The Effects of Prolonged Exposure to Weightlessness on Postural Equilibrium

JERRY L. HOMICK, MILLARD F. RESCHKE, AND EARL F. MILLER II

In his normal gravitational environment man has four sources of sensory information which can be used to maintain postural equilibrium: vision, vestibular inputs, kinesthesia, and touch. Of these senses the superiority of vision as a basis of postural stability has been demonstrated by a number of investigators (refs. 1,2,3,4,5, 6,7,8). Even when other systems are nonoperative, vision can be employed to maintain upright posture. On the other hand, provided that the mechanoreceptors are intact, vision is not essential as evidenced by the observation that blind people have little difficulty in maintaining postural equilibrium (ref. 3).

There is also little doubt that functional disturbances in the vestibular, kinesthetic, and tactile sensory modalities can affect postural stability. People who have experienced unilateral labyrinthine or cerebellar damage will often fall to the side of the lesion (ref. 9). Patients with bilateral labyrinthine disturbances, on the other hand, frequently appear to exhibit little disability in maintaining a steady posture when standing with feet together and eyes closed in the Romberg position (ref. 10). When the testing procedure is improved, however, and a sharpened Romberg is employed (ref. 11), bilateral labyrinthine defects as well as other less dramatic vestibular disturbances do result in postural difficulties that are evident when the eyes are closed (ref. 12). These observations suggest that, in a closed loop system, the sensory basis of postural stability must include inputs from kinesthetic, pressure, and touch receptors, as well as visual and vestibular inputs (refs. 13, 14).

That exposure to the dramatically altered environment encountered during weightless space flight may affect postural stability has been under investigation by our laboratories beginning with the Apollo 16 mission. Although complete data are not available from Apollo 17, preflight and post-flight testing of the Apollo 16 crewmen indicated some decrement in postural equilibrium 3 days following recovery when the crewmen were tested with their eyes closed (ref. 15). Using a measurement procedure referred to as stabilography, investigators in the Soviet Union have reported that the crewmen of the 18-day Soyuz 9 mission manifested difficulty in maintaining a stable vertical posture which did not normalize until 10 days after the flight. The greatest disturbances were measured during an eyes closed test condition (ref. 16).

On the basis of these observations it was hypothesized that, with prolonged exposure to a weightless environment, those sensory systems, with the possible exception of vision, necessary for the maintenance of postural stability, will undergo some changes. Further, these changes are most likely originally peripheral, and involve the modification of inputs from the receptors serving kinesthesia, touch, pressure, and otolith function. As exposure is prolonged, habituation responses occur at a central level in the nervous system which constitute learning in a new environment. When the environment is again changed from weightlessness to one-g reference, ataxia and postural instability will be manifested as the result of the neural reorganization that has occurred in weightlessness.The specific objective of this investigation was to assess the postural equilibrium of the Skylab astronauts following their return to a one-g environment and to suggest possible mechanisms involved in any measured changes.

Method

Postural equilibrium was tested by a modified and shortened version of a standard laboratory method developed by Graybiel and Fregly (ref. 11). Metal rails of four widths, 1.90, 3.17, 4.45, and 5.72 centimeters (0.75, 1.25, 1.75, and 2.25 inches), provided the foot support for the crew-man during the preflight and postflight tests. In addition, rail widths of 1.27 and 2.54 centimeters (0.5 and 1.0 inches) were available for preflight testing only. A tape approximately 10.16 centimeters (4.0 inches) wide and 68.5 centimeters (27.0 inches) long served as a foot-guide alignment when the crewman was required to stand on the floor. Each crewman was fitted with military-type shoes for this test, both preflight and postflight to rule out differences in footwear as a variable in intra-subject and intersubject comparisons.

The test rails and required body posture are illustrated in figure 12-1. Time, which was the performance measure of balance, began when the crewman, while standing on the prescribed sup-port with his feet in a tandem heel-to-toe arrangement, folded his arms. His eyes remained open in the first test series. In the second series the time measurement was initiated after the crewman attained a balanced position and closed his eyes. During initial preflight testing several practice trials were allowed on representative rails until the crewman demonstrated full knowledge of the test procedure and reasonable confidence in his approach to this balancing task.

During a test session the initial rail width for testing with eyes open was typically 3.17 centimeters (1.25 inches). Three test trials with a maximum required duration of 50 seconds each were given. If the time limit was reached in the first two trials, a third was not performed, and a perfect score of 100 seconds was recorded for the initial support width. If the crewman failed to obtain a perfect score, the two largest time values for the three trials were summed to obtain the final score. The choice of the second rail width depended upon the crewman’s performance on the initial support width. If his score was greater than or equal to 80 seconds, the next smaller sup-port width was used; if his score was less than 80 seconds, the next larger support width was used. Testing on a third rail size was required when both of the two previous support width scores fell either above or below the 80-second performance level. Testing with eyes closed followed the same procedure except that a larger rail support, 5.72 centimeters (2.25 inches) was typically used initially. Eyes closed testing always followed testing with eyes open. The time required to perform the entire test was approximately 18 minutes. All tests were conducted with normal laboratory illumination.

Three preflight baseline tests were performed on each of the Skylab 2, 3, and 4 crewmen approximately 6 months prior to their space flights. These postural equilibrium tests were part of a comprehensive battery of vestibular tests completed by each of the crewmen at the Naval Aerospace Medical Research Laboratory.

Tests following the 28-day Skylab 2 mission were limited to balancing with eyes open and eyes closed while standing on the floor only. These tests were conducted during the first and second day following splashdown. Postflight tests on the Sky-lab 3 Scientist Pilot and Pilot were conducted on the 2^nd, 9^th, and 29^th day following termination of their 59-day mission. The Skylab 3 Commander was excluded from postflight testing because of an acute back muscle strain acquired on the first day postflight which might have been aggravated by the test procedure and which, in any event, would have affected his performance on the rails. Postflight tests on each of the Skylab 4 crewmen were conducted on the second, the 4^th, the 11^th, and the 31^st day postflight. The Skylab 4 flight was 84 days in duration. With both of the latter two crews the tests on the second day following splashdown were conducted onboard the recovery ship which was tied to a dock and, therefore, provided a stable platform. All subsequent postflight tests were conducted at the Johnson Space Center.

Results

Postural Equilibrium Tests.—Preflight data obtained on these crewmen indicated that they were all well within the range of postural equilibrium performance typically exhibited by young, healthy aviator-type subjects.

The limited postflight data collected on the Skylab 2 crewmen indicated that they all experienced considerable difficulty with standing on the floor during the eyes closed test condition. They had no trouble, however, in meeting the performance criterion when permitted the use of visual cues. In considering the significance of these data, it must be remembered that the tests were performed on a moving ship.

Data obtained preflight and postflight on the Skylab 3 Scientist Pilot and Pilot and the Skylab 4 Commander, Scientist Pilot, and Pilot are presented in figures 12-2 to 12-6, respectively. In these figures eyes open and eyes closed postural equilibrium performance on each of the rail sizes used, plus the floor, is plotted as a function of test day. The baseline data point shown against which the postflight data are compared is the mean of the preflight data for that condition. The standard error of the mean was selected as a descriptor of the variance observed in the baseline data and is represented by dashed lines. Approximately 50 percent of those cases where no variance is indicated are the result of having only a single data point on the rail size in question; otherwise, the standard error of the mean is less than one.

Visual inspection of figures 12-2 and 12-3 indicates that the Skylab 3 Scientist Pilot and Pilot showed a decrease of approximately the same magnitude in eyes open postural equilibrium performance when tested on the second day after splashdown. However, a more pronounced decrement in ability to maintain an upright posture was observed in the eyes closed test condition. This change was more evident in the Pilot and is clearly demonstrated by the 5.72 centimeter (2.25 inches) rail size data seen in figure 12-3. Indeed, without the aid of vision on the second day after recovery, the Pilot experienced considerable difficulty even when attempting to stand on the floor, a condition he was never confronted with preflight because of his excellent balance on the 4.45 centimeter (1.75 inches) and 5.72 centimeter (2.25 inches) rail sizes. Complete recovery to preflight levels of performance did occur in both the eyes open and eyes closed conditions for both of these crewmen. However, the rate of recovery for the Pilot was apparently slower as evidenced by his relatively poor score on the 5.72 centimeter (2.25 inches) rail on the ninth day after recovery.

In contrast to the Skylab 3 crewmen, the Skylab 4 Commander and Pilot demonstrated no decrease in their postflight eyes open postural equilibrium as measured by this procedure (figure 12-4 and figure 12-5). They did, however, show a very large deficit in ability to balance with eyes closed. In the case of the Commander, this postflight change is clearly indicated on the first day after recovery with the 5.72 centimeter 2.25 inches) wide rail. Also, it can be seen that on the first day after recovery he was almost unable to maintain the required vertical posture while standing on the floor with his eyes closed. Improvement was evident on the 4^th day after recovery, and the data obtained on the 11^th day indicates that both of these crewmen had regained their preflight level of ability on the eyes closed portion of this task.

Data obtained on the Skylab 4 Scientist Pilot are presented in figure 12-6. It can be seen that, like the Skylab 3 crewmen, the Skylab 4 Scientist Pilot experienced a postflight decrease in ability to maintain postural equilibrium in both the eyes open and eyes closed test conditions. The magnitude of change was much greater without vision. On the 4^th day after recovery this change was still very evident, but by the 11^th day this crewman’s ability to balance on the test rails had returned to baseline proficiency.

Subjective Reports and Observations.—The postflight decrease in postural stability demonstrated by the rail tests are supported by observations of and subjective reports by the crewmen.

Although all of the Skylab crewmen were able to walk with minimal or no assistance immediately after exiting the Command Module, they did so with noticeable difficulty. During this initial post-flight period on the recovery ship, they tended to use a wide-stanced shuffling gait with the upper torso bent slightly forward. With each passing hour back in the one-g environment, they gained confidence and proficiency in their ability to walk about unaided. By the end of the first recovery day all of the crewmen showed considerably improved ambulatory performance and by the time they were ready to disembark the recovery ship on the second day after recovery, they manifested few noticeable signs of ataxia or postural instability.

During the first several days following splashdown, and especially on the first recovery day, all of the crewmen reported that the simple act of walking required a conscious effort. The Skylab 3 Commander, for example, reported that, when he stepped forward, he had a feeling that he was moving sideways. Also, nearly all of the crewmen reported that they had to be especially careful when walking around corners because they had a tendency to fall to the outside. This problem was described by a few of the crewmen as a sensation of forced lateral movement.

Related to these subtle disturbances in postural stability was the report by all of the crewmen that rapid head movements produced a sensation of mild vertigo. This sensation could be effectively controlled by holding the head steady. Several of the crewmen, including the Skylab 4 Commander and Pilot, indicated a particular need to hold their head steady while attempting to balance on the test rails. Any slight head movement, especially during the eyes closed test condition, would induce the vertigo sensation and cause them to lose balance. The movement-induced vertigo diminished gradually and in most cases was gone within 3 to 4 days following splashdown; however, the Skylab 4 Pilot reported that he occasionally experienced mild vertigo with rapid head turns as late as 11 days after recovery. It is also of interest to note that on the second and fourth days after recovery, the Skylab 4 Pilot reported experiencing a "wide dead-band" when attempting to balance on the test rails with his eyes closed. In other words, he was unable to accurately sense small displacements of his head and body.

Because the postflight test intervals were infrequent and not at the same times for each crew, the time course to complete recovery cannot be clearly specified. However, on the basis of observations and data obtained, it appears that the Skylab crewmen required up to 10 days to regain their normal postural stability. These results are in close agreement with the Soyuz-9 postflight postural stability findings reported from the Soviet Union.

Discussion

The results from the present study provide evidence that postural stability can be affected by prolonged periods of exposure to weightlessness. Support for the hypothesis that central neural reorganization occurs in response to environmental change is obtained when the postflight decrease in stability on the rails and the time course for recovery is compared with preflight performance.

That adaptive changes may occur and contribute to disturbances of equilibrium following exposure to a weightless environment is reasonable from a physiological point of view. As one basis of postural stability, vision can expect to undergo little change. However, the vestibular apparatus (particularly otolith input), kinesthesia, and touch will be those sensory systems most affected by exposure to zero-g.

Subgravity levels can be experienced in parabolic flight, free fall, and short jumps. Water immersion and sensory deprivation procedures minimize stimulation of kinesthetic and touch receptor systems without lifting the gravitational load on the otolith receptors. It is only in space flight that prolonged periods of weightlessness can be achieved. During these periods, kinesthetic and touch stimulation is reduced and otolith input is considerably modified. Static otolith output cannot in this latter situation provide information for spatial orientation (spacecraft vertical) nor can kinesthesia or touch provide reliable sensations unless the crewman is in contact with a rigid surface to provide some reference point.

That these sensory systems can habituate to the weightless environment is suggested by the increased ability with time for the crewmen to maneuver with decreasing difficulty. In this regard physiological evidence has been obtained that suggests adaptation toward the norm in the frog’s otolith system following 4 to 5 days exposure to weightlessness (ref. 17). It is also possible that habituation in weightlessness of the sensory system, basic for postural stability, is similar to the changes experienced in other unusual force environments such as prolonged exposure to slowly rotating rooms and movements encountered on ships.

If this is the case, then several mechanisms could be proposed to account for the changes occurring as a result of exposure to weightlessness. First, a central nervous system "pattern center" concept (ref. 18) could be postulated to help understand the possible mechanism encountered in the habituation process. For example, following insertion into orbit the crewmen may experience difficulty in maneuvering and find orientation to be a problem. After 4 to 5 days, movement from one area of the vehicle to another would become somewhat easier. Fine motor control to determine displacement would be established. Adaptation in the postural mechanicomotor system would have occurred.

On the basis of the postulated pattern center, the radical environmental change encountered in transitioning from one-g to zero-g would result in vastly different outputs from the otolith, kinesthetic, and touch receptors. These altered outputs would then be sent to their corresponding centers and these in turn relayed to the pattern center, where a copy of the appropriate movement was stored progressively over time. Once an adequate memory of the pattern is built up, the pat-tern center would take over movement and automatic balance control. Further, under control of peripheral inputs from the otolith, kinesthetic, and touch receptors relaying the actual movement, the center would permit anticipation of the coming movement. Return to a one-g environment would result in a recurrence of difficulty, both in locomotion and postural equilibrium. Habituation to a gravity reference would begin almost immediately and a new effective pattern in the pattern center would be established possibly in a time proportional to the previous duration of weightless exposure.

A second mechanism could possibly be responsible for the changes noted in postural stability. Biostereometric analysis of body form indicated that the crewmen experienced a measurable postflight reduction in body tissue volume, part of which was muscle tissue (ch. 22). A significant percentage of the total volume loss noted was in the thighs and calves. A postflight decrease in leg strength was also measured (ch. 21). In the case of the Skylab 3 crew the average leg strength loss was approximately 20 percent. As the present task required standing on the rails in a sharpened Romberg position, it is possible that the crewmen were physically incapable of completing the task due to disuse atrophy of the major weight bearing muscles.

A third alternative is also possible. Both a hyper Achilles tendon reflex and an increased gastrocnemis muscle potential were observed postflight in the Skylab 3 and Skylab 4 crewmen (ch. 15). This hyperactivity could have resulted in overreaction and overcompensation on the part of the crewman, thus making rail performance difficult.

The fourth mechanism that could be responsible for the degradation of postural stability observed postflight in the Skylab crewmen is one which would include as contributing factors all of the possibilities mentioned. Once the pattern center serving the postural, mechanomotor system has been established in weightlessness and must begin habituation to a one-g reference, increased reflex sensitivity may be only a single aspect of the process.

A second aspect may be that the loss of tissue volume would contribute to a reduction in mechan-ical damping of leg movements. For example, if we look at the pattern center serving the postural, mechanomotor system as one in which control depends on negative feedback (as the muscle spindle control system does), then it is possible for instability to occur both in locomotion and postural equilibrium. The instability results because the error signal takes time to generate a corrective response. This means that, if no compensation for the error is programmed, the corrective signal would arrive at such a time that the leg, in this case, has already moved on to a new position. A second correction would be necessary which would also result in overshooting. To stop this oscillation around the desired point, the limb movement must be damped. Pure mechanical damping is provided by the in-series elastic elements in the muscles as well as the viscosity of muscle tissue and joints (ref. 19). More tissue in the leg adds increased mechanical damping while less tissue would tend to permit underdamped movements.

An alternate way of viewing damping is to suggest that the reflex control system depends on an output determining both position error and the rate-of-change of muscle length. When the system has rate-of-change information available, anticipation of the new limb position is predictable and a corrective signal can be initiated to begin corrective adjustment (ref. 20). The hyperreflex activity observed could be a compensatory reaction generated in the mechanism responsible for programing the position center as a result of modified otolith input and a mechanically under-damped system.

Our results tend to support this fourth hypothesized mechanism. Decreased postural stability was observed in all crewmen when tested post-flight. Although the larger deficits were obtained when visual cues were not available, there were greater changes in postflight equilibrium in the Skylab 3 crew with vision than there were in the Skylab 4 crew. Correspondingly, the Skylab 3 crew did not exercise to the same degree in-flight as the Skylab 4 crew and, as a result, exhibited a greater loss in leg muscle strength and muscle tissue. This suggests that vision compensated less with increasing muscle mass loss.

These overall findings argue for an environment dependent memory store (pattern center) of frequently repeated sensory inputs that is under the guidance of a combined otolith, kinesthetic, and touch system which registers the actual movement and allows for anticipation and compensation of each movement as it occurs. Being environmentally dependent, such a mechanism could account for the buildup of postural responses (such as hyperreflex activity) in zero-g that would be inappropriate upon return to a one-g reference. A mechanism of this type could be applied to account for sensory physiological habituation in a variety of situations. In particular, such a mechanism could provide an adequate basis for change when the acquired response patterns are no longer congruent with the environment.

References

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