When the force applied to a muscle exceeds the force produced by the muscle it will lengthen, absorbing mechanical energy. These eccentric contractions, which result in both braking and storing
elastic recoil energy in normal locomotion, require very little metabolic energy, yet they are
characterized by high force production.
Any time the magnitude of the force applied to a muscle
exceeds that produced by the muscle, it will lengthen.
Lengthening, or eccentric, muscle contractions have a surprisingly
long history in physiological studies. (Note that this word
was first introduced as “excentric” by Asmussen in 1953. This
original spelling is more enlightening as it combines the prefix
ex, “from or away,” with centric, “center,” hence a muscle contraction
that is moving away from the muscle’s center.) In 1882,
Fick observed that a muscle could exert greater force when
stretched while contracting. Fifty years later, Hill reported
another feature of eccentric contractions, namely that there is
decreased energy liberation in a muscle that is stretched during
a contraction. But the first revelation of the functional significance
of these properties occurred by way of a clever demonstration
devised by Bud Abbott, Brenda Bigland, and Murdoch
Ritchie (1). They connected two stationary cycle ergometers
back-to-back with a single chain, such that one cyclist pedaled
forward and the other resisted this forward motion by braking
the backward-moving pedals. Because the internal resistance
of the device was low, the same force was being applied by
both individuals, yet the task was much easier for the individual
braking. This demonstration cleverly revealed that a tiny
female resisting the movement of the pedals (in this case,
Bigland) could easily exert more force than, and hence control
the power output of, a large burly male pedaling forward
(Ritchie).
However intriguing, relatively little more was done to probe
the properties of lengthening muscle contractions. Conventional
wisdom continued to focus on work done by shortening
muscles as essential during locomotion. Furthermore, most of
the classic studies in muscle physiology, which have formed
the foundation of our basic understanding of how muscle
works, are founded on two important experimental
approaches: isometric (constant length) and isotonic (shortening
against a constant load) muscle contractions. As a consequence,
much less is known of both the mechanics and the
energetics of activated muscle during forced lengthening than
during shortening or remaining at a fixed length. In fact, so little
is known that the late muscle biomechanist Tom McMahon
and his student Jason Harry characterized lengthening contractions
as “the dark side of the force-velocity curve”; a reference
to the relative lack of knowledge about this region of the
classic model of Hill that describes the relationship between a
muscle’s shortening velocity and its force production. Only
recently are both the importance and prevalence of lengthening
contractions in normal locomotion receiving increasing
attention (see references in Ref. 5).
Muscles as compressible shock absorbers.
When the force exerted on the muscle exceeds the force
developed by the muscle, work is done on the stretching muscle
and in the process the muscle absorbs mechanical energy.
This is often referred to as the muscle doing “negative work”
(1). What becomes of that absorbed energy depends on how
the muscle is being used. The energy can be dissipated as heat,
in which case the muscle is functioning as a damper or shock
absorber. When hiking downhill, especially a steep hill, this is
the primary function of the locomotor muscles (Fig. 1). For
example, a 70-kg person descending 500 m absorbs ~350 kJ
of energy, enough energy to increase body temperature by 4-
5°C. However, the energy absorbed during locomotion can
also be stored temporarily as elastic recoil potential energy and
subsequently recovered. For example, when running, kinetic
energy is absorbed each time the foot hits the ground and continues
to be until the center of mass passes over the foot, the
point at which both the gravitational potential energy and
kinetic energy are at their minima (hence elastic recoil potential
energy is at its maximum) during a normal running stride
(see, e.g., Refs. 3, 5, and 6). A large portion of this absorbed
energy is recoverable, adding to the active force produced on
the subsequent stride. For example, during running, trotting,
hopping, and jumping the muscle-tendon system functions as
a spring when the muscle lengthens while activated, before
subsequently shortening (Fig. 1). This stretch-shortening cycle
results in improved running economy by a significant
enhancement of the power output of the subsequent contraction.
In vivo measurements demonstrate that this increase in
force production may exceed 50% (8, 13).
In this capacity, the muscles and their tendons are behaving
as springs that cyclically absorb and recover elastic recoil
energy. Significantly, this function is time dependent; if not
recovered, this energy too is lost as heat (3). Hence combining
both of these important properties (shock absorber and timedependent
spring) into a single model, the muscle is functioning
like a shock absorber in series with a spring. This conceptual model captures two features of eccentric contractions:
energy absorption and its time-dependent recovery (Fig. 1).
Because the spring function is time dependent, any shift in the
cycle duration of muscle use, for example stride frequency,
will also result in a shift in the fraction of the energy that is
recovered vs. that lost as heat, thus impacting the cost of locomotion.
While not strictly analogous to a resonating frequency
(but see Ref. 6), the time course of muscle stretch and subsequent
shortening may be the single most important variable
dictating stride frequency among animals; animals should be
expected to move by using a stride frequency that will maximize
energy recovery. In fact, running mammals spanning
three orders of magnitude in body mass have been successfully
modeled as a simple mass and spring system. The conclusion
of this modeling is that stride frequency among running mammals
can be predicted by the relatively simple concept that
muscles and their tendons and ligaments function to maximally
recover stored elastic energy (6).
A physiology teaching laboratory that we use, inspired by
the work of Claire Farley and C. R. Taylor, demonstrates quantitatively
both the energy saving and time dependency of muscles
functioning as springs that temporarily store and recover
elastic recoil energy. When hopping in place, a student volunteer
quickly selects a preferred hopping frequency that feels
comfortable and is highly reproducible for any given individual.
By measuring oxygen uptake, it can be demonstrated that
this preferred frequency is the frequency that minimizes the
energetic cost per hop. When forced to hop at half this frequency
(controlling for hop height, we use a vertical jump
height equal to 107% of the subject’s eye height for this lab),
the cost per hop doubles. This lab demonstrates the striking
energy savings that results when elastic recoil supplements the
force that the muscles must produce when operating cyclically,
in this case against gravity alone; the cost is halved or 50% of
the energy is recovered. In addition, this lab demonstrates the
body size dependency of this frequency. When the specific
preferred frequency is plotted on the graph that describes stride
frequency as a function of body mass across a full size range
of galloping mammals (15), it falls very close to the value predicted
for a mammal of the subject’s body size (see Ref. 6). Taylor
has made the point that hopping on two feet in a biped is
biomechanically similar to galloping in a quadruped. Usually,
this lab demonstrates yet another principle of (novel or naïve)
eccentric contractions: the subject is almost certain to experience
some muscle soreness the next day. If hoping frequency
is set solely to maximize elastic recoil in humans, perhaps
stride frequency is chosen to maximize energy recovery in all
mammals. This may also explain why, within any gait, animals
select a relatively constant stride frequency and change speed
primarily by changing stride length. It would be energetically costly to deviate from this preferred, energy-recovering frequency.
Muscles can recover 50% (or more) of the energy that
would otherwise be lost by simply “tuning” the frequency of
their use.
Adaptability of the muscle spring.
If the “spring property” of muscle is crucial for energy saving,
one might speculate that shifts in demand (i.e., the pattern
or nature of muscle use) might result in alterations in the muscle’s
spring properties. In other words, perhaps this muscle
characteristic, like the contractile and metabolic properties of
muscle, is also phenotypically plastic. If a muscle is chronically
subjected to an eccentric load, does it respond with
increased stiffness of the muscle spring? One might expect that
a stiffer spring could have two impacts. First, it could act to
protect the stretching muscle from stretch overload damage.
For example, someone unaccustomed to hiking downhill is
likely to experience delayed onset muscle soreness from a single
downhill hike (or being a subject in the hopping lab),
whereas anyone who hikes downhill regularly has no discomfort
whatsoever (in response to a stiffer spring). Second, a stiffer
spring could enhance the amount of elastic recoil energy available
in the stretch-shortening cycle (8). Seyforth et al. (13) have
demonstrated the importance of this enhancement in a task
such as a long jump. Could a stiffening of the muscle spring
result in greater net force during this kind of activity? We have
used two different models to examine these possibilities.
We have developed an eccentric cycle ergometer that uses
a 3-hp motor to drive the pedals in a backward direction. In
resisting or slowing this pedal movement, the subject experiences
eccentric contractions of the knee (quadriceps) and hip
extensors (hamstrings and gluteals). We found that when the
workload was increased slowly (in both intensity and duration)
over several days, previously sedentary subjects experienced
no muscle injury (i.e., no loss of muscle strength), little discomfort
(10), and after 8 wk were producing force eccentrically
during their 1/2-h daily training periods that exceeded in
magnitude the current 1-h cycling record if it had been produced
concentrically. Following 8 wk of training, both muscle
strength (measured isometrically) and apparent cross-sectional
area (of biopsied muscle fibers) increased by ~40% (Fig. 2A).
In contrast, subjects exercising at the same metabolic exercise
intensity (measured as exercise heart rate) on a standard
ergometer had no change in either muscle strength or size (9).
Furthermore, this activity apparently resulted in a stiffening of
the “muscle spring.” All of the subjects in this study selected a
higher preferred hopping frequency at the conclusion of 8 wk
of chronic eccentric training (Fig. 2A). In fact, the 11% increase
in hopping frequency (P = 0.001) is equivalent to the increase
in frequency predicted for a 50% reduction in body size
among mammals (15). Thus not only did eccentric training
result in an apparent protection from muscle damage (which
would have been severe in naïve subjects exercising at this
high intensity), but, significantly, there was a shift in the muscles’
fundamental spring property. This stiffer spring manifests
itself with a change in the preferred hopping frequency.
To probe the nature and cause of this shift, we have
employed an animal model (11). With only positive reinforcement,
rats were easily taught to move downhill on a treadmill
while wearing small “backpacks” that held an additional 15%
of each animal’s body mass. This weighted downhill model
represents a significant eccentric load, because the rats must
use their locomotor muscles for braking. After 8 wk of downhill
locomotion, we measured both the isometric force produced
by the triceps muscles as well as the increment increase
in that force when the active muscle was stretched (i.e., when
the muscle is stretched during an isometric contraction). A
lengthening of just less than 2% of the muscle length (0.58 mm in a
muscle 30 mm long) increased the force production by ~38%
in a control (nontrained) muscle, whereas the identical stretch
in eccentrically trained animals resulted in an enhancement of
force equal to 54% over the control isometric (despite no
increase in muscle size; Fig. 2B; Ref. 11). This large increase in
the “dynamic stiffness” of the muscle could be useful not only
for increasing the magnitude of elastic recoil energy recovered
per stride, it could also be important in protecting the muscle
against eccentric injury.
Eccentrics: high force can cause muscle injury.
Because muscle produces force, any substantial shift in the
normal pattern of muscle use may result in muscle soreness if
either the nature or the magnitude of the force production
changes significantly (for example, a new exercise or novel
repeated task, etc.). Since muscle damage induced by exercise
is such a common phenomenon, the mechanisms responsible
for damage, recovery, and prevention have received a great
deal of attention. In identifying the responses of muscle to
damage and injury, these studies have contributed greatly to
the process of understanding muscle regeneration and how
muscle can be protected from damage. The most notorious
symptom after unaccustomed activity is a delayed onset of
pain, which is usually accompanied by the presence in the
serum of intracellular muscle enzymes or proteins, suggesting
damaged fibers (references in Ref. 12). The key functional
change, which provides the confirmation of impaired fibers
and hence muscle injury, is a decreased ability to produce
muscular force.
Perhaps because of the strong association of eccentric contractions
and muscle damage/injury, chronic eccentric training
has seldom been attempted experimentally. The norm in science
seems to be that much less evidence is required to establish
an idea as a “fact” than is required to dislodge an idea
once established (the “sufficiency of proof” axiom). Once
accepted, any observed cause-effect relationship becomes the
paradigm within which future experiments are designed and
interpreted. In fact, we have learned a great deal about how
muscle responds to damage/injury through this valuable model
of high-force, acute eccentric contractions. However, it is
essential to note that although eccentric contractions can and
often do result in muscle damage/injury, eccentric contractions
need not cause any muscle damage or injury whatsoever.
Unfortunately, the notion linking eccentric contractions and
muscle damage/injury persists and likely accounts for the
dearth of chronic eccentric training studies.
Just as any novel task can result in muscle soreness, regularly
repeating that task usually results in specific muscle accommodations
that function to protect against damage or even
soreness. It may not be eccentrics per se that are damaging but
rather that muscle damage results from exposure to any highforce,
novel muscle task. Hence, when eccentric contractions
are low force initially and increased in both force and duration
slowly over time, no injury occurs. Proposed explanations for
the apparent protective effect of repeated eccentrics (“the
repeated-bout effect”) include elimination of weak areas of
certain muscle fibers following an initial exercise bout,
changes in the recruitment of motor units with subsequent
exposures to eccentric contractions, and the formation of a
more resilient muscle structure (12, 14). We speculate that stiffening
of the muscle spring, though its exact nature may be
poorly described (see below), must also contribute significantly.
What is certain, however, is that muscle injury is not a
necessary prerequisite for these protective adaptations to
occur.
Eccentrics in rehabilitation and sport.
Chronic eccentric exercise is characterized by a unique
suite of attributes that result in several functional modifications
to muscle. Collectively, these changes may have profound
applications to patient populations and/or to those interested
in enhancing sport performance (Fig. 3).
Because much greater force can be produced eccentrically
than concentrically, it has the capability of “overloading” the
muscle, the goal of resistance strength training. Force of this
magnitude (in excess of the maximum isometric force) is only
possible during eccentric (vs. isometric or concentric) contractions.
However, not all eccentric contractions result in high
loads. If an exercise is designed to simply recover eccentrically
the forces generated concentrically, then that exercise does not
take advantage of this unique property. It is the electric motor
of the eccentric cycle ergometry that is generating the high
forces that the muscles oppose; these greatly exceed in magnitude
the muscular force that could be generated concentrically.
Furthermore, because eccentric muscle contractions occur
with very little metabolic cost, muscles contracting eccentrically
produce “more for less”; they generate high mechanical
muscle tensions at low metabolic costs. Eccentric contractions
not only produce the highest forces but do so at a greatly reduced oxygen requirement; an observation first documented
by the pioneering work of Bigland-Ritchie et al. (2), who
reported that the oxygen requirement of submaximal eccentric
cycling is only 1/6-1/7 of that for concentric cycling at the
same workload.
Thus eccentric training can increase the size and strength of
locomotor muscle (Fig. 2A) with very little demand on the cardiovascular
system (9). The magnitude of observed increases in
both strength and fiber area with eccentric training often
exceeds that seen following a similar duration of traditional
resistance strength training. With chronic eccentric training
there is also a resultant stiffening of the muscle spring that can
occur independent of, or in addition to, increases in size and
isometric strength of the muscle (11). In all probability, the
force enhancement and spring changes following chronic
eccentric training are likely due to both structural and neural
influences.
Application to rehabilitation and sport.
The potential application of chronic eccentric exercise to the
elderly and patients suffering from diseases that limit either the
uptake or delivery of oxygen, e.g., chronic obstructive pulmonary
disease or chronic heart failure, is alluring. These individuals
may be so severely exercise limited that walking may
be at or beyond their aerobic capacities, eliminating exercise
at intensities sufficient to prevent muscle wasting (sarcopenia).
Any exercise that requires a significant increase in ventilation
and cardiac output may be not only uncomfortable but for
many elderly impossible. Therefore, chronic eccentric training
may be a high-force yet nonstrenuous (low metabolic cost)
rehabilitation countermeasure with the potential to overcome
these skeletal muscle deficits and diminished ability to function
independently (Fig. 4). In addition, as a result of the
increased stiffness (tighter muscular spring) in muscle following
eccentric exercise, there may be improvements in sport
performance activities, such as jumping (13). In a preliminary
study comparing basketball players trained for 6 wk with either
high-force eccentric cycle ergometry or with a traditional
strength/power resistance program, we noted increases in vertical
jumping height in excess of 8% in the eccentrically
trained group, whereas those in a traditional resistance training
group showed no change in jump height.
Where is the muscle spring?
Because tendon was historically thought to be the source of
passive tension, the production of passive tension and storage
and release of elastic recoil energy in skeletal muscle had been
considered negligible (16). However, coupling the physiology
of lengthening muscles with the emergent knowledge of the
cytoskeletal proteins within the muscle cell, it is becoming
clear that these proteins contribute greatly to the storage of
elastic energy.
Likewise, intact fiber elasticity and passive tension production
were thought to reside predominantly in the extracellular
collagen matrix. However, within the physiological limits of
stretch most of the passive tension produced by a myofibril is
due to the elastic titin filament, whereas collagens and intermediate
filaments become important only with further stretch
(see references in Ref. 4).
Although normally studied under passive stretch, perhaps
titin contributes significantly to the production of active tension
when the muscle actively lengthens in resisting an external
load. Titin may contribute by enhancing elastic energy storage
and release and by maintaining sarcomere alignment,
ensuring efficient muscle contraction (16). Quantitative gel
electrophoretic mobility studies on SDS gels as well as recent
molecular studies have identified the existence of several isoforms
within the I band region of titin. Because there is only
one titin gene, titin isoforms are generated by the differential
splicing of the elastic region of the molecule. It is thought that
the expression of different titin isoforms could adjust the spring
properties of the fiber to the physiological demands placed on
the muscle to best maintain sarcomere structure (see references
in Ref. 7). A stiffer, shorter titin, therefore, may explain
the greater passive (spring constant) as well as active lengthening
force-producing capabilities following eccentric training.
Is there evidence supporting titin as a major contributor to
the muscle spring? We can compare quantitatively titin’s
potential contribution with the measured stretch potentiation
of the triceps muscle. By use of laser tweezers, the maximum
force has been estimated for individual titin molecules; published
values range from 5 to 70 pN. In estimating the possible
force that could be attributable to titin, we make the following
assumptions: 1) there are thought to be six titin molecules per
half myosin filament; 2) there are 7 × 108 thick filaments per
square millimeter of myofibril; and 3) we calculated the crosssectional
area of the triceps muscle of these rats to be 35 mm2.
Together, we estimate the total force attributable to the stretch
of titin to be
(5-70 pN/titin-1) × (6 titins/thick filament) × (7 × 108 thick/mm2) ×
(35mm2/cross section)
or a range of 0.74-10.3 N, which includes the range of
increased tension that we measured in the rat triceps muscle of
5-7 N, resulting from a stretch of a muscle under tetanic contraction.
Because this is a pinnate muscle, the functional crosssectional
area may be considerably higher, hence the maximum force attributable to titin may even exceed our estimated
values.
Titin’s role in lengthening contractions may also include the
initiation of cellular signaling to enhance cross-bridge recruitment
while decreasing the cost. Hence, a differential expression
of titin isoforms could alter the magnitude of elastic recoil
storage and subsequent utilization as well as effect crossbridge
cycling and efficiency.
Summary and conclusions.
Our view of muscle is usually that of a tension-producing
machine that, when shortening, provides the work necessary
for organisms to move about. However, movement also
requires that muscles function to absorb kinetic energy, fluctuations
that are inevitable during locomotion. Any time the
force acting on the muscle exceeds the force produced by the
muscle, the muscle will lengthen while producing force. During
normal locomotion, these eccentric contractions function
in two capacities: 1) they dissipate absorbed energy as heat, to
function as a damper or shock absorber, reducing the kinetic
energy via braking, and 2) conversely, the energy absorbed in
stretched muscle (and tendon) may be stored as elastic recoil
potential energy and subsequently recovered, allowing the
muscle to effectively function as a spring. This “spring property”
of muscle is both time dependent, which may be the rule
that sets stride frequency among mammals, and adaptable, the
muscle spring becoming stiffer in response to chronic eccentric
loading. Two unique properties of eccentric contractions
are physiologically fundamental. The energy cost for eccentric
contractions is unusually low and the magnitude of the force
produced is unusually high. As a consequence, muscles
exposed to chronic eccentric training respond with significant
increases in strength and size as well as alterations in the
spring properties of the muscle. These predictable responses
have both clinical and physical performance consequences.
Loss of muscle mass and strength are thought to be nearly
inevitable consequences of aging, accelerated by both heart
and respiratory disease. Chronic eccentric exercise, which
requires minimal energy and thus oxygen support, may be ideally
suited for both rehabilitation for this population as well as
increasing both strength and power in all individuals. Finally,
while the muscle spring properties are often attributed to collagen
and tendons (structures outside the muscle fiber), evidence
suggests that the gigantic protein titin may contribute
significantly to these important and adaptable functions of
skeletal muscle inside the fiber.