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Department of Biomedical Engineering, Cleveland Clinic Foundation, Cleveland, Ohio 44195-5254
ABSTRACT
INTRODUCTION
CONTRIBUTIONS TO PERFORMANCE
CONSEQUENCES OF ECCENTRIC CONTRACTIONS
NEURAL CONTROL OF ECCENTRIC CONTRACTIONS
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Enoka, Roger M. Eccentric contractions require unique
activation strategies by the nervous system. J. Appl.
Physiol. 81(6): 2339-2346, 1996.
Eccentric
contractions occur when activated muscles are forcibly lengthened. This
mode of muscle function occurs frequently in the activities of daily
living and in athletic competition. This review examines the
experimental evidence that provides the foundation for our current
understanding of the benefits, consequences, and control of eccentric
contractions. Over the past several decades, numerous studies have
established that eccentric contractions can maximize the force exerted
and the work performed by muscle; that they are associated with a
greater mechanical efficiency; that they can attenuate the mechanical
effects of impact forces; and that they enhance the tissue damage
associated with exercise. More recent evidence adds a new feature to
this repertoire by suggesting a new hypothesis: that the neural
commands controlling eccentric contractions are unique. Examination of this hypothesis is critical because the existence of such a control scheme would increase substantially the complexity of the strategies that the nervous system must use to control movement.
muscle work; exercise; movement control
INTRODUCTION HUMAN MOVEMENT IS ACCOMPLISHED by using muscles to
exert forces against objects and support surfaces. In Fig.
1A, for example, the
elbow flexor muscles can exert a torque to control the rotation of the
forearm about the elbow joint and thereby move the load represented by
the mass of the forearm, hand, and weight. When the muscle and load
torques are equivalent under such conditions, the load does not move,
and the elbow flexor muscles perform an isometric (constant length)
contraction. However, when the two torques are different, the load is
either raised or lowered. When the muscle torque exceeds the load
torque, the elbow flexor muscles shorten and perform a concentric
contraction to raise the load (Fig.
1B). In contrast, when
the muscle torque is less than the load torque, the activated muscle is
lengthened and performs an eccentric contraction to lower the load.
Eccentric contractions occur frequently in everyday activities and in
athletic competition. They are characterized by the ability to achieve
high muscle forces, an enhancement of the tissue damage that is
associated with muscle soreness, and perhaps require unique control
strategies by the central nervous system. The purpose of this article
is to review the experimental evidence that provides the foundation for
our current understanding of the benefits, consequences, and neural
control of eccentric contractions. The outcome of examining this
evidence is a new hypothesis: the neural commands controlling eccentric
contractions are unique.
CONTRIBUTIONS TO PERFORMANCE The actual force that a muscle can exert is not solely
a function of the activation level produced by a voluntary command but
also depends on the speed at which the muscle changes its length: the
so-called "force-velocity relationship" of muscle (Fig.
1C) (20, 50). The faster a muscle
shortens during a concentric contraction, the less the maximum force it
can exert. Conversely, the maximum force that a muscle can achieve
during a voluntary eccentric contraction is largely unaffected by
changes in the speed of lengthening, at least beyond an initial limit. In highly motivated subjects, the greatest forces occur during eccentric contractions (Fig. 1C).
Furthermore, eccentric contractions require lower levels of voluntary
activation by the nervous system (as indicated by the electromyogram)
to achieve a given muscle force (Fig.
1D) (4).
Although concentric contractions provide the propulsive force necessary
for such movements as running, jumping, throwing, and lifting, a common
human-movement strategy is to combine eccentric and concentric
contractions into a sequence known as the stretch-shorten cycle (26).
The prevalence of this movement strategy can probably be attributed to
several factors, such as its ability to maximize performance, to
enhance mechanical efficiency, and to attenuate impact forces (27, 43).
The stretch-shorten cycle involves an initial eccentric contraction
(typically a small-amplitude stretch at a moderate-to-fast velocity)
that is followed immediately by a concentric contraction (Fig.
2). Although inclusion of the stretch-shorten cycle in a movement can require substantial training (e.g., the movement known as the "clean" in Olympic
weightlifting), it appears in most movements without the need for
specialized training.
The most commonly recognized attribute of the stretch-shorten cycle is
its ability to maximize the work done by the muscle (6). This effect is
accomplished by the initial eccentric contraction producing a greater
muscle force at the beginning of the concentric contraction, compared
with a movement that involves only a concentric contraction. In the
example shown in Fig. 2, where the goal was to jump as high as
possible, the Achilles tendon force is plotted against muscle velocity
for two jumps; one jump (upper line) included a stretch-shorten cycle,
whereas the other jump involved only a concentric contraction. For
these two jumps, the Achilles tendon force at the beginning of the
concentric contraction (y-intercept) was
greater for the jump that included the stretch-shorten cycle. As a
result, the area under the concentric part of the force-velocity curve,
which represents the work done by the muscles during the propulsive
phase of the jump, was greater for the jump that used the
stretch-shorten cycle. Use of the stretch-shorten strategy can increase
the vertical-jump height of athletes by ~6 cm (28).
The inclusion of eccentric contractions in human movements, however, is
not limited to the stretch-shorten cycle. For example, consider the
task of raising and lowering the load shown in Fig. 1A. The lowering phase of this
movement, which is accomplished by an eccentric contraction of the
elbow flexor muscles, differs from the eccentric contraction in a
stretch-shorten cycle in the magnitude of the displacement experienced
by the muscle fibers. When the stretch-shorten cycle is used to
maximize the power produced by a muscle, the increase in muscle length
during the eccentric contraction is relatively small compared with that
required during the controlled lowering of a load. Such observations
suggest that there are at least two other reasons why eccentric
contractions are included in a movement: the greater mechanical
efficiency and the energy dissipation that can be achieved with
eccentric contractions. Komi (27; see also Ref. 48), for example,
reported that the mechanical efficiency (ratio of work performed to
energy expenditure) of a stretch-shorten movement performed by the legs on an inclined-sled apparatus was ~40% compared with the
conventionally cited 20-25% for concentric contractions. This
comparison suggests that it is more economical to perform a given
amount of work with a movement that involves a stretch-shorten cycle
than with one involving only a concentric contraction. Furthermore, the
ability of muscle to absorb energy during an eccentric contraction can be used to brake a movement and probably serves to protect less compliant elements (e.g., bone, cartilage, ligament) of the
neuromuscular system from damage due to high-impact forces and
repetitive low-level forces (27, 51). These considerations suggest that
the reasons for including an eccentric contraction in a movement may
vary across tasks but that the net effect is an enhancement of
performance.
CONSEQUENCES OF ECCENTRIC CONTRACTIONS Based on the cross-bridge theory of muscle contraction,
the force exerted by muscle is generated by the interaction of actin and myosin, which results in the myofibrillar proteins translating relative to one another. However, when the muscle fibers are lengthened in an eccentric contraction, the actomyosin bonds are probably disrupted mechanically rather than undergo an ATP-dependent detachment (15). This loading profile undoubtedly places high stresses and strains
on the involved structures and may contribute to the tissue damage that
occurs with eccentric contractions. Numerous structural abnormalities
are evident in muscle after exercise, especially exercise that involves
eccentric contractions. These abnormalities include
sarcolemmal disruption, dilation of the transverse tubule
system, distortion of myofibrillar components, fragmentation of the
sarcoplasmic reticulum, lesions of the plasma membrane, cytoskeletal
damage, changes in the extracellular myofiber matrix, and swollen
mitochondria (16, 43).
Accompanying these changes, there can be a gradual increase in the
soreness of the involved muscles that peaks 24-48 h after the
exercise. This effect is known as delayed-onset muscle soreness. It
occurs frequently after the performance of unfamiliar exercises that
include eccentric contractions and is attenuated as the exercises are
repeated in subsequent sessions (8, 13). Although some investigators
have attempted to establish an association between delayed-onset muscle
soreness and the exercise-induced remodeling of musculotendinous
tissues (7, 43), two observations suggest an alternative explanation.
First, delayed-onset muscle soreness appears to be related temporally
more to an inflammatory response than to the appearance of structural
damage (42). Second, gains in muscle strength that result from
eccentric contractions appear to be achieved by changes in the neural
activation of muscle rather than by an enhancement of the hypertrophic
response (9, 14). Although the role of neural mechanisms in strength
gains is not unique to eccentric contractions, the relative
significance of these mechanisms seems greater for this type of
activity. These findings suggest that the short- and long-term
consequences of including eccentric contractions in an exercise program
can be to induce structural adaptations in muscle, to activate an
inflammatory response, and to modify the neural commands used to
control the movement. Whereas these adaptations can also be induced by
other types of contractions, they seem to be maximized by eccentric contractions.
NEURAL CONTROL OF ECCENTRIC CONTRACTIONS In contrast to the decades of research on
performance-related aspects of eccentric contractions, it is only in
the last decade that much attention has been focused on the control of
eccentric contractions by the nervous system. The fundamental issue can be identified by asking the question, Does the nervous system issue a
specific command for an eccentric contraction? The most conservative
answer is that the nervous system simply grades the amount of muscle
activation, and hence the muscle torque, so that when the muscle torque
is less than the load torque, the result is an eccentric contraction
(Fig. 1B). In this scheme,
activation of the motoneurons innervating the muscle is independent of
the contraction type (viz. isometric, concentric, eccentric), and only
the activation intensity is modulated in accordance with the desired
muscle torque. This scheme would enable the nervous system to employ a
single strategy, such as the size principle (10), to activate the
involved motoneurons in the different types of muscle contractions.
Alternatively, if the activation sequence of motoneurons is different
for an eccentric contraction, as suggested by Nardone et al. (33), then
the response to the question must be that the nervous system does
indeed command an eccentric contraction, as distinct from a concentric
or an isometric contraction.
A separate control strategy for eccentric contractions, however, would
complicate the task of the nervous system to control movement. For
example, this would mean that for movements involving both concentric
and eccentric contractions (e.g., Fig.
1A) there must be change in the
control strategy at the transition between the two types of
contractions. Consistent with this possibility, we have found that
older adults have greater difficulty than younger individuals in
smoothly grading the force exerted by a hand muscle at the transition
from a concentric to an eccentric contraction as they raise and lower a
submaximal load (30).
Given the possibility that the control of eccentric contractions may be
different, we examine the evidence underlying the hypothesis that the
neural commands used to control eccentric contractions are unique. The
experimental evidence that addresses this hypothesis has been gleaned
from a number of protocols, such as those involving studies of maximum
voluntary contractions, motor unit behavior, motor-evoked potentials
and reflex testing, and muscle fatigue.
Fig. 1.
Mechanical and activation characteristics of eccentric contractions.
A: movement depends on ratio of muscle
and load torques. B: ratios of muscle
and load torques that produce isometric (no change in muscle length),
concentric (shortening), and eccentric (lengthening) contractions.
C: variation in maximum muscle force as a function of muscle velocity. D:
differences between concentric and eccentric contractions in required
muscle activation (EMG) to achieve a given muscle force.
[View Larger Version of this Image (18K GIF file)]
Fig. 2.
Idealized force-velocity relationship for calf muscles (soleus and
gastrocnemius) during 2 jumps to reach maximum height (see Refs. 7, 16,
21). In one jump (dashed-solid line), muscles performed a
stretch-shorten cycle. In other jump (dashed line), muscles performed
only a concentric contraction. Each jump began (based on ground
reaction force) at solid circle and concluded with takeoff at open
circle. Maximum force (measured at tendon), greater positive work (area
under force-velocity curve for velocity >0), and highest jump were
achieved with stretch-shorten cycle.
[View Larger Version of this Image (12K GIF file)]
Fig. 3.
Evidence of incomplete muscle activation despite a maximum voluntary
effort during eccentric contractions (see Refs. 41, 42).
A: variation in torque exerted by knee
extensor muscles on an isokinetic device during a maximum concentric
contraction (dashed line), eccentric contraction (solid
line), and an eccentric contraction with superimposed supramaximal
electric shocks (dotted line). B:
although maximum torque is greater during an eccentric contraction,
amplitude of EMG (muscle activation) was greater during concentric
contraction and increased with velocity.
[View Larger Version of this Image (12K GIF file)]
Another feature of motor unit behavior affected by the type of muscle contraction is the force at which a motor unit is recruited. This is known as the recruitment threshold and it is depicted in Fig. 4 as the force level at which each motor unit discharged its first action potential. For a given motor unit, the recruitment threshold is lower during nonisometric (concentric and eccentric) contractions compared with isometric contractions (45, 47). Because this reduction in threshold was evident even at very slow limb velocities (1.5°/s), it is probably not caused by the mechanical properties of muscle, as expressed in the force-velocity relationship (45). Furthermore, the decline in threshold does not appear to depend on sensory feedback, as it was not observed during contractions that the subjects intended to be isometric but which the investigators allowed to be nonisometric (44). These findings suggest that the change in the recruitment threshold of motor units during nonisometric contractions is mediated by descending signals from the brain. The neural commands associated with eccentric contractions not only alter the recruitment order, discharge rate, and thresholds of motor units within a muscle but also influence the relative activity of motor units among synergist muscles (39). For example, Nakazawa et al. (32) found that the EMG activity in brachioradialis relative to biceps brachii during concentric contractions was greater than that during eccentric contractions at longer muscle lengths (more extended elbow joint). As a result, the ratio of EMGs in brachioradialis and biceps brachii changed as a function of elbow joint angle for eccentric but not concentric contractions. Nardone and Schieppati (34) observed a similar interaction between soleus and lateral gastrocnemius for the task shown in Fig. 4. The selective recruitment of the fast-twitch muscle lateral gastrocnemius over the slow-twitch soleus has been reported previously for the paw-shake response performed by the cat hindlimb (40). This is a rapid movement that involves all segments of the leg and requires significant eccentric contractions to control the intersegmental dynamics (41). Perhaps the selective recruitment of lateral gastrocnemius is necessary because of the need to involve eccentric contractions. On the basis of these differences, the neural commands for eccentric contractions appear to be unique because they specify which motor units should be activated, how much they should be activated, when they should be activated, and how this activity should be distributed within a group of muscles. Motor-evoked potentials. The hypothesis that the neural commands for eccentric contractions are unique is underscored by the observation that the potentials evoked in muscle by transcranial stimulation differ for concentric and eccentric contractions (1). When subjects exerted forces or lifted loads that required comparable levels of EMG, the area (expressed in mV · ms) of the motor-evoked potential in brachioradialis was greater for concentric contractions compared with isometric contractions. In contrast, the size of the motor-evoked potentials was less in both brachioradialis and biceps brachii during eccentric contractions compared with isometric contractions. Furthermore, the amplitude of the Hoffmann (H) reflex evoked in brachioradialis by electrical stimulation of the radial nerve was modulated in a similar manner, such that it was greatest during concentric contractions and least during eccentric contractions (see also Ref. 38). Because the variation in the evoked potentials across the contraction types was similar for the cortical (transcranial) and peripheral (H reflex via the radial nerve) stimuli, it is likely that the effect was mediated by a mechanism located in the spinal cord. Abbruzzese et al. (1) proposed that subtle changes in cortical excitability may modulate the response of the motoneurons to synaptic input and thereby produce changes in motor unit behavior. For example, the descending signals associated with an eccentric contraction may include a component that modifies the excitability of the motoneurons so that an input signal directed to the motoneuron pool causes different members of the population to be activated. Perhaps eccentric contractions involve a reduced excitability of smaller motoneurons (1). Muscle fatigue. One functional consequence of the specificity in neural commands for the different types of muscle contractions is the effect on muscle fatigue [for issues related to strength training, see reports by Hortobágyi et al. (21, 22)]. Most studies have found that the decline in muscle force is less during fatiguing protocols involving voluntary eccentric contractions compared with concentric contractions. For example, Tesch et al. (46) had subjects perform three sets of 32 maximal contractions with the knee extensor muscles on an isokinetic device and reported that the decline in force was negligible when the task involved only eccentric contractions but decreased by 34-47% in each set for concentric contractions (Fig. 5). Furthermore, the EMG for the vastus lateralis and rectus femoris muscles, which was lower for the eccentric contractions, increased in each set of maximal contractions for both the concentric and eccentric conditions (Fig. 5). This effect appears to be robust over a range of speeds (30-180°/s) and ranges of motion (70-90°) for the knee extensor muscles on an isokinetic device (11, 18, 36) but not for the leg-press task (29).
, Eccentric contractions; 
,
concentric contractions.
The significance of the neural commands in the observed behavior during voluntary fatiguing contractions is underscored by a comparison with the performance when the muscles are activated by percutaneous electrical stimulation. Binder-Macleod and Lee (5) examined the fatigability of the quadriceps femoris muscles during evoked concentric and eccentric contractions performed on an isokinetic device. For both conditions, the stimulator output (10 pulses at ~14 Hz) was set to elicit a force that was ~20% of the maximum force that could be exerted during a voluntary isometric contraction. The protocol involved 180 contractions, each performed at a rate of 100°/s over a 70° range of motion about the knee joint. The force exerted by the quadriceps femoris declined during both the concentric and eccentric contractions (Fig. 6). For the concentric contractions, the force decreased by ~40% during the first 40 contractions and then remained constant. In contrast, the force declined linearly by about the same amount during the eccentric contraction protocol. Thus a muscle can experience fatigue during an eccentric contraction provided there is sufficient activation.
The difference in the neural commands for eccentric and concentric contractions is further demonstrated by the effect on a limb that does not participate in the fatigue test. Owings and Grabiner (36) had subjects perform a single-leg protocol in which the knee extensor muscles performed maximal eccentric or concentric contractions on an isokinetic device (30°/s). Before and after the fatiguing contractions, the subjects performed maximal contractions with the uninvolved leg. For the subjects who performed concentric contractions, the force exerted by the uninvolved knee extensors during a maximum concentric contraction was not altered by the fatigue task. In contrast, the subjects who performed the eccentric contractions experienced an 11% increase in the maximum force exerted by the uninvolved knee extensors during an eccentric contraction immediately after the fatigue task. This finding suggests that the series of eccentric contractions was associated with a facilitation of the neuronal circuitry, perhaps at the spinal level, that controls the homologous muscles in the uninvolved leg. A similar effect was not observed during the concentric contractions. Conclusion. Compared with isometric and concentric contractions, eccentric contractions appear to require unique activation strategies by the nervous system. The experimental evidence supporting this hypothesis includes the reduced activation of muscle during maximum eccentric contractions, an altered recruitment order of motor units during submaximal eccentric contractions, a decrease in the size of the potentials evoked in muscle by transcranial and peripheral nerve stimulation during eccentric contractions, and a greater resistance to fatigue (decline in force) during repeated contractions. Variation in the neural strategy may be accomplished by modulation of the relative excitability within the populations of motoneurons innervating a muscle, its synergists, and the contralateral homologous muscle. The principal functional outcome of the unique activation scheme may be to maximize the activity and thereby preserve the health of high-threshold motor units. These motor units are used minimally during daily activities but are essential for intense athletic competition and for emergency movements that require high levels of muscle power.
ACKNOWLEDGEMENTS
I am grateful to Drs. Jacques Duchateau (University of Brussels), Robert G. Gregor (Georgia Institute of Technology), Richard L. Lieber (University of California, San Diego), T. Richard Nichols (Emory University), and Douglas R. Seals (University of Colorado at Boulder) for their comments on a draft of the manuscript.
FOOTNOTES
Address for reprint requests: R. M. Enoka, Dept. of Kinesiology, Univ. of Colorado, Boulder, CO 80309-0354.
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