Sports Med 2006; 36 (11): 977-999

REVIEW ARTICLE 0112-1642/06/0011-0977/$39.95/0

 2006 Adis Data Information BV. All rights reserved.

The Stretch-Shortening Cycle

A Model to Study Naturally Occurring
Neuromuscular Fatigue
Caroline Nicol,1 Janne Avela2 and Paavo V. Komi2
1 Department of Physiology of Physical Activity, UPRES-EA 3285, University of the
Mediterranean, Marseilles, France
2 Neuromuscular Research Center, Department of Biology of Physical Activity, University of
Jyväskylä, Jyväskylä, Finland

Contents
Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 977
1. The Stretch-Shortening Cycle (SSC) as a Model to Study the Interaction Between Neural,
Mechanical and Structural Events . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 978
2. Definitions of Fatigue as They Apply to Repeated SSC Loading . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 982
3. Bimodal Response of Neuromechanical Parameters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 983
3.1 Basic Response . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 983
3.2 ‘Time-Dependent’ Effect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 984
3.3 ‘Testing Task-Dependent’ Effect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 986
4. Are Contralateral Effects Possible? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 987
5. Do All Skeletal Muscles Respond Similarly to SSC Exercise? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 988
6. Potential Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 989
6.1 Structural Changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 989
6.2 Neural Adjustments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 991
6.2.1 Supraspinal Fatigue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 991
6.2.2 Alteration in the Fusimotor-Muscle Spindle Function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 992
6.2.3 Reflex Adjustments of the Neural Activation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 994
7. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 995

Abstract Neuromuscular fatigue has traditionally been examined using isolated forms of
either isometric, concentric or eccentric actions. However, none of these actions
are naturally occurring in human (or animal) ground locomotion. The basic
muscle function is defined as the stretch-shortening cycle (SSC), where the
preactivated muscle is first stretched (eccentric action) and then followed by the
shortening (concentric) action. As the SSC taxes the skeletal muscles very
strongly mechanically, its influence on the reflex activation becomes apparent and
very different from the isolated forms of muscle actions mentioned above. The
ground contact phases of running, jumping and hopping etc. are examples of the
SSC for leg extensor muscles; similar phases can also be found for the upper-body
activities. Consequently, it is normal and expected that the fatigue phenomena
should be explored during SSC activities.
The fatigue responses of repeated SSC actions are very versatile and complex
because the fatigue does not depend only on the metabolic loading, which is
978 Nicol et al.

reportedly different among muscle actions. The complexity of SSC fatigue is well
reflected by the recovery patterns of many neuromechanical parameters. The basic
pattern of SSC fatigue response (e.g. when using the complete exhaustion model
of hopping or jumping) is the bimodality showing an immediate reduction in
performance during exercise, quick recovery within 1–2 hours, followed by a
secondary reduction, which may often show the lowest values on the second day
post-exercise when the symptoms of muscle soreness/damage are also greatest.
The full recovery may take 4–8 days depending on the parameter and on the
severity of exercise. Each subject may have their own time-dependent bimodality
curve.
Based on the reviewed literature, it is recommended that the fatigue protocol is
‘completely’ exhaustive to reduce the important influence of inter-subject varia-
bility in the fatigue responses. The bimodality concept is especially apparent for
stretch reflex responses, measured either in passive or active conditions. Interest-
ingly, the reflex responses follow parallel changes with some of the pure mechani-
cal parameters, such as yielding of the braking force during an initial ground
contact of running or hopping. The mechanism of SSC fatigue and especially the
bimodal response of performance deterioration and its recovery are often difficult
to explain. The immediate post-exercise reduction in most of the measured
parameters and their partial recovery 1–2 hours post-exercise can be explained
primarily to be due to metabolic fatigue induced by exercise. The secondary
reduction in these parameters takes place when the muscle soreness is highest.
The literature gives several suggestions including the possible structural dam-
age of not only the extrafusal muscle fibres, but also the intrafusal ones. Tempora-
ry changes in structural proteins and muscle-tendon interaction may be related to
the fatigue-induced force reduction. Neural adjustments in the supraspinal level
could naturally be operative, although many studies quoted in this article
emphasise more the influences of exhaustive SSC fatigue on the fusimotor-muscle
spindle system. It is, however, still puzzling why the functional recovery lasts
several days after the disappearance of muscle soreness. Unfortunately, this and
many other possible mechanisms need more thorough testing in animal models
provided that the SSC actions can be truly performed as they appear in normal
human locomotion.

1. The Stretch-Shortening Cycle (SSC) as
a Model to Study the Interaction
Between Neural, Mechanical and
Structural Events
Before discussing stretch-shortening cycle (SSC)
fatigue, it needs to be explained why SSC fatigue
should be discussed separately from other forms of
muscle fatigue. There is no doubt that much before
the true SSC studies had started, muscle fatigue had
been widely explored for decades. These studies
have introduced a vast amount of information and
several mechanisms have been proposed and proven
to explain the various fatigue events (for an excel-
lent review, see Gandevia[1]). This information has,
however, come primarily from studies utilising iso-
lated forms of muscle action (isometric, concentric
or eccentric) in human and animal models. Many of
these fundamental fatigue mechanisms may not be
transferred directly to SSC fatigue without consider-
ing the special features of the SSC in general and the
nature of SSC fatigue loading in particular. Al-
though SSC fatigue is a relatively young object of

 2006 Adis Data Information BV. All rights reserved. Sports Med 2006; 36 (11)
The Stretch-Shortening Cycle
research, it has now been explored enough so that its
peculiarities can be presented in a review form.
To begin our review of SSC fatigue, we would
like to emphasise that SSC-type muscle function is
not the same as eccentric muscle contraction or
action. The SSC includes by definition an eccentric
component, but its loading mode is different from
traditionally accepted eccentric action. Consequent-
ly, the results obtained from studies utilising these
two different modes of muscle function can be quite
different. The impact loads and the nature of stretch-
es involved in the active braking phase of SSC are
usually very fast, of short duration and controlled
simultaneously by reflex and central neural path-
ways. In addition, the metabolic loading of SSC
exercise may differ considerably from those of pure
concentric and eccentric exercises. Thus, we are
dealing with a complex activity, which in itself is
often difficult to understand in all its features. Ex-
tending the thoughts to the SSC fatigue requires
rearranging of the traditional thinking of the possi-
ble mechanisms involved. In the following few
paragraphs we try to start with characterising the
SSC action with emphasis on its natural form in
every day activities. Pure eccentric and pure concen-
tric muscle actions are not natural forms of exercise.
In order to examine the functional loading of the
human body during exercise, the mode of exercise
or activity should be as natural as possible. Specifi-
cally, and very importantly, this requirement applies
to the neuromuscular system and its important ‘mo-
tor’, the skeletal muscle. If, for example, the func-
tion of the human skeletal muscle is measured under
pure isometric, concentric or eccentric actions, the
principle of natural conditions will not apply. This
does not mean that numerous physiological and
biomechanical studies performed under these isolat-
ed conditions will have no meaning or relevance.
Many fundamental concepts of muscular exercise
have been obtained with measurements of these
isolated actions, either in human or animal studies.
The same is true for many key metabolic changes
observed during isometric fatigue.[1] In locomotion,
however, exercise seldom involves a pure form of
these types of muscle actions. The natural variation
 2006 Adis Data Information BV. All rights reserved.
979
of muscle function is more often, if not always, a
SSC, and thus this model provides a good basis from
which to study neuromuscular fatigue.
Two important aspects to characterise SSC are
related to the variation of: (i) the pre-activation; and
(ii) of the subsequent braking and push-off parts of
the functional phase of a given SSC movement (e.g.
ground contact for the leg extensor muscles during
running). The neural control, including central and
peripheral components, plays a key role in the opti-
mal muscle activation. It may naturally be related to
corresponding adjustments in mechanical behaviour
and structural modifications of the muscle-tendon
unit. This happens especially in the phase of muscle
damage, a common feature in intensive and exhaus-
tive SSC exercise. The neural adaptations are some-
times so dramatic that they have influence on the
overall control of movement of the exercising mus-
cle. Other aspects that need to be addressed regard-
ing SSC fatigue are length changes in muscle versus
tendon and the role of stretch reflexes in stiffness
regulation in the course and following SSC fatigue.
These problems then lead to the description of how
muscle-tendon elasticity is adapted to the different
phases of SSC fatigue itself and during its recovery.
The SSC of muscle function comes from the
observation that body segments are periodically
subjected to impact or stretch forces. Running,
walking and hopping are typical examples in human
locomotion of how external forces (e.g. gravity)
lengthen the muscle. In this lengthening phase, the
muscle is acting eccentrically, thereafter a concen-
tric (shortening) action follows. The true definition
of eccentric action indicates that the muscles must
be active during stretch. This combination of eccen-
tric and concentric actions forms a natural type of
muscle function called the SSC (figure 1).[2-4] The
braking (or impact) phases are naturally different
depending on the activity. Cross-country skiing is a
typical form of locomotion in which the braking
phase is long and relatively smooth in both free and
traditional techniques. In the latter technique, the
vertical force (Fz) ski forces seldom exceed 1.5
times bodyweight.[5] Consequently, the repeated
SSCs in this event will have much smaller function-
Sports Med 2006; 36 (11)
980
a b c
Preactivation Stretch Shortening
Fig. 1. In human walking, hopping and running, considerable im-
pact loads occur when contact takes place with the ground. This
requires preactivation from the lower-limb extensor muscles before
the ground contact to make them ready to resist the impact (a) and
the active braking phase (b). The stretch phase is followed by a
shortening (concentric) action (c) [reproduced from Komi,[3] with
permission].
al and structural (and damaging) effects on muscle
when compared with running, for example (table I).
In running, the impact peak is much higher and the
duration of the braking (‘eccentric’ phase) very
short (50–120ms). The repeated loading will conse-
quently have greater stretch-induced effects than in
cross-country skiing. These two events represent a
good comparison, especially regarding the long-
term fatiguing effects. It is not possible for a runner
to repeat the marathon race in 1-week intervals due
to the typical SSC fatigue-induced structural dam-
age. In cross-country skiing, even when performed
with the same intensity and duration as the marathon
run race, the recovery processes from possible mus-
cle damage take place much faster and the athletes
are usually ready to repeat the 50km race after a few
days only. This emphasises that the SSC, when
repeated long enough and with high intensity,
causes reversible neural, structural and mechanical
disturbances, severity and duration of which are
dependent on the nature of the SSC task.
In the SSC, the sequence in muscle function
(stretch-shortening) also involves the important fea-
tures of preactivation and variable activation. SSC
muscle function has a well recognised purpose: en-
hancement of performance during the final phase
(concentric action) when compared with the isolated
concentric action. This can be demonstrated in iso-
lated preparations with constant electrical stimula-
 2006 Adis Data Information BV. All rights reserved.
Nicol et al.
tion,[32,33] in animal experiments with natural and
variable muscle activation[34] and in maximal effort
conditions of human SSC actions.[33,35] Considerable
effort has been devoted to explain the mechanisms
for force and power potentiation during a SSC.
Cavagna et al.[32] were among the first to argue that
this enhancement is primarily from stored elastic
energy. Since that time, many additional alternative
explanations have been presented.[36-38] However,
no convincing evidence has been presented that
negates elasticity as an important element in force
potentiation during a SSC.
The schematic presentation of figure 1 takes into
consideration the common assumption that in a SSC
the contractile and tensile elements are stretched
during the eccentric phase. There are, however, ar-
guments in the literature suggesting that the contrac-
tile component may maintain a constant length[39,40]
or even shorten[41] during the early phase of ground
contact. As will be discussed in section 5, it is
important to know that the fascicles and tendinous
tissue components may not necessarily stretch (and
shorten) in phase with the entire muscle-tendon
unit.[42] It is now well confirmed that while the
fascicle length changes are clearly muscle and
movement specific, the tendinous tissue has similar
characteristics, but not necessarily in phase with the
contractile tissue.[43] The observation of intensity
dependence of changes in these muscle-tendon unit
components adds an additional problem to the com-
plexity of understanding the mechanism of neuro-
muscular fatigue during SSC. In this regard, the
interaction between contractile and tendinous tis-
sues becomes critical when, for example, high-in-
tensity SSC exercise is continued until complete
exhaustion.[25]
The present article reviews the work of SSC
fatigue performed during human experiments. Many
of the studies come from our laboratory, but effort
has been made to also refer to work of the others.
The SSC model will be introduced for fatigue exper-
iments where its unique loading characteristics can
be used to examine neuromuscular fatigue in a very
comprehensive way. The article is a follow-up of
our earlier reviews on the topic.[4,38,44]
Sports Med 2006; 36 (11)
 2006 Adis Data Information BV. All rights reserved.

The Stretch-Shortening Cycle

Table I. Relative changes induced by fatiguing stretch-shortening cycle (SSC) exercises in the peak values of maximal voluntary contraction (MVC) and electrically induced twitch
response in a passive condition (twitch)a
Study SSC fatiguing protocols MVC Twitch
after 20 sec–1h 2h 1–2d 4–8d after 20 sec–1h 2h 1–2d 4–8d
Acute recovery phase
Davies and Thompson[6] 4h treadmill run –35
Millet et al.[7]
65km ultramarathon run –30 18
Forsberg et al. [8] 97km (60-mile) XC skiing race –28
Place et al.[9] 5h treadmill run at 55% MAV –28 –30 18 0
Nicol et al.[10] Marathon run –26
Millet et al.[11] 30km running race –24 –8
Gollhofer et al.[12,13] 100 submax. intermit. arm rebounds –23
Lepers et al.[14] 2h run at 75% MAV –19
Strojnik and Komi[15] Exhaustive submax. leg rebounds –18 –12
Martin et al.[16] Downhill treadmill run –15 –15
Davies and White[17] 1h treadmill run at 80% –9 –13
Millet et al.[18] Ski skating marathon –8 8
Skurvydas et al.[19] 100 max. drop jumps 21 21
Viitasalo et al.[20] 65km XC skiing race –10

Delayed recovery phase

Pullinen et al.[21] Marathon run –38 –25
Kuitunen et al.[22] Max. and exhaustive submax. leg rebounds –30 NS –14 NS
Avela et al.[23] Marathon run –30 –17 NS NS
Kuitunen et al.[24] Max. and exhaustive submax. leg rebounds –29 NS NS NS –38 NS NS NS
Ishikawa et al.[25] Max. and exhaustive submax. leg rebounds –25 –5 –10 NS
Nicol et al.[26] 10km run –25 NS NS NS NS
Max. and exhaustive submax. leg rebounds –25 –60 –25 NS NS
Regueme et al.[27] Exhaustive intermit. submax. leg rebounds –20 –24
Dousset et al.[28] Max. and exhaustive submax. leg rebounds –20 NS –6 NS
Skurvidas et al.[29] –23 –49 –14 –70 –62 –34
Sports Med 2006; 36 (11)

100 intermit. drop jumps

100 continuous drop jumps –20 –15 –8 –48 –48 –27
Regueme et al.[30] Exhaustive intermit. submax. leg rebounds –13 –34
Martin et al.[31] One-legged downhill treadmill run –14 –14 –15 –45 NS NS
a Some of the values have been estimated from the data presented in the individual articles.

981
intermit. = intermittent; MAV = maximum aerobic velocity; max. = maximal; NS = not statistically significant; submax. = submaximal; XC = cross-country.
982
2. Definitions of Fatigue as They Apply to
Repeated SSC Loading
Gandevia[1]has given an extensive discussion on
the problems related to defining fatigue correctly.
Without going into the details of these problems, we
try to keep in mind two widely used definitions: (i)
fatigue refers to failure to maintain the required or
expected force;[45] or (ii) fatigue is failure to contin-
ue working at a given exercise intensity.[46] As early
as 1979, Asmussen[47] defined fatigue during the
course of an exercise as: “decrease in performance
capacity of muscles, when they have been active for
a certain period of time, usually evidenced by a
failure to maintain or develop a certain expected
force or power”. In the following discussions of SSC
fatigue, we will primarily rely on the definitions of
Gandevia,[1] although the majority of the studies to
be referred to have concentrated on the ‘complete
exhaustion concept.’
As already mentioned, in section 1 intensive and/
or unaccustomed eccentric or SSC-type exercise
results often in reversible muscle damage. This is
associated with delayed-onset muscle soreness, and
with proprioceptive and neuromuscular impairments
that may last for several days. After SSC exercises,
these neuromuscular perturbations are typically as-
sociated with large acute and delayed changes in
muscle mechanics and activation that result in major
consequences on joint and muscle stiffness regula-
10
(n = 5) (n = 6)
(n = 3) (n = 11)
0 As will be emphasised in sections 3.1 and 3.2, the
-10
D% Pre
(n = 13)
-20
-30
-40
-50
Pre Post 20 sec–1h 2h 1–2d 4–8d
Testing time
Fig. 2. Summary graph of maximal voluntary contraction (MVC)
from the studies that followed the stretch-shortening cycle recovery
phase until 4–8 days post-exercise (Post). The number of studies
varied from 3 to 13 depending on the testing time as indicated in the
figure. To calculate the averaged changes (±SD) in MVC compared
with pre-exercise (Pre), nonsignificant data have been replaced by
zero.
 2006 Adis Data Information BV. All rights reserved.
Nicol et al.
EMG
M1
SR
(n = 3) (n = 6)
0
(n = 5)
(n = 3)
(n = 5) (n = 5)
-10
D% Pre
(n = 8)
(n = 8)
(n = 5)
(n = 5)
-20
(n = 5)
(n = 5)
-30
Pre Post 2h 1-2d 6-8d
Testing time
Fig. 3. Summary data from the studies listed in table II showing the
bimodality of electromyographic (EMG) activity changes during re-
covery from stretch-shortening cycle fatigue. Both acute (immedi-
ately after) and delayed (up to 6–8 days) decreases were observed
in mean voluntary activation (EMG) in a maximal voluntary contrac-
tion (MVC) test, in short-latency reflex amplitude (M1) in a submax-
imal rebound test, and in stretch-reflex amplitude (SR) measured in
passive dorsiflexion test. The number of studies is indicated in each
measurement point (see table II) Post = post-exercise; Pre = pre-
exercise.
tion, especially in SSC-type performances.[4] These
fatigue-induced performance deteriorations and sub-
sequent long-term recovery usually take place in a
bimodal fashion (figure 2, figure 3). In this bimodal-
ity, the acute metabolically induced reduction is
followed during a few hours by a short-term recov-
ery, which is in turn followed by a secondary reduc-
tion with longer lasting recovery. The bimodality
concept is not always valid, especially if the SSC
fatigue has not been exhaustive enough.
fatigue response, especially that of metabolic and
neural nature, is very individual and thus the proto-
cols using fixed exercise duration may not reveal
true effects of fatigue. It is very often possible that
because of this individual response, and in contrast
to the observed inhibitory neural effects after ex-
haustive SSC exercises,[4] the fixed fatigue protocol
may cause facilitatory responses in most subjects.[48]
Additional problems come from the choice of the
‘fatigue parameters’. Very often the submaximal
tests reveal facilitation of performance, whereas
tests involving high-intensity maximal or near maxi-
Sports Med 2006; 36 (11)
The Stretch-Shortening Cycle 983
Table II. Relative changes in the voluntary activation (electromyogram [EMG] during maximal voluntary contraction [MVC]) and in the short-latency stretch-reflex component (EMG

mal tests reveal performance deterioration more

–38/NM

–33/NM
NS/NM
NM/NS
NS/NS

NS/NS
clearly.[12]
4–8d
amplitude measured in either passive stretch-reflex amplitude [SR] or active [M1] stretching conditions) after fatiguing stretch-shortening cycle (SSC)-type exercisesa

3. Bimodal Response of
–32/–34

NM/–19

–32/NM
–44/NS

NS/NM
NM/NS
NM/–7
Neuromechanical Parameters
0/NM
1–2d

3.1 Basic Response

NS/NM
NS/NM
NM/NS
NS/NS

0/NM
Passive SR and/or M1

0/0
2h

SSC fatigue causes considerable changes in sev-

eral neuromechanical parameters. The exact conse-
quences of these changes are often difficult to assess
–46/–34

–19/–37
–30/NM

–32/NM

because of differences in the protocols used. The

NS/NM
NM/NS
NM/–9
NM/0
after

literature review (table I) shows that approximately

half of the studies have examined the acute recovery
phase (up to 2 hours post-exercise), whereas in the
4–8d
NS
NS
NS
NS
NS

other half the follow-up was extended to the delayed

recovery phase (up to 7 days).
1–2d

Most of the SSC fatiguing studies (24 of 26) have

–14
–15

–46
–23
0

NS
NS

observed an immediate (22 ± 11%) drop in maximal

voluntary contraction (MVC). When re-examined 2
max. = maximal; NM = not measured; NS = not statistically significant; submax. = submaximal.
–29
Mean voluntary EMG

NS
NS
NS
NS
2h

hours post-exercise, i.e. when most of the metabolic

Some of the values have been estimated from the data presented in the quoted articles.

parameters had recovered, a partial or even com-

after–30 sec

plete recovery of MVC was frequently observed.

From the 12 studies that re-examined this parameter
during the subsequent days (figure 2), eight studies
–39
–26
–20
–17
–5
0
0

demonstrated a secondary decline 1–2 days post-

exercise.
Max. and exhaustive submax. leg rebounds
Max. and exhaustive submax. leg rebounds
Max. and exhaustive submax. leg rebounds
Max. and exhaustive submax. leg rebounds

10km run or exhaustive submax. rebounds

Exhaustive intermit. submax. leg rebounds
Exhaustive intermit. submax. leg rebounds

The respective analysis of an ‘electrically evoked

twitch response’ in a passive testing condition re-
Exhaustive submax. leg rebounds

Exhaustive submax. leg rebounds

vealed in 8 of 12 studies an acute 8–70% reduction

in the peak twitch torque (table I). Large immediate
increases were reported only after ultralong (5–8.5
SSC fatiguing protocols

hours) SSC performances. From the four studies that

have examined the delayed fatigue effects, three of
them showed a complete recovery already 1–2 days
Marathon run

post-exercise.[24,26,31] However, in the fourth

study,[29] the 50–70% acute reductions measured
after two different rebound protocols were not fully
recovered on day 2. With regard to the twitch poten-
tiation in ultralong SSC exercise, Place et al.[9] sug-
Regueme et al.[30]
al.[27]

gested that it may be related to an increase in sensi-

Kuitunen et al.[22]
Kuitunen et al.[24]

Ishikawa et al.[25]
al.[28]

Horita et al.[51]
Avela et al.[23]

tivity of the myosin light chain phosphorylation that

Nicol et al.[26]
Nicol et al.[52]
Regueme et
Dousset et

could also increase the rate of force production.

Whether this can be truly demonstrated to occur is
Study

an open question, especially for SSC exercise. How-

a

 2006 Adis Data Information BV. All rights reserved. Sports Med 2006; 36 (11)
984
Pre-marathon Post-marathon
**
VL
*
SOL
**
Fz
200ms
Fig. 4. Parallelism of the immediate stretch-shortening cycle fatigue
effects (marathon run) on the short-latency stretch-reflex (M1) peak
of the vastus lateralis (VL) and soleus (SOL) muscles and the
vertical force (Fz) of the force plate on the sledge jumping appara-
tus. Please note the disappearance of the M1 response after the
marathon and the concomitant yielding in the force curve ex-
pressed as amplitude (arrow) of the force reduction upon impact
with the force plate (reproduced from Avela et al.,[23] with permis-
sion). * p < 0.05; ** p < 0.01.
ever, it emphasises further the importance of the task
dependence as will be discussed in section 3.3.
Changes in ‘neural activation’ of both global and
reflex electromyographic (EMG) responses revealed
varying strategies during the SSC fatigue recovery.
This suggests existence of both ‘fatigue-dependent’
(or ‘time-dependent’) and ‘testing task-dependent’
neural adjustments to the contractile failure.[4] Sec-
tions 3.2 and 3.3 compare the neural activation
changes reported by different SSC studies. Special
emphasis will be given to the most recent data.
3.2 ‘Time-Dependent’ Effect
The concept of ‘time-dependent’ effect has been
observed in several SSC fatigue studies, and the
findings vary from neural compensations of the con-
tractile failure to protective inhibitions of the fa-
tigued muscles.[12,30,49,50] In the case of a longer post-
exercise follow-up, this effect is reinforced by the
general observation of a bimodal recovery (table II
and figure 2). In particular, the mean voluntary
 2006 Adis Data Information BV. All rights reserved.
Nicol et al.
activation (measured in the maximal MVC test) as
well as the stretch-reflex EMG response (measured
in either passive or active stretching conditions)
decreased immediately post-exercise, recovered
partially within the next 30 minutes to 2 hours, and
decreased again 1–2 days later (figure 3).
The inter-individual variability may deserve a
comment, however, as reflex facilitation has been
reported for a few subjects in the acute recovery
phase (immediately after to 2 hours after exercise),
in both passive and active (M1) stretch reflex re-
sponses.[24,26] Depending on the study, this reflex
facilitation was followed either by a complete recov-
ery[26] or by a secondary inhibition on day 2.[24]
Based on these observations, it is emphasised that
the bimodal shape of recovery should not be gener-
alised to all subjects as ‘fast-recovering’ subjects
have also been observed in SSC fatigue studies.[26]
EMG modifications in the SSC testing tasks can
be central and/or reflex in nature. In both maximal
and submaximal SSC tasks, changes have been ob-
served in the centrally pre-programmed activation
(prior to ground impact) and in the active stretch-
reflex response (M1). In addition, significant rela-
tionships have been found between the fatigue-in-
duced changes in the preactivation and in the
postlanding stiffness.[53,54] Supporting the functional
role of a prolonged reduction in M1, Avela et al.[23]
showed a parallelism in bimodal trend of changes in
M1 and in tolerance to high ground impact loads
(figure 4). In the delayed phase of recovery,
Regueme et al.[27] demonstrated highly inter-corre-
lated drops in soleus muscle preactivation and in
short-latency stretch reflex (M1) response. These
findings are in agreement with the original sugges-
tions of Asmussen[47] and it is consequently a good
demonstration that changes in mechanical and neu-
ral parameters do occur in parallel after exhaustive
SSC exercise.
Neural adjustments resulting from the SSC fa-
tigue task may not, however, be always as straight
forward as shown in figure 3. The neuromuscular
system may adjust in the recovery phase to the
contractile failure in a more flexible way. For exam-
ple, Regueme et al.[30] demonstrated in submaximal
Sports Med 2006; 36 (11)
The Stretch-Shortening Cycle 985

SSC testing tasks varying neural changes immedi-
ately after and 2 days after an exhaustive SSC exer-
cise (figure 5). Immediately after exercise, large
increases in soleus muscle activation occurred both
during the preactivation and the early braking phase.
Differing from these observations immediately after
exercise, the increased soleus muscle preactivation
at 2 days after exercise was not associated with an
increased activation during the early braking phase,
but during the late push-off phase. This shift of
muscle activation may thus be considered to reflect
a neural strategy to protect the recovering muscles at
the 2-day point from the stressful stretching phase,
while securing the rebound performance by in-
creased work during the push-off phase. Further-
more, the 2-day test revealed a 36% increase in
gastrocnemius muscle preactivation. These results
are supported by the earlier SSC fatigue study of
Horita[54] who demonstrated progressive inter-mus-
cular compensations for the exercise-induced con-
tractile failure. Interestingly, the respective central
and reflex EMG components reported by Regueme
et al.[30] did not vary in a similar way along the
recovery period. Differing from the increase in cen-
tral activation (preactivation and 0–M1 periods) in
both immediately after and 2 days after an exhaus-
tive SSC exercise, the M1 reflex response showed a
trend of immediate and 2-day delayed reductions
(figure 5). This is in line with the bimodal decrease

Pre Preactivation
Post 0 to M1
1600
M1
Early braking
Late push-off
SOL EMG (mV)

1200
0.6

160 *
800
SOL EMG (D% Pre)

0.4
120
*
*
400 80
0.2
40

0 0 0
-200 0 200 400 600 800
-40
Fz (N)

Pre
2d 1600
SOL EMG (mV)

1200
0.6

800 160
0.4 *
SOL EMG (D% Pre)

120

400 80
0.2
40 *

0 0 0
-200 -100 0 100 200 300 400 500 600 700 800
-40
Time (ms) *
Fig. 5. The left figures show group averaged records of vertical force (Fz) and soleus (SOL) electromyographic (EMG) activity compared at
three measurement points after exhaustive stretch-shortening cycle exercise: pre-exercise (Pre), immediately after (Post) and 2 days post-
exercise (2d). The figures on the right present the relative EMG changes (histograms) for the preactivation, 0–M1 and M1 periods, the early
braking (first 200ms) and late push-off (last 200ms) of the contact phase. * p < 0.05, significantly different from the Pre absolute values
(reproduced from Regueme et al.,[30] with permission).

 2006 Adis Data Information BV. All rights reserved. Sports Med 2006; 36 (11)
986
0.4
SOL (mV)
0.2
Inhibition
0.0
200 0 200
Time (ms)
Fig. 6. Group (n = 10) averaged records of vertical force (Fz) and soleus (SOL) electromyographic activity compared at two measurement
points after exhaustive stretch-shortening cycle exercise (unpublished observations).
in stretch-reflex response reported after SSC exer-
cise (see table II).
3.3 ‘Testing Task-Dependent’ Effect
If the ‘time dependency’ is a factor to take into
consideration in SSC fatigue studies, the ‘testing
task-dependent’ effect should be equally considered.
The literature shows that in the isometric testing
condition, for example, most of the SSC fatigue
studies report significant declines in maximal force
and mean voluntary EMG activation (figures 2 and
3). From the few studies that have examined the
SSC fatigue effect on maximal dynamic perform-
ances, different effects may be observed depending
on the testing tasks. For example, when Nicol et
al.[55] used maximal SSC tests with high ground
impact (drop jump, five jumps and sprint) the per-
formances were impaired on average by 13% in the
acute recovery phase. When the SSC test (counter-
movement jump) did not include high impact or was
a pure concentric performance (squat jump), no
significant changes were observed. Similar differ-
ences have been observed in the delayed phase of
recovery by Horita et al.[56] who reported larger
performance decrements in the drop-jump than in
the squat-jump test.
The hypothesis of ‘testing task-dependent’ neural
adjustments to fatigue is further reinforced by the
 2006 Adis Data Information BV. All rights reserved.
Nicol et al.
Pre 1600
2d
1200
Fz (N)
800
400
0
400 600 800
opposite trend of changes recently reported in sub-
maximal[30] compared with maximal[22,27,53,56,57] re-
bound tests. In maximal drop-jump performances,
where stretch loads are high and muscle stiffness
must be well regulated to meet the external
loads,[4,57] fatigue is usually associated with an over-
all decrease in activation, with major reductions
during both preactivation and braking phases (figure
6).[27,53,56] In most cases, the reduced soleus muscle
preactivation was associated with soleus muscle
EMG reductions in the subsequent braking phase
and during the specific M1 stretch-reflex phase.
These observations support the existence of neural
attempts of protection of the fatigued muscle in
maximal drop-jump performance. In addition, they
support the findings of Komi and Gollhofer[38] who
found in tasks varying from sub- to supra-maximal
levels of ground impacts, that protective neural
mechanisms (reduced short, medium and long laten-
cy components of the stretch reflex) took place only
in the most extreme testing condition (falls on the
floor). In that study, the SSC exercise was per-
formed with arms on the sledge apparatus.
The previous discussion refers primarily to the
maximal testing conditions. The situation may be
different in the submaximal SSC rebound tests. For
example, large acute (+74%) and delayed (+79%)
increases in soleus muscle preactivation were ob-
Sports Med 2006; 36 (11)
The Stretch-Shortening Cycle
served in a submaximal SSC rebound task after a
similar fatiguing protocol (see figure 5). It is well
known that a link exists between the increases in
preactivation and impact peak.[12,13,58] In the SSC
fatiguing condition, a loss of tolerance to ground
impact occurs frequently.[12,13,23,55] In such a case, an
increased preactivation should be functionally detri-
mental in maximal rebound jumps, but useful in
submaximal rebound conditions. In this line, the
only SSC fatigue study that reported post-fatigue
increases in muscle preactivation in maximal drop-
jumps was characterised by large decreases in per-
formance.[57] Deviating slightly from this ‘general
rule’ of testing task dependency, Avela and Komi[53]
revealed large, but similar fatigue-induced reduc-
tions in preactivation in SSC performances per-
formed from submaximal (70%) and supramaximal
(130%) dropping heights, but in both cases with
maximal rebound effort. This would suggest that
SSC fatigue exercise allows greater variations in
neural adjustment when the rebound performance is
varied (sub-maximal vs maximal rebound height)
compared with the condition of varying stretch in-
tensity (sub- vs supra-maximal dropping height).
Importantly, however, although EMG analysis of
submaximal SSC tasks can reveal the existence of a
contractile failure, this may not necessarily be ob-
servable in the kinematic and kinetic analysis of the
movement. For example, Kyröläinen et al.[59] and
Finni et al.[60] observed no measurable kinetic and
kinematic changes at submaximal running speed
after a fatiguing 10km running exercise. It is very
likely that in order to observe true changes in these
parameters one may need to fatigue the subjects
more exhaustively, as was the case in the marathon
study of Nicol et al.[61] In their study, only those with
>40% reduction in the knee extensor MVC demon-
strated clear modifications of the running pattern.
Despite no change in the group averaged running
pattern, significant EMG increases were observed in
the leg extensor muscles during both braking and
push-off phases of the ground contact. In the sub-
maximal running tasks, the higher the testing veloc-
ity, the larger was the increase in neural activation
after the marathon run.[61]
 2006 Adis Data Information BV. All rights reserved.
987
In summary, our analysis of the relevant litera-
ture emphasises the flexibility of the neural adjust-
ments within and across homonymous muscles to
meet the functional requirement of the peripheral
system. Central and peripheral activation changes
may be opposite in a given task (central facilitation
vs peripheral inhibition). They may also vary de-
pending on the task intensity (maximal vs submax-
imal) and recover at different pace (acute vs
delayed).
4. Are Contralateral Effects Possible?
The preceding paragraphs have included material
with the assumption that the SSC fatigue effects are
primarily unilateral in case the exercise has been
performed with one limb only. There is, however,
information in the literature that could also imply
contralateral effects. Unilateral perturbations such
as musculoskeletal disorders, inflammation or mus-
cle pain have been reported to affect the contralater-
al side in pathological conditions in humans[62] and
in various experimental conditions in animals.[63,64]
Contralateral changes in humans are usually ob-
served in the case of chronic (>3 weeks) musculo-
skeletal disorders, suggesting the progressive devel-
opment of compensations along time. These obser-
vations raise the question as to whether contralateral
changes result from long-term adaptations in the
human behaviour, or whether short-term and/or re-
versible musculoskeletal disorders may affect the
contralateral side. Leading to short-term muscle dis-
orders, with reversible muscle damage, inflamma-
tion and pain, exhaustive SSC exercises are thus of
particular interest.
For this purpose, Regueme et al.[27] have recently
examined the possibility of contralateral effects of
unilateral SSC fatigue of the triceps surae muscle
group in unilateral as well as in bilateral testing
conditions. Ipsilateral versus contralateral fatigue
effects were compared in a single-joint task of maxi-
mal isometric plantarflexion (MVC), and in multi-
joint SSC tasks that included either ten intermittent
maximal drop-jumps or a continuous series of 15
submaximal rebounds. These tests were carried out
before and after the fatiguing exercise and were
Sports Med 2006; 36 (11)
988
repeated 2 days later, at the time of expected peak of
damage and pain in the exercising muscles, as well
as 8 days later. In all testing conditions, both in
MVC and drop-jump tests, the overall fatigue ef-
fects occurred at day 2 only, and were restricted to
the exercised leg in both uni- and bilateral tests.
These observations are in line with the minimal
contralateral changes in force previously reported
after maximal, but isometric contraction.[65-67]
Rattey et al.[67] reported a significant contralateral
reduction in voluntary muscle activation, and sug-
gested that the crossover effect is greater for the
lower body than that previously described for the
upper limbs.[65,66] According to Zijdewind et
al.,[32,33,68] central crossover effects would also be
likely to occur in a motor task performed at a high
level of effort and for a prolonged time. Supporting
this hypothesis, the continuous testing rebound task
used by Regueme et al.[27] revealed positive correla-
tions between the fatigue-induced changes in mus-
cle activity of the exercised and non-exercised legs.
This task lasted 15 seconds with high visual atten-
tion (to remain within the rebound targets), and
required anticipatory neural strategies at each im-
pact. These factors may have favoured the occur-
rence of contralateral neural adjustments. Finally,
the observation of restricted contralateral effects at
day 2 is likely to support the involvement of central
structures associated with pain. Based on these re-
sults, it seems that acute muscle disorders do not
lead to contralateral changes in performance in ei-
ther single or intermittent maximal motor tasks.
Some evidence of cross-over of central fatigue ex-
ists, however,[67] thus emphasising the need for fur-
ther exploration.
5. Do All Skeletal Muscles Respond
Similarly to SSC Exercise?
In section 1, it was suggested that the interaction
between contractile tissue (fascicles) and tendinous
tissue may be a complex one. In fact, several studies
have shown results – usually for one muscle only –
that cannot be generalised. Animal studies have
usually utilised sonomicrometers implanted surgi-
cally into the muscle to observe contractile tissue
 2006 Adis Data Information BV. All rights reserved.
Nicol et al.
(fascicle length changes) during walking or run-
ning.[41]
In human studies, medium to high speed ultraso-
nography has been mostly used to describe and
measure these attributes. For example, Fukunaga et
al.[69] showed that in normal human walking, which
is also an example of SSC activity, the gastrocnemi-
us fascicles usually shortened or remained isometric
in a similar manner as Griffiths[41] and Roberts[70]
reported for animal walking or slow running. Our
group has done extensive work by trying to utilise
methods to measure simultaneously at least two
muscles, and apply SSC activities that differ in the
type and intensity.[42] The ultrasonography probe(s)
can be successfully fastened on the muscle during
natural movements that can be quite explosive.[71]
The results of these human studies confirm the
possibility that the contractile tissue does not always
follow the basic concept of SSC of the whole mus-
cle-tendon unit.[42] The general observation was that
the gastrocnemius muscle usually demonstrates fas-
cicle shortening during the braking phase at low-
impact conditions of the drop jumps. With very high
dropping heights, the fascicles may become dramat-
ically lengthened during the braking phase. This was
interpreted to indicate reduced resistance to stretch
through possible detachment of crossbridges. The
soleus and vastus lateralis muscles, on the other
hand, showed usual stretch-shortening type beha-
viour in the fascicles. Thus, in the present state of
these studies in progress, one can only conclude that
care should be exercised to generalise how the fasci-
cles of the leg extensor muscles change their lengths
during the braking phase (or push-off phase as well)
of SSC. The tendinous tissue (aponeurosis and outer
tendon) may behave even more differently from the
basic muscle-tendon unit SSC concept. Future stud-
ies should definitely continue to explore these
problems so that the fascicle-tendon interaction be-
comes better known, as it determines so importantly
the stiffness regulation of the human skeletal muscle
during locomotion, especially during the SSC. At
present, the following problems have already been
addressed:[43,71] (i) fascicle-tendon interaction is
muscle-specific in a given SSC task; (ii) the impact
Sports Med 2006; 36 (11)
The Stretch-Shortening Cycle
load determines the fascicle behaviour in a specific
muscle; and (iii) the effort intensity after the braking
phase has some influence on this interaction by
affecting the tendon recoil in the final push-off.
If the questions raised above deal with the non-
fatigue situation, the understanding of the changes
in fascicle length and orientation during exhaustive
SSC fatigue is even more open. In our recent
study,[25] the bimodality could not be observed in the
fascicle parameters, although the fascicles were
lengthened in a passive (resting) situation immedi-
ately after the exercise, and remained lengthened
until 2 days post-exercise (figure 7). During maxi-
mal isometric action, the final fascicle length mea-
sured at peak force increased on day 2 post-exercise
and recovered completely to the original length on
day 8 post-exercise. It is too early to interpret these
findings in terms of functional mechanisms. More
studies are needed with the ultrasound method that
should also take into consideration the entire fasci-
cle-tendon interaction.
6. Potential Mechanisms
As has been discussed in sections 1 and 3, SSC
muscle action loads the neuromuscular system in a
more complex way than any isolated forms of mus-
cle action. Consequently, the possible mechanisms
involved in SSC-type fatiguing exercise are great in
* Active
*
5 long-lasting but reversible ultrastructural muscle
Fascicle length (cm)
*
4
* evidenced directly from histological analysis and
3
# indirectly from reductions in strength and range of
Cntrl Pre Post 2h 2d
Testing time
Fig. 7. Fascicle length changes (mean ± SD) of the soleus muscle
during and after an exhaustive stretch-shortening cycle exercise
performed on a sledge apparatus. The fascicle length was mea-
sured with high speed (94Hz) ultrasonography at different intervals
in the passive (resting) and active (maximal isometric plantarflex-
ion) situations (reproduced from Ishikawa et al.,[25] with permission).
Ctrl = control day; Post = immediately after exercise; Pre = pre-
exercise. * p < 0.05; # p < 0.0001.
 2006 Adis Data Information BV. All rights reserved.
989
number and they may be discussed in terms of short-
and long-term consequences. As is the case in the
isolated forms of muscle action, we are, however,
dealing with both central and peripheral fatigue
mechanisms. We could first begin with the peripher-
al fatigue, that has been traditionally defined as a
‘transient decrease in the muscle group’s capacity
for exercise’[47] and can be located distally to the
motoneurones in the transmission and/or contractile
mechanisms. From the bimodal nature of the SSC
fatigue recovery curve (figure 2), it is obvious that
the immediate reduction of performance deals most-
ly with the metabolic fatigue. As this type of fatigue
has been discussed extensively as a basic fatigue
concept for isolated forms of muscle function (usu-
ally either isometric or concentric)[1] we would like
to emphasise that, in addition to metabolic influ-
ences, SSC fatigue effects are more versatile and
include special features of structural and/or neural
origins.
6.1 Structural Changes
Supporting the mechanical source of peripheral
fatigue, intense or long-lasting SSC exercise is typi-
cally associated with delayed-onset muscle sore-
ness. This soreness was suggested as early as in
1902[72] to be due to exercise-induced muscle injury.
In a classical paper of Asmussen,[73] the possible
Passive mechanisms of exercise-induced muscle soreness/
damage were outlined more thoroughly. Since then,
damage has been frequently reported after exercises
involving eccentric muscle action.[74] This obviously
also includes SSC muscle action. Damage has been
motion as well as from increases in blood concentra-
8d
tion of muscle proteins.[75,76] It is known that there is
a shift in active length-tension relation after eccen-
tric fatigue,[77,78] and this phenomenon is now con-
sidered as one of the most reliable indicators of
damage.[79] It is also well documented that cytos-
keletal and myofibrillar abnormalities observed af-
ter eccentric muscle actions reach a peak 2–3 days
after the exercise with normal muscle architecture
Sports Med 2006; 36 (11)
990
being lost from the areas adjacent to the damaged
sarcomeres and fibres.[80,81]
Armstrong et al.[82,83] differentiated four subse-
quent phases for exercise-induced muscle damage
and ensuing inflammation: the initial-, the autoge-
netic-, the phagocytic- and the regenerative phase.
These phases include the whole process from initial
damage to repair. Even though the purpose of this
article is not to give a detailed description of the
processes related to muscle damage, it is rather
obvious that the different phases mentioned above
can have some short- and long-term consequences
directly on the contractile properties of the muscle
itself and, on the other hand, on its neural control
mechanisms. It must be noted, however, that not all
researchers agree with the traditional concept of
muscle damage and recovery. Some of them believe
strongly in the concept of remodelling,[84] even
without any parallel inflammatory process.[85,86]
In addition to possible muscle damage, repeated
SSC muscle action can be expected to modify the
mechanical properties of the muscle tendon unit.
This modification and its direct effects on the con-
tractile machinery are difficult to identify in active
fatigue conditions. Therefore, passive stretching
protocols have frequently been used for this pur-
pose. Several experiments have demonstrated with a
variety of protocols that passive dynamic or static
stretching of a human skeletal muscle can impair its
force-generating capacity.[23,87,88] The cause of this
contractile impairment has often been attributed to
the increased compliance of the muscle tendon unit
induced by the stretch. According to Taylor et al.[89]
the mechanical changes of the muscle-tendon unit
are time- and history-dependent because of the vis-
coelastic nature of the tissue. Two different re-
sponses in this regard have been suggested. The first
one is stress relaxation,[90,91] which is purely
mechanical in nature and is mainly responsible for
the reduced passive tension of the muscle-tendon
unit over time. The second one is called ‘plastic
deformation’, which means reorientation of the sup-
porting connective and soft tissue-supporting tissue
into more parallel arrays.[92] This response is sug-
gested to be more time-dependent of the maintained
 2006 Adis Data Information BV. All rights reserved.
Nicol et al.
tissue strain. Independently on the exact mecha-
nism, an increased compliance of the muscle-tendon
unit could then result in impaired force transfer from
the muscle fibres via the tendon to the bone.[93] In
addition, there is some evidence that it could lead to
a downward and rightward shift in the force-length
relationship of the muscle tendon unit.[94] On the
other hand, it has been demonstrated that the early
phase (2 hours) of the post-SSC exercise recovery
may be associated with an increased stiffness of the
muscle-tendon unit (unpublished data).[23,25]
Increased stiffness could be expected to result in
increased response to stretch of the muscle spindle
and, thus, to lead to facilitation of the stretch reflex
response. This could explain why some authors[24]
demonstrated in the early recovery phase reflex am-
plitudes that in some subjects were higher than in the
before-fatigue measurements. However, this possi-
ble effect of increased stiffness would not last long
because, in contrast, several experiments have
shown that a secondary reduction in reflex response
begins within a few hours after the initial recovery
period.[23,52,57] These latter observations could indi-
cate the possibility of direct mechanical damage in
the intrafusal fibres themselves, leading to reduced
muscle spindle sensitivity.[95] However, this hypoth-
esis has been recently challenged by Gregory et
al.[96] They showed that in an anaesthetised cat the
responses of muscle spindles to stretch and fusimo-
tor stimulation were not altered by a series of eccen-
tric contractions. Therefore, Gregory et al.[96] con-
cluded that the intrafusal fibres of muscle spindles
are not prone to damage of the kind seen in ex-
trafusal fibres after a series of eccentric contrac-
tions.
Trappe et al.[97] were able to show disruption of
titin and nebulin structures in extrafusal fibres after
eccentric fatigue. Yu et al.[85] produced convincing
evidence for a remodelling model that would ex-
plain, in the early recovery phase from eccentric
exercise, the release of alpha-actinin, titin and nebu-
lin and most likely also some Z-disk and I-band
associated proteins. Provided that the mechanical
coupling truly exists between extra- and intrafusal
Sports Med 2006; 36 (11)
The Stretch-Shortening Cycle
fibres, this finding may provide evidence to keep the
hypothesis of intrafusal fibre damage alive.
6.2 Neural Adjustments
During and after fatiguing SSC exercises, neural
failure and/or adjustments may also be expected to
take place and to affect the activation pathways at
different levels. Modified from Bigland-Ritchie[98]
and Löscher et al.,[99] these potential sites include:
(i) excitatory input to supraspinal motor centres; (ii)
excitatory drive to α-motoneurones; (iii) modulation
of interneuronal circuits; (iv) motoneurone excita-
bility; (v) peripheral reflex activity from small diam-
eter afferents; and (vi) muscle spindle activity. As
previously discussed in section 3.3, the manifesta-
tion and the contribution of the central and reflex
neural adjustments to SSC fatigue may vary depend-
ing on the testing task. This variation in neural
adjustments has been addressed by the following
mechanisms to: (i) compensate for the contractile
failure;[12] (ii) optimise the neural drive in propor-
tion to the contractile failure (also known as ‘muscle
wisdom’);[100] and (iii) induce contractile failure
with inadequate neural drive.[101] It is not very well
known why neural drive itself should be a limiting
factor for the force output of the muscle. However,
in a fatiguing exercise where muscle damage takes
place, inadequate neural drive can be an attempt of
the neuromuscular system to protect the muscle-
tendon unit from additional damage.[15,30,50,54] If the
result of these neural adjustments is reduced neural
drive, regardless of the mechanism, development of
central fatigue exists.
6.2.1 Supraspinal Fatigue
The most common protocol to reveal the changes
in neural drive to motoneurones is the twitch inter-
polation technique.[102] The problem with this tech-
nique is that it is not able to identify exactly which
mechanism would be responsible for such changes.
Transcranial magnetic stimulation (TMS) over the
motor cortex has been recently used to assess possi-
ble changes in cortical excitability during fa-
tigue.[101-106] According to Gandevia et al.[101]
supraspinal fatigue has developed if an association
can be found between cortical inhibition and decline
 2006 Adis Data Information BV. All rights reserved.
991
in muscle force. Brasil-Neto et al.[103,104] and partly
Kalmar and Cafarelli[106] found this association and,
therefore, suggested that fatigue can also result from
reduced efficiency in the generation of the motor
command possibly as a consequence of cortical
neurotransmitter depletion. This is in contradiction,
however, with the absence of changes in motor
cortex excitability reported, especially during
lengthening actions, by Löscher and Nordlund.[105]
To the best of our knowledge, TMS has not been
used to study supraspinal factors in SSC fatigue. On
the other hand, despite its limitations, the twitch
interpolation technique has been used and it has
revealed inadequate voluntary activation after pro-
longed running exercises.[9,107] Interestingly, this
was not the case after a freestyle ski skating mara-
thon.[11] However, the concept of supraspinal fatigue
cannot be ruled out when considering the large
reductions in maximal neural activation reported
immediately after prolonged SSC exercises, where
eccentric loads exceed the ones of cross-country
skiing.[10,21,53] During the delayed phase of recovery,
this possibility is reinforced further by the potential
effect of muscle pain. Qerama et al.[108] suggested
that stimulation (capsaicin and hypertonic saline) of
muscle nociceptors induced a reduction in motoneu-
rone firing rates. Using TMS, Le Pera et al.[109]
demonstrated that tonic muscle pain can inhibit the
motor system. During the peak pain, the absence of
effects on the H-reflex response suggested that the
observed reduction in the size of the motor-evoked
potentials was probably due to decreased excitabili-
ty of the motor cortex. Twenty minutes after pain,
the motor-evoked potential amplitude was found to
be further depressed and the H-reflex amplitude
reduced, suggesting an inhibition of the spinal
motoneurones, possibly overlapping the cortical in-
hibitory processes. This observation of a delayed
depression of the H-reflex response has been clearly
demonstrated for H-reflex peak-to-peak amplitude
after exhaustive rebound exercise on the sledge[110]
as well as after 75 minutes of electrical stimulation
combined with mechanically induced stretches (un-
published observations).
Sports Med 2006; 36 (11)
992 Nicol et al.

These results are in contrast with the absence of
change reported by Svensson et al.[111] and Matre et
al.[112] It should be mentioned, however, that Matre
et al.[112] observed in some of the H-reflex record-
ings a delayed depression (lasting for >40 minutes
after the end of pain), which was then attributed to
the potential inhibitory effect originating from
group III muscle afferents. The same hypothesis was
also suggested by Nicol et al.[110] when the H-reflex
response did not recover until 5 days after each SSC
exercise (figure 8a). After prolonged SSC simula-
tion in an ankle ergometer, H-reflex has also been
shown to decrease in parallel with increased interpo-
lated twitch torque.[88] Consequently, this reduction
in H-reflex amplitude may include the possibility of
supraspinal modulation of the α-motoneurone pool
during SSC fatigue. It further emphasises the com-
plexity of SSC fatigue and the possible interaction
with other mechanisms in neural adjustment to fa-
tigue and to the testing task. This article concen-
a hypothesis of Ia-afferent supported reduction in mo-
20
H/M-wave amplitude (D%)
trates on the most obvious ones. They include altera-
tion of the fusimotor-muscle spindle system and
reflex adjustments of the neural activity, namely via
activation of group III and IV muscle afferents.
6.2.2 Alteration in the Fusimotor-Muscle
Spindle Function
The monosynaptic reflex loop originating from
muscle spindle is well known to be under fusimotor
control (γ-loop).[113] In the case of muscle fatigue,
various spinal and/or peripheral feedback mecha-
nisms may be suggested to occur.[1] In general, these
mechanisms can be related to either presynaptic or
postsynaptic inhibitory effects coming from differ-
ent feedback sources or decreased net facilitation
(disfacilitation) of the Ia-afferents coming from the
muscle spindle. Some direct evidence comes from
microneurographic recordings that reflex facilitato-
ry influence provided by muscle afferents indeed
declines as fatigue develops.[114] Even though the
tor unit firing rates have been recently challenged,[1]

0
it is very likely that especially since the eccentric
part of the SSC muscle action induces a powerful
-20 loading of the muscle spindles, continuous SSC
loading can modify the γ-loop system. Unfortunate-
-40
ly, because of technical difficulties, no direct
-60 microneurographic recordings have so far been
made from human muscle afferents during SSC
-80
d0b d0a d2 d5b d5a d7 d10b d10a d12 d15 fatigue.
b
Although the exact mechanism inducing the re-
duced Ia-afferent activity has not yet been thorough-
H-reflex amplitude (D%)

20 ly explained, three major possibilities have been

0
-20 presented: (i) withdrawal of the fusimotor support to
-40 the muscle spindles;[115,116] and/or (ii) intrafusal fi-
*
-60 bre fatigue itself;[117] and/or (iii) mechanical unload-
-80
*** ing of the muscle spindle.[87,118] Methodologically, it
d0b d0a 2h d2 d7 is very difficult to separate the effect of fusimotor
Testing sessions support to muscle spindles from the effects of the
Fig. 8. Relative changes (mean ± SD) in the H/M-wave ratio (a) in
muscle spindles themselves in fatigue. In some SSC
the course of a 15-day follow-up during which an exhaustive short-
term stretch-shortening cycle exercise was repeated on days 0, 5 fatigue experiments listed in table II[23,52] large acute
and 10[110] and in H-reflex (b) after 75 minutes of electrical stimula- and delayed reductions in stretch-reflex responses
tion combined with mechanically induced stretches (unpublished
have been measured in both passive and active con-
observations). In both studies, the changes are expressed as a
percentage of the pre-fatigue value. dxa = day x after exercise; dxb ditions.[23,24,27,30,52] At present, however, it can only
= day x before exercise; *** p < 0.001. be hypothesised that both direct and indirect fatigue

 2006 Adis Data Information BV. All rights reserved. Sports Med 2006; 36 (11)
The Stretch-Shortening Cycle 993

Beginning
effects on the fusimotor-muscle spindle system ex- End
ist. a Ankle displacement
Direct influences include both metabolic and 90

Ankle displacement (o)

Fascicle length (cm)

mechanical factors. Bongiovanni and Hagbarth[116] 6

were able to show that metabolic fatigue can influ- 86

ence the fusimotor support to the muscle spindles. In

82
addition, they also suggested that there is a possibili- 4

ty for some more direct fatigue effects on the in- 78

trafusal fibres themselves. The theory of intrafusal
fatigue relies on a fatigue-induced decline in in- 74 2

trafusal contraction force, which could then reduce 0 100 200 300 400 500 600
Time (ms)
the afferent discharge. However, direct fatigue ef-
b
fects on the intrafusal fibres are scarce. Some signs 0
of metabolic fatigue in intrafusal fibres have been
Fascicle length (D%)

observed following prolonged stimulation of static -2

γ-axons in the cat[119] through the effect of NH3 and
-4
CO2 on the sensory ending of cat muscle spin-
dles[120] or during prolonged swimming of mice.[121] -6
With regard to the possibility of mechanical
changes in the intrafusal fibres, one can assume that -8
the SSC fatigue can potentially influence the in- 0 200 400 600
trafusal fibre force. This could take place without Time (ms)
direct damage to the fibres. Some signs of this Fig. 9. Mean data from eight subjects illustrating the behaviour of
possibility have been reported by Avela et al.[88] in the fascicle length changes (p < 0.05 to p < 0.01) during one
passive stretch cycle (average of ten cycles) at the beginning and
an experiment where long-lasting SSC fatigue re- end of a passive stretching protocol, in both absolute (a) and rela-
sulted in an acute 14% reduction in stretch-resisting tive (b) scales.[118] The shaded area in graph b represents + stan-
force of the triceps surae muscle group. This was dard deviation above the mean.

taken as an evidence for increased muscle-tendon

compliance immediately after fatigue, which could
then modify the mechanical response of the muscle
spindle. Since investigation of this hypothesis again
meets the problem of isolating each possible mecha-
nism, continuous passive stretches have been used
as an exercise task.
Avela et al.[118] demonstrated a clear reduction
(41% and 27.5% for medial gastrocnemius and
soleus muscles, respectively) in stretch-reflex peak-
to-peak amplitude measured immediately after re-
peated passive muscle stretching of 1-hour duration.
In that experiment, the parameters for muscle
stretching simulated those of normal endurance run-
ning. Avela et al.[118] also measured H-reflexes
(stimuli at 25% of maximal M-wave) during ten
stretching ramps for the beginning and the end of the
stretching protocol. This measurement showed that
during the stretching protocol H-reflex was reduced
from 3.6 to 1.9mV. Results from the reflex measure-
ments were then taken as a clear indication of some
neural modification induced by the passive stretch-
ing. Interestingly, ultrasound measurements re-
vealed simultaneously a significant reduction in fas-
cicle length of the medial gastrocnemius muscle
(figure 9). Therefore, the authors suggested that the
increased compliance of the muscle-tendon unit
takes place somewhere in the aponeurosis-tendon
system. Thus, their final interpretation was that the
increased compliance of the muscle results in a
reduced mechanical response of the muscle spindle
leading to reduced Ia-afferent activity and, finally,
to disfacilitation of the α-motoneurone pool.

 2006 Adis Data Information BV. All rights reserved. Sports Med 2006; 36 (11)
994
6.2.3 Reflex Adjustments of the Neural Activation
It was originally suggested by Asmussen and
Mazin[122] and later supported by Bigland-Ritchie et
al.[123] that reduction in the neural activation could
depend on some reflex response from the con-
tracting muscle itself. This hypothesis has been later
challenged by Löscher et al.[124] for sustained iso-
metric contractions. The nature of SSC fatigue
could, however, favour the intervention of such
mechanisms. It is of interest for the present discus-
sion on the functional effects of SSC-induced mus-
cle damage that small diameter, group III and IV,
muscle afferents could be likely candidates for such
influences.
Briefly, these muscle afferents are known to be
mostly polymodal, being sensitive to several param-
eters associated with either metabolic fatigue or
muscle injury.[125,126] In the acute phase of SSC
fatigue, extracellular increases in potassium,
phosphate and lactic acid may constitute stimuli of
the muscle metaboceptors.[127] In the case of muscle
damage, biochemical substances, such as
bradykinin[128] and prostaglandin, are known to be
released, which may also increase the spontaneous
discharge of both group III and IV mechanorecep-
tors and nociceptors. Once activated, the nocicep-
tors also release neuropeptides, which cause vasodi-
latation, oedema and release of histamine. These
processes lead then to a further and long-lasting
activation of some of the sensory endings.[129] In
terms of their influence on the neural activation,
both facilitatory and inhibitory influences have been
reported.
Group III and IV muscle afferents may have a
facilitatory effect (‘vicious circle’[130]) on the γ-
motoneurones. Several experiments have shown
that, especially in the cat, the activity of the group III
and IV muscle afferents can result in a reflexively
induced increase of fusimotor discharge[131,132] and
increase spindle discharge during long lasting iso-
metric contraction.[133,134] Some signs of similar be-
haviour have also been found in humans.[135] In the
case of SSC fatigue, this mechanism has been sug-
gested to play a role in the large stretch reflex
facilitation observed in a passive resistance to
stretch.[23] Understanding of this facilitation and of
 2006 Adis Data Information BV. All rights reserved.
Nicol et al.
the functional effect of small muscle afferents be-
comes more complicated, since it is known from the
animal studies[136] that these small muscle afferents
make a powerful input to inhibitory interneurones,
which could inhibit the Ia-afferent terminals.[137]
Some convincing, although indirect, evidence
exists in favour of a presynaptic inhibitory effect on
α-motoneurones.[138,139] For example, Garland and
McComas[138] showed that the H-reflex was signifi-
cantly depressed after electrically induced fatigue of
human ankle plantarflexors under ischaemia. How-
ever, they failed to observe similar reduction in H-
reflex with ischaemia alone and with electrical stim-
ulation without ischaemia. Support for the involve-
ment of group III and IV muscle afferents comes
from the finding that selective damage of these
afferents (by application of capsaicin) abolishes the
depression of the monosynaptic reflex induced by
muscle fatigue.[140] In addition, Duchateau and Hai-
naut[137] discovered that the decrement in H-reflex
does not recover as long as the fatigue-induced
metabolic accumulation is maintained by ischaemia.
Avela et al.[88] were able to show the same phe-
nomenon after long-lasting SSC fatigue. Similarly,
the secondary decline of performance in SSC fa-
tigue, which usually lasts for a few days after the
exercise, supports the hypothesis of a potential ef-
fect of prolonged activation of group III and IV
muscle afferents by the exercise-induced inflam-
matory process. This is well in line with the recent
findings of Dousset et al. (unpublished data) that the
delayed changes in reflexes and isometric force oc-
curred concomitantly with an increase in muscle
thickness, C-reactive protein and substance P con-
centration, as well as in serum creatine kinase activi-
ty. With regard to the slow conducting velocity of
small muscle afferents (2.5–3 m/sec), their continu-
ous activation by these polymodal stimuli gives
support to their potential role in the delayed and
prolonged SSC recovery phase. Thus, it is very
likely that the presynaptic inhibition is triggered by
the group III and IV muscle afferents and may then
contribute to the bimodal pattern observed along the
recovery period.
Sports Med 2006; 36 (11)
The Stretch-Shortening Cycle
7. Conclusions
This article has attempted to demonstrate that
naturally occurring, but exhaustive, SSC exercise
often induces a dramatic reduction in force and
power production. Although these effects are in
some cases somewhat similar to those occurring
after intensive eccentric exercise, the SSC fatigue is
much more complex because of its more compre-
hensive way of loading the neuromuscular system
mechanically, metabolically and neurally. Thus, it
must be emphasised that SSC fatigue is not the same
as pure eccentric fatigue. The complex features of
SSC loading are also represented in the bimodal
nature of performance deterioration and recovery.
The bimodality in SSC-induced fatigue response
means immediate reduction of performance, quick
recovery within 1–2 hours, followed by a secondary
reduction, which may often show the lowest values
on the second day post-exercise. The full recovery
may take 4–8 days depending on the parameter and
on the severity of exercise. Several neural factors
including the monosynaptic stretch reflex follow
usually well the bimodal trend and are coupled with
the respective changes in mechanical parameters.
The literature gives several suggestions including
possible structural damage as a potential causal
mechanism including both extra and intrafusal fib-
res. This would have consequences on the Ia-affer-
ent activation. Neural adjustments in the supraspinal
level could naturally be operative; however, the
many studies quoted in this article further emphasise
the influences of exhaustive SSC fatigue on the
muscle spindle directly, and to some extent to the
modification in the γ-motoneurone input to the spin-
dle.
In addition to the possible damage of intrafusal
muscle fibres, one strong candidate has been pro-
posed to explain the reduction in Ia-afferent re-
sponse in the certain points of the bimodal response
curve. This is activation of small (III and IV) affer-
ents during both the acute and delayed fatigue
phases. The role of these small muscle afferents has
been regarded as an attractive factor to cause
presynaptic inhibition with subsequent reduction in
the stretch reflex response. Unfortunately this and
 2006 Adis Data Information BV. All rights reserved.
995
many other possible mechanisms need more thor-
ough testing in animal models provided that the SSC
actions can be truly performed as they appear in
normal human locomotion.
Acknowledgements
Professor Komi was supported by grant 88/627/2005 from
the Ministry of Education (Finland). The authors have no
conflicts of interest that are directly relevant to the content of
this review.
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Correspondence and offprints: Prof. Paavo V. Komi, Neuro-
muscular Research Center, Department of Biology of Phys-
ical Activity, University of Jyväskylä, P.O. Box 55 (LL) FIN-
40351, Jyväskylä, Finland.
E-mail: Paavo.Komi@sport.jyu.fi
Sports Med 2006; 36 (11)