestibular labyrinth, located bilaterally in the inner ear. The vestibular system senses head movements and provides the brain with the necessary information about our spatial orientation. The vestibular system consists of two main parts: the semicircular canals, which sense rotational movements, and the otolith organs detecting the sum of linear accelerations acting on the head. The sum is referred to as the gravito-inertial acceleration (GIA) vector (see Fig. 1).

Fig. 1.

Fig. 1.

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The Visual and Vestibular Investigation System (VVIS) chair. During off-axis centrifugation, the net linear acceleration stimulating the otoliths is the vector sum of the centripetal force (Ac) and gravity (Ag), i.e., the GIA. The vector sum is shown. The gravity vector is pictured pointing upward (as a balancing force) to visualize the tilt illusion sensed during centrifugation. When the GIA is interpreted as the spatial vertical, the subject experiences a sensation of tilt. In this case, the constant force of gravity together with centripetal force, each of them 1 g, gives a perceived tilt of 45°. Reprinted from Hallgren et al. (2015) with permission of Macmillan Publishers Ltd, copyright 2015.

Otolith-driven eye movements reflect the response of the sensory epithelia to both translation and tilt (with respect to gravity) of the head. One example of an otolith-driven response is ocular counterrolling (OCR), which is generated when we turn around a corner (walking, driving, or biking) (Imai et al. 2001) or undergo centrifugation (MacDougall et al. 1999; Miller and Graybiel 1971; Woellner and Graybiel 1959). The OCR tends to orient the eyes toward the GIA. The ability to complete the orientation is thought to be crucial for our postural stability during movements (Imai et al. 2001).

The importance of the vestibular system, as well as the importance of gravity, for our ability to maintain balance becomes particularly clear when studied in relation to spaceflight. When orbiting around Earth, the space crew inside the International Space Station (ISS) is in a so-called “free fall,” meaning that instead of the 1-g gravity environment humans experience on Earth, the gravity is reduced to 10−6 g, i.e., microgravity. The vestibular receptors (the utricle and saccule) are the primary gravity sensors of the body, and their gravity dependence makes them especially vulnerable in a microgravity environment. In the absence of gravitational inputs, the otoliths will be forced to adapt to the new condition to be able to orient in space (Clarke et al. 2000). During the adaptation process, a deconditioning (decrease in gain of otolith-mediated reflex) of the otolith system is thought to take place, which is hypothesized to be the cause of several of the symptoms reported in returning astronauts, such as balance problems and dizziness (Anderson et al. 1986; Clement and Reschke 1996; Dai et al. 1994; Homick and Reschke 1977; Paloski et al. 1992; Reschke et al. 1986; Young et al. 1984). When the astronauts reenter the gravitational environment on Earth, a majority of them experience, among other effects, orthostatic intolerance and spatial disorientation as well as gaze control problems (Buckey et al. 1996; Fritsch-Yelle et al. 1996). Several studies have shown an activation of sympathetic outflow in response to postural changes, and therefore the otolith system is also hypothesized to be important in the prevention of orthostatic intolerance (Yates et al. 2014). A recent study has added evidence for the link between the vestibular and autonomic systems (Hallgren et al. 2015).

Since OCR is an accepted way to evaluate the condition of the otolith system (Clement and Reschke 1996), a number of studies have used the OCR as a measurement of the effect of microgravity on the vestibular system (Arrott and Young 1986; Diamond and Markham 1998; Hofstetter-Degen et al. 1993; Vogel and Kass 1986; Yakovleva et al. 1982; Young and Sinha 1998). However, there are contradicting results from studies showing an increase, a decrease, or no change in OCR on return compared with before flight. Clément and colleagues wrote a review covering all OCR data induced by static whole body tilt after (short term) shuttle missions in 2007. The 18 astronauts showed no significant change in OCR after flight compared with before flight (Clément et al. 2007). An important limitation of the studies evaluating centrifuge-induced OCR so far is the fact that all researchers investigated a small sample size, mostly because of the overall difficulty and restrictions on astronaut access. In addition, the above-mentioned results mostly come from short-term spaceflight, which makes it difficult to generalize to the effect of long-term exposure to microgravity. More recently, a couple of studies focusing on OCR induced by head tilt, the so-called static torsional otolith-cervical-ocular reflex (OCOR), have been performed by Kornilova and colleagues. They concluded that the otolith function was suppressed early after spaceflight and that it recovered within 8 or 9 days (Kornilova et al. 2007a, 2007b, 2011, 2012).

The aim of the present study was to investigate whether long-term exposure to microgravity results in changes in the otolith-mediated response OCR in returning astronauts. As hypothesized, a possible otolith deconditioning could be responsible for a number of negative effects seen in returning astronauts (see above). We aimed to collect sufficient data to make more convincing conclusions concerning the effect of spaceflight on the OCR response. With a bigger sample size, we were also able to look into the more subtle physiological effects, which could be learning effects due to spaceflight experience and adaptation as well as possible differences in OCR response between the two directions of rotation during centrifugation.

METHODS

We measured the otolith-mediated OCR response induced by centrifugation in a space crew before and after spaceflight to evaluate the otolith-mediated vestibular reflex.

We conducted our experiments in the Gagarin Cosmonaut Training Centre (Star City) near Moscow, Russia. A group of 25 (24 men and 1 woman) cosmonauts (average age of 46 yr, SD ± 6 yr) from the Russian Space Agency (Roscosmos) and 1 from the European Space Agency (ESA) (all denoted here as astronauts) took part in the study. The astronauts were tested before and after a 6-mo stay in the ISS. The average number of days spent in space was 164 (SD ± 22). The first astronaut participating in the study was tested in 2007 (ISS expedition 16) and the last one in 2015 (expedition 43). The preflight data were based on two baseline experiments [baseline data collections (BDCs)] that were conducted on average 55 (SD ± 29) days before launch. The astronauts were tested again two or three times after flight. The first postflight experiment took place 2 or 3 days after return (R+2/3), the second one 4 or 5 days after return (R+4/5), and the last one 9 or 10 days after return (R+9/10). Because of medical and organizational issues, we were not able to test all of the astronauts on the same day after return. On average, the first measurement took place 3.6 days (SD ± 1.2 days) after return to Earth.

All participants provided written informed consent prior to their participation. The study protocol was designed in accordance with the Declaration of Helsinki and was approved by the Institutional Review Boards of ESA, Antwerp University Hospital, and Roscosmos.

VVIS—evaluation of the otolith system.

For the experiment, the subject was seated in the Visual and Vestibular Investigation System (VVIS), a small centrifuge (rotation chair; see Fig. 1) built for the Neurolab shuttle mission. The astronaut was securely fixed in the chair, and head movements were restricted. The entire room was darkened to avoid visual motion feedback during rotation. The centrifuge allowed earth vertical rotation on a fixed distance of 0.5 m from the axis of rotation. In front of the astronaut, a screen was placed on which visual targets were present during parts of the experiments. After calibration of the video-goggles and a baseline recording, the astronaut was subjected to 1 g for 5 min in a counterclockwise (CCW) direction and 5 min in a clockwise (CW) direction subsequently. The rotation was always performed first in CCW and then in CW direction with a short pause in between (when the chair was turned around). The subject was facing the direction of motion for both CCW and CW rotation, right ear out during CCW rotation and left ear out during CW rotation. The maximum velocity of 254°/s was chosen to obtain a centripetal acceleration of 1 g outward. Combined with gravity, such a shear force constitutes a virtual sideways tilt of 45° (θ = 45° in Fig. 1), inducing an OCR of typically 5–7°, given a OCR gain of ∼15% in normal conditions (Collewijn et al. 1985).

Measurements of the OCR were taken before and during rotation according to a fixed protocol. The first measurement was taken during standstill, which meant no centripetal force acting on the body and an expected OCR of 0°. The second measurement was taken 40 s after the stable phase of rotation was reached. The 40 s of delay was implemented to allow the cupula of the horizontal semicircular canal to return to its original position, to make sure the measured OCR was based on contribution of the otolith system only. During the 20-s period when the OCR was measured, the subject observed a fixation dot that was visible on the screen in front of the subject. The dot was implemented to suppress other eye movements, such as saccades, during centrifugation. The OCR value was calculated as the average eye torsion over the 20-s-long recording (see example of raw OCR data in Fig. 2). The recording consisted of between approximately 600 and 1,000 frames representing a data point each. In addition, the standard deviation and the standard error of the OCR response were calculated for all the frames for every experiment. The difference in OCR between standstill and rotation was defined as the OCR outcome value, the “ΔOCR.” The preflight data, ΔOCRpreflight, was compared with the ΔOCRs recorded on return, the ΔOCRpostflight. The difference in ΔOCR preflight vs. postflight gave us an indication of the influence of microgravity on the otolith-mediated vestibular response. (We use the notation “OCR” during the rest of the article, always referring to the difference between standstill and rotation).

Fig. 2.

Fig. 2.

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Example of raw preflight and early postflight OCR data for 1 subject. A: example of OCR raw data for 1 subject, recorded before flight, left eye CCW rotation. B: OCR raw data for the same subject early after flight. This is what the data looks like when extracted from the video files in LabVIEW.

We recorded the induced OCR during the experiment using three-dimensional infrared videooculography (Moore et al. 1996).

Statistics.

The video files containing recordings of the eye movements were analyzed to calculate the torsion of the eyes, i.e., the OCR. To do this, we ran the files in a visual programming language. The program we used was custom made in National Instruments LabVIEW by one of the authors. An example of raw OCR data for one subject (left eye, CCW rotation) can be found in Fig. 2. Figure 2A shows a preflight measurement and Fig. 2B a corresponding plot with postflight data. Further statistical analyses were made in R (version 3.1.2) and Excel. To model the change in OCR between the preflight and postflight measurements, a linear mixed model was fitted with the OCR as dependent variable. Time (BDC, R+2/3, R+4/5, and R+9/10), direction of rotation (CCW and CW), and eye (left and right) were chosen as fixed factors, and in addition a random intercept for individuals was introduced to account for the dependence between observations within the same individual. Each OCR observation represents the average of a recording lasting up to 20 s. The 20 s consists of ∼1,000 frames, each frame representing 1 OCR value. We calculated an average and standard deviation of OCR over all those frames. Because of blinking and closed eyes, not all of the frames could be used for all subjects. The median number of frames that could be used for calculation of the average OCR was 815 frames, with median absolute deviation of 185. To take the individual variance into account, we weighted each OCR observation by the inverse of its variance. Time was entered as a categorical variable with four levels: BDC, R+2/3, R+4/5, and R+9/10. The two other independent variables (eye and rotation) were also categorical. Significance of the fixed effects was tested with an F-test with Kenward-Roger correction for the number of degrees of freedom. An F-test is superior to an asymptotic χ2-test for investigating the significance of the fixed effects in a linear mixed model, but this needs a balanced study design (i.e., the same number of observations within each group and at each time point). When this balance requirement cannot be met in practice, the Kenward-Roger correction on the number of degrees of freedom is recommended to obtain valid inferences based upon the F statistic (Halekoh and Højsgaard 2014). A post hoc analysis, to test whether pairwise differences in OCR between preflight and postflight time points were significant, was carried out with a Dunnett correction for multiple comparisons with the preflight time point as reference level.

RESULTS

Differences in OCR at different time points.

To model the change in OCR following a spaceflight, a linear mixed model of OCR vs. time was fitted, as described in methods, with time including all four time points [BDC, R+2/3, R+4/5, last experiment after flight (R+9/10)]. Not all astronauts were available for testing three times after flight, because of the evident restrictions in astronaut schedule and access. Therefore, the first postflight measurement was either 2 or 3 days (1 astronaut was tested on R+1) or 4 or 5 days after reentry. The linear mixed model showed a highly significant effect of time on the OCR (P < 0.001). A post hoc analysis, comparing preflight OCR with OCR at the three postflight time points, showed a statistically significant decrease in OCR at R+2/3 and at R+4/5. At R+9/10, there was no longer a difference in OCR compared with preflight OCR values. In Table 1, the OCR values, including standard deviation and standard error, can be found.

Table 1.

Weighted pre- and postflight OCR data

OCR, ° SD SE Gain n
BDC 6.99 1.99 0.66 0.155 ± 0.015 25
R+2/3 5.33 2.34 0.78 0.118 ± 0.017 12
R+4/5 5.99 1.71 0.57 0.133 ± 0.013 21
R+9/10 7.17 2.19 0.73 0.159 ± 0.016 22
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Values are the OCR values for the preflight experiment and the 3 postflight experiments, including SD and ± SE. The OCR was on average 6.99° (SE = 0.66°) before flight. At R+2/3, the OCR was significantly lower compared with preflight measurements. At the R+4/5 experiments, if available, the OCR was 5.99° (SE = 0.57°). Nine days after return, on the day of the late postflight experiment, the difference from the preflight value was no longer significant, indicating a recovery of the otolith system.

Of the 25 subjects, 19 had a decreased OCR after flight, 3 had no change or a very small change, and 1 had an increase in OCR after spaceflight. Two of the 25 subjects were not available for testing R+2/3 or at R+4/5, because of complications. For those two, we only have preflight data and OCR data from R+9/10. For comparison purpose, we also report the gain (see Table 1). This was computed by dividing all OCR values by 45°, the tilt of the GIA.

Figure 3 shows the mean values of OCR (including standard error) for the four time points, averaged over directions and eyes; the figure displays the OCR for the preflight experiment (6.99 ± 0.66°) as well as for the three postflight experiments. Figure 4 shows the average raw OCR data response grouped according to the direction of rotation; in each diagram, i.e., for each rotation, the recorded OCR of the two eyes is also individually presented.

Fig. 3.

Fig. 3.

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Change in OCR response, preflight compared with postflight: weighted OCR data, averaged over eyes and rotation. The OCR response is presented with the weighted standard error. The first measurement was performed before spaceflight, and the last 3 experiments were performed after flight. The first postflight experiment took place 2 or 3 days after return, the second 4 or 5 days after return, and the late postflight experiment 9 or 10 days after return from a 6-mo stay in the ISS. At the preflight experiment (BDC) all 25 subjects were available for testing; 12 subjects were tested at R+2/3, 21 at R+4/5, and 22 at R+9/10. At R+2/3 OCR was 2.21° (SE = 0.20°) lower compared with preflight OCR, a significant decrease in OCR response (P < 0.001). Nine days after return, during the late postflight experiment, OCR returned back to preflight values.

Fig. 4.

Fig. 4.

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Alteration of OCR for the 2 directions of rotation and the 2 eyes separately: mean raw OCR values for the 2 directions of rotation divided into 2 graphs. Each graph represents the OCR for the 2 eyes separately. The mean raw OCR data are plotted together with the standard error. A: average OCR for the first direction of rotation, the CCW rotation, for the 25 astronauts. B: average OCR for the second direction of rotation, the CW rotation, for the 25 astronauts. The pure raw data (and not the mean OCR) were analyzed with a linear mixed model to investigate whether there were any differences in OCR between the 2 directions of rotation and between the 2 eyes.

Differences in OCR between two directions of rotations.

During the centrifugation, the subject was always rotated first CCW and then in the CW direction, with a short pause in between. When comparing the OCR data from the two directions of rotations for the preflight experiment, using the linear mixed model, we observed a significantly higher OCR for the CCW (first direction of) rotation. The recorded OCR value was 0.57° (SE = 0.22°, P = 0.008) lower during CW rotation compared with that recorded during CCW rotation. For the postflight experiments, no significant difference between the rotation directions was found.

First-time fliers vs. experienced fliers.

Of the 25 astronauts, 13 were first-time fliers and 12 had been flying at least once prior to our study, with 2 of them already flying four times before participating in our experiment. We compared OCR vs. flight experience for the two groups, using the linear mixed model. We saw a trend in the difference in OCR between the two groups. The OCR was consistently lower, across all time points, for the group of experienced fliers compared with the first-time fliers, but at none of the time points was this difference significant. A model across all time points gave an OCR that was on average 0.99° lower (SE ± 0.68°) for the experienced fliers (P > 0.05).

DISCUSSION

Effect of microgravity on OCR reflex.

The aim of this study was to investigate the effect of long-term exposure to microgravity on the otolith-mediated vestibular response in a considerably large group of 25 astronauts returning from the ISS after 6-mo missions. Our main finding was that the OCR response was significantly decreased early after spaceflight (at R+2/3 and R+4/5). This indicates that the otolith-mediated vestibular response among the astronauts was affected during the first days after return, likely because of the absence of gravitational input during the preceding 6 mo. A recording of a lower OCR after spaceflight agrees with a number of studies performed in the last decades (Dai et al. 1994; Diamond and Markham 1998; Kornilova et al. 2012; Moore et al. 2005; Young and Sinha 1998). Clément and colleagues found no significant change in OCR after flight compared with before flight in 18 astronauts tested after (short term) shuttle missions (Clément et al. 2007). A possible reason for this could be the duration of the shuttle missions, <2 wk, while the data collected in the present study cover astronauts who spend 6 mo in space. Another difference, however, may be due to the difference in vestibular stimulation between static tilt (which elicits response from the vertical semicircular canals) and centrifugation (which does not). An important limitation of the studies evaluating centrifuge-induced OCR so far is the fact that all investigated a small sample size, which has made generalization difficult.

Kornilova and colleagues (Kornilova et al. 2012) measured static torsional OCOR in 17 cosmonauts before and after spaceflight. Of these 17 subjects, 7 had a 50% decrease of OCOR at the first day after return (R+1 or R+2), in 3 a reversed OCOR was measured, in 4 no OCOR was registered, and 3 showed no difference between pre- and postflight OCOR. The results for OCOR presented by Kornilova and colleagues showed a preflight gain of 0.21 and 0.11, 0.15, and 0.22 for the three postflight time points, respectively (with the absolute values 6.59°, 2.94°, 4.25°, and 6.81°). Our results, reported in Table 1, show a preflight gain of 0.15 and postflight OCR gains of 0.12, 0.13, and 0.16. This suggests that when proprioceptive input from the neck afferents is available the response to tilt seems enhanced, at least during the period when microgravity effects are not dominant. The present experiment differs from previous experiments by Kornilova et al. in the fact that no neck influence is present in the centrifugation paradigm, where all subjects are seated upright with the head fixed in the vertical position. Consequently, no proprioceptive afferent input is given to the vestibular system. To solely study the otolith-mediated response and the effect of microgravity, centrifugation appears to be a purer stimulus.

Moreover, no previous study covered as many as 25 astronauts returning from a 6-mo stay in space. The strong significance of the decreased OCR adds to the evidence that microgravity causes adaptive changes in the otolith-mediated vestibular response. At the last postflight experiment, 9 days after return, there was no longer a significant difference of the measured OCR response compared with preflight values. This suggests that the OCR reflex was back at baseline level and that the otolith-mediated system was fully recovered, which agrees with the results of Kornilova et al. (2012). This delay in adaptation of the otolith-mediated vestibular response can have negative consequences for astronauts when reentering gravity. In our study, we were not able to correlate the change in OCR with any of those parameters associated with disequilibrium. Entering a gravitational environment other than the one here on Earth, such as for example Martian gravity, while not being able to fully function during the first days after landing may have severe consequences for the crew. There will be no room for mistakes during a recovery period. Preferably, it would not be necessary to recover if the cause (lack of gravity) could be removed in the first place. The present data suggest a recovery rate of a little over 1 wk, but this reflects the vestibular response. A recent single case study, however, has shown that even 9 days after return an astronaut still showed alterations in the cortical vestibular network, as measured by means of functional MRI (Demertzi et al. 2015). This suggests that the underlying neural adaptation takes longer than is seen in the vestibular reflex based on peripheral end organs, e.g., the otoliths. Evidently, this must be investigated further in a larger sample size, but the question arises of where the impact of microgravity takes place, i.e., on the peripheral end organ at the level of the otoliths or more centrally.

Differences in OCR between two directions of rotations.

The OCR response was found to be higher during the CCW (first rotation) than for the recording during the CW rotation, which could be a consequence of habituation. During postflight experiments, the difference was no longer significant between the two tests (CCW and CW). It could be speculated that a difference in OCR between the two rotations was still present, but because of the lower postflight OCR values the difference was too small to detect. Up front, we did not expect to find a difference in OCR between the two directions. To our knowledge, this has not been seen in previous studies. To make any conclusion concerning a learning effect, further testing would be necessary, preferably with a counterbalanced order of the two directions of rotation.

Experienced fliers.

Even though the mean OCR was consistently lower across all time points for the group of experienced fliers, for none of the time points was this difference significant. Within both groups the variance in OCR was large, so even if a lower OCR was observed the P value was not significant. Moreover, the large variance is likely due to the fact that the experienced fliers' group was a heterogeneous mixture of second-, third-, and fourth-time fliers. Preferably, the same subject should be measured at least twice, first as a first-time flier and then again as an experienced flier. From a study design point of view, pairwise tests within subjects are a much stronger and more powerful analysis, as each subject acts as his/her own control. Therefore, we cannot exclude that flight experience can have a significant influence on the OCR response. A test-retest study with the same subjects is currently ongoing to further investigate this phenomenon.

Countermeasures.

One suggested way to counteract negative effects related to spaceflight is to create artificial gravity in space (Clément et al. 2015; Moore et al. 2001). This could also be an efficient solution when it comes to otolith-based problems. If stimulating the otolith system with artificial gravity during spaceflight could prevent adaptation, we might not see those problems upon return. After the 16-day-long NASA-led Neurolab mission in 1998, the artificial gravity hypothesis was presented. Four crewmembers were exposed to artificial gravity by means of centrifugation during spaceflight. It turned out that the magnitude of the OCR reflex was maintained throughout the flight as well as on return. (Moore et al. 2005). However, in 2007, Clément and colleagues reviewed the OCR response in 18 astronauts retuning from six different short-term shuttle missions (Clément et al. 2007). They did not find any change in OCR response even without in-flight centrifugation. It is important, though, to keep in mind that the shuttle missions are short-term flights compared with the 165 days our subjects on average spent in space. The number of subjects was also much smaller than that in our study. To make further recommendations concerning artificial gravity as a countermeasure against a decreased otolith function, further testing needs to be done, preferably evaluating artificial gravity during long-term spaceflights.

Conclusions.

After a long-term exposure to microgravity, the otolith-mediated vestibular response among returning astronauts was highly affected. The OCR reflex was significantly decreased in the 25 astronauts taking part in the study. Nine days after return, the OCR was back at preflight values, indicating a full recovery of the peripheral otolith system. During this study, sufficient data have been collected to make general physiological conclusions about the effect of microgravity on the otolith system.

GRANTS

This study is funded by the European Space Agency (ESA) (ESA-AO-2004-093), the Russian Federal Space Agency (Roscosmos), Belgian Science Policy (Prodex), the University of Antwerp, and the Russian Academy of Sciences Institute of Biomedical Problems (IBMP). A. Van Ombergen is a research assistant for the Research Foundation Flanders (Belgium, FWO-Vlaanderen, Grants 11U6414N and 11U6416N).

DISCLOSURES

No conflicts of interest, financial or otherwise, are declared by the author(s).

AUTHOR CONTRIBUTIONS

E.H., D.G., and F.L.W. performed experiments; E.H. and E.F. analyzed data; E.H., E.F., and F.L.W. interpreted results of experiments; E.H. prepared figures; E.H. drafted manuscript; E.H., L.K., E.F., S.T.M., G.C., A.V.O., and F.L.W. edited and revised manuscript; E.H., L.K., E.F., D.G., S.T.M., G.C., A.V.O., H.G.M., I.N., and F.L.W. approved final version of manuscript; L.K., S.T.M., G.C., H.G.M., and F.L.W. conception and design of research.

ACKNOWLEDGMENTS

We thank all participating crewmembers and Pieter Rombaut for the drawing of the VVIS chair.

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