-
Motor Unit Recruitment and the Gradation of
Muscle Force
The capabilities of the dzfferent types of motor units are reviewed, and theirproperties in a variety of muscles are discussed. Because the tendon-generating capacities of nwtor units are so dzfferent, the order in which they are recruited will have
a strong influence on the way force output of the whole muscle is graded. Activation of motor units in a random order produces a roughly linearforce increase
with progressive recruitment, whereas recruitment of motor units in order of increasingforce produces an approximately exponentialforce increase as the number of active motor units increases. The latter scheme allowsfine control of weak
movememts and rapid production of powefil movements. Motor units are shown
to be well adapted to the tasks they must peform, and a "compromise" motor
unit will not fulfill all the tasks demanded of it. Finally, changes in motor unit
properties produced by dzferent activity pattern and by muscle reinnmation are
revieweti and the implicationsfor rehabilitation are discussed. [Clamann HP.
Motor unit recruitment and the gradation of muscleforce. Phys Ther. 1993;73:
H Peter Clamann
830-843.1
Key Words: Force gradation, Motor units, Plasticity, Recruitment.
The force output of a typical skeletal
muscle can be modulated over an
enormous range, typically more than
ten thousandfold. It is generally stated
that this modulation of force output is
accomplished by a combination of
rate coding of individual motor units
and recruitment of more o r fewer
motor units. These processes are so
well known and so generally accepted
that less thought is given them than
they deserve. The purpose of this
article is to examine some of the
strengths and limitations of these
processes. I will suggest some answers to such questions as: Why is it
functionally useful to subdivide a
muscle into motor units? Are motor
units of very different types needed?
Is a fixed recruitment order advantageous, and is this always so?
These questions have been discussed
before, but the answers given have
not always been the same. It may be
useful to summarize recent findings
and to show how the study of motor
units in the laboratory deepens our
understanding of how a muscle functions, and may produce results useful
to the practicing physical therapist.
Not all muscles are subdivided into
motor units, nor is rate coding a possible way of modulating force in all
muscles. The best example of a muscle in which force modulation is not
possible either by rate coding o r by
recruitment of motor units is the
HP Clamann, PhD, is Professor of Anatomy, Department of Physiology, University of Berne, Buhlplatz 5, CH 3012 Berne, Switzerland.
This work: was supported in part by a grant from the Swiss National Science Foundation.
Physical Therapy/Volume 73, Number 12iDecember 1993
mammalian heart. The heart muscle is
an extremely slow, fatigue-resistant
muscle, much more so than the
much-studied soleus muscle of the
cat. The action potential of ventricular
muscle lasts about 300 milliseconds,
and a twitch lasts about as long. Because the muscle membrane is refractory during the action potential, it is
difficult o r impossible to stimulate
heart muscle until the twitch is nearly
past. A fused tetanus cannot be produced, and although a partly fused
tetanus may be generated, the necessary stimulus frequency is too slow to
produce much force increase. The
heart pumps with a series of twitches
of the individual muscle fibers. This
process is described in textbooks on
human physiology,l.2 and particularly
good accounts may be found in the
books edited by Mountcastles and by
Schmidt and Thews4
Because heart muscle cells are electrically coupled, an action potential
830 / 11
produced in one is conducted to its
neighbors and excites them. Contraction proceeds over the muscle in a
wave, involving all the muscle cells in
a sequence determined by the current
paths and with a speed determined by
the conduction velocity of the coupled fibers. Heart muscle is said to act
as a functional unit, a syncytium. Stirnulate one part of it, and the whole
muscle contracts. There is no organization into motor units, and the recruitment of only a part of the muscle
is not possible, at least in the normal
heart. This way of controlling a muscle may seem strange to one who is
accustomed to thinking mainly of
skeletal muscles, but it works very
well for the heart.
Skeletal muscles are called on to
perform a very different series of
tasks. The work of the heart changes
from a minimum when pumping
blood for a person at rest to about 10
times the work pumping blood for
the same person working at his or
her aerobic maximum. The working
range of a skeletal muscle is several
orders of magnitude larger. The heart
accomplishes its task with a series of
twitches. A skeletal muscle may produce an impulsive force, a steady
tetanic contraction, or any of a variety
of time-varying forces in between. It is
not surprising that skeletal muscle is
designed in a different way to produce this far greater variety of tasks.
On the other hand, the heart must
carry out its stereotyped task without
interruption for a lifetime, whereas
even the most fatigue-resistant skeletal
muscle is granted periods of rest. This
is also reflected in the muscle's design. We may say that a muscle divided into motor units offers the advantage that a greater or lesser part of
the muscle may be activated, allowing
a range of force outputs limited
largely by the number of motor units.
Motor Unit llTypes"
Henneman and co-workers5s6 were
the first to examine the mechanical
properties of individual motor units
(reviewed by Henneman and Mendell3 and to show that motor units
have very different speeds and
strengths of contraction. At the same
time, histological evidence8 showed
that three distinct types of muscle
fibers could be identified, distinguishable by their oxidative metabolic
capabilities, fiber diameters, and other
properties. Henneman and coworkers inferred that all the muscle
fibers of a motor unit were of the
same histological type; this fact was
directly demonstrated 3 years later by
Edstrom and Kugelberg.9
At about this time (1967), Burke and
co-workers (reviewed by Burkelo) set
about defining mechanical criteria
that would separate motor units into
three distinct types matching those
found histologically. They succeeded
in separating motor units into fast and
slow, fatigable and fatigue-resistant
units in such a way that three motor
unit types emerged according to these
mechanical criteria. A stubbornly
unclassifiable motor unit type, with a
fast twitch and an intermediate fatigue
resistance, proved to appear consistently in cat hind-limb muscles and
was designated as a fourth type (Fl)
in studies after 1974. The three basic
motor unit types could be shown to
be uniquely identifiable according to
the metabolic pathways they used to
produce force (reviewed by Burkelo).
The histologically elusive intermediate
unit was later identified by McDonagh
and co-workers." The names and
correspondence of these motor unit
types are
Fast, fatigable (FF) = fast, glycolpic
(FG)
Fast, intermediate in fatigability (FI, F
[int]) = FI (McDonagh et all1)
Fast, fatigue resistant (FR) = fast, oxidative glycolpic (FOG)
Slow (S) = slow, oxidative (SO), utilizing glycogen and fat for energy
Most of the early studies were performed on the triceps surae group of
muscles in the cat; in particular, the
medial gastrocnemius (MG) and soleus muscles were studied in great
detail. The soleus muscle turned out
to be an unusual muscle, composed
exclusively of slow motor units. The
MG muscle was found to be a mixed
muscle and can be regarded as typical. Many other muscles had histological staining patterns that showed they
also possessed three muscle fiber
types, but for a variety of technical
reasons, mechanical properties of
their motor units were not examined
immediately. As a consequence, the
tests of speed and fatigue resistance
so suitable for motor units of the MG
muscle became standard tests. This is
unfortunate, because some muscles,
particularly in humans, differ so much
from the cat MG muscle in speed and
fatigability that the "standard tests" are
of little use.
The histochemical classifications have
also been questioned. Many histochemical studies, particularly those
involving human muscles, divide mo,
tor units into the three types (IIIa,
and IIb),12-l4whereas a type intermediate between types I and IIa, called IIc,
is occasionally mentioned.14-16The
following equivalence is often made in
the histochemical domain alone:
SO=I=B
FOG = IIa = C
FG = IIb = A
where the A, B, C classification used
by Henneman and Olson in their
original work8 matches the SO, FOG,
FG classification quite well, but is less
commonly used today. A number of
other classifications have been used,"
which will not be mentioned here.
Making such a table of equivalences is
risky because different histochemical
methods are used to establish the
classification schemes, and they need
not be truly equivalent. The reason is
worth examining briefly because data
from the literature are often misinterpreted. A detailed discourse of histochemical classification schemes, however, could easily form a review on its
own and is best left to an expert in
that field. It is beyond the scope of
this review. Brooke and Kaiser attempted to make a table of equivalent
classifications and abandoned the idea
with the words
. . . although it is true that in a given
animal or even another muscle in the
Physical Therapy/Volume 73, Number 12/December 1993
1
i
same animal such a correlation can be
made, when another animal or even
another muscle in the same animal is
consiclered, the correlations are different. To take a very simple example, the
type IIa fiber in a rat gastrocnemius is
a red or C fiber; however, in the human biceps, the type IIa fiber is an
intermediate or B fiber.17@135)
The problem arises because a muscle
fiber is a complex system, the function of which can be tested in many
ways that are not equivalent. Henneman and co-workers, in their original
work (this has been reviewed in detail?, stained the mitochondria in
muscle fibers; they described A fibers
with fenr mitochondria (white, FG), C
fibers that stained richly for mitochondria (red, FOG), and an intermediate type B (SO). Peter et all8 and
later Burke10 used stains that demonstrated the oxidative capacity of the
myofibri.1~of muscle fibers to identify
them as SO, FOG, or FG fibers. Often,
several stains were used on successive
sections of the same fiber.
The methods used to classify fibers as
I, IIa, or IIb are quite different.12 The
muscle fibers are incubated at a
known pH @reincubation). They are
then stained with chemicals that show
the ability of the muscle fiber to utilize adenosine triphosphate, an ability
that may have been destroyed by the
preincubation. If the adenosine triphosphatase (ATPase) activity remains
intact in the pH range of 3.9 to 10.8, it
is considered acid stable and identifies the fiber as type I. Group I1 fibers
are acid labile and retain their ATPase
activity after preincubation in a bath
within a pH range of 4.5 to 10.8 (type
IIb) or 4.9 to 10.8 (type IIa). These
values are for human biceps or vastus
lateralis muscles12 and may differ in
other muscles or in animals.14j15317It
is now known that the pH stability
depends on the structure of a heavy
chain of the myosin molecule; the
significance of this for myosin ATPase
activity is not fully understood.19
In humans, types IIa and IIb also
overlap greatly in their aerobic capacity (ie, in the ability to identify them
as FOG or FG).I4J5The classical IIa
fiber of rodents, with its strong oxidative and glycolytic capacity, is quite
different from the human IIa fiber,
which stains only moderately for the
enzymes of oxidative and glycolytic
activity.19 This d8erence should not
be surprising; there is no compelling
reason to suppose that the acid stability of the enzyme ATPase in a muscle
fiber (I, IIa, IIb), the oxidative and
glycolytic enzyme content of the fiber
(SO, FOG, FG), and the number of
mitochondria the fiber contains (A, B,
C) should all be perfectly correlated.
Some histochemists have pursued this
idea, performing multiple staining
tests and dividing muscle fiber into as
many as nine types.20Jl
Motor units in different muscles may
differ widely, even when they carry
the same names. The Table lists the
motor unit populations of several
muscles and gives some properties of
the motor unit types. All data listed
were obtained from muscles of the
cat. The list is neither representative
nor complete. Instead, the muscles
have been selected deliberately because their motor unit compositions,
or the properties of their motor units,
are very different. Because of its familiarity, the classification of Burke and
co-workers has been retained in most
publications, even when the original
definitions do not apply. It is important to realize that a fast motor unit in
one muscle may be very different
from a fast motor unit in another
muscle of the same animal. The properties of motor units of the same
muscle in different animals may also
differ widely. Figure 1 shows model
twitches of FF and S motor units in
the MG muscle. The twitches have
been generated with a simple mathematical equation but represent the
typical shape of a twitch. In the upper
panel, forces are shown to scale; in
the lower panel, they are normalized
so that speed differences are easier to
compare. In any one muscle, it is
fairly easy to identify three or four
district motor unit types by differences in speed, strength, and fatigability. It is risky to extrapolate and assume that the properties of motor
units with the same names in another
muscle are the same.
Physical Therapy/Volume 73, Number 12December 1993
Figure 2 makes this point by showing
two FF units from different muscles,
the flexor carpi radialis (FCR) and the
diaphragm. Note that the FF unit of
the FCR muscle is more powerful and
faster than the corresponding FF unit
in the diaphragmatic muscle.
Several interesting features of the
relationship among motor units may
be derived from the Table. In any
muscle, FF motor units are the strongest, usually two to three times as
strong as FR units (FI units tend to be
an ambiguous group and, as discussed previously, lie in a position
intermediate between FF and FR
units). Note that the diaphragm is an
exception in that FR units produce
75% as much force as FF units, on
average. Measurements were made
from intact diaphragms and from
portions of the diaphragm detached at
the costal margin. Only data obtained
from the latter experiments were
reported, because the tetanic force of
all motor unit types was about 25%
greater when the portion of the diaphragm was detached from the ribs.
Type S units are, as a rule, less than
half as strong as FR units. The FCR
muscle represents an extreme motor
unit relationship. The average type S
unit is only one fifth as strong as the
average FR unit. Note also that the
muscle is composed of 40% of these
type S units. Thus, this large population of weak units produces only 8%
of the muscle's maximum force.22
Twitch contraction times of type S
units tend to be about twice as long
as those of FF units. An exception is
the extensor digitorum longus (EDL)
muscle, in which all motor units are
3
remarkably similar in ~ p e e d . ~Notice
the differences in the motor unit
populations of the diaphragm and of
the peroneus longus muscle in this
regard (Table). In both muscles, average twitch contraction times span a
range of two to one. Yet the type S
motor units of the peroneus longus
muscle, with a mean twitch contraction time of 30.9 milliseconds, are
actually faster than the average FF unit
of the diaphragm, with a mean twitch
contraction time of 34 milliseconds.
These findings emphasize the state-
scheme. First, these muscles contain a
population of nontwitch (NT) motor
units, which only produce force when
stimulated repetitively at rather high
frequencies. Second, it has recently
been shown that these muscles contain a population of slow, fatigable
(SF) motor units.28It should be mentioned that all extraocular motor units
are at least an order of magnitude
faster and weaker than those of limb
muscles; therefore, the tests by which
speed and fatigability are measured
must be strongly modified.28
o
20
40
m
80
100
120
140
160
1 0
120
140
180
1W
200
Time (ms)
0
20
40
60
60
100
Time (ms)
Figure 1. Mathematically generated model twitches of fast, fatigable (FF) and slow
(S) motor units of medial gastrocnemius (MG) muscle: (Top) Twitch time course plotted
against twitch force. (Bottom) Twitchforces scaled so that muximum force=l.
ment made earlier that the tetrapartite
motor unit classification works well
within one muscle but should not be
used as a global classification.
Finally, the percentages of the different motor unit types making up any
muscle differ greatly. The classic example, not listed in the Table, is the
cat soleus muscle, which consists
exclusively of type S motor units. This
homogeneity is true for the cat6a and
guinea pig,24 but not for most other
14 / 833
animals. For example, in the rat25 and
in humans,26 the soleus muscle is a
mixed muscle in which type S motor
units predominate. The FCR muscle in
the cat is composed of almost half
type S motor
whereas the EDL
muscle contains a mere 6% of these
units23
The muscles that move the eye are a
world unto themselves (reviewed by
Goldberg?. It is difficult to fit their
motor units into the usual tetrapartite
Although it is convenient to speak of
motor unit types, this does not mean
that their properties are discrete and
nonoverlapping. In any muscle, it is
possible to find type S motor units
that are stronger than some type FR
motor units of the same muscle; the
same is often true for speed. Although
the Table may appear to list discrete
properties of the various motor unit
types, overlaps among most properties occur. The exception is usually
fatigability; FF and FR motor units are
readily distinguished according to
fatigability using the test developed by
Burke.l0 Of all the tests of motor unit
properties, the results of this test are
the easiest to interpret. Nevertheless,
even this test has had to be modified,
albeit with some controversy, to accommodate unusually fast muscles
such as the FCR, peroneus longus,
and extraocular rn~scles.22~28~29
By almost all measures then, motor
units are most readily arranged in a
continuum, and certainly they are
brought into activity not according to
some type o r grouping, but smoothly
in a continuous order.' A classification
into "types" selves as a useful shorthand to identify extreme properties.
Such classification shows the differences among motor unit properties
such as speed, strength, metabolic
pathways used to produce energy,
and fatigability in a clear, readily understandable way. There are gradations in all motor unit properties,
however, and all gradations show a
continuum from one extreme to the
other. It is this spectrum of properties
that is taken advantage of when motor
Physical Therap)r/Volume 73, Number 12December 1993
II
0
20
40
BO
80
100
120
140
180
180
200
Time (ms)
FCR
0
20
Diaphragm
40
BO
80
100
120
140
1 0
180
'I'irne (ms)
Figure 2. Model twitches of two fast, fatigable (FF) motor units&m the flexor
carpi radialis (FCR) mmtrle faster, stronger unit) and&m the diaphragm (weaker,
slower unit): (Top) Twitch time course plotted against twitch force. (Bottom) Twitch
forces scaled so that maximum force=l. Note the great dtrerence in strength and speed
of these two motor units.
units are recruited to grade muscle
force.
There has been considerable difficulty
in classifying human motor units
according to mechanical properties,
in part because they cannot be isolated by the invasive techniques used
in animal experiments. Human motor
units are usually studied by mi-
crostimulation of fine nerve terminals
in the muscle o r by percutaneous
nerve stimulation,30-32or by spiketriggered averaging.33A weak stimulus
delivered percutaneously o r through
an electrode inserted into a muscle
may trigger action potentials in a
single axon o r axon branch. The
spike propagates into all the branches
of the axon, activating a single motor
Physical Therapy/Volume 73, Number 1 2 ~ e c e m b e 1993
r
unit. Spike-triggered averaging is
somewhat more complex. A fine-wire
electromyographic (EMG) electrode
in the muscle is used to identify the
action potentials of a single motor
unit, which is only possible at low to
intermediate force output. It is assumed that the action potential can be
reliably identified and isolated. The
action potential is used to trigger a
computer, which measures the force
output of the same muscle. The computer stores the muscle force as a
function of time for a short period
(eg, 300 milliseconds) after the trigger
pulse and adds up successive force
records. Because the twitch from the
motor unit in which the EMG spike is
used as the trigger always occurs at
the same time relative to the trigger,
successive twitches are added in the
computer. The twitches of other units
occur randomly in relation to the
trigger and tend to be smoothed out.
In this way, the twitch of one unit
may be selected.
In the first method, the number of
motor units it is possible to isolate is
small, and, in the second method,
serious errors in measurement are
possible.34 Because, even at low discharge rates, motor units produce
partially fused contractions, the time
course of individual twitches is distorted and their amplitude is underestimated. Additionally, the spiketriggered averaging method is based
on the assumption that only the signal
of interest occurs in a Fured time
relation to the trigger; synchronous
discharges of motor units would produce artifacts.
These problems have been largely
circumvented in a recent study on
thenar muscles by a group working in
the laboratory of Johansson in
S~eden.3~-s6
Fine tungsten electrodes
were inserted into single axons of the
median nerve to allow the stimulation
of single motor units in the thenar
muscles. Tetanic force ranged from 28
to 174 mN (2.9-17.7 g). Twitch contraction times ranged from 35 to 80
milliseconds. In contrast to the findings of most animal experiments,
there was no correlation between
strength and speed of motor units.
-
Table. Some Properties of Motor Unit Type in Seven Muscles of the Cat
Muscle
Motor
Unit
Typea
Percentage
of
Population
Force
(mN)
X
SD
Mean Twltch
Contraction Tlrne
(rns)
The relation between fiber composition and function is most readily seen
in the extensive study of the muscles
of birds by George and Berger.38 I
know of no other example in which
the same muscle has been studied in
such a wide variety of species and
shown to exhibit such a variety of
fiber compositions. Although the
relevance of bird flight muscles to
physical therapy in humans may not
be immediately apparent, this digression is presented for two reasons.
First, it is intended to impress on the
reader that the same muscle may have
entirely different properties in different species. The "typical" cat MG
muscle may tell us little about properties of that muscle in humans. Similarly, humans trained to perform
specialized tasks, in a sport, for example, o r subjected to movement constraints, as after a stroke, show a remarkable diversity in properties of
the same mu~cle.14~26~39.40
Second, a
particular muscle is marvelously
adapted to its particular function. This
is most easily seen in the variety of
flight muscles adapted to a variety of
styles of flight. Flight is a form of
locomotion with severe constraints
produced by the laws of aerodynamics, so flight muscles must represent
an extremely specialized design.
Extensor digitorum
longus23
Flexor carpi radialis22
Rectus lateralis28
Medial gastrocnemius57
Peroneus 10ngus~~
Tibialis anterior23
aFF=fast, fatigable; FI-fast, intermediate in fatigability; FR=fast, fatigue resistant; S=slow; SF=slow,
fatigable; NT=nontwitch.
usio ion frequencies (s-') instead of twitch contraction times given for rectus lateralis muscle
That is, there was no tendency for the
strongest motor units to be the fastest,
as is the case for the motor units
shown in the Table, nor was it possible to divide the units studied into
types in the conventional way.
Motor Unlt Populatlonr and
Muscle Functlon
We have seen that the percentage of
each motor unit type in a muscle
differs widely from muscle to muscle.
16 / 835
been studied, to my knowledge. At
the other extreme are the tensor
nluteofemoralis musfasciae latae and cles, which are composed almost
exclusively of type FG muscle fibers24
(cited by McDonagh et al33.
This difference is related to the task
the muscle is most commonly required to perform. The vast majority
of muscles are mixed, being composed of three o r four motor unit,
and hence muscle fiber, types. The cat
soleus muscle is perhaps the bestknown exception, being composed
solely of type S motor units. The
vastus intermedius muscle is also
composed predominantly o r exclusively of type SO muscle fibers,Z*.37
although its motor units have not
Only the muscle fiber types and their
percentages are presented in the
monograph by George and Berger,38
and these fiber types are referred to
as red, white, and intermediate. It is
safe to assume that these fiber types
correspond approximately to FOG,
FG, and SO fibers, respectively, of the
modem nomenclature. The authors
describe the fiber compositions of the
pectoral muscles, the flight muscles of
birds of several classes.
Domestic fowl have pectoral muscles
in which FG fibers predominate. This
predominance is consistent with the
flight behavior of chickens, a sprint-
Physical Therapy/Volume 73, Number 12December 1993
like activity with little endurance.
Ducks and geese, by contrast, have
pectoral muscles consisting predominantly of FOG fibers. This predominance is what one might expect of a
migratory bird, which must be an
endurance flier and yet engages in
rapid wing movements. Pigeons and
doves have pectoral muscles consisting of a mixture of FOG and FG fibers. Several other birds of unrelated
types (eg, the cattle egret) have muscles of like composition. These birds
may be considered to be sprinting
fliers, but spend far more time in the
air and are better fliers than fowl.
A group of birds that spends much
time in the air would be expected to
have flight muscles designed for endurance. Pectoral muscles composed
exclusively of oxidative muscle fibers
(FOG and SO) are found in a large
variety of birds, including swallows
and swifts, crows, red-winged blackbirds, and robins, to name a few.
Hummingbirds, as might be expected,
have pectoral muscles composed
exclusively of FOG fibers. To my
knowledge, there is no muscle composed only of FOG fibers in a marnmal. Finally, several types of birds
have pectoral muscles composed
exclusively of SO fibers, like the soleus muscle of the cat. Such a muscle
would be designed to produce steady
force without fatigue for long periods
of time, but would not be designed
for rapid movement. This type of
muscle is found in soaring birds such
as kites and vultures. Although soaring is clearly locomotion, it can be
argued that a soaring bird maintains a
posture more than it engages in a
locomotory movement.
The idea that muscle structure is
exquisitely adapted to function is
readily carried over to mammals. In
the cat, the ankle flexor tibialis anterior (TA:) muscle is composed predominantly of FG fibers23 (Table).
The cat stands on its toes and uses
this muscle for locomotion, but not
for posture. In humans, this muscle is
composed of 65% to 80% SO fibers,26
and it is used to maintain our upright
posture. We may conclude that there
is no "typical" muscle; the fiber com-
position of a muscle depends on the
use to which it is put by the particular
animal, or human, it serves. Humans
seem to vary in their physical fitness
more than animals, and so show a
wider range in the composition of
their muscle fiber types than do most
animals. This is bome out by studies26840 in which examination of the
same muscles in autopsy or biopsy
samples from numerous subjects
shows a remarkable variability.
It is not yet known what determines
the fiber type composition of a motor
unit or of a muscle. The use to which
it is put undoubtedly plays a role. It is
likely that fiber type is determined in
part genetically. Hoh41 has suggested
that myoblasts exist in characteristic
types, each with a limited range of
functional plasticity. Motor nerves or
stimulation can only modify the phenotype of muscle fibers within that
range. The particular range of the
fiber is thus an intrinsic property
determined genetically; it depends on
the type of muscle and the genetic
history of the fiber itself. This is consistent with the cross-innervation
studies of Gordon and co-workers.42
They cross-reinnervated a flexor and
an extensor muscle group, so that the
triceps surae muscle received input
from the common peroneal nerve.
The reinnervated soleus muscle produced no FG muscle fibers, although
such fibers were found in the MG and
lateral gastrocnemius muscles. A similar suggestion has been made by
Gunning and Hardemana43They suggest that embryonic cells destined to
become muscle fibers differentiate
under genetic control, a control that
determines what types of myosin they
will make. Slow and fast fibers differentiate early and become difficult to
interconvert later. It is only at a later
stage that the fast fiber types differentiate further. Environmental and functional information can influence the
genetic control, however, so that
adaptation is possible.
Bouchard and co-workers44 studied
the fiber composition in biopsy samples of muscles obtained from dizygotic and monozygotic twin brothers.
The finding that identical twins
Physical Therapy/Volume 73, Number 12December 1993
showed greater similarity in their
fiber type composition than did the
other groups suggests a genetic component to muscle fiber composition.
Considerable variability, however,
remains. The system is flexible, and,
although genetics clearly plays a role,
it is not the whole story.
In animals and humans, the fiber
composition of a muscle changes if its
use is changed or if it is chronically
stimulated. This was first shown by
Salmons and Vrbova,45 who were able
to convert a muscle with a predominance of FG muscle fibers into a
muscle composed only of SO fibers.
Recently, this knowledge has been put
into practice. Attempts have been
made to convert muscles to serve a
desired function quite deliberately.
For example, the latissimus dorsi
muscle, a muscle that in humans is
rather fatigable, has been used as a
pump to assist the heart, the ultimate
fatigue-resistant muscle. In order to
succeed in this, considerable information on the properties of muscles and
their response to chronic stimulation
had to be available (reviewed by
Nemeth39 and Keme1146).Paradoxically, although muscles may readily
be rendered SO by chronic stimulation, the pattern needed to convert a
muscle to one with a predominance
of FG fibers is still not known, and
studies are in progress to find 0ne.46
It may be that genetic determination
plays a stronger role than has been
suspected and that SO fibers are too
stable to be converted completely.
ActMty and Adaptation In
Motor Unlts
Since the classic work of Buller et
al,47 it has been known that the speed,
strength, and fatigue resistance of
muscles and their motor units are not
fixed properties; rather, they depend
on the activity pattern the muscle
undergoes. Buller and co-workers cut
the nerves to the MG and soleus
muscles and switched them, so that
the MG muscle was reinnervated with
the soleus muscle nerve, and vice
versa. The muscles changed their
properties in the direction determined by their new innervation: The
soleus muscle became faster, and the
MG muscle became slower. Buller
and co-workers did not formulate the
hypothesis explicitly in terms of activity. They also considered the possibility that a trophic influence of the
nerve, rather than activity alone, might
influence muscle fiber type. It remained for Salmons and Vrbova,45
and later Lomo and co-workers,48 to
show that chronic stimulation of a
muscle nerve, or of the muscle itself,
alone would suffice to cause it to
adopt properties of speed and fatigue
resistance similar to those of the soleus muscle. As we have seen, however, the attempts to produce a conversion from slow to fast muscle fiber
types have met with far less success.
Kernel and co-workers were unable
to show a clear correlation between
activity patterns and motor unit
strength and speed in chronically
stimulated motor units; it proved to
be easy to slow a muscle down and
weaken it, whereas it was difficult or
impossible to speed up o r strengthen
the muscle. Their extensive efforts
have recently been reviewed by
Kerr~ell.~~
Activity is likely a factor that determines the strength, fatigability, and
speed of motor units. Thus, the observation that motor units are recruited
in order of increasing force production must be interpreted with care,
because it is possible that the recruitment order comes first and force
production adapts to it.
The fiber type composition of the
appropriate muscles in trained athletes appears to be adjusted to the
tasks they perform (see Tab. 9 in the
chapter by Saltin and Gollnickl4).
Thus, the lower-extremity muscles of
sprinters are composed predominantly of fast-twitch fibers, whereas
slow-twitch fibers predominate in
long-distance runners. Similarly, the
deltoid muscles of elite canoeists
contain a predominance of slowtwitch fibers. It may be argued that
these differences are genetic, and that
genetically endowed persons become
athletes and choose the appropriate
sport. Although there is a significant
element of truth in this possibility,
plasticity furthered by training can
also play a major role.
In humans, training can produce
changes in muscle strength, speed,
endurance, and fiber type composition. It is generally easier to change
the metabolic properties of a muscle
than its contractile properties.16J9 The
large body of literature on the effect
of training has been reviewed. Endurance training appears to readily produce changes in the oxidative capacity
of muscles. Thus, for example, the
oxidative capacity of type I fibers may
increase; in this respect, these fibers
become more like IIa fibers. The
contractile speeds need not change,
however, and the distinction between
I and IIa fibers may remain clear. This
adds to the difficulty, mentioned earlier, of reconciling the fiber type
classifications SO, FOG, and FG and I,
IIa, and IIb. Not only does this difficulty in reconciling fiber type classifications create difficulties between
animals and humans, it can create
ambiguities in distinguishing fiber
types between well-trained and sedentaly humans. Fiber type conversions,
such as those that occur during
chronic stimulation, have been shown
in longitudinal studies on the same
person. l6
The training required to produce
changes in fiber types may need to be
more rigorous and enduring than that
usually used if fiber changes from IIb
to IIa and from IIa to I are to be
produced to a large degree. Even
training of several hours a day is a far
lesser demand than chronic stimulation, which goes on around the clock.
Changes in fiber size and type can be
induced by certain hormones. Important among these are the thyroid
hormones and testosterone.l9 This is
the basis of doping to improve athletic performance.
Motor unit strength is not determined
solely by the strength of its muscle
fibers, but also by the number of
muscle fibers the nerve fiber innervates. It is unlikely that this factor
changes with activity, although it can
change with reinnervation.46 The
"innervation ratio" has been calculated in a number of motor units.
Usually, this ratio is determined by
the percentages of the different muscle fiber types in the muscle based on
histologcal data, the total number of
motoneurons innervating the muscle,
and the percentages of each motor
unit type.49 This indirect method
allowed Burke49 to calculate relative
innervation ratios for a variety of
muscles. The most extreme values
given are for the TA muscle, in which
FF motor units have 2.74 times as
many fibers per unit than do S motor
units. In a number of other muscles,
the difference between innervation
ratios of FF and S units is less than 2
to 1. These muscles include the MG
(1.2:I), flexor digitorum longus
(1.83:1), tibialis posterior (1.28:1),TA
(1.33:I), and peroneus longus
(1.21:l). If all muscle fibers had the
same strength, this should also be the
force difference between the FF and S
motor units. We have seen that this is
not so.
A third factor determining the
strength of a motor unit is the "specific tension" of its muscle fibers, the
force produced per cross-sectional
area by the fiber (for a discussion of
this issue, see Burke49). This is a controversial subject. If specific tension is
assumed to differ among motor unit
types, it can be argued whether specific tension changes with activity o r
with reinnervation of a muscle. Burke,
using indirect methods, calculated
that the specific force differed systematically with muscle fiber type. An
experiment to measure specific tension directly suggested that there is
no difference among muscle fiber
types?O which is supported by indirect measurements obtained by Stein
et al.5l This issue is by no means
settled, and may provide important
information on the causes of force
differences among the diverse motor
unit types seen normally, after reinnervation, o r when they have been
chronically stimulated.
It is interesting to note the extent of
recovely of a reinnervated muscle
and the degree to which the orderly
recruitment of motor units reestab-
physical Therapy/Volume 73, Number 12mecember 1993
1
disorderly recruitment order on the
ability to grade muscle force smoothly?" has not received critical attention.
When the issue is discussed, it is
addressed as I have done, by showing
that the cumulative force curve becomes less smooth. How important
this is for standing o r walking is not
known.
Rate Coding
Flgure 3. Graph of mean tetanic tension (abscissa) against mean twitch tension
(ordinate) for motor units listed in the Table.
lishes itself. This occurs when a muscle is denervated and reinnervated
with the same muscle nerve. Initially,
the normal relationships between
motoneuron size and motor unit
strength and speed are absent, but
they return with time.52 Because
nerve fibers d o not reinnervate their
original muscle fibers, a respecification must take place, as also occurs
with chronic stimulation.
Such a respecification occurs even in
the extreme case in which an extensor muscle group is reinnervated with
a nerve normally supplying a flexor
muscle.42 In this case, muscle force
returns to normal for that muscle,
exceeding that of the flexor muscles
by a factor of 2 to 3. Speed is comparable to that of the flexor muscles,
consistent with what has been discussed previously. The nature of the
variable that is respecified, however,
is controversial. As discussed previously, motor unit strength depends
on the number of muscle fibers innervated, their cross-sectional areas,
and the force per unit area (specific
tension) each fiber produces. The
results of Gordon et a142 suggested
that the specific tension was the major
variable that changed. Yet, it is not at
all clear that specific tension even
differs with fiber type, as the authors
point out.42 In fact, opposite views on
this issue are presented by Stein et
alsl and by Burke.*9
The adaptability of muscle and its
motor units has great relevance in
physical therapy. This adaptability
should form the basis for therapeutic
measures to restore muscle strength
after injury to the muscle o r its nerve;
inactivity produced by injury, casts, or
splints; o r central nervous system
disease o r lesions such as stroke. The
relevance may be extended to functional electrical stimulation (FES). If a
nerve is stimulated by implanted o r
percutaneous electrodes, increased
stimulus strength is likely to recruit
motor units roughly in the reverse of
the normal recruitment order.53 If the
electrode lies within the muscle, the
situation is harder to define. It is
likely that no consistent recruitment
order will be found (Stuart BinderMacleod, PhD, PT,and colleagues;
unpublished research). If FES is applied chronically, however, we may
speculate that the stimulated muscle
units may adapt to their imposed
activity patterns and change their
speed and strength characteristics.
What effect this may have on the
smoothness of induced movements is
not known; at present, FES is in such
an early stage of development that the
question is not yet of great importance. To my knowledge, the question
"What are the consequences of a
Physical. Therapy/Volume 73, Number 12December 1993
The force of a motor unit, o r of a
whole muscle, ranges from a minimum (ie, the twitch force) to a maximum (ie, the force produced by tetanic stimulation). This range may be
expressed as tetanic tension divided
by twitch tension, the tetanus:twitch
ratio. The reciprocal of this value, the
twitch:tetanus ratio, is frequently given
in the literature. Figure 3 shows the
twitch force plotted against tetanic
force for motor units of each type for
a variety of different muscles in the
cat. These muscles include the diaphragm, MG, TA, EDL, personeus
longus, abductor cruris caudalis, and
rectus lateralis (a muscle that moves
the eye). The slope of a straight line
through these points gives the twitch:
tetanus ratio. Figure 3 shows a
roughly linear relationship between
twitch and tetanic tension, and the
actual values show no consistent difference between motor unit types in
this regard. In part, this may be due
to the fact that twitch tension is a
notoriously variable quantity, because
it changes rapidly with repetitive
stimulation, showing potentiation and,
in FF units, the beginnings of fatigue.
Studies on potentiated motor units
show a lower tetanus:twitch ratio than
those on unpotentiated units, and it is
not always stated how the studies
were done.
The tetanus:twitch ratio is generally
said to range from about 2 to 15; the
data from which Figure 3 was made
suggest that 5 is a reasonable mean
value. Thus, rate coding, or varying
the frequency at which motor units
are driven, allows force to be varied
by a factor of 5. That is not very
much. Clearly, the additional feature
of recruitment of more motor units is
needed to provide the full range of
tensions needed for normal
movements.
Rate coding has the advantage over
recruitment that the force gradation is
smooth. Recruitment, on the other
hand, must occur in steps. The two
mechanisms likely occur together.
Although it was suggested many years
ago that rate coding is the predominant mechanism for varying muscle
force,54,55the situation is not quite so
simple. Kukulka and Clamann56 were
able to show that recruitment of new
motor units occurred throughout the
range of forces produced by the brachial biceps muscle in humans. In
contrast, they were unable to show
the recruitment of more motor units
in the adductor pollicis muscle after
that muscle produced about 50% of
its maximum force; the remainder of
the force had to be produced by rate
coding, that is, by increasing the frequency with which the already active
motor units were driven. This finding
was in agreement with the earlier
work of Milner-Brown et a1,54who
had also studied a muscle of the
hand. The relative importance of rate
coding and recruitment probably
depends on the muscle and its function, although this problem has not
been studied systematically,
Recruitment of Different
Motor Unlts
The greatest range of forces may be
produced by recruiting more motor
units. The weakest motor unit of a
typical skeletal muscle such as the cat
MG muscle may produce a force of
about 0.5 g,5 whereas the whole muscle produces a maximum tetanic force
of almost 13 kg.1° This is a range of
more than 20,000 to 1,which we can
compare with that possible with rate
coding, between 2 and 15 to 1. Zajac
and Fade115~ have shown that MG
muscle motor units are recruited in
order of increasing force, from the
least to the most powerful. Although
the mechanism that determines the
recruitment order is not yet understood, this finding is supported by
other studies.1°~58This orderly recruitment pattern has interesting consequences, for it leads to a convenient
means of regulating muscle force
referred to as "proportional control."
In proportional control, a variable
such as force is adjusted in steps that
are proportional to the force already
present. A weak force is graded by
changing it slightly (eg, by steps of
5%), and a stronger force is graded
using larger absolute increments, but
still by 5% of the force already present, This means of regulating muscle
force is accomplished by recruiting
motor units in order of increasing
strength.
The benefit of recruiting more motor
units from weak to strong was already
recognized by Henneman et a1.59
When total force output is weak, as it
is when few motor units are active,
force is increased by the recruitment
of additional weak motor units. The
steps in force produced by this recruitment pattern are small, and force
gradation is rather smooth. As force
increases, the motor units remaining
to be recruited are progressively
more powerful. In an ideal proportional control system, the force added
by the recruitment of each new motor
unit is a fixed percentage of the force
already present. If we plot force output against the number of active motor units, we obtain an exponential
curve. The force increase of muscles
resembles such a curve rather closely,
but not perfectly. As Henneman et a1
pointed out,
. . . this grading of output is reminiscent of the Weber fractions known in
the field of sensory discrimination. We
are not proposing a precise mathematical relationship for the motor system
comparable to Weber's rule of the just
noticeable difference of sensation, but
the analogy is clear: the smallest increment that can be added to the force
exened by a muscle becomes the
greater as the force of contraction
increases.59@57@
A brief digression may be appropriate
here. Further information on sensory
physiology may be found in physiology te~ts.l~3~*
Weber was a sensory
physiologist of the last century who
was interested in the accuracy of our
ability to "measure" sensations. His
first experiments involved the ability
of a subject to judge weights. The
same principle, however, applies to
the ability to judge the brightness of
light, the intensity of sound, the pressure on the skin, and, as discussed
earlier, the ability to adjust force output. Weber found that the ability to
sense differences in a stimulus depended on the strength of the stimulus. Thus, it was as easy to distinguish
a 1-g change in a 10-g weight as it
was to notice a 100-g change in a 1-kg
weight, a 10% change in each instance. The smallest such detectable
change (just noticeable difference)
could be expressed as a fraction, the
quotient of the change in stimulus
strength (As) divided by the stimulus
strength (s). This proved to be a constant (K) over a wide range of stimulus strengths, leading to Weber's law:
As/s=K. In this example, if the just
noticeable difference is actually lo%,
a 1-g change, o r even a 10-g change,
in a kilogram weight could not be
detected, although it is readily detected in a 10-g weight.
The perceived magnitude of a change
in the intensity of a stimulus (eg,
loudness of a sound, heaviness of a
weight) depends on the size of the
stimulus that is changed. The same
principle applies for changes in force
output. By recruiting weak motor
units to increase a weak force,
roughly the same percentage of
change is produced as when powerful
motor units are recruited to increase
a powerful force. This way of grading
force is practical: The recruitment of
one o r two weak quadriceps femoris
muscle motor units producing 50 mN
(5 g) of force will hardly affect the
accuracy (or anything else) of a basketball player's slam dunk. Large
forces are graded by the recruitment
of large motor units.
Motor units display a range of forces,
even in a muscle as homogeneous as
the soleus muscle (31-1,630 mN, o r
3.2-40.4 g, of force33. This may be
incorporated into a model of recruitment by assuming that the forces of
the population of motor units are
distributed according to Gaussian
statistics. The distribution within each
motor unit type is probably skewed,
Physical Therapy./Volume 73, Number 12December 1993
motor unit type (ie, the randomness
of a Gaussian distribution) produces a
smoothing of force gradation.
We can rescale the ordinate to a logarithmic scale, converting the exponential rise into a roughly linear rise. The
graph becomes approximately linear
for high force levels, but not for low
forces. This is consistent with recruitment curves for a variety of real muscles, such as MG,58 FCR,22 and human
thenar mu~cles.3~~35
0
20
40
80
80
Number of Motor Units
Figure 4. Cumulativeforce as a function of number of motor units recruited for
the soleus muscle, using two recruitment models. Upper curve produced with the assumption that motor units are recruited in random order; lower curve produced with
the assumption that motor units are recruited in order of increasing strength. Force is
scaled so that maximum force =1 and it is assumed that the muscle has 100 motor
units. Abscissa therefore represents percentage of motor units recruited.
with a preponderance of weaker
units, but, to my knowledge, data are
not available. If the motor units of
such a population are recruited at
random, force will increase in a more
or less straight line as a hnction of
the number of motor units recruited.58 Individual increments will be
large or small, so that the line will
have a lot of jumps or kinks, but, on
average, it will resemble a straight
line rather than a smooth curve. Figure 4 presents force against the number of active motor units for a model
soleus muscle. The maximum force
has been normalized to 1, and the
number of motor units has been
normalized to 100. The upper curve
shows the results of a random recruitment order.
If we rank order the population of
motor units according to increasing
force and recruit them in that rank
order, the force rises in a manner
more closely predicted by Weber's
law (Fig,.4, curved line). A system in
which force is graded in proportion
to the force already present is said to
be under proportional control. The
recruitment of motor units by their
size and their progressively increasing
strengths ensures proportional
control.
A far more interesting example is that
of a mixed muscle. I have chosen to
model two such muscles, the EDL and
the FCR. These muscles were chosen
because of their extremely different
distributions of motor unit types: The
EDL muscle has 6% type S motor
units and 48% type FF motor units,
whereas the FCR muscle has 40% type
S motor units and only 22% type FF
motor units.
Figure 5 shows the modeled recruitment curves for these two muscles
superimposed, as linear plots in the
upper panel and as semilogarithmic
plots in the lower panel. The linear
plots are smooth in shape, rising
slowly at first, then more and more
steeply, as would be expected from a
proportional control system. In addition, because the model allows considerable scatter in motor unit force,
as does an actual muscle, motor units
are not recruited according to type
when they are recruited in order of
increasing strengths57 Some type S
motor units are stronger than some
type FR motor units and are assumed
to be recruited later. Thus, the transition from one type of motor unit to
the next is smoothed. We have the
remarkable result that scatter in the
force output in the population of each
Physical Therapy/Volume 73, Number 12December 1993
A tangent to the curve on a linear
scale gives the force change produced
per motor unit recruited. As the curve
becomes progressively steeper, the
recruitment of a few additional units
produces a large change in force.
Figure 5 (top) shows that about 70%
of the motor units are required to
produce half of the EDL muscle's
maximum force, whereas about 75%
of the motor units are needed to
produce half of the FCR muscle's
force. Conversely, half of the motor
units of the FCR muscle, with its large
number of S motor units, produce
only 10% of its maximum force,
whereas half of the EDL muscle's
motor units produce about 25% of its
force.
A number of sophisticated models of
motor unit recruitment have been
proposed in which additional factors
such as rate coding for force modulation, the properties of reflex inputs,
and motoneuron properties are also
considered. The most detailed recruitment models are those of K e ~ n e l l ~ ~
and Heckrnan and Binder." Heckman
and Binder used tetanic force distributions for whole muscles obtained
from the literature without considering muscle unit types explicitly. This
was convenient, because their model
is of the cat MG muscle only. A major
addition to such models was the incorporation of rate coding. They thus
created a muscle model rather like
the biceps brachii muscle model
described by Kukulka and Clamann,56
in which recruitment and rate coding
occur throughout the muscle force
range. The intent of this model is to
create an input-output relationship for
a muscle, in which the input is the
840 / 21
same tendon. Long muscle fibers
forming relatively weak, fatigueresistant motor units make the soleus
muscle ideally designed to make
slow, finely graded movements and to
shorten over a considerable length.
The gastrocnemius muscle, with its
pennate fiber arrangement and powerful, fatigable motor units, is designed to do just the opposite: provide powerful, fast contractions with
less endurance, and over a shorter
range of lengths. Henneman and
Olson concluded that nature decided
that to move the ankle, two heads are
better than one.
0.00)01
I
0
10
40
60
80
100
Number of Motor Units
Flgure 5. Comparison of cumulatiue force curves of extensor digitorum longus
(EDL) and flexor carpi radialis (FCR) mmzrscles: (top) linear force scale; (bottom) logarithmic force scale. Maximum force and motor unit number are scaled as in Figure 4.
atferent drive to the motoneuron pool
and the output is the force. In principle, this model could be used to
examine the relationship for a reinnervated muscle and to determine
how smoothly force is graded.
As Henneman and Olson8 pointed out
Solely to obtain proportional force
gradation, it appears to be desirable
for a muscle to possess a population
of motor units with a range of forces.
Such an arrangement seems to be
superior to that of a muscle consisting
of a population of identical motor
long ago, one could expect muscles
serving very different functions to
develop different capabilities. They
then raised the more difficult issue of
two closely synergistic muscles, the
gastrocnemius and the soleus, which
perform the same function to extend
the foot, and even insert onto the
22 / 841
units. But why is it desirable to have
motor units of discretely different
capabilities (ie, motor units of different types)?
The problem becomes more difficult
in a single mixed muscle, because the
architecture of the individual motor
units is likely to be the same. Thus, all
motor units will be involved in a
pennate, o r perhaps fusifom, construction, and all motor units will be
forced to make contractions over the
same length and will usually work at
the same mechanical advantage (a
well-known exception is the cat sartorius muscle6l). Even in such a homogeneous environment, however, it is
difficult to envision a compromise
motor unit type that can perform all
functions reasonably well. Although
FR motor units may appear to offer
such a compromise, the Table shows
that they are less than half as strong
as FF units. This loss of strength could
be dearly bought in trylng to flee
from a predator. It is well known that
sprinters and marathon runners train
their motor units differently and are
unwilling to produce compromise
muscles by training.
Clearly, strength requires muscle
fibers filled with contractile structures,
leaving little room for the storage of
energy-rich molecules and mitochondria, the chemical factories that make
the energy available. Type FF muscle
fibers are designed this way, and their
large diameter and poor blood supply
make them well suited for powerful
contractions that fatigue rapidly. When
a muscle produces a powerful contraction, it generates considerable
internal pressure and cuts off its own
blood s ~ p p l y . ~ 6Hence,
~ 6 ~ powerful
muscle fibers cannot be resupplied
Physical TherapyIVolume 73, Number 12December 1993
,
with oxygen and nutrients and are
dependent on their own stores and
anaerobic metabolism. Type FF motor
units are ideally suited for this
function.
Oxidative motor units are weaker and
their muscle fibers are of smaller
diameter than are anaerobic (FG)
muscle fibers in most species (they
are more homogeneous in humans,
but still tend to be smallerl4; however, see Simoneau and Bouchardm);
much of their intracellular space is
devoted to the production of energy.
These motor units are also richly
supplied with capillaries. Because
these motor units are unlikely to cut
off their own blood supply with powerful contractions, they can receive
oxygen and nutrients and function for
long periods of time. The fibers of
these motor units are scattered
throughout a cross-section of the
muscle, and not arranged in clumps.
This construction prevents the generation of local muscle pressure, which
would tend to block blood flow.
Hence, the interdigitation of motor
units in a normal muscle and their
asynchronous discharge help support
the supply of oxygen and nutrients. It
is dficult to conceive of a compromise motor unit that would perform
the different functions of powerful
contractions on the one hand and
steady, sustained contractions on the
other equally well or even adequately.
Most muscle exertions, especially very
strong ones, tend to be phasic; running and even walking are good examples. For such rhythmic force output, blood flow is not occluded, or
occluded only briefly, and may even
be assisted, as venous return is facilitated by muscle activity. An additional
consideration is that the activities we
can perform for long periods of time,
such as walking, are probably performed by fatigue-resistant motor
units alone. Thus, for example, the
walking cat recruits 25% of its MG
muscle and even less of its lateral
gastrocnemius muscle when walking63
(Table), well within the range of
fatigue-resistant motor units.
It is clear that the knowledge of the
properties of muscles and their motor
units is applied in athletics and therapeutics, and forms a core of the
knowledge influencing such new
techniques as FES. As more knowledge of muscle function and muscle
organization emerges from basic
science and clinical laboratories, it
will have a profound influence on the
nature of the therapeutic process.
References
1 Gupon AC. Textbook ojMedical Physiology.
7th ed. Philadelphia, Pa: WB Saunders Co;
1986: chap 13.
2 Berne RM, Levy MN. Electrical activity of the
heart. In: Berne RM,Levy MN, eds. Physiology.
2nd ed. St Louis, Mo: CV Mosby Co; 1988: chap
27.
3 Milnor WR. Properties of cardiac tissue. In:
Mountcastle VB,ed. Medical Physiology. 14th
ed. St Louis, Mo: CV Mosby Co; 1980: chap 36.
4 Antoni H; Biederman-Thorson M, trans.
Function of the heart. In: Schmidt RF,Thews
G, eds. Human Pbysiology. 2nd ed. New York,
NY:Springer-Verlag New York Inc; 1989: chap
19.
5 Wuerker RB, McPhedran AM, Henneman E.
Properties of motor units in a heterogeneous
pale muscle (m. gastrocnemius) of the cat.
J Neurophysiol. 1965;28:85-99.
6 McPhedran AM, Wuerker RB, Henneman E.
Properties of motor units in a homogeneous
red muscle (soleus) of the cat. J Neurophysiol.
1965;28:71-84.
7 Henneman E, Mendell LM.Functional organization of motoneuron pool and its inputs.
In: Brooks VB, ed. Handbook ojPhysiology,
Volume 2: Motor Control. Bethesda, Md:
American Physiological Society; 1981: chap 11.
8 Henneman E, Olson CB. Relations between
structure and function in the design of skeletal
muscles. J Neurophysiol. 1965;28:581-598.
9 Edstrom L, Kugelberg E. Histochemical composition, distribution of fibres and fatigability
of single motor units: anterior tibia1 muscle of
the rat. J Neurol Neurosurg Psychiatry. 1968;
31:424-433.
10 Burke RE. Motor units: anatomy, physiology, and functional organization. In: Brooks
VB, ed. Handbook ojPhysiology, Volume 2 :
Motor Control. Bethesda, Md: American Physiological Society; 1981: chap 10.
11 McDonagh JC, Binder MD, Reinking RM,
Stuart DG. Tetrapartite classification of motor
units of cat tibialis posterior. J Neurophysiol.
1980;44:696-712.
12 Brooke MH, Kaiser KK. Three "myosin
adenosine triphosphatase" systems: the nature
of their pH lability and sulhydryl dependence.
J Hisrochem Cytochem. 1970;18:670-672.
13 Garnett RAE,O'Donovan MJ, Stephens JA,
Taylor A. Motor unit organization of human
medial gastrocnemius. J Physiol (Lond). 1978;
287:33-43.
14 Saltin B, Gollnick PD. Skeletal muscle
adaptability: significance for metabolism and
performance. In: Peachey LD, ed. Handbook o j
Physical Therapy/Volume 73, Number 12December 1993
Physiology. Bethesda, Md: American Physiological Society; 1983: chap 19.
15 Pette D, Vrbova G. Neural control of phenotypic expression in mammalian muscle fibers. Muscle Newe. 1985;8:676-689.
1 6 Howald H, Hoppeler H, Claassen H, et al.
Influences of endurance training on the ultrastructural composition of the different muscle
fiber types in humans. PJugers Arch. 1985;403:
369-376.
17 Brooke MH, Kaiser KK. The use and abuse
of muscle histochemistry. Ann NYAcad Sci.
1974;228:121-144.
18 Peter JB, Barnard RJ, Edgerton VR, et al.
Metabolic profiles of the three fiber types of
skeletal muscle in guinea pigs and rabbits.
Biochemistry. 1972;11:2627-2633.
1 9 Billeter R, Oetliker H, Hoppeler H. Structural basis of muscle performance. In: Jones
JH, ed. Comparative Vertebrate Exercise Pbysiology, Volume 37: Advances in Veterinary Science and Comparative Medicine. San Diego,
Calif: Academic Press Inc. In press.
20 Romanul FCA. Enzymes in muscle, I: histochemical studies of enzymes in individual
muscle fibers. Arch Neurol. 1964;11:355-368.
21 Lowry CV, Kimmey JS, Felder S, et al. Enzyme patterns in single human muscle fibers.
J Biol Chem. 1978;253:8269-8277.
22 Botterman BR, Iwamoto GA, Gonyea WJ.
Classification of motor units in flexor carpi
radialis.J Neuropbysiol. 1985;54:676-690.
23 Dum RP,Kennedy 'IT. Physiological and histochemical characteristics of motor units in cat
tibialis anterior and extensor digitorum longus
muscles.J NeumpLysioI. 1980;43:1615-1630.
24 Ariano Mq Armstrong RB, Edgerton VR
Hindlimb muscle fiber populations of five mammals.J Hisiochem Cytochem. 1973;21:51-55.
25 Davies AS, Gunn HM. Histochemical fibre
types in the mammalian diaphragm. JAnat.
1972;112:41-60.
26 Johnson MA, Polgar J, Weightman D, Appleton D. Data on the distribution of fibre types
in thirty-six human muscles: an autopsy study.
J Neurol Sci. 1973;18:111-129.
27 Goldberg SJ. Mechanical properties of extraocular motor units. In: Binder MD, Mendell
LM, eds. The Segmental Motor System. New
York, NY:Oxford University Press Inc; 1990:
chap 12.
28 Shall MS, Goldberg SJ. Extraocular motor
units: type classification and motoneuron stimulation frequency-muscle unit force relationships. Brain Res. 1992;587:291-300.
29 Kernell D, Eerbeek 0,Verhey BA. Motor
unit categorization on the basis of contractile
properties: an experimental analysis of the
composition of the cat's m. peroneus longus.
Exp Brain Res. 1983;50:211-219.
30 Buchthal F, Schmalbruch H. Contraction
times and fibre types in intact human muscle.
Acta Pbysiol Scand. 1970;79:435-452.
3 1 Sica REP, McComas AJ. Fast and slow twitch
units in a human muscle. J Neurol Neurosurg
Psychiatry. 1971;34:113-120.
32 Taylor A, Stephens J k Study of human motor
unit contractions by controlled intramuscular
microstimulation. Brain Res. 1976;117:331-335.
33 Milner-Brown HS, Stein RB, Yemm R. The
contractile properties of human motor units
during isometric voluntary contractions.
J Physiol (Lond). 1973;228:285-306.
34 Thomas CK, Bigland-Ritchie B, Westling G,
Johansson RS.A comparison of human thenar
es
bv intraneural
motor-unit ~ r o ~ e r t i studied
motor-axon stimulation and spike-triggered
averaging.J Neuroplysiol. 1990;64:1347-1351.
35 Westling G, Johansson RS,Thomas CK,
Bigland-Ritchie B. Measurement of contractile
and electrical properties of single human thenar motor units in response to intraneural
motor-axon stimulation. J Neurophysiol. 1990;
64:1331-1338.
36 Thomas CK, Johansson RS, Westling G,
Bigland-Ritchie B. Twitch properties of human
thenar motor units measured in response to
intraneural motor-axon stimulation. J Neurophysiol. 1990;64:1339-1346.
37 McDonagh JC, Binder MD, Reinking RM,
Stuart DG. A commentary on muscle unit
properties in cat hindlimb muscles. J Morphol.
1980;166:217-230.
3 8 George JC, Berger AJ. Avian Myology. New
York, NY: Academic Press Inc; 1966: chap 4.
39 Nemeth PM. Metabolic fiber types and influences on their transformation. In: Binder
MD, Mendell LM,eds. The Segmental Motor
System. New York, NY:Oxford University Press;
1990: chap 14.
40 Simoneau J 4 Bouchard C. Human variation in skeletal muscle fiber-type proportion
and enzyme activities. Am J Physiol. 1989;257:
E567-E572.
41 Hoh JFY. Myogenic regulation of mammalian skeletal muscle fibres. News in Physiological Sciences. 1991;6:1-6.
42 Gordon T, Thomas CK, Stein RB, Erdebil S.
Comparison of physiological and histochemical properties of motor units after crossreinnervation of antagonistic muscles in the
cat hindlimb. J Neurupbysiol. 1988;60:365-378.
43 Gunning P, Hardeman E. Multiple mechanisms regulate muscle fiber diversity. FASEBJ
1991;5:30643070.
44 Bouchard C, Simoneau J 4 Lortie G.. Genetic effects in human skeletal muscle fiber
. .
type distribution and enzyme activities. Can J
Physiol P h a m c o l . 1986;64:1245-1251.
45 Salmons S, Vrbova G. The influence of activity on some contractile characteristics of
mammalian fast and slow muscles. J Plysiol
(Lond). 1969;201:535-549.
46 Kernell D. Organized variability in the
neuromuscular system: a survey of task-related
adaptations. Arch Ital Biol. 1992;130:1946.
47 Buller AJ, Eccles JC, Eccles RM. Interactions
between motoneurones and muscles in respect of the characteristic speeds of their responses.J Physiol (Zond). 1960;150:417439.
48 Lamo T, Westgaard RH, Dahl HA. Contractile properties of muscle: control by pattern of
muscle activity in the rat. Proc R Soc Lond
[Biol]. 1974;187:99-103.
49 Burke RE. Motor unit types: some history
and unsettled issues. In: Binder MD, Mendell
LM,eds. The Segmental Motor System. New
York, NY: Oxford University Press Inc; 1990:
chap 11.
50 Lucas SM, Ruff RL, Binder MD. Specific tension measurements in single soleus and medial gastrocnemius muscle fibers of the cat.
Exp Neurol. 1987;95:142-154.
5 1 Stein RB, Gordon T, Totosy de Zepetnek J.
Mechanisms for respecifying muscle properties
following reinnervation. In: Binder MD, Mendell LM,eds. The Segmental Motor System.
New York, NY: Oxford University Press Inc;
1990: chap 15.
52 Gordon T, Stein RB. Reorganization of
motor-unit properties in reinnervated muscles
of the cat. J Neurophysiol. 1982;48:1175-1190.
53 Clamann HP, Gillies JD, Skinner RD,Henneman E. Quantitative measures of output of a
motoneuron pool during monosynaptic reflexes.JNeurophysiol. 1974:37:1328-1337.
54 Milner-Brown HS, Stein RB, Yemm R. The
orderly recruitment of human motor units
during voluntary isometric contractions.
J Plysiol (Lond). 1973228359-370.
55 Milner-Brown HS, Stein RB, Yemm R.
Changes in firing rate of human motor units
during linearly changing voluntary contractions. J Physiol (Lond). 1973;228:371-390.
56 Kukulka CG, Clamann HP. Comparison of
the recruitment and discharge properties of
motor units in human brachial biceps and adductor pollicis during isometric contractions.
Brain Res. 1981;219:45-55.
57 Zajac FE, Faden JS. Relationship among
recruitment order, axonal conduction velocity,
and muscle-unit properties of type-identified
motor units in cat plantaris muscle. J Neurophy~iol.1985;53:1303-1322,
5 8 Fleshman JW, Munson JB, Sypert GW,
Friedman WA. Rheobase, input resistance, and
motor-unit type in medial gastrocnemius motoneurons in the cat. J Neurophysiol. 1981;46:
1326-1338.
59 Henneman E, Somjen G, Carpenter DO.
Functional significance of cell size in spinal
motoneurons. J Neuropbysiol. 1965;28:560-580.
60 Heckman CJ, Binder MD. Computer simulation of the steady-state input-output function
of the cat medial gastrocnemius motoneuron
pool. J Neurophysiol. 1991;65:952-967.
6 1 Hoffer JA, Loeb GE, Sugano N, et al. Cat
hindlimb motoneurons during locomotion, 111:
functional segregation in sartorius. J Neurophysiol. 1987;57:554562.
62 Salmons S. Functional adaptation in skeletal muscle. In: Evans EV,Wise SP, Bousfield D,
eds. The Motor System in Neuroblology.
Amsterdam, the Netherlands: Elsevier Science
Publishers BV; 1985:23-29.
6 3 Loeb GE, He J, Levine WS. Spinal cord circuits: Are they mirrors of musculoskeletal mechanics?Journal of Motor Behavior. 1989;21:
473491.
64 Fournier M, Sieck C. Mechanical properties
of muscle units in the cat diaphragm. J Neuropbysiol. 1988;59:1055-1066.
Physical Therapy/Volume 73, Number 12December 1993
I
i
!
I
!
I
,
1