INTRODUCTION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

ASTRONAUTS RETURNING FROM spaceflight exhibit a variety of postural control problems. These include deficits while balancing on rails of varying widths (13), increased sway of the body's center of gravity (33, 34), modifications in body segment motion (1), and increased response latencies to external perturbations (17). Preliminary reports indicate that returning astronauts have difficulty assembling the coordination strategies necessary to perform rapid voluntary arm raises efficiently during bipedal stance (20, 21). These deficits are accompanied by decreases in lower limb strength (12), in part stemming from muscular atrophy (22) and hyperactive proprioceptive and neuromuscular reflexes (16, 18, 35). Moreover, returning astronauts experience alterations in vestibular system functioning (36), head movement control (4), and abnormal proprioceptive functioning (38), which also can contribute to postural control deficits.

Previous research examining postural control has primarily centered on various manipulations of sensory input or responses to external perturbations. Few investigations have assessed returning astronauts' ability to perform voluntary limb movements with the constraint that bipedal equilibrium must be maintained (7, 8, 30). The present study quantifies the degree to which human bipedal postural control is modified during voluntary arm movements after extended periods of microgravity (3-6 mo). The arm movement utilized, a rapid unilateral arm raise, has been used extensively as a method to investigate the ability of normal and patient populations to control self-generated postural perturbations. Belen'kii and colleagues (2) were the first investigators to report that trunk and lower limb muscles are activated before the initiation of arm motion. This "anticipatory" postural activity is specific to the particular arm-raise task (e.g., unilateral vs. bilateral, weighted vs. nonweighted) and counters the potentially destabilizing reactive forces arising from upper limb motion (6). A variety of patient populations exhibit postural control problems while performing voluntary arm movements. These difficulties are manifested as inappropriate anticipatory neuromuscular activation strategies, increased motion of the center of pressure (COP), and decreased arm-movement velocity relative to normal subjects (14, 37). Therefore, the rapid arm raise is an ideal task with which to evaluate the ability of returning astronauts to maintain upright bipedal posture while performing a voluntary limb movement. We hypothesized that, during the arm-raise task after extended periods of microgravity, subjects would display diminished postural control quantified by using COP measures (see METHODS). Measures of COP motion as indexes of postural control have often been used to assess differences between normal subjects and patients (9, 23, 25) and between healthy young adults and the elderly (11, 26, 29).

In addition, we were interested in how neuromuscular activation characteristics associated with the arm raise were affected by spaceflight. Therefore, we assessed potential modifications in muscle activation strategies in response to long-duration spaceflight. We were particularly interested in two questions regarding neuromuscular activation: whether, after spaceflight, subjects could produce neuromuscular phasic patterns that were similar to preflight patterns 1) during the movement-initiation phase and 2) after the self-generated perturbation (i.e., after arm acceleration was completed). Previous investigators have detailed changes in proprioceptive functioning and loss of muscle strength, both of which may impact the ability to produce task-appropriate neuromuscular control (22, 38). Thus we hypothesized that the neuromuscular patterns associated with maintaining preflight postural control in response to the reactive forces produced during the arm movement would be more disrupted after flight than those associated with the initiation of the arm movement.

	METHODS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

Subjects. Eight subjects (2 US astronauts, 6 Russian cosmonauts, mean age 43 ± 8 yr) who experienced 3-6 mo of microgravity aboard the Mir space station participated in this study. All were volunteers and had completed the NASA Institutional Review Board for Human Research Informed Consent form.

Protocol. The task comprised 15 right-shoulder flexions performed from a bipedal standing position. Subjects assumed a comfortable stance on a force plate (Kistler Instruments, Amherst, NY) with their arms resting at their sides with the right elbow extended. The self-initiated movements consisted of first closing their eyes and then raising the arm by flexing the shoulder as rapidly as possible until the arm was parallel to the force plate. Throughout the task, subjects were required to maintain their upright bipedal stance (i.e., no stepping or falling). Preflight measures were obtained ~10 days before spaceflight, and postflight measures were obtained, with one exception, 1 day after landing. One crewmember was tested on landing day. All subjects were well-practiced before the preflight data collection. To ensure that subjects adopted the same foot placement before and after spaceflight, during preflight testing the borders of the feet were marked relative to the axes of the force plate. These markings were then used to position the subjects properly during postflight testing.

Data collection and processing. Tangential arm acceleration was measured by using a uniaxial accelerometer (Kistler Instruments) mounted on a wrist splint. Additionally, ground reaction forces from the force plate and surface electromyography (EMG) from the right anterior deltoid, left and right biceps femoris, left paraspinals, right lateral gastrocnemius, and right tibialis anterior were obtained during data collection. These muscles were monitored because they are activated in most subjects in preparation for and/or during the arm-raise task (2, 7, 14, 24). After the skin was cleaned, preamplifier electrodes (Therapeutics Unlimited, Iowa City, IA) were attached to the skin over the muscles using adhesive collars. To prevent motion artifacts, the electrodes were further secured with neoprene wraps or hypoallergenic tape. All data were digitally sampled at 500 Hz. Because of temporal and programmatic constraints, we were unable to obtain kinematic data.

Arm angular acceleration. For each trial, the gravity component of the tangential arm acceleration was removed, and the remaining linear acceleration component was divided by the radius of the arm to provide arm angular acceleration (28). Arm-movement initiation was determined by using the resulting angular acceleration waveform. For each trial, the time of arm-movement initiation was used to synchronize the force plate and EMG data records that were collected on separate computers. The arm-acceleration signal was recorded on both computers, which enabled data synchronization. Arm-movement initiation time was also used to obtain a data window for each trial that consisted of 1 s before and 1.25 s after arm-movement initiation. The 1-s interval before arm-movement initiation was chosen to obtain a quiet EMG and COP baseline before the initiation of anticipatory neuromuscular activity and associated COP motion. The 1.25-s interval after arm-movement initiation encompassed the arm movement itself and the time required for the subjects' COP maximal excursion to be reached and begin to return to its initiation point. This data window was of appropriate length to investigate the features of postural control and the underlying neuromuscular activation during the arm-raise task. With the use of the appropriate zero crossing of the accelerometer waveform, two movement phases were identified: 1) the initiation phase, which is from the beginning of the data record through the end of arm acceleration, and 2) the recovery phase, which is from the beginning of arm deceleration until the end of the data record (Fig. 1). The division of the trial into the initiation and recovery phases enabled us to assess the similarity of the initial phasic activation features used to prepare for and initiate arm movement separately from the activity primarily used to arrest the arm motion and maintain and/or regain bipedal postural control. Peak acceleration values were obtained from the arm-acceleration records of each trial.

View larger version (26K): [in this window] [in a new window]   Fig. 1.   Preflight (top) and postflight (bottom) exemplar mean left paraspinals (LPA) activation waveforms (mean: thick solid trace; +1 SD: dashed trace) and accelerometer records (thin solid trace). The initiation phase consists of data 1 s before the initiation of arm motion through arm acceleration. The recovery phase consists of data from the completion of acceleration until the end of the data record. EMG, electromyography.

COP. For each trial, the COP signals were obtained from commercially available software (Bioware 2.0, Kistler Instruments) and then low-pass filtered with a 10-Hz cutoff (Butterworth, 4th order, 0-phase response). Our operational measures of postural control were anterior-posterior (A-P) and mediolateral (M-L) peak-to-peak motion and COP pathlength. Peak-to-peak COP motion within each trial in the A-P and M-L plane and the COP pathlength within the two identified phases were obtained, and within-subject averages were calculated. As our subjects were healthy and well practiced in the task, we considered our preflight COP measures (A-P and M-L peak-to-peak motion, COP pathlength) as representative of stable postural control. Therefore, we considered subjects experiencing significantly different COP motion during the postflight arm-raise task relative to their preflight measures as demonstrating deficits in bipedal postural control.

Muscle activation. For each muscle of each subject, the EMG signals were first band-pass filtered (20-300 Hz), full-wave rectified, smoothed (10-ms time constant), and averaged. Arm-movement initiations for each of the 15 trials obtained from the accelerometer waveform were used as the synchronization point for signal averaging. Muscle activation latencies (relative to arm-movement initiation) were determined by using an interactive graphics program (EGAA, RC Electronics, Santa Barbara, CA) and visual inspection (Fig. 1). To be considered active, a muscle's voltage had to exceed the baseline voltage by 2 SDs and remain active for at least 30 ms (5). Because the nature of the task dictated that the subjects adopt quiet stance before arm-movement initiation, in all cases muscle activation levels were very low. This made muscle activation onset identification straightforward. To assess the degree of similarity between pre- and postflight muscle activation features, cross-correlation coefficients were calculated for the two phases of the individual subject mean waveforms.

	RESULTS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

One purpose of this report is to provide quantitative information that illustrates how spaceflight differentially impacts individuals in terms of postural control during self-initiated perturbations. Consistent with our laboratory's and others' previous work (4, 16, 19, 31), we have observed that, in holistic tasks requiring sensory-motor integration, spaceflight is associated with a wide range of adaptive postflight behavioral responses. Therefore, we believe it is important that individual subject data be presented whenever appropriate. Thus throughout this report each subjects' pre- and postflight responses are presented. However, to provide a statistical indication of the magnitude of the potential pre- vs. postflight differences of the measures, paired t-tests were applied to the data of each subject.

Arm angular acceleration. Figure 2 displays the pre- and postflight peak arm-acceleration data for each subject. Four subjects significantly decreased (A, C, D, and F), two subjects increased (G and H), and two subjects (B and E) displayed no change in their peak acceleration after spaceflight.

View larger version (21K): [in this window] [in a new window]   Fig. 2.   Individual subject mean (+1 SD) pre- and postflight peak arm angular acceleration. Black bars, preflight performance; gray bars, postflight performance. A-H: subjects A-H. * Statistical significance, pre- vs. postflight, P < 0.05.

COP. Figure 3 displays pre- and postflight peak-to-peak, A-P, COP motion. Peak-to-peak, A-P, COP motion increased significantly in six subjects (B, C, D, F, G, and H), decreased in one subject (A), and was unchanged in the remaining subject (E) after spaceflight. Figure 4 displays pre- and postflight peak-to-peak, M-L, COP motion. Four subjects showed significant increases (B, C, E, and G) after spaceflight, whereas subject A displayed significantly decreased motion. Three subjects' M-L peak-to-peak motion was unchanged by spaceflight (D, F, and H).

View larger version (21K): [in this window] [in a new window]   Fig. 3.   Individual subject mean (+1 SD) pre- and postflight anterior-posterior peak-to-peak center of pressure (COP) motion. Bars are as defined in Fig. 2 legend. * Statistical significance, pre- vs. postflight, P < 0.05.

View larger version (22K): [in this window] [in a new window]   Fig. 4.   Individual subject mean (+1 SD) pre-and postflight mediolateral peak-to-peak COP motion. Bars are as defined in Fig. 2 legend. * Statistical significance, pre- vs. postflight, P < 0.05.

View larger version (21K): [in this window] [in a new window]   Fig. 5.   One example trial showing pre- (A) and postflight (B) COP trace. Increased postflight motion is shown during both the initiation and recovery phases of the arm movement.

View larger version (23K): [in this window] [in a new window]   Fig. 6.   Individual subject mean (+1 SD) pre- and postflight COP pathlength during the initiation phase. Bars are as defined in Fig. 2 legend.

View larger version (20K): [in this window] [in a new window]   Fig. 7.   Individual subject mean (+1 SD) pre- and postflight COP pathlength during the recovery phase. Bars are as defined in Fig. 2 legend. * Statistical significance, pre- vs. postflight, P < 0.05.

Muscle activation. Pre- and postflight muscle activation latencies are tabulated in Table 1. Although there were large individual differences, there was no consistent trend to suggest that spaceflight modifies the time of initial activation of muscles during the task. Spaceflight had minimal effect on the sequence of muscle activation. In general, and consistent with previous reports (2, 14, 24), the postural muscles right biceps femoris and left paraspinals were activated in an anticipatory fashion well in advance of arm-movement onset during both pre- and postflight testing.

	DISCUSSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

The present findings are the first describing the degree to which long-duration spaceflight affects returning astronauts' ability to initiate and control self-generated postural perturbations in the form of voluntary arm movements. The results generally indicate that, although subjects can initiate the necessary neuromuscular activation sequences to perform rapid arm movements, upright postural control during the task is compromised after long-duration flight. The results of this study are consistent with those of other investigators who have reported that astronauts returning from spaceflight display a variety of postural control problems (1, 3, 19, 31, 34). Previous spaceflight-related research has primarily focused on postural control in the context of bipedal stance in response to externally generated perturbations and manipulations of the sensory input (for exceptions, see Refs. 7, 8, 30).

The arm-raise task contains at least two explicit behavioral goals: 1) move the arm as rapidly as possible until it is parallel to the floor, and 2) maintain an upright bipedal posture with the feet remaining in contact with the support surface. These two goals may not be mutually compatible and, therefore, suggest a possible trade off, such that the potential postural perturbation resulting from the arm movement can be reduced or increased by reducing or increasing arm acceleration. This potential trade-off in postural stability for arm acceleration makes the subjects' perception of, and confidence in, their ability to control bipedal stance an important consideration. Astronauts who perceive themselves as having postural control decrements after spaceflight can reduce their arm acceleration relative to preflight levels to ensure that they remain upright. Conversely, returning astronauts with full confidence in their ability may choose to increase arm acceleration at the risk of challenging upright stance. Most interesting, perhaps, is the possibility that astronauts may misperceive the degree of diminished postural control after spaceflight because of modified proprioceptive processing (18). Thus they may still threaten their bipedal stability, despite decreased arm acceleration.

Our measures of A-P and M-L peak-to-peak COP motion and COP pathlength generally reflect deficits in postflight postural control relative to preflight. With the exception of subject A, our subjects generally displayed increases in COP motion. These increases in COP motion were observed despite the fact that the majority of our subjects decreased their peak arm acceleration. The increases in COP motion may be related to the subjects' misperception of their postflight postural control capabilities. We suggest that these subjects correctly perceived that they were experiencing compromised postural control but were unable to perceive the degree to which their control was compromised after spaceflight. This possibility may be reflected in the increased COP motion, despite decreases in arm acceleration.

Two subjects significantly increased their peak arm angular acceleration and displayed significant increases in postflight peak-to-peak A-P COP motion (87% for subject G, 41% for subject H). On the assumption that these subjects had full confidence in their ability and wished to retain their preflight performance levels, these increases may suggest the inability of these subjects to perceive their postflight postural control capabilities correctly.

It is noteworthy that, after spaceflight, only subject A displayed decreases in peak arm acceleration, peak-to-peak COP motion, and pathlength in both movement phases compared with his preflight values. In other words, this subject accompanied his decreased postflight arm acceleration by a generalized depression of the associated COP motion. This pattern of decreased motion may suggest that this subject was able to accurately perceive that his postural control was compromised after spaceflight. Therefore, he utilized a strategy that enabled him to complete the task while maintaining postural stability. This is in contrast to the remaining subjects who, for most measures, showed a significant increase in COP motion.

The suggestion that subjects may experience adaptive postflight proprioceptive problems leading to misperception of postural control capabilities is reasonable. Both Watt et al. (38) and Kozlovskaya et al. (18) reported that returning astronauts display disordered proprioception that results in inaccurate perceptions of the interaction between themselves and the environment. Additionally, anecdotal evidence indicates that many astronauts experience sensations of "heaviness" and/or illusions of "sinking" into the floor while standing (C. S. Layne, personal observation). Such sensations would be expected to influence our subjects' perceptions of their postural control capabilities. This disruption in perceptual abilities and associated neuromuscular control may be related to a combination of several physiological changes associated with spaceflight. Changes in postflight ankle proprioceptive functioning could result in greater ankle sway before adequate detection and/or interpretation by the proprioceptive system. Altered functioning of the vestibular system could also result in deficits in sway detection after spaceflight (3, 33, 34). It is also possible that spaceflight affects muscle spindle sensitivity in such a way that the interaction between central motor commands and peripheral feedback is altered. Thus, although the command for movement is initiated properly after spaceflight, as evidenced by the generally high correlations between the pre- and postflight waveforms in the initiation phase, the ability to sustain or generate additional bursts of muscle activity is impaired. Loss of muscle strength, particularly in the ankle and trunk musculature, may also play a role in our subjects' inability to prevent increases in postflight COP motion. The antigravity musculature, including the trunk muscles, tends to show a preferential loss of strength after spaceflight (12, 22), which may also have influenced the ability to generate the subtle neuromuscular features necessary for optimal control.

The loss of optimal neuromuscular control after spaceflight would negatively impact the kinematic strategies used to produce the arm movement and associated postural control. Although cross-correlation analysis generally revealed that the neural activation patterns needed for the preparation and initiation of the arm movement remained similar during testing 1 day after spaceflight, we observed increases in COP motion during the initiation phase. These seemingly paradoxical findings can be explained as follows. Despite the fact that the shape of pre- and postflight EMG waveforms was quite similar during the initiation phase of the movement, the timing of the activation pattern relative to arm-movement initiation was generally altered by spaceflight. Ninety-seven percent of the lower limb and trunk muscle comparisons during the initiation phase indicated that the postflight waveforms either lagged or led the preflight waveforms at the point of maximum correlation. Thus the postflight temporal relationships associated with muscle force generation relative to arm-movement initiation were different than those observed preflight. Moreover, the magnitudes of the muscle force associated with the altered postflight neuromuscular activation features were unlikely to be the same as those of preflight, particularly because loss of muscle strength typically accompanies extended stays in weightlessness. Additionally, we only obtained EMG from a limited number of muscles. Other musculature undoubtedly contributed to the control of the bipedal arm-raise task. The force-generating capabilities of these muscles could also be expected to be impacted by exposure to long-duration spaceflight. Thus precise force magnitudes and the optimal timing of when forces are being produced with respect to arm-movement initiation may have been significantly altered as a result of spaceflight. These disruptions could lead to the diminishment of postural control reflected in the observed increases in COP motion during the initiation phase.

The cross-correlation analyses of the lower limb and trunk EMG waveforms during the recovery phase revealed that 87.5% of the comparisons indicated either a lag or lead in the postflight waveform at the point of maximum correlation relative to preflight. Additionally, 80% of the lower limb and trunk muscle cross-correlation coefficients during the recovery phase were significantly different (r  0.71), indicating that the phasic features of postflight neuromuscular activation generally did not conform with those observed preflight. These findings further suggest a consequential loss of neuromotor control after spaceflight that is reflected in the increases in postflight COP motion observed during the recovery phase.

The finding that the vast majority of initial muscle activation patterns during the initiation phase of the movement was not different pre- vs. postflight is somewhat inconsistent with the report of Massion and colleagues (30). These authors reported that, during backward trunk bending, the early activation of the soleus observed preflight was replaced by early tibialis anterior activation during their first postflight session. They attributed this change in neuromuscular patterning to a vestige of the neuromuscular activation sequence used during in-flight trunk bending. The normal sequence of activation was restored by the second postflight data collection session (8 days after landing). However, in general, our subjects did display the same initial phasic muscle activation characteristics pre- and postflight. These patterns were quite similar to the patterns our subjects used during rapid in-flight arm movements performed when they were restrained to the support surface of the Mir space station (Layne, unpublished observations). Thus the neuromuscular synergies observed preflight were also appropriate to accomplish the in-flight arm movement; thus it is not particularly surprising that we found the "shapes" of the pre- and postflight activation waveforms during the initial phase of movement to be similar. However, the fact that 97% of the postflight EMG waveforms obtained during the initiation phase either led or lagged the preflight waveforms is consistent with the findings of Massion et al. of disrupted postflight neuromuscular activation.

Because of programmatic constraints, data were collected for seven of the subjects 1 day after landing. Undoubtedly the diminished postural control and modified neuromuscular activation characteristics exhibited by our subjects would have been exacerbated had we had the opportunity to test them on landing day. One of the subjects, who was scheduled for testing on landing day, was unable to perform the task despite a strong desire to do so. This finding is consistent with previous reports indicating that bipedal postural control recovers rapidly toward preflight performance after spaceflight, especially in the first hours after landing, but recovery is not complete for several days after landing. In particular, Paloski and colleagues (34) calculated that subjects recover 50% of the postflight equilibrium deficits experienced at the time of landing within 2.7 h after short-duration spaceflight.

To summarize, the present results indicate that astronauts returning from long-duration spaceflight are able to initiate rapid voluntary arm movements without difficulty. However, these movements are accompanied by decreases in bipedal postural control as assessed by measures of COP motion. This is consistent with previous reports that postflight postural control is compromised in response to external perturbations and/or during tests of static postural control in altered sensory environments (3, 18, 34). Additionally, there were often significant modifications in neuromuscular activation that may have contributed to the compromised postural control exhibited by our subjects. These modifications in neuromuscular activation may have resulted from central and peripheral physiological changes associated with spaceflight. Our subjects' behavior may also suggest that returning crewmembers' ability to perceive the full functional capabilities of their postural control systems may also be compromised, particularly after long-duration spaceflight. Our findings contribute to a growing body of evidence defining the precise nature of task-specific sensory-motor integration deficits experienced by crewmembers returning from spaceflight (4, 7, 18, 19, 30, 31, 34). Although we chose to investigate a task that included a well-documented anticipatory postural component associated with vigorous arm motion, all movements necessarily involve a postural component. Therefore, the finding that the postural control associated with voluntary limb motion is compromised after flight is important. Understanding the underlying adaptive processes is an important step toward mitigating the postflight postural control problems experienced by returning astronauts.