Download Chapter 7: Skeletal Muscle

Chapter 7:
Skeletal Muscle
Purpose
1.
Describe skeletal muscle structure.
2.
Describe the passive and active properties of skeletal muscle.
3.
Relate muscle structure to function.
4.
Describe how muscles can be injured and how they are repaired.
5.
Describe how muscles change with aging and adapt to exercise and disuse.
Muscle Structure:
During the past century, extensive investigations have revealed the general structure and
function of skeletal muscle. Though much is known about the structural organization of muscle,
the constitutive equations describing its behavior have yet to be derived. Descriptions of the
contractile characteristics of muscle and structure/function relationships are given in the
following section. In this section emphasis is placed on describing the structural organization of
skeletal muscle. The description begins at the level of the gross whole muscle and proceeds to
the smaller subunits, concluding with the proteins making up the myofilaments. The description
given here is quite detailed since muscle behavior is directly related to its structure. An
understanding of the material in this section will greatly facilitate understanding the material that
follows.
Muscle is composed of many subunits and complex structural arrangements (see Figure
1). Whole muscle is surrounded by a strong sheath called the epimysium. The gross muscle is
divided into a variable number of subunits called fasciculi. Each fasciculus is surrounded by a
connective tissue sheath called the perimysium. Fascicles may be further divided into bundles of
fibers (or muscle cells) which are surrounded by a sheath called the endomysium (Fung, 1981;
Anthony and Thibodeau, 1983; Ishikawa, 1983).
73
The orientation of fibers relative to the orientation of the whole muscle varies among
different muscles. Various fiber arrangements observed in the human body are illustrated in
Figure 2. Muscle may be classified as fusiform, unipennate, bipennate, triangular, and strap.
Fibers attach at both ends to tendon or other connective tissue.
Muscle fibers are multinucleated cells with the nuclei generally located along the cell
periphery. The population density of nuclei is estimated to be 50 - 100 per millimeter of fiber
length (Ishikawa, 1983).
Muscles have a rich supply of blood vessels. Capillary networks are arranged around
each fiber with the capillary density varying around different fiber types (Ishikawa, 1983).
A motor unit consists of a single motoneuron and all the fibers it innervates. The number
of fibers per motor unit is variable, ranging from just a few in ocular muscles, requiring fine
control, to thousands in large limb muscles (Bucthal and Schmalbruch, 1980; Ishikawa, 1983).
In intact whole muscle, motor units intermingle throughout the entire muscle cross-sectional
area.
The literature is filled with different naming schemes that have been used to identify
motor units. The first naming scheme used was based on gross muscle appearance. Fibers were
labeled as either red or white. In a second naming scheme, three classifications (red, white, and
intermediate) were introduced based on mitochondrial density as viewed under an electron
microscope. Based on mechanical properties, a third naming scheme was established classifying
fibers as either fast-twitch or slow-twitch (S), with the fast-twitch being further subdivided into
fast-twitch fatigue resistant (FR) and fast-twitch fatigable (FF) (Burke and Edgerton, 1975;
Bucthal and Schmalbruch, 1980; Chapman, 1985). A fourth naming scheme was established
when it was shown that some fibers stain differently when subjected to enzyme sensitive stains.
The staining technique has been used to identify three fiber types; slow-twitch oxidative (SO),
fast-twitch oxidative-glycolytic (FOG), and fast-twitch glycolytic (FG). To complicate the
muscle fiber identification process further, a second enzymatic histochemical naming scheme is
commonly used. Fibers are classified as either Type I or Type II, with Type II fibers further
divided into Type IIa, Type IIb, and Type IIc (Brook and Kaiser, 1970). Type I fibers are high in
oxidative enzymes and low in phosphorylase and ATPase. The reverse is true for the Type II
fibers. Efforts have been made to unite the different nomenclatures, but without success
(Spurway, 1981). Though the various naming schemes result in similar fiber classifications, they
are not the same (Nemeth and Pette, 1981). Regardless of the naming scheme used, fibers within
each classification exhibit different chemical and mechanical properties from fibers in other
classes.
74
Figure 1- Illustrated is a schematic representation of the organizational structure of muscle. The
gross muscle is composed of bundles of fascicles that consist of groups of fibers. Fibers can be
further divided into myofibrils that contain the myofilaments making up the sarcomeres.
75
Figure 2- Shown are six possible fiber orientations that may occur in intact whole muscle A)
fusiform, B and C) unipennate, D) bipennate, D) triangular, and F) strap.
Fibers have an extensive membrane network (see Figure 3). The muscle fiber is
completely enclosed by the plasma membrane which is usually referred to as the sarcolemma
(Peachey, 1985; Ishikawa, 1983). The sarcolemma may be resolved into three layers, the
plasmalemma, basal lamina, and a thin layer of collagenous fibrils (Peachey, 1985; Ishikawa,
1983). Multinucleated satellite cells can be found between the basal lamina and the
plasmalemma. These cells may be involved in forming new fibers following muscle trauma
(Peachey, 1985). The muscle fiber contains two distinct membranous systems between the
myofibrils; the transverse tubular system (T-system) and the sarcoplasmic reticulum (SR)
(Ishikawa, 1983). These membrane systems are distinct membrane networks separate from one
another and are responsible for communicating the external stimulus provided by the motor
neuron inward to the center of the fiber. The time and process of this communication is termed
excitation-contraction coupling (Peachey, 1985; Ishikawa, 1983). The T-system is part of the
plasmalemma and makes a network of invaginations into the cell (Ishikawa, 1983). The Tsystem associates in a specific way with the SR. Two terminal cisternae (part of SR) run parallel
to the T-system to form a triad (Peachey, 1985). The excitation of the sarcolemma spreads
inward through the T-system which communicates this excitation to the SR. The SR then
releases calcium ions along the length of the fiber which activates the contractile material within
the cell (Peachey, 1985, Ishikawa, 1983). The extent of the T-system varies among different
types of muscle fibers. In mammalian muscles, fast twitch fibers have a T-system that is about
twice as extensive as that of slow twitch fibers (Ishikawa, 1983). This property gives rise to
faster relaxation rates in fast twitch fibers.
76
Figure 3- Illustrated is a schematic representation of the membrane network of muscle fibers.
The muscle fiber is enclosed by the sarcolemma. The membranous networks of the sarcoplasmic
reticulum and transverse tubules are responsible for communicating the external stimulus
provided by the motor neuron inward to the center of the fiber.
Within a muscle fiber can be found bundles of myofibrils, sarcoplasm, and mitochondria.
Myofibrils constitute 75 - 85 percent of the fiber volume (Bagshaw, 1982, Ishikawa, 1983). The
myofibrils are separated from each other by the sarcoplasm and membranous organelles
(Ishikawa, 1983). Mitochondria supply energy for contraction through their oxidative
metabolism. The number of mitochondria present within a cell reflects the metabolic pattern of
the fiber. Fibers relying on oxidative metabolism have a greater number of mitochondria
compared to fibers relying on anaerobic metabolism (a discussion of the different metabolic
pathways is presented later in this chapter).
Myofibrils are composed of a serial arrangement of sarcomeres (Loeb and Gans, 1986)
(see Figure 1). Sarcomeres are the basic unit of shortening and force generation. A sarcomere is
a regular array of parallel overlapping thick and thin filaments (Anthony and Thibodeau, 1983;
Loeb and Gans, 1986). Thick and thin filaments are composed primarily of the proteins myosin
77
and actin respectively. A myofibril volume is 55 percent myosin and 25 percent actin (Bagshaw,
1982).
The terminology used to describe sarcomere anatomy is largely the result of muscle
observations using polarizing microscopes (see Figure 1). When viewed with a polarizing
microscope, specific zones of a muscle fiber appear darker than other zones. The dark zones
have dense protein bands and stain deeply with basic dyes causing the plane of polarization of
light to be rotated strongly. These zones have been labeled A-bands (for anisotropic). Other
zones are less protein dense, stain weakly and rotate the plane of polarization of light weakly.
These zones have been labeled I-bands (for isotropic) (Fung, 1981; Bagshaw, 1982; Loeb and
Gans, 1986). In the middle of the I-band is a dense protein zone called the Z-line or Z-disk (for
Zwischen-Scheibe meaning interim disk) (Eisenberg, 1985). In the middle of the A-band is a
dense protein zone called the H-zone (for Helle-Scheibe) (Bagshaw, 1982; Loeb and Gans,
1986). In the center of the H-zone is a region called the M-line (for middle). The A-band
corresponds to the zone of thick filaments. The H-zone is that region of the thick filaments that
is not overlapped by the thin filaments. The M-line is composed of a connective tissue network
binding the thick filaments and maintaining them in a hexagonal pattern when viewed in a
transverse plane. The Z-disk is composed of a connective tissue network binding the thin
filaments. Thin filaments are attached at the Z-disk but are free to interdigitate with the thick
filaments at their other end. Myosin filaments are separated by 40 - 50 nanometers (nm)
(Ishikawa, 1983) while the myosin/actin spacing is 20 - 30 nm (Bagshaw, 1982). A sarcomere is
defined as the region between Z-disks in a myofibril. As a muscle shortens the sarcomere I-band
and H-zone decrease in length while the A-band length remains constant. These observations
lead to development of the sliding filament theory which is discussed in the section on muscle
contractile characteristics.
Thick filaments are composed of myosin molecules. Each thick filament contains nearly
180 myosin molecules (assuming two myosin heads per axial repeat location) (Fung, 1981).
These molecules are 160 - 170 nm long (Squire, 1981; Bagshaw, 1982) and arranged to give a
total thick filament length of 1.55 micrometers (µm) and 12 - 15 nm diameter (Ishikawa, 1983).
The myosin molecule may be divided into two heavy chains and four light chains
(Bagshaw, 1982). Each heavy chain forms the bulk of a single head with the remaining portion
of the two chains intertwining to form a tail. Two light chains are associated with each myosin
head. The myosin molecule structure has been defined in terms of two general regions, the light
meromyosin (LMM), and the heavy meromyosin (HMM). The LMM represents part of the tail
and accounts for the self association property of myosin. The HMM contains the two heads and
the remaining part of the tail not considered part of the LMM. HMM is further divided into
subfragment one (S1) and subfragment two (S2). S2 is similar to LMM but allows S1 to project
out up to 55 nm (Bagshaw, 1982). S1 contains binding sites for two light chains, ATP, and actin.
S1 is where ATP hydrolysis takes place and is needed for acto-myosin binding (Bagshaw, 1982).
HMM is often referred to as the cross-bridge because it is the structure that reaches out and binds
to actin during contraction.
The thin filament is composed of actin, tropomyosin, and troponin. G-actin molecules
polymerize to form F-actin in a right handed double helix chain with an axial repeat length of 35
- 36 nm. G-actin molecules repeat every 5.5 nm (Bagshaw, 1982). One tropomyosin molecule
runs in the groove of the F-actin chain a length of seven G-actin molecules. There is one
troponin molecule for each tropomyosin molecule. Because of symmetry (a groove on either
side of the helix chain) there are two tropomyosin/troponin complexes for a given length of F-
78
actin. The troponin molecule can be further divided into troponin-C, I, and T (Squire, 1981).
Troponin-C regulates calcium ion sensitivity with the other two components (I and T) being less
well defined.
Though the general structure (i.e. actin and myosin filament lengths and their lattice
arrangement) are similar among vertebrate muscle fibers, there are differences in the regulatory
proteins of the myosin - isoforms (Gollnick, 1981; Saltin and Gollnick, 1983; Huxley, 1985).
These isoforms exhibit different amino acid sequences, ATPase activity, and affinity for calcium
(Perry, 1985). Myosin molecules in fast and slow twitch skeletal fibers have different ATPase
activity (Saltin and Gollnick, 1983; Perry, 1985; Reiser, et al., 1985; Greaser, et al., 1988). These
differences have been correlated with the different shortening velocities that exist between these
fiber types (Gollnick, 1981; Reiser, et al., 1985; Edgerton, et al., 1986; Greaser, et al., 1988;
Fitts, et al., 1989). There are also differences in the Troponin-C protein in fast and slow twitch
fibers. Only one Ca+2 site has to be filled to trigger contraction in slow fibers compared to
multiple sites in fast fibers (Perry, 1985).
To summarize, the contractile characteristics of a whole muscle depend on both gross
muscle architecture and the properties of the fibers comprising the muscle. All vertebrate
skeletal muscle fibers are similar in their structural arrangement of actin and myosin (Huxley,
1985), but have variations in their membrane structures, density of mitochondria, specific protein
isoforms, and possibly myofibril packing density (Saltin and Gollnick, 1983; Perry, 1985; Reiser,
et al., 1985; Greaser, et al., 1988). These differences, at the cellular level, cause differences in
fiber contractile characteristics (i.e. fiber force, maximum shortening velocity, and resistance to
fatigue). At the level of the whole muscle, differences exist between muscles in their
arrangement of fibers and percentages of each fiber type. Variations in fiber properties and gross
muscle structure translate into different muscles having different contractile characteristics.
Muscle Contractile Characteristics:
There are many questions yet to be answered regarding the way muscles generate force.
To answer these questions we must build from past experience and knowledge. A description of
what is currently known about muscle behavior is given in this section. Muscle contractile
characteristics are defined in terms of structural and theoretical considerations where possible
and empirical relations otherwise.
Determining the fundamental principles underlying muscle contraction is not a simple
task. There have been and continue to be discrepancies in experimental results. Discrepancies in
early work were shown to be due, in part, to unidentified structural differences existing between
various muscles tested (e.g. fusiform vs. penniform, slow-twitch vs. fast-twitch). Many of the
structural factors that affect the dynamics of muscle contraction have been identified, but it is
likely that there are still others that have not yet been recognized. These unrecognized factors
may be the cause of discrepancies reported in experimental data today (e.g. specific tension,
maximum shortening velocity, fatigue properties).
Experimental observations indicate that there are many factors that contribute to the
overall characteristics of muscle contraction. One of these factors is the force generated per fiber
cross-sectional area. All vertebrate muscle filaments are of similar lengths and they are arranged
with similar longitudinal cross-bridge spacing (Squire, 1981; Huxley, 1985). This structural
similarity might suggest that all vertebrate muscle fibers have similar specific tensions (i.e.
maximum force per unit area). However, this is an area of continued debate. Some researchers
suggest that fast and slow twitch fibers have different specific tensions (Burke and Tsairis, 1973;
79
Bodine, et al., 1987), while others suggest that they are similar (Saltin, 1983; Huxley, 1985;
Faulkner et al., 1986). The structural similarity among vertebrate myosin filaments suggests that
the force generated by the interaction of a single myosin filament and its associated actin
filaments must be similar to that which can be generated by other filaments. If differences do
exist in specific tension values, then it is likely that these differences are not due to differences in
the force generated by individual cross-bridges, but rather due to differences in myofibril
packing density in different fiber types and different species.
There is some uncertainty as to the constancy of myofibril packing density among
various fiber types. In avian muscles it has been shown that there may be as much as a 50
percent difference in the myofibril packing density between slow and fast twitch fibers with the
slow twitch fibers having the lower packing density. This difference is believed to be due to
more mitochondria and sarcoplasm taking up space between myofibrils in the slow twitch fibers.
Assuming packing density differences exist in mammalian muscles, lower specific tension values
would be expected for muscle composed of predominately slow twitch fibers. Such findings
have been reported for the cat soleus muscle (Edgerton et al., 1986).
Since the time of the classical experiments of Hill and Huxley in the 1920s, there has
been further supportive evidence and general agreement that the amount of force that a muscle
can produce depends on its length and shortening velocity (Bucthal and Lindhard, 1939; Bucthal,
1942; Zahalak, et al., 1976; Gans, 1982; Baildon and Chapman, 1983; van Kaam, et al., 1984;
Chapman, 1985; Bobbert, et al., 1986). Early light microscope studies revealed that the
maximum force developed by a muscle fiber depends on the fiber length. Specifically, the force
is proportional to the overlap of thick and thin filaments. This observation led to the
development of the sliding filament theory. This theory states that muscle force is created by
small cross-bridges acting between thick and thin filaments. Cross-bridges act as individual
force generators to pull thin filaments toward the center (M-line) of the thick filament. The fiber
length determines the amount of thick and thin filament overlap which determines the number of
cross-bridges capable of attaching and developing force. The relation between fiber force and
actin and myosin overlap is shown in Figure 4.
80
Figure 4- Shown is a schematic representation of the active force-length relationship of frog
muscle and its corresponding relationship to the overlap of thick and thin filaments (from
McMahon, 1984). There is an optimal range of muscle fiber length over which the fiber can
produce its greatest force. At longer fiber lengths not all cross-bridges may contribute to the
force generation and the force declines. At shorter lengths actin filaments from adjacent
sarcomeres begin to interfere with each other and the force also declines.
From experimental studies it has been shown that as muscle force increases, the rate of
muscle shortening decreases in a hyperbolic fashion as shown in Figure 5. Unlike the
force-length relation, the structural basis of the force-velocity relation has not been identified. It
81
is likely related to the kinetics of the various protein isoforms and their interactions. Nonetheless
the force-velocity relation is quite useful for predicting the force generated by a shortening
muscle.
Hill observed that the rate of heat produced by a shortening muscle is proportional to the
shortening velocity (rate of heat production = aV). He showed experimentally that the rate of
heat production (aV) plus the rate of mechanical work performed (F•V) depended linearly on the
load as given in Equation 1.
(aV + FV) = (Fo - F)b
where:
F
Fo
V
a,b
(1)
= force
= maximum isometric force
= shortening velocity
= constants
Figure 5- Illustrated is Hill's force-velocity relationship for muscles shortening (Hill, 1970). As
the muscle force increases, the rate of muscle shortening decreases in a hyperbolic relationship.
In recent years as researchers expanded upon earlier work, it became evident that factors
other than length and shortening velocity influence the properties of muscle contraction. These
factors may be summarized as muscle composition, architecture, activation level, and history.
82
Work by Thorstensson et. al. (1976), Viitasalo and Komi (1978), Coyle et al. (1979), and
Rall (1985) showed that muscles with a greater percentage of fast twitch fibers generate greater
force for a given speed of contraction, are more susceptible to fatigue, and have a shorter delay
from the time of activation to the onset of tension. The influence that muscle composition
(relative percentage of each fiber type within a muscle) has on the F-V relation is illustrated in
Figure 6. As the composition of a muscle changes from having predominately slow-twitch fibers
to having mostly fast-twitch fibers, the F-V relation shifts along the force axis resulting in greater
force for the same shortening velocity.
As discussed in the previous section, the structural arrangement of the filaments of
various vertebrate muscles is the same, however there are differences in the biochemical
constituents comprising different fiber types. Different protein isoforms have different rates of
actomyosin ATPase activity which results indifferent fiber types having different
contraction/relaxation times and maximal shortening velocities (Barany, 1967; Pette, 1985;
Reiser et al., 1985; Metzger and Moss, 1987). Fast fibers have maximum shortening velocities
three to five times faster than the slow fibers (Rall, 1985; Reiser et al., 1985; Faulkner, 1986;
Edgerton, 1986, Fitts et al., 1989). Though there does appear to be agreement that fast fibers can
shorten faster than slow fibers, there are differences in the reported values for the absolute
shortening velocities. Close (1972) reports maximum shortening velocities of 7-8 resting lengths
per second for Wistar rat gracilis anticus fibers at 17.5 degrees Centigrade and 18.7 resting
lengths per second for Wistar rat extensor digitorum longus fibers at 35 degrees Centigrade.
Faulkner (1986) cites maximum shortening velocities for human slow and fast fibers at 37
degrees Centigrade of 2 and 6 resting lengths per second respectively. For rabbit soleus at 15
degrees Centigrade Reiser et al. (1985) report values of between 0.5 and 1.0 muscle resting
lengths per second for slow and 1.33 to 2.99 fiber lengths per second for fast fibers. Fitts et al.
(1989) tested fragments of human deltoid fibers at 15 degrees Centigrade and found maximal
shortening velocities to be 0.86 and 4.85 fiber lengths/second for slow and fast fibers
respectively. More recently it was demonstrated in rat muscle that SO, FOG, and FG have
different maximum shortening velocities (1.5, 4.5, and 6.0 fiber lengths/second respectively at 15
degrees Centigrade) (Fitts, 1989, personal communication).
One must be careful when comparing these values. Muscle bioenergetics are temperature
dependent and hence the temperature at which a muscle is tested can alter the maximum
shortening velocity results. The fibers tested in the study by Reiser et al. (1985) and Fitts et al.
(1989) were maintained at 15 degrees Centigrade. The Q10 value (change in intrinsic shortening
speed for a ten degree Centigrade change in temperature) is about 2.0 for the range 15 to 25
degrees Centigrade (Close, 1972; Bennett, 1985). Converting Reiser's data to equivalent values
at normal body temperature (37 degrees Centigrade) by using temperature conversion graphs
(Bucthal, 1942) or a Q10 value of 2.0 results in maximal shortening velocities of 3.5 and 13
resting lengths per second for slow and fast fibers respectively. Slightly higher values are
obtained if the data by Fitts et al. are converted (3.5 and 21 fiber lengths/second). The much
lower values reported by Faulkner are likely due to differences in the procedure used to obtain
the shortening velocity.
83
Figure 6 - Illustrated is an example of the effect that muscle composition has on the force
producing ability of a muscle (modified from Thorstensson et al., 1976). Muscle composed of a
greater percentage of fast fibers compared to a muscle with similar pcsa, can produce greater
force for the same contraction velocity.
Figure 7 - Shown is an example of the effect that muscle architecture has on the force-length and
force-velocity relationships (modified from Woittiez, 1983). Muscles represented in A and B
have similar overall lengths. Muscle A has more fibers, shorter fibers, and a greater
physiological cross-sectional area (pcsa) than muscle B. Muscles with longer fibers have greater
maximum shortening velocities, and a greater total range over which they can produce force
compared to muscles with shorter fibers, which tend to have greater pcsa enabling them to
generate larger maximal forces.
84
In muscle reviews by Burke and Edgerton (1975), Bucthal and Schmalbruch (1980),
Gollnick (1981), Gans (1982), Woittiez et al, (1983), and Huijing and Woittiez (1984), the
architectural arrangement of muscle fibers within a muscle is stated to affect the amount of force
exerted along the axis of the muscle, and the speed of contraction. Longer fibers containing
more sarcomeres in series tend to have greater contraction velocities. Muscles with more fibers
in parallel can generate greater force. Accordingly, pennate muscles are able to produce more
tension than fusiform muscles of similar volume. The influence that muscle architecture may
have on the force-length and force-velocity relationships of a given muscle as modeled by
Woittiez (1984) are illustrated in Figure 7.
Many investigators have demonstrated that the level of muscle activation and hence the
number of fibers recruited affect the force generated during muscle contraction (Bouisset, 1973;
Zahalak, et al., 1976; Gans, 1982; Baildon and Chapman, 1983; Chapman, 1985; Herzog, 1985;
Bobbert, et al., 1986; Zajac, et al., 1986; Hasan, 1987). The level of force generated by
voluntary contraction of skeletal muscle is controlled by at least two mechanisms, motor unit
recruitment and modulation of the firing rate of active motor units (rate coding). It is generally
accepted that motor units are recruited in an orderly manner consistent with the "size principle"
put forth by Henneman et al. (1965, 1974). According to Henneman the excitability or threshold
level at which a motor unit is recruited is directly related to the diameter of the motoneuron.
Thus the participation of a motor unit in graded motor activity is dictated by the size of its
neuron. Studies conducted by other researchers lend support to this finding (Hannerz, 1974;
Clamann et al., 1974; Freund et al., 1975; Freund, 1983; Broman et al., 1985; Grimby, 1987;
Secher, 1987).
The force a muscle generates is not only a function of the number of fibers stimulated,
but also both the frequency (i.e. rate coding) and duration of stimulation (Broman et al., 1985;
Hennig and Lomo, 1987). There is a frequency of stimulation above which twitch responses
become fused and fibers generated their maximal force. Below the fusion frequency, fibers
generate submaximal forces.
During gross muscle studies, the effects that rate coding and motor unit recruitment have
on electrical signals recorded from the muscle are generally lumped together and expressed as a
general activation level. The level of activation tends to alter the F-V relation as shown in Figure
8. As the level of neural activation increases, more fibers are recruited and/or more force is
generated per fiber and the force increases for the same shortening velocity.
85
Figure 8- Shown is an example of the effect that the level of muscle activation has on the forcevelocity relationship (modified from Zahalak et al., 1976). As the activation level increases, the
force-velocity curve is shifted upward causing greater force for the same shortening velocity.
It has been known for some time that the past history of a muscle affects the force it can
generate (Abbot et al., 1952; Asmussen, 1953; Cavagna et al., 1968; Asmussen, 1979). Both
fatigue and enhancement may occur depending on the past history of the muscle.
Fatigue acts to reduce the force that the entire muscle can generate. However, fatigue
does not necessarily affect each fiber type the same. To understand some of the mechanisms of
fatigue, a brief description of the fuel sources and supply pathways utilized by muscle tissue is
needed. Muscle contractile proteins utilize the high-energy phosphate compound adenosine
triphosphate (ATP) as their single fuel source. The splitting of ATP into adenosine diphosphate
(ADP) and inorganic phosphate (Pi), in the reaction shown below, provides the energy for crossbridge cycling during force production.
ATP ---> ADP + Pi
<The amount of ATP present in living muscle can provide enough energy for roughly eight
muscle twitches. Obviously the body provides some means of quickly replenishing the ATP
available. There are actually three primary energy pathways used by muscle tissue to produce
ATP. The pathway most commonly used during the onset of physical activity combines ADP
with phosphocreatine (PCr) to produce ATP and creatine (Cr) in the reaction shown below:
ADP + PCr ----> ATP + Cr
ÅThis reaction is commonly referred to as the Lohmann reaction and can take place in either
direction. However, the equilibrium constant for the reaction favors the production of ATP by a
86
factor of about 20. The concentration of ATP within a muscle remains constant except under
conditions of either extreme fatigue or muscular disorder. For the Lohmann reaction to proceed
toward ATP production there must be PCr present in the muscle. Muscle maintains a small
reserve of PCr, but not enough to supply the amount of ATP needed for sustained activities. In
fact the amount of PCr stored in muscle tissue can provide enough ATP to sustain about 100
twitches. This is much greater than the stores of ATP can supply, but still not sufficient to
supply the energy demands placed on the body during daily activities.
Aerobic oxidative phosphorylation, and anaerobic glycolysis are two other primary
pathways utilized for ATP production. Actually anaerobic glycolysis can be considered either a
process in itself or a precursor to oxidative phosphorylation. Whether or not oxidative
phosphorylation occurs depends on oxygen availability to the muscle cell and the content of
cytochromes and myoglobin present within the cell. During anaerobic glycolysis, which takes
place in the cytoplasm, a series of reactions take place to breakdown glucose to form 2 pyruvic
acid, two hydrogen, and 4 ATP molecules. Anaerobic glycolysis utilizes 2 ATP molecules to
breakdown glucose, hence the net yield is 2 ATP. Only 1 ATP molecule is needed to breakdown
glycogen so the net yield from anaerobic glycolysis of glycogen is 3 ATP. The pyruvic acid and
hydrogen molecules generated from anaerobic glycolysis enter the mitochondria where the
Kreb's cycle (also referred to as the tricarboxylic acid cycle TCA) takes place. For each pyruvic
acid molecule entering the Kreb's cycle 3 CO2 molecules, 5 hydrogen molecules and 2 or 3 ATP
molecules are formed (3 ATP result if carried into the mitochondria by NADH or 2 ATP if
carried in by FADH2). Fast twitch fibers rely on FADH2 and therefore are less efficient. The
hydrogen atoms released from both the Kreb's cycle and anaerobic glycolysis enter an electron
transport system by combining with nicotinamide-adenine dinucleotide (NAD) or flavin-adenine
dinucleotide (FAD). Oxidative phosphorylation occurs if sufficient oxygen is available to meet
the supply of hydrogen transported to the mitochondria via NAD or FAD. If the oxygen supply
is not sufficient, then NADH reacts with the pyruvic acid to form lactic acid. Lactic acid can
accumulate in the muscle causing fatigue. At some point, usually during a recovery period, the
lactic acid is cleared from the muscle and carried to the liver where it is synthesized into glucose.
The nature of the reactions taking place in the electron transport system is not of prime concern,
but the results are. From the electron transport system (ETS) 32 ATP molecules are produced
along with carbon dioxide (CO2) and water (H2O). Energy is needed to transport the two
hydrogen molecules generated during anaerobic glycolysis from the cytoplasm into the
mitochondria. This process utilizes one ATP per hydrogen molecule transferred. Thus the net
yield of ATP per glucose molecule from aerobic metabolism is between 36 and 38 (37 to 39 if
start with glycogen). The aerobic processes are much more efficient than anaerobic glycolysis
acting alone, which yields only 2 ATP per glucose molecule. Also no lactic acid is formed, only
CO2 and H2O. Type I fibers are more efficient than type II fibers (42% vs. 38% respectively
based on 39 ATP *7.3 kcal/mol ATP/686 kcal/mol of glycogen OR 36 ATP *7.3 kcal/mol
ATP/686 kcal/mol of glucose).
As discussed previously, different fibers have different myosin proteins and
mitochondrial densities. The structural design of SO and FOG fibers allows them to be relatively
resistant to fatigue. These fibers are rich in mitochondria and oxidative enzymes. They have the
ability to use metabolites from the blood to sustain the metabolic activity needed for continued
contraction. This allows them to generate force for long periods of time with or with out
depleting their glycogen stores. Fatigue of these fibers occurs when glycogen stores are depleted
and insufficient oxygen is supplied to maintain aerobic metabolism. Their rate of fatigue is likely
87
related to the muscle force generated, and the duration of contraction relative to the duration of
recovery, commonly expressed as the duty cycle (duty cycle = time of muscle activation/total
cycle time).
The other history related factor to consider is enhancement. The term enhancement has
been used in the literature to describe basically two different effects, (1) elastic energy storage,
and (2) force potentiation (increased force above that of a similar contraction initiated from rest).
The first of these effects is related to muscle-tendon elastic properties. The second effect is
related to force potentiation of the fiber cross-bridges.
For both forms of enhancement, the magnitude of the effect depends on several factors.
Firstly, for any enhancement to occur a stretch/shortening cycle (eccentric contraction followed
by a concentric contraction) must take place. Other factors of relevance are the time delay
between the two contraction modes (referred to as coupling time), stretch velocity, initial muscle
length prior to stretch, and the amplitude of stretch (Edman et al., 1978, 1981, 1982; Bosco et al.,
1979, 1981, 1982; Aura and Komi, 1986; Goubel, 1987).
Like fatigue, the exact mechanisms responsible for enhancement have not been isolated.
Storage of elastic strain energy in the tendon and SEC of muscle has been suggested as a
possible source of the improved mechanical efficiencies reported during certain activities (Abbot
et al., 1952; Asmussen, 1953; Cavagna et al., 1968, 1981, 1985; Cavagna, 1970, 1977; Asmussen
and Bonde-Petersen, 1974; Thys et al., 1972, 1975; Curtain and Davies, 1975; Alexander and
Bennet-Clark, 1977). The amount of strain energy that an active muscle can store has been
reported to be 5 J/kg while that of the tendon and other collagenous tissue is 2000-9000 J/kg
(Alexander and Clark, 1977). These data suggest that muscle elasticity plays only a small part in
storage of elastic energy compared to tendon.
Like elastic strain energy, force potentiation is a complex issue. Cavagna et al. (1985)
state that force potentiation created by a stretch/shortening cycle is due in part to greater force
developed by each cross-bridge attached. There appears to be an optimal eccentric force or
amplitude of stretch, below which the magnitude of the force potentiation increases with
increased stretch amplitude, and above which it begins to decrease (Asmussen and BondePetersen, 1974). If cross-bridges are stretched too far, then they break and the increased force is
lost. The mechanisms responsible for this force potentiation are not known, but it may be that
during an active stretch the myosin heads are rotated to a higher energy state which enables them
to generate greater force during the following concentric contraction.
The publications cited above suggest that there are many factors that contribute to the
overall contraction characteristics of a given muscle. These factors may be summarized as
muscle length, shortening or lengthening velocity, composition, architectural design, activation,
and history. Not only do each of these factors affect the contractile force directly, but they also
affect each other. For example, golgi tendon organs located between the muscle fiber and the
tendon sheath are able to relay information about the force exerted by the muscle to the central
nervous system (Burke and Edgerton, 1975; Bucthal and Schmalbruch, 1980). Through central
processing, this information may elicit a certain activation response. Another example might be
the interaction of muscle length and architectural factors. Fiber orientation affects the amount of
force that is transmitted along the axis of the muscle, but the orientation is affected by the length
of the muscle. The point to emphasize is that there are many circular relationships. Many
factors do not act independently and their interactions are not well understood. It is likely that
these factors do not have the same effect under all circumstances of muscle contraction. There
may be a complex network of feedback loops from the muscle to the brain and/or spine that
88
provide a path for sensing and processing neuromuscular conditions. The responses to these
conditions create the individual force characteristics exhibited by each muscle during a
movement task. It is these many interactions that make muscle modeling a complex yet
fascinating area of study.
Muscle Development (Maturation and Aging)
Skeletal muscles develop by differentiation of cells from the mesoderm, the middle layers
of the embryo. The developmental process seems to start once mitotic cell division ceases, and
is characterized by fusion of cells and synthesis of myofibrillar protein. The earliest form of a
muscle cell is called the myoblast (see Figure 9). Myoblasts fuse to form myotubes, these are
multinucleated cells with centrally located nuclei. They contain actin and myosin in the form of
filaments, but not yet organized. Cells become packed with myofibrils and the nuclei migrate to
the periphery.
Beyond the observations stated above, very little is known about the actual process of
muscle assembly. There is evidence that there is an inherent ability of actin and myosin to align
themselves to form contractile units. Within a myotube the myofibrils form at the outside first
and then fill in toward the middle. It is not known which comes first the ordering of the actin
and myosin or the cytoskeleton to force them to develop orderly. The sarcoplasmic reticulum
seems to develop early on with the T-system developing toward the end of the myotube stage.
It is important to note that all the development discussed so far can occur without any
nervous input. Also during these stages muscle size increases due to increased cell number, cell
fusion, and increases in cell size. This seems to continue until birth after which the mechanisms
of muscle growth seem to change.
Fetal Muscle
Development
myoblast
mytubes
SR early in myotube
development,
T-system later
fibril packed myotubes
fibrils develop
outside-in
migration of nuclei
to periphery and
structural organizing
Figure 9 - Schematic of the sequence of events involved in fetal muscle development.
Postnatal development is guided by interactions between fibers and nerves (Ridge et al,
1984). At birth some muscle fibers may be innervated by multiple neurons. However, during
the first few weeks after birth some neurons withdraw. The mechanism responsible for dictating
which neuron remains intact is not known.
89
Humans are born with about 40 % type I fibers in each muscle. During the first two
years after birth the muscle composition changes to 60 % type I in the deltoid and 55 % in the
vastus lateralis (Oertel, 1988). Thus, it appears that muscle composition shifts as a function of
ageing and muscle utilization.
Muscle growth is achieved primarily by fiber hypertrophy. There is very little increase in
cell number. Growth is substantially influenced by the effects of motor nerves. Longitudinal
growth tends to occur at the myofibril ends although the exact mechanisms still remain
unknown. Lateral growth occurs as myofibrils grow than split. It may also be possible for new
myofibrils to develop.
With ageing muscle cross-sectional area tends to decrease. This decrease in area
primarily results from a decrease in the cross-sectional area of type II fibers. Lexell (1991)
showed a 35 % reduction in the cross-sectional area of type II fibers taken from the quadriceps
muscles of 69-84 year old males compared to 19-35 year old males. For the same two groups
there was only a 6 % reduction in the cross-sectional area of type I fibers.
Some motor control changes have been noted to occur as a function of age. Moritani, et
al (1989) tested ankle plantar flexors in young (9 years) and adult men and evaluated the
activation scheme of soleus and medial gastrocnemius (MG) during 4 motor tasks (1 leg stand, 1
leg toe raise, 2 leg hop, 2 leg jump). They found that during postural tasks young subjects used
the MG more than older subjects. This suggests that maybe the motor program to use oxidative
fibers has not yet been well established in the younger subjects. There were no differences noted
in the jumping tasks. Adults did show signs of more MG activation during eccentric contractions
which would suggest that they have learned how to the enhancement achieved through a stretchshortening-cycle.
There tends to be a reduction in the force generated per cross-sectional area in muscles
from elderly subjects compared to young adults. It has been suggested that older muscle does
not have the ability to recruit all its fibers, or that active fibers do not recruit all their x-bridges,
or that x-bridge force decreases with age. Anyone of this effects could cause the observed loss in
force. (Bemben et al, 1991)
Adaptation to Exercise and Disuse:
Muscle responds differently to different exercise modes. Therefore two general modes of
exercise are considered - Endurance and Strength. Long duration training at less than 75 % of
VO2 max is considered to be endurance training. During such training there may be some
selective hypertrophy of oxidative fibers, but no strong evidence for large bulk gains. There is
evidence from rat studies that fiber conversion can occur (Lynch et al, 1991). Several other
studies have noted the changes in response to endurance training: 1) increased VO2 max, 2)
increased glycogen stores, 3) increased enzymes for oxidation of carbohydratess and fats, 3)
increased oxygen extraction capabilities, 4) increased z-line thickness, 5) increased
mitochondrial density, 6) increased capillary density, and 7) decreased rate of Ca+2 transport and
uptake by SR.
Several changes have also been noted to occur in response to strength training. The most
notable change is the increase in muscle bulk, which since 85 % of muscle volume is fibers and
15 % extrafiber material, we can assume that bulk gains are due in large part to fiber volume
increases which results from increases in contractile proteins. Other changes that have been
noted to occur in response to strength training are 1) increased fatigue resistance to this type of
exercise, 2) decreased mitochondrial density, 3) fiber conversion to fast twitch fibers, 4)
90
decreased capillary density, 5) decreased time to peak tension, 6) increased rate of Ca+2
transport and uptake by SR, and 7) increased power potential.
A muscle will respond to disuse by returning to its normal state prior to training.
However, there does seem to be some type of a memory effect that results from training. A
person that trains, then experiences a period of disuse, and then trains again will be to gain
strength at a faster rate during the second training period. The muscle appears to keep the
adaptation mechanisms "on-call" for a period of 1 to 30 weeks following the cessation of training
Staron et al, 1991).
Muscle Trauma and Repair:
There are basically five types of trauma that may occur to skeletal muscle: 1) cold, 2)
puncture, 3) contusion, 4) ischemia, and 5) overload. The types of damage that may occur focal
subfiber necrosis (if injury is localized to a part of a fiber), segmental necrosis ( if the injury
extends across the whole fiber axially), and regional necrosis (if injury occurs to several fibers).
It should be noted that muscles are continually damaged and repaired during our daily physical
activities. An noticeable injury occurs when the damage is great enough to cause pain or
dysfunction.
Different fibers appear to be susceptible to injury during different types of loading
conditions. If a muscle is stretched and immobilized damage will occur in the Type I fibers. If a
muscle is loaded eccentrically damage tends to occur in the type II fibers.
There are two common types of healing: continuous and discontinuous. Continuous
healing occurs after minor damage and is simply an outgrowth from the partially damaged cells.
Discontinuous healing occurs after more sever trauma and consists of complete destruction of an
area of the muscle with new fibers arising from myoblasts. Muscle is capable of massive
regeneration. Vascularization and neuronal input appear to be very important to the repair
process. Severed vessels or nerves will cause a longer healing period. Mechanical stress also
seems to be an important factor for healing, but its exact role is not known. If the basal lamina is
intact, complete healing occurs can occur in a few days to a week. If however, the basal lamina
is broken then some scar tissue may remain and healing may take one to two years. Studies
suggest that some remnant of an original fibers is needed to stimulate regeneration as well as
some macrophage stimulant to invoke satellite cell response.
Summary:
Muscles are dynamic tissues which generate the active forces which act to stabilize and
move our limbs. Skeletal muscle is structurally designed to generate large forces for its relative
small volume. Different muscles have different architectural designs presumably to facilitate
their different functional roles within the body.
Muscle is a robust tissue. It is capable of generating large forces and it has the potential
for massive regeneration should it become damaged. Muscle also has the ability to adapt rather
quickly to changes in the demands placed upon it during daily life.
References
Abbot, B.C., B. Bigland, J.M. Ritchie. The physiological cost of negative work. Journal of
Physiology. 117(3):380-390, 1952.
91
Alexander, A.S., J.A. Nicholas, D. Sokolow, and A. Saraniti. The nature of torque "overshoot"
in Cybex isokinetic dynamometry. Medicine and Science in Sports and Exercise. 14(5):368375, 1982.
Alexander, R.M. and A. Vernon. The dimensions of knee and ankle muscles and the forces they
exert. Journal of Human Movement Studies. 1:115-123, 1975.
Alexander, R.M., and H.C. Bennet-Clark. Storage of Elastic Strain Energy in Muscle and other
Tissues. Nature. 265:114-117, 1977.
Amis, A.A., D. Dowson, and V. Wright. Muscle strength and musculo-skeletal geometry of the
upper limb. Engineering in Medicine. 8(1):41-48, 1979.
An, K.N., F.C. Hut, B.F. Morrey, R.L. Linscheid, and E.Y. Chao. Muscles across the elbow
joint: A biomechanical analysis. Journal of Biomechanics. 14(10):659-669, 1981.
Andrews, J.G.. On the relationship between resultant joint torques and muscular activity.
Medicine and Science in Sports and Exercise. 14(5):361-367, 1982.
Anthony, C.P. and G.A. Thibodeau. Textbook of anatomy and physiology 11th edition. The
C.V. Mosby Company. St. Louis, 1983.
Armstrong, R.B., and M.H. Laughlin. Metabolic indicators of fiber recruitment in mammalian
muscles during locomotion. Journal of Experimental Biology: Design and Performance of
Muscular Systems. Edited by J.E. Treherne. The Company of Biologists Limited. Cambridge,
Great Britain. 115:201-213, 1985.
Assmussen, E. Positive and negative muscular work. Acta Physiologica Scandinavia. 28:364382, Fasc 4, 1953.
Asmussen, E. and E. Bonde-Petersen. Storage of elastic energy in skeletal muscles in man. Acta
Physiologica Scandinavia. 91:385-392. 1974.
Asmussen, E. and E. Bonde-Petersen. Apparent efficiency and storage of elastic energy in
human muscle during exercise. Acta Physiologica Scandinavia. 92(4):537-545, 1974.
Asmussen, E.M.. Muscle fatigue. Medicine and Science in sports. 11(4):313-321, 1979.
Aura, O. and P.V. Komi. Effects of prestretch intensity on mechanical efficiency of positive
work and on elastic behavior of skeletal muscle in stretch-shortening cycle exercise.
International Journal of Sports Medicine. 7(1):137-143. 1986.
Bagshaw, C.R.. Outline studies in biology muscle contraction. Chapman and Hall, New York,
1982.
92
Bandman, E. Myosin Isoenzyme transition in muscle development, maturation, and disease.
International Review of Cytology. 97:97-131, 1985.
Barany, M. ATPase activity of myosin correlated with speed of muscle shortening. The journal
of General Physiology. 50(No.6,part2):197-218, 1967.
Basmajian, J.V., and C.J. DeLuca. Muscles alive their functions revealed by electromyography,
5th ed.. Williams and Wilkins, Baltimore, Maryland 1985.
Bell, D.G. and J. Jacobs. Electro-mechanical response times and rate of force development in
males and females. Medicine and Science in Sports and Exercise. 18(1):31-36,1986.
Bellemare, F., A. Grassino. Effect of pressure and timing of contraction on human diaphram
fatigue. Journal of Applied Physiology. 53:1190-1195, 1982.
Bellemare, F., B. Bigland-Ritchie, and J.J. Woods. Contractile properties of the human
diaphram in vivo. Journal of Applied Physiology. 61(3):1153-1161, 1986.
Bennett, A.F. Temperature and muscle. Journal of Experimental Biology. Design and
Performance of Muscular Systems. Cambridge, Great Britain. 115:332-344, 1985.
Bigland-Ritchie, B. EMG/Force relations and fatigue of human voluntary contractions. Exercise
Sport Science Reviews. 9:75-117, 1981.
Bigland-Ritchie, B., EMG and fatigue of human voluntary and stimulated contractions. Human
Muscle Fatigue, Pitman Medical, London. pp. 130-156, 1981.
Bigland-Ritchie, B. and J.J. Woods. Changes in muscle contractile properties and neural control
during human muscular fatigue. Muscle and Nerve. 7:691-699, 1984.
Bigland-Ritchie, B., F. Bellemare, and J.J. Woods. Excitation frequencies and sites of fatigue.
Human Muscle Power, Human Kinetics Publishers, Inc. Champaign Ill, pp. 197-214, 1986.
Bigland-Ritchie, B., F. Furbuch, and J.J. Woods. Fatigue of intermittent submaximal voluntary
contraction: control and peripheral factors. Journal of Applied Physiology. 61(2):421429,1986.
Bigland-Ritchie, B., Fatigue of human limb and respiratory muscles. Medicine and Sport
Science. Edited by P. Marconnet and P.V. Komi, Karger, Basel. 26:110-118, 1987.
Bjorksten, M. and B. Jonsson. Endurance limit of force in long-term intermittent static
contractions. Scandinavian Journal of Work Enviroment and Health. 3(1):23-27, 1977.
Bodine, S.C., R.R. Roy, E. Eldred, and V.R. Edgerton. Maximal force as a function of
anatomical features of motor units in the cat tibialis anterior. Journal of Neurophysiology,
57(6):1730- 1745, 1987.
93
Bosco, C. and P.V. Komi. Potentiation of the mechanical behavior of the human skeletal muscle
through prestretching. Acta Physiologica Scandinavia. 106(4):467-472, 1979.
Bosco, C. and P.V. Komi. Mechanical characteristics and fiber composition of human leg
extensor muscles. European Journal of Applied Physiology. 41:275-284, 1979.
Bosco, C., P.V. Komi, and Akiraito. Prestretch Potentiation of Human Skeletal Muscle During
Ballistic Movement. Acta Physiologica Scandinavia. 111:135-140, 1981.
Bosco, C., A. Ito, P.V. Komi, P. Luhtanen, P. Rahkila, H. Rusko, and J.T. Viitasalo.
Neuromuscular Function and Mechanical Efficiency of Human Leg Extensor Muscles During
Jumping Exercises. Acta Physiologica Scandinavia. 114(4):543-550, 1982.
Bosco, C., J.T. Viitasalo, P.V. Komi, and P. Luhtanen. Combined Effect of Elastic Energy and
Myoelectrical Potentiation During Stretch-shortening cycle exercise. Acta Physiologica
Scandinavia. 114(4):557-565, 1982.
Bosco, C., S. Zanon, H. Rusko, A. DalMonte, P. Bellotti, F. Latteri, N. Canderlero, E. Locatelli,
E. Azzaro, R. Pozzo, and S. Bonomi. The influence of extra load on mechanical behavior of
skeletal muscle. European Journal of Applied Physiology. 53:149-154, 1984.
Bouisset, S. EMG and muscle force in normal motor activities. New Developments in
Electromyography and Clinical Neurophysiology. Edited by J.E. Desmedt. Karger, Basel. pp.
547-583, 1973.
Brand R.A., R.D. Crowninshield, C.E. Wittstock, D.R. Pedersen, C.R. Clark, and F.M. Krieken.
A Model of Lower Extremity Muscular Anatomy. Journal of Biomechanical Engineering.
104(3):304-310, 1982.
Broman, H., C.J. DeLuca, and B. Mambrito. Motor unit recruitment and firing rates interaction
in the control of human muscles. Brain Research. 337:311-319, 1985.
Brook, M.H. and K.K. Kaiser. Muscle fiber types: How many and what kind? Archives of
Neurology. 23(4):369-379, 1970.
Buchanan, T.S.. A biomechanical analysis of the neural control of muscles about the human
elbow joint during isometric tasks. PhD dissertation, Northwestern University., 1986.
Bucthal, F., and J. Lindhard. The physiology of striated muscle fiber. Det Kgl. Danske
Videnskabernes Selskab. Biologiske Meddelelser XIV, 6. Kobenhavn, Ejnar Munksgaard,
1939.
Bucthal, F.. The mechanical properties of the single striated muscle fiber at rest and during
contraction and their structural interpretation. Det Kongelige Danske Videnskabernes Selskab.
Biologiske Meddelelser XVII, 2. Kobenhavn, Ejnar Munksgaard, 1942.
94
Buchthal, F., and E. Kaiser. The rheology of the cross striated muscle fiber with particular
reference to isotonic conditions. Det Kongelige Danske Videnskabernes Selskab. Biologiske
Meddelelser 21, 7. Kobenhavn, Ejnar Munksgaard, 1951.
Buchthal, F. and H. Schmalbruch. Motor unit of mammalian muscle. Physiology Reviews.
60(1):90-143, 1980.
Budingen, H.J. and H.J. Freund. The relationship between the rate of isometric tension and
motor unit recruitment in a human forearm muscle. Pflugers Archives. 362:61-67, 1976.
Burke, E.R., F. Cerny, D. Costill, and W. Fink. Characteristics of skeletal muscle in competitive
cyclists. Medicine and Science in Sports. 19(2):109-112, 1977.
Burke, R.E., D.N. Levine, and F.E. Zajac. Mammalian motor units: physiological-histochemical
correlation in three types in cat gastrocnemius. Science. 174(4004-4010):709-712, 1971.
Burke, R.E., D.N. Levine, P. Tsairis, and F.E. Zajac. Physiological types and histochemical
profiles in motor units of the cat gastrocnemius. Journal of Physiology. 234:723-748, 1973.
Burke, R.E., and P. Tsairis. Anatomy and innervation ratios in motor units of cat gastrocnemius.
Journal of Physiology. 234:749- 765, 1973.
Burke, R.E. and V.R. Edgerton. Motor unit properties and selective involvement in movement.
Exercise and Sport Sciences Reviews. 3:31-81, 1975.
Cavagna, G.A., B. Dusman, and R. Margaria. Positive Work Done by a Previously stretched
muscle. Journal of Applied Physiology. 24(1):21-32, 1968.
Cavagna, G.A.. Elastic Bounce of the Body. Journal of Applied Physiology. 39:279-282, 1970.
Cavagna, G.A.. Storage and utilization of elastic energy in skeletal muscle. Exercise and Sports
Science Reviews. Edited by R.S. Hutton. Journal Publishing Affiliates, Santa Barbara,
California. 5:89-129, 1977.
Cavagna, G.A., G. Cittero, and P. Jacini. Effects of speed and extent of stretching on the elastic
properties of active from muscle. Journal of Experimental Biology. Edited by J.E. Treherne,
W.A Foster, and P.K. Schofield. Cambridge University Press, Cambridge, Great Britain.
91:131-143, 1981,
Cavagna, G.A., M. Mazzanti, N.C. Heglund, and G. Citterio. Storage and release of mechanical
energy by active muscle: A non-elastic mechanism?. Journal of Expermental Biology. Edited
by J.E. Treherne. The Company of Biologists Limited, Great Britain. 115:79-87, 1985.
95
Cavanagh, P.R. and P.V. Komi. Electromechanical delay in human skeletal muscle under
concentric and eccentric contractions. European Journal of Applied Physiology. 42:159-163,
1979.
Chapman, A.E.. The mechanical properties of human muscle. Exercise and Sport Science
Reviews. 13:443-501, 1985.
Cittero, G. and E. Agostoni. Selective activation of quadriceps muscle fibers according to
bicycling rate. Journal of Applied Physiology. 57(2):371-379, 1984.
Clamann, H.P., J.D. Gillies, R.D. Skinner, and E. Henneman. Quantitative measures of output of
a mortoneuron pool during monosynaptic reflexes. Journal of Neurophysiology. 37(5-6):328338, 1974.
Close, R.L. Dynamic Properties of Mammalian Skeletal Muscles. Physiological Reviews.
52(1):129-196, 1972.
Cooper, R.G., R.H.T. Edwards, H. Gibson, and M.J. Stokes. Human
muscle fatigue: Frequency dependence of excitation and force generation. Journal of
Physiology. 397:585-599, 1988.
Costill, D.L., J. Daniels, W. Evans, W. Fink, G. Krahenbuhl, and B. Saltin. Journal of Applied
Physiology. 40(2):149-154, 1976.
Coyle, E.F., D.L. Costill, and G.R. Lesmes. Leg extension power and muscle fiber composition.
Medicine and Science in Sports. 11(1):12-15, 1979.
Crowninshield, R.D., R.C. Johnston, J.G. Andrews, and R.A. Brand. A biomechanical
investigation of the human hip. Journal of Biomechanics. 11(1/2):75-85, 1978.
Curtin, N.A. and R.E. Davies. Very high tension with very little ATP breakdown by active
skeletal muscle. Journal of Mechanochemistry and Cell Motility. 3(2):147-154, 1975.
DeLuca, C.J., R.S. LeFever, M.P. McCue, and A.P. Xenakis. Behaviour of human motor units in
different muscles during linearly varying contractions. Journal of Physiology. 329:113-128,
1982.
DeLuca, C.J., R.S. LeFever, M.P. McCue, and A.P. Xenakis. Control scheme governing
concurrently active human motor units during voluntary contractions. Journal of Physiology.
329:129-142, 1982.
DeLuca, C.J.. Control properties of motor units. Journal of Experimental Biology. Edited by
J.E. Treherne. The Company of Biologists Limited, Great Britain. 115:125-136, 1985.
Dolan, P., C. Greig, and A.J. Sargeant. Muscular weakness following prolonged exercise in
man. Journal of Physiology. 366:126p, 1985.
96
Dostal, W.F., and J.G. Andrews. A three-dimensional biomechanical model of hip musculature.
Journal of Biomechanics. 14(11):803-812, 1981.
Draganich L.F., Andriacchi T.P. (1985) Three Dimensional Moments Produced by the Knee
Joint Musculature. Abstract 31st Annual ORS Meeting, Las Vegas Nevada.
Edgerton, V.R., R.R. Roy, R.J. Gregor, C.L. Hager and T. Wickiewicz. Muscle fiber activation
and recruitment. Biochemistry of Exercise. Edited by H.G. Knuttgen, H.A. Vogel, and J.
Poortmans. 13:31-49,1983.
Edgerton, V.R., R.R. Roy, R.J. Gregor, and S. Rugg. Morphological basis of skeletal muscle
power output. Human Muscle Power, Human Kinetics Publishers, Inc. Champaign Ill, Edited
by N.L. Jones and A.L. McComas. pp. 43-58, 1986.
Edman, K.A.P., G. Elzinga, and M.I.M. Noble. Enhancement of mechanical performance by
stretch during tetanic contractions of vertebrate skeletal muscle fibers. Journal of Physiology.
281:139-155, 1978.
Edman, K.A.P., G. Elzinga, and M.I.M. Noble. Greatest sarcomere extension required to recruit
a decaying component of extra force during stretch in tetanic contractions of from skeletal
muscle fibers. Journal of General Physiology. 78(4):365-382, 1981.
Edman, K.A.P., G. Elzinga, and M.I.M. Noble. Residual force enhancement after stretch of
contracting frog single muscle fibers. Journal of General Physiology. 80(5):769-784, 1982.
Edwards, R.H.T.. Human muscle function and fatigue. Human muscle fatigue: physiological
mechanisms. Ciba Foundation Symposium 82, Pitman Medical, London, pp. 1-18, 1981.
Eisenberg, B.R. Adaptability of ultrastructure in the mammalian muscle. The Journal of
Experimental Biology: Design and Performance of Muscular Systems. Edited by J.E. Treherne.
The Company of Biologists Limited. Cambridge, Great Britain. 115:55-68, 1985.
Ekbolm, B. External and internal factors influencing physical performance. Medicine and Sport
Science: Muscular Function in Exercise and Training. Edited by P. Marconnet and P.V. Komi,
Karger, Basel. 26:90-97, 1987.
Essen, B. and J. Henriksson. Glycogen content of individual muscle fibers in man. Acta
Physiologica Scandinavia. 90:645-647, 1974.
Faulkner, J.A., D.R. Claflin, and K.K. McCully. Power output of fast and slow fibers from
human skeletal muscles. Human Muscle Power, Human Kinetics Publishers, Inc. Champaign
Ill, Edited by N.L. Jones and A.L. McComas. pp. 81-91, 1986.
Fitts, R.H., D.L. Costill, and P.R. Gardetto. Effect of swim exercise training on human muscle
fiber function. Journal of Applied Physiology. 66(1):465-475, 1989.
97
Freund, H.J., H.J. Budingen, and V. Dietz. Activity of single motor units from human forearm
muscles during voluntary isometric contractions. Journal of Neurophysiology. 38(4):933-946,
1975.
Freund, H.J. Motor unit and muscle activity in voluntary motor control. Physiological Reviews.
63(2):387-436, 1983.
Fung, Y.C.. Elasticity of soft tissues in simple elongation.
213(6):1532-1543, 1967.
American J. of Physiology,
Fung, Y.C. Biomechanics: mechanical properties of living tissues. Springer-Verlag, New York,
New York, 1981.
Gans, C.. Fiber architecture and muscle function.
10:160-207, 1982.
Exercise and Sport sciences Reviews.
Garnett, R.A.F., M.J. O'Donovan, J.A. Stephens, and A. Taylor. Motor unit organization of
human medial gastrocnemius. Journal of Physiology, 287:33-43, 1979.
Gibson, H., and R.H.T. Edwards. Muscular exercise and fatigue. Sports Medicine. 2:120-132,
1985.
Gillispie, C.C. Dictionary of Scientific Biography. Charles Scribner's Sons Publishing. New
York, New York, 1972.
Gollnick, P.D., K. Piehl, and B. Saltin. Seletive glycogen depletion pattern in human muscle
fibers after exercise of varying intensity and at varying pedaling rates. Journal of Physiolgy.
241:45-57, 1974.
Gollnick, P.D.. Muscle Characteristics as a Foundation of Biomechanics. Biomechanics
VIII-A:9-31, 1981.
Gollnick, P.D., M. Riedy, J.J. Quintinskie, and L.A. Bertocci. Differences in metabolic potential
of skeletal muscle fibers and their significance for metabolic control. Journal of Experimental
Biology: Design and Performance of Muscular Systems. Edited by J.E. Treherne. The Company
of Biologists Limited. Cambridge, Great Britain. 115:191-199, 1985.
Gordon, A.M., A.F. Huxley, and F.J. Julian. Tension development in highly stretched vertegrate
muscle fibers. Journal of Physiology London, 184:143-169, 1966.
Gordon, A.M., A.F. Huxley, and F.J. Julian. The variation in isometric tension with sarcomere
length in vertebrate muscle fibers. Journal of Physiology London, 184:170-192, 1966.
Gottlieb, G.L. and G.C. Agarwal. Dynamic relationship between isometric muscle tension and
the electromyogram in man. Journal of Applied Physiology. 30(3):345-351, 1971.
98
Goubel, F. Muscle mechanics fundamental concepts in stretch-shortening cycle. Medicine and
Sport Science. Edited by P. Marconnet and P.V. Komi. Karger, Basel. 26:24-35, 1987.
Grabiner, M.D. Bioelectric characteristics of the electromechanical delay preceding concentric
contraction. Medicine and Science in Sports and Exercise. 18(1):37-43, 1986.
Greaser, M.L., R.L. Moss, and P.J. Reiser. Variations in contactile properties of rabbit single
muscle fibers in relation to troponin T isoforms and myosin light chains. J. of Physiology,
406:85-98, 1988.
Green, H.J.. Muscle power: Fiber type recruitment, metabolism and fatigue. Human Muscle
Power, Human Kinetics Publishers, Inc. Champaign Ill, Edited by N.L. Jones and A.L.
McComas. pp. 65-81, 1986.
Gregor, R.J. R.R. Roy, W.C. Whiting, R.G. Lovely, J.A. Hodgson, and V.R. Edgerton.
Mechanical output of the cat soleus during treadmill locomotion: in-vivo vs in-situ
characteristics. Journal of Biomechanics 21:721-732, 1988.
Grieg, G., T. Hortobagyi, and A.J. Sargeant. Quadriceps surface e.m.g. and fatigue during
maximal dynamic exercise in man. Journal of Physiology, 369:180p, 1985.
Grimby, L., J. Hannerz, J. Borg, and B. Hedman. Firing properties of single human motor units
on maintained maximal voluntary effort. Human muscle fatigue: physiological mechanisms.
Ciba Foundation Symposium 82, Pitman Medical, London, pp. 157-166, 1981.
Grimby, L., J. Hannerz, and B. Hedman. The fatigue and voluntary discharge of single motor
units in man. Journal of Physiology. 316:545-554, 1981.
Grimby, L. Motor unit recruitment during normal locomotion. Medicine and Sport Science.
Edited by P. Marconnet and P.V. Komi. Karger, Basel. 26:142-151, 1987.
Hannerz, J. Discharge properties of motor units in relation to recruitment order in voluntary
contraction. Acta Physiologica Scandinavia. 91(3):374-384, 1974.
Hasan, Z., R.M. Enoka, and D.G. Stuart. The interface between biomechanics and
neurophysiology in the study of movement: Some recent approaches. Exercise and Sport
Science Reviews, 169-234, 1987.
Heglund, N.C. and G.A. Cavagna. Efficiency of vertebrate locomotory muscles. Journal of
Experimental Biology: Design and Performance of Muscular Systems. Edited by J.E. Treherne.
The Company of Biologists Limited. Cambridge, Great Britain. 115:283-292, 1985.
Henneman, E., G. Somjen, and D.O. Carpenter. Functional significance of cell size in spinal
motoneurons. Journal of Neurophysiology. 28(2):560-580, 1965.
99
Henneman, E. and C.B. Olson. Relations between structure and function in the design of skeletal
muscle. Journal of Neurophysiology. 28(3):581-598, 1965.
Henneman, E., H.P. Clamann, J.D. Gillies, and R.D. Skinner. Rank order of motoneurons within
a pool: Law of combination. Journal of Neurophysiology, 37:5-6:1338-1349, 1974.
Henneman, E.. The size-principle: A deterministic output emerges from a set of probabilistic
connections. Journal of Experimental Biology: Design and Performance of Muscular Systems.
Edited by J.E. Treherne. The Company of Biologists Limited. Cambridge, Great Britain.
115:105-112, 1985.
Hennig, R. and T. Lomo. Gradation of force output in normal fast and slow muscles of the rat.
Acta Physiologica Scandinavia. 130:133-142, 1987.
Henriksson-Larsen, K., J. Freden, and M-L, Wretling. Distribution of fiber sizes in human
skeletal muscles. An enzyme histochemical study in tibialis anterior. Acta Physiologica
Scandinavia. 123(2):171-173, 1985.
Hermansen, L.. Effect of metabolic changes on force generation in skeletal muscle during
maximal exercise.
Human muscle fatigue: physiological mechanisms. Ciba Foundation
Symposium 82, Pitman Medical, London, pp. 75-82, 1981.
Hill, A.V.. First and last experiments in muscle mechanics. Cambridge University Press,
London, 1970.
Hochachka, P.W.. Fuels and pathways as designed systems for support of muscle work. Journal
of Experimental Biology: Design and Performance of Muscular Systems. Edited by J.E.
Treherne. The Company of Biologists Limited. Cambridge, Great Britain. 115:149-164, 1985.
Huijing, P.A., and R.D. Woittiez. The effect of architecture on skeletal muscle performance: A
simple planimetric model. Netherlands Journal of Zoology. 34(1):21-32, 1984.
Huijing, P.A., and R.D. Woittiez. Length range, morphology and mechanical behaviour of rat
gastrocnemius muscle during isometric contraction at the level of the muscle and muscle tendon
complex. Netherlands Journal of Zoology. 35(3):505-516, 1985.
Hultman, E., H. Sjoholm, K. Sahlin, and L. Edstrom. Glycolytic and oxidative energy
metabolism and contraction characteristics on intact human muscle. Human muscle fatigue:
physiological mechanisms. Ciba Foundation Symposium 82, Pitman Medical, London, pp.
20-40, 1981.
Huxley, H.E.. The mechanisms of muscular contraction recent structural studies suggest a
revealing model of cross-bridge action at variable filament spacing. Science, 164:1356-1366. 20,
June 1969.
Huxley, H.E.. Reflections on muscle. Princeton University Press, Princeton, N.J., 1980.
100
Huxley, H.E.. The crossbridge mechanism of muscular contraction and its implications. Journal
of Experimental Biology: Design and Performance of Muscular Systems. Edited by J.E
Treherne. The Company of Biologists Limited. Cambridge, Great Britain. 115:17-30, 1985.
Ishikawa, H. Fine structure of skeletal muscle. Cell and Muscle Motility. Edited by B.M.
Dowben and J.W. Shay. Plenum Press, New York, New York. 4:1-50, 1983.
Johnson, M.A., J. Polgar, D. Weightman, and D. Appleton. Data on the distribution of fiber
types in thirty-six human muscles An autopsy study. Journal of the Neurophysiology Sci.,
18:111-129, 1973.
Kanosue, K., M. Yoshida, K. Akazawa, and K. Fujii. The number of active motor units and their
firing rates in voluntary contraction of human brachialis muscle. Japanese Journal of Physiology.
29(4):427-443, 1979.
Karlsson, J., B. Sjodin, I. Jacobs, and P. Kaiser. Relevance of muscle fiber type to fatigue in
short intense and prolonged exercise in man. Human muscle fatigue: physiological
mechanisms. Ciba Foundation Symposium 82, Pitman Medical, London, pp. 59-74, 1981.
Katz, B. The relation between force and speed in muscular contraction.
Physiology. 96:45-64, 1939.
The Journal of
Komi, P.V.. Measurement of the force-velocity relationship in human muscle under concentric
and eccentric contractions. In Biomechanics III 3rd Int Seminar, Rome. pp. 224-229. Basler: S
Karger, 1973.
Komi, P.V. and J.H.T. Viitasalo. Signal characteristics of EMG at different levels of muscle
tension. Acta Physiologica Scandinavia. 96:267-276, 1976.
Komi, P.V. and C. Bosco. Utilization of Elastic Energy in Jumping and its Relation to Skeletal
Muscle Fiber Composition in Man. Biomechanics VI-A, pp 79-85, 1978.
Komi, P.V. and C. Bosco. Utilization of stored elastic energy in leg extensor muscles by men
and women. Medicine and Science in Sports. 10(4):261-265, 1978.
Komi, P.V.. The stretch-shortening cycle and human power output. Human Muscle Power,
Human Kinetics Publishers, Inc. Champaign Ill, pp. 27-38, 1986.
Komi, P.V. Neuromuscular factors related to physical performance. Medicine and Sport
Science. Edited by P. Marconnet and P.V. Komi. Kargel, Basel. 26:48-66, 1987.
Kushmerick, M.J.. Patterns in mammalian muscle energetics. Journal of Experimental Biology.
Design and Performance of Muscular Systems. Edited by J.E. Treherne. The Company of
Biologists Limited. Cambridge, Great Britain. 115:165-177, 1985.
101
Lippold, O.C.J.. The relation between integrated action potentials in a human muscle and its
isometric tension. Journal of Physiology London. 117:492-499, 1952.
Loeb, G.E., and C. Gans. Electromyography for experimentalists. University of Chicago Press,
Chicago, 1986.
Matsumoto, Y.. Validity of the force-velocity relation for muscle contration in the length region
l<lo. Journal of General Physiology. 50:1125-1137, 1967.
Matsumoto, Y.. Theoretical series elastic element length in Rana pipiens sartorius muscles.
Journal of General Physiology. 50:1139-1156, 1967.
McMahon, T.A.. Muscles, reflexes, and locomotion. Princeton University Press, Princeton,
New Jersey, 1984.
Metzger, J.M. and R.L. Moss. Shortening velocity in skinned single muscle fibers. Influence of
filament lattice spacing. Biophysical Journal. 52(1):127-131, 1987.
Miller, N.R.. Effect of load, speed and configuration on the electromyographic activities of the
skeletal muscles. PhD dissertation. Univeristy of Michigan, 1976.
Milnar-Brown, H.S., R.B. Stein, and R. Yemm. Changes in firing rate of human motor units
during linearly changing voluntary contractions. The Journal of Physiology. 230(2):371-390,
1973.
Nemeth, G. and H. Ohlsen. In vivo moment arm lengths for hip extensor muscles at different
angles of hip flexion. Journal of Biomechanics. 18(2):129-140, 1985.
Nemeth, P.M. and D. Pette. The limited correlation of myosin-based and metabolism-based
classifications of skeletal muscle fibers. The Journal of Histochemistry and Cytochemistry.
29(1):89-90, 1981.
Newmiller, J., M.L. Hull, and F.E. Zajac. A mechanically decoupled two force component
bicycle pedal dynamometer. Journal of Biomechanics. 21(5):375-386, 1988.
Nichols, T.R. The regulation of muscle stiffness implications for control of limb stiffness.
Edited by P. Marconnet and P.V. Komi. Karger, Basel. Medicine and Sport Science. 26:36-47,
1987.
Norman, R.W. and P.V. Komi. Electromechanical delay in skeletal muscle under normal
movement conditions. Acta Physiologica Scandinavia. 106(3):241-248, 1979.
Peachey, L.E.. Excitation-contraction coupling: The link between the surface and the interior of
a muscle cell. Journal of Experimental Biology. Design and Performance of Muscular Systems.
Edited by J.E. Treherne. The Company of Biologists Limited. Cambridge, Great Britain.
115:91-98, 1985.
102
Perrine, J.J. and V.R. Edgerton. Muscle force-velocity and power-velocity relationships under
isokinetic loading. Medicine and Science in Sports. 10(3):159-166, 1978.
Perry, S.V. Properties of the muscle proteins - A comparative approach. Journal of
Experimental Biology: Design and Performance of Muscular Systems. Edited by J.E. Treherne.
The Company of Biologists Limited. Cambridge, Great Britain. 115:31-42, 1985.
Person, R.S. and L.P. Kudina. Discharge frequency and discharge pattern of human motor units
during voluntary contraction of muscle. Electroencephalography and Clinical Neurophysiology.
32(4-6):471-483, 1972.
Pette, D.. Metabolic heterogeneity of muscle fibers. Journal Experimental Biology: Design and
Performance of Muscular Systems. Edited by J.E. Treherne. The Company of Biologists
Limited. Cambridge, Great Britain. 115:179-189, 1985.
Pierrynowski, M.R. and J.B. Morrison. Length and Velocity Patterns of the Human Locomotor
Muscles. Biomechanics IX-A, pp 33-38, 1983.
Pinto, J. and Y.C. Fung. Mechanical properties of the heart muscle in the passive state. Journal
of Biomechanics. 6(6):597-616, 1973.
Pollack, G.H.. The cross-bridge theory. Physiology Reviews. 63:1049- 1113, 1983.
Rall, J.A.. Energetic Aspects of skeletal muscle contraction:
Exercise and Sport Sciences Reviews. 13:33-73, 1985.
Implications of fiber types.
Reiser, P.J., R.L. Moss, G.G. Giulian, and M.L. Greaser. Shortening velocity in single fibers
from adult rabbit soleus muscles is correlated with myosin heavy chain composition. Journal of
Biological Chemistry. 260(16):9077-9080, 1985.
Reiser, P.J., R.L. Moss, G.G. Giulian, and M.L. Greaser. Shortening velocity and myosin heavy
chains of developing rabbit muscle fibers. Journal of Biological Chemistry. 260(27):1440314405, 1985.
Reiser, P.J., C.E. Kasper, M.L. Greaser, and R.L. Moss. Functional significance of myosin
transitions in single fibers of developing soleus muscle. American Physiological Society, pp.
c605-c613, 1988.
Rohmert, W. Ermittung von Erholung-spausen fur statische arbeit des menschen. Int. Angew.
Phyisol., 18:123, 1960.
Saltin, B.. Muscle fiber recruitment and metabolism in exhaustive dynamic exercise. Human
muscle fatigue: physiological mechanisms. Ciba Foundation Symposium 82, Pitman Medical,
London, pp. 41-52, 1981.
103
Saltin, B. and P.D. Gollnick. Skeletal muscle adaptability: significance for metabolism and
performance. In Handbook of Physiology: Skeletal Muscle. section 10, Chp 19, American
Physiological Society, Bethesda, Maryland, 1983.
Secher, N.H. Motor unit recruitment. A pharmacological approach. Medicine and Sport
Science. Edited by P. Marconnet and P.V. Komit. Karger, Basel. 26:152-162, 1987.
Seigler, S., H.J. Hillstrom, W. Freedman, and G. Moskowitz. Effect of myoelectric signal
processing on the relationship between muscle force and processed EMG. American Journal of
Phys. Medicine. 64(3):130-149, 1985.
Seireg, A. and A. Arvikar. A mathematical model for the evaluation of forces in the lower
extremities of the musculoskeletal system. Journal of Biomechanics. 6(3):313-326, 1973.
Sjogaard, G. Muscle fatigue. Medicine and Sport Science. Edited by P. Marconnet and P.V.
Komi. Karger, Basel. 26:98-109, 1987.
Spector, S.A., P.F. Gardiner, R.F. Zernicke, R.R. Roy, and V.R. Edgerton. Muscle architecture
and force-velocity characteristics of cat soleus and medial gastrocnemius: Implications for
motor control. Journal of Neurophysiology. 44(5)951-960, 1980.
Spurway, N. Interrelationship between myosin-based and metabolism-based classifications of
skeletal muscle fibers. The Journal of Histochemistry and Cytochemistry. 29(1):87-88, 1981.
Squire, J. The Structural Basis of Muscular Contraction. Plenum Press, New York, New York,
1981.
Squire, J. Muscle Design, Diversity, and Disease. 1986.
Stephens, J.A. and A. Taylor. Fatigue of maintained voluntary muscle contraction in man.
Journal of Physiology. 220(1):1-18, 1972.
Stephens, J.A., and T.P. Usherwood.
Physiology, 250:37p, 1975.
The fatigability of human motor units. Journal of
Taylor, C.R.. Force development during sustained locomotion: a determinant of gait speed and
metabolic power. Journal of Experimental.Biology: Design and Performance of Muscular
Systems. Edited by J.E. Treherne. The Company of Biologists Limited. Cambridge, Great
Britain. 115:253-262, 1985.
Thorstensson, A.. Muscle strength fiber types and enzyme activities in man. Acta Physiologica
Scandinavia Supplementum 443, 1976.
Thorstensson, A., G.Grimby, and J. Karlsson. Force-velocity relations and fiber composition in
human knee extensor muscles. Journal of Applied Physiology. 40(1):12-16, 1976.
104
Thys, H., T. Faraggiana, and R. Margaria. Utilization of Muscle Elasticity in Exercise. Journal
of Applied Physiology. 32(4):491-494, 1972.
Thys, H., G.A. Cavagna, and R. Margaria. The Role Played by Elasticity in an Exercise
Involving Movements of Small Amplitude. Pflugers Archives, 354:281-286, 1975.
van Eijden, T.M.G.J., W De Boer, and W.A. Weijs. The orientation of the distal part of the
quadriceps femoris muscle as a function of the knee flexion-extension angle. Journal of
Biomechanics. 18(10):803-809, 1985.
van Kaam, F.A.M., E.L. De Beer, G.L.M. Steinen, and T. Blange. The influence of velocity of
length change on tension development in skeletal muscle: Model calculations and experimental
results. Journal of Biomechanics. 17(7):501-511, 1984.
Viitasalo, J.T. and P.V. Komi. Interrelationship between electromyographic, mechanical, muscle
structure, and reflex time measurements in man. Acta Physiologica Scandinavia. 111(1):97-103,
1981.
Viitasalo, J.T. and P.V. Komi. Force-time characteristics and fiber composition in human leg
extension muscles. European Journal of Applied Physiology. 40(1):7-15, 1978.
Vollestad, N.K. Motor unit recruitment. A historical approach. Medicine and Sport Science.
Edited by P. Marconnet and P.V. Komi. Karger, Basel. 26:128-141, 1987.
Whalen, R.G. Myosin Isoenzymes as molecular markers for muscle physiology. Journal of
Experimental Biology: Design and Performance of Muscular Systems. Edited by J.E. Treherne.
The Company of Biologists Limited. Cambridge, Great Britain. 115:42-53, 1985.
Wilkie, D.R.. Shortage of chemical fuel as a cause of fatigue: studies by nuclear magnetic
resonance and bicycle ergometry.
Human muscle fatigue: physiological mechanisms. Ciba
Foundation Symposium 82, Pitman Medical, London, pp. 102-114, 1981.
Woittiez, R.D., P.A. Huijing, and R.H. Rozendal. Influence of muscle architecture on the
force-length diagram A model and its verification. Pflugers Archives. 397:73-74, 1983.
Wood, J.J. and B. Bigland-Ritchie. Linear and non-linear surface EMG/force relationships in
human muscles. American Journal of Phys. Med.. 62(6):287-299, 1983.
Zahalak, G.I., J. Duffy, P.A. Stewart, H.M. Litchman, R.H.
Hawley, and P.R. Paslay. Partially activated human skeletal muscle: An experimental
investigation of force, velocity, and EMG. Journal of Applied Mechanics, pp. 81-86, March
1976.
105
Zajac, F.E. and J.S. Faden. Relationship among recruitment order, axonal conduction velocity,
and muscle-unit properties of type-identified motor units in cat plantaris muscle. Journal of
Neurophysiology. 53(5):1303-1322, 1985.
Zuniga, E.N. and D.G. Simons. Nonlinear relationship between averaged electromyogram
potential and muscle tension in normal subjects. Archives of Physical Medicine and
Rehabilitation. 50(1):613-620, 1969.
Sample Problems:
1. Describe each of the following.
a. motor unit
b. innervation ratio
c. rate coding
d. recruitment
e. tetanus
f. twitch
2. Estimate the maximum isometric force that a fusiform muscle having a physiological crosssectional area of 10 cm2 could generate. State all assumptions.
3. Would a muscle shorten in the body if it were activated while the joints that the muscle
spanned remained fixed? Explain the rationale for your response. If the muscle were to shorten,
then please explain what factors would affect the amount of shortening that would occur.
4. Please explain the structural and functional differences between a fast-twitch and a slowtwitch motor unit.
5. Please explain what is meant by excitation-contraction coupling.
6. Estimate the force that a muscle would generate if fully activated (all motor units) and
shortening at 40 cm/s. Assume the muscle can generate a maximum isometric force of 1000 N
and has a maximum unloaded shortening velocity of 90 cm/s. State all assumptions.
7. Explain why slow-oxidative fibers might require more energy to maintain vs. fast-glycolytic
fibers.
8. Explain how you think a relatively inactive muscle would adapt to a strength training
program.
9. If a muscle becomes denervated, then how would the muscle change?
10. If the bicep muscle has 13 cm length fibers, an overall muscle length of 31 cm, a constant
moment arm length of 5 cm about the elbow, and contracts to displace the forearm to cause an
elbow angle change of 100 degrees, then what length change would you expect the muscle to
experience and how the force in the muscle be affected throughout the elbow motion.?
106