INTRODUCTION

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SINCE THE BEGINNING of the spaceflight era, weightlessness was shown to lead to substantial changes in muscle function (for a review, see Ref. 11). These changes, globally defined as deconditioning, consist mainly of loss of muscle mass and force, increased muscle fatigability, and abnormal reflex patterns (17, 19, 21, 27). They are likely due to an imbalance between muscle protein synthesis and catabolism, brought about by the absence of the constant pull of gravity, particularly in weight-bearing muscles, and similar to that observed during immobilization of fractured limbs or during prolonged bed rest without exercise (13, 23, 28, 31, 32). Animal studies have also shown significant changes in rat muscle, as a consequence of 12.5-22 days of spaceflight. These changes consisted of reduction of mass and diameter of slow-twitch fibers and decrease in muscle force, as well as molecular rearrangements of myosin heavy chains occurring already within the first week of spaceflight (5, 6, 12, 24, 26).

In humans, muscle force and velocity were studied by using a Cybex dynamometer before and after the Skylab missions (2, 3, and 4 of 28, 59, and 84 days, respectively) during which the crews performed minimal to vigorous physical exercise to prevent muscular decay. Nevertheless, the leg extensor force was reduced by 25% after the 28-day Skylab-2 mission (35) and by 6.5% after the 84-day Skylab-4 mission (19). Isokinetic (eccentric and concentric) force was also measured before and after 5-11 days of spaceflight in 19 subjects. At reentry, concentric muscle force of the quadriceps, trunk flexors, and trunk extensors had decreased significantly (13, 10, and 23%, respectively) compared with preflight values (19). However, isovelocity muscle contractions never, or only seldom, occur in everyday life. We therefore set out to compare the effects of microgravity on maximal muscular power of the lower limbs of astronauts and cosmonauts during short efforts, in which either the velocity was imposed by the experimenters or both variables (force and velocity) were dependent on the subjects' muscle action. The experiments were performed before and after the two missions, Euromir '94 and '95, jointly organized by the European and Russian space agencies.

	MATERIALS AND METHODS

The procedures reported in the literature to determine the maximal power during very short all-out efforts in humans can be subdivided into two broad groups: 1) "instantaneous" methods, in which the power is assessed during a single, very short (<1-s) contraction of the extensor muscles of the lower limbs, such as a standing high jump off both feet; and 2) "average" methods, in which the power is determined on a longer time basis (5-7 s) over an even number of contractions of the muscles of one limb at a time, such as pedaling maximally or running upstairs (for reviews, see Refs. 7 and 13a). In this study we determined the maximal power according to both procedures by means of a newly developed instrument, the multipurpose ergometer dynamometer [MED (3, 37)], the technical characteristics of which are summarized below (see MED).

Subjects. Four male subjects (S1-S4), whose characteristics are reported in Table 1, were studied before and after spaceflights of 31- to 180-day duration. An additional subject (S5) has been studied only after reentry from the longest mission in manned spaceflight history so far (438 days).

View this table: [in this window] [in a new window]   Table 1.   Anthropometric characteristics of subjects, preflight O2 max, and flight duration

The MED. The MED (Fig. 1) consists of two rectangular (3 × 0.9-m) metal frames hinged at one end. Two precision rails are fixed to the upper frame, which can be inclined by means of a hydraulic jack up to an angle of 30° with respect to the lower one. A seat is fixed on a carriage that is free to move by means of four ball bearings on the rails. An isokinetic cycloergometer, powered by a 4-kW electric motor, is fixed to the hinged end of the MED, between the rails. The electric motor is controlled by an inverter so that the pedaling frequency can be varied from 0.5 to 4 Hz. The power of the motor is large enough to avoid being overridden by the subject, even during an instantaneous all-out effort. A strain-gauge system (SRM Powermeter and Powercontrol II), mounted on the chain ring, yields continuous measurements of the force exerted by the subject on the pedals. The mechanical power, as given by the product of the torque times the angular velocity, is calculated on a 10-ms basis and displayed to the subject on the front panel for visual feedback control. When the MED is used as a cycloergometer, the carriage seat is fixed in a given position by means of adjustable electromagnetic blocks.

View larger version (23K): [in this window] [in a new window]   Fig. 1.   Schematic view of multipurpose ergometer dynamometer (MED) configured to assess maximal explosive power (MEP). Subject sitting on carriage seat (C-S) pushes with both feet on force platforms (FP). Velocity (V) of consequent backward movement of C-S is determined by means of a wire tachometer (WT). Force (F) exerted by subject is measured by 2 load cells indwelling into FP. Instantaneous power () is calculated as  = F · V. Hinges (Hi) allowing tilting up of MED's mobile frame, by action of hydraulic jack (HJ), and isokinetic cycloergometer (Cy), are also indicated. When MED is used as an isokinetic cycloergometer, mobile frame is positioned horizontally, and FP are tilted upward. See text for details.

(1)

Experimental protocol. The maximal power of the lower limbs was assessed after both an instantaneous and an average method as defined by Capelli and di Prampero (7). The instantaneous procedure consisted of a series of six maximal pushes with both feet on the force platforms, with a resting interval of 2 min between pushes. To optimize the force developed by the quadriceps femoris, the maximal pushes were performed from a knee angle of 110° (22, 25). The requested knee angle was obtained by adjusting the position of the mechanical blocks, which also prevented the motion of the carriage seat toward the platforms, thus impeding any countermovement and, consequently, recovery of elastic energy (37). The subjects sat on the carriage seat of the MED with arms on the handlebar and soles of the feet leaning against the platforms. The platforms were positioned perpendicularly to the rails, and the main frame was inclined 20° with respect to the horizontal position (see Fig. 1). The time course of force, velocity, and power (as calculated from Eq. 1) during a maximal instantaneous push is reported in Fig. 2. Analysis of the time course of allowed us to assess its peak (_peak, kW) and mean (_mean, kW) values. In turn, _mean was determined as

(2)

where t is the duration of the work phase. Throughout this report, the power assessed by means of this procedure will be defined "maximal explosive power" (MEP).

View larger version (15K): [in this window] [in a new window]   Fig. 2.   Time course of F (kN), V (m/s), and (kW) during actual determination of MEP. Instantaneous power was obtained multiplying force signal by speed ( = F · V). Arrows, duration of work phase (t).

View larger version (31K): [in this window] [in a new window]   Fig. 3.   F (N) exerted on pedals of isokinetic cycloergometer during all-out effort of 5 s plotted as a function of time. Pedal frequency was 1 Hz, so 2 consecutive peaks result from action of right and left limb, or vice versa. Maximal cycling power (MCP) was calculated from average of 3 indicated cycles (1, 2, and 3).

Statistical procedures. The differences between the parameters observed in the different postflight baseline data collections were investigated by using an ANOVA. A post hoc Bonferroni test (Systat 5.2.1 for Macintosh) was then applied to determine the significance of the differences between the average values obtained pre- vs. postflight from repeated measures of any given parameter. The differences were considered significant for P < 0.05.

	RESULTS

The average values (±1 SD) of _peak and _mean for both MEP and MCP are reported in Table 2 in percentage of preflight values, together with the subjects' body masses. In Table 2, the absolute preflight values of _peak and _mean are reported in brackets for preflight conditions only.

In S1, the preflight baselines of MEP and MCP were calculated by averaging the values obtained in all experimental sessions. For S2, however, the data obtained at L  48 were not considered because of his suboptimal physical status. In the case of S3 and S4, we observed a learning or training effect between L  75 and L  15, on the order of 10% for both MEP and MCP for S3 and of 5 and 30% for MEP and MCP for S4, respectively. Therefore, in these subjects, the preflight baseline values retained for comparison were those recorded at L  15.

S5 was not investigated before flight; in this case, therefore, preflight MEP, when expressed per kilogram of body mass, was assumed to be equal to the average observed preflight in the other subjects. MCP was not assessed in this subject.

Before flight _peak ranged from 3.74 to 2.88 kW for MEP and from 1.33 to 1.05 kW for MCP, whereas _mean ranged from 1.70 to 1.41 kW for MEP and from 0.79 to 0.59 kW for MCP. Table 2 shows that _peak and _mean for both MEP and MCP were substantially reduced, approximately by the same amount, after reentry.

Indeed, at R+2 (R+3) expressed as a percentage of preflight values, MEP amounted to ~68% in S1 (31 days in microgravity) and to ~50% in the three subjects who spent 169-180 days in microgravity (S2, S3, and S4). Furthermore in subject S5, who remained in space for 438 days, MEP did not seem to fall below ~50% of the preflight value. It should be remembered, however, that preflight MEP was not determined in S5: it was assumed to be equal (per kg body mass) to that observed on the other subjects.

After flight, MCP was reduced to a lesser extent than was MEP (see Table 2). In addition, the effects of the flight duration seemed to be less pronounced for MCP than for MEP. Indeed, MCP at R+2 (R+3) (average of _peak and _mean) amounted to ~81% of preflight after 31 days in microgravity (S1) and to ~70% after 169-180 days (S2, S3, and S4).

The recovery of MCP after flight seemed to be rather fast. Indeed, with the possible exception of S4, it was essentially complete within 2 wk (Table 2). At variance with MCP, the recovery of MEP seemed to follow a slower time course and, as a first approximation, could be described by a monoexponential function (Fig. 4)

(3)

where y(d) is _mean (W/kg) at day d, A and A_R+2 are the corresponding individual values assessed preflight or after reentry at R+2 (or R+3), and B is a time constant in days.

View larger version (14K): [in this window] [in a new window]   Fig. 4.   Recovery of MEP mean (mean; W/kg) after reentry in 1 subject (S3). Continuous curve is described by y(d) = AR+2 +(A  AR+2) · (1  ed/B; see text for details and Table 3 for actual values of coefficients of equation). , Means; bars, SD; dashed line, asymptotic value of mean (assumed to be equal to preflight value).

By using an iterative statistical package (Systat 5.2.1), Eq. 3 was solved for each subject. A and B, together with the determination coefficient (r²) and the number of points (n) of each individual regression, are reported in Table 3. Because the asymptote of an exponential is reached after about five time constants, the time (days) for complete recovery (R) was calculated as R = 5 · B and tends to be longer, the longer the duration of the preceding flight.

The instantaneous procedure yielding MEP allowed us to determine several other variables of physiological interest, such as peak force (F_peak; kN), peak velocity (V_peak; m/s); maximal acceleration during the backward movement [(dV/dt)_max; m * s²], and duration of the positive work phase (t; s). These values are reported below in some detail. For simplicity, only nonsignificant differences are indicated by NS.

Force. The preflight F_peak ranged from 1.74 to 2.06 kN. It decreased by 11.7% after 31 days (S1 at R+2), 26.2% after 169 days (S2 at R+3), and 31.5 and 27.0% after 180 days of spaceflight (S3 and S4 at R+2, respectively). The recovery of F_peak after reentry was faster for S1, who at R+6 and at R+11 had attained values of only ~5% (NS) to 10% lower than preflight. On the contrary, in the three subjects who spent 169-180 days in microgravity, F_peak was still 15-24% lower than preflight at R+11 and R+12, and, in subjects S3 and S4, 12-22% lower at R+26.

Speed. V_peak attained during the push phase ranged from 2.76 to 2.29 m/s. It was substantially reduced in all subjects after reentry: 24.2% after 31 days (S1 at R+2) and 27.8 to 35.8% after 169-180 days (S2, S3, and S4 at R+2 or R+3). As was the case for F_peak, the recovery of V_peak was faster in S1, who had attained the preflight value (actually 98.6%, NS) at R+11, than in the three other subjects. Indeed, S2 recovered only to 13.4% at R+12, whereas S3 and S4 were still below the preflight values (5.7 and 24.0%, respectively) at R+26.

2

2

	DISCUSSION

Maximal muscle power was determined by two different means: 1) an instantaneous procedure of ~0.3-s duration, yielding MEP and 2) an average procedure, consisting of a 5- to 6-s all-out pedaling bout on an isokinetic cycloergometer, yielding MCP.

Both procedures, despite their widely different duration, depend energetically on anaerobic alactic sources (mainly phosphocreatine splitting). In addition, in both cases the active muscles are essentially the same (primarily knee extensors), and the recovery of elastic energy is negligible, a fact that is obvious for MCP and that has been recently demonstrated for MEP (37). Thus the main difference between MEP and MCP is the velocity of movement, which is much higher for MEP. With this in mind, we will now briefly discuss the salient characteristics of both procedures with the purpose of drawing a comparison between the two.

The power developed during very short all-out efforts can be assumed to depend on 1) the active muscle mass, 2) the intrinsic characteristics of the recruited motor units, and 3) a fast and coordinated recruitment pattern. If this is so, the decrease in MEP and MPC observed after spaceflight could be due to any of these three factors or to a combination thereof.

Morphological data obtained by Zange et al. (38), by means of nuclear magnetic resonance of the subjects' calf muscles immediately after reentry, demonstrate a decrease in the muscle cross-sectional area (CSA) ranging from 9% in S1 to 13%, on average, for S2, S3, and S4. In addition, in two subjects (S3 and S4) the CSA of the thigh was estimated from measurements of the circumference 20 cm above the upper margin of the patella. The resulting changes in the CSA at R+2 were 9.0% for S3 and 17.8% for S4, with no differences between the left and right thigh. Because, at R+2, the body mass of S3 and S4 had decreased by 6 and 3% only (see Table 2), respectively, the above changes in CSA of the thigh are due essentially to changes in muscle mass. These changes are on the same order as observed in the same subjects for the CSA of the calf, which amounted to 13 and 20% for S3 and S4, respectively (J. Zange, personal communication). Thus the percent changes observed by Zange et al. (38) in the calf can be assumed to be a measure of the changes in CSA of all active muscles. If an unchanged muscle length is assumed, the observed changes in CSA must be equal to the changes in muscle mass. Thus the percent MEP values observed after flight can be expressed relative to the muscle mass in percentage of preflight values. For MEP, these calculations at R+2 (R+3) amount to 0.67/0.91 = 0.74 for S1 and to 0.47/0.87 = 0.54 for S2, S3, and S4 (average).

It is therefore apparent that, in the case of MEP, the decrease in muscle mass is much smaller than the decrease in the power output throughout the investigated microgravity duration (31-180 days). It necessarily follows that other mechanisms must be responsible for the observed decline in MEP.

Under all experimental conditions, the fall in MEP was due to essentially equal declines in force and velocity (see RESULTS). For all subjects, with the exception of S1, the duration of the push increased after flight, this being presumably an attempt to reduce the fall in force by increasing its time of application. This set of observations can be tentatively attributed to either 1) changes in the motor unit types, which tend to become slower; and/or 2) a slower motor unit recruitment pattern.

The former possibility seems rather unlikely in view of the data obtained in animals after microgravity, which show the opposite trend (11, 12, 33). Similar "slow-to-fast" changes in muscle characteristics have been shown in humans as a consequence of spaceflights of short duration (15, 39).

We therefore think that, besides the above-mentioned decrease in muscle mass, the major factor responsible for the decline in MEP is a change in the motor unit recruitment patterns brought about by the absence of gravity. This hypothesis is similar to that put forward by other authors as "hypogravitational ataxia" (17). In essence, this state of affairs is the opposite of the early effects of muscle strength training, in which case the changes in muscle force precede, and are larger than, those in muscle mass, presumably because of more effective motor unit recruitment patterns (30). In addition, data recently reported by Koryak (20) suggest that the fall in maximal voluntary contraction force of the triceps surae after 7 days of simulated microgravity ("dry" water immersion) are mostly due to a reduction in motor drive.

Ferretti (16) has recently reported a 24% average reduction in the maximal power in 6 subjects during a standing high jump off both feet after 41 days of head-down tilt (6°) bed rest, accompanied by a 13.4% mean decrease in the CSA of the extensor muscle groups. Thus, after 41 days of bed rest, the explosive power relative to the muscle mass amounted, on average, to 0.76/0.866 = 0.88, a value substantially larger than that of 0.74 observed in S1, who remained in space for a comparable period of time. The procedure utilized in this study to determine MEP is not directly comparable to standing high jumps off both feet, the latter, but not the former, permitting a substantial recovery of elastic energy (37). When it is considered that Ferretti's bed rest study lasted 42 days with no exercise at all, compared with a spaceflight of 31 days with 2 h/day of aerobic exercise for S1, the large fall in MEP seems to be a specific characteristic of spaceflight that cannot be easily reproduced by bed rest.

The fall in MCP was substantially less than that of MEP, as indicated in Fig. 5, in which the MCP data lie above the identity line. In addition, when the MCP data are expressed per unit muscle mass, as was done above for MEP, the resulting values are 0.82/0.91 = 0.90 for S1 and ~0.70/0.87 = 0.80 for S2, S3, and S4, i.e., substantially larger than those observed for MEP.

View larger version (16K): [in this window] [in a new window]   Fig. 5.   MCP plotted as function of MEP assessed in same experimental session. Both variables are expressed in %preflight values. For all subjects [S1 (), S2 (), S3 (), and S4 ()] and all experimental sessions, data lie above identity line.

The different responses of MEP and MCP to microgravity presumably arise because, for MCP, the pedal frequency, and hence the speed, is imposed by the isokinetic cycloergometer, as opposed to MEP, where both force and velocity are set by muscle action. In addition, whereas in one case (MEP) the time from zero force (and speed) to peak force (and speed) was ~200 ms (see Fig. 2), in the other (MCP) the time for full muscle activation was 500 ms (Fig. 3). The larger decline in MEP, compared with MCP, after spaceflight is consistent with the data reported by Thornton and Rummel (36) during torque-velocity tests performed on the extensor muscles of the legs and trunk of the astronauts participating in the Apollo project. Indeed, Thornton and Rummel showed a larger loss of force at the higher velocities of shortening. Any effects interfering with fast and coordinated motor unit recruitment are therefore likely to have a greater impact on MEP than on MCP.

To the authors' knowledge, the data reported above are the first and only observations of the effects of microgravity on maximal muscular power. In contrast, the effects of microgravity on posture and muscle tone have been reported by numerous studies. These consistently show a generalized flexor prevalence (8-10), resulting from 1) a greater inhibition of the extensors; 2) a greater facilitation of the flexors, arising from muscles and joints proprioceptors (14); and 3) the absence of the reflex activation of the extensor muscles, arising from the pressure of the pads of the feet on the floor as shown in simulated microgravity (1). This muscle tone resetting in the direction of a flexor bias is also shown by the "fetal" resting position in space, reported by Thornton et al. as early as 1977 (34) and persisting even after reentry on Earth (10). Finally, comparisons of pre- with postflight characteristics of gait and standing jump have shown postflight changes attributable to the effects of microgravity on locomotor coordination (4).

In summary, all these data indicate that the absence of gravity brings about a substantial rearrangement of muscle postural tone and of locomotor coordination. We propose that microgravity, favoring, as it does, smooth and delicately balanced muscle actions as opposed to forceful ones, brings about a rearrangement of the motor control system that is responsible, at least to a large extent, for the observed decline in the maximal muscular power during all-out, short-lasting muscle actions. We are not in the position of proposing at this stage any clear-cut hypothesis as to the mechanisms underlying these changes. However, recent data show that the fall in MEP after spaceflight is mirrored by a similar fall in electromyographic activity of the vastus lateralis, vastus medialis, and rectus femoris (2). In addition, the time course of the electromyographic recovery of the vastus medialis is much slower than that of the two other heads of the quadriceps femoris. Although these data were obtained in only one subject, they do support the hypothesis that microgravity interferes substantially with the normal motor unit recruitment patterns during very short all-out exercises.