Download Changes in muscle size, architecture, and neural activation after 20

Eur J Appl Physiol (2001) 84: 7±12
Ó Springer-Verlag 2001
ORIGINAL ARTICLE
Yasuo Kawakami á Hiroshi Akima á Keitaro Kubo
Yoshiho Muraoka á Hiroshi Hasegawa
Motoki Kouzaki á Morihiro Imai á Yoji Suzuki
Atsuaki Gunji á Hiroaki Kanehisa á Tetsuo Fukunaga
Changes in muscle size, architecture, and neural activation
after 20 days of bed rest with and without resistance exercise
Accepted: 18 September 2000
Abstract Nine healthy men carried out head-down bed
rest (BR) for 20 days. Five subjects (TR) performed
isometric, bilateral leg extension exercise every day,
while the other four (NT) did not. Before and after BR,
maximal isometric knee extension force was measured.
Neural activation was assessed using a supramaximal
twitch interpolated over voluntary contraction. From a
series cross-sectional magnetic resonance imaging scans
of the thigh, physiological cross-sectional areas (PCSA)
of the quadriceps muscles were estimated (uncorrected
PCSA, volume/estimated ®bre length). Decrease in mean
muscle force after BR was greater in NT [)10.9 (SD
6.9)%, P < 0.05] than in TR [0.5 (SD 7.9)%, not signi®cant]. Neural activation did not di€er between the
two groups before BR, but after BR NT showed smaller
activation levels. Pennation angles of the vastus lateralis
muscle, determined by ultrasonography, showed no
signi®cant changes in either group. The PCSA decreased
in NT by )7.8 (SD 0.8)% (P < 0.05) while in TR
PCSA showed only an insigni®cant tendency to decrease
[)3.8 (SD 3.8)%]. Changes in force were related more to
changes in neural activation levels than to those in
PCSA. The results suggest that reduction of muscle
strength by BR is a€ected by a decreased ability to activate motor units, and that the exercise used in the
present experiment is e€ective as a countermeasure.
Key words Pennation angle á Physiological crosssectional area á Twitch interpolation á Countermeasure
Y. Kawakami (&) á H. Akima á K. Kubo
Y. Muraoka á H. Hasegawa á M. Kouzaki
M. Imai á H. Kanehisa á T. Fukunaga
Department of Life Sciences (Sports Sciences),
The University of Tokyo, Komaba 3-8-1, Meguro,
Tokyo 153-8902, Japan
e-mail: [email protected]
Tel.: +81-3-54546866; Fax: +81-3-54544317
Y. Suzuki á A. Gunji
Seigakuin University, Tosaki 1-1,
Ageo, Saitama 362-0053, Japan
Introduction
The maximal force that a muscle can exert has been
shown to be highly correlated with its physiological
cross-sectional area (PCSA; Roy and Edgerton 1992).
The PCSA is thus the major determinant of muscle
force. However, muscle architecture, i.e. geometrical
arrangement of ®bres within a muscle, has been shown
to have a substantial in¯uence on the force-generating
capabilities of the muscle (Kawakami et al. 1993; Lieber
1992). Most skeletal muscles in humans are more or less
pennated (Gans and Bock 1965), in which muscle ®bres
are arranged at an angle with respect to the line of action
of the muscle. This angulation (pennation angle) has
been shown to a€ect force transmission from muscle
®bres to tendon, and hence muscle force generation
(Gans and Bock 1965; Kawakami et al. 1993, 1995;
Lieber 1992; Roy and Edgerton 1992).
Maximal voluntary muscle strength exerted by humans has also been shown to be a€ected by the ability to
activate the motor units of the muscles in action. In fact,
previous studies (Allen et al. 1995; Belanger and
McComas 1981; Dowling et al. 1994) have revealed that
humans cannot fully activate all motor units during
maximal voluntary contraction. It has been shown that
resistance training enhances this ability for neural activation, increasing speci®c tension (muscle force per
PCSA) (Ikai and Fukunaga 1970; Jones and Rutherford
1987; Ploutz et al. 1994).
Decreases in strength as well as atrophy of skeletal
muscles have been observed as a result of decreased
physical activity and prolonged bed rest (BR). Muscle
atrophy has been shown to be pronounced in the lower
limb muscles (LeBlanc et al. 1988, 1992), and it has often been observed that the reduction of strength is
greater than that of muscle size (LeBlanc et al. 1988;
Suzuki et al. 1994). It has not been clear, however, what
proportions of the loss of strength may be attributed to
changes in contraction properties, neural drive, and
muscle dimensions.
8
Reduction of muscle mass and strength of bedridden
people could impede their rehabilitation for resuming
daily activities. Resistance exercise during BR could be a
countermeasure against muscle weakening, but at present there is no clear understanding of the ecacy of
resistance exercise during BR on changes in morphological and functional characteristics of muscles. The
purpose of the present study was to delineate changes in
the muscles due to prolonged BR with respect to their
size and architecture as well as neural activation, and to
obtain insights into an e€ective countermeasure.
Methods
de®ned as the distance between the most proximal and distal images in which the muscle (excluding the tendinous tissue) was visible. Series ACSA were summed for each muscle, and multiplied by
the slice interval to give muscle volume. The PCSA of each muscle
was computed by dividing the muscle volume by respective muscle®bre length, which was determined from the measured muscle
length and a reported ®bre length:muscle length ratio (Wickiewicz
et al. 1983) and total PCSA of the quadriceps muscles was determined. This method is similar to those reported in previous studies
(Fukunaga et al. 1992; Kawakami et al. 1994, 1995; Narici et al.
1992) except that the pennation angle was not taken into account
(Friedrich and Brand 1990). Therefore the present values were
``uncorrected'' not ``functional'' PCSA (Roy et al. 1984). It was
assumed that the ®bre length:muscle length ratio would not have
been changed by BR, based on a ®nding in an animal study (Heslinga et al. 1992). Reliability, reproducibility, and validity of the
measurements have been established in our laboratory (Fukunaga
et al. 1992; Kawakami et al. 1994, 1995).
Subjects and BR protocol
The subjects were nine healthy men [age range 18±28 years; mean
height 172.0 (SD 4.6) cm; mean body mass 68.4 (SD 10.6) kg].
They were volunteers in good health with no history of neurological disease or musculoskeletal abnormality. Each subject was fully
informed of the procedures and signed a consent form prior to the
experiment. This study carried the approval of the Ethics Committee of the Faculty of Medicine, the University of Tokyo. The
experiments carried out in this study complied with the current laws
of Japan.
The subjects carried out a programme of BR with a 6° headdown tilt for 20 days. During transportation the subjects were laid
on a stretcher. To avoid depression due to isolation, all subjects
shared the same room which was air-conditioned to keep temperature and humidity at a comfortable level. Nursing sta€ were
present to assist in the subjects' transportation, maintenance of
hygiene (including toilet and shower, which were carried out with
the subject in a supine position), provision of food and medical
care, as well as support of subjects. The subjects were supervised
24 h a day. Care was taken to avoid systematic changes in the
subjects' body masses throughout BR.
Exercise protocols
During BR, ®ve out of the nine subjects executed resistance exercises every day, using a commercially available apparatus (VR4100, Cybex Corp., USA) modi®ed for the study. The subject, in a
supine position on the apparatus, performed bilateral isometric leg
extensions (i.e. hip/knee extension and ankle plantar ¯exion at the
same time). The hip and knee were ¯exed by 70° and 90°, respectively, and the ankle was dorsi¯exed by 10°. The foot was placed on
the steel plate of the apparatus and the trunk was secured on a
sliding bench which was ®xed to the frame by a steel wire. A force
transducer at the end of the wire measured the force exerted by the
subject. During exercise the subject was encouraged to exert maximal force for 3 s, followed by 3 s rest, repeated 30 times. All sessions were supervised. These subjects were classi®ed as the training
group (TR). The other four subjects (no training group, NT) did no
exercise and adhered to strict BR. There were no statistical di€erences in physical characteristics between groups.
Physiological cross-sectional area of the quadriceps muscles
Series transverse scans of the thigh were made using magnetic
resonance imaging (MRI, GYROSCAN T10-NT, Philips Medical
Systems, USA). The subject lay supine on the unit's gantry bed
with his lower limb extended and relaxed. Transverse scans were
carried out with a slice thickness of 10 mm and an inter-slice gap of
7 mm. In each cross-sectional image, outlines of the quadriceps
femoris muscles were traced, and the anatomical cross-sectional
area (ACSA) of each muscle was determined. Muscle length was
Pennation angle of the vastus lateralis muscle
A single sectional (longitudinal) plane was imaged by B-mode
ultrasonography (SSD-2000, Aloka, Japan) half way between the
great trochanter and the popliteal fossa. This site is where total
ACSA of the quadriceps muscles was largest. The position, half the
width of the super®cial surface of the vastus lateralis muscle, was
determined and used as a measurement site. A transducer with a
7.5 MHz scanning head was placed perpendicular to the deep
aponeurosis of the vastus lateralis muscle. The scanning head was
coated with water-soluble transmission gel which provided acoustic
contact without depressing the dermal surface. The subject stood
upright and relaxed the quadriceps muscles. The angle between the
echo of the deep aponeurosis and echoes from the fascicles in one
dimension was measured as being representative of the pennation
angle of the vastus lateralis muscle as reported by Fukunaga et al.
(1997) and Kawakami et al. (1993, 1995). Care was taken to observe
the fascicles along their whole lengths, by which one can be assured
that the plane of the ultrasonic image is parallel to that of the
fascicles (Fukunaga et al. 1997; Kawakami et al. 1993, 1995). Reliability and reproducibility of the technique have been con®rmed
elsewhere (Kawakami et al. 1993). The measurements of MRI and
ultrasound were carried out before and within 1 day after BR.
Assessment of muscle strength and neural activation
Maximal voluntary isometric strength (maximal voluntary contraction, MVC) of the knee extensor muscles was determined using a
specially designed myometer. This myometer consisted of steel
frames to ®x the thigh and leg with the knee ¯exed at 90°, and a force
transducer which was ®xed with a cu€ on to the lower leg proximally
to the lateral malleolus. The subject sat in a chair with the myometer
attached to it, and secured at the waist and chest with the hip joint
¯exed by 80°. Care was taken to ®x the trunk and lower limb with
identical hip and knee joint angles before and after BR. After a warmup using submaximal and maximal contractions, the subjects were
required to exert maximal knee extension force for 3±4s. They were
loudly exhorted in a standard way to encourage maximal performance. The hip joint angle for this test was slightly di€erent (10°)
from the exercise during BR due to the limitation of the apparatus.
During MVC, evoked twitch contractions were imposed by supramaximal electrical stimulations. The stimulating surface electrodes (4 ´ 7 cm) were placed on the skin over the femoral nerve at
the inguinal region (cathode) and the mid-belly of the quadriceps
muscles (anode). A high-voltage stimulator [SEN-3301, having a
specially modi®ed isolator (SS-1963), Nihon-Koden, Japan] generated rectangular pulses (triple stimuli with a 500 ls duration for one
stimulus and an interstimulus interval of 10 ms). The stimulation
intensity was con®rmed by setting the output of the stimulator to a
level at which there was no further increase in twitch torque. Triple
stimuli were used to take up series compliance and to minimize the
e€ect of the background sti€ness on twitch torque. In all subjects, the
9
stimuli increased the force during MVC at the appropriate latency.
Shortly (within 1±2 s) after MVC when the potentiation e€ect of the
contraction still persisted (Belanger and McComas 1981), the same
stimulation was given to the muscle at rest (control twitch). The
voluntary force at the instant of the stimulation was used as the MVC
force. Two separate e€orts were made routinely, and a third extension was performed if more than a 5% di€erence existed. The highest
scores were adopted for analysis. The twitch force (di€erence between peak twitch force and MVC force) was measured, from which
the level of muscle activation with voluntary e€ort (%activation) was
assessed from the following equation (twitch interpolation technique, Allen et al. 1995; Belanger and McComas 1981; Dowling
et al. 1994; Duchateau 1995), i.e. %activation ˆ [1 ) (twitch force
during MVC/control twitch force)] ´ 100 (%) where control twitch
represents the twitch imposed on the resting muscle after MVC.
Statistical analyses
Statistical analysis of the data was accomplished using a paired
Student's t test for each parameter before (pre) and after (post) BR.
Relative changes were calculated by [(post value ) pre value)/pre
value] ´ 100. A linear regression analysis was performed on the
relationships between relative changes in muscle force, PCSA, and
%activation. In each analysis the level of signi®cance was set at
P < 0.05.
Results
The peak force exerted during exercise in TR during BR
dropped initially, then increased and remained constant
throughout BR (Fig. 1). The inter-subject variability
(shown as SD bars in this ®gure) tended to increase as
BR proceeded.
Table 1 shows the measured variables of TR and NT
before and after BR. In TR, knee extension force increased in four of ®ve subjects, while all subjects in NT
showed a decrease in force (Fig. 2, top). Relative
changes in force ranged between )16 and +5% [mean
+0.5 (SD 7.9)% on average] in TR and between )35
and )3% [mean )10.9 (SD 6.9)% on average] in NT.
Mean control twitch force showed no signi®cant
di€erences between pre- and post-BR in either group
[TR: pre 335.9 (SD 30.3) N, post 330.1 (SD 17.3) N;
NT: pre 356.2 (SD 80.7) N, post 386.8 (SD 114.3) N].
Mean twitch force during MVC, on the other hand, was
unchanged in TR [pre 26.8 (SD 13.5) N, post 21.1
(SD 7.5] but increased in NT [pre 47.4 (SD 15.0) N,
post 78.0 (SD 29.0) N].
Fig. 1 The peak force exerted during exercise in the training group
during bed rest (BR). Average values of ®ve subjects with standard
deviations are shown
The mean PCSA of the quadriceps muscles showed a
signi®cant decrease in NT by )7.8%. In TR, however,
mean PCSA tended to decrease by )3.8% (four subjects
demonstrated slight decreases and one showed an
increase) but the change did not reach a statistically
signi®cant level. The middle panels of Fig. 2 show
individual values of PCSA of the two groups. The
relationship between PCSA and knee extension force
was not signi®cant (for all subjects, r ˆ 0.420 and 0.418,
before and after BR, respectively). The mean force
per PCSA [2.5 (SD 0.6) (TR) and 2.2 (SD 1.1) (NT)
N á cm)2] did not change after BR [2.6 (SD 0.7) and
2.2 (SD 1.2) N á cm)2).
There were tendencies for the pennation angles of the
vastus lateralis muscle to decrease in both groups, but the
decreases were not signi®cant (Table 1). This was due to a
large variability of the individual responses. In TR one
subject showed an increase and two showed a decrease,
and the other two showed no change in pennation angles.
In NT one subject showed a decrease while in the other
three there was no change in pennation angles. The
change in pennation angle, however, was 1° at the largest.
Typical examples are shown in Fig. 3 of the results of
the knee extension force from the subjects in TR and NT.
Table 1 Knee extension force, and total physiological cross-sectional area (PCSA) of the quadriceps femoris muscles, %activation, and
pennation angles for the vastus lateralis muscle (VL) of training (TR) and no training (NT) groups before (pre) and after (post) bed rest.
Relative change was calculated as (post ) pre)/pre ´ 100
TR (n = 5)
Pre
Mean
Knee extension force (N)
PCSA (cm2)
%Activation (%)
VL Pennation angle (°)
a
731.6
296.8
91.9
17.7
NT (n = 4)
Post
SD
157.3
13.8
4.2
2.3
Signi®cantly di€erent between pre and post
Mean
738.0
285.3
92.3
17.6
SD
188.8
12.3
3.8
1.8
Change (%)
Pre
Mean
Mean
0.5
)3.8
0.5
)0.2
SD
7.9
3.8
4.8
4.4
607.8
268.2
86.0
19.8
Post
SD
339.7
33.5
5.3
3.9
Change (%)
Mean
a
546.0
247.2a
80.2a
19.5
SD
Mean
SD
325.2
30.9
1.9
4.1
)10.9
)7.8
)6.5
)1.4
6.9
0.8
7.3
2.8
10
Fig. 3 Typical examples of the recordings of knee extension force
from the subjects in the training group (a) and non training group
(b) before (pre) and after (post) bed rest. Arrows indicate where
supramaximal twitch contractions were imposed (during and after
contraction). Note a remarkable increase in twitch force during
contraction in (b) after bed rest
Discussion
Fig. 2 Knee extension force (top), total physiological crosssectional area (PCSA) of the quadriceps femoris muscles (middle),
and %activation (bottom) before (pre) and after (post) bed rest in
training group (TR) and no training group (NT ). Individual values
are shown with means (d). See text for calculation of %activation.
*Signi®cant di€erence between pre and post
The %activation of the knee extensor muscles, calculated
from the twitch responses during and after MVC, ranged
from 87% to 95%, and from 82% to 94%, in TR and
NT, respectively, before BR (Fig. 2, bottom). There was
no signi®cant di€erence in %activation between groups
before BR. After BR, %activation ranged from 87% to
96% in TR and from 78% to 82% in NT. In NT all
subjects showed decreases in %activation.
The changes in knee extension force were not related
to those of PCSA (Fig. 4, top). However, direct proportionality seemed to exist between the changes in
%activation and those of force (Fig. 4, bottom).
Mean knee extension force decreased after BR in NT
()10.9%), which was accompanied by a signi®cant decrease in mean PCSA ()7.8%). In TR, neither force nor
PCSA changed signi®cantly. These results suggest that
BR lasting for at least 20 days results in signi®cant
muscle atrophy as well as a decrease in muscle force, and
that the present training regimen was e€ective as a
countermeasure during BR against these reductions of
muscle size and strength. Lower limb muscles have been
shown to be predominantly a€ected by BR and decreased
physical activity (Bloom®eld 1997; Dudley et al. 1992;
LeBlanc et al. 1992). The present study shows that these
muscles are also highly responsive to training during BR.
The training was isometric leg extensions with a total
contraction time of 90 s each day. It appears therefore
that dynamic limb movements with longer durations, as
have been frequently adopted (Bamman et al. 1997; Ellis
et al. 1993; Germain et al. 1995), are not necessarily essential for maintaining muscle size and function during
BR. This could have signi®cant implications for training
and rehabilitation of bedridden people.
In animal experiments it has been shown that the
maximal tetanic muscle force is linearly related with
PCSA of that muscle (Roy and Edgerton 1992). In humans, however, a large variability in muscle force per
PCSA has been found (Fukunaga et al. 1992; Kawakami
et al. 1994; Narici et al. 1992). Likewise, in the present
study, muscle forces of individual subjects were not signi®cantly related to their PCSA. In humans, the level of
activation of muscle ®bres would be a factor that in¯uences the relationship between muscle size and force, because in many cases it has been found that humans cannot
fully activate all motor units during MVC (Allen et al.
1995; Belanger and McComas 1981; Dowling et al. 1994).
In this study, there was an increase in force by electrical
11
Fig. 4 The relationships between relative changes in %activation
and knee extension force (bottom) and between relative changes in
physiological cross-sectional area (PCSA) and knee extension force
(top). s Training group, d No training group
stimulation over that of MVC in all subjects. Furthermore, a greater decrease in muscle strength than that of
muscle size was observed in NT. These results substantiate the existence of incomplete motor unit activation,
which is further attenuated by BR. Even in the TR group
which showed no change in knee extension force after BR,
maximal leg extension force decreased in a few days from
the onset of BR, then inter-subject variability tended to
increase thereafter (Fig. 1). It is not surprising therefore,
that in the NT group the decrement of knee extension
force was much greater and signi®cant.
The above notion might be further supported by the
relationship between changes in %activation and those
of force. If we tentatively perform linear regression
analysis on these two parameters over all subjects from
the TR and NT groups, the correlation was signi®cant
(r ˆ 0.745, P < 0.05, Fig. 3, bottom, dashed line). Although this analysis is not statistically correct because
the two groups belong to di€erent populations (one
trained and the other not), this apparent proportionality
suggests that the changes in neural activation were in¯uential in producing the muscle force decrement by BR.
Previous studies have reported similar results (LeBlanc et al. 1988; Suzuki et al. 1994). Suzuki et al. (1994)
found that after 10 days of BR, knee extension MVC
force decreased by 13%±21% which was accompanied by
a smaller decrease in cross-sectional areas of the quadriceps muscles by 4%±10%. For one subject who underwent a programme of 5 weeks of BR, Duchateau
(1995) found a 45% decrease in strength. He attributed it
to a 33% reduction in central activation, and 19% decrease in force-generating capacity of muscle. Sale et al.
(1982) have also found after 5 weeks of cast immobilization a 57% decrease in MVC force in human thenar
muscle, accompanied by a 29% decrease in the estimated
number of functioning motor units and a 45% decrease
in re¯ex potentiation in the immobilized muscle. The
present results also provide evidence for decreased
motoneuron excitability and an impairment of the ability
to activate motor units as a mechanism for the decrements in muscle strength after a period of disuse. Although knee extension force per PCSA of the quadriceps
muscle did not change after BR in either TR or NT, this
result might have been due to the large variability of this
parameter and a small number of subjects. The mean
PCSA and %activation in NT after BR were 92.2% and
93.5%, respectively, of pre-BR values. Multiplication of
these two values yeilds 86.2%, which virtually agrees with
the post BR force which was 89.1% of the pre-BR value.
The ability to activate available motor units has been
shown to increase as a result of resistance training (Ikai
and Fukunaga 1970; Jones and Rutherford 1987; Ploutz
et al. 1994). In the present study, subjects in TR maintained %activation after BR, which can be considered as
an e€ect of the training. It is concluded therefore that
the present training programme was e€ective for maintaining force-generating capabilities as well as muscle
mass. However, joint angle-speci®city of training e€ect
on muscle force has to be considered, especially when
the training is performed isometrically (Kitai and Sale
1989). The hip joint angles during training and testing
were slightly di€erent (10°), but it appears that this
di€erence did not signi®cantly a€ect the results. Neural
adaptation to training during BR for di€erent joint angles and di€erent muscle groups should be clari®ed in
further studies.
It has been shown that muscle pennation is larger in
hypertrophied than in normal muscles (Kawakami et al.
1993). Pennation angles have also been shown to increase
by resistance training (Kawakami et al. 1995). We expected therefore, that pennation angles would be smaller
in atrophied muscles. Since the pennation angle has been
shown to a€ect the force-generating characteristics of
muscle (Gans and Bock 1965; Kawakami et al. 1993,
1995; Lieber 1992; Roy and Edgerton 1992), we hypothesized that the muscle force would be a€ected by
changes in pennation angles as a result of BR. Pennation
angles of the vastus lateralis muscle tended to decrease
after BR in NT, but the changes were not large enough to
reach statistical signi®cance. It is suggested therefore that
muscle atrophy by up to 10% does not substantially alter
12
pennation angles, and that the changes in muscle force
after BR are not a€ected by changes in pennation. A
previous study (Huijing and Heslinga 1991) showed that
muscle architecture changes during detraining do not
necessarily reverse the process of muscle hypertrophy,
which could explain the present results. It should be
noted however that the pennation angle was measured
from the mid-belly of the muscle. A variation in pennation angles within a muscle has been reported (Scott
et al. 1993), so there might be an intramuscular inhomogeneity in changes of pennation. Although this possibility should be tested by further studies, we feel that
intramuscular di€erences in responsiveness to BR, if any,
have only a minor in¯uence on muscle functions.
In summary, knee extension muscle strength decreased after a prolonged BR which was more related
with decreases in neural activation than with those in
PCSA. Pennation angles of the vastus lateralis muscle
were not signi®cantly a€ected by BR. Isometric leg extension training during BR prevented changes in these
parameters. The results suggest that reduced muscle
strength by BR is more a€ected by a decreased ability to
activate motor units than muscle atrophy, and that the
present training programme is e€ective as a countermeasure against decreases in muscle mass and strength.
Acknowledgement The authors thank Dr. Y. Makita and the sta€
in Makita Hospital for assistance with the MRI procedure. This
study was funded in part by Ground Research for Space Utilization, promoted by the National Space Development Agency and
Japan Space Forum.
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