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70 Õ Vol. 125, FEBRUARY 2003 Copyright © 2003 by ASME Transactions of the ASME
M
velocity (V max ) of whole muscles from mice and rats is unaltered
or only slightly diminished with age 关26,27兴, single muscle fibers
关12,23,24兴 often exhibit substantial 共up to 50%兲 age-related reduc-
M
tions in V max . Based on the data available, it was assumed that
maximum contraction velocity of human muscle is decreased with
age, but that the overall change is probably less than the loss in
isometric strength 关1兴. Therefore V maxM
was decreased by 20%
from the value used for young adults, from 10 to 8 optimal fiber
lengths per second.
During lengthening contractions, the relative weakness in old
age is not as substantial as during isometric contractions. Studies
of isolated mice muscles have found that lengthening muscle
forces, normalized to isometric strength, are 15–30% higher in
old animals compared to young animals 关28,29兴. Similarly studies
of humans show that lengthening muscle strength is better pre-
served with age than isometric or concentric muscle strength
关8,30,31兴. To reflect this difference, the maximum normalized
M
force achievable during lengthening (F̄ len ) was increased from
1.4 for young adults 关19兴 to 1.8 for older adults.
Fig. 1 A Hill-type model was used to describe musculo-tendon
contraction mechanics. The model consists of a muscle con- Active Force-Length. Studies of isolated rat muscles and hu-
tractile element in series and parallel with elastic elements. „a… man skeletal muscle cells have found that both the optimal fiber
A Gaussian curve was used to describe the active force-length length and shape of the active force-length relationship are rela-
relationship of muscle. „b… The muscle force-velocity function
was scaled with activation such that the unloaded contraction
tively unchanged with age 关12,32兴. Therefore the active force-
velocity was reduced during sub-maximal activation. „c… Ten- length relationship of the contractile element was assumed to be
don force was assumed to increase exponentially with strain the same for both the young and old adult muscle models.
during an initial toe region, and linearly with strain thereafter.
Passive Force-Length. Passive muscle tension accounts for a
greater proportion of total tension 共active plus passive兲 in old
muscles during stretch 关32兴, which may result from an age-related
Effects of Age on Muscle Mechanics. Age-related changes increase in the amount of noncontractile tissue contained in
incorporated into the musculo-tendon model 关Table 1兴 were those muscle 关33,34兴. In the model, the passive muscle strain due to
considered representative of muscle atrophy and remodeling that
maximum isometric force, 0M , was reduced from 0.60 for young
occur between the ages of 30 and 70 years of age.
adults 关19兴 to 0.50 for older adults to account for the relative
Isometric Strength. Loss of isometric strength by the 7th de- increase in passive stiffness.
cade of life is reported to be 20 to 40%, depending on the study
and muscles considered 关1–3兴. This loss in strength is primarily Activation Dynamics. The rate of muscle deactivation, i.e. the
attributed to muscle atrophy due to a decrease in the total number rate of uptake of calcium ions by the sarcoplasmic reticulum, is
and size of muscle fibers with aging 关1,3,9兴. In addition to atro- slowed in old muscles 关35,36,37兴. In rats, the magnitude of the
phy, the decrease in strength with age seems to also result from a slowing of calcium uptake rate with age varies from 0% to 50%,
decrease in the specific strength 共force/area兲 of muscle 关4,20兴, depending on the muscle considered 关36兴. In humans, the esti-
though this issue is less clear 关21,22兴. In the current study, isomet- mated rate of calcium ion uptake in the quadriceps was 37% lower
ric strength of individual muscles was reduced 30% from values in old females compared to young females, a difference that was
used for young adults, which is comparable to the loss of isomet- partially reduced through high resistance training 关37兴. Slowing of
ric strength measured in muscles of the lower extremities 关2兴. calcium uptake rate with age was reflected in the model by in-
creasing the deactivation time constant ( deact ) from 50 to 60 ms.
Force-velocity. In old human muscle, reductions in maximum How the rate of muscle activation changes with age is not well
contraction velocity likely occur because of a preferential loss of understood so act was left unchanged in the older adult muscle
fast twitch motor units 关2兴 and fast twitch fiber cross-sectional model. It is noted that activation dynamics, i.e. calcium release
area 关10兴, as well as changes in the contraction characteristics of and diffusion, are relatively fast compared to contraction dynam-
specific fiber types 关12,23,24兴. Larsson et al. 关25兴 measured a ics in muscles with tendon length/fiber length ratios greater
slight 共7%兲 decrease in maximum knee extension velocity be- than five 关18兴. Thus, changes in act that may arise with age
tween the ages of 25 and 65. While the maximum contraction would likely have little affect on the dynamic contractions of
plantarflexor muscles 共which have tendon length/fiber length ra-
tios greater than eight, Table 2兲 but may influence the dy-
Table 1 Parameters of the musculo-tendon model were ad- namic characteristics of muscles with shorter tendons such as the
justed to reflect nominal changes in muscle mechanics that dorsiflexors.
occur between the ages of 30 and 70. In addition to the param-
eter adjustments shown, maximum isometric muscle forces Tendon Stiffness. The tendon strain due to maximum isomet-
were also reduced 30% from values used for young adults. ric force ( T0 ) was set to 0.04 in the old adult musculo-tendon
M
model, the same value used for the young adults 关38兴. Since maxi-
deact V max mum isometric force is lower for the old adults, this assumes that
共ms兲 M
(L o /s) 0M M
F̄ len the old adult tendon is more compliant in absolute terms. This is
Young 50 10 0.6 1.4 consistent with biomechanical tests of tendon specimens, which
Old 60 8 0.5 1.8 have found that the tensile modulus 共slope of the linear region of
the tendon stress-strain curve兲 of tendon tends to decrease with
deact-deactivation time constant, V max
M
-maximum muscle contraction velocity ex- age 关39,40兴, though the decrease is not always significant 关41,42兴.
pressed in optimal fiber lengths (L oM ) per second, 0M -passive muscle strain due to
M
maximum isometric force, F̄ len -ratio of maximum lengthening muscle force to iso- Ankle Simulations. Four muscles were included in an ankle
metric force. model: dorsiflexors, soleus, gastrocnemius and other plantarflex-
1
Table 3 Simulated contraction times „CT… and one-half relaxation times „ 2RT… in response to unit pulse muscle excitations of 5
ms duration. Both simulations and experimental data reflect an age-related slowing in contraction and relaxation. The model
1
predicted contraction times that tended to be slightly faster than experimental data, while predicted 2RT were of comparable
magnitude with measured values.
1
CT 共ms兲 2RT 共ms兲
Ankle
Angle Young Old Young Old
Dorsiflexion „DF…
Simulated 10 deg PF 50 60 73 94
Vandervoort and McComas, 1986 30 deg PF 96 共8兲 113 共10兲 110 共12兲 119 共28兲
Van Schaik et al., 1994 10 deg PF 55 共9兲 73 共5兲 55 共8兲 63 共6兲
Plantarflexion „PF…
Simulated 5 deg DF 88 104 87 122
Davies et al., 1983 10 deg PF 113 共11兲 148 共15兲 78 共4兲 99 共13兲
Vandervoort and McComas 关1986兴 10 deg DF 146 共21兲 183 共23兲 123 共12兲 143 共27兲
The ages 共in years兲 of subjects included in the representative studies were: Davies et al., 1983: Young⫽20– 24, Old⫽69.7⫾1.3
van Shaik et al., 1994: Young⫽20– 40, Old⫽60– 80 Vandervoort and McComas, 1986: Young⫽20– 32, Old⫽70– 80
Table 4 Maximum isometric ankle torques and times required to reach 50% of maximum torque „ T 50… during simulations of rapid
isometric contractions from rest. The mean „SD… maximal isometric torques and T 50 values from experimental studies are shown
for comparison. T 50 values are not shown separately for males and females since simulated values were identical for each gender.
The ages 共in years兲 of subjects included in the representative studies were: Vandervoort and McComas, 1986: Young⫽20– 32, Old⫽70– 80
Thelen et al., 1996: Young⫽19– 29, Old⫽65– 86
ducted and found that the prolonged contractions predicted by the where act is the activation time constant and deact is the deacti-
model were primarily a result of the assumed decrease in maxi- vation time constant. This relationship predicts that the activation
mum contraction velocity and increase in the deactivation time slows as activation level increases due to less efficient calcium
constant. release and diffusion. Similarly deactivation slows when muscle
The model also predicted that ankle power development during activation level decreases due to there being less calcium ions
high-speed shortening is adversely compromised with aging. This available for uptake by the sarcoplasmic reticulum 关19兴.
effect resulted from the assumed changes to the normalized force-
velocity function with age: i.e., a decrease in the maximum con- Muscle and Tendon Properties. The passive force-length re-
traction velocity and increase in the maximum normalized force lationship of muscle is represented by an exponential function:
during lengthening. The result of these parameter adjustments was PE ¯ M
共 L M ⫺1 兲 / 0
a larger percentage loss in joint torque, and correspondingly ek ⫺1
F̄ PE
⫽ k PE
(3)
power, development at high contraction velocities that that seen e ⫺1
during isometric or lengthening contractions. This prediction is
consistent with isokinetic strength studies, which have found that where F̄ PE is the normalized passive muscle force, k PE is an
eccentric strength is better preserved in old age than isometric or exponential shape factor, and 0M is the passive muscle strain due
concentric strength 关5,8,31,50兴. to maximum isometric force. The shape factor, k PE , was set equal
In summary, accounting for changes in muscle properties is an to five, while 0M was set differently for young and old adults as
important consideration when using forward dynamic models to described in the Methods.
interpret movement performance of older adults, particularly The active force-length relationship of muscle is represented by
when simulating tasks that require large strengths, rapid changes a Gaussian function 关46兴
in force or substantial power development.
¯ M ⫺1 兲 2 / ␥
f l ⫽e ⫺ 共 L (4)
Acknowledgments M
where f l is an active force-length scale factor, L̄ is the normal-
The financial support of the National Science Foundation 共BES- ized muscle fiber length, and ␥ is a shape factor. A value of 0.45
9702275兲, the National Institute on Aging 共AG13759-01兲 and the was selected for ␥ which approximates the force-length relation-
contributions of the University of Michigan Biomechanics Re- ship of individual sarcomeres 关51兴.
search Laboratory to the experimental portion of this study are The force-strain relationship of tendon is represented by an ex-
gratefully acknowledged. ponential function during an initial nonlinear toe region and by a
linear function thereafter:
再
T
Appendix F̄ toe
共 e k toe
T / T
toe ⫺1 兲 ; T ⭐ toe
T
再
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b⫽ 共 2⫹2/A f 兲共 a f l F̄ len
M
⫺F̄ M 兲 (7) 关23兴 Xiaopeng, L., and Larsson, L., 1996, ‘‘Maximum Shortening Velocity and
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M
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In Eq. 共7兲, F̄ len
M
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