J Appl Physiol
90: 1825–1832, 2001.
Plasticity of monkey triceps muscle fibers
in microgravity conditions
P. KISCHEL, L. STEVENS, V. MONTEL, F. PICQUET, AND Y. MOUNIER
Laboratoire de Plasticité Neuromusculaire, Université des Sciences
et Technologies de Lille 1, F-59655 Villeneuve d’Ascq Cedex, France
Received 26 July 2000; accepted in final form 2 December 2000
skinned fibers; atrophy; contractile proteins; myosin heavy
chain; calcium affinity
larly histochemical studies, have shown that extensor
and flexor muscles from monkey upper limbs have
different functions (23). For instance, extensors have a
relatively greater potential for force production and
force maintenance than flexors.
In this study, we examined the effects of microgravity induced by exposure of monkeys to the 14-day
BION 11 spaceflight on the triceps brachii muscle
(caput medialis). The triceps muscle, an upper limb
extensor, is composed of a large proportion of slow
fibers in its deepest zone. Our objective was to characterize, for the first time, the contractile properties of
the extensor triceps muscle. Moreover, this work permitted analysis of the effects of microgravity in this
muscle and comparison of these effects with 1) data
obtained on extensors from other species such as rat
soleus muscles and 2) data obtained on monkey soleus
muscle, a hindlimb extensor, and data reported by
Fitts’ group (12, 37) after the same spaceflight. Finally,
this spaceflight offered the opportunity to distinguish
some specific effects of microgravity from those resulting from confinement or immobilization conditions
generally associated with the space environment.
We have demonstrated that functional modifications
occurred after this spaceflight. These modifications
consisted of an atrophic process more marked in slow
fibers, a decrease in force associated with a decrease in
Ca2⫹ affinity of the contractile system, and slow-to-fast
changes in myosin-based fiber typing. These effects
were distinguishable from those due to arm immobilization, since in the latter case, no atrophy and no
change in the steepness of the tension-pCa (T-pCa)
relationships were observed. Finally, we have discussed the implication of the different regulatory contractile proteins.
PREVIOUS FINDINGS ON ANIMALS exposed to microgravity or
simulated non-weight-bearing conditions have shown a
marked atrophy of some hindlimb muscles. For instance, studies on rat muscles after spaceflights demonstrated that microgravity induced a spectacular atrophy of slow-twitch extensors such as the soleus. Our
experiments performed after those flights showed that
this atrophy was characterized by a decrease in fiber
diameter and isometric force and was accompanied by
slow-to-fast changes in contractile properties (15, 27,
29) and in myosin isoform composition (30). These
results were confirmed by numerous studies (1, 6, 13).
Data from primates flown on biosatellites have provided an excellent opportunity to study the effects of
microgravity on the neuromuscular system (3). Indeed,
monkeys appear to be a suitable model for investigating muscle contractile and biochemical properties, as
well as other activities, such as work capacity and
electromyogram recording. Previous studies, particu-
Animals. The experiments were performed on rhesus monkeys (Macaca mulatta) weighing 3.7–4.8 kg at the time they
were selected (⬃5 mo before the flight). They were divided
into four groups. The first (Cont) group included 11 monkeys
on which biopsies were obtained 5 mo before launch. On the
basis of results after the preliminary tests required by the
Address for reprint requests and other correspondence: Y.
Mounier, Laboratoire de Plasticité Neuromusculaire, Université des
Sciences et Technologies de Lille 1, Bâtiment SN4, 59655 Villeneuve
d’Ascq Cedex, France (E-mail : [email protected]).
The costs of publication of this article were defrayed in part by the
payment of page charges. The article must therefore be hereby
marked ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734
solely to indicate this fact.
http://www.jap.org
METHODS
8750-7587/01 $5.00 Copyright © 2001 the American Physiological Society
1825
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Kischel, P., L. Stevens, V. Montel, F. Picquet, and Y.
Mounier. Plasticity of monkey triceps muscle fibers in microgravity conditions. J Appl Physiol 90: 1825–1832, 2001.—
We examined the changes in functional properties of triceps
brachii skinned fibers from monkeys flown aboard the BION
11 satellite for 14 days and after ground-based arm immobilization. The composition of myosin heavy chain (MHC) isoforms allowed the identification of pure fibers containing type
I (slow) or type IIa (fast) MHC isoforms or hybrid fibers
coexpressing predominantly slow (hybrid slow; HS) or fast
(hybrid fast) MHC isoforms. The ratio of HS fibers to the
whole slow population was higher after flight (28%) than in
the control population (7%), and the number of fast fibers was
increased (up to 86% in flight vs. 12% in control). Diameters
and maximal tensions of slow fibers were decreased after
flight. The tension-pCa curves of slow and fast fibers were
modified, with a decrease in pCa threshold and an increase in
steepness. The proper effect of microgravity was distinguishable from that of immobilization, which induced less marked
slow-to-fast transitions (only 59% of fast fibers) and changed
the tension-pCa relationships.
1826
MONKEY TRICEPS ADAPTATION TO MICROGRAVITY
trations that induce 50% of maximum Ca2⫹ and Sr2⫹ tension
responses (pCa50 and pSr50, respectively). These characteristics described the affinity of the contractile system for Ca2⫹
and Sr2⫹. Other parameters derived from the T-pCa curves
were used: the threshold for activation by Ca2⫹ (pCathr) and
the steepness of the curves, indicated by the Hill coefficient
(nH). The protocol for data fitting to the Hill equation has
been previously described (15).
Fiber type identification. As described in our previous studies (29, 34), fiber type was determined according to the
difference in Ca2⫹ and Sr2⫹ activation characteristics between fast (F) and slow (S) skeletal muscle fibers. Indeed, it
is generally assumed that F skeletal muscle fibers are less
sensitive to Sr2⫹ than S fibers (10, 16, 32). The pCa50-pSr50
difference (or ⌬ criterion) is used to reflect the relative affinity of a fiber to Ca2⫹ and Sr2⫹. Thus, in our experiments, a
fiber showing a ⌬ of 0.1–0.3 was identified as the S type. On
the contrary, an F-type fiber could be characterized by ⌬ close
to 1. Moreover, the pCathr, pCa50, and nH parameters also
permitted identification of the fiber type. In S fibers, pCathr
and pCa50 values were higher (lower Ca2⫹ concentrations)
and nH was lower than in F fibers.
After physiological measurements (T-pCa and T-pSr), the
myosin heavy chain (MHC) composition of the fibers from the
biopsies of the different monkeys was determined on a 7.5%
polyacrylamide slab gel (35). After the gel run, the gel slabs
were silver stained. This protocol permitted identification of
four MHC isoforms in rat muscles: the S type I isoform and
the three F type IIa, IId/x, and IIb isoforms. The electrophoresis was used here only to determine the fiber type, i.e.,
the proportions of pure and hybrid slow (HS) and hybrid fast
(HF) fibers.
Statistical analysis. Values are means ⫾ SE. The results
were analyzed statistically using a one-way ANOVA followed
by a Bonferroni test to estimate differences among means.
The acceptable level of significance was set at P ⬍ 0.05.
RESULTS
Because we did not have previous data relative to the
characteristics of monkey triceps fibers, we chose to
constitute large-size samples of S and F fibers and,
therefore, to search F fibers, although they were rarely
present (⬃12%; Table 1; see Experimental procedures
and solutions) in the deep part of the triceps from Cont
monkeys. Therefore, the pools of S and F fibers were
similar (52 and 48 fibers, respectively), and to give a
correct typing of the triceps muscle, we reported in
Table 1 the data from Desplanches et al. (7) obtained
from the same triceps biopsies. For the Immo and
Flight groups, the fibers were taken randomly within
the different biopsies.
Fiber type identification: data on control monkeys. A
total of 117 fibers was examined (ⱖ10 fibers were
isolated from each of the 11 Cont monkeys).
Fibers were functionally classified as S or F according to the ⌬ criterion. Electrophoretic analysis revealed
four groups defined according to their composition in
slow and fast MHC (Fig. 1). S and F fibers expressed
only the slow type I and fast type IIa MHC isoforms,
respectively. The two other groups were identified as
composed of hybrid fibers, which coexpressed the type
I and IIa MHC isoforms; they were called HS and HF
according to the predominant isoform, S or F, respectively. In these Cont monkeys (Table 1), the proportion
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different investigators, two monkeys (357 and 484) were
selected for flight aboard the BION 11 satellite for 14 days
(designated the Flight group). One day immediately after the
satellite landed, a second biopsy was obtained. The third
group consisted of cage growth-control (Growth) monkeys
from the initial control pool; with this group it was possible to
differentiate the eventual proper effects of growth, with 5 mo
separating the control and the flight biopsies. Four animals
were selected and kept in cages: biopsies were obtained from
two monkeys (470 and 513) at the time of launch and from
two others (474 and 503) 2 days after landing. The fourth
group, arm-immobilized (Immo) animals (447, 501, and 534),
were used as ground-based simulation controls; they were
placed in a mock-up flight capsule simulating flight conditions (e.g., temperature and sound). Not only were these
animals subjected to restraint conditions in the seats, but
also the upper part of the right arm was maintained close to
the body. The aim of this arm immobilization was to oblige
the monkeys to work with the left arm during the flight to
perform different tests necessary for electromyogram recordings. Therefore, the right arm was subjected to microgravity
and reduced activity.
Biopsies. Muscle biopsies (⬃20–30 mg) were surgically
obtained from the triceps brachii (caput medialis) from the
upper limb. All the biopsies were obtained from the deepest
portion of the midbelly zone of the triceps. In normal conditions, the deep triceps contained a majority of slow fibers.
Another investigator (7) used ATPase staining of the same
biopsies to measure the proportion of type I fibers in the Cont
monkeys (n ⫽ 11, 88.33 ⫾ 3.45%) and the percentages of type
IIa and IIb fibers (9.95 ⫾ 3.15 and 1.7 ⫾ 0.57%, respectively).
For the Flight monkeys, the proportions of type I, IIa, and IIb
fibers were 82.4, 14.8, and 2.8, respectively (for monkey 357)
and 88.0, 10.0, and 2.0, respectively (for monkey 484).
Experimental procedures and solutions. The biopsies were
chemically skinned by exposure to a “skinning solution” (38).
The skinned biopsies were stored at ⫺20°C in a 50% glycerol50% skinning solution. Experimental procedures and solutions have been described in detail in previous studies (18,
28). Briefly, a single skinned fiber was isolated from a biopsy
and transferred to the experimental chamber. A ⬃1.5-mmlong segment was mounted between a small fixed forceps and
a force transducer (Fort 10, WPI, Aston, UK). All the experiments were performed at 19 ⫾ 1°C. With the diffraction of
an He-Ne laser beam, the sarcomere length was adjusted to
2.90 ␮m and controlled during the experiments. At this
sarcomere length, the maximal isometric force (Po) could be
elicited. The diameter of each fiber was measured using a
binocular micrometer (⫻80). The skinned fiber was activated
with various concentrations of Ca2⫹, buffered with EGTA,
and expressed as pCa values (i.e., negative logarithm of Ca2⫹
concentration). The composition of the solutions was calculated by the computer program of Fabiato (9). After exposure
to each pCa, a tension P was recorded and immediately
followed by a maximal tension (Po) elicited using a fully
activating Ca2⫹ concentration (pCa 4.2). This allowed the
calculation of the relative isometric force (P/Po). Then, a
relaxing solution was applied, and the fiber was washed to
eliminate the EGTA traces from the relaxing solution before
initiation of a new tension activation. The relations between
P/Po and the different pCa were given by the T-pCa curves.
After a succession of Ca2⫹ activations, a new range of tensions was obtained using another divalent cation, Sr2⫹, and
T-pSr curves were established as for the T-pCa curves. This
protocol was performed to identify the fiber type (see below).
From the T-pCa and T-pSr relationships, several characteristics could be derived, including the Ca2⫹ and Sr2⫹ concen-
1827
MONKEY TRICEPS ADAPTATION TO MICROGRAVITY
Table 1. Fiber type proportions of control,
arm-immobilized, and flight monkeys
Immo (n ⫽ 3)
HS/WSP
HF/WFP
Cont
(n ⫽ 11)
Pre
Post
7.1
(56)
21.3
(61)
7.6
(17)
19
(21)
33
(15)
31.8
(22)
27
S
Table 2. Contractile parameters of the control triceps
muscle fibers
Flight
Pre
(357 ⫹ 484)
Parameters
Post
357
484
24.8
(4)
23.1
(26)
10
28.2
(7)
19.9
(15)
22.9
13.5
18.9
3.3
20
9
13.6
40.5
66.6
54.5
6.6
(14)
25
(10)
88.3
HS
HF
11.6
F
of HS fibers within the whole slow population (WSP,
HS ⫹ S fiber types) was low and equal to ⬃7%. On
some biopsies we did not find any HS fibers. The ratio
of the number of HF fibers to the whole fast population
(WFP, HF ⫹ F fiber types) was ⬃21%; these fibers were
present in all biopsies.
No variability between the different animals was
found. Indeed, we obtained similar ⌬ criterion values
for the relative Ca2⫹-Sr2⫹ activation properties for the
different control monkeys, in agreement with the data
of fiber typing established by Desplanches et al. (7) (see
METHODS). Therefore, for each fiber type (S, HS, HF, and
F), we pooled the functional data we had obtained in
the 11 Cont monkeys.
Functional properties of control monkey triceps fibers. The results are summarized in Table 2. Diameter
was not significantly different between S, HF, and F
fiber populations. The HS fibers presented the lowest
mean diameter, although it was significantly different
only from that of F fibers. All populations of fibers
exhibited similar Po. However, when expressed per
cross-sectional area, Po of the F group appeared lower
than that of the S group. The Ca2⫹ activation properties of S and F types were not significantly different
(Table 2). The pCathr was clearly lower for F and HF
than for S and HS fibers. The pCa50 values were sig-
Fig. 1. Representative profiles for slow (S), hybrid slow (HS), hybrid
fast (HF), and fast (F) fibers as determined by SDS-PAGE (7.5% slab
gel) of types I and II myosin heavy chain (MHC).
HS (n ⫽ 4)
HF (n ⫽ 13)
F (n ⫽ 48)
⌬
0.22 ⫾ 0.02 0.18 ⫾ 0.05 0.95 ⫾ 0.10* 1.08 ⫾ 0.03*
Diameter, ␮m 60.0 ⫾ 1.6
50.5 ⫾ 3.1
61.4 ⫾ 3.6
66.6 ⫾ 1.9†
Po
␮N
374 ⫾ 20
240 ⫾ 27
292 ⫾ 31
313 ⫾ 19
kN/m2
126.5 ⫾ 9.7 122.2 ⫾ 13.7 101.2 ⫾ 10.9 92.6 ⫾ 5.7*
pCathr
6.72 ⫾ 0.02 6.76 ⫾ 0.13 6.32 ⫾ 0.05* 6.35 ⫾ 0.02*
pCa50
5.90 ⫾ 0.02 5.86 ⫾ 0.13 5.71 ⫾ 0.03* 5.78 ⫾ 0.01*
nH
1.85 ⫾ 0.08 1.66 ⫾ 0.15 2.54 ⫾ 0.09* 2.29 ⫾ 0.08
Values are means ⫾ SE; n, number of fibers. Fibers are from the 11
control monkeys. ⌬, pCa50-pSr50; Po, maximal tension; pCathr,
threshold for Ca2⫹ activation; pCa50, pCa at which tension is halfmaximal; nH, Hill coefficient. * Significantly different from S and HS
fiber types, P ⬍ 0.05. † Significantly different from HS, P ⬍ 0.05.
nificantly lower for F and HF fibers than for S fibers.
Thus the T-pCa relationships of F and HF fibers were
shifted toward higher Ca2⫹ concentrations (Fig. 2, C
and D) than the T-pCa curves of the S and HS fibers
(Fig. 2, A and B). Moreover, the F and HF curves were
steeper than the S and HS curves, as shown by significantly larger nH values. All Ca2⫹ activation parameters (pCathr, pCa50, and nH) exhibited very close values
within a whole population defined by the Sr2⫹ test
(WSP or WFP). Thus we did not observe any difference
between the data obtained for the S and HS fibers or
for the F and HF fibers. Because this result remained
true regardless of the experimental group (Growth,
Immo, or Flight), we gathered the data of functional
characteristics for S and HS fibers in a single group
and for F and HF fibers in another single group (Fig. 2,
E and F). Similar T-pCa relationships were obtained
for S ⫹ HS or F ⫹ HF fibers from all the control
monkeys pooled together (n ⫽ 11) or from individual
groups used as controls in Growth (n ⫽ 4), Immo (n ⫽
3), and Flight (n ⫽ 2) experiments. The groups were
chosen to constitute the controls (or Pre data) of the
different experimental groups. Therefore, Pre and Post
data were obtained in the same animals, with 5 mo
separating the two biopsies. The possible growth effect
is stated below.
Growth effect analysis. For the Growth group, no
differences in diameter and Po (kN/m2) values were
observed in the 5-mo delay between the period of animal selection and the flight. This result is shown for S
(n ⫽ 23 for Pre and Post growth) and F fibers (n ⫽ 21
for Pre and Post growth) in Fig. 3, A and D. T-pCa
relationships obtained for WSP and WFP 5 mo before
launch are reported in Fig. 2, E and F. T-pCa curves for
the biopsies at landing were not different from those at
the time of animal selection (data not illustrated). Thus
all the studied parameters indicated that there was no
growth effect between the time the monkeys were selected and the flight.
Effects of arm immobilization. Data were collected
from three monkeys (447, 501, and 534) whose right
arms were submitted to immobilization. For these
three monkeys, the HS-to-WSP and HF-to-WFP ratios,
established on 35 fibers, before arm immobilization
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Proportions are expressed as percentages of slow (S), hybrid slow
(HS), hybrid fast (HF), and fast (F) fiber types in the pool of 11
control monkeys (Cont) and in individualized groups of animals
before (Pre) and after (Post) arm immobilization (Immo) or Flight
conditions. HS/WSP and HF/WFP, proportion of HS or HF fibers,
respectively, within the whole slow population (WSP) or the whole
fast population (WFP) identified by SDS-PAGE and Sr2⫹ test; numbers in parentheses represent number of fibers. Values for control
monkeys (in boldface) are results from ATPase staining from
Desplanches et al. (7).
S (n ⫽ 52)
1828
MONKEY TRICEPS ADAPTATION TO MICROGRAVITY
were 7.6 and 19%, respectively; these values are close
to those reported above for the 11 Cont monkeys. After
immobilization, the percentage of hybrid fibers increased (Table 1). Indeed, the HS-to-WSP ratio reached
33% and the HF-to-WFP ratio was ⬃32%. Moreover,
the proportion of the four fiber types established from
the 37 fibers taken randomly in the three biopsies of
the Immo monkeys showed an increase in the HF and
F fiber proportions compared with data reported by
Desplanches et al. (7) (Table 1).
After immobilization, there were no significant differences in fiber diameter and maximal force, regardless of fiber type (Fig. 3, B and E). On the contrary,
changes were found in Ca2⫹ activation parameters:
pCathr and pCa50 were decreased for the S and F fibers
(Table 3). Therefore, the T-pCa relationships were
shifted toward higher Ca2⫹ concentrations (Fig. 4). The
nH values were very close before and after immobilization, and, as a consequence, the T-pCa curves of the
two fiber types were parallel.
Effects of flight conditions. After flight, a primary
result is the increased proportion of HS fibers (25 and
28% HS-to-WSP ratio for monkeys 357 and 484, respectively; Table 1) compared with that before flight (6.6%).
A secondary effect of weightlessness is the decrease in
the proportion of S and HS fibers relative to the whole
content in fibers at the expense of a large increase in F
fibers, especially pure F fibers. Monkeys 357 and 484
exhibited the same shift from an S to an F typing.
After flight, diameter and maximal forces significantly decreased in S fibers but did not change in F
fibers (Fig. 3, C and F). For both fiber types, the main
change in Ca2⫹ activation parameters was observed in
the pCathr and the slopes of the T-pCa relationships
(Table 3). The values of pCathr were decreased after
flight, with a larger effect for the S fibers. The nH
was significantly increased for S and F fibers (Table 3,
Fig. 4).
DISCUSSION
For the first time, data on contractile properties of
the triceps brachii, a monkey forelimb muscle, in control and weightlessness conditions are reported. Micro-
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Fig. 2. Tension-pCa (T-pCa) curves of S, HS, F, and HF
fibers from triceps muscles of 11 control monkeys. F,
Pooled data from all control monkeys; E, Œ, and ‚, data
from separated groups used as controls before growth,
immobilization, and flight experiments, respectively.
Curves are drawn according to the Hill equation. Values are means ⫾ SE; n, number of fibers. P/Po, relative
isometric force.
1829
MONKEY TRICEPS ADAPTATION TO MICROGRAVITY
Fig. 4. Tension-pCa relationships in control conditions, after arm
immobilization, and in spaceflight. A: S ⫹ HS fibers. B: F ⫹ HF
fibers. Dotted curves in A and B correspond to the curves in Fig. 2, E
and F, respectively.
gravity induces a slow-to-fast shift of the triceps phenotype, as demonstrated by a large increase in the HS
and pure F populations to the detriment of the pure S
fiber content. Although only S fibers appeared atrophied and exhibited a decrease in their Ca2⫹ sensitivity after weightlessness, the cooperativity between the
proteins of the thin filament increased in all fibers,
indicating an effect of weightlessness on many proteins
involved in the contractile process. Moreover, we have
provided evidence that, in a situation such as spaceflight, in which immobilization is accompanied by microgravity, with both conditions inducing a slow-to-fast
shift in the triceps contractile properties, the proper
effect of weightlessness can be identified. Indeed, most
of the previous results after exposure to microgravity
were obtained in rats. Therefore, it was difficult to
assess the hypokinetic factor; in this study, however,
the immobilization of the monkey could be strictly
simulated and controlled.
Muscle fiber types in monkey triceps. According to
electrophoretic analysis, four fiber types were found in
the triceps muscle: pure S and F fibers and hybrid
fibers, which coexpressed S and F myosin isoforms. In
control monkeys, few HS fibers (7%) were found within
the WSP, whereas the proportion of HF fibers (21%)
within the WFP was more important. Moreover, differences in the Ca2⫹ activation properties between S and
Table 3. Contractile parameters of the pre- and post-arm-immobilized and -flight triceps muscle fibers
Immo
⌬
WSP
WFP
pCathr
WSP
WFP
pCa50
WSP
WFP
nH
WSP
WFP
Flight
Pre
Post
Pre
Post
0.27 ⫾ 0.03 (17)
1.06 ⫾ 0.03 (21)
0.23 ⫾ 0.06 (15)
1.01 ⫾ 0.04 (22)
0.22 ⫾ 0.02 (14)
1.07 ⫾ 0.06 (10)
0.18 ⫾ 0.06 (11)
1.15 ⫾ 0.01 (41)
6.72 ⫾ 0.04
6.37 ⫾ 0.02
6.53 ⫾ 0.07*
6.22 ⫾ 0.02*
6.79 ⫾ 0.02
6.40 ⫾ 0.05
6.50 ⫾ 0.03*
6.30 ⫾ 0.03
5.90 ⫾ 0.04
5.74 ⫾ 0.02
5.73 ⫾ 0.06*
5.65 ⫾ 0.03*
5.93 ⫾ 0.04
5.76 ⫾ 0.05
5.84 ⫾ 0.04
5.77 ⫾ 0.02
2.17 ⫾ 0.14
2.79 ⫾ 0.15
2.13 ⫾ 0.11
2.74 ⫾ 0.12
1.99 ⫾ 0.09
2.60 ⫾ 0.12
2.87 ⫾ 0.18*
3.52 ⫾ 0.12*
Values are means ⫾ SE of number of fibers in parentheses. * Significantly different from Pre, P ⬍ 0.05.
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Fig. 3. Fiber diameters and maximal tensions (Po) of the whole slow
population (WSP, including S ⫹ HS fibers) and the whole fast
population (WFP, including F ⫹ HF fibers) in control experiments
before (Pre) and after (Post) growth (A and D), before and after arm
immobilization (B and E), and before and after flight conditions (C
and E). *Significant difference between Pre and Post, P ⬍ 0.05.
1830
MONKEY TRICEPS ADAPTATION TO MICROGRAVITY
to a change in the properties of the two isoforms of
MHC, I and IIA, normally expressed in the muscle. It is
now well known that the length at which a muscle is
immobilized determines its degree of atrophy (17, 21):
a neutral position produces more moderate changes
than those induced by shortening (25), as in antigravity extensor muscles in real or simulated microgravity
conditions (21).
In our experimentation on ground-based monkeys,
the arm immobilization did not induce any atrophy (no
change in fiber diameters and maximal tensions) in S
and F fibers compared with control animals. This can
be related to the neutral position of the immobilized
triceps. A similar result was obtained for a forelimb
extensor, the soleus, after restraint of monkeys seated
in a replica of a flight chair in ground-based experiments performed in parallel with a 14-day spaceflight,
Cosmos 2044 (2). Fiber diameters of the soleus and
median gastrocnemius remained unchanged. In the
same way, no change in muscle mass (i.e., no atrophy)
was reported in the rat soleus immobilized in a neutral
position (31), although other data (26) reported decreases in the cross-sectional areas of slow oxidative
and fast oxidative-glycolytic soleus fibers after 4 wk of
immobilization. The manner in which the animals
were restrained, the duration of restraint, and interspecies variation in susceptibility to the length at
which the muscle was maintained might explain differences in the results.
After immobilization, the Ca2⫹ affinity of the contractile system decreased, since pCa threshold and
pCa50 were significantly reduced in S as well as in F
fibers. However, in both fiber types the nH values
remained unchanged. Therefore, the T-pCa relationships after immobilization were shifted toward higher
Ca2⫹ concentrations, remaining parallel to the control
curves. A slight shift has already been described for the
T-pCa curve of S soleus fibers after 17 days of bed rest
in humans (36). In our conditions of arm immobilization, the amplitude of the shift was larger for S than for
F fibers (0.17 vs. 0.09 pCa unit).
Effects of weightlessness. The WSP appeared clearly
lower after flight than in the control condition, since its
proportion in monkeys 357 and 484 represented 13 and
31% of the total number of fibers, respectively. Even if
the comparison with control data uses the reference of
ATPase staining for monkeys 357 and 484 (personal
communication, D. Desplanches), it is clear that there
was a large S-to-F transition of the triceps muscle after
microgravity. Thus the whole F proportion was enhanced after flight, and the changes appeared more
extensive than those resulting from the arm immobilization. Indeed, according to Table 1, the proper effect of
microgravity seems to be the reinforcement of the pure
F fiber content. Obviously, for this distinction it was
assumed that the arm immobilization effect was similar at 1 and 0 G, an assumption that cannot be verified.
Moreover, the S-to-F changes also concerned the HSto-WSP ratio, which was increased by a factor of ⬃3.5.
After weightlessness, fibers of the WSP exhibited
decreases in diameter and tensions. Therefore, the
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F fibers were found and appeared similar to those
described previously, especially in rat muscle (18).
Thus the pCa threshold and pCa50 values were lower
and nH was higher for F than for S fibers. Ca2⫹ activation properties in HS and HF fibers were similar to
those in S and F fibers, respectively. This suggested
that the Ca2⫹ activation properties were dictated by a
predominant type of isoform (S or F) and that the
hybrid fibers might modulate other functional properties. For instance, they might contribute to the continuum in the maximal shortening velocity changes observed in rat soleus fibers (34).
The maximal specific force developed by the triceps S
fibers appeared clearly larger than that produced by F
fibers. This might seem surprising, since only a slight
difference or no differences between fiber types have
generally been reported (when a difference existed, the
larger forces were developed by F fibers). Indeed, Fitts
et al. (11) reported no significant differences in Po
between type I and type II fibers from soleus and
gastrocnemius muscles of rhesus monkeys, in agreement with our previous data (5) that described no
statistical differences between the specific Po values of
the S, HS, HF, and F fibers in the rhesus soleus
muscles. The difference between S and F fiber Po values observed here for the triceps muscle did not appear
to result from differences in the size of the two fiber
types. In the triceps muscle, diameters of S and F fibers
were comparable (60 ⫾ 1.6 and 66.6 ⫾ 1.9 ␮m, respectively), as observed for S and F fibers in monkey soleus
muscle (5, 11). However, these values appeared
slightly lower than those reported previously for the S
fibers of the extensor soleus muscle of the monkey (5,
11) and rat (29) hindlimbs. This suggested that data
obtained from the monkey forelimb triceps, although it
is an extensor muscle, cannot be integrated in the
scheme already proposed (37), which predicted that
type I fiber diameters increased as species size increased. These type I fibers developed specific forces
with amplitudes (126.5 ⫾ 9.7 kN/m2) similar to those
found in type I fibers of other species (see Table 2 in
Ref. 37). A possible explanation can be proposed if we
take into account that S fibers in the triceps were found
in the deepest part of the muscle close to the bone. It
might be supposed that these fibers were submitted to
higher mechanical strains and, thus, were trained to
develop larger forces than the F fibers.
Effects of immobilization. After immobilization, the
WSP, including S and HS fibers, attained 40%. Compared with the proportion of type I fibers (mean 88%)
established for the control animals by ATPase staining,
immobilization induced an S-to-F shift of the triceps
phenotype. Moreover, the proportion of HS fibers
within the WSP clearly increased by a factor of 4.5
after immobilization. Our results appeared to be in
agreement with previous data (25, 31) that reported, in
rat soleus muscles immobilized in a neutral position,
an increase in the proportion of fast type IIA MHC in
association with a decrease in type I MHC, whereas
type IIB MHC appeared insensitive to immobilization.
Therefore, the transitions appeared relatively limited
MONKEY TRICEPS ADAPTATION TO MICROGRAVITY
aptation process of the contractile system to the absence of gravity during the BION 11 flight. Increases in
nH have been clearly related to the proportions of fast
troponin T and tropomyosin isoforms (22, 24), and
changes in the troponin T and troponin I isoforms have
already been described in simulated microgravity conditions (4).
In conclusion, despite complex factors due to the
association of microgravity with inevitable other environmental conditions, the changes in muscular properties specifically due to weightlessness can be discriminated and suggested that many proteins of the
contractile system participated in the functional adaptation of the muscle.
The authors thank Dr. D. Desplanches for providing histochemical data.
This work was supported by Centre National d’Etudes Spatiales
Grant 2000/3027 and Fonds Européen de Développement Economique
Régional Grant F007.
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