Human motor unit recordings: Origins and insight into the integrated motor system

Abstract

Soon after Edward Liddell [1895-1981] and Charles Sherrington [1857-1952] introduced the concept of a motor unit in 1925 and the necessary technology was developed, the recording of single motor unit activity became feasible in humans. It was quickly discovered by Edgar Adrian [1889-1977] and Detlev Bronk [1897-1975] that the force exerted by muscle during voluntary contractions was the result of the concurrent recruitment of motor units and modulation of the rate at which they discharged action potentials. Subsequent studies found that the relation between discharge frequency and motor unit force was characterized by a sigmoidal function. Based on observations on experimental animals, Elwood Henneman [1915-1996] proposed a "size principle" in 1957 and most studies in humans focussed on validating this concept during various types of muscle contractions. By the end of the 20th C, the experimental evidence indicated that the recruitment order of human motor units was determined primarily by motoneuron size and that the occasional changes in recruitment order were not an intended strategy of the central nervous system. Fundamental knowledge on the function of Sherrington's "common final pathway" was expanded with observations on motor unit rotation, minimal and maximal discharge rates, discharge variability, and self-sustained firing. Despite the great amount of work on characterizing motor unit activity during the first century of inquiry, however, many basic questions remain unanswered and these limit the extent to which findings on humans and experimental animals can be integrated and generalized to all movements.

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Review
Human motor unit recordings: Origins and insight into the
integrated motor system
☆
Jacques Duchateau
a,
⁎, Roger M. Enoka
b
a
Laboratory of Applied Biology, Université Libre de Bruxelles, 808 Route de Lennik, CP 640, 1070, Brussels, Belgium
b
Department of Integrative Physiology, University of Colorado, Boulder, CO 80309–0354, USA
ARTICLE INFO ABSTRACT
Article history:
Accepted 2 June 2011
Available online 13 June 2011
Soon after Edward Liddell [1895–1981] and Charles Sherrington [1857–1952] introduced the
concept of a motor unit in 1925 and the necessary technology was developed, the recording of
single motor unit activity became feasible in humans. It was quickly discovered by Edgar Adrian
[1889–1977] and Detlev Bronk [1897–1975] that the force exerted by muscle during voluntary
contractions was the result of the concurrent recruitment of motor units and modulation of the
rate at which they discharged action potentials. Subsequent studies found that the relation
between discharge frequency and motor unit force was characterized by a sigmoidal function.
Based on observations on experimental animals, Elwood Henneman [1915–1996] proposed a
“size principle”in 1957 and most studies in humans focussed on validating this concept during
various types of muscle contractions. By the end of the 20th C, the experimental evidence
indicated that the recruitment order of human motor units was determined primarily by
motoneuron size and that the occasional changes in recruitment order were not an intended
strategy of the central nervous system. Fundamental knowledge on the function of Sherrington's
“common final pathway”was expanded with observations on motor unit rotation, minimal and
maximal discharge rates, discharge variability, and self-sustained firing. Despite the great
amount of work on characterizing motor unit activity during the first century of inquiry,
however, many basic questions remain unanswered and these limit the extent to which findings
on humans and experimental animals can be integrated and generalized to all movements.
© 2011 Elsevier B.V. All rights reserved.
Keywords:
History
Electrophysiology
Motoneuron
Rate coding
Recruitment
Spinal cord
Contents
1. Introduction .......................................................... 43
2. Recording of single motor unit activity ........................................... 44
2.1. Concentric needle electrode ............................................. 44
BRAIN RESEARCH 1409 (2011) 42–61
☆
The research of the authors on motor units is currently supported, in part, by the Fonds National de la Recherche Scientifique of
Belgium and the Research Council of the Université Libre de Bruxelles (J.D.) and by the National Institute of Neurological Disorders and
Stroke (NS43275) and the National Institute on Aging (AG009000) (R.M.E.).
⁎Corresponding author at: Laboratory of Applied Biology, Faculty for Motor Sciences, Université Libre de Bruxelles, Campus Erasme, Route
de Lennik 808, CP 640, 1070 Bruxelles, Belgium. Fax: + 32 2 555 69 96.
E-mail address: jduchat@ulb.ac.be (J. Duchateau).
Abbreviations: AHP, afterhyperpolarization; AP, action potential; CNS, central nervous system; EMG, electromyogram; MVC, maximal
voluntary contraction
0006-8993/$ –see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.brainres.2011.06.011
available at www.sciencedirect.com
www.elsevier.com/locate/brainres

Author's personal copy
2.2. Fine wire electrode ................................................... 45
3. Motor unit recruitment .................................................... 46
3.1. Orderly recruitment and the size principle...................................... 46
3.2. Recruitment threshold ................................................. 48
3.3. Anisometric contractions ............................................... 49
3.4. Changes in recruitment order during voluntary contractions ........................... 50
3.5. Motor unit types .................................................... 52
3.6. Motor unit rotation .................................................. 52
4. Rate coding of motor unit discharge ............................................. 52
4.1. Minimal discharge rate ................................................ 53
4.2. Maximal discharge rate ................................................ 53
4.3. Rate coding and muscle force ............................................. 55
4.4. Discharge variability .................................................. 55
4.5. Tonic and phasic motor units ............................................. 56
5. Concluding thoughts ..................................................... 57
Acknowledgments ......................................................... 57
References .............................................................. 57
1. Introduction
It appears from the literature that the concept of a motor unit
was implicitly deduced in the early experiments of Keith Lucas
[1879–1916]
1
in Cambridge when he noted that increasing the
intensity of a stimulus applied to a muscle nerve of an
experimental animal caused stepwise increases in muscle
twitch contractions (Lucas, 1905, 1909). Further evidence came
from the observations of Georges Mines [1886–1914]
2
that
these steps were much larger than those produced by
stimulating the same muscle directly after application of
curare (Mines, 1913). From these results, Mines concluded
that: “There can be little doubt that each step is the result of
the excitation of a fresh nerve fibre or of nerve fibres, thus
bringing a new group of muscle fibres into play.”However, the
term “motor unit”was first introduced by Edward Liddell
[1895–1981]
3
and Charles Sherrington [1857–1952]
4
as a result of
studies on the mechanisms of reflex inhibition in the decerebrate
cat. They defined a motor unit as the “motoneurone axon and its
adjunct muscle fibres”(Liddell and Sherrington, 1925). As he
recognized that action potentials (APs) are generated in the axon
hillock of the motoneuron, Sherrington (1925) subsequently
extended the definition to include “The muscles fibres innervated
by the unit and the whole axon of the motoneuron from its hillock
ontheperikaryondowntoitsterminalsinthemuscle.”In modern
usage, a motor unit comprises the entire motoneuron, including
its dendrites and axon, and the muscle fibers innervated by the
1
Lucas was a British scientist who worked at Trinity College,
Cambridge. He was a pioneer in physiology, with significant
contributions on the mechanisms of cell excitation and the
transmission of impulses along motor nerves. His contributions
included showing that the response of a muscle or nerve fiber to
an electrical stimulus was an “all-or-none”response. He trained
the 1932 Nobel Laureate Adrian. Lucas died at a young age
(37 years) in an aircraft accident during WWI when he was
developing navigational aids for the Royal Aircraft Establishment.
More details on his contributions can be found in an article
written by Alexander Forbes [1882–1965] in 1916.
2
After completing a fellowship to Sydney Sussex College in
Cambridge, Mines rose rapidly through the academic ranks. His
appointments included a lectureship at the University of London in
1912, directorship of physiology at the Balfour Laboratory of Girton
College at Cambridge in 1913, and a professorship at McGill
University in Montreal in 1914. George Mines died in his laboratory
in Montreal at the age of 29 years, apparently performing
cardiology experiments on himself. More information on Mines
can be found at: http://factoidz.com/george-ralph-mines-
cardiologys-forgotten-genius.
3
Liddell entered Trinity College in Oxford to read medicine in
1914. He completed a first-class degree in physiology in 1918 and
three years later accepted a research fellowship at Trinity that
included an assistantship with Sherrington. As Sherrington was
president of the Royal Society of London (1920–1925) at that time,
Liddell was largely responsible for the experiments. Although
Liddell's contributions to the experimental work were clearly
recognized (see the preface of the monograph “Reflex Activity of
the Spinal Cord”by Richard Creed [1898–1984] et al., 1932), they
were somewhat overshadowed by Sherrington. After 1930, his
experiments focused on the control of postural reflexes by
descending inputs from different areas of the brain. He became
Wainflete professor of physiology at Oxford University in 1940.
4
Sherrington was trained as a physician in Cambridge and at St.
Thomas's Hospital in London (1878). After a brief stay at Edinburgh, he
returned to Cambridge in 1879 to study physiology with John Langley
[1852–1925]. He was appointed as professor of physiology at the
University of Liverpool in 1895 and remained there until 1913, when he
finally achieved his goal of being selected as the Chair of physiology at
Oxford University. During his earlier years in Cambridge, Sherrington
studied the function of the spinal cord. Later, he investigated spinal
reflexes and the efferent nerve supply of muscles. Subsequently, he
studied the distribution of the segmented skin field, the innervation of
antagonistic muscles, and the connection between the brain and the
spine. In 1932 he shared the Nobel Prize in Physiology or Medicine with
Adrian. Sherrington trained many prominent physiologists, including:
Wilder Penfield [1891–1976], John Fulton [1899–1960], Denny-Brown,
Liddell, Eccles, William Gibson [1913–2009], Granit, and David Lloyd
[1911–1985]. More details on Sherrington's contributions can be found
in the biography written by Liddell (1952).
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axon. Identification of the motor unit was a major discovery in our
understanding of how the central nervous system (CNS)
controls motor output (see Clarac and Barbara, 2011; Stuart and
Brownstone, 2011).
The current review provides a historical perspective on the
contribution of human experiments to our understanding of the
output transmitted by Sherrington's “final common pathway”
5
and its role in the control of movement. The key topics addressed
in this review include the development of techniques to record
motor unit activity in humans, the recruitment of motor units
during voluntary contractions, and the timing characteristics of
the APs discharged by motor units during voluntary contractions.
In keeping with the historical emphasis in this series of
articles, the life spans and a brief footnote bio-sketch appear
below for those who made a significant contribution to motor
unit physiology, either directly or indirectly. Note also that this
review is preceded by a preface (Stuart et al., 2011), two historical
articles on the origin of our understanding of the link between
nervecellsandmusclefibers(Barbara and Clarac, 2011; Clarac
and Barbara, 2011) and two subsequent articles on the properties
of the motoneuron component of motor units (Brownstone and
Stuart, 2011; Stuart and Brownstone, 2011).
2. Recording of single motor unit activity
Although the techniques used to record and analyze motor
unit activity in humans continue to evolve, this section
focuses on the pioneering work that contributed to the
foundation of our knowledge on the function of the final
common pathway in humans.
2.1. Concentric needle electrode
Hans Piper [1877–1915]
6
is usually considered the first to have
recorded the surface electromyogram (EMG) during a voluntary
contraction, which he accomplished with a string galvanometer
(1912). He found distinctive rhythms in the signal for each
muscle, which he interpreted as the rate of stimuli received
from the CNS. In 1921, Herbert Gasser [1888–1963]
7
and Harry
Newcomer [1887–1988] reported that the EMG was a reasonable
copy of the multi-unit recording obtained from the nerve
innervating a muscle (electroneurogram). In the 1920s, Kurt
Wachholder [1893–1961]
8
seems to have been the first to publish
data on motor unit discharge during voluntary contractions by
humans (see Wiesedanger, 1997). This work, which was
synthesized in a monograph written in German (Wachholder,
1928), involved recording a “single action current”with two
intramuscular fine needle electrodes and the signal being
amplified with a string galvanometer. This work did not receive
the recognition it deserved, perhaps due to the lack of
information on the recording technique.
Consequently, Edgar Adrian [1889–1977]
9
from Cambridge and
Detlev Bronk [1879–1975]
10
are usually credited with being the first
to record unitary recordings of single motor units in humans
(Adrian and Bronk, 1929). They recorded activity in the triceps
brachii muscle with an intramuscular electrode, which they
called a concentric needle electrode. The electrode consisted of
an insulated copper wire inserted in the lumen of a hypodermic
needle and held in position by a plug. The tip of the wire was
bared and acted as one electrode and the barrel of the needle
provided the other electrode. With the introduction of the
loudspeaker, the sounds of the recording were added to the
technique, which Adrian and Bronk found tobe useful to follow
slight differences in intensity and quality of the activity. An
5
See Burke (1985) for a more recent view on the integration of
sensory input and descending commands by segmental interneur-
ons and their role in the motor output discharged by the spinal cord.
6
Piper was a German physiologist who was head of the depart-
ment for physics at the Institute of Physiology in Berlin. After initial
works on embryology, he became interested in physiology and
studied the function of muscles and nerves. His name is associated
with the rhythmical grouping of motor unit potentials during steady
contractions of human muscles (so-called Piper Rhythm).
7
Gasser studied physiology, medicine, and pharmacology at the
University of Wisconsin. He spent two years (1923–1925) in Europe
studying with Archibald (“A.V.”) Hill [1886–1977], Walther Straub
[1874–1944], Louis Edouard Lapicque [1866–1952], and Henri Dale
[1875–1968]. In 1931 he was appointed professor of physiology and
head of the Medical Department at Cornell University (New York
City) and four years later became Director of the Rockfeller Institute
for Medical Research and remained there until his retirement in
1953. His major contribution to neurophysiology involved a produc-
tive collaboration with Joseph Erlanger [1874–1965] in which they
investigated the electrophysiology of nerves.He and Erlanger shared
the Nobel Prize in Physiology or Medicine in 1944. A more complete
biographical memoir was written by Adrian (1964).
8
As a professor of physiology at the University of Breslau in
Germany, Wachholder made major contributions to the field of
human motor control with his work on surface EMG activity and
the description of the three-burst EMG pattern during ballistic
actions. He seems also to have been the first, in 1928, to record
EMG activity with intramuscular needle electrodes. He showed
that “single action currents”(he seemed to ignore the concept of
motor unit introduced by Liddell and Sherrington in 1925) varied
between 5 and 75 Hz, which contrasted with the work of Piper
(1912) on the rhythmicity of “action currents”at a fixed frequency
of 50 Hz. Unfortunately, his work with Hans Altenburger (11
papers published in Pflügers Archivs within 4 years) was written
in German and did not receive the recognition it deserved. More
information on his contributions can be found in reviews
published by Wiesedanger (1997) and Sternad (2001).
9
After studying physiology at Cambridge University, Adrian
worked with Lucas on the impulses transmitted by motor nerves.
Subsequently, he studied medicine in London and after WWI he
inherited Lucas' laboratory. He contributed to the improvement of
electrodes, amplifiers (thermionic valves), and recording systems,
which enabled him to record electrical discharges in single nerve
and muscle fibers of animals and groups of muscle fibers in
humans during voluntary contractions. Together with Sherring-
ton, Adrian was awarded the Nobel Prize in Physiology or
Medicine in 1932 for his work on the function of neurons. Alan
Hodgkin [1914–1998] wrote a more complete biography on Adrian
in 1979.
10
Bronk completed a PhD in physics and physiology from the
University of Pennsylvania in 1926. Two years later, he spent one
year as a post-doctoral fellow in the Cambridge laboratory of
Adrian, with whom he published two seminal papers. He
contributed significantly to the development of the concentric-
needle electrode (known as Bronk's electrode in clinical electro-
myography), which was acknowledged by Adrian. After his stay in
England, he was first appointed as professor of medical physics at
the University of Pennsylvania from 1929 to 1940 and then as
professor of physiology and biophysics at Cornell Medical School
(1940–1949). More information on Bronk can be found at: www.
nap.edu/html/biomems/dbronk.
44 BRAIN RESEARCH 1409 (2011) 42–61

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early feature of this work was the “all-or-none”impulses and
the “frequency code”as the mode of signaling in the peripheral
nervous system. Adrian and Bronk (1929) concluded that “… the
gradation in force is brought about by changes in the discharge
frequency in each fibre and also by changes in the number of
fibres in action.”(Fig. 1). This conclusion on the underlying
mechanisms for force gradation extended their findings on
singlefibers of the rabbit phrenicnerve (Adrian and Bronk,1928).
Progressive developments by several investigators improved
the signal-to-noise ratio and the selectivity of the electrode at
higher forces. One major change was to insert two or more
insulated fine wires (~0.1 mm) into the lumen of the needle to
improve the selectivity of the recordings (bipolar electrode;
Bigland and Lippold, 1954; Donald Lindsley [1907–2003], 1935;
Forbes Norris [1928–1983] and Edgar Gasteiger [1886–1967],
1955). Despite these improvements in the concentric needle
electrode and its widespread use in neurology, a limitation of
the technique is the variability in the recordings due to small
movements of the electrode with increases in muscle force.
2.2. Fine wire electrode
Although Brenda Bigland
11
and Lippoldused a wire electrode in
1954, the next major improvement in the recording of single
motor unit activity came from the introduction of the fine-wire
electrode by John Basmajian [1921–2008]
12
(Basmajian and
Stecko, 1962). The electrode was made from a pair of nylon-
insulated, Karma alloy wires (25 μm in diameter) and inserted
into the muscle with a hypodermic needle. As the ends of the
wires inserted into the muscle werebent to resemble a hook, the
wires remained in the muscle when the needle was slowly
withdrawn. The flexibility of the wires minimized pain and
displacement of the electrodes during muscle contractions.
Furthermore, the electrode was able to detect APs from single
motor units and the signals from different motor units could be
recognized on the basis of differences in size and shape.
One limitation of fine wire electrodes is that once the needle
is withdrawn the only way to change its location is to pull the
wires progressively towardthe skin. Furthermore,the small size
of the detection site means that even small movements of the
electrode relative to the muscle fibers will change the shape of
the AP and hinder its detection. To overcome these problems,
Alexander Gydikov [1929–1989]
13
and colleagues introduced a
variant of the wire electrode in 1986,whichisknownasthe
subcutaneous branched-wire electrode. The electrode com-
prises two insulated wires that are glued together with three
~1 mm regions of the insulation removed; two regions ~1 mm
on one wire, separated by 3 mm, and a single exposed ~1 mm
region on the other wire positioned in between the two regions
of the other wire. The sites where the insulation is removed
form the detection areas,which means that one wire represents
the conventional pole and the other one corresponds to the
branched pole. The electrode is inserted subcutaneously and
transversely across the muscle with a hypodermic needle that
exits the skin after a few centimeters. The needle is then
withdrawn and both ends of the electrode are external to the
subject with the detection areas remaining over the belly of the
muscle. With this arrangement, it is possible to move the wires
to improve motor unit detection. Although the stability of the
recording is maximized by the subcutaneous location of the
electrode, especially during movements, a limitation of the
technique is that it can only detect superficial motor units
(Enoka et al., 1988, 1989; Gydikov et al., 1986).
All of the early work on human motor unit activity during
voluntary contractions was based on recordings obtained with
Fig. 1 –Fig. 14 in Adrian and Bronk (1929). The original figure
legend read “Action currents in human triceps (E.D.A.)
recorded with concentric needle electrodes during gradually
increasing voluntary contraction. A, beginning of contraction;
B, follows on A;C, powerful contraction.”Reprinted with
permission of the publisher (Wiley-Blackwell).
11
Bigland began her scientific career at the University College
London by working with Hill and Olof Lippold. She married
Murdoch Ritchie [1925–2008], an American biophysicist, in the
early 1950s and her subsequent publications appeared, therefore,
under the name of Bigland-Ritchie. Her contributions to the field
of muscle fatigue were honored at an international symposium
held in Miami, FL (November 10–13, 1994) and summarized in a
subsequent book (Gandevia et al., 1995).
12
Basmajian completed a medical degree at the University of
Toronto in 1945 and became known for his work in rehabilitation
science, especially in the areas of electromyography and biofeed-
back. He was a pioneer in the use of fine-wire electrode to study
single motor unit activity during voluntary contractions in
humans. His book, entitled “Muscles Alive”and first published
in 1975 by Williams and Wilkins, achieved international recogni-
tion and influenced many scientists and clinicians in the field of
electromyography. He trained Carlo De Luca, who helped him
write the 4th edition of the book. The tribute to Basmajian written
by Steven Wolf can be found at (www.aapb.org/tl_files/AAPB/files/
BasmajianTribute.pdf).
13
After graduating from the Higher Medical Institute of Sofia in
1953, Gydikov completed a PhD degree in 1959 (Candidate of
Medical Sciences) and a Doctor of Sciences in 1966 (Medicine). He
joined the Bulgarian Academy of Sciences in 1964 as the Head of
the Laboratory of Biophysics at the Institute of Physiology and the
Bionics Section at the Institute of Engineering Cybernetics. He
was Director of the Central Laboratory of Biophysics from 1982
until his death in 1989. In the early 1970s, he focused on single
motor unit APs and his group developed several new methods
and electrodes (surface multi-electrode and subcutaneous
branched electrode) to measure motor unit activity. His efforts
to facilitate interactions between scientists from the former
Soviet block and Western countries led to regular international
symposia on Motor Control that began in 1969. His associates and
students include Plamen Gatev, Lubomir Gerilovsky, Dimitar
Kosarov [1928–2010], Andon Kossev, and Nicolina Radicheva.
(This information was kindly provided by Tanya Ivanova).
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various versions of the concentric needle electrode and the
fine wire electrode.
3. Motor unit recruitment
A considerable amount of work during the 20th C focused on
identifying the rules that governed the activation of motor
units during voluntary contractions. The major issues includ-
ed the recruitment order of motor units in a muscle, the
factors that influence the recruitment threshold force and
recruitment order, the relative contribution of motor unit
recruitment to muscle force, and the duration that motor units
can discharge APs continuously.
3.1. Orderly recruitment and the size principle
A major question in the first half of last century was whether
the order of recruitment was highly stereotyped or whether it
varied as a function of the task. After the initial observation of
Adrian and Bronk (1929) that increases in force were achieved
by the recruitment of additional motor units and an increase
in discharge rate, Derek Denny-Brown [1901–1981]
14
and
Joseph Pennybacker [1907–1982] reported in 1938 that “… a
particular voluntary movement appears to begin always with
discharge of the same motor unit…More intense contraction is
secured by the addition of more units …” The fixed order of
motor unit recruitment was called “orderly recruitment”.
These observations were met with skepticism, however, as
the small APs detected during the initial part of a contraction
in which muscle force was increased gradually were consid-
ered to represent the activity of distant muscles fibers and,
conversely, the later recorded larger potentials were attributed
to nearby muscle fibers by Fritz Buchthal [1907–2003]
15
et al.
(1954; see also Calancie and Bawa, 1990).
`In 1957, Elwood Henneman [1915–1996]
16
published a brief
paper demonstrating that single motor axons in a ventral root
filamentwere recruited in order of AP amplitude as the intensity
of electrical stimulation to the sciatic nerve was increased.
Furthermore, the individual axons stopped discharging APs in
the reverse order in which they were recruited as the stimulus
intensity was decreased. This finding, which was based on
extracellular recordings in which axon size is proportional to
spike height, was generalized to infer that the susceptibility to
discharge is determined by motoneuron size, which had
previously been shown to be proportional to axon size by Gasser
in, 1941. The observation was generalized to all neurons and it
was hypothesized that the susceptibility of neurons to discharge
varied as a function of their size. In 1965, Henneman and
colleagues published seminal papers in the Journal of Neuro-
physiology that provided a detailed account of motor unit
properties, motoneuron recruitment properties, and how the
relations between these two sets of properties could be
summarized in terms of a unifying principle that they called
the “size principle”. The concept was later formalized by
Henneman (1977) as: “The amount of excitatory input required
to discharge a motoneuron, the energy it transmits as impulses,
the number of fibres it supplies, the contractile properties of the
motor unit it innervates, its mean rate of firing and even its rate
of protein synthesis are all closely correlated with its size. This
set of experimental facts and interrelations has been called the
‘size principle’.”
There was much interest in evaluating the size principle in
humans. Indirect evidence for the orderly recruitment of
motor units during graded voluntary contractions was sug-
gested on the basis of the size of the APs recorded by
intramuscular needle electrodes (Kugelberg [1913–1983]
17
and
Carl-Rudolf Skoglund [1910–1989], 1946; Camilla Olson [1888–
1974] et al., 1968; Tanji and Kato, 1973a). However, variations in
14
Denny-Brown was born in New Zealand and after studying
medicine received a fellowship to Sherrington's Oxford laboratory
where he investigated motoneuron physiology. His initial con-
tributions included the validation of Sherrington's concept of the
motor unit and development of the antidromic stimulation
technique to study motoneuron responses. He worked at several
different locations (Oxford and London, GBR and Boston, USA)
and made major contributions to the field of neurology, such as
the development of electromyography, physiology of micturition,
and many neurological diseases. After he became established at
Harvard Medical School in 1950, he trained many influential
neurology professors. A more complete biography can be found
at: http://users.ipfw.edu/vilensk/dbwebintro.htm and in a book
written by Langworthy (1970).
15
Buchthal was a German-born scientist who studied anatomy,
physiology, and genetics at Stanford University in California. He
subsequently returned to Germany and completed a medical
degree from the Humboldt University (Berlin) in 1931. The
following year he was appointed as an instructor at the Institute
of Physiology of Berlin University, but then moved to Denmark
and became the first Director of the Institute of Neurophysiology
at Copenhagen University (1952). He is usually recognized as the
founder of clinical neurophysiology. He studied motor units in
both healthy subjects and patients with various neuromuscular
diseases, using novel recording devices such as multiwire needle
electrodes. His career is described in an obituary written by
Steven Horowitz and Christian Krarup (2004).
16
After graduating from Harvard College (1937), Henneman
completed a medical degree from McGill University, Canada
(1943). Subsequently, he performed an internship at the Royal
Victoria Hospital and Montreal Neurological Institute, where he
trained in neurosurgery under the supervision of Penfield and
William Cone [1897–1959]. After two years as a neurosurgeon in
the US Naval Medical Corps, he studied the somatic afferent
system in cats and monkeys at John Hopkins, interacted with
Warren McCulloch [1898–1969] in Chicago and Gasser and Lloyd
in New York, and then was appointed professor in 1969 and chair
of physiology (1971–1984) at Harvard Medical School. Henneman's
research on the function of sensory neurons and motoneurons
led him to formulate the “size principle”and a collaboration with
Lorne Mendell resulted in the development of the spike-triggered
averaging technique. A biography on Henneman was written by
Robert Young (1997) and a book edited by Marc Binder and Lorne
Mendell (1990) summarized his influence on the field.
17
Kugelberg received a medical education at the Karolinska
Institute in Stockholm (Sweden). He subsequently trained in
Granit's laboratory with Skoglund. He was the first professor in
clinical neurophysiology at the Karolinska Institute and served as
chair from 1948 until 1954, when he was appointed chair of the
Department of Neurology. His scientific interests spanned a broad
spectrum to include electromyography, reflex physiology, motor
unit physiology, and histochemistry. He supervised the training
of many Swedish basic and clinical neuroscientists. More
information on Kugelberg is available in an obituary written by
Lars Edström and Lennart Grimby (1985).
46 BRAIN RESEARCH 1409 (2011) 42–61

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the order of recruitment were also observed. In agreement
with the results of Virginia Harrison [1907–2003] and Otto
Mortensen [1902–1979] (1962), for example, Basmajian (1963,
1967) asserted that under certain conditions it was possible for
humans to use visual and audio feedback of motor unit
discharge to vary the recruitment order of motor units with
different recruitment thresholds. He reported that a trained
subject was able to “…recall into activity different single motor
units by an effort of will while inhibiting the activity of
neighbours”.Henneman et al. (1976) countered that their
published records did not provide clear support for this
conclusion. Nonetheless, both Ashworth et al. (1967) and
Grimby and Hannerz (1968, 1970) concurred with Basmajian
when they observed occasional reversals of recruitment order
during slow contractions. When subjects performed ramp-
and-hold contractions, for example, Grimby and Hannerz
(1968) reported that the first unit to discharge APs could
become silent as the second recruited unit continued to
discharge; they described this pattern of activity as motor
unit “rotation”.Grimby and Hannerz (1968) also reported that
the recruitment order of motor units with similar thresholds
could be modulated by proprioceptive afferents during both
voluntary and reflex activities. A few years later, they even
asserted “…normal man can select in advance the recruitment
order of motor units most appropriate for the work intended”
(Hannerz and Grimby, 1973).
The first convincing evidence that the size principle
governed the recruitment order of human motor units can
be credited to Stein and colleagues (Milner-Brown et al.,
1973b). They developed a technique to measure the contractile
properties of single motor units in the first dorsal interosseus
muscle of the hand during voluntary isometric contractions
(Fig. 2A; Stein
18
et al., 1972; Milner-Brown et al., 1973a). This
technique involved extracting the mechanical contribution of
an identified single motor unit to the force exerted by the
whole muscle with the spike-triggered averaging method
(Mendell and Henneman, 1971). The data allowed Stein and
colleagues to compare motor unit force and contraction time
with the recruitment threshold force during a slowly increas-
ing isometric contraction (ramp contraction). After a method-
ological paper on the new technique (Stein et al., 1972), they
identified the human motor unit characteristics that varied
systematically with the threshold force for voluntary activa-
tion (Milner-Brown et al., 1973b). Based on a strong linear
correlation coefficient (>0.8) between the force of a motor unit
and its recruitment threshold, they concluded that human
motor units were recruited during ramp contractions in an
orderly sequence that depended on motor unit force (Fig. 2B).
They further noted that high-threshold motor units had faster
contraction times than low-threshold units. These results
were consistent with the size principle of Henneman et al.
(1965a, 1965b).
A number of different indexes of motor unit size (e.g.,
twitch amplitude, motor axon or muscle fiber conduction
velocity, amplitude of the evoked EMG waveform measured
with intramuscular electrode) have confirmed the orderly
recruitment of motor units during slow isometric contractions
in a wide variety of human muscles (see Calancie and Bawa,
1990; Stuart and Enoka, 1990).
AB
Fig. 2 –The spike-triggered averaging technique for studying single motor units in humans. (A) The experimental arrangement
developed by Stein et al. (1972) using the spike-triggered averaging method to extract the force developed by single motor units
in the first dorsal interosseus during a sustained voluntary contraction. The isolated action potential of the motor unit is used to
trigger an averaging device that samples the muscle force. By accumulating many triggered events, the mechanical contribution
of the unit can be extracted from the contribution of all other units. Adapted from McComas (1977). (B) Relation between the
spike-triggered average force and recruitment threshold force for motor units in first dorsal interosseus during a slow ramp
contraction.
From Milner-Brown et al. (1973b) with permission of the publisher (Wiley-Blackwell).
18
A tribute to the research career of Richard Stein was written by
Stuart (2004).
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3.2. Recruitment threshold
As observed by Adrian and Bronk (1929), the force that a
muscle can exert depends on the number of motor units that
are activated (recruitment) and the rate at which the
motoneurons discharge APs (rate coding). Although the two
mechanisms contribute to the force exerted by a muscle over
much of its operating range (Bigland and Lippold, 1954;
Gydikov and Kosarov, 1974; Milner-Brown et al., 1973b,
1973c; Monster and Chan, 1977; Person and Kudina, 1972;
Hendrik Seyffarth [1907–1985]
19
,1940), the relative contribu-
tions change with the force and speed of the muscle
contraction.
The force at which the largest motor unit in a muscle is
recruited during a voluntary contraction corresponds to the
upper limit of motor unit recruitment, beyond which only rate
coding contributes to increments in force. The upper limit of
recruitment seems to vary between muscles (Kukulka and
Clamann, 1981): most motor units in adductor pollicis were
recruited at forces less than 30% MVC (maximal voluntary
contraction) and none were recruited at forces greater than
50% MVC (Duchateau and Hainaut, 1981; Kukulka and
Clamann, 1981), whereas motor units in biceps brachii were
recruited up to 88% MVC force (Kukulka and Clamann, 1981).
At about the same time, De Luca et al. (1982a, 1982b) also
reported that intrinsic hand muscles (first dorsal interosseus)
have a lower recruitment range compared with limb muscles
(deltoid).
As established by Stein and colleagues (see Milner-Brown
et al., 1973a), the spike-triggered average forces of the motor
units belonging to the first dorsal interosseus muscle exhibit
an exponential distribution, which led them to conclude “… if
the additional number of motor units recruited declines
exponentially as the level of a voluntary contraction is
increased, while the force of the extra unit units recruited
increases linearly, then recruitment will account for less and
less of the increases in force at high force levels.”Subsequent
experiments using intraneural stimulation of motor axons
have confirmed the exponential distribution for motor unit
forces (Thomas et al., 1990) and the interpretation of Milner-
Brown et al. (1973a). These findings indicate that motor unit
pools comprise many low-threshold motor units and fewer
high-threshold motor units (Thomas et al., 1986; Van Cutsem
et al., 1997), which suggests that the control of force during
slow, low-force contractions relies mainly on the recruitment
of motor units (Enoka, 1995; Fuglevand et al., 1993; Heckman
and Binder, 1991).
The relative contribution of motor unit recruitment to
muscle force changes with contraction speed; the absolute
force at which a motor unit is recruited decreases with an
increase in contraction speed (Fig. 3;Büdingen and Freund,
1976; Freund et al., 1975; Tanji and Kato, 1973a; Seyffarth,
1940). The seminal study published by Jean-Edouard (John)
Desmedt [1926–2009]
20
and Godaux in 1977a, 1977b, recorded
the spike-triggered average force (Stein et al., 1972) of motor
units in the human tibialis anterior when subjects performed
“ballistic”contractions, which correspond to strong, rapid
contractions that are followed immediately by relaxation
(Richer, 1895). They demonstrated that motor units are
activated earlier during ballistic contractions (Fig. 3) and
approximately three times as many motor units are recruited
to produce a given peak force during ballistic contractions
compared with slow ramp contractions (Desmedt and Godaux,
1977a, 1977b). These results suggested that most motor units
are likely to be recruited when performing a rapid contraction
with a load equivalent to 1/3 of maximum. They also found
that the reduction in recruitment threshold was related to the
fiber-type composition of the muscle and was, for example,
greater for units in slow-contracting muscles (e.g., soleus)
compared with fast-contracting muscles (e.g., masseter)
(Desmedt and Godaux, 1978, 1979). They concluded that:
“The greater reduction in recruitment thresholds for slow
muscles likely facilitates their ability to perform fast contrac-
tions.”Furthermore, there were no differences in recruitment
order between slow, ramp contractions and ballistic contrac-
tions (Desmedt and Godaux, 1977a, 1977b;Fig. 3).
In contrast, some investigators suggested that peak force
during rapid contractions might best be accomplished by
the selective recruitment of fast motor units (Grimby and
Hannerz, 1977; Tanji and Kato, 1973a). However, Desmedt and
Godaux were unable to replicate the findings of Grimby and
Hannerz (1977), but instead found that the recruitment order
of motor unit pairs from the tibialis anterior (Figs. 3A and B)
and first dorsal interosseus (Figs. 3C and D) during slow ramp
contractions was the same as that for fast ballistic contrac-
tions (Desmedt and Godaux, 1977a, 1977b). Although there
were some reversals in recruitment order (~11% of trials),
these typically involved units with similar recruitment
thresholds during slow ramp contractions (Desmedt and
Godaux, 1977b). Furthermore, apparent recruitment reversals
for pairs of motor units with substantial differences in
recruitment threshold were likely due to the faster axonal
conduction of a high-threshold unit compared with a low-
19
Seyffarth received a medical education at the University of
Oslo. In 1940, he completed a PhD thesis on the behavior of
human motor units in healthy and paretic muscles under the
supervision of Professors Fredrik Leegaard [1891–1970] and Georg
Monrad-Krohn [1884–1964]. One outcome of his doctoral work
was that he proposed a theory about the control of discharge
frequency of motor units during fatiguing contractions, which
influenced subsequent work in the field. His pioneering work was
published in Acta Neurologica Scandinavica in 1941a, 1941b (see
reference list). Subsequently, he became a Rockfeller Foundation
Fellow from Oslo University and spent approximately one year in
Denny-Brown's laboratory at Harvard, with whom he published a
paper (1948). Subsequently, Seyffarth focused mostly on neuro-
logical disorders. His obituary was written in Norwegian and
translated by Karin Roelevelt.
20
Desmedt was a Belgian neurologist. He was student of Frédéric
Bremer [1892–1982], whom he succeeded as head of the Labora-
tory of Physiology and Physiopathology of the Medical Faculty of
the Université Libre de Bruxelles in Brussels. He was also the
director of the Brain Research Unit. Desmedt had a productive
collaboration with Emile Godaux, who is currently professor of
neurophysiology at the Medical Faculty of the Université de Mons
in Belgium. Their seminal publications on human motor unit
activity during various types of muscle contractions strongly
supported the size principle. Desmedt organized an international
meeting in Brussels (1971) and the 3-volume proceedings were
extremely influential in the field.
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threshold unit even though they were recruited in the spinal
cord according to size (Desmedt and Godaux, 1979). Indeed, it
is possible to observe 5–10 ms differences in the timing of APs
recorded in the muscle due to differences in axonal velocities
when two motoneurons discharge nearly simultaneously in
the spinal cord.
3.3. Anisometric contractions
Even among the early investigators there was an interest in
determining if recruitment order is consistent across contrac-
tion types (Desmedt and Godaux, 1979; Maton, 1980; Seyffarth,
1940). Desmedt and Godaux (1979) were the first to compare
recruitment order during isometric and shortening contrac-
tions. Recruitment order during slow and ballistic isometric
contractions with the first dorsal interosseus muscle was
similar to that during shortening contractions that abducted
the index finger (Fig. 4). Furthermore, the motor units were
derecruited in the reverse order during the subsequent
relaxation.
Subsequently, Thomas et al. (1987) compared the recruit-
ment order for pairs of motor units in the first dorsal
interosseus and adductor pollicis brevis during isometric
contractions and the movements associated with opening
and closing a pair of scissors. Although orderly recruitment
was largely preserved during both actions for the two muscles,
there were some recruitment reversals even for units with
dissimilar thresholds (>50% MVC). One factor that may have
contributed to the high incidence of recruitment reversals was
the complexity of the motor task. Although Tax and colleagues
confirmed that recruitment order is consistent with the size
principle during shortening contractions, recruitment thresh-
olds are often lower (Tax et al., 1989) but not always (Sturm et
al., 1997) during shortening contractions compared with
isometric contractions.
More controversial, however, is whether or not recruitment
order is preserved during lengthening contractions (Duchateau
and Enoka, 2008). The functional distinction between shorten-
ing and lengthening contractions is simply whether the muscle
fibres shorten or lengthen as the activated muscle exerts a force
Ballistic threshold (Kg)
Ramp threshold (Kg)
D
A
B
Ramp threshold
MU1
MU2
MU3
CMU1
MU2
Time (sec)
Fig. 3 –The influence of the rate of torque development on the recruitment threshold of motor units. (A) Recruitment threshold
of a motor unit from the tibialis anterior at different rates of increase in dorsiflexion force to a target force of 12 kg (~50% of
maximal voluntary contraction). The most rapid (ballistic) contraction reached peak force in ~0.15 s. (B) Recruitment threshold
of three different motor units (MU1–MU3) decreased when the time to reach peak force was reduced and became zero for the
most rapid contraction. Note that the decrease in recruitment threshold was greater for highest threshold unit. Modified from
Desmedt and Godaux (1977a). (C) Recruitment of two motor units (MU1, MU2) in the first dorsal interosseus during slow ramp
(upper traces) and ballistic (lower traces) contractions. Recruitment order was the same during the slow ramp contraction and
the four ballistic contractions. Adapted from Desmedt and Godaux (1977b). (D) Recruitment thresholds for 54 single motor units
in the first dorsal interosseus during slow ramp and ballistic contractions. The dashed line denotes the line of identity.
From Desmedt and Godaux (1978) wih permission of the publisher (Wiley-Blackwell).
49BRAIN RESEARCH 1409 (2011) 42–61

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against a load.
21
Whereas shortening contractions are used
solely to displace a load, lengthening contractions can be used
either toresist an imposed loador to control the displacement of
a load. One distinction between the two lengthening contrac-
tions is the extent to which the neural activation is modulated
during these actions. It is not clear, however, why studies on the
neural control of lengthening contractions are more recent than
those on isometric and shortening contractions.
A seminal study on recruitment order during lengthening
contractions recorded the discharge of single motor units in
soleus, lateral gastrocnemius, and medial gastrocnemius as
subjects performed isometric and anisometric contractions
with the plantarflexor muscles (Nardone et al., 1989). The
anisometric contractions involved lifting and lowering an
inertial load to match a prescribed trajectory. In contrast to
the strategy used to increase and decrease torque during the
isometric contractions, the distribution of EMG activity across
the involved muscles changed when lifting and lowering the
load with shortening and lengthening contractions, respective-
ly. The main conclusion of the study was that lengthening
contractions involved a change in strategy and that such
contractions are not simply the converse of a shortening
contraction (Nardone and Schieppati, 1988). In a subsequent
study on motor units (n= 99), Nardone et al. (1989) found that
15% of the units in soleus and 50% of the units in the two
gastrocnemii were recruited only during lengthening contrac-
tions (Fig. 5). These motor units invariably had high recruitment
thresholds as measured during isometric contractions. When
the task involved a shortening-isometric-lengthening sequence
of contractions, the recruitment of these units during the
lengthening contraction was accompanied by the derecruit-
ment of other units that were active during the shortening and
isometric contractions (Fig. 5). Significantly, the selective
recruitment of high-threshold motor units during the length-
ening contraction only occurred when dictated by the target
angular velocity. Nardone et al. (1989) proposed that the more
rapid relaxation of the force profile for thehigh-threshold motor
units enabled the subjects to match the torque to the prescribed
trajectory more accurately during faster lengthening contrac-
tions. They suggested that such a change in strategy might be
accomplished by a selective reduction in net excitation of low-
threshold motor units so that the desired decrease in force can
be achieved more readily.
Subsequent studies have not found systematic differences in
recruitment order between shortening and lengthening con-
tractionseither when lifting an inertial load (Garlan d et al., 1996;
Laidlaw etal., 2000; Søgaard et al., 1996; Stotz and Bawa, 2001)or
pushing against a torque motor (Pasquet et al., 2006; Stotz and
Bawa, 2001). These findings indicate that motor unit recruit-
ment order does not consistently vary during lengthening
contractions, especially when the task does not require match-
ing the displacement to a target trajectory. Thus, the recruit-
ment order of motor units is usually similar during shortening
and lengthening contractions, but it may vary when the task
requires the individual to perform a relatively fast lengthening
contraction that matches a prescribed trajectory.
3.4. Changes in recruitment order during voluntary
contractions
Although the size principle seems to govern the recruitment
order of motor units during slow and fast isometric and
anisometric contractions, some exceptions have been
reported during voluntary contractions in humans even
under carefully controlled conditions. In general, the excep-
tions involve either multifunctional and compartmentalized
muscles or changes in cutaneous input.
Many muscles can exert a force about more than one degree
of freedom at a joint and some evidence indicates that
recruitment order can vary when the muscle changes its action
about the joint. For example, Desmedt and Godaux (1981)
observed that 8% of the 142 pairs of motor units recorded from
the first dorsal interosseus muscle consistently reversed
recruitment order during contractions to produce a flexion
force with the index finger compared with an abduction force.
On the basis of a stronger correlation coefficient between the
spike-triggered averaged force of the motor unit and its
recruitment threshold for abduction compared with flexion of
Fig. 4 –Comparison of motor unit activity during a voluntary
isometric contraction (upper panel) and an abduction
movement (Isotonic) of the index finger (lower panel). (A and F)
Discharge of two motor units (1, 2) from the first dorsal
interosseus is illustrated during a slow ramp contraction (top)
and four ballistic contractions (B–E and G–J). In each panel,
upper traces represent intramuscular EMG activity and torque
(Isometric, A) or displacement (Isotonic, F).
Modified from Desmedt and Godaux (1979).
21
Early studies on the mechanical characteristics of lengthening
contractions were performed by Gasser and Hill in 1924, Bernard
Katz [1911–2003] in 1939, and Xavier Aubert [1919–1998] in 1954.
Jacques Duchateau and Roger Enoka (2008) wrote a recent review
on the control of lengthening contractions.
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the index finger, Desmedt and Godaux (1981) suggested that the
distribution of central inputs onto the motoneuron pool of the
first dorsal interosseus differed during the two actions. Simi-
larly, Thomas et al. (1986) found a greater incidence of
recruitment reversals during contractionsin different directions
with first dorsal interosseus and abductor pollicis brevis, which
led them to conclude that direction-dependent reversals of
recruitment order between different motor units can be
observed when muscle groups are involved in different tasks.
As the reversals were consistent across trials, these observa-
tions may explain some of the changes in recruitment
order reported previously (Basmajian, 1963, 1967; Grimby and
Hannerz, 1968, 1970; Kato and Tanji, 1972).
As a consequence of the different actions to which a
muscle can contribute, motor units in some portions of a
muscle may be involved in motor tasks quite distinct from
those to which other units in the muscle contribute (Loeb,
1985; Scott and Mendell, 1976; Stuart and Binder, 1977). An
example in the human is biceps brachii, which contributes to
both flexion about the elbow joint and supination of the
forearm. Ter Haar Romeny et al. (1982) showed that some
motor units in the long head of biceps brachii were recruited
when only a single force was exerted, whereas most units
were activated when the task involved various combinations
of flexion and supination forces. Subsequently, the specificity
of the motor unit activity was related to the medial–lateral
location in the long head of biceps brachii (Ter Haar Romeny et
al., 1984), which led to the concept of “task-specific”activation
of motor unit subpopulations within multifunctional muscles
(Loeb, 1985). Consequently, the size principle was suggested to
govern recruitment order within subpopulations of a moto-
neuron pool in some muscles: “…the various tasks that
multifunctional muscles have to perform in our activities of
daily living, necessitates a continuum of patterns of central
connectivities onto the same motor pool that can lead to some
disorderly recruitment.”(Desmedt, 1983).
In the same vein, Butler et al. (1999) reported that the
recruitment thresholds of most diaphragmatic motor units
were related to inspiratory volume, but that the thresholds of
some units (~20%) varied with the task being performed. The
task-sensitive units discharged later than expected when the
target inspiratory volume was high and earlier than expected
when the target volume was low. The change in recruitment
threshold in some units was accompanied by a slight change
in recruitment order when voluntary inspiratory tasks were
matched with involuntary breaths, but this observation was
mainly limited to higher inspiratory flows. These findings
suggest that there may be subtle differences in the drives
reaching the motoneurons during voluntary and involuntary
breathing (Watson and Whitelaw, 1987).
Together, these findings demonstrated that humans are
not able to modify the recruitment order of motor units during
a voluntary contraction unless the muscle action is changed.
The other variable that can influence recruitment order is
the amount of cutaneous afferent feedback received by the
motoneuron pool. For example, Garnett and Stephens (1981)
found that digital nerve stimulation of the index finger
increased recruitment threshold for low-threshold units and
decreased it for high-threshold units in first dorsal inter-
osseus. Garnett and Stephens (1980) suggested that the
distribution of synaptic input to the motoneuron pool differed
for cutaneous and muscle afferents, and may be preferentially
organized with respect to motor unit type. Subsequently,
Kanda and Desmedt (1983) recorded motor unit pairs from first
dorsal interosseus during a precision grip task and found that
20% of the units exhibited a decrease in recruitment threshold
after the motoneuron pool had received cutaneous input
caused by rubbing the tips of the thumb and index finger
against each other. The changes in recruitment threshold
were limited to high-threshold units and were often accom-
panied by a reversal of recruitment order, which led Kanda
and Desmedt (1983) to conclude that cutaneous stimulation
facilitates the recruitment of high-threshold units. The re-
sults, which confirmed those obtained in animal studies
(Kanda et al., 1977), suggested that cutaneous input to the
motoneuron pool during such actions as prehension, tactile
grasping, and the withdrawal reflex might modify the orderly
recruitment of motor units.
Fig. 5 –Activation of the triceps surae muscles during shortening and lengthening contractions. The subject performed ankle
movements at various controlled velocities. From top to bottom, traces correspond to the intramuscular EMG for gastrocnemius
lateralis, foot position, and surface EMGs for soleus and gastrocnemius lateralis. During a slow shortening contraction (left
panel), the soleus EMG activity was greater than that for gastrocnemius lateralis, but the distribution of EMG activity during the
lengthening contraction differed from that observed during the shortening contraction. Top traces indicate that motor units in
gastrocnemius lateralis were selectively recruited within the recording volume of the electrode during slow lengthening and
fast shortening contraction but not during slow shortening contraction.
Adapted from Nardone et al. (1989) with permission of the publisher (Wiley-Blackwell).
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3.5. Motor unit types
In 1973, Burke and colleagues developed a classification
scheme for motor units based on the physiological properties
of the motor units and the histochemical profiles of the
associated muscle fibers in the cat medial gastrocnemius.
Motor units were classified into three main types based on
fatigability and the “sag”property.
22
Motor units that did not
exhibit sag were classified as slow contracting (type S),
whereas those that displayed sag were denoted as fast
contracting (type F). The type F motor units were further
distinguished into those that were fast to fatigue (type FF) and
those that were fatigue-resistant (type FR) in response to a
standardized stimulus protocol. Although some studies have
suggested that this classification scheme is also appropriate
for human muscles (Garnett et al., 1979; Mayer and Young,
1979; Stephens and Usherwood, 1977), others have reported
the absence of distinct motor unit types in humans (Bigland-
Ritchie et al., 1998).
A key outcome of this classification scheme was the
demonstration of a strong association between recruitment
order and the metabolic and physiological capabilities of motor
units (Henneman and Olson, 1965; Kernell, 1992). The earliest
recruited motor units exert the smallest forces and fatigue the
least during one standardized protocol, which explains why
low-contraction forces can be sustained for long durations.
Conversely, the last-recruited motor units exert greater forces
and can only do so for brief periods of activity. Despite the
appeal of this scheme, the physiological properties of motor
units in both experimental animals and humans do not exhibit
discretedistributions, butrather they extendalong a continuum
from one extreme to another (Burke and Tsairis, 1974; Garnettet
al., 1979; McDonagh et al., 1980; Romaiguère et al., 1989; Van
Cutsem et al., 1997). Therefore, the concept of motor unit type is
useful for characterizing changes in muscle properties, but it is
not the basis for motor unit recruitment during voluntary
contractions (Bigland-Ritchie et al., 1998; Enoka, 1995).
3.6. Motor unit rotation
One of the early questions about motor unit recruitment was
whether or not motor units with similar recruitment thresh-
olds could alternate activity during constant-force contrac-
tions. Forbes
23
suggested, for example, that motor units might
rotate into and out of activity during fatiguing contractions
(1922): “A motor unit of similar threshold is now recruited,
while the fatigued unit cannot continue to discharge. After
some minutes, this second motor unit falls silent, and the
originally discharging unit resumes tonic discharge”. None of
the early work, however, found any evidence of motor unit
rotation in triceps brachii (Adrian and Bronk, 1929), biceps and
triceps brachii (Olive Smith [1883–1978], 1934), various limb
muscles (Lindsley, 1935), or in flexor digitorum sublimis
superficialis (Arthur Gilson [1896–1991] and Warren Mills
[1914–2004], 1941) during sustained contractions.
Smith (1934) reported that the recruitment of additional
units was sometimes observed during long recordings (20–
30 min) as fatigue developed, but these units did not replace
previously activated units. Furthermore,she emphasized “…the
surprisingly slow rates of discharge…are in themselves suffi-
cient to explain absence of fatigue in moderate degrees of
tension.”However, morerecent studies on trapezius (Westgaard
and De Luca, 1999) and on forearm and lower leg muscles (Bawa
et al., 2006) demonstrated rotation among motor units with
similar recruitment thresholds during long-lasting submaximal
contractions. Nonetheless, Bawa and colleagues suggested that
rotation is not a strategy used by the CNS but “…reflects the
intrinsic (or local) organization of motoneuron pools innervat-
ing the muscles …”, perhaps involving transient changes in
voltage threshold for generating APs (Manning et al., 2010).
By the end of the 20th C, therefore, the experimental
evidence indicated that the recruitment order of human motor
units was primarily determined by motoneuron size. Changes
in recruitment order can be observed in multifunctional
muscles when they contribute to different actions and when
there are changes in sensory feedback received by the
motoneuron pool. The consistent changes in recruitment
order associated with these conditions differ from the
irregular changes in recruitment order reported earlier. In
contrast to a common viewpoint in the literature on experi-
mental animals, human motor units are recruited during
voluntary contractions along a continuum as a function of
their size and not according to motor unit type.
4. Rate coding of motor unit discharge
Soon after the pioneering work of Sherrington and colleagues in
the early 1900s, there was interest in measuring the activity of
single motoneurons during natural activities to learn about the
control of voluntary movement. Such studies were technically
difficult, however, and the first indirect observations on
motoneuron activity were achieved through motor unit re-
cordingsduring weak reflex contractions in animals(Adrian and
Bronk, 1928; Denny-Brown, 1929; John Eccles [1903–1997]
24
and
Sherrington, 1930) and during volitional activity in humans
(Adrian and Bronk, 1929).
From the first experiments in humans, it was apparent that
motor units discharged APs repetitively during sustained
contractions and that such discharges could continue for a
long time. As characterized by Adrian and Bronk (1929),“With
22
The sag property is often used to distinguish fast contracting
motor units from those that are slow contracting. It comprises a
submaximal tetanic force profile that exhibits a rapid increase in
force and a subsequent decrease that may or may not return to
the initial peak value. As with other contractile properties,
however, the magnitude of sag is distributed continuously across
a motor unit population (Carp et al., 1999).
23
Forbes was a pioneer in the development of electrophysiology
in the USA. After graduating from Harvard Medical School in 1910,
he spent a year (1911–1912) with Sherrington in Liverpool and
learned about spinal reflexes. While in England, he visited the
Laboratory of Physiology in Cambridge where Lucas introduced
him to “modern”electrophysiology. The influence of these two
luminaries was obvious in a subsequent article he wrote (1922).
He was also the first to use a vacuum tube amplifier in
neurophysiological experiments. Further information on Forbes'
career can be found at: www.nap.edu/html/biomems/aforbes.pdf.
24
The contributions of Eccles to the field of motor control can be
found in the companion paper of Stuart and Brownstone (2011).
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a slight degree of voluntary contraction sharply isolated
actions currents appear at a rate which may begin as low as
6 a sec. and rises gradually as the contraction develops.”and
that “…voluntary contraction in man is maintained, like the
reflex contractions in the cat, by a series of nerve impulses
which range from 5 to 50 or more a sec. in each nerve fibre,…”.
Smith (1934) and Lindsley (1935),bothfromthesame
laboratory at Harvard Medical School, subsequently confirmed
the main results of Adrian and Bronk (1929). Additionally,
Smith (1934) noted that during increases in muscle force:
“There is great independence of rhythm in different units.”
and Lindsley (1935) reported that “…individual motor units
usually began discharging APs at frequencies of 5 to 10 per
second,evenasslowas3persecond,butthatthese
frequencies could be increased to about 30 per second and
even as high as 50 per second”.
Since the early recognition that rate coding contributes
significantly to the control of muscle force, investigators have
focused on identifying the mechanisms that limit minimal
and maximal discharge rates, the association between rate
coding and muscle force, and the discharge patterns exhibited
by motor units.
4.1. Minimal discharge rate
In the first part of the 20th C, the idea emerged from
experiments on animals that the minimal repetitive discharge
rate was due to an intrinsic mechanism located in the
motoneuron itself (Eccles and Hebbel Hoff [1907–1987], 1932).
Kernell (1965b) was the first to provide direct evidence of the
mechanism when he noted that the lower limit for repetitive
discharge by motoneurons in the cat was related to the
duration of the afterhyperpolarization (AHP) phase of the AP.
Furthermore, he found a strong correlation between the time
course of the motoneuron AHP and the contractile kinetics of
the corresponding muscle fibers, which indicated that the
minimal discharge rate corresponded to the rate at which
consecutive motor unit twitches began to summate.
Subsequent studies in humans, however, reported that
subjects are able to discharge APs repetitively with interspike
intervals that were much longer than the estimated AHP
duration (Kato and Tanji, 1972; Kudina and Alexeeva, 1992b).
For example, Kato and Tanji (1972) reported that humans are
able to control discharge frequencies as low as 0.5 or 1 Hz.
They even report that such low frequencies are easier to
control than higher discharge frequencies. Nonetheless, the
minimal rate at which most motor units discharge APs
repetitively in humans during voluntary contractions is 5–
8 pulses per second depending of the muscle and the motor
unit size (Adrian and Bronk, 1929; Kudina and Alexeeva, 1992b;
Lindsley, 1935; Macefield et al., 1993; Milner-Brown et al.,
1973c; Monster and Chan, 1977; Seyffarth, 1940). However, the
observation that humans can discharge APs repetitively with
interspike intervals that were longer than the AHP duration
(~90 ms in barbiturate-anesthetized cat motoneurons supply-
ing slow-twitch muscle fibers; Eccles et al., 1958) led Kudina
and Alexeeva (1992b) to conclude that: “…AHP is not the only
leading mechanism controlling the low firing rate of moto-
neurones under conditions of their natural activity in man.”.
Consistent with this suggestion, Brownstone et al. (1992)
found that AHP amplitudes in motoneurons during trains of
impulses elicited in decerebrate cats by stimulation of the
mesencephalic locomotor region are decreased significantly
compared with amplitudes recorded during comparable
frequencies of discharge induced by intracellular current
injections. More recent work suggests that synaptic inputs
can modulate the intrinsic AHP conductances during motor
tasks, such that the AHP properties and motoneuron dis-
charge rate can be modulated to meet the needs of a particular
task (Stauffer et al., 2007).
With the discovery by Hultborn and colleagues in the 1970s
(Hultborn et al., 1975) that a motoneuron can produce self-
sustained firing following a brief stimulus due to a calcium-
activated membrane potential (plateau potential) (Hounsgaard
et al., 1984; Schwindt and Crill, 1980), a new era emerged in the
understanding of how discharge rates can be modulated.
Indeed, recent studies on experimental animals indicate that
the discharge rate of a motoneuron can be modified by
monoaminonergic inputs to the spinal cord that boost the
gain of the frequency-current relation (Conway et al., 1988;
Hounsgaard et al., 1988; Lee and Heckman, 1996). Work on
animal preparations suggests that the initial increase in
discharge rate is likely mediated by the activation of the
dendritic persistent inward currents (PIC) that seem to
establish the minimal rate for repetitive discharge (see
Brownstone, 2006 for a review).
4.2. Maximal discharge rate
Early on in the study of motor unit activity, it was reported
that the timing of the APs might have a significant influence
on the force exerted by a motor unit (Gilson and Mills, 1941;
Lindsley, 1935; Seyffarth, 1938, 1940). It was known, for
example, that brief intervals (5–55 ms) between successive
APs can increase the rate of force development during a rapid
contraction and may transiently augment motor unit force
during submaximal contractions (Sybil Cooper [1900–1970]
and Eccles, 1930; Eccles and Hoff, 1932). The first recordings of
motor unit activity during fast contractions were obtained
from the flexor digitorum sublimis during a rapid flexion
movement of the fingers (Gilson and Mills, 1941). The findings
included greater discharge rates during rapid movements
than during sustained contractions and, for the first time, the
existence of double discharges of APs by the same motor unit
(see their Fig. 1). They also recognized that “Occasionally the
spikes of the double response have been separated by as little
as 10 msec …” Subsequent studies reported similar high
maximal rates (up to 100 Hz) during rapid, brief contractions
(Grimby and Hannerz, 1977; Tanji and Kato, 1973b).
Desmedt and Godaux (1977a) provided a more detailed
description of motor unit discharge during rapid contractions
when they compared the discharge of 24 units from the tibialis
anterior muscle during both ramp and ballistic contractions.
Discharge rates ranged from 60 to 120 Hz during ballistic
contractions, but only reached values of ~30 Hz for slow
contractions to similar peak torques (Fig. 6). They also
reported that units usually began to discharge at high
instantaneous rates during a ballistic contraction and that
the rate declined progressively with successive APs. The same
discharge pattern was observed during ballistic contractions
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with first dorsal interosseus (Desmedt and Godaux, 1977b) and
the masseter (Desmedt and Godaux, 1979), but contrasted with
that observed during fast ramp contractions (Desmedt and
Godaux, 1977a). The main conclusion of this work was that the
decrease in recruitment threshold during fast contractions
meant that rapid force development depended on rate coding
(Desmedt and Godaux, 1977a).
The double discharges (doublets) initially observed by
Gilson and Mills (1941) were further investigated in 1948 by
Stedman Denslow [1906–1982]; he reported double discharges
with intervals as brief as 3.5 ms (286 Hz) and their presence
during sustained submaximal contractions. He noted that
“double discharges occurred most frequently as the unit
started or stopped”and that “…the striking feature of double
discharge was the long periods which intervened between a
double discharge and the next action potential.”In agreement
with data from the decerebrate cat (Hoff and Grant [1910–
1987], 1944), Denslow suggested that double discharges are a
consequence of motoneurons being in a “supernormal peri-
od”. Later, Kudina (1974) observed double discharges by high-
threshold motor units during sustained isometric contrac-
tions and reported that the incidence varied across subjects.
However, most double discharges seem to occur at the start of
motor unit activity (Bawa and Calancie, 1983; Denslow, 1948;
Hoff and Grant, 1944; Kudina, 1974) or when motor units are
discharging at minimal rates (Bawa and Calancie, 1983). These
observations suggest that double discharges usually occur
during tasks when force changes rather than during steady
isometric contractions.
Bawa and Calancie (1983) observed fewer repetitive double
discharges in the flexor carpi radialis muscle with an increase
in the speed or force of a ramp contraction, which was
consistent with the finding of fewer repetitive doublets as the
excitatory drive for the stretch reflex was increased in the
decerebrate cat (Hoff and Grant, 1944). They further reported
that both low- and high-threshold units discharged repetitive
doublets, but those that could discharge doublets showed
higher maximal discharge rates. In contrast, Gurfinkel et al.
(1972) found an increase in the incidence of double discharges
(<30 ms) with an increase in contraction speed. Similarly,
short interspike intervals (<10 ms) were observed at the onset
of ballistic contractions (Desmedt, 1980; Desmedt and Godaux,
1977a).
However, Bawa and Calancie (1983) suggested that the
mechanisms underlying double discharges at interspike in-
tervals of approximately 20 to 30 ms differ from those for
intervals of < 10 ms. Brief interspike intervals (<10 ms) may
result from the generation of a second AP when a motoneuron
is in a state of increased depolarization, or delayed depolar-
ization, that occurs during the falling phase of the AP. Delayed
depolarization was proposed to result from an antidromic
invasion of the dendrites following the initial AP, which
causes a small inflection on the falling phase of the initial AP
(Baldissera et al., 1982; Calvin and Schwindt, 1972; Ragnar
Granit [1900–1991]
25
et al., 1963; Kernell, 1964; Nelson and
Burke, 1967). Motoneurons are presumed to be more respon-
sive to slight increases in synaptic input during the phase of
delayed depolarization. The second AP in the double discharge
is usually followed by a longer period of hyperpolarization
than after a single discharge as the AHP phases of the two APs
summate (Calvin and Schwindt, 1972). In contrast to these
types of double discharges, Bawa and Calancie (1983) proposed
that the discharge pattern at the onset of ballistic contraction
25
Granit completed a medical degree at Helsinki University in
1927 and became docent in physiology in 1929. He spent 1929–
1931 in the laboratory of Bronk at the University of Pennsylvania
and 1932–1933 in the laboratory of Sherrington in Oxford. After
these experiences, he became a professor of physiology at
Helsinki University (1937) and at the Karolinska Institute of
Stockholm (1940). He received the Nobel Prize in Physiology or
Medicine in 1967 for his work on the primary physiological and
chemical visual processes in the eye although, at that time, he
was working on motoneuron characteristics. A complete biogra-
phical memoir was written by Sten Grillner (1995).
Fig. 6 –Comparison of the discharge rate of a single motor unit in tibialis anterior during a slow ramp contraction (a) and a
ballistic contraction (b) to similar peak dorsiflexion forces. The graph (c) illustrates the changes in instantaneous discharge rate
for this unit as a function of the force produced by the muscle. Note that peak discharge rate of the unit was much greater during
the fast contraction (filled circles) compared with the slow contraction (open circles).
From Desmedt and Godaux (1977a) with permission of the publisher (Wiley-Blackwell).
54 BRAIN RESEARCH 1409 (2011) 42–61

Author's personal copy
results from the motoneuron receiving massive amounts of
synaptic input.
More recently, Kudina and Alexeeva (1992a) suggested that
repetitive and single doublets during sustained, low-level
contractions are due to a common mechanism, such as a
“certain descending synaptic input.”Although the descending
pathway is unknown, Day et al. (1989) and Bawa and Lemon
(1993) found that double discharges can be evoked by a
magnetic stimulus applied over the motor cortex. Further-
more, the incidence of double discharges can increase with
training (Bawa and Calancie, 1983; Denslow, 1948; Van Cutsem
et al., 1998), even though the role of double discharges in
natural behavior is unknown (see Garland and Griffin, 1999).
4.3. Rate coding and muscle force
Despite the recognition by Adrian and Bronk (1929) that force
gradation during voluntary contractions depends on both
recruitment and rate coding, they ascribed a more significant
role to rate coding based on what was known at the time about
rate coding in sensory neurons. This interpretation was
tempered by subsequent investigators (Denny-Brown and
Pennybacker, 1938; Lindsley, 1935; Smith, 1934) as the early
work did not examine the relation between discharge rate and
muscle force. In 1940, Seyffarth seems to have been the first
person to examine this association: “As the first unit increases
in frequency, the new units, just after their appearance,
accelerate, and soon attain the frequency of those previously
active”. He also reported that during a slow decrease in
tension: “… the units usually disappear in the reverse order to
that in which they appeared, and the order of the units will
remain constant during the whole series of contractions.”
The first study to characterize the relation between mean
discharge rate and muscle force in humans was that of Bigland
and Lippold (1954). They recorded single motor unit activity in
the abductor digiti minimi brevis and reported that “…most
units started and stopped abruptly and varied in their
discharge rates relatively little, in the course of a contraction.”
and that “Units active at low tensions (below 5% MVC), on the
other hand, usually had a lower starting frequency and
showed a greater frequency range than those active only at
higher tensions.”They further concluded that, “…the starting
rate of most units is quite high in the region of 20/sec and that
this frequency changes little until the contraction of the
muscle is almost maximal.”The recordings indicated that the
relation between discharge rate and muscle force could be
characterized with a sigmoidal function, which suggested to
Bigland and Lippold that force gradation was largely achieved
by motor unit recruitment, except at low and high contraction
forces.
Bracchi et al. (1966) observed a similar relation between
discharge rate and force on the basis of single motor unit
recordings in twelve different muscles, similar to the subse-
quent findings of Gydikov and Kosarov (1974) in the biceps
brachii. The seminal study on the influence of rate coding on
muscle force was published a few years later by Monster and
Chan (1977) when they recorded the discharge of ~ 500 units of
the extensor digitorum communis muscles of 8 men during
steady 1-s periods of a slowly varying intermittent voluntary
isometric contraction (Fig. 7). The data indicated that the
minimal discharge rate was similar for all units and most of
them discharged over the same range (8 to 16–24 Hz).
Surprisingly, the high-threshold units displayed the smallest
range in discharge rate.
Two years later, Kanosue et al. (1979) reported a similar
relation to that of Bigland and Lippold (1954); the discharge of
~35 units from the brachioradialis muscle in each of three
subjects exhibited a sigmoidal function with muscle force, and
high-threshold units reached greater frequencies (~50 Hz) in
the force range between 75 and 100% of MVC. To explain the
discrepancy with the study of Monster and Chan (1977),
Kanosue and colleagues suggested that “…small muscles as
those of the fingers whose tension must be adjusted delicate-
ly, rate coding may be the major mechanisms for controlling
force, whereas in large muscles of extremities which generate
strong force, recruitment would be more important.”Although
it has been shown that maximal discharge rates likely differ
across muscles (De Luca et al., 1982a) and are related to the
contractile properties of the muscle (Bellemare et al., 1983), the
finding that high-threshold units do not reach the greatest
discharge rate in small muscles seems to contradict the
greater frequency (~ 50–100 Hz) of intraneural stimulation
often required for single motor unit to achieve maximal
tetanic force (Fuglevand et al., 1999; Macefield et al., 1996;
Thomas et al., 1991). This issue remains unresolved largely
due to technical factors that limit the ability to record the true
maximal discharge rate of high-threshold units and to follow
low-threshold units over the full range of contraction forces.
4.4. Discharge variability
Although the first studies on motor unit activity focused mainly
on the range of discharge rates and the contribution of rate
coding to maximal force, subsequent studies investigated
Fig. 7 –Repetitive discharges of 59 motor units in the extensor
digitorum communis muscle of a single human volunteer
during isometric voluntary contractions in which force was
increased progressively. The graph shows that most units
discharged over a similar range (8 Hz to 16–24 Hz), with the
highest threshold units displaying the smallest range.
From Monster and Chan (1977) with permission of the
publisher (The American Physiological Society).
55BRAIN RESEARCH 1409 (2011) 42–61

Author's personal copy
discharge variability. For example, Toshihiko Tokizane [1909–
1973]
26
and Tsuyama (1952) noticed that although APs occur at
nearly regular intervals during sustained submaximal contrac-
tions, there was some variability in the interspike intervals and
that this depended on contraction strength. Thereafter, they
confirmed that the variability in discharge frequency is marked
at the initial stage when each motor unit is recruited, but
declines with an increase in contraction intensity (Mori, 1973;
Person and Kudina, 1972; Tanji and Kato, 1973b).
From experiments performed on animals and humans,
Tokizane and Shimazu (1964) proposed that “spinal factors”
lead motor units to discharge with regular frequency but that
“cortical factors”cause them to discharge with enhanced
variability. However, a subsequent study in animals by Calvin
and Stevens (1968) demonstrated that variability in motoneu-
ron discharge is caused by membrane noise, which is primarily
synaptic in origin. Fluctuations in membrane potential arise
from temporal and spatial summation of postsynaptic poten-
tials caused by random impulse activity from various sources.
More recent studies indicate, however, that the intrinsic
properties of the motoneuron membrane may influence the
amplitude of the noise, and thereby change the variability of its
discharge (Antonov et al., 2003).
4.5. Tonic and phasic motor units
In the early 1950s, Tokizane published 3 papers (Tokizane, 1954,
1955; Tokizane and Tsuyama, 1952) that were practically
unnoticed in the international scientific community because
they were written in Japanese. This information became
available subsequently when it appeared in a book written in
English (Tokizane and Shimazu, 1964). Tokizane and colleagues
analyzed the discharge characteristics of motor units at various
forces of contraction in the human soleus muscle. By plotting
the mean discharge intervals against the standard deviations at
several mean rates across motor units, they concluded that “…
they do not distribute themselves at random, but cluster along
to definite curves…”. The dichotomous distribution was inter-
preted as representing two types of motor units (called
“neuromuscular unit”by these authors) that were categorized
as “tonic”and “phasic”motor units (Tokizane, 1955). Tonic u nits
had low discharge variability and a reduced range of modula-
tion, whereas “kinetic”units were more variable and capable of
a greater rangeof frequencies. By comparing the dischargerates
of motor units in many different muscles, Tokizane further
reported functional differences among muscles. However, Jack
Petajan [1930–2005] and Philip (1969) were skeptical of this
distinction due to the difficulties associated with maintaining
the target discharge rates during the experimental protocols.
In support to the concept of tonic and kinetic units, Granit
et al. (1956, 1957) published two papers distinguishing two
major motoneuron characteristics that they called “tonic”and
“phasic”motoneurons. Tonic motoneurons displayed long-
lasting repetitive discharges (tonic discharge) when they were
penetrated with a microelectrode and stimulated with a long-
lasting depolarizing current. In contrast, a high percentage of
motoneurons failed to discharge more than a single spike or a
brief train of APs (phasic discharge), regardless of the
stimulation intensity. The two discharge characteristics were
ascribed to differences in intrinsic motoneuron properties; for
26
Tokizane graduated from the University of Tokyo with a
medical degree in 1934. His scientific activities were interrupted
for several years during the WWII, after which he completed a
PhD in medical sciences (1952). In 1954, he became an associate
professor and chair of the Department of Neurophysiology with
an appointment to the Institute of Brain Research at the
University of Tokyo. Most of his time from 1947 to 1954 was
devoted to investigating the electromyogram and the analysis of
the discharge patterns of human motor units during muscular
activity. He trained many of Japan's prominent neurophysiolo-
gists, several of whom published a book in his honor. For further
details on this Japanese publication, contact Yoshiko Shinoda
(yshinoda.phy1@med.tmd.ac.jp).
Fig. 8 –Illustration of a high-threshold motor unit from the extensor indicis during a slow ramp (A) and step (B) increases in force
during an isometric contraction. The step increases in force were accompanied by the transient activation of this unit, which
then stopped discharging once the plateau was reached. At higher forces, however, the motor unit remained active during the
plateau phase.
From Büdingen and Freund (1976) with permission of the publisher (Springer).
56 BRAIN RESEARCH 1409 (2011) 42–61

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example, motoneurons with large axons often discharged APs
in phasic bursts, whereas those with thinner axons produced
long-lasting tonic discharges (Granit et al., 1956, 1957).
Although Kernell (1965a) suggested that motoneurons
unable to discharge APs repetitively were damaged when
impaled by the microelectrode, Gydikov and colleagues resur-
rected these ideas 20 years later when they characterized the
stretch response of humanmotor units in bicepsbrachii as tonic
or phasic (Gydikov and Kosarov, 1974; Kosarov et al., 1976). The
presence of tonic and phasic motor units during voluntary
contractions, however, depends on whether the subject per-
forms slow ramp contractions or step increases in force
(Büdingen and Freund, 1976; Freund et al., 1975; Maton., 1980;
Person and Kudina, 1972). For example, Freund and colleagues
(1975) demonstrated that step increases in force are achieved by
the transient activation of high-threshold units that are
activated at small rapid force increments, but stop discharging
once the plateau is reached (Fig. 8). In contrast, lower-threshold
motor units will remain active during the plateau phase but at a
reduced discharge rate. The number of units that are recruited
and remain active during the plateau phase increases with the
size of the step, which led to the conclusion that: “Because
recruitment threshold depends on the speed of muscle con-
traction, all motor units can be phasically activated during rapid
contractions as long as the total force is below their tonic
threshold (Freund et al., 1975).In contrast, all motor units can be
tonically activated if the steady-force level is above the tonic
threshold. The tonic or phasic discharge pattern simply reflects
whether the unit operates below or above its tonic threshold.”
After these studies of Freund and colleagues (Büdingen and
Freund, 1976; Freund et al., 1975), the terms “tonic”and “phasic”
motor unit have been abandoned as it is recognized that a given
motor unit can exhibit both discharge profiles (Freund, 1983).
In summary, ever since the first motor unit recordings in
humans it has been obvious that discharge rate can be
modulated over a wide range of frequencies. Minimal discharge
rates during voluntary contractions are about 5 Hz, and the
variability in discharge times is greatest at low rates. The peak
discharge rate that can be achieved depends on the type of
muscle contraction; it reaches values of about 30–50 Hz during
ramp contractions, but values of 100 Hz are not uncommon
during ballistic contractions. The influence of discharge rate on
motor unit force can be characterized with a sigmoidal function,
which indicates that the gain of the relation is greatest at
intermediate discharge rates. Despite early suggestions that
motor units could be distinguished as “tonic”or “phasic”
depending on discharge characteristics, it is now seems that a
given motor unit can discharge APs either repetitively or
intermittently.
5. Concluding thoughts
After the pioneering work of Sherrington and colleagues in the
early 1900s on decerebrate animals, the possibility emerged
that the mechanisms underlying muscle activation in more
natural conditions could be determined. Although the record-
ing of single motor unit activity was technically difficult at
that time, the remarkable contribution of Adrian and Bronk
(1928, 1929) in animals and humans created a new era that led
to major progress in the understanding of the motor output
discharge from the spinal cord. With Henneman's seminal
observations on the stereotyped activation order of motor
units according to the size of the motoneuron (size principle),
a foundation was established for the systematic study of
motor unit activity. The 1970s were without doubt a critical
period for the expansion of our knowledge on the control of
motor function in humans. Although many questions remain
unanswered, the work described in this review identifies the
critical issues in this field and underscores how progress will
depend on the successful integration of observations derived
from studies on experimental animals and humans.
Acknowledgments
Some of the above was presented by J.D. in collaboration with
R.M.E. in an historical session at the international meeting
“Towards translational research in motoneurons,”Paris, FRA,
July 91–3, 2010 (Organizers: CJ Heckman, Didier Orsal, Jean-
François Perrier,Daniel Zytnicki). We thank Nga Nguyen (AHSC
library, University of Arizona) for her library research and Joel
Enoka for his assistance in finding some of the original articles.
We also thank François Clarac and Douglas Stuart for their
helpful comments on various drafts of our article.
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61BRAIN RESEARCH 1409 (2011) 42–61

Corrigendum
Corrigendum to “Human motor unit recordings: Origins and
insight into the integrated motor system”
[Brain Res. 1409 (2011) 42–61]
Jacques Duchateau
a,
⁎, Roger M. Enoka
b
a
Laboratory of Applied Biology, Université Libre de Bruxelles, 808 Route de Lennik, CP 640, 1070, Brussels, Belgium
b
Department of Integrative Physiology, University of Colorado, Boulder, CO 80309–0354, USA
Page 52, column 1, last line and column 2, lines 1-5 should
read as follows:
[In 1922, Forbes raised the possibility of fiber group rotation
during fatiguing contractions but emphasized that it required
testing. As described by Bawa and coworkers (2006), motor
unit rotation can be characterized as follows: “A motor unit
of similar threshold is now recruited, while the fatigued unit
cannot continue to discharge. After some minutes, this sec-
ond motor unit falls silent, and the originally discharging
unit resumes tonic discharge”.]
BRAIN RESEARCH XX (2011) XXX
BRES-41788; No. of page: 1; 4C:
DOI of original article: 10.1016/j.brainres.2011.06.011.
⁎Corresponding author. Fax: +32 2 555 69 96.
E-mail address: jduchat@ulb.ac.be (J. Duchateau).
Available online at www.sciencedirect.com
www.elsevier.com/locate/brainres
Please cite this article as: Duchateau, J., Enoka, R.M., Corrigendum to “Human motor unit recordings: Origins and insight into
the integrated motor system”, Brain Res. (2011), doi:10.1016/j.brainres.2011.09.024
0006-8993/$ –see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.brainres.2011.09.024