Astronauts eye-head coordination dysfunction over the course of twenty space shuttle flights

Abstract

BACKGROUND:

Coordination of motor activity is adapted to Earth’s gravity (1 g). However, during space flight the gravity level changes from Earth gravity to hypergravity during launch, and to microgravity (0 g) in orbit. This transition between gravity levels may alter the coordination between eye and head movements in gaze performance.

OBJECTIVE:

We explored how weightlessness during space flight altered the astronauts’ eye-head coordination (EHC) with respect to flight day and target eccentricity.

METHODS:

Thirty-four astronauts of 20 Space Shuttle missions had to acquire visual targets with angular offsets of 20°, 30°, and 49°.

RESULTS:

Measurements of eye, head, and gaze positions collected before and during flight days 1 to 15 indicated changes during target acquisition that varied as a function of flight days and target eccentricity.

CONCLUSIONS:

The in-flight alterations in EHC were presumably the result of a combination of several factors, including a transfer from allocentric to egocentric reference for spatial orientation in absence of a gravitational reference, the generation of slower head movements to attenuate motion sickness, and a decrease in smooth pursuit and vestibulo-ocular reflex performance. These results confirm that humans have several strategies for gaze behavior, between which they switch depending on the environmental conditions.

Keywords

Eye-head coordination microgravity vestibulo-ocular reflex saccades gaze space motion sickness

1 Introduction

Previous experiments on visual target acquisition during space flight have given conflicting results. Saccadic peak eye velocity has been reported to increase in some astronauts, and to decrease in others. Also, the amplitude of eye movements during horizontal and vertical tracking increased in orbit in some cosmonauts, but decreased in others [1 , 30].

One problem when comparing the results across these previous studies is that measurements were obtained on different flight days (FD). Also, the first in-flight measurements of eye-head coordination (EHC) in these studies were made from flight day 5 [1], so the immediate effects of exposure to 0 g were not documented.

Conflicting results were also found in other cognitive performances in weightlessness. Wollseitfen et al. [32] reported faster reaction time in a complex mental task, as well as in combination with oddball paradigm [31]. In contrast, Stahn et al. [21], using visual-spatial updating task found impaired pointing performance and increased reaction time. Similarly, increased reaction time of Go/No-Go continuous performance task was reported in a very recent article of Friedl-Werner et al. [9]. These performances, however, were studied only during weightlessness in parabolic flights.

The purpose of the present study was to explore whether and how entry into weightlessness altered EHC for visual target acquisition. We report here the results obtained in 34 astronauts starting on FD1 and up to FD15. Because of the changes in vestibular and proprioceptive sensory signals, perceived space orientation, background brain activity, biomechanics of head motion immediately after insertion into orbit, we hypothesized that eye-head coordination during visual target acquisition would be altered in 0 g compared to 1 g, and this alteration would decrease over a period of two weeks in space.

2 Materials and methods

2.1 Subjects

Thirty-four NASA astronauts (30 males and 4 females) ranging in age from 34 to 54 years (mean 41 years) participated in this investigation. These astronauts flew on board 20 Space Shuttle missions. None of the participants had any oculomotor, vestibular abnormalities, or were taking any drugs with effects on the nervous system. The experimental protocol was approved by the NASA Johnson Space Center Institutional Review Board. All astronauts gave their written informed consent to participate in this investigation in accordance with the tenets of the Declaration of Helsinki.

2.2 Visual targets

Visual targets subtending 0.5° were fixed to a screen at a distance of 86.4 cm from the subjects. Targets were located at angular distances of 20°, 30°, and 49° off center in the horizontal plane at subject’s eye level. To easily differentiate between targets, each target corresponding to its degree of angular offset from center was color-coded (20° green, 30° red, 49° blue).

2.3 Eye and head measurements

Horizontal eye positions were measured using standard electro-oculography (EOG). Two electrodes were applied to the outer canthus of each eye, and one ground electrode was applied to a neutral surface behind the right ear. The EOG signals were amplified and digitized at a sampling rate of 500 Hz. Extraneous high frequency noise was digitally removed by filtering before processing with a finite impulse response low-pass Hamming window filter with a cutoff frequency of 30 Hz.

Horizontal head velocities were measured using a tri-axial angular rate sensor fixed to the head with the webbing from a hardhat liner. The angular rate sensor was located approximately on the apex of the skull and adjusted prior to each test session to minimize cross talk between all 3 axes. The signals from the rate sensor were digitized at 500 Hz and filtered using the same procedure as the EOG signals.

Horizontal head position was calibrated using a low power laser mounted on the hardhat liner that could be adjusted so that the laser was located centrally on the forehead between the two eyes. When activated, the subject moved the laser point on the central target and to each of the color-coded targets.

2.4 Experimental protocol

Eye movement calibration was performed by having the subjects oscillating their heads at approximately 0.25 Hz at amplitude of 30° to the right and to the left while fixating the central target. Based on the vestibulo-ocular reflex (VOR) thus generated, the calculated angular head position was used to determine the expected eye position required to maintain visual fixation. These expected eye positions were compared with the corresponding EOG signals to yield the volts-to-degree relationship necessary for calculating a calibration curve.

Eye velocity was obtained through differentiation of the filtered eye position signal. During the visual target acquisition task, the operator called out the various targets (“right green”, “left green”, “right red”, “left red”, “right blue”, “left blue”) in a predetermined random order. The crewmembers were asked to look from a central fixation point to the called target as quickly and accurately as possible using both the head and eyes.

Crewmembers maintained fixation on the called target for a minimum of 1.5 s, and then returned their gaze to the center target for approximately 10 s. This was to ensure that the cupula of the horizontal semicircular canals had returned to its original position before the next trial. Each target was tested between 2–5 trials depending on time constraints.

For the 20° and 30° targets, data was collected 10 days before launch (Pre, n = 34) and then on FD1 (n = 32), FD2 (n = 33), FD5 (n = 20), and FD 15 (n = 6). A subset of our astronaut subjects performed the experiment for the 49° target. This condition was considered a supplemental objective, and unfortunately no preflight data was collected for this target eccentricity.

Nevertheless, in orbit, the experiment with the 49° target was performed on FD1 (n = 12), FD2 (n = 10), FD3 (n = 3), FD5 (n = 11), FD7 (n = 9), FD11 (n = 13), FD13 (n = 2), and FD15 (n = 6).

Figure 1 represents a typical target acquisition trial. Gaze is the sum of head and eye positions. The following duration, position, and velocity parameters were calculated from the eye, head, and gaze measurements: (a) time to primary saccade; (b) duration of primary saccade; (c) amplitude of primary saccade; (d) peak velocity of primary saccade; (e) time to final position; and (f) final position. The peak acceleration of the primary head saccade was also calculated.

Fig. 1

Record of target acquisition.

2.5 Statistical analysis

Two-way (session day: Pre, FD1, FD2, FD5, FD15; target offset: 20°, 30°) ANOVAs were used. The measurement prior flight was taken only at 20° and 30° offsets. One-way ANOVAs were used for the 49° target offset with factor days: FD1, FD2, FD3, FD5, FD7, FD11, FD13, and FD15.

After the completion of the ANOVAs, Fisher Least Significant Difference (LSD) tests were used for pairwise comparisons of the means, valid only for the significant effects. A plot of the residuals versus fitted values and the quantiles plots (Normal and Half-Normal) was used for each response variable to demonstrate the adequacy of the distributional assumptions regarding use of linear regressions and ANOVAs.

All analyses were conducted using statistical package GenStat [10], R environment (R Core Team) [23], and R package ggplot2.

3 Results

3.1 Eye and head coordination strategy

During the acquisition of visual targets situated 20° off-center and more, humans typically use both eye and head movements. The closer the target is to the extreme oculomotor range (about 55°), the more the head contributes to the performance [11]. The head, having greater inertia than the eye, typically moves after the eye has moved in the orbit. At the end of the eye saccade the gaze has already reached its final position, but the head continues to move. The head movement stimulates the horizontal semicircular canals, which produces an eye movement through the VOR that is opposite in direction and velocity to that of the head. When moving to a target gaze often undershoots or overshoots the target and corrective eye saccades occur to reposition the gaze on the target. In general, the total gaze movement is greater than the total head movement, so that the final position of the eye is offset in the direction of head movement [17]. The results from the statistical analysis using ANOVAs are presented in Tables 1 and 2.

Table 1
Statistical significance (P-value) of the main effects and the interaction of factors ‘day’ and ‘target’ for head, gaze and eye. Results of two-way ANOVA’s for the 20°, 30° and 49° targets

Response Variable Factors Gaze Head Eye

Time to Final Position day <0.001 <0.001 <0.001

target <0.001 0.012 0.002

day×target 0.074 <0.001 0.097

Final Position day <0.001 <0.001 <0.001

target <0.001 <0.001 <0.001

day×target <0.001 0.048 <0.001

Time to Primary Saccade day <0.001 <0.001 <0.001

target <0.001 <0.001 <0.001

day×target 0.002 0.009 <0.001

Amplitude of Primary Saccade day <0.001 <0.001 <0.001

target <0.001 <0.001 <0.001

da×target <0.001 0.161 0.027

Peak Velocity of Primary Saccade day <0.001 NS <0.001

target <0.001 <0.001 NS

day×target NS NS NS

Duration of Primary Eye Saccade day NA NA <0.001

target NA NA <0.001

day×target NA NA 0.034

Acceleration of Primary Head Saccade day NA 0.018 NA

target NA <0.001 NA

day×target NA 0.018 NA

Response Variable	Factors	Gaze	Head	Eye
Time to Final Position	day	<0.001	<0.001	<0.001
		target	<0.001	0.012	0.002
		day×target	0.074	<0.001	0.097
Final Position	day	<0.001	<0.001	<0.001
		target	<0.001	<0.001	<0.001
		day×target	<0.001	0.048	<0.001
Time to Primary Saccade	day	<0.001	<0.001	<0.001
		target	<0.001	<0.001	<0.001
		day×target	0.002	0.009	<0.001
Amplitude of Primary Saccade	day	<0.001	<0.001	<0.001
	target	<0.001	<0.001	<0.001
	da×target	<0.001	0.161	0.027
Peak Velocity of Primary Saccade	day	<0.001	NS	<0.001
	target	<0.001	<0.001	NS
	day×target	NS	NS	NS
Duration of Primary Eye Saccade	day	NA	NA	<0.001
		target	NA	NA	<0.001
		day×target	NA	NA	0.034
Acceleration of Primary Head Saccade	day	NA	0.018	NA
		target	NA	<0.001	NA
		day×target	NA	0.018	NA

NS: not significant; NA: not applicable.

Table 2

Statistical significance (P-value) of the main effects of factor day for gaze, head, and eye. Results of one-way ANOVA for 49° target

Response variable	Factor	Gaze	Head	Eye
Time to Final Position	day	0.007	<0.001	<0.001
Final Position	day	NS	<0.001	<0.001
Time to Primary Saccade	day	<0.001	<0.001	<0.001
Amplitude of Primary Saccade	day	<0.001	<0.001	<0.001
Peak Velocity of Primary Saccade	day	<0.001	0.036	<0.001
Duration of Primary Eye Saccade	day	NA	NA	<0.001
Acceleration of Primary Head Saccade	day	NA	<0.001	NA

NS: not significant; NA: not applicable.

3.2 Gaze dynamics

The final position of gaze was right on target for all preflight and in- flight trials (Fig. 2A). However, the time to reach this final position was different across flight days (Fig. 2B). This duration was longer than preflight with a peak on FD2 for the 20° and 30° targets. On FD15 the time for the gaze to reach the target had returned to baseline. For the 49° target the peak was on FD5 and also decreased gradually till FD15. The ANOVA indicated a significant effect of target, day, and interaction between the two(Table 1).

Fig. 2

Gaze parameters changes (mean±standard error) across the flight days in target acquisition of 20°, 30° and 49° targets. Abbreviations: PRE – preflight, FD1 – flight day 1, FD2 – flight day 2, FD3 – flight day 3, FD5 – flight day 5, FD7 – flight day 7, FD11 – flight day 11, FD13 - flight day 13, FD15 – flight day 15.

Significant changes appeared also in all other parameters as shown in Tables 1 and 2, and Fig. 2. The peak velocity of the primary saccade and its amplitude decreased (the peak was FD2 for the velocity to all targets; and FD2 for the amplitude to 20° and 30° targets and FD1 and FD7 to 49° target) while the time to primary gaze saccade increased (Fig. 2C and D) (the peak was on FD2 to all targets).

3.3 Head dynamics

Since the mass of the head is larger than the mass of the eye, we expected that the change seen above in the gaze strategy during space flight were caused mainly by the change in the head strategy. As expected, for the 20° and 30° targets the time to final head position was significantly longer on FD2 compared to preflight (Fig. 3A). It then decreased till FD15 but remained longer than preflight. For the 49° target the time to final head position was significantly larger on FD5 than for the subsequent flightdays.

Fig. 3

Head parameters changes (mean±standard error) across the flight days in target acquisition of 20°, 30° and 49° targets. For the abbreviations see Fig. 2.

The final head position was significantly different across days and targets. For the 20° and 30° targets, the lowest amplitude of head movement was observed at FD15 (Fig. 3B). Less changes were seen for the 49° target. For the 20° and 30° targets the time to primary head saccade was longer on FD1 and FD2 compared to preflight (Fig. 3C). This duration decreased during the rest of the flight with values above the baseline. F or the 49° target the maximal increase of the primary head saccade duration was on FD5 and then it decreased till FD15. The changes in the amplitude of the primary head saccade were similar to those of the final head position, i.e. significant for factors day and target, but not significant interaction between both (Fig. 3D).

The changes of the peak velocity (Fig. 3E) and acceleration (Fig. 3F) of the primary head saccade were significant for both target eccentricity and day. The interaction was also significant for the acceleration. For the 20° and 30° targets the head peak velocity and acceleration were smaller inflight with maximal decrease on FD2. For the 49° target the peak head velocity and acceleration was smaller on FD1, FD5, and FD11 than for the other days.

3.4 Eye dynamics

The time to final eye position was significantly different across days and target, but there was no interaction. For the 20° and 30° targets it was the longest on FD1, returned to baseline on FD2, and then increased again during the rest of the flight (Fig. 4A). A similar decrease in time to final eye position between FD1 and FD2 was observed for the 49° target.

Fig. 4

Eye parameters changes (mean±standard error) across the flight days in target acquisition of 20°, 30° and 49° targets. For the abbreviations see Fig. 2.

The final eye position was significantly different across target, day, and their interaction. For the 20° and 30° targets the final eye position decreased on FD1 compared to preflight, then returned to baseline on FD2 and decreased again on FD5 (Fig. 4B). The maximal increase was on FD15. For the 49° target the final eye position was the smallest on FD5 and the largest on FD15.

The time to primary eye saccade was different across target, day, and their interaction. However, the pattern of change across flight days was not the same as for the final position time (Fig. 4C). For the 20° and 30° targets the time to primary eye saccade was the longest on FD2. For the 49° target there was an increase between FD1 and FD2 similarly to 20° and 30° targets but it was the longest on FD5.

The amplitude of the primary eye saccade was significantly different across target, day, and their interaction. For the 20° and 30° targets the amplitude was smaller than preflight on FD2, returned to baseline on FD5, and then decreased again on FD15 (Fig. 4D). For the 49° target it was smaller on FD1 and FD2 compared to FD5 where was the peak increase.

The peak velocity of the primary eye saccade was significantly different across day but not across eccentricity and their interaction. For the 20° and 30° targets the peak eye velocity decreased on FD1 and FD2 compared to preflight, and returned to baseline on FD5 (Fig. 4E). For the 49° target the peak eye velocity similarly decreased on FD2, compared to FD1. It was the smallest on FD2 and the highest on FD3 and FD5.

The duration of the primary eye saccade was significantly different across day, eccentricity, and their interaction. For the 20° and 30° targets the duration increased with peak on FD2 compared to baseline, and then returned to normal (Fig. 4F). For the 49° target, the eye saccade duration also increased on FD2 and after that, till the end of the flight, it was relatively lower.

The correlations between head and eye movements calculated for factors day and target for the 20°, 30°, and 49° were the following:

Time to primary saccade: r = 0.529 (P < 0.05)

Amplitude of primary saccade: r = 0.639 (P < 0.05)

Time to final position: r = 0.294 (NS)

Final position: r = 0.194 (NS)

Peak velocity of primary saccade: r = 0.394 (NS)

4 Discussion

This study investigated the dynamics of EHC in target acquisition in 34 astronauts participating in 20 Space Shuttle missions lasting 10–15 days. The results showed that the transition from 1 g to 0 g followed by two weeks in 0 g significantly affected eye-head coordination during the acquisition of visual targets at different angular distances. We observed an increase in the duration required to reach the target (final position), which indicates a decrease in performance. We also observed significant changes in amplitude/velocity/acceleration of the primary eye and head saccades as a function of flight day. These findings show a clear adaptation in astronauts’ gaze strategy after insertion into weightlessness.

4.1 Saccades and smooth pursuit during previous studies

Previous studies on visual target acquisition in humans during space flight are rare and show conflicting findings. Uri et al. [28] studied saccadic eye movements toward 10° and 20° targets in 6 astronauts during 6–8 days Space Shuttle flights. Peak eye velocity decreased in 5 subjects, but increased in 1 subject. The amplitude of the primary eye saccade tended to decrease, but this change was not found to be significant. However, only one subject was tested from FD1 to FD 5; the other 4 subjects were tested only 1 or 2 days during the flight.

Tomilovskaya et al. [25] studied visual target acquisition in 7 cosmonauts before and after 6-month space flights. After landing, 3 subjects showed a decrease in peak eye velocity but no significant decrease in peak head velocity, whereas 4 subjects showed an increase in peak head velocity. The authors tried to explain the difference by the fact that some subjects were pilots and the others not. A recent report [17] showed that the mean time to acquire visual targets after the flight was slower than before the flight, and that performance returned to baseline after 48 hours. Results were similar after space flight with duration ranging from 6 to 17 days.

Andre-Deshays et al. [1] showed that the amplitude of the primary eye saccades to horizontal targets overshot when tested on FD5 in 1 cosmonaut, and returned to baseline on FD18 and FD22 (the primary saccades of the second cosmonaut tested only on FD20 were on target). The two cosmonauts did not show any change in vertical and horizontal smooth pursuit in orbit. By contrast, Kornilova et al. [14] reported changes in pursuit tracking of targets moving vertically during space flight in 5 cosmonauts. Early in microgravity the pursuit was lagging behind the stimulus and corrective saccades appeared. As the flight progressed smooth pursuit deteriorated. Immediately postflight smooth pursuit improved, which the authors consider as indicating that the deficiency in microgravity may be of central origin. The authors however did not specify in which flight days their data were collected.

A decrease in corrective saccades velocity and amplitude during horizontal sinusoidal smooth pursuit was observed in 4 astronauts on flight days 2, 5, 10, and 16 [20]. An immediate recovery occurred after landing, because no differences in saccade velocity and amplitude were seen postflight compared to preflight. Vesterhauge et al. [30] found that the velocity of the saccades did not change significantly in 9 subjects during the microgravity phase of parabolic flight compared to normal gravity. Finally, experiments on monkeys in space showed gaze hypermetrics, a decrease in head amplitude and velocity, and an increase in saccadic velocity [5 , 15].

4.2 Eye-head coordination strategies for gaze performance

Our experiment performed on a larger number of days, beginning with FD1, and on a larger number of subjects than previous studies shows more comprehensive and consistent results than the previous studies above. For the 20° and 30° targets, on FD1, the time to reach the final gaze position increased compared to preflight because of a decrease in gaze velocity.

This decrease in gaze velocity is caused by a decreased velocity of both eye and head primary saccades. In addition, the head movement is slower than the eye movement and, interestingly, with increased amplitude. At the beginning of the flight, the astronauts presumably reduce their head motion to mitigate space motion sickness. Any head movement that provokes the nauseogenic sensations leads to an increased duration for the head movement. On FD2 the time to reach the final gaze position also increased, presumably because of a different gaze strategy. We believe this increase is due to a further decrease of the eye and head velocity because the amplitude of the head movement decreased. The time to reach the final gaze position on FD5 and FD15 showed gradual return to baseline, which suggests an adaptation to microgravity.

Both the peak velocity and amplitude of the primary eye saccade returned to baseline earlier (on FD5) compared to head velocity/acceleration. This indicates an earlier adaptation of the saccadic movement compared to the head velocity/acceleration, which remained consistently slower than normal, presumably to minimize space motion sickness. For the 49° target the time to reach the final gaze position had its peak of increase later, on FD5, compared to short distance targets (20° and 30°). This also indicates a change in gaze strategy. After FD5, the time to reach the targets gradually reduced with a maximum on FD13 and FD15, which we assume i s close to normal values, basing on the dynamics of the results of the 20° and 30° targets. We explain the target distance effect by two reasons. One is the strategy of rotation of the head with its big mass toward an approximately double angular distance. The second reason is the astronauts’ reduction of their head motion toward a larger angular distance in order to attenuate space motion sickness symptoms.

These reasons are supported by the decrease in head in velocity and amplitude throughout the flight.

4.3 Underlying adaptive mechanisms

The observed changes in eye-head coordination during target acquisition are presumably due to a combination of several factors and mechanisms. One is the velocity storage mechanism, which is generated in the vestibular nuclei and controlled through the nodulus and uvula of the vestibulo-cerebellum. It has been shown that in microgravity the velocity storage orientation moves from an allocentric, gravity-referenced frame to an egocentric, head-referenced frame [6, 16]. Another hypothesis is that humans can have several different sets of reflexes, between which they are able to switch rapidly based on the environment in which they are immersed. Procedures that help to transfer sensorimotor skills from one environment (e.g. gravitational) to another must be learned [19]. Factor that supposedly influences eye-head coordination in the gaze performance is a change in the perception of space. Weightlessness modifies the vestibular and somatosensory inputs, which contribute to a mental representation of 3D space in the vestibular cortex [4]. A change in the mental representation of space may have an effect on the estimation of target eccentricity and distance, and therefore target acquisition performance.

Alterations in pursuit eye movements related to space flight have been attributed to changes in the tonic levels of otolith activity in the vestibulo-cerebellum [1]. Such change in tonic activity inflight could affect also gaze target acquisition. In a gravitational field, the otoliths contribute to the brain function in defining the position of the head in space by detecting head tilt with respect to the gravity vector. In the absence of a gravitational reference during space flight, the static otolith signals are ineffective and astronauts relay mainly on visual and proprioceptive information to interpret the position of the head. Therefore the altered vestibular and somatosensory inputs may lead to changes in mental representation of space [2]. The wrong interpretation of the head’s position in space would lead to an altered perception of gaze position, which could alter the brain commands for head and eye movement during gaze target acquisition.

Other contributing factors for altered eye-head coordination in gaze performance during space flight are body fluid shifts and microcirculatory changes in brain, head and neck tissues, muscles and ligaments [18, 22]. These changes affect not only the mass of head and neck, but also the cues from the proprioceptors and motor performance including mechanically [24]. The absence of gravity causes increase in the interdiscal space in the cervical region due to absence of weight pressure from the body mass, which is another biomechanical factor that could influence target acquisition when head movement participates [12].

It has been reported [18, 22] that in 0 g the long-term redistribution of blood results in an increase of blood volume and blood pressure within the head. The associated increased supply of oxygen to the brain could lead to physiological changes in the central nervous system (CNS), which can affect performance [8]. In addition, it has been found that the electro-cortical activity in the frontal brain regions (Brodman areas 6 and 9) increased in weightlessness during parabolic flight [3]. These frontal brain regions play a critical role in the planning and coordination of movements and in spatial memory. An increase in cortical activity may reflect mechanisms by which the CNS detects and processes changing gravity conditions in order to maintain motor performance. Other evidence of changes in brain cortical activity in weightlessness comes from studies showing increased beta oscillation and decreased cognitive performance [18, 26]. And very recent experiments [31, 32] reveal altered spatial cognition and impaired attentional processing during different gravity conditions in-flight.

Motion sickness symptoms, like somnolence, malaise and lethargy, also influence sensorimotor performance by causing delay, and producing slower, less accurate saccades [27]. Among the probable factors underlying the observed changes in eye- head coordination in the present study could be neural mechanism of functional rearrangement in the brain centers regulating patterns of motor behavior. A number of investigators have assessed the role of vestibular-based subsystems during space flight (see review in Clément & Reschke [4]). Another hypothesis is a mechanism of separation between the neural networks that control the eye and head during a coordinated action.

Vasudevan & Bastian [29] have demonstrated that there is partial overlap in the functional networks coordinating different motion. Similar findings are established in other vertebrates [13].

5 Conclusion

The findings of this study are important in two aspects. One, show alteration of gaze performance during target acquisition as a function of flight days and target eccentricity in space flights. The other, for space exploration because the control of eye-head coordination in gaze performance is critical for spatial orientation, piloting, and locomotion in altered gravity. The current plan of space agencies is to send humans in space on long-duration missions to explore the surface of Moon and Mars. These missions will include transitions between different gravity levels (1 g, 0 g, 0.16 g, 0.38 g). It is critical to know the dynamics of gaze dysfunction and how the brain strategies of eye-head coordination in gaze behavior adapt to these transitions for minimizing the risks of impaired control of spacecraft and the spatial disorientation due to vestibular and other sensorimotor alterations.

Funding

This study was funded by the Extended Duration Orbiter Medical Project of the NASA Johnson Space Center Space Life Sciences Directorate (Reschke) and Centre National d’Etudes Spatiales (Clement).

Footnotes

Acknowledgments

We would like to thank the participating crewmembers and the personnel of the Neuroscience Laboratory at the NASA Johnson Space Center for their help with data collection and data analysis.

Author contribution

O.I.K., M.F.R., and G.C. contributed for the main text. O.I.K. prepared Figs. 1–4 and Tables 1, 2 with the statistics.

Competing interest

None of the authors has any competing interests with regard to this manuscript.

References

André-Deshays

, Israël

, Charade

, Berthoz

, Popov

and Lipshits

, Gaze control in microgravity. 1. Saccades, pursuit, eye-head coordination, J Vestib Res 3 (1993), 331–343.

Bigelow

R.T.

and Agrawal

Vestibular involvement in cognition: Visuospatial ability, attention, executive function, and memory, J Vestib Res 25 (2015), 73–89.

Brümmer

, Schneider

[...] and Csuhaj

, Coherence between brain cortical function and neurocognitive performance during changed gravity conditions, J Vis Exp 23(51) (2011), pii: 2670. 10.3791/2670.

Clément

and Reschke

M.F.

, Compensatory eye movement Chapter 6 In:

Clement and

M.F.

Reschke , Eds, Neuroscience in Space. Springer NY, 2010, pp. 163–186.

Cohen

, et al., Vestibular experiments in space. In:

Sonnenfeld , Ed.Experimentation with Animal Models in Space. Elsevier. BV, 2005, pp. 105–164.

Dai

, McGarvie

, Kozlovskaya

, Raphan

and Cohen

, Effects of spaceflight on ocular counterrolling and the spatial orientation of the vestibular system, Exp Brain Res 102 (1994), 45–56.

Dai

, Raphan

, Kozlovskaya

and Cohen

, Vestibular adaptation to space in monkeys, Otolaryngol Head Neck Surg 119(1) (1998), 65–77.

De Santo

N.G.

, et al., Anemia and erythropoietin in space flights, Semin Nephrol 25 (2005), 379–387.

Friedl-Werner

, Machado

M.-L.

, Balestra

, Liegard

, Philoxene

, Brauns

and Besnard

, Impaired attentional processing during parabolic flight, Frontiers in Physiology 12 (2021), 675426. 10.3389/fphys.2021.675426.

10.

GenStat for Windows 20th Edition. VSN International, Hemel Hempstead, UK, 2020.

11.

Guitton

and Volle

, Gaze control in humans: Eye-head coordination during orienting movements to targets within and beyond the oculomotor range, J Neurophysiol 58(3) (1987), 427–459.

12.

Kolev

O.I.

and Reschke

M.F.

, Acquisition of predictable vertical visual targets: Eye-head coordination and the triggering effect, J Mot Behav 48 (2016), 552–561.

13.

McLean

D.L.

, Masino

M.A.

, Koh

I.Y.

, Lindquist

W.B.

and Fetcho

J.R.

, Continuous shifts in the active set of spinal interneurons during changes in locomotor speed, Nat Neurosci 11 (2008), 1419–1429.

14.

Kornilova

L.N.

, Grigorova

and Bodo

, Vestibular function and sensory interaction in space flight, J Vestib Res 3 (1993), 219–230.

15.

Kozlovskaya

I.S.

, et al., Microgravity effects on properties of the yaw vestibular-ocular reflex (yVOR) in primates, Cosm Biol i Aviokosm Med 6 (1994), 13–14.

16.

Moore

S.T.

, Cohen

, Raphan

, Berthoz

and Clément

, Spatial orientation of optokinetic nystagmus and ocular pursuit during orbital space flight, Exp Brain Res 160 (2005), 38–59.

17.

Reschke

M.F.

, Kolev

O.I.

and Clément

, Eye-head coordination in 31 space shuttle astronauts during visual target acquisition, Sci Rep 7(1) (2017), 14283. 10.1038/s41598-017-14752-8.

18.

Schneider

, Brümmer

, Carnahan

, Dubrowski

, Askew

C.D.

and Strüder

H.K.

, What happens to the brain in weightlessness? A first approach by EEG tomography, Neuroimage 42(4) (2008), 1316–1323. 10.1016/j.neuroimage.2008.06.010.

19.

Shelhamer

and Clendaniel

R.A.

, Context-specific adaptation of saccade gain, Exp Brain Res 146(4) (2002), 441–450.

20.

Somers

J.T.

, Reschke

M.F.

, Berthoz

and Taylor

L.C.

, Smooth pursuit tracking: Saccade amplitude modulation during exposure to microgravity, Ann N Y Acad Sci 956 (2002), 426–429.

21.

Stahn

A.C.

, Riemer

, Wolbers

, Werner

, Brauns

and Besnard

, Spatial updating depends on gravity, Front Neural Circuits 14 (2020), 20. 10.3389/fncir.2020.00020.

22.

Stevens

S.A.

, Lakin

W.D.

and Penar

P.L.

, Modeling steady-state intracranial pressures in supine, head-down tilt and microgravity conditions, Aviat Space Environ Med (2005), 329–338.

23.

R.D.C. Team, R: A Language and Environment for Statistical Computing. R Core Team, R Foundation for Statistical Computing. Vienna, Austria, 2016.

24.

Thornton

W.E.

, Moore

T.P.

and Pool

S.L.

, Fluid shifts in weightlessness, Aviat Space Environ Med 58(Suppl 9) (1987), A86–A90.

25.

Tomilovskaya

E.S.

, Reschke

M.F.

, Krnavek

J.M.

and Kozlovskaya

, Effect of long-duration space flight on target acquisition, Acta Astronautica 68 (2011), 1454–1461.

26.

Schneider

, Brümmer

, Göbel

, Carnahan

, Dubrowski

and Strüder

H.K.

, Parabolic flight experience is related to increased release of stress hormones, Eur J Appl Physiol 100 (2007), 301–308.

27.

Thornton

W.E.

, Moore

T.P.

, Pool

S.L.

and Vanderploeg

, Clinical characterization and etiology of space motion sickness, Aviat Space Environ Med 58(Suppl 9) (1987), A1–A8.

28.

Uri

J.J.

, Linder

B.J.

, Moore

T.D.

, Pool

S.L.

and Thornton

W.E.

, Saccadic eye movements during space flight. NASA Johnson Space Center, Houston, TX, 1989, TM–100475.

29.

Vasudevan

E.V.

and Bastian

A.J.

, Split-belt treadmill adaptation shows different functional networks for fast and slow human walking, J Neurophysiol 103 (2010), 83–91.

30.

S. Vesterhauge, A. Mansson and T.S. Johansen, Vestibular and oculomotor function during Gz variations. In: AGARD Conference Proceedings No. 372. Motion Sickness: Mechanisms, Prediction, Prevention and Treatment, 24-1. NATO, NTIS, Springfield 1984.

31.

Wollseiffen

, Klein

, Vogt

, Abeln

, Strüder

H.K.

and Stuckenschneider

, et al., Neurocognitive performance is enhanced during short periods of microgravity-Part 2, Physiol Behav 207 (2019), 48–54. 10.1016/j.physbeh.2019.04.021.

32.

Wollseiffen

, Vogt

, Abeln

, Strüder

H.K.

, Askew

C.D.

and Schneider

, Neuro-cognitive performance is enhanced during short periods of microgravity, Physiol Behav 155 (2016), 9–16. 10.1016/j.physbeh.2015.11.036.