Chapter 7

Muscle Function: Strength, Speed,

and Fatigability
Roger M. Enoka1 and Jacques Duchateau2
1
Department of Integrative Physiology, University of Colorado, Boulder, CO, United States, 2Laboratory of Applied Biology and Neurophysiology,
ULB Neuroscience Institute, Universite´ Libre de Bruxelles, Brussels, Belgium

7.1 INTRODUCTION nervous system transmits an activation signal to muscle

(Duchateau and Enoka, 2011).
All physical actions performed by the human body A typical muscle contains a few hundred motor units
involve the controlled activation of selected muscles by that are referred to as a motor unit pool. The associated
the nervous system. For each action, the nervous system motor neurons, which cluster in the spinal cord or brain
must decide which muscles to activate, how much they stem, are known as a motor nucleus. The motor neurons
should be activated, and when they should be activated. receive thousands of synaptic contacts from other neu-
Moreover, the nervous system must attenuate the rons, including those located in the spinal cord, those con-
unwanted actions produced by the intended muscle activ- veying information from sensory receptors, and those
ity when it disturbs a desired posture. transmitting information from brain stem and cortical neu-
To understand how the nervous system solves these rons (Heckman and Enoka, 2012). Once the synaptic
problems, the chapter begins by discussing the basic func- inputs depolarize the membrane potential of a motor neu-
tional unit that connects the nervous system to muscle— ron above a threshold, it will generate an action potential
the motor unit—and the basic contractile unit of that is propagated along its axon to the synaptic
muscle—the sarcomere. All actions involve, at a mini- contacts—neuromuscular junctions—with all the muscle
mum, the activation of hundreds of motor units and fibers it innervates. Due to the secure synaptic connection
millions of sarcomeres. between the axon of a motor neuron and the muscle fibers
To activate an appropriate set of motor units for a spe- it innervates, the action potential generated by a motor
cific action, the nervous system must know about the bio- neuron typically results in several hundred muscle fiber
mechanical and physiological properties of the muscles action potentials.
that could be used to perform the action. The key proper- The action potentials generated in the muscle fibers
ties of muscle that the nervous system must consider are are conducted in both directions from the neuromuscular
its force capacity, the direction in which it exerts a force, junction, which is often located near the middle of the
the rate at which it can generate force, and how long it can muscle fiber, to the ends of the muscle fiber. The muscle
sustain a desired force. The final part of the chapter dis- fiber action potentials involve the same transmembrane
cusses the neuromuscular determinants of these attributes. currents as those that produce axonal action potentials.
The action potential currents produce changes in the
electrical potential that can be recorded with electrodes.
7.2 MUSCLE ACTIVATION The technique used to record muscle fiber action poten-
The activation signal sent from the nervous system to tials is known as electromyography and the recording
muscle arises from motor neurons in the spinal cord or corresponds to an electromyogram (EMG). EMG signals
brain stem. Each motor neuron innervates from a few tens provide information about muscle activation (muscle
to several hundreds of muscle fibers. A motor neuron and fiber action potentials) and are useful for studying the
the muscle fibers it innervates are known as a motor unit; control of movement by the nervous system (Farina
it comprises the final common pathway by which the et al., 2016).

Muscle and Exercise Physiology. DOI: [Link]

© 2019 Elsevier Inc. All rights reserved. 129
130 SECTION | II Muscle Energetics and Its Performance

EMG recordings can also record muscle fiber action and Fuglevand, 2001). Because the peak force that a
potentials that have been evoked by electrical stimulation motor unit can produce mainly depends on its innervation
applied to a peripheral nerve. A technique based on this number, motor unit force varies exponentially across a
principle can be used to estimate the number of function- motor unit pool. When motor units are activated by the
ing motor units in a muscle; it is known as the Motor nervous system, therefore, muscle force does not increase
Unit Number Estimation (MUNE) technique. The linearly with the number of activated motor units. For the
approach requires the measurement of two surface- example shown in Fig. 7.1, 50% of the total number of
recorded EMG signals: motor unit action potentials during fibers in the muscle (n 5 44,000) are innervated by 102
a voluntary contraction and the response evoked by a out of the 120 motor units in the pool. Although the accu-
strong electrical current applied to the peripheral nerve racy of these estimated innervation numbers remains to
innervating the muscle. The average amplitude of the be determined, the key point is that there is a nonlinear
motor action potentials relative to the maximal amplitude relation between innervation number and motor unit size
of the evoked response provides an estimate of the num- (Kernell, 1992).
ber of functioning motor units in a muscle. With this The muscle fibers belonging to one muscle unit are
approach Power et al. (2010) found that the number of distributed among those belonging to other muscle units.
motor units in the tibialis anterior muscle of old men In a transverse section through a muscle, the density of
(91 6 22) was much less than that of age-matched masters fibers belonging to the same muscle units ranges from 2
runners (140 6 53) and young men (150 6 43). Although to 5 fibers per 100 muscle fibers, which means that a
cadaver-based estimates indicate that there are B445 given cross-sectional area of muscle contains fibers from
number of motor units in tibialis anterior muscle 20 to 50 different muscle units. Similarly, the territory of
(Feinstein et al., 1955), more recent measurements of the a muscle unit can occupy from 8% to 50% of the muscle
number of motor axons in peripheral nerves suggest the volume. Moreover, muscle fibers typically do not span
cadaver estimates are likely too high (Gesslbauer et al., the distance from the proximal to distal attachments of
2017). the muscle onto the skeleton, as indicated for some
human leg muscles in Table 7.1. Consequently, the force
generated by each muscle fiber after it has been activated
7.2.1 Muscle Unit by an action potential must be transmitted to the skeleton
through various connective tissue structures (Hughes
The muscle fibers that belong to a motor unit are known et al., 2015).
as a muscle unit. The number of fibers in a muscle unit—
known as the innervation number—varies across the
motor unit pool. A typical example of this distribution is 7.2.2 Muscle Fiber Types
shown for a hand muscle in Fig. 7.1. In this example, the One approach to estimating the physiological properties
motor unit with the lowest innervation number comprised of muscle fibers is to characterize their responses to vari-
22 muscle fibers, whereas the motor unit with the highest ous histochemical, biochemical, and molecular assays.
innervation number contained 1550 muscle fibers (Enoka The two most commonly used schemes provide a mea-
surement that is associated with the contraction speed of
1600 44,000
the muscle fiber. One scheme distinguishes muscles by
1400 38,500 their reactivity to histochemical assays for the enzyme
myosin adenosine triphosphatase (ATPase), which is
Innervation number

1200 33,000
involved in the power stroke of the cross-bridge cycle.
1000 27,500
Faster contracting muscle fibers tend to have greater
800 22,000
amounts of myosin ATPase. Histochemical stains for
600 16,500 myosin ATPase can identify two types of muscle fibers:
400 11,000 type I and type II. Type I fibers typically have slower
contraction times, on average, than type II fibers. The
200 5500
type II fibers can be further classified as being less (type
0 0
IIa) or more (type IIx) fatigable in response to standard-
0 20 40 60 80 100 120 ized tests involving contractions evoked with electrical
Motor unit number stimulation (Enoka and Duchateau, 2015).
The other classification scheme distinguishes muscle
FIGURE 7.1 Distribution of innervation number across the motor unit
pool (n 5 120) that innervates B44,000 fibers in a hand muscle (Enoka fibers on the basis of isoforms of the myosin heavy chain
and Fuglevand, 2001). The right-axis indicates the cumulative sum of (MHC). Each molecule of myosin in the thick filament
muscle fibers across the motor unit pool. contains several proteins that differ in molecular weight,
 Muscle Function: Strength, Speed, and Fatigability Chapter | 7 131

TABLE 7.1 Average Anatomical Properties for Some Human Skeletal Leg Muscles

Muscle Mass Muscle Length Fiber Length Pennation Angle Cross-sectional Area
(g) (cm) (cm) ( ) (cm2)
Thigh
Sartorius 78 45 40 1 2
Rectus femoris 111 36 8 14 14
Vastus lateralis 376 27 10 18 35
Vastus intermedius 172 41 10 5 17
Vastus medialis 239 44 10 30 21
Gracilis 53 29 23 8 2
Adductor longus 75 22 11 7 7
Adductor brevis 55 15 10 6 5
Adductor magnus 325 38 14 16 21
Biceps femoris (long) 113 35 10 12 11
Biceps femoris (short) 60 22 11 12 5
Semitendinosus 100 30 19 13 5
Semimembranosus 134 29 7 15 18
Lower leg
Tibialis anterior 80 26 7 10 11
Extensor hallucis 21 24 7 9 3
longus
Extensor digitorum 41 29 7 11 6
longus
Peroneus longus 58 27 5 14 10
Peroneus brevis 24 24 5 11 5
Gastrocnemius 113 27 5 10 21
(medial)
Gastrocnemius (lateral) 62 22 6 12 10
Soleus 276 41 4 28 52
Flexor hallucis longus 39 27 5 17 7
Flexor digitorum 20 27 4 14 4
longus
Tibialis posterior 58 31 4 14 14

Source: Adapted, with permission, from Ward, S.R., et al., 2009. Orthop. Relat. Res. 467, 1074 1082 (Ward et al., 2009).

the heaviest of which is the MHC. There are three slightly Although both fiber-classification schemes (myosin
different versions (isoforms) of MHC due to variations in ATPase and MHC isoforms) suggest that there are only
the amino acid sequence: MHC-I, MHC-IIa, and MHC- three types of muscle fibers, this interpretation is too sim-
IIx. The MHC isoforms are associated with differences in plistic for two reasons. The first reason is that significant
the attachment time of actin and myosin during the cross- numbers of muscle fibers contain more than one MHC
bridge cycle and the maximal shortening velocity the isoform (Bottinelli et al., 1996) and the proportions of
muscle fiber can achieve during a muscle contraction pure and hybrid fibers change with age (Purves-Smith
(Canepari et al., 2010). et al., 2014). The second reason is that there is
132 SECTION | II Muscle Energetics and Its Performance

(A) 20

16

Motor unit number (%)

8
Number of fiber

12
6

4 8
s

2 4

0 0
I 20 30 40 50 60 70 80 100
I-IIA
Time to peak (ms)
M
yo

IIA 0.05
sin

IIA-X 0.04
(B) 30
he

0.03
av

IIX 0.02
L/s)
y

*
er (P o
0.01
ch

25

Motor unit number (%)

Pow
ai

0
n

20
FIGURE 7.2 Peak power produced by segments of single muscle fibers
from vastus lateralis with different types of MHC isoforms. Power was 15
calculated as the product of peak tetanic force (Po) and maximal shorten-
ing velocity expressed as fiber lengths per second (L/s). Adapted with 10
permission from Bottinelli, R., et al., 1996. J. Physiol. 495, 573 586.
5

0
0 20 40 60 80 100 120 140 160 180
Peak twitch torque (mN•m)
considerable overlap in the contractile properties of the
different fiber types (Fig. 7.2). Based on measurements FIGURE 7.3 Distributions of (A) times to peak twitch torque and (B)
performed on fiber segments obtained by muscle biopsy peak twitch torque for 528 motor units in the tibialis anterior of young
men. Adapted with permission from Van Cutsem, M., et al., 1997.
from the vastus lateralis muscle of young men, Bottinelli Canad. J. Physiol. 22, 585 597.
et al. (1996) found that the muscle comprised three pure
fiber types (MHC I, IIa, and IIx) and two hybrid fibers
(I-IIa and IIa-IIx) and that there was considerable overlap
among these different fiber types in the power the fiber
segments could produce. Consequently, the fiber-typing rate at which Ca21 is released from the sarcoplasmic
schemes do not identify fibers with distinct sets of con- reticulum, which is a critical step in the activation of the
tractile properties. Rather, Fig. 7.2 indicates that the cross-bridge cycle (Ørtenblad et al., 2000). The contrac-
capacity of muscle fibers to produce power—and other tion times (time to peak force) of the motor units in a
contractile properties—is distributed continuously across muscle are distributed continuously (Van Cutsem et al.,
the different fiber types. 1997) and do not comprise distinct sets of slow- and fast-
contracting motor units (Fig. 7.3).
The other measure of contractile speed is the maximal
7.2.3 Contractile Properties shortening velocity, which is more difficult to measure
The contractile properties of motor units can be character- than contraction time. It involves the maximal activation
ized with measurements of contractile speed, peak force, of a single motor unit and measuring the peak rate at
and fatigability. Contractile speed refers to the rate at which muscle length shortens when pulling against the
which force is generated during a muscle contraction. lightest load possible (Schiaffino and Reggiani, 2011).
There are two ways to measure contractile speed for a The measured speed is typically expressed relative to the
motor unit: contraction time and maximal shortening lengths of the muscle fibers and reported in fiber lengths
velocity. Contraction time corresponds to the time it takes per second (Fig. 7.2). Maximal shortening velocity indi-
a motor unit to reach peak twitch force during an isomet- cates the speed at which the thick and thin filaments slide
ric contraction after it has been activated by a single past one another, which is limited by the rate of ADP
action potential. Contraction time mainly depends on the release during the cross-bridge cycle. As with contraction
 Muscle Function: Strength, Speed, and Fatigability Chapter | 7 133

specific tension (Faulkner et al., 2007; Narici et al., 2016;

(A)
Harridge and Lazarus, 2017).
Frequency
50 pps The third contractile property of motor units is fatiga-
2 5 6 10 15 20 30 50 80 100 bility, which is usually quantified as the rate of decline in
a measure of performance. For example, the decline in
Dorsiflexion force
force after the motor unit has been activated artificially
100 mN
with a series of electrical stimuli that elicit action poten-
2s tials in the axon of the motor unit. One of the first proto-
100 cols to use this approach applied sets of 13 stimuli at a
Peak Force (% maximum)

(B)
rate of 40 Hz for 330 ms and measured the decline in the
80 evoked force after 2 min of stimulation (Burke et al.,
60 1973). The results indicated that some motor units exhib-
ited no decline in peak force, whereas for other motor
40
units it declined by .75%. Such protocols provide a mea-
20 sure of fatigability as it is limited by physiological pro-
0
cesses distal to the neuromuscular junction, such as
0 20 40 60 80 100 excitation-contraction coupling, metabolic changes that
Frequency (pps) influence the supply of ATP and impede the function of
the cross bridges, changes in the ionic constituents inside
FIGURE 7.4 The sigmoidal relation between stimulation frequency the muscle fibers, and an adequate perfusion of the active
(pulses per second; pps) and the force produced by single motor units in
human foot muscles. (A) Motor unit force produced by electrical stimu- muscles. Although this protocol is able to distinguish
lation delivered via intraneural electrodes (upper trace). (B) Average motor units that are fatigable from those that are not fati-
motor unit force normalized to the peak force for each of 13 motor units. gable in the muscles of experimental animals, the artifi-
The half-maximal force was produced with a stimulation rate of cial activation of motor units with electrical stimulation
B10 pps. Adapted with permission from Macefield, V.G., et al., 1996. J. does not identify distinct groups of motor units in human
Neurophysiol. 75, 2509 2519.
muscle (Bigland-Ritchie et al., 1998).
One of the reasons for this discrepancy is that the rate
at which motor neurons generate action potentials is not
constant during voluntary contractions. Even when a pro-
time, there is a continuous distribution of maximal short- tocol produces only a small decrease in maximal muscle
ening velocity across the motor unit pool (Petit et al., force, for example, motor neurons that are most active
1993). during the task exhibit significant reductions in the rates
The second contractile property of motor units is peak at which they generate action potentials (Farina et al.,
force. Peak twitch force does not indicate the force capac- 2009). In general, the fatigability of a motor unit depends
ity of a motor unit because the amount of Ca21 released on the capacity of its muscle fibers to produce the requi-
in response to a single action potential is not sufficient to site force and the ability of the motor neuron to sustain an
engage a majority of the force-generating elements, the adequate rate of action potential generation (Enoka and
cross bridges. Rather, the force produced by a motor unit Duchateau, 2016). Both of these capabilities are influ-
increases as a sigmoidal function of the rate at which enced by the details of the task being performed.
action potentials are generated (Fig. 7.4). Peak motor unit
force is achieved when action potentials are delivered at a
rate of $ 50 per second (Macefield et al., 1996). 7.2.4 Motor Unit Activation
The force capacity of a motor unit depends on the
number of fibers innervated by the motor neuron (inner- The nervous system controls muscle force by varying the
vation number), the average cross-sectional area of its number of motor units recruited during a contraction and
muscle fibers, and the specific tension of its muscle the rates at which each of the activated motor neurons dis-
fibers. Cross-sectional area reflects the number of con- charges action potentials. Gradual increases in muscle
tractile protein (thick and thin filaments) arranged in par- force depend mainly on the recruitment of additional
allel, whereas specific tension indicates the density of the motor units, whereas rapid increases in force require high
contractile proteins within the fiber. Of these three fac- discharge rates. For both slow and fast increases in force,
tors, innervation number has the greatest influence on however, motor units are recruited progressively from
motor unit force. Nonetheless, changes in motor unit force weakest to strongest. The muscle force at which a motor
after various physical activity interventions are usually unit is recruited during an increase in force is known as
due to increases or decreases in cross-sectional area or its recruitment threshold (Fig. 7.5).
134 SECTION | II Muscle Energetics and Its Performance

100

Twitch force (mN)

10

0.2 1 10 20
Recruitment threshold (N)

FIGURE 7.6 Relation between recruitment threshold during slow

increases in muscle force and spike-triggered average force for 65 motor
units in a hand muscle. Data from Milner-Brown, H.S., et al., 1973. J.
Physiol. 230, 359 370 (Milner-Brown et al., 1973).

toward threshold is greatest in the small motor neurons

due to their greater input conductance (Ohm’s Law).
FIGURE 7.5 Recruitment of motor units during a voluntary contraction Consequently, the smallest (and weakest) motor neurons
with a hand muscle. (A) The recruitment of two motor units. Unit 1 has a
lower recruitment threshold force (down arrow) than unit 2 (up arrow).
will reach threshold and discharge action potentials with
(B) The average force produced by each motor unit as estimated with less excitatory synaptic input than larger motor neurons.
spike-triggered averaging. Unit 1 is weaker and has a longer time to peak The role of motor neuron size in establishing the recruit-
force. Adapted with permission from Desmedt, J.E., Godaux, E., 1977. J. ment order of motor units is known as the size principle
Physiol. 264, 673 693. (Duchateau and Enoka, 2011).
The last motor unit recruited during a gradual increase
in muscle force differs across muscles, ranging from 60%
The order in which motor units are recruited is highly to 85% of maximal force. Consequently, increases in
correlated with several indices of motor unit size, includ- muscle force beyond the upper limit of motor unit recruit-
ing the number of muscle fibers innervated by the motor ment depend solely on increases in discharge rate.
neuron. With the use of a technique known as spike- However, recruitment threshold and hence the upper limit
triggered averaging (Duchateau and Enoka, 2011), it has of motor unit recruitment decreases during fast contrac-
been shown that the recruitment thresholds of motor units tions (Fig. 7.7). For example, most motor units in a mus-
are linearly related to their peak twitch forces (Fig. 7.6). cle are recruited with a load of approximately 40% of
Spike-triggered averaging involves concurrently measur- maximum during the fastest (ballistic) contractions. The
ing the force exerted by a muscle during a voluntary con- speed-related reduction in recruitment threshold is neces-
traction and the discharge times of action potentials for a sary to accommodate the electromechanical delay
single motor unit. By averaging the muscle force for a between the timing of the action potential on the onset of
brief interval (B200 ms) each time an action potential is muscle force, and is produced by a more effective sum-
detected, the averaged force estimates the twitch force of mation of excitatory synaptic inputs onto motor neurons.
the motor unit (see examples in Fig. 7.5). The data in As indicated in Fig. 7.4B, maximal motor unit forces
Fig. 7.6 show that recruitment order, as indicated by require discharge rates $ 50 pps but the greatest changes
recruitment threshold, is linearly related to motor unit in motor unit force (i.e., the steepest part of the sigmoidal
force. relation) occurs at discharge rates in the range of
In addition to recruitment order being related to motor 10 20 pps. The only action for which discharge rates
unit force, it is also highly correlated with motor neuron achieve values on the plateau of the sigmoidal function
size. Indeed, it is the differences in motor neuron size that (Fig. 7.4B) is during ballistic contractions. Otherwise, the
are largely responsible for the orderly recruitment of observed discharge rates are typically # 35 pps during
motor units. When a motor nucleus receives excitatory such actions as force-matching tasks (Erim et al., 1996;
synaptic input, the depolarization of membrane potential Moritz et al., 2005), shortening and lengthening
 Muscle Function: Strength, Speed, and Fatigability Chapter | 7 135

FIGURE 7.7 Changes in motor unit

recruitment threshold and discharge rate
with increased rate of torque development.
Panel A illustrates the reduction in recruit-
ment threshold for 3 motor units in the
tibialis anterior with an increase in the rate
of force development during isometric
contractions performed with the ankle dor-
siflexor muscles. The inset shows the 6 dif-
ferent rates of increase in force to a target
of 120 N (B50% MVC), with the most
rapid contraction (B0.15 s to peak force)
at the left-hand side. Panel B displays the
discharge rate (Hz) of a motor unit during
a slow increase in force (ramp; a) and
during a contraction to a similar force but
performed as fast as possible (ballistic; b).
The change in motor unit discharge rate
during the two contractions is illustrated in
(c). Adapted from Desmedt, J.E., Godaux,
E., 1977. J. Physiol. 264, 673 693.

contractions (Pasquet et al., 2006), steady submaximal 7.3 MUSCLE FORCE

contractions (Almuklass et al., 2018; Negro et al., 2009;
Pascoe et al., 2014), and fatiguing contractions Once an activation signal has been received by a muscle
(Carpentier et al., 2001; Mottram et al., 2005). Except at fiber, it will engage the contractile proteins to produce a
the lowest forces, therefore, variation in discharge rate force that pulls on the skeleton and contributes to an
has a greater influence on muscle force than does changes intended action. The amplitude and timing of the force
in the number of active motor units (Enoka and produced by the activated muscle fibers depends on the
Duchateau, 2017). number of muscles that are activated, how they are
The sum of all the motor unit action potentials com- arranged in the muscle, and where the muscle attaches to
prise the neural drive to muscle, which establishes the the skeleton.
amplitude and time course of the force to be exerted by
the muscle. In contrast, the amplitude of a surface EMG
recording indicates the sum of the muscle fiber action
7.3.1 Sarcomere
potentials. Due to the nonlinear distribution of innervation The basic contractile unit of muscle is the sarcomere. It
number across the motor unit pool (Fig. 7.1), the ampli- comprises overlapping sets of thick and thin filaments
tude of the surface EMG signal does not provide an that are bounded by Z disks. Sarcomere length ranges
appropriate estimate of the neural drive to muscle (Enoka from 1.5 to 3.5 μm within and across muscles (see
and Duchateau, 2015). Chapter 2: Functional Morphology of the Striated Muscle).
136 SECTION | II Muscle Energetics and Its Performance

Each sarcomere contains the contractile proteins and bio- 7.3.2 Muscle Fiber Length
chemical compounds that are necessary for the generation
of force. Thousands of sarcomeres are connected end-to- Even with adequate levels of Ca21 and ATP, however,
end to form a myofibril, and a muscle fiber comprises the total amount of cross-bridge activity can be limited by
hundreds of myofibrils arranged in parallel to one the availability of binding sites on the thin filament. This
another. Moreover, the fibers in a muscle can be oriented can occur when the amount of overlap between the thick
in the same direction as the pulling force exerted by the and thin filaments changes during a contraction. As
muscle on the skeleton or, more typically, at an angle shown in Fig. 7.8, peak force (maximal cross-bridge
(pennation angle) to the direction of the pulling force activity) occurs at intermediate sarcomere lengths when
(Table 7.1). the number of available binding sites is maximal. At
Transformation of the activation signal (action poten- shorter and longer sarcomere lengths, the availability of
tial) into a muscle contraction begins with a series of pro- binding sites and hence sarcomere force decreases.
cesses known as excitation-contraction coupling. These In addition to the influence of sarcomere length on
processes enable the proteins that comprise the thick and muscle fiber force, the rate of change in sarcomere
thin filaments to interact with one another via several bio- length—contraction velocity—can influence the availabil-
chemical reactions and to produce a contractile force. The ity of binding sites and hence muscle fiber force. The
interaction that produces the force is known as the cross- peak force that a muscle fiber can produce, for example,
bridge cycle and involves one component of the myosin declines with an increase in velocity during shortening
molecule (thick filament) binding to actin (thin filament) contractions (Fig. 7.9). As the velocity at which the thick
and, in the presence of ATP, performing work. The force and thin filaments slide past one another increases, more
generated by a muscle fiber depends on the amount of available binding sites are missed by the attaching part of
cross bridge activity. the myosin molecule and there is a decrease in the aver-
Each cross-bridge cycle involves a detachment phase, age amount of work performed by each cross bridge.
an activation phase, and an attachment phase. The work In contrast to shortening contractions, the peak force
performed by the contractile proteins occurs during the that can be produced by a muscle fiber during a lengthen-
attachment phase when one part of the attached myosin ing contraction increases with velocity initially and then
molecule rotates and causes the thick and thin filament to plateaus (Fig. 7.9). Muscle fibers (and muscles) perform
slide relative to one another and decreases the length of lengthening contractions when the magnitude of the load
the sarcomere (5 10 nm/cross-bridge cycle). The cycling against which they are acting is greater than the force pro-
of the cross bridges during a sustained contraction con- duced by the fiber (Duchateau and Enoka, 2016). The
tinues as long as there are sufficient amounts of Ca21 and greater force capacity during lengthening contractions is
ATP in the muscle cell. When the action potential has attributable to the stretching of incompletely activated
passed, Ca21 is returned to its storage location and cross sarcomeres, an increase in cross-bridge force, a more
bridge cycling is terminated. rapid reattachment phase, and—most importantly—the

FIGURE 7.8 The force a muscle fiber can exert varies as a function of sarcomere length. The peak force occurs when the amount of overlap between
the thick and thin filaments is maximal. The graph shows the force (Relative tension) produced at five different sarcomere lengths varies with the
amount of overlap between the two sets of filaments. Adapted from Enoka, R.M., Pearson, K.G., 2013. Principles of Neural Science, fifth ed. McGraw
Hill: New York, pp. 768 788.
 Muscle Function: Strength, Speed, and Fatigability Chapter | 7 137

10

Estimated force (N)

6

0
0 2 4 6 8 10
Tetanic force (N)

FIGURE 7.10 The relation between observed and estimated maximal

FIGURE 7.9 The relation between force and velocity for a single fiber forces for 10 muscles in the hindlimb of an experimental animal. The mea-
from a frog muscle. Positive velocity indicates shortening contractions, sured maximal forces were evoked by electrical stimulation of the muscle
and negative velocity corresponds to lengthening contractions. The maxi- nerves at stimulus rates (200 Hz) that elicited tetanic force. The estimated
mal shortening velocity occurs when the fiber acts against a zero load. values were derived from measurements of muscle cross-sectional area.
Data from Edman, K.A.P., 1988. J. Physiol. 404, 301 321 (Edman, The graph shows a strong positive correlation between maximal force and
1988). the cross-sectional area of muscle. The slope of the regression line indi-
cates specific tension, which was 22.5 N/cm2. Data from Powell, P.L.,
et al., 1984. J. Appl. Physiol. 57, 1715 1721 (Powell et al., 1984).
engagement of a third contractile protein known as titin.
The force contributed by titin increases during the length-
ening of an activated sarcomere due to its ability to
increase stiffness. This is accomplished by titin binding The anatomical data for human leg muscles listed in
Ca21 and then attaching at specific locations on actin to Table 7.1 indicate that muscles analyzed from 21 cada-
reduce the length it can be stretched (Herzog et al., 2016). vers comprise various combinations of fiber length, mus-
The force produced by activated sarcomeres, therefore, cle cross-sectional area, and pennation angle. In the leg,
depends on the interactions of three filaments (actin, myo- for example, pennation angle ranges from 1 (sartorius) to
sin, and titin). 28 degrees (soleus) and 30 degrees (vastus medialis), fiber
length ranges from 4 (soleus) to 40 cm (sartorius), and
cross-sectional area ranges from 2 (sartorius) to 52 cm2
(soleus). These anatomical characteristics suggest that sar-
7.3.3 Muscle Fiber Anatomy
torius can experience the greatest amount of shortening
The force capacity of muscle is influenced by the anat- during a muscle contraction and it has the greatest maxi-
omy of its muscle fibers. The key parameters are the mal shortening velocity, but it is one of the weakest leg
length of the muscle fibers, the number of fibers arranged muscles. In contrast, soleus has a low capacity for short-
in parallel, and pennation angle. When a sarcomere is ening and maximal shortening velocity, but it is easily the
activated and the thick and thin filaments slide past one strongest of the leg muscles.
another, sarcomere length can decrease up to some limit Table 7.1 also indicates that muscle fiber length is
and by some maximal shortening velocity. The maximal usually less than muscle length, indicating that muscle
length a muscle fiber can shorten and its maximal short- fibers are often connected serially within a muscle and
ening velocity, therefore, depends on the number of sarco- has given rise to the term staggered muscle fibers. The
meres arranged in series within the myofibrils in the existence of staggered muscle fibers means that surround-
muscle fiber. In contrast, the length of a muscle fiber ing connective tissues must transmit the forces generated
does not influence the peak force it can produce. Rather, by individual muscle fibers so that they can contribute to
muscle fiber force depends on the number of contractile the muscle force (Harris et al., 2005; Hughes et al., 2015).
proteins that are arranged in parallel, which is estimated Functionally coupled muscles tend to have complemen-
by measuring the cross-sectional area of the muscle fiber. tary combinations of these properties. For example, the
This concept translates directly to muscle force vasti muscles have similar muscle fiber lengths (10 cm)
(Fig. 7.10). One of the reasons why muscle fibers are but they differ in pennation angle (intermedius is the
arranged with a nonzero pennation angle is to maximize smallest) and cross-sectional area (lateralis is the largest).
the cross-sectional area of muscle per unit volume of A similar relation exists for soleus and the two heads
tissue. (medial and lateral) of gastrocnemius (Table 7.1).
138 SECTION | II Muscle Energetics and Its Performance

7.3.4 Force Transmission to the Skeleton

In addition to the transmission of muscle fiber force by
connective tissues within a muscle, the force produced by
a muscle is transmitted through other connective tissues
to neighboring muscles and eventually to its attachments
on the skeleton. The connective tissues that distribute
muscle force beyond the active muscle comprise exten-
sive dense planar sheets that include septa, muscle envel-
opes, and joint capsules. These tissues are often referred
to as fascia. Significantly, fascia contains several types of
sensory receptors (e.g., free nerve endings, Ruffini end-
ings, and Pacinian corpuscles) that are innervated by
Group III IV afferents and seem to be capable of detect-
ing changes in pressure.
Bojsen-Møller et al. (2010) provided a convincing
description of the fascial connections between calf mus-
cles when they used ultrasound to measure the displace-
ment of muscle fascicles in soleus when the length of
gastrocnemius was increased by passively extending the
knee joint. With participants seated in a chair, the knee
joint was passively (10 degrees
s21) extended over a 90
degrees range and fascicle displacement for medial gas-
trocnemius and soleus was measured at several locations,
including attachments to the deep aponeurosis. Even
though the soleus muscle does not cross the knee joint,
passive extension of the knee joint caused the attachment
of the soleus fascicles to be displaced by 4.3 mm, which
is similar to the value for the medial gastrocnemius fasci-
cles (4.2 mm). This observation and several other mea-
surements performed in the study by Bojsen-Møller and FIGURE 7.11 The location of the attachment sites of a muscle on the
colleagues (2010) provide strong evidence for lateral skeleton influences its (A) moment arm relative to the joint and (B) the
variation in muscle torque as a function of joint angle. Adapted from
force transmission among the triceps surae muscles Rassier, D.E., et al., 1999. J. Appl. Physiol. 86, 1445 1457.
in vivo.
The functional attributes of muscle depend not only
on the characteristics of the force it transmits to the skele-
ton, but also where that force is applied on the skeleton
relative to the joints about which it acts. The critical a greater peak torque, but muscle A can produce its peak
action of muscle at the joint level is not the force it exerts, torque over a broader range of motion about the joint. As
but rather the torque—product of force and moment an example, consider the three major elbow flexor mus-
arm—it produces about a joint. The moment arm (some- cles: brachialis, biceps brachii, and brachioradialis. The
times referred to as the lever arm) corresponds to the per- three muscles have quite distinct attachment locations in
pendicular distance (length) from the muscle force vector the upper extremity, which means their torque profiles
to the joint about which the rotation occurs. Due to the about the elbow joint differ markedly. Similar distinctions
combined influence of force and moment arm on torque, are obvious among other groups of synergist muscles.
the capacity of a muscle to produce torque throughout the
range of motion about a joint is influenced by where the
muscle attaches on the skeleton.
Fig. 7.11 provides an example of this effect. Two sim-
7.4 MUSCLE FUNCTION
ilar muscles (A and B) share the same proximal attach- Human performance capabilities depend on at least three
ment site, but differ in the distal attachment locations on attributes of muscle function: strength, speed, and fatiga-
the skeleton and hence the distance from the force vector bility. The remaining sections of the chapter describe the
to the joint. The torque produced by the two muscles also key determinants of these attributes and the extent to
differs throughout the range of motion. Muscle B achieves which they can be modified by physical activity.
 Muscle Function: Strength, Speed, and Fatigability Chapter | 7 139

7.4.1 Strength and Power continuously. With this approach, the joint angle at which
the net torque is maximal can be easily determined. The
[Link] Assessment maximal torque for some muscles occurs in the middle of
The in vivo performance of a muscle or a muscle group is the range of motion (e.g., elbow flexors or extensors),
commonly evaluated by measuring its neuromechanical whereas for others it occurs closer to the end of the range
properties, which represent the bases for muscle function of motion (e.g., plantar flexors) (Fig. 7.12). This property
during movement. In laboratory or field settings, muscle explains why the failure angle usually occurs at B90
strength is often measured as either the maximal torque degrees of elbow-joint flexion for activities such as the
produced during a maximal voluntary contraction (MVC) push-up or pull-up, whereas it occurs at a greater plantar-
performed in an isometric condition at a specific joint flexion ankle angle for the calf-rise exercise.
angle or by the heaviest load that can be lifted for one Once activated, the action produced by a muscle
complete repetition (one-repetition maximum or 1 RM) of depends on the ratio of the net muscle torque to the load
an exercise. However, the MVC torque and the 1-RM torque. When muscle torque exceeds load torque, the
load may not represent the true maximal strength of a activated muscle performs a shortening (concentric) con-
muscle group. As the moment arm changes throughout traction. When a muscle is acting against an immovable
the range of motion, the torque produced by each muscle load or when the muscle torque equals the load torque,
varies accordingly and is typically greatest at the longest no displacement occurs about the joint and the resulting
moment arm. Consequently, the torque produced at the action is known as an isometric contraction. In contrast,
weakest point in the range of motion limits 1-RM load. when the load torque is greater than the muscle torque,
This is one of the reasons why training-related gains for the activated muscle is lengthened while resisting the
1-RM load can be sometimes disproportionally greater load torque. The gradual lengthening of a muscle by an
than MVC torque (Rutherford and Jones, 1986). applied torque is referred to as lengthening (eccentric)
To circumvent these problems, strength is often mea- contraction.
sured in laboratory settings as the peak torque produced The capacity of muscle during movement is com-
during movements performed at a constant angular veloc- monly characterized by its torque-velocity relation, which
ity (isokinetic contractions). Isokinetic dynamometers can be measured with an isokinetic dynamometer. When
control angular velocity throughout the range of motion the rotation about the joint occurs in the same direction
and the torque exerted by the limb is monitored as the displacement of the lever arm of the dynamometer,

FIGURE 7.12 The relation between the torque and the joint angle for the elbow flexor and plantar flexor muscles. Peak torque for the elbow flexors
occurs when the elbow angle is flexed to 90 degrees, whereas peak torque for the ankle plantar flexors occurs when the ankle is dorsiflexed at 15
degrees. Data for elbow flexors are from Pertuzon, E., 1972. C. R. Seances Soc. Biol. Fil. 165, 328 333 (Pertuzon, 1972) and plantar flexors from
Sale, D., et al., 1982. J. Appl. Physiol. 52, 1636 1642 (Sale et al., 1982).
140 SECTION | II Muscle Energetics and Its Performance

the muscle performs a shortening contraction. In contrast, As the product of force and velocity, the power
the muscles perform a lengthening contraction when produced by a muscle can be calculated from the force
resisting the motion of the lever arm. An example torque- (torque)-velocity relation. Peak power occurs at 30% 50%
velocity relation for the ankle dorsiflexor muscles of 10 of maximal velocity during shortening contractions
young adults (B25 year) is illustrated in Fig. 7.13 (Klass (Fig. 7.14). Muscle absorbs power from the applied load
et al., 2005). The data show that the peak torque produced (energy is transferred from the load to the limb) during
during shortening contractions decreases progressively as lengthening contraction. In many activities, the power
the angular velocity increases. Conversely, the peak tor- production capacity of muscle is more critical than its
que was greater during lengthening contractions than iso- strength. For example, power is a more discriminant pre-
metric contraction and remained relatively constant over dictor of functional limitations than maximal strength in
the range of angular velocities studied. The torque pro- older adults (Reid and Fielding, 2012). Similarly, the
duced during lengthening contractions, however, is not peak height a person can reach during a vertical jump is
always greater during maximal isometric contractions in more limited by the power capacity than the strength of
untrained individuals (Fig. 7.15C). the leg muscles (Voigt et al., 1995).
One limitation of isokinetic dynamometers is that the The torque-velocity relation measured in isolated mus-
greatest achievable velocity (B360 degrees
s21) is often cles or single muscle fibers in animal studies differs from
less than 50% of the velocity observed during natural con- in vivo measurements by two main characteristics: a lesser
ditions. Also, the torque-velocity relation measured with curvature for the shortening phase and a smaller difference
an isokinetic dynamometer may underestimate the force- between the torque produced during lengthening and
velocity capacity of muscle due to the variations in the isometric contractions. The less curved torque-velocity
rate of change in muscle length. This limitation can be relation of the shortening phase in human experiments can
partly overcome by modeling the geometry of the main be explained by the concurrent activation of several
muscles involved in the movement (Rassier et al., 1999; muscles (mono- and biarticular muscles) around the joint
Sartori et al., 2015) or by recording the rate of change in with different torque-velocity profiles that tend to linearize
the length of muscle fascicles by ultrasonography (Reeves the relation for the activated muscles. Furthermore,
and Narici, 2003; Pasquet et al., 2006). contractions evoked in human muscle by electrical
stimulation, as in animal studies, generate a more curved
torque-velocity relation than during voluntary activation

FIGURE 7.13 Torque-velocity relation for the ankle dorsiflexor mus- FIGURE 7.14 Torque-velocity and power-velocity relations computed
cles during voluntary contractions in a group of young men (B25 year in the adductor pollicis in response to tetanic contraction (80 Hz). Data
old). Data (mean 6 SEM; n 5 10) are expressed in percentage of the (mean 6 SEM; n 5 6) for the torque-velocity relation (black dots) are fit-
maximal torque recorded during the isometric condition. Positive veloci- ted by Hill’s equation and expressed as percentage of isometric torque.
ties indicate shortening contractions, whereas negative velocities indicate The power curve (dashed line) was computed from the torque-velocity
lengthening contractions. Data from Klass, M., et al., 2005. J. Appl. relation and is expressed as percentage of the maximal power. Data from
Physiol. 99, 31 38. de Ruiter, C.J., et al., 1999b. Eur. J. Appl. Physiol. 80, 386 393.
 Muscle Function: Strength, Speed, and Fatigability Chapter | 7 141

(Baudry and Duchateau, 2007b). This observation suggests This procedure assumes that the superimposed stimulation
that the less synchronous activation of muscle during a recruits muscle fibers that are not activated by the volun-
voluntary contraction relative to an electrically evoked tary effort, eliciting additional torque to the ongoing vol-
contraction further contributes to linearize the torque- untary action (Fig. 7.15A). When the applied stimulation
velocity relation. The functional significance of these fails to evoke extra torque, the activation is assumed to be
differences is that peak power during shortening contrac- maximal. The magnitude of voluntary activation can be
tions occurs at B33% of maximal load during electrically quantified with either of two methods: the interpolated
evoked contractions and B50% of maximal load during twitch ratio (ITR; Gandevia, 2001) or the central activa-
voluntary contractions. tion ratio (CAR; Kent-Braun and Le Blanc, 1996). The
ITR involves calculating the ratio of the superimposed
torque during the MVC relative to the evoked torque
[Link] Voluntary Activation measured at rest (control torque). Voluntary activation is
The maximal strength of a muscle can only be achieved expressed as a percentage and calculated as follows:
when all the motor units are recruited and activated at (1-superimposed torque/control torque) 3 100. The CAR
maximal discharge rates. A widely used technique to technique is defined as the proportion of the total torque
assess the ability of an individual to achieve complete attributable to voluntary activation, and is calculated and
activation of a muscle by the nervous command during an expressed as a percentage as follows: [MVC/(MVC 1
MVC is the “interpolated twitch” technique (Merton, superimposed torque)] 3 100.
1954). It involves superimposing a single, double, or brief Although these methods can detect whether or not vol-
train of supramaximal electrical stimuli during an MVC. untary activation is maximal, they cannot determine the

FIGURE 7.15 Assessment of muscle activation using the interpolated-twitch technique. It involves superimposing a single supramaximal electrical
stimulus or a short train of electrical stimuli during an MVC (A). The generation of extra force by the superimposed electrical stimulation (ES) during
the ongoing MVC force indicates that the subject is unable to produce a maximal activation of the muscle and there is a deficit in voluntary activation.
In B, the histograms show the mean deficit in activation (expressed in % of maximum) during an isometric MVC for selected muscles. In C, the
torque-velocity relation of the knee extensors is compared for voluntary activation alone (VA) and when electrical stimulation (ES) is superimposed
(VA 1 ES). The deficit in voluntary activation was mainly limited to the eccentric and isometric contractions. The first two panels (A and B) were
adapted from Kent-Braun, J.A., Le Blanc, R., 1996. Muscle Nerve 19, 861 869 and Behm, D.G., et al., 2002. Muscle Nerve 25, 236 243 (Behm
et al., 2002) and panel C was redrawn from Westing et al. (1990).
142 SECTION | II Muscle Energetics and Its Performance

source of the reduction, which could occur anywhere addition, initial gains in muscle strength during a training
from the motor cortex to the spinal motor neurons. Some program can be accompanied by a decrease in antagonist
insight on the location of the limiting mechanisms can be coactivation (Carolan and Cafarelli, 1992; Pensini et al.,
obtained with transcranial magnetic stimulation (TMS). 2002). In contrast, ageing is accompanied by an increase
The presence of extra torque in response to a superim- in antagonist coactivation (Klein et al., 2001; Hortobágyi
posed single TMS indicates that some of the deficit in and DeVita, 2006).
voluntary activation occurred at a cortical level. A similar
procedure to the ITR is used to quantify the deficit in vol-
untary activation with TMS except that: (1) the superim- [Link] Stretch-Shorten Cycle
posed torque is applied at three torque levels (50%, 75%, In many activities, a common pattern of muscle action
and 100% MVC); and (2) the stimulated torque at rest is during movements is to stretch an active muscle before
estimated from the y-intercept of the linear regression it performs a shortening contraction. This sequence of
between the amplitude of the superimposed torque evoked activity is known as the “stretch-shorten cycle” (Komi,
by TMS and the three torque levels rather than measured 2011). An example of its occurrence is lengthening and
directly (Todd et al., 2016). This extrapolation is neces- then shortening of plantar flexor and knee extensor mus-
sary to avoid methodological issues in the determination cles after foot strike in running. Soon after foot contact
of the level of voluntary activation due to the differences with the ground (braking phase), the leg extensor mus-
in corticospinal excitability when tested at rest and during cles resist the impact and undergo a lengthening con-
a contraction. traction, which is immediately followed by a shortening
Despite the limitations of the three methods (Shield contraction (push-off phase). Another example of the
and Zhou, 2004), the results indicate that many untrained stretch-shorten cycle is the golf swing. The trunk rota-
individuals exhibit a deficit in voluntary activation during tors and the left upper back and shoulder muscles (for
an isometric MVC. However, the level of voluntary acti- right-handed golfers) are stretched during the back
vation that can be achieved during an isometric contrac- swing and store elastic energy that accelerates the club
tion varies among muscles. For example, it is greater for during the shortening contractions involved in the
the knee extensors than the elbow flexors or ankle plantar downswing.
flexors (Behm et al., 2002; Fig. 7.15B). In contrast, the The advantage of the stretch-shorten cycle is that
deficit in voluntary activation is minimal for the dorsi- muscle can perform more positive work and produce
flexor muscles. Moreover, the deficit in voluntary activa- more power, and thus improve performance, when it is
tion is greater during lengthening contractions than actively stretched before being allowed to shorten than
isometric and shortening contractions (Fig. 7.15C; when it only performs a shortening contraction (Komi,
Westing et al., 1990; Amiridis et al., 1996). This differ- 2011). This specific behavior can be illustrated by com-
ence explains, at least in part, why the torque produced paring vertical jump height performed from a squat
by humans during lengthening contractions is not system- position (squat jump) or preceded by a countermove-
atically greater than that during isometric contractions or ment (countermovement jump) (Fig. 7.16). The counter-
does not increase in the same proportion as that observed movement jump (left part of Fig. 7.16) involved the
in animal studies (Fig. 7.9; Duchateau and Enoka, 2016). subject beginning from a standing position and flexing
However, the deficit in voluntary activation during the legs before jumping up. The squat jump, in contrast,
lengthening contractions can be reduced by training required a jump upward from an initial squatting posi-
(Amiridis et al., 1996), but tends to increase in most indi- tion (right part of Fig. 7.16) and involved a continuous
viduals with advancing age (Klass et al., 2007). extension about the ankle joint (1st trace from top) and
The deficit in voluntary activation may also involve shortening of the muscle fascicles (2nd trace) in the
both the relative activation of different motor unit pools medial gastrocnemius. In the countermovement jump,
and the connectivity within and between pools. These the muscle fascicles are first stretched when the ankle is
activations can modulate the amount of antagonist coacti- flexed during the initial part of the movement before
vation and the level of activation of the different synergist remaining at a nearly constant length (isometric contrac-
muscles. Although antagonist coactivation is often needed tion) for most of the downward phase and finally short-
to stabilize the joint, excessive activation of antagonist ening as the ankle extends. In many fast actions, the
muscles may counteract the torque produced by the ago- isometric phase between the lengthening and shortening
nist muscles. Training can reduce the level of coactiva- contractions is minimal (e.g., drop jumps; see Sousa
tion. For example, elite athletes exhibit less coactivation et al., 2007; Komi, 2011).
of the semitendinosus muscles compared with untrained Several mechanisms have been suggested to explain
individuals when performing isokinetic actions with the the superior muscle performance during the stretch-
knee extensors muscles (Amiridis et al., 1996). In shorten cycle. First, the muscle becomes more fully
 Muscle Function: Strength, Speed, and Fatigability Chapter | 7 143

Counter movement Squat FIGURE 7.16 Comparison of a counter-

movement jump (left) and a squat jump
Ankle joint angle (rad)

2.1
(right) performed by one individual. The
1.9 traces (top to bottom) show the changes
1.7 in ankle joint angle, length of muscle fas-
cicles in the medial gastrocnemius, verti-
1.5 cal ground reaction force (GRF), and
1.3 rectified EMG for medial gastrocnemius.
Reprinted from Kawakami, Y., et al.,
70 2002. J. Physiol. 540, 635 646
Fascicle length (mm)

(Kawakami et al., 2002).

60

50

40
1200
30
800

GRF (N)
400

0
1.5
EMG (mV)

1.0

0.5

0.0
–1.0 –0.8 –0.6 –0.4 –0.2 0 –0.8 –0.6 –0.4 –0.2 0
Time before toe-off (s)

activated after an initial lengthening due to the increase in

time to develop force relative to a shortening contraction
performed from a resting condition (Van Ingen Schenau
et al., 1997). As a consequence, the positive work (area
under the force-length curve) is greater during the stretch-
shorten cycle due to the greater force at the onset of the
shortening contraction. Second, energy is stored in the
series elastic components of the muscle-tendon unit dur-
ing the stretch phase and reused, as a spring, during the
subsequent shortening contraction (Komi, 2011). Third,
the stretch reflex elicited by the forced lengthening of the
muscle at the onset of the stretch-shorten cycle potentiates
the force produced during the shortening phase (Komi
and Nicol, 2011).
Although the relative contribution of these mechan-
isms to the increased positive work and power during the
stretch-shorten cycle can vary between different types of
actions and training status of individuals, the first-two FIGURE 7.17 Vertical jump height reached after drop jumps per-
mechanisms seem to be the main contributors to the formed from heights ranging from 20 to 100 cm in two elite athletes.
enhancement of muscle performance (Enoka, 2015). A Peak height (arrow) was achieved at a greater drop height for the triple
practical example of the influence of the stretch-shorten jumper relative to the sprinter.
cycle on the performance of elite athletes from different
athletic disciplines is shown in Fig. 7.17. The peak jump production by the utilization of elastic energy, it also
height is greater for drop jumps performed at a greater improves the economy at which a submaximal effort is
height for the triple jumper than for the sprinter. As the performed by reducing the contribution of metabolic
stretch-shorten cycle increases positive work and power energy to the total energy required by the activity.
144 SECTION | II Muscle Energetics and Its Performance

Interestingly, the inclusion of plyometric exercises that the increase in voluntary activation. Together, these
mimic and amplify the stretch-shorten cycle in the train- observations obtained with various methods indicate that
ing program of endurance runners improves both running agonist muscle activation is increased after strength train-
economy and performance (Spurrs et al., 2003). ing. Such adaptations, however, are largely limited to the
first few weeks of training and involve changes at both
supraspinal and spinal levels (Duchateau and Baudry,
[Link] Training Adaptations 2011). Because neural adaptations also include improve-
The neuromuscular system is highly adaptable and pro- ments in coordination among the involved muscles, the
vided the stimulus is adequate (i.e., overload principle), a increase in performance is relatively specific to the task
training program involving heavy loads will increase the being performed during training.
maximal strength of muscle. The strength gain can be Strength training also increases the intrinsic strength
attributed to changes in both the contractile properties of of a muscle. The magnitude of the adaptation can be
muscle and the neural drive to muscle (Duchateau et al., assessed in humans by recording the tetanic torque pro-
2006; Duchateau and Baudry, 2011). duced by a muscle in response to a train of supramaxi-
Some indirect evidence, such as the dissociation mal stimuli delivered to its motor nerve. Studies
between structural (muscle size) and functional changes, performed in humans with this approach have found an
suggests a role for neural adaptations in strength gains. increase in tetanic torque following heavy-load training
For example, a program of strength training can increase (.60% 1 RM; Duchateau and Hainaut, 1984, 1988;
the 1-RM load dramatically without any significant Davies et al., 1985) and is associated with an increase
changes in cross-sectional area of the muscle or the mus- in the torque produced by the individual motor units
cle fibers. Moreover, surface EMG activity during an (Hainaut et al., 1981).
MVC (Aagaard et al., 2000; Vila-Chã et al., 2010), At the muscle level, the increase in maximal strength
interpolated-twitch ratio (Amiridis et al., 1996; Pucci is usually associated with an increase in muscle mass.
et al., 2005), and discharge rate of motor units during Although two mechanisms can augment muscle mass—an
MVC (Kamen and Knight, 2004) have also been found to increase in the cross-sectional area of individual muscle
increase after strength training. Additional evidence fibers (hypertrophy) and the number of muscle fibers
comes from the comparison of the gains in MVC torque (hyperplasia)—most evidence favors the former as the
and tetanic torque after a training program. Duchateau primary mechanism. An additional training-related adap-
and Hainaut (1988), for example, observed a greater tation is the increase in pennation angle of muscle fasci-
increase in MVC (22%) than tetanic torque (15%) in the cles, which increases the force capacity per unit volume
adductor pollicis after 6 weeks of strength training of muscle (Aagaard et al., 2001).
(Fig. 7.18). The difference in the gains in torque (7%) The mechanism underlying muscle hypertrophy is an
between the two testing methods represents the extent of increase in protein synthesis over degradation, resulting
in a net contractile protein increase. This adaptation is
accompanied by the fusion of satellite cells with the mus-
cles fibers, which adds new nuclei to the existing fibers
and augments the number of sites for DNA transcription
in the muscle cell. The increase in protein synthesis fol-
lowing stress and strain induced by training on muscle
structures is mediated via mechano-transduction and
involves a number of intracellular signaling pathways
(Goldspink and Harridge, 2004; Thalacker-Mercer et al.,
2013; Marcotte et al., 2015). The functional outcome of
an increase in protein synthesis is an augmentation in the
number of actin and myosin filaments in each muscle
fiber, which increases the number of potential cross
bridges and thereby the force capacity of the muscle
fibers. These structural adaptations are slower than the
FIGURE 7.18 Comparison of the increase in strength of the adductor neural adaptations and take several weeks before contrib-
pollicis muscle when tested by a maximal voluntary contraction (MVC) uting to gains in muscle strength.
and maximal electrical stimulation (ES) after a 6-week strength-training
program with a load of B65% of maximum. The difference between the
Whereas adaptations in the force-generating capacity
increase in MVC torque (22%) and tetanic torque (15%) indicates the of muscle after training are relatively well characterized,
extent (7%) of the increase in neural adaptation. Data from Duchateau, adaptations in the passive (tendon) and active (cross
J., Hainaut, K., 1988. Med. Sci. Sports. Exerc. 20, 99 104. bridges) structures of the series elastic component and the
 Muscle Function: Strength, Speed, and Fatigability Chapter | 7 145

cytoskeletal structures responsible for force transmission [Link] Assessment

within the contracting muscle are less understood. One way to characterize the speed-related properties of
In addition to the described muscle adaptations, muscle during a voluntary contraction is to measure the
improvement in performance of the stretch-shorten cycle speed of a movement performed against an inertial load.
to exercise training can be related to changes in the series Speed can be measured either as the linear displacement
elastic component of the muscle-tendon complex. An of the load or the angular displacement about the joint. A
increase in the stiffness of the series elastic component complete characterization of the speed-related properties
may be suitable for transmitting the force more effec- of a muscle group involves measuring the load-velocity
tively (Cavagna et al., 1981) by reducing the time relation during shortening contractions and extrapolating
between the stretching and shortening phase (“coupling to the maximal velocity at zero load (Fig. 7.19;
time”; Ishikawa et al., 2005). In multijoint movements, Duchateau and Hainaut, 1984; Baudry and Duchateau,
such as drop jumps, preactivity of muscles increases after 2007b). High-speed ultrasonography can detect changes
plyometric training, which likely increases muscle-tendon in fascicle length and thereby estimate the instantaneous
stiffness at foot impact and produces greater stress in the shortening velocity during such contractions (Hauraix
muscle tendon and thereby increases the recoil of elastic et al., 2015) or natural movements (Ishikawa et al., 2005).
energy (Kyröläinen et al., 1991; Kubo et al., 2006). However, it is challenging to obtain accurate measure-
In addition to an increase in muscle activation preced- ments of the change in fascicle length during fast
ing the stretch-shorten cycle, Pousson et al. (1990) contractions.
reported an increased stiffness of the series elastic compo- Another way to assess the speed-related capacities is
nent, assessed by means of a quick-release technique in to record the rate at which an individual can develop tor-
the elbow flexor muscles after 6 weeks of training with que (RTD) during an isometric contraction. Because it
lengthening contractions. More recently, ultrasonography takes B300 ms to develop maximal muscle force, fast
measurements indicated that the stiffness of the tendon- movements typically involve less than the maximal force.
aponeurosis complex increased after a strength training An increase in RTD results in a greater area under the
with heavy loads (Kubo et al., 2001, 2006, 2007) and force-time curve (force impulse) that augments the subse-
lengthening contractions (Duclay et al., 2009). quent movement. RTD provides a better predictor of the
Surprisingly, training with plyometric exercises does not performance for fast actions than does either maximal tor-
appear to have much effect on tendon stiffness, but que or power (Maffiuletti et al., 2016). RTD can be mea-
because joint stiffness was increased during drop jumps sured during either of two tasks: (1) increase force as
after plyometric training, the main adaptations were pre- quickly as possible up to a target force that is maintained
sumably located in the contractile rather than in the ten- for a few seconds (step-and-hold contraction); and (2)
don structures (Kubo et al., 2007). Such adaptations of increase force as fast as possible followed by the relaxa-
cytoskeletal structures surely contribute to the increase in tion of the muscle immediately after the target force is
muscle stiffness and force transmission (Féasson et al., reached (ballistic contraction; Desmedt and Godaux,
2002; Woolstenhulme et al., 2005). Although the specific 1977). RTD is greater for ballistic contractions than for
mechanisms remain to be determined, it is clear that the step-and-hold contractions (Duchateau and Baudry,
structures associated with force transmission adapt to 2014). As the upper limit of motor unit recruitment in
chronic loading of the muscle-tendon complex and con- tibialis anterior declines from B90% of maximal force
tribute, in addition to contractile properties and voluntary during slow contractions down to B40% of maximum
activation, to increase the rate at which force can be during rapid contractions (Fig. 7.7; Desmedt and Godaux,
developed. 1977; Van Cutsem et al., 1997), discharge rate assumes a
more prominent role in the control of muscle force during
fast contractions. Ballistic contractions are characterized
7.4.2 Speed-Related Properties by a high initial discharge rate (60 120 pps) at the onset
of activation (Desmedt and Godaux, 1977; Bawa and
The performance of the neuromuscular system can also be Calancie, 1983; Van Cutsem et al., 1998; Van Cutsem
characterized by the speed at which the muscles can con- and Duchateau, 2005; Klass et al., 2008a).
tract and produce fast movements. This involves measur-
ing either the rate at which muscle develops force or the
maximal speed achieved when moving inertial loads. In [Link] Voluntary Activation
this section, the term “rate of torque development” (RTD) The maximality of voluntary activation during fast
will be used to characterize a rapid action performed dur- actions can be evaluated by comparing contractions gen-
ing isometric contractions and “speed” will be used when erated by voluntary activation and electrical stimulation
referring to movements performed as quickly as possible. (de Ruiter et al., 2004; Klass et al., 2008a). The
146 SECTION | II Muscle Energetics and Its Performance

FIGURE 7.19 Relations between load and

velocity for tetanic (train of 15 pulses at a fre-
quency of 250 Hz) (A) and voluntary (B) con-
tractions performed before (dashed line) and
1 min after (continuous line) a 6-s MVC. The
insert in A shows the displacement traces (top)
and their first derivative (bottom) for tetanic
contractions against the various loads in con-
trol condition for one of the 10 subjects. All
relations were fitted with Hill’s equation to
calculate power before (dashed line) and
1 min after (continuous line) the 6-s MVC.
* Significant difference (P ,.05) with control
values. Data from Baudry, S., Duchateau, J.,
2007b. J. Appl. Physiol. 103, 1318 1325.

intrinsic speed-related properties of a muscle, indepen- Comparison of RTD during contractions generated by
dent of the neural drive to muscle, can be assessed voluntary activation and maximal electrical stimulation
during electrically evoked isometric and shortening con- indicates that for most individuals it is less during volun-
tractions. Due to the submaximal activation of muscle tary activation (Maffiuletti et al., 2016). Despite consider-
in response of a single electrical stimulus, the maximal able variability among subjects, the force attained 40 ms
speed capacity of muscle should be measured during after the onset of a rapid voluntary knee extension was
tetanic contractions (Duchateau and Hainaut, 1984). As less (260%) than for an electrically evoked contraction
for voluntary activation, the speed of movement against (Fig. 7.20; de Ruiter et al., 2004). Similarly, the maximal
different loads can be measured during tetanic contrac- movement velocity extrapolated from the load-velocity
tions and the load-velocity relation computed (Fig. 7.19; relation in the adductor pollicis was greater during an
Duchateau and Hainaut, 1984; Baudry and Duchateau, electrically evoked contraction than a voluntary contrac-
2007b). In the isometric condition, the ascending tion (Baudry and Duchateau, 2007b). Together, these
phase of the tetanic force profile is used to measure observations suggest that voluntary activation is less than
the RTD (Duchateau and Hainaut, 1984; Baudry and maximal at the onset of a fast contraction in most indivi-
Duchateau, 2007a). duals (Duchateau and Baudry, 2014).
 Muscle Function: Strength, Speed, and Fatigability Chapter | 7 147

FIGURE 7.20 Illustration of the early phase of the torque- and EMG-time curves of the knee extensor muscles in two subjects during a rapid volun-
tary isometric contraction (continuous line) and in response to electrical stimulation (8 pulses at 300 Hz; dashed line). The rate of torque development
during the two contractions was similar for subject 2 (B), but substantially less during voluntary activation for subject 1 (A). Note that EMG activity
(expressed as % of EMG during MVC) for the vastus lateralis was much greater at the onset of muscle activation for subject 2 (D) than for subject 1
(C). These data indicate that the rate of torque development was mainly limited by muscle activation (neural factors) in subject 1, whereas it was
more likely constrained by muscular factors in subject 2. Arrows and vertical lines indicate, respectively, the onset of torque development and the
force attained 40 ms after the onset of the contraction. Adapted from de Ruiter, C.J., et al., 2004. J. Appl. Physiol. 97, 1693 1701.

The intrinsic speed-related properties of muscle and Ca21 activation due to phosphorylation of the myosin
its RTD are constrained by other factors in addition to light chains and intensification of Ca21 kinetics.
neural drive. These other factors include myosin ATPase
activity, the rate of Ca21 release, and the stiffness of the
muscle-tendon complex (Maffiuletti et al., 2016). [Link] Speed-Related Adaptations
Moreover, contractile speed can be further influenced The maximal discharge rate of motor units achieved dur-
acutely by such factors as muscle temperature and postac- ing ballistic contractions is adaptable. For example, sev-
tivation potentiation. For example, an increase in muscle eral weeks of training the ankle dorsiflexor muscles to lift
temperature is known to increase the maximal speed of a moderate inertial load (30% 40% of maximum) with
shortening and peak power in the adductor pollicis (de rapid contractions increased both the RTD (82% of initial)
Ruiter and de Haan, 2000) and the maximal RTD induced and the average discharge rate of motor units in the tibia-
by tetanic contraction (de Ruiter et al., 1999a). Similarly, lis anterior at the onset of a ballistic contraction
performance of a maximal voluntary or electrically evoked (Fig. 7.21; Van Cutsem et al., 1998). In addition, training
contraction B1 2 min before a fast action transiently with rapid contractions increased the number (from 5% to
increases both movement speed and RTD (i.e., postacti- 33%) of motor units that exhibited double discharges with
vation potentiation) without any change in maximal discharge rates greater than 200 pps at the onset of the
strength (Fig. 7.19; Baudry and Duchateau, 2007a,b). contraction. Because the average rate of increase in the
Postactivation potentiation is likely attributable to an spike-triggered average torque for single motor units was
increase in the sensitivity of the contractile proteins to not statistically changed after the training intervention,
148 SECTION | II Muscle Energetics and Its Performance

FIGURE 7.21 Comparison of motor unit activ-

ity during ballistic contractions performed before
(A) and after (B) 3 months of dynamic training.
Traces correspond to the ankle dorsiflexor torque
(a) and intramuscular EMG plotted at slow (b)
and expanded (c) time scales. Panel A shows the
typical discharge pattern of a motor unit the
untrained tibialis anterior muscle, comprising a
longer interspike interval between the first two
spikes (action potentials). Panel B illustrates the
usual motor unit pattern after training, which
included a high initial instantaneous discharge
frequency that was maintained during the subse-
quent spikes. The asterisks indicate the discharge
frequency of the same motor unit and their traces
are superimposed with an expanded time scale
(b). Panel C indicates the mean maximal dis-
charge frequency (averaged for the first three
interspike intervals) during ballistic contractions
for motor units before and after training. Panel D
shows the percentage of motor units from the
total sample that displayed double discharges of
# 5 ms before and after training. ***Denotes sig-
nificant difference (P , .001) before and after
training. Data from Van Cutsem, M., et al., 1998.
J. Physiol. 513, 295 305.

the marked increase in whole-muscle RTD during ballistic 7.4.3 Fatigability

contractions was attributable to the adaptations in maxi-
mal discharge rate. Other studies have shown, however, In discussing the capacity of the neuromuscular system to
that training with fast contractions can increase the intrin- sustain physical activity, it is critical to distinguish
sic RTD of the muscle (Duchateau and Hainaut, 1984) between the concepts of fatigue and fatigability. Fatigue
and myofibrillar ATPase activity (Bell et al., 1992). is a symptom that characterizes the current capacity of an
These findings suggest that the initial component of individual to perform work. It can only be measured by
the increase in force during rapid contractions is con- self-report based on sensations experienced either recently
strained by the capacity of motor units to discharge action (preceding several days) or at a specific moment in time.
potentials at high rates. This association and the underly- These two measurements quantify fatigue as either a trait
ing mechanisms have been further examined with a characteristic or a state variable, respectively. In studies
computational model (Fuglevand et al., 1993). When the of clinical populations, participants are often character-
motor units in the model were assigned experimentally ized with a measurement of the trait level of fatigue,
observed contractile properties (Van Cutsem et al., 1998), which can be obtained with an instrument that has been
an increase in peak discharge rates to the range of validated for the cohort. Some of the available instru-
100 200 pps substantially augmented the RTD for all ments include Brief Fatigue Inventory (cancer), Center of
motor units in the population (Duchateau and Baudry, Epidemiologic Studies Depression Scale (individuals who
2014). Further increases in discharge rate only increased may be depressed, such as older adults), Chalder Fatigue
RTD for the fastest-contracting motor units, as expected Scale (chronic fatigue syndrome), Fatigue and Energy
from the difference in speed-related properties of low- Scale (chronic fatigue syndrome), Fatigue Severity Scale
and high-threshold motor units. Taken together, these (a range of clinical conditions), Modified Fatigue Impact
experimental and modeling studies underscore the critical Scale (multiple sclerosis), Multidimensional Fatigue
role of the nervous system in limiting the RTD develop- Inventory (a range of clinical conditions), Profile of
ment at the onset of rapid contractions (Duchateau and Mood States (general population), and Short Form-36
Baudry, 2014; Enoka and Duchateau, 2017). Vitality subscale (a range of clinical conditions). These
 Muscle Function: Strength, Speed, and Fatigability Chapter | 7 149

instruments provide a measure of the level of fatigue fatigability. For example, the Pittsburgh Fatigability Scale
experienced by the individual in the preceding days to asks respondents to rate (0 5 no fatigue; 5 5 extreme
weeks (Enoka and Duchateau, 2016). fatigue) the level of fatigue they expect to experience when
The Fatigue Severity Scale, for example, quantifies performing five physical and five cognitive tasks (Glynn
the influence of fatigue on activities of daily living. It et al., 2015). The score provides a measure of perceived
asks respondents to rate the following nine questions on a fatigability; that is, the ratings indicate how well the respon-
scale of 1 (strongly disagree) to 7 (strongly agree) based dents anticipate they would do on the ten tasks. Perceived
on their experiences during the previous week: fatigability as assessed with the Pittsburgh Fatigability
Scale is able to predict future declines in mobility of older
1. My motivation is lower when I am fatigued.
humans (Simonsick et al., 2016).
2. Exercise brings on my fatigue.
At the other end of the performance spectrum, elite
3. I am easily fatigued.
endurance athletes interpret sensory feedback signals to
4. Fatigue interferes with my physical functioning.
provide a measure of perceived fatigability. The percep-
5. Fatigue causes frequent problems for me.
tions inform the athlete about the expected rate of change
6. My fatigue prevents sustained physical functioning.
in key homeostatic variables so that performance can be
7. Fatigue interferes with carrying out certain duties and
maximized. This involves adjusting their work rate so that
responsibilities.
the challenge to homeostasis does not compromise energy
8. Fatigue is among my three most disabling symptoms.
expenditure. The adjustments are referred to as a pacing
9. Fatigue interferes with my work, family, or social life.
strategy (Hettinga et al., 2012; St Clair Gibson et al.,
The responses are quantified as the average rating for 2013). For example, the power produced by the legs of
the nine statements. An average rating of $ 4.0 represents elite cyclists declines with an increase in time-trial dis-
a clinically significant level of fatigue (Learmonth et al., tance, but nonetheless it varies during the course of the
2013). time trial depending on the perceived rating of exertion
The momentary level of fatigue, which quantifies (Fig. 7.22). Indeed, performance by elite endurance ath-
fatigue as a state variable, is measured with such self- letes is often regulated by the rate of change in the rating
report scales as a Visual Analog Scale, a Rating of of perceived exertion (perceived fatigability), which is
Perceived Exertion, or the fatigue scale from the Profile of derived from both outgoing motor commands and incom-
Mood States questionnaire. When using a Visual Analog ing sensory signals (Joseph et al., 2008; Zwart et al.,
Scale, for example, a respondent is presented with a 10 cm 2009; Levels et al., 2014).
line and asked to place a mark on the line to indicate the
level of fatigue “right now.” The scale is anchored by
“fatigue is absent” on the left “most fatigue ever” on the [Link] Fatigue Taxonomy
right. Such scales are typically used to measure changes in On the basis of these distinctions between fatigue and
fatigue during various physical and cognitive challenges. fatigability, Enoka and Duchateau (2016) proposed a tax-
In contrast, fatigability refers to how long it takes a per- onomy that provides a conceptual framework for the
son to reach a prescribed level of fatigue. A person who is study of fatigue (Fig. 7.23). In this scheme, the symptom
less fatigable can perform more work before achieving a of fatigue emerges from interactions between the two
target level of fatigue. In terms of work capacity, fatigabil- domains of fatigability (performance and perceived fatiga-
ity can be measured as the change in an outcome variable bility). Performance fatigability corresponds to the rate of
during or after an intervention. For example, the reduction decline in an objective measure of performance due to
in the MVC force, the time to task failure, the decrease in adjustments that compromise either the contractile func-
peak power production, the decline in foot-tapping speed, tion of muscle or the capacity of the nervous system to
time to complete a time trial, distance completed in a test provide an activation signal. In the other domain, per-
of walking endurance, and the number of errors when per- ceived fatigability is derived from sensations that regulate
forming the Stroop test. Consequently, a person who the integrity of the performer based on either the psycho-
experiences less of a reduction in MVC force after per- logical state of the individual or the physiological capac-
forming a prescribed protocol is less fatigable than one ity to maintain homeostasis.
who exhibits a greater decrease in MVC force. An important feature of this taxonomy is to recognize
But fatigability actually has two domains: performance that there are often interactions between the two fatigabil-
fatigability and perceived fatigability. Changes in an out- ity domains. For example, 77% of the variance in the
come variable described in the preceding paragraph pro- level of fatigue exhibited by persons with multiple sclero-
vide a measure of performance fatigability. In addition, it is sis (score on the Fatigue Severity Scale) was explained by
possible to obtain a measure of fatigability for actions that the strength of a hand muscle, the decline in MVC force
have not yet been performed; this is known as perceived during a sustained isometric contraction (performance
150 SECTION | II Muscle Energetics and Its Performance

(A) 400 fatigability), and the level of depression (perceived fatiga-

bility) (Steens et al., 2012). Similarly, the time it took
trained cyclists and triathletes to complete a time trial was
350
altered by the oral ingestion of neurotransmitter reuptake
Power (W)

inhibitors, and this was accompanied a depression of vol-

300 untary activation (performance fatigability) and a decline
in attention (perceived fatigability) but no change in the
final value for the rating of perceived exertion (Klass
250
et al., 2012). Moreover, the decline in maximal force
exerted by the knee extensors during a 2 min isometric
200 contraction (a measure of performance fatigue) was
0 0.2 0.4 0.6 0.8 1 greater after participants had cycled in the heat for 60 min
Time (relative to end) and was accompanied by a greater reduction in voluntary
activation (Nybo, 2008). According to the taxonomy, the
(B) 10 prior exercise in the heat would have imposed a homeo-
Rating of perceived exertion

9 static challenge (elevated core temperature) that persisted

during the subsequent test of performance fatigability.
8
These examples demonstrate that differences in fatigue
7 and fatigability depend on the characteristics of the indi-
vidual (e.g., age, sex, neurological health, hydration sta-
6
tus), the environmental conditions at the time of testing
5 (e.g., altitude, ambient temperature, relative humidity),
and the details of the task being performed (Enoka and
4
Stuart, 1992). Due to these interactions, alleviating the
3 symptom of fatigue in clinical populations requires inter-
0 0.2 0.4 0.6 0.8 1 ventions that target the pathological changes responsible
Time (relative to end) for the illness (Kluger et al., 2013; Penner and
Friedmann, 2017). Similarly, the influence of environ-
FIGURE 7.22 Average power production on an electrically braked mental conditions and task details on fatigability demands
cycle ergometer (A) and rating of perceived exertion (B) by 10 cyclists
during simulated time trials for 2.5 (filled circles), 5 (open circles), and
that the tests used in an assessment of fatigability chal-
10 (filled triangles) km. Data from Joseph, T., et al., 2008. Med. Sci. lenge the adjustments that constrain performance on func-
Sports. Exerc. 40, 381 386. tionally meaningful tests (Enoka and Duchateau, 2016).

[Link] Task Dependency

Fatigue The task details that can influence the rate-limiting
mechanisms and thereby constrain fatigability include con-
Perceived fatigability Performance fatigability traction intensity (target force and duty cycle), the type of
load supported by the limb, the type of muscle contrac-
tion (isometric, lengthening, or shortening), the number
Homeostasis Psychological Contractile Muscle
state function activation of muscle groups engaged in the task, and the cognitive
• Blood glucose • Arousal • Calcium kinetics • Voluntary activation demands of the activity. For example, the target force sus-
• Core temperature • Executive function • Force capacity • Activation patterns tained during an isometric contraction will influence the
• Hydration • Expectations • Blood flow • Motor neurons
• Neurotransmitters • Mood • Metabolism and • Afferent feedback extent to which adjustments in muscle activation contrib-
• Metabolites • Motivation products • Neuromuscular
• Oxygenation • Pain propagation
ute to the different declines in MVC force (a measure of
• Wakefulness • Performance performance fatigability). When sustaining an isometric
feedback
contraction with the elbow flexors (Gandevia et al., 1996;
FIGURE 7.23 Fatigue as a symptom that emerges from interactions Søgaard et al., 2006), MVC force decreased to 30% of the
between two fatigability domains. Fatigue is defined as a symptom that initial value during a 1.5 min maximal contraction whereas
depends on the physiological properties that establish a level of perfor- it declined to 60% of the initial value after 45 min of
mance fatigability for a specific action in combination with baseline matching a target force of 15% of maximal (Fig. 7.24).
values and rates of change in physiological and psychological factors
that influence perceived fatigability. Reproduced with permission from Significantly, the measurement of muscle activation—
Enoka, R.M., Duchateau, J., 2016. Med. Sci. Sports. Exerc. 48, voluntary activation (Klass et al., 2007)—decreased more
2228 2238. during the low-force contraction ( 30% of initial)
 Muscle Function: Strength, Speed, and Fatigability Chapter | 7 151

(A) 100 100 (A)

Voluntary activation (%)

MVC force (% initial)

80 80

60 60

40 40

20 20

0 0
0 0.3 0.6 0.9 1.2 1.5
Time (min)

(B) 100 100

Voluntary activation (%)

MVC force (% initial)

80 80
(B)

60 60

40 40

20 20

0 0
0 5 10 15 20 25 30 35 40 45
Time (min)

FIGURE 7.24 Decline in maximal voluntary contraction (MVC) force

(gray circles) and voluntary activation (black circles) during isometric
contractions sustained at (A) maximal and (B) submaximal (15%; dashed
line) target forces with the elbow flexor muscles. Data are mean 6 SE.
The subject was seated with the upper arm placed in a horizontal posi-
tion, the elbow resting on a support with the elbow joint at a right angle,
and the wrist pulling against a load. Data were obtained from (A) FIGURE 7.25 Changes in the discharge characteristics (mean 6 SE) of
Gandevia, S.C., et al., 1996. J. Physiol. 490, 529 536 and (B) Søgaard, action potentials by motor units in biceps brachii during force and position
K., et al., 2006. J. Physiol. 573, 511 523. control. (A) The decline in discharge rate for the same motor units (n 5 32)
was greater during position control than force control. (B) Coefficient of
variation (CV) for discharge times did not change during force control, but
increased during position control presumably due to differences in synaptic
input onto motor neurons. Data from Mottram, C.J., et al., 2005. J.
Neurophysiol. 93, 1381 1392.

compared with the maximal contraction ( 20% of initial).

This result indicates that a greater amount of the perfor-
mance fatigability (decrease in MVC force) was explained are referred to as position control and force control,
by a depression of muscle activation during the longer, respectively. The rate of change in motor unit activity,
low-force contraction. including the decrease in discharge rate (Fig. 7.25) and
At target forces # 30% of maximum, the duration that the increase in discharge variability, is more rapid during
an isometric contraction can be sustained—time to task position control than force control (Baudry et al., 2009;
failure—is less when the limb supports an inertial load Gould et al., 2016). Moreover, the responsiveness of spi-
than when it pulls against a rigid restraint (Hunter et al., nal reflex pathways, such as presynaptic inhibition of
2002; Maluf and Enoka, 2005; Rudroff et al., 2011). In group Ia afferents onto motor neurons, occurs more rap-
both tasks, the subject is required to match a target dis- idly during position control than force control (Baudry
played on a monitor, but the target comprises a joint angle et al., 2011). Due to the similar net muscle torque and
when supporting the inertial mass and an applied force EMG amplitude at failure for the two tasks, the different
when pulling against the restraint. These two conditions time course of the decrease in Ia presynaptic inhibition
152 SECTION | II Muscle Energetics and Its Performance

suggests qualitative differences in the synaptic input and knee extensors and longest for the plantar flexors,
received by the motor neurons during the two tasks (Klass even though there were no statistically significant differ-
et al., 2008b). ences in the decrease in MVC force immediately after
Rehabilitation exercises analogous to force and position task failure (Table 7.2). Performance fatigability in this
control are known as closed- and open-chain kinetic exer-
cises, respectively. When performing a knee extension
exercise, the foot exerts a force on the ground during
(A)
closed-chain exercises, whereas the lower leg acts against
an external load during open-chain exercises (Fleming
et al., 2005). Consistent with the differences in time to task
failure for force and position control, the amount of quadri-
ceps muscle activity—as indicated by shifts in signal inten-
sity detected in magnetic resonance images—was greater
when the knee extension exercise involved an open-chain
exercise than for a closed-chain exercise (Enocson et al.,
2005). The greater demand on muscles during position
control is the basis of some training techniques, such as
those that use straps to support the body against gravity in a
range of postures (TRX Suspension Training).
In addition to the influence of load type on perfor-
mance fatigability, the decline in outcome measures dif-
fers across contraction types. For example, Baudry et al. (B)
(2007) found that the decline in MVC torque for the ankle
dorsiflexor muscles during a series of maximal dynamic
contractions was greater for shortening contractions than
for lengthening contractions, for both young and old
humans (Fig. 7.26). The decrease in MVC torque exhib-
ited by the young adults after the 150 contractions was
40.9% for the shortening contractions and 27.1% for the
lengthening contractions, compared with reductions of
50.2% and 42.1%, respectively, for the old adults. The
old adults, therefore, demonstrated greater performance
fatigability than the young adults for both types of muscle
contractions during this protocol.
Due to differences in the functional demands experi-
enced by various muscle groups during activities of daily FIGURE 7.26 Decline in MVC torque (mean 6 SE) for the ankle dor-
siflexor muscles during protocols that comprised 5 sets of 30 maximal
living, the decline in MVC torque during fatiguing con-
shortening (open circles) or lengthening (filled circles) contractions on
tractions can differ across muscle groups. When sustain- an isokinetic dynamometer. (A) Young adults (31 6 3 years). (B) Old
ing an isometric contraction at 50% MVC force, for adults (77 6 1 years). Data from Baudry, S., et al., 2007. Eur. J. Appl.
example, time to failure was shortest for the elbow flexors Physiol. 100, 515 525.

TABLE 7.2 Times to Failure and Neuromuscular Adjustments (Mean 6 SD) for Four Muscle Groups When Sustaining a
Submaximal (50%) Isometric Contraction

Outcome Elbow Flexors Knee Extensors Thumb Abductor Plantar Flexors

Time to failure (s) 72 6 14 77 6 25 114 6 27 220 6 64
MVC force (%Δ) 2 40 6 12 2 34 6 15 2 37 6 13 2 30 6 11
Voluntary activation (%Δ) 2 6 6 13 2 5 6 10 2 2 6 11 2 13 6 6
Twitch force (%Δ) 2 59 6 15 2 28 6 15 2 60 6 24 2 7 6 12

Source: Data from Neyroud, D., et al., 2013. J. Appl. Physiol. 114, 1426 1434.
 Muscle Function: Strength, Speed, and Fatigability Chapter | 7 153

study, therefore, was greatest for the elbow flexors and one study, Steens et al. (2012) attempted to explain the
knee extensors, and least for the plantar flexors. Muscle fatigue (Fatigue Severity Scale) reported for persons with
activation, as indicated by voluntary activation, was not multiple sclerosis (5.3 6 0.9) relative to the values of for
compromised for the most fatigable muscle groups, but age- and sex-matched control subjects (2.9 6 0.6). The
was slightly depressed for the least fatigable muscle group outcome measures included the strength (MVC force),
(plantar flexors). Moreover, the reduction in the potenti- voluntary activation, and performance fatigability (force
ated twitch force was significant for the two muscle and EMG) of a hand muscle, and a depression score
groups in the upper limb, but not those in the lower limb. (Hospital Anxiety and Depression Scale questionnaire).
Thus, the adjustments during the fatiguing contraction Performance fatigability was quantified as the decline in
(sustained, submaximal isometric contraction) differed force during a 2-min maximal isometric contraction.
across the four muscle groups and there was no correla- Multiple regression models were able to explain signifi-
tion in the time to failure for pairs of muscle groups cant amounts of the variance in the fatigue score for the
within subjects. multiple-sclerosis group (R2 5 0.77), but not the control
group. The model that explained most the variance in
fatigue score comprised three predictor variables: perfor-
[Link] Translation to Human Performance mance fatigability (decrease in MVC force), muscle
The influence of task details on the adjustments observed strength (MVC force), and perceived fatigability (depres-
during fatiguing contractions underscores the importance sion). The fatigue reported by persons with multiple scle-
of ensuring that tests of fatigability are based on protocols rosis, therefore, is attributable to changes that occur in
that predict performance on functional tests. For example, both fatigability domains. Not surprisingly, clinical treat-
the time it takes trained cyclists to complete a time trial is ments for depression can reduce the fatigue experienced
strongly associated with the value for critical power by individuals with multiple sclerosis (Kluger et al.,
(Black et al., 2014), which can be assessed with a 3-min 2013).
laboratory protocol (Vanhatalo et al., 2007). As described
in more detail in the chapter on critical power
(Chapter 10: The Coupling of Internal and External Gas 7.5 CONCLUSIONS
Exchange During Exercise), the value for critical power The functional capabilities of muscle are characterized by
has been characterized as the greatest exercise intensity at its strength, contractile speed, and fatigability. Muscle
which the physiological adjustments can accommodate the strength—at least during isometric contractions—largely
challenge to intramuscular homeostasis (Jones et al., depends on the cross-sectional area (number of muscle
2010). The adjustments that may influence critical power fibers in parallel) and is usually not limited by the capac-
range from sodium-potassium pump activity in muscle ity of the nervous system to provide an activation signal.
fibers (McKenna et al., 2006) to the ability to sustain max- In contrast, contractile speed (rate of increase in muscle
imal levels of voluntary activation (Klass et al., 2012). force during a fast contraction) is mainly determined by
In a cohort of 1155 humans (65 102 years), the rate at which motor units generate action potentials
Vestergaard et al. (2009) found that those individuals who and less influenced by the properties of muscle fibers.
reported functionally significant levels of fatigue exhib- The factors that establish fatigability for a given individ-
ited lower average speeds when performing a test of ual, however, depend on how it is measured, and can
walking endurance. Fatigue was quantified with the range from an inability to maintain homeostasis through
Center of Epidemiologic Studies Depression Scale on the to the person’s mood state. Studies on the mechanisms
basis of experience in the preceding week; 29.1% of the that limit the ability to sustain physical activity, therefore,
women and 15.3% of the men reported an elevated level must be based on fatigability protocols than can predict
of fatigue. Those old adults who self-identified as being performance on an intended functional task.
fatigued had weaker handgrip strength, greater activity
limitations, and worse walking endurance than those who
did not report being fatigued. The whole-body measure of REFERENCES
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et al., 2018). A., Magnusson, S.P., et al., 2001. A mechanism for increased con-
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Almuklass, A.M., Davis, L., Hamilton, L.D., Vieira, T., Botter, A., Cavagna, G.A., Citterio, G., Jacini, P., 1981. Effect of speed and extent
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