ARTICLE

A Principle of Neuromechanical Matching for Motor

Unit Recruitment in Human Movement
Anna L. Hudson, Simon C. Gandevia, and Jane E. Butler
Neuroscience Research Australia and University of New South Wales, Sydney, New South Wales, Australia
Downloaded from https://journals.lww.com/acsm-essr by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AWnYQp/IlQrHD3PxsYRkX7FpPHk6SczqiRfgRI05gXZMYf1wGKSIj9Cl5xRn+jj+ZnmA== on 09/24/2020

HUDSON, A.L., S.C. GANDEVIA, and J.E. BUTLER. A principle of neuromechanical matching for motor unit recruitment in hu-
man movement. Exerc. Sport Sci. Rev., Vol. 47, No. 3, pp. 157–168, 2019. What determines which motor units are active in a motor task?
In the respiratory muscles, motor units are recruited according to their mechanical advantages. We describe a principle of motor unit recruitment
by neuromechanical matching due to mechanisms in the spinal cord that sculpt descending drive to motoneurons. This principle may be applicable
to movements in nonrespiratory muscles. Key Words: neuromechanical matching, respiratory muscles, motor control, motor unit, motoneurons,
spinal distribution network

properties of motoneurons, and the summation of multiple ex-

Key Points
• In the respiratory muscles, motor units are recruited accord-
ing to their inspiratory mechanical advantage, which pro-
vides an efficient strategy to ventilate the lungs.
• This recruitment is adaptable, not related to the intrinsic
properties of motor units, and inconsistent with motor unit
recruitment according to the classic size principle.
• We propose a principle of motor unit recruitment by
neuromechanical matching.
• The mechanisms are likely to involve premotoneuronal
neurons in the spinal cord that sculpt descending drive to
the motoneurons depending on the motor task.
• There is evidence of motor unit recruitment by neurome-
chanical matching in nonrespiratory muscles, and, thus,
this principle may extend to many movements.
INTRODUCTION
Motor tasks involve the recruitment and discharge of motor
units, both within and across muscles, which work in synergy
to develop force. A motor unit is defined as a motoneuron, its
axon and the muscle fibers it innervates. The firing pattern of
a motoneuron is determined by the conversion of synaptic in-
puts into action potentials, which depends on the intrinsic
properties of motoneurons, neuromodulation of the biophysical
Address for correspondence: Anna Hudson, Neuroscience Research Australia, Margarete
Ainsworth Building, Barker St., Randwick, Sydney, New South Wales 2031, Australia
(E-mail: a.hudson@neura.edu.au).
Accepted for publication: March 28, 2019.
Editor: Janet L. Taylor, M.D.
0091-6331/4703/157–168
Exercise and Sport Sciences Reviews
DOI: 10.1249/JES.0000000000000191
Copyright © 2019 by the American College of Sports Medicine
citatory and inhibitory synaptic inputs to the motoneuron (1).
Given the one-to-one relationship between motoneuron dis-
charge and a motor unit action potential in the muscle, record-
ings of motor unit activity are a surrogate for direct recordings
from the motoneurons in the ventral column of the spinal cord,
with the major advantage of being able to make motor unit re-
cordings in vivo in human participants. The discharge of action
potentials in the muscle, or single motor unit (SMU) activ-
ity, can be recorded with an intramuscular electrode, in-
cluding from the respiratory muscles during the motor
tasks of breathing and nonrespiratory contractions with
the appropriate safety precautions (see hereinafter). By sam-
pling from large populations of motor units during motor tasks,
the output of motoneuron pools across synergistic muscles can
be compared. Here, the term motor units will be used in refer-
ence to a muscle and motoneurons in reference to a motor nu-
cleus or motoneuron pool.
The presiding principle of motor unit recruitment is Henneman’s
size principle, informed mostly by recruitment of limb motor units
(2,3). In this review, we briefly summarize the evidence for the size
principle. Then, based on our data, from recordings in the axial or
respiratory muscles, we hypothesize that the mechanics of muscles
also may govern motor unit recruitment, in other words, motor
unit recruitment by a principle of neuromechanical matching. The po-
tential mechanisms by which neural activity is matched to muscle
mechanics are discussed. Finally, we explore how motor unit re-
cruitment by neuromechanical matching may be integral to many
movements, including nonrespiratory movements. This princi-
ple of motor unit recruitment by neuromechanical matching
may explain some previously observed limitations and apparent
deviations from the size principle, especially changes in motor unit
behavior across different motor tasks.
Here, we define a motor task as the resultant movement or
intended movement (in an isometric contraction) due to ac-
tivation of motor units in one or more muscles. On the gross

157

Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
anatomical level, a muscle is defined as the collection of muscle
fibers contained between the anatomical origin and insertions
(tendons or aponeuroses). However, all muscle fibers contained
in a muscle typically are not activated simultaneously, nor is ac-
tivation of muscle fibers necessarily evenly distributed through-
out the muscle. There is regional activity of subpopulations of
muscle fibers due to activation of subpopulations of motor units
(see “Neuromechanical Matching in the Human Respiratory
Muscles” and “Neuromechanical Matching in Nonrespiratory
Muscles” sections). Therefore, the use of the term “muscle” here
does not always imply activation of all fibers and in these cir-
cumstances we have clarified this detail. The mechanics of mus-
cle action of an individual muscle can differ between tasks. By
extension, differential activation of groups of motor units
within and across synergistic muscles can result in drastically
different movements. The amount of force that a muscle and
its motor units can produce in a motor task depends on key bio-
mechanical factors such as its length-tension relation, velocity
of shortening, the muscle’s physiological cross-sectional area
and specific tension, the pennation angle of the muscle fibers,
and the moment arm of the muscle-tendon unit (see (4)). For
the respiratory muscles discussed here, the measure of their
“mechanical advantage” (see “Neuromechanical Matching in
the Human Respiratory Muscles” section) incorporates the
length-tension, pennation angle, and moment arm elements
of these biomechanical factors and respiratory effect also captures
the muscle’s physiological cross-sectional area and specific ten-
sion. Respiratory effect evaluates the contribution to pressure
(i.e., force) a respiratory muscle can produce in breathing.
MOTOR UNIT RECRUITMENT AND THE SIZE PRINCIPLE
Henneman and colleagues (2) discovered the relation be-
tween the threshold at which motoneurons discharge and their
size and the orderly recruitment of motoneurons according to
their size (or threshold that reflects the input resistance of mo-
toneurons) and termed it the size principle of motor unit recruit-
ment (for review see (3)). According to this principle, if all
motoneurons within a pool receive the same excitatory and in-
hibitory synaptic inputs, motoneurons are recruited in a system-
atic fashion that is dependent on their intrinsic properties. It
has since been shown that many properties of motoneurons or
motor units correlate with recruitment threshold such as soma
size, membrane resistance, intrinsic excitability, axonal size, ax-
onal conduction velocity, spike amplitude, twitch contraction
time, force, and fatigability (for review see (3,5)). Therefore,
during a contraction, the motoneurons of small motor units,
which produce low forces and are fatigue resistant, require less
depolarizing current and are recruited before motoneurons of
large motor units that can produce more force, but fatigue more
quickly due to glycolytic metabolism. This ensures both control
of fine movements and rapid production of force for stronger
movements and minimizes fatigue in everyday tasks requiring
low-level contractions.
Stable motor unit recruitment according to size has been
demonstrated in many circumstances (for review see (3,5,6)).
As most physiological systems have an inherent level of noise,
stable is taken to mean the same motor unit recruitment order
for at least 80% of motor units in a contraction or the same mo-
tor unit recruitment order in at least 80% of contractions. For
example, in cats, for motoneuron pairs recorded from L7 and
158 Exercise and Sport Sciences Reviews
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
S1 roots in response to stimulation of supraspinal centers, the
smallest cell is recruited before the larger cell ~ 90% of the time
(7). In voluntary isometric contractions of first dorsal interosseous
(FDI) muscle in humans, the linear correlation coefficient be-
tween twitch tension (i.e., motor unit size) and threshold force
at which motor units are recruited is greater than 0.8, but not all
data points fall on the line of identity (8). It was subsequently
noted that although orderly size-related recruitment occurs
in isometric contractions for intrinsic hand muscles FDI
and abductor pollicis brevis, only about a third of motor unit
pairs were always recruited in order (as predicted by their rel-
ative twitch amplitudes) in dynamic contractions (rhythmic
scissoring movement) (9,10).
Given such examples of altered motor unit recruitment in
different types of contractions or tasks, within the context of
the anatomical and functional complexities of skeletal muscles,
Loeb and colleagues (11,12) conceived the idea of the task
group, that is a set of motor units recruited in an ordered manner
for a particular task or motor behavior. It was thought that the
exact motor units recruited may vary between different tasks,
but there is still orderly recruitment of the motor units accord-
ing to their size in a particular task group. For example, task
groups of motor units are observed in the biceps femoris in the
cat for hip extension and knee flexion (12), in the biceps
brachii in humans for flexion and supination (13,14), in exten-
sor digitorum to extend different digits (15), and in the abdom-
inal muscles for respiratory and nonrespiratory tasks (16).
Just as one muscle produces force in more than one direction,
many muscles can contribute to force production in a given di-
rection. Cope and Sokoloff (6) proposed that the idea of motor
unit task groups should be extended such that they contain mo-
tor units from more than one muscle. Therefore, when more
than one muscle can contribute to force generation in a partic-
ular direction, motor units recruitment is coordinated across
muscles, and such that there is an ensemble-based scheme of mo-
tor unit recruitment rather than a “muscle-based” scheme (6).
This seems to be the case in the decerebrate cat as, for motor
unit pairs in medial and lateral gastrocnemii, motoneurons with
slower conduction velocities are recruited before those with
higher conduction velocities (17). Thus, as for task groups
within a muscle, recruitment by Henneman’s size principle
across muscles would ensure coordinated recruitment of motor
units that would result in smooth, graded increases in force.
Relevant to this review, motor units in the diaphragm are re-
cruited in a relatively stable order within repeated voluntary
breaths of different sizes and rates (18). Furthermore, based on
the size of motor unit action potentials at a given recording site
using a monopolar needle electrode (exposed tip of 0.15 mm2),
small diaphragmatic motor units are recruited before larger units
in a voluntary breath (see Fig. 1 in (18)). However, during vol-
untary breaths at fast flows (i.e., double the flow in quiet breath-
ing) or when the input to the motoneurons changes, such as
from the motor cortex in slow voluntary breaths to the medul-
lary respiratory centers in automatic breaths, motor unit recruit-
ment order is altered for two in every four motor units in the
population (18), suggesting some nonuniformity in the distribu-
tion of descending drives to the phrenic motoneurons. As for
the diaphragm, the recruitment order in the human parasternal
intercostal muscles also is relatively stable in quiet breathing,
but altered for one to two in every four motor units during
www.acsm-essr.org
Figure 1. Differential activity in the human inspiratory muscles during quiet breathing. A. Schematic of the human inspiratory muscles. The majority of the
muscles shown are obligatory, active in every breath, but the sternomastoid is active only in large breaths. Pale colors are used for more superficial muscles
and darker colors for deeper muscles. Panels (B), (C), and (D) depict the graded patterns of inspiratory muscle activity that have been demonstrated in humans.
Relative muscle activation during breathing is indicated by the reference color scale, with greatest activation in warm colors and less activity in cooler colors. For
example, the muscles shown in purple (e.g., third ventral external intercostal and sternomastoid) are only active in larger breaths. There are rostrocaudal gradients
in the parasternal intercostal muscles from the first-to-fifth interspaces (panel B) and the external intercostal muscles from the third, fifth, and seventh interspaces
(panel C). There also is a dostroventral gradient of activity in the external intercostal muscles in the third interspace (panel D). For the inspiratory muscles in the
neck (panels B and D), the scalene muscles are active in every breath, but the sternomastoid is only active in larger breaths.

voluntary hyperventilation (19), although only 31 units were
sampled in the parasternal intercostals compared with 60 motor
units in the diaphragm (18).
One assumption of the size principle is that synaptic input or
drive is distributed equally to all the motoneurons within a par-
ticular pool. However, modeling experiments have highlighted
the role of synaptic input in differential recruitment of moto-
neurons. Kernell and Hultborn (20) showed that changes in
recruitment gain could be achieved only if the distribution of
synaptic input was differential across the motoneuron pool.
Recruitment gain is defined as the number of motoneurons
recruited for a given synaptic input (20). An increase in re-
cruitment gain reduces the range of activation thresholds for
motoneurons as more motoneurons are recruited by the same
synaptic input. When the model assumed that synaptic input
was equally distributed, it was possible to change motoneuron
recruitment thresholds but not recruitment gain (20).
Uneven distribution of synaptic input or drive across moto-
neuron pools may account for some of the variability in motor
unit recruitment order that has been described when the muscle
contracts in a different manner (e.g., dynamically) or the con-
traction requires selective activation of units, in other words,
a task group. The uneven distribution of synaptic inputs may
result from descending, afferent or propriospinal inputs to
motoneurons, and here, we argue these inputs may be orga-
nized to ensure recruitment of motor units depending on their
relative mechanics for the motor task.
NEUROMECHANICAL MATCHING IN THE HUMAN
RESPIRATORY MUSCLES
Motor units from many muscles are recruited during inspira-
tion to generate negative pleural pressure (see Fig. 1; for review
see (21)). Compared with other skeletal muscles, the respiratory
motoneurons are automatically and rhythmically depolarized by
descending neural drive that originates in the respiratory cen-
ters in the ponto-medullary region of the brain (22). However,
respiratory muscles also can be activated volitionally, in both
respiratory (i.e., large breaths) and nonrespiratory (i.e., trunk
movements) tasks, and consequently their motoneurons also re-
ceive neural drive from higher brain areas including the motor
cortex (for review see (22)). These drives depolarize the same
motoneurons, and current evidence suggests that the integra-
tion of drives occurs at the spinal cord, rather than at the brain
stem (22). Irrespective of whether volitional drive bypasses the
medulla or not, the output of the final common path, the mo-
toneurons, can be assessed by SMU discharge.
For the motor task of breathing, SMU recordings have re-
vealed that the output of the various human inspiratory

Volume 47 • Number 3 • July 2019 Motor Units and Neuromechanical Matching 159

Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
synergist muscles is not uniform with differential motor unit ac-
tivity across five pump muscles in terms of the timing and am-
plitude of inspiratory activity (for review see (22,23)). Within
the intercostal muscles, the timing and amplitude of motor unit
activity varies across interspaces, but also between different re-
gions of a muscle in an interspace ((24,25); see Fig. 1). For ex-
ample, motor units in the dorsal region of the external
intercostal muscle in the third interspace contract earlier in in-
spiration and discharge at a faster rate compared with motor
units in the ventral region of the same interspace innervated
by the same motoneurons pool (25). Anatomically, the dorsal
and ventral regions of the external intercostal muscle may be
considered a single muscle, based on data from dogs that dem-
onstrate motoneurons from different regions of an intercostal
space are colocated in the ventral horn (26). Despite this, the
delay in recruitment between the dorsal and ventral regions is
~1 s, far longer than any difference due to transmission of neural
signals along the intercostal nerve. Inspiratory motor unit activ-
ity is similar in the medial and lateral portions of the second hu-
man parasternal intercostal muscle, suggesting no regional
difference in activation along an interspace for this muscle (24).
These rostrocaudal and dorsoventral gradients of motor unit
output in the human intercostal muscles are remarkable because
they correlate with the mechanics of these muscles for the motor
task of inspiration, in other words with inspiratory mechanical ad-
vantage (Fig. 2). Stemming from theoretical and experimental
work in dogs and humans by De Troyer and colleagues, the inspi-
ratory mechanical advantage of many human respiratory muscles
has been computed (for review see (28)). In brief, for the respira-
tory muscles, mechanical advantage is computed as the relative
change in muscle length during passive inflation of the lungs
(i.e., %/l). It is a surrogate measure for the respiratory effect of a

Figure 2. Neuromechanical matching in the human intercostal muscles. A. Time and frequency plots reveal a rostrocaudal gradient of activity in the
parasternal intercostal muscles during quiet breathing. Each horizontal line represents data from one motor unit recorded in the first, third, and fifth interspaces
in five healthy male participants. The onset and end of inspiration are shown by vertical dashed lines (from 0% to 100%) of inspiratory time (horizontal axis). Thin
horizontal lines at the bottom of each plot indicate those units that discharged tonically. The thick horizontal lines show the time that the discharge frequency in-
creased during inspiration. Discharge frequency is coded by color (shown in inset). The color of thick lines shows the peak firing frequency, and the smaller circles
at the start and end show the frequencies at recruitment and derecruitment, respectively. The large black circles show the time at which the peak frequency occurred.
The ascending unbroken white line in each panel represents the onset time of the multiunit electromyography (EMG) ordered by onset time (see (27)). The onset of
activity is earlier and the peak discharge rate of the motor units is higher in the rostral first interspace compared with caudal third and fifth spaces. B. Using single
motor unit (SMU) recordings to estimate neural drive to the parasternal intercostal muscles in different interspaces, we first demonstrated that the rostrocaudal gra-
dient of activity across the five interspaces (black circles) is tightly coupled to the inspiratory mechanical advantage of the same regions of muscles (24). We have
replicated the results that there is neuromechanical matching in the human parasternal intercostal muscles during quiet breathing (gray circles) and demonstrated
that the matching is maintained in targeted voluntary breaths (white circles) (data from (27)). The lines are colored to indicate the rostrocaudal gradient, with warm-
to-cold gradient representing a decrease in both neural activity and inspiratory mechanical advantage. All correlations have r-squared values of 0.99 or greater.

160 Exercise and Sport Sciences Reviews www.acsm-essr.org

Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
muscle, which is defined as the change in airway pressure gener-
ated by the muscle if it were active in isolation. Given isolated
muscle contraction is not possible in human participants, the
inspiratory mechanical advantage and respiratory effect of the
human respiratory muscles is estimated using computed tomog-
raphy and measurements from cadavers (28). With passive lung
inflation, a muscle that shortens more has a greater inspira-
tory mechanical advantage, also meaning it has a greater respi-
ratory effect; in other words, it can evoke a greater change in
airway opening pressure.
By comparison of measures of inspiratory mechanical advan-
tage for different regions of the human intercostal muscles with
an estimate of neural drive (i.e., number of motor unit spikes
during inspiration from our SMU data) to the pools of moto-
neurons that innervate these regions of muscle, we discovered
a strong linear relationship between neural drive and mechani-
cal advantage, in other words neuromechanical matching (see also
(29)). This occurs for both the external intercostal and parasternal
intercostal muscles during quiet breathing (24,25) and the
parasternal intercostal muscles during voluntary breaths (27).
Motor unit recruitment by neuromechanical matching reduces
the metabolic cost of muscle activation (28), thus providing an
efficient strategy for ventilation. Figure 2 highlights replication
of our finding that the neural drive to the human parasternal inter-
costal muscles during quiet breathing is tightly coupled to inspira-
tory mechanical advantage ((24,27) see also (30)). In addition to
the intercostal muscles, we also have demonstrated that the hu-
man scalene and sternocleidomastoid muscles in the neck, obliga-
tory and accessory muscles of inspiration, respectively (see Fig. 1),
also are active according to their relative mechanical advantages
for inspiration in large inspiratory efforts (31).
Respiratory muscles are multifunctional and are active in
other motor tasks that have different mechanical requirements.
For example, the parasternal intercostals elevate the ribs verti-
cally in quiet breathing, but translate the ribs laterally in trunk
rotation. By direct comparison of the motor unit activity, we
have recently shown that the differential activation of the
parasternal intercostals across interspaces for inspiration is effec-
tively reversed for the different motor task of trunk rotation
((30); Fig. 3). These changes in motor unit behavior do not re-
flect noise in motoneuron recruitment by a size-related principle
of recruitment. Based on data for muscle shortening in dogs and
rib and muscle fiber angulation in humans, there is a strong case
that these changes in motor unit activity match the mechanical
advantage of the muscles in the different tasks (30). Thus,
neuromechanical matching in the human respiratory muscles
adapts across tasks and, as proposed for the graded output in
breathing, may be due to neural organization in the spinal cord
((30); see “Mechanisms of Neuromechanical Matching in the
Respiratory Muscles” section). Altered neural drive to the in-
spiratory muscles in rotation compared with breathing does
not occur for all obligatory inspiratory muscles. The parasternal
intercostal muscles show strong activity in rotations to the ipsi-
lateral side (30,32), whereas the diaphragm shows minimal ac-
tivity in similar rotations (see (23)). This suggests that the
observed behavior of motor unit output to the parasternal inter-
costal muscles in our recent study (30) is related to task-specific
muscle function, rather than a widespread phenomenon among
the inspiratory muscles. Although the observed changes in mo-
tor unit output between tasks occurred across muscles that are
Volume 47 • Number 3 • July 2019
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
anatomically distinct, this is evidence for a change in the
timing of excitatory inputs to these motoneurons and not just
recruitment according to motoneuron size.
Is neuromechanical matching in the respiratory muscles
during breathing adaptable? Given their position in the
quasi-rigid three-dimensional ribcage, most respiratory muscles
are relatively impervious to acute changes in their mechanics
as it is difficult to manipulate the bones onto which they origi-
nate or insert. Thus, we used an acute change in body posture,
to an upside-down posture, to elicit changes in respiratory mus-
cle mechanics (33). A change in the gravitational vector in the
upside-down posture changes the mechanics of the respiratory
system (i.e., chest wall, lung, and respiratory muscles) compared
with that in standing. The inspiratory activity in two inspiratory
muscles, scalenes and diaphragm, was affected differentially dur-
ing quiet breathing in an upside-down posture. There was di-
minished activity in the scalenes compared with standing, but
activity in the diaphragm was unaltered (33). Although the me-
chanics of the muscles were not quantified, we interpreted the
decrease in scalene activity as an adaptation to the change in
the mechanical advantage of the muscle given the reduced
requirement of the scalenes to elevate the ribcage in an upside-
down posture (33). Thus, motor unit recruitment in the respira-
tory muscles is adaptable across tasks when the mechanics of the
muscles change (i.e., breathing vs rotation), or within a task
when the mechanics of the muscles change (i.e., breathing in
the upright vs upside-down postures).
MECHANISMS OF NEUROMECHANICAL MATCHING IN
THE RESPIRATORY MUSCLES
The mechanism responsible for the differential distribution
of neural drive to the inspiratory muscles has been investigated
mainly in the canine intercostal muscles where similar gradients
of inspiratory mechanical advantage and matched neural activ-
ity are observed (for review see (28)). However, complementary
observations from other animal preparations are discussed
where relevant or where data in humans or dogs are lacking.
As for other skeletal muscles, if we assume that respiratory
motor units are recruited in a systematic fashion due to the “size
principle” only (see “Motor Unit Recruitment and the Size
Principle” section), then the differential activity observed in
the intercostal muscles will be reflected by differences in the in-
trinsic properties of the motoneurons that innervate these mus-
cles. Fiber-type composition is a good indicator of motoneuron
properties as slow-twitch oxidative (SO) fibers are generally in-
nervated by small, low-threshold motoneurons, and fast-twitch
oxidative-glycolytic (FOG) and fast-twitch glycolytic fibers are
supplied by large higher-threshold motoneurons (for review see
(3)). However, the proportions of muscle fiber type do not differ
between human external intercostal muscles for SO fibers
(60%–65% SO fibers) (see (25)), or either between or within
parasternal intercostals in dogs (~60% SO and 40% FOG fi-
bers) (for review see (28)). In addition, the somal surface area
and volume of motoneurons innervating the canine parasternal
intercostal muscles does not differ between different inter-
spaces, or between medial and lateral portions of the parasternal
intercostal muscles (26). The motoneurons that innervate me-
dial and lateral motor units are colocated in the ventral horn in
dogs (26), as are motoneurons that innervate the different layers
of intercostal muscle in any given interspace in cats (34),
Motor Units and Neuromechanical Matching 161
Figure 3. Adaptability of parasternal intercostal motor unit recruitment in different motor tasks. Recruitment of parasternal intercostal motor units in the first
(black bars), second (gray), and fourth (white) spaces during quiet breathing (left panel) and rotation (right panel). Median values for each interspace are shown
on each histogram by arrows above the histograms. For quiet breathing (panel A), motor unit recruitment is indicated relative to inspiratory time during record-
ings, and for rotation (panel B), motor unit recruitment is indicated relative to torque of maximal voluntary rotation contractions (% MVC). In quiet breathing,
motor units from the first and second interspaces are recruited early in the breath, before those from the fourth space. The graded neural activity of human
parasternal intercostal muscles during quiet breathing is matched to the known mechanics of these muscles for inspiration. This pattern is effectively reversed
in rotation as motor units in the first interspace are recruited late in rotation, compared with the second and fourth spaces. PSIC, parasternal intercostal.

suggesting that there is not task-dependent topographical orga-
nization in intercostal motoneuron pools. In the cat, the propor-
tion of fiber types does vary along a rostrocaudal gradient in the
external intercostal muscles, with a greater proportion of SO fi-
bers in the rostral interspaces (in the regions where the muscles
have greater inspiratory activity), but again, there is no differ-
ence in the distribution of fiber type in different parasternal in-
tercostals (35). Therefore, the distribution of activity in the
intercostal muscles is not likely to be solely determined by an in-
trinsic, size-related property of the motoneurons. Although the
quiet breathing and trunk rotation tasks where neuromechanical
matching has been observed (see “Neuromechanical Matching
in the Human Respiratory Muscles” section) are low-force tasks,
reversed recruitment across spinal levels of the same motor units
(30) provides strong evidence against motor unit recruitment
exclusively by motoneuron size.
The role of afferent input has been assessed by section of ei-
ther the phrenic nerves or thoracic dorsal roots in spontane-
ously breathing dogs. Removal of feedback does not alter the
rostrocaudal pattern of activity in the parasternal intercostal
muscles (for review see (23)). With support from our finding
in humans that the typical activation of the scalenes and ster-
nocleidomastoid muscles according to their relative inspiratory
mechanical advantages was not altered with changes in lung
volume (i.e., when feedback from the lungs and inspiratory
muscles would differ) (31), on-going peripheral feedback plays
a minimal role for the usual differential recruitment of inspira-
tory muscles in breathing. Although not implicated in the pat-
tern of activation of inspiratory muscles in breathing, afferent
feedback may be critical to changes in inspiratory muscle activity
when the task or mechanics of the muscles change. In nonres-
piratory muscles, for example, cutaneous afferent stimulation
can affect differentially slow- and fast-twitch motor units in the
cat (36) or modify motor unit behavior in humans compared
with size-related recruitment in voluntary contractions without
cutaneous stimulation (37,38). Regarding descending drive to
the respiratory motoneurons, the strength of bulbospinal connec-
tions to different intercostal motoneurons at different spinal
levels does not differ (28,39). Thus, the differential motoneuron
output along a rostrocaudal gradient in breathing does not seem
to depend on differential input from respiratory centers. Of
course, motoneuron gain may vary across the intercostal spaces,
but as discussed hereinafter, evidence of neuromodulation for in-
spiratory intercostal motoneurons output is lacking.
Alternatively, a mechanism at the spinal cord that sculpts
the descending drive to the motoneurons may generate the to-
pographic distribution of drive to intercostal muscles. This
would provide motor unit recruitment by neuromechanical
matching during both automatic and voluntary breaths with
descending drive from bulbospinal and corticospinal projec-
tions, respectively, but also allow adaptability of motor unit
output in different motor tasks (see Fig. 3). DiMarco and
Kowalski (40) have shown that the usual pattern of output
from canine intercostal motoneurons (i.e., graded activity be-
tween and within an interspace during spontaneous breathing)
can be reproduced using high-frequency spinal cord stimula-
tion over the ventral spinal cord at thoracic level T2. As these
dogs also had a complete spinal section at the cervical level C2
(albeit in an acute preparation, see (41)), these data suggest
that mechanisms within the spinal cord can produce the usual
pattern of inspiratory output from the intercostal motoneurons
according to the relative mechanics of the muscles (28), at
least in the dog. Consistent with this is the preservation of
the rostrocaudal gradient of the parasternal intercostal motor

162 Exercise and Sport Sciences Reviews www.acsm-essr.org

Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
unit output in quiet breaths and matched voluntary breaths in
human participants (27).
What might this spinal mechanism be? We previously postu-
lated a role for “spinal distribution networks” of propriospinal, seg-
mental, and intersegmental neurons that distribute neural drive to
the different inspiratory motoneuron pools in different motor tasks
(22; see Fig. 4). In animals, there is increasing evidence for spinal
interneurons that contribute to respiratory motoneuron output
(for review see (42)). These data also show that respiratory inter-
neurons project between spinal segments and to the contralateral
ventral horn. Thus, it is likely that there is a type of propriospinal
system for phrenic and intercostal motoneurons (22,30,40) as
there is for forelimb motoneurons in tasks such as reaching that re-
quire coordinated activity across multiple muscles.
Synaptic inputs to respiratory motoneurons from central re-
spiratory centers or spinal interneurons also may be modulated
by mechanisms that alter the gain of the motoneurons. Active
dendritic mechanisms involving persistent inward currents or
ligand-gated channel-mediated synaptic inputs may amplify
synaptic signals in some motoneurons (for review see (1)). For
phrenic motoneurons, the amplification of synaptic excitation
from central respiratory drive potentials occurs via ligand-
mediated mechanisms (NMDA), but expiratory motoneurons
in the thoracic region (that presumably innervate the expira-
tory intercostal muscles) show persistent inward currents in de-
cerebrate cats (43). It is not known if inspiratory motoneurons
in the thoracic region (i.e., that innervate the inspiratory inter-
costal muscles where regional differences in electromyography
(EMG) are observed) have persistent inward currents like their
expiratory counterparts. Regional differences in the density of
serotonergic inputs to canine parasternal intercostal motoneu-
rons occur mediolaterally, but not rostrocaudally (26), and the
topographic distribution of inspiratory activity in this muscle oc-
curs along both gradients (for review see (28)). Replication in
the varied density of serotonergic input to motoneurons that in-
nervate the medial and lateral canine parasternal intercostal
muscles only would confirm that other excitatory inputs or
other mechanisms may generate the regional differences in
EMG, at least along the rostrocaudal gradient.
If descending neuromodulation is important for intercostal
motoneurons output, this would be another spinal mechanism,
in addition to spinal distribution networks of interneurons, by
which inspiratory output of different “task groups” of motor
units is sculpted to match the inspiratory mechanical advantages
of the muscles for breathing (Fig. 4). Furthermore, it may provide
a mechanism that adapts neuromechanical matching in the respi-
ratory muscles across motor tasks, as it has been postulated that
neuromodulation allows motoneurons to have different states for
different functions or tasks (e.g., postural, voluntary, and oscilla-
tory behaviors) (1). However, without evidence for neuromod-
ulation in inspiratory intercostal motoneurons, this potential
mechanism for neuromechanical matching remains unproven.
NEUROMECHANICAL MATCHING IN
NONRESPIRATORY MUSCLES
The respiratory muscles are skeletal muscles like those of the
limbs and trunk. Therefore, perhaps unsurprisingly, neuro-
mechanical matching also may operate in other skeletal mus-
cles. Limb muscles also provide a model in which to investigate
further the adaptability of neuromechanical matching.
Volume 47 • Number 3 • July 2019
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
In the human triceps surae muscle group, recruitment of mo-
tor units in medial gastrocnemius (MG) is delayed when the
knee is flexed, such that the plantar flexion torque and level of
soleus EMG at which they are recruited are significantly greater
compared with when the knee is extended (44). This was pro-
posed to reflect a reduction in the force-producing capability of
MG to plantar flexion torque with the knee flexed, although
the mechanical properties of the muscles were not measured.
However, based on the methodology to assess the mechanical
advantage of the respiratory muscles (see “Neuromechanical
Matching in the Human Respiratory Muscles” section), the rel-
ative contribution of a limb muscle to torque around a joint
could be assessed by the fractional change in muscle length/
joint angle for a passive movement around a joint. Kawakami
and colleagues (45) measured the change in muscle fascicle
length of the soleus and gastrocnemii muscles over a range of
knee and ankle angles in the passive condition. For MG, the
mechanical advantage for plantar flexion is 0.42 mm per degree
when the knee is fully extended, but only 0.13 mm per degree
with the knee flexed at 90 degrees. In contrast, with a change
in knee angle from 0 to 90 degrees, the change in mechanical
advantage of soleus is unchanged. These differences are consis-
tent with the relative change in force contribution and activity
of gastrocnemius and soleus during plantar flexion with a
change in knee angle (44) and thus fit with motor unit recruit-
ment by neuromechanical matching (Fig. 5).
For the upper limb, we have demonstrated coupling between
the neural and mechanical behavior for synergist muscles (FDI
and long finger flexors) for flexion of the index finger (4). Fur-
thermore, this matching is adaptable. If the moment arm of FDI
for index finger flexion is acutely increased (indicated by ultra-
sound) thereby increasing flexion twitch force (evoked by ulnar
nerve stimulation), the proportion of neural drive to this mus-
cle increases (4).
Although the changes in motor unit recruitment are not
specifically linked to known changes in the contribution of
a muscle at a joint (i.e., its mechanical advantage or mechanical
effectiveness), many studies have suggested that some motor
units or muscles are recruited in relation to their direction
of pull or contribution to force for limb (e.g., (13,46,47))
and axial (e.g., (48–50)) muscles. Therefore, recruitment of
motor units by neuromechanical matching may explain di-
vergence from recruitment purely based on the size-principle
in some nonrespiratory muscles, particularly in studies that
observed altered motor unit recruitment across motor tasks.
Our proposed principle of motor unit recruitment comple-
ments that of the size principle and provides a central mech-
anism to produce efficient voluntary movements.
RECONCILIATION BETWEEN NEUROMECHANICAL
MATCHING AND THE SIZE PRINCIPLES OF MOTOR
UNIT RECRUITMENT
From its inception, Henneman’s size principle provided a hy-
pothesis by which the recruitment of motor units in most con-
tractions could be explained, even for task groups of motor
units within a muscle (11) or ensemble-based task groups across
muscles (6). Although orderly recruitment of motor units across
muscles by the size principle would result in smooth gradation of
force, it has been noted previously that a fixed order of motor unit
recruitment would limit the muscle to perform only tasks that
Motor Units and Neuromechanical Matching 163
Figure 4. Recruitment of motoneurons by neuromechanical matching. A. Diagrammatic representation of the proposed spinal distribution networks that dis-
tribute neural drive to the intercostal motoneurons depending on task and the mechanical advantage of the muscles for those tasks. Motoneuronal (MN) pools in
the first, second, and fourth thoracic spinal levels and the corresponding muscle fibers in the first, second, and fourth parasternal intercostal muscles are depicted.
The angulation of the muscle fibers varies along a rostrocaudal gradient (see (30)). Spinal distribution networks of propriospinal, segmental, and intersegmental
neurons are depicted as a column of cells ipsilateral to the motoneurons, but some of these neurons may have their cell bodies in the contralateral side of the
spinal cord. As for the motoneurons, the spinal distribution network neurons vary in their intrinsic properties (e.g., somal size) and also may be influenced by
changes in their biophysical properties by neuromodulation (see text). Given the size-related intrinsic properties of motor units in the parasternal intercostal mus-
cles is similar between interspaces (see text), if motor unit recruitment was governed by the size principle alone, the onset and amplitude of inspiratory activity
during quiet breathing or trunk rotation would be similar in the first, second, and fourth parasternal intercostal muscles (depicted by the same red color of the
muscles in the ribcage, panel B), but this is not the case. For panels B, C, and D, the reference color scale for relative muscle activation is shown on the bottom left
of the figure. Shown in purple (panel A) is the spinal distribution network for inspiration that sculpts descending drive from the bulbospinal pathways during
automatic breathing and from the corticospinal (CS) pathways during voluntary breaths. Spinal distribution networks for inspiration on both sides of the spinal
cord receive similar input as bulbospinal projections are largely bilateral. When activated via the inspiratory spinal distribution networks, the relative input to the
parasternal intercostal motoneurons is distributed along a rostrocaudal gradient with earlier and greater activity in the first and second interspaces compared with
the fourth space (24,30). This graded activity (depicted by the color of the muscles in the ribcage and purple arrow, panel C) is matched to the relative mechanical
advantage of these interspaces for inspiration, that is, neuromechanical matching. The graded output persists during voluntary breaths in humans (27) and dur-
ing high-frequency stimulation of the thoracic spinal cord in dogs with an acute C2 spinal section (indicated by the dashed line) (40). Shown in blue (panel A) is
the spinal distribution network for another motor task, voluntary trunk rotation, which sculpts descending drive via CS pathways. During rotation, the relative
input to the same parasternal intercostal motoneurons by the rotation spinal distribution network is depicted to be different to that distributed by the inspiratory
spinal distribution network as the output of the motor units is effectively reversed compared with that in inspiration (30). During trunk rotation, there is delayed
recruitment of motor units in the first interspace compared with the second and fourth spaces (depicted by the color of the muscles and blue arrow, panel D). The
output is matched to the predicted mechanical advantage of these muscles (see (30)). Given neuromechanical matching is adaptable (e.g., altered inspiratory
muscle output with changes in posture (33)), the proposed spinal distribution networks are responsive to afferent inputs and other descending drive (e.g., from
vestibular system), indicated by the pink arrows (panel A). BS, bulbospinal; CS, corticospinal; PSIC, parasternal intercostal.

164 Exercise and Sport Sciences Reviews www.acsm-essr.org

Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
Figure 5. Example of neuromechanical matching in the triceps surae muscles for plantar flexion contractions. A. Participants performed plantar flexion torque
contractions (ankle angle, 90 degrees) in two positions: knee extended (knee angle, 0 degrees) and knee flexed (knee angle, 90 degrees) designed to alter medial
gastrocnemius (MG) muscle length but not soleus muscle length. Using data from Kawakami et al. (45) to estimate the mechanical advantage (mech adv) of these
muscles during plantar flexion contractions (see text), the change in knee angle from 0 (extended) to 90 degrees (flexed) would decrease the mechanical advantage
of the MG significantly (by 0.29 mm per degree), but have little effect on that of soleus (0.02 mm per degree). B. Motor units were recorded from MG (bottom panel)
during ramped plantar flexion contractions in the knee extended and knee flexed positions. Intramuscular soleus electromyography (EMG) (top panel) and plantar
flexion torque (middle panel) also are shown. Compared with the onset of torque (indicated by “A”), the level of soleus EMG and torque at which an MG motor unit
was recruited (indicated by “B”) was delayed in the knee flexed position compared with knee extended position (indicated by the greater A-to-B delay shaded in gray
in the right panel). C. Group data for soleus EMG and plantar flexion torque at which MG motor units were recruited in the knee extended (black circles) and knee flexed
(white circles) positions. With the knee flexed, the soleus EMG and torque at which MG units were recruited was significantly greater, likely due to the reduced mechan-
ical advantage of MG in this flexed position. rec, recruitment; SOL, soleus. [Adapted from (44). Copyright © 2000 Springer Nature. Used with permission. Adaptations are
themselves works protected by copyright. In order to publish this adaptation, authorization must be obtained both from the owner of the copyright in the original work
and from the owner of copyright in the translation or adaptation.]

Volume 47 • Number 3 • July 2019 Motor Units and Neuromechanical Matching 165

Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
depended on graded motor unit force (51). As such, Cope and
Sokoloff (6) proposed a selection process, by which the appropriate
motor units, in other words, those that generate force in the de-
sired direction, have to be selected for use and are then recruited
by their size-related properties. We are not the first to observe
changes in the motor unit behavior with different tasks, but our
work in human respiratory muscles provides direct evidence for a
mechanism that matches neural output to the relative mechanics
of muscles (or regions of muscles) for different movements.
The size principle relies on the assumption that synaptic in-
put is distributed equally to all the motoneurons within a partic-
ular pool. As described previously, historical data and our data
from respiratory muscles that demonstrate divergence from mo-
toneuron recruitment according to their size-related properties
(e.g., in different contraction types or motor tasks) highlight
the importance of this assumption when testing the size princi-
ple because inputs to motoneurons may change in these circum-
stances. Our recent finding of varied recruitment behavior in
the same parasternal intercostal motor units when the task
changed (30) shows that the differential synaptic input is more
important than the size-related properties of the motor units for
recruitment according to the principle of neuromechanical
matching. This mechanism is likely to occur at the spinal cord
and involves changes in synaptic input that select the units
based on their mechanical advantage for the task. How might
this occur and how widespread is it?
The spinal mechanisms postulated for the respiratory muscles
(i.e., spinal distribution network of interneurons) are applicable
to any skeletal muscle where motor unit recruitment by neuro-
mechanical matching may occur. These interneurons may in-
clude afferent connections between the muscle and spinal
cord, which are localized to a particular segment or neuromus-
cular compartment of the muscle (i.e., akin to task groups for ef-
ferent control). This was termed reflex partitioning and provides
a potential mechanism for fine control of activity within a task
group (see (52)). However, it does not operate in the human
tibialis anterior muscle at least for low-threshold motoneurons
(52). McKeon and colleagues (52) suggested reflex partitioning
may be related to “muscle architecture and function” and not
applicable to “simple muscles with single physiological functions”
(cf. (53) in vastus medialis). The presence of any reflex par-
titioning may correspond to the presence of motor unit compart-
ments or small motor unit territories for regional activation of
muscle fibers. Motor unit compartments are absent in the MG,
a muscle with single distal and proximal tendons (54), but pres-
ent in muscles with more complex anatomy and broad muscle or-
igins such as axial and trunk muscles (e.g., (25,48)). In this
respect, muscle architecture and function may dictate the bal-
ance between the neuromechanical matching and size principles
of motor unit recruitment. Muscles with large motor unit terri-
tories and muscles that transmit their force through discrete ori-
gin and insertions (i.e., single, long tendons) are instances where
motor unit recruitment by neuromechanical matching may not
occur. As described by Heroux and colleagues (54) for MG:
“In the absence of a separate bony attachment that
would confer a mechanical advantage to muscle fi-
bres in the proximal (knee flexion) or distal (ankle
plantar flexion) portion of the MG muscle, there
is no benefit for [motor units] with small spatial
166 Exercise and Sport Sciences Reviews
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
territories to be grouped in close proximity to either
joint given that [motor unit] activity will generate
tension at the proximal and distal muscle insertions.”
CONCLUSIONS
A principle of neuromechanical matching for motor unit re-
cruitment in human movement is significant to the fields of ex-
ercise science and sports medicine. For example, physiological
studies that measure motor unit output in movements (e.g., lo-
comotion) must now consider mechanisms beyond the size
principle. This new principle will improve our understanding
of the mechanisms behind altered movement control (e.g.,
with motor impairments or injury) and the improvements that
can be realized with training. Furthermore, uptake of this con-
cept by the exercise science and sports medicine fields will ex-
pedite answers to outstanding research and clinical questions,
some of which are noted hereinafter.
The adaptability of neuromechanical matching described
previously is for acute changes in the mechanics of muscles.
How the coupling of neural and mechanical behavior is altered
by chronic changes to muscle mechanics in motor impairments
is not known. If damage to spinal distribution networks occurs,
then neuromechanical matching may be impaired. Similarly, if
neuromechanical matching is disrupted because of injury or dis-
eases that alter biomechanics or skeletal muscle function, then
optimization of neuromechanical matching may provide a tar-
get for physiotherapy or therapeutic biofeedback.
To test neuromechanical matching in all skeletal muscles, the
methodology to measure muscle mechanics is required. Given
the amount of force a muscle can produce in any motor task de-
pends on several key factors; studies that use physiological cross-
sectional area alone to infer the mechanics of a muscle should be
interpreted with caution as the mechanics of a muscle may vary
independently to physiological cross-sectional area. For example,
the moment arm of a muscle can change with different postures
of the structure into which the muscle inserts (see (4)). Although
the techniques to measure mechanical advantage or mechanical
effectiveness for the respiratory muscles are established, current
methodology uses computed tomography scans (28). There is a
need for a method to make comparable measures of respiratory
mechanical advantage using safer and cheaper technologies such
as ultrasound. Ideally, these methods can then be applied to as-
sess mechanical advantage in the respiratory muscles during tasks
other than breathing and in postures other than supine, and in
various motor tasks for nonrespiratory muscles. The typical con-
traction of the respiratory muscles (i.e., during quiet breathing) is
orchestrated — a cyclical contraction from the same muscle
length (at end expiratory lung volume) at a comparable ex-
tent and contraction velocity. Therefore, factors such as the
velocity of the contraction that has been shown to affect mo-
tor unit recruitment (e.g., (18,55)) and contraction history
(e.g., (51)) that may affect the force a muscle can generate
in a contraction will need to be considered and explored in
the application of the principle of neuromechanical matching
to nonrespiratory muscles.
Acknowledgments
A.L.H. was supported by a Lung Foundation Australia/Boehringer Ingelheim
COPD Research Fellowship; S.C.G. and J.E.B. were supported by the NHMRC
(Australia).
www.acsm-essr.org
References
1. Johnson MD, Thompson CK, Tysseling VM, Powers RK, Heckman CJ.
The potential for understanding the synaptic organization of human motor
commands via the firing patterns of motoneurons. J. Neurophysiol. 2017;
118:520–31.
2. Henneman E. Relation between size of neurons and their susceptibility to
discharge. Science. 1957; 126:1345–7.
3. Henneman E, Mendell LM. Functional organisation of motoneuron
pool and its inputs. In: Brookhart JM, Mountcastle VB, editors. Hand-
book of Physiology, Section 1, The Nervous System. Volume 2, Motor Con-
trol, part 1. Volume 2. Bethesda (MD): American Physiological Society;
1981. p. 423–508.
4. Hudson AL, Taylor JL, Gandevia SC, Butler JE. Coupling between me-
chanical and neural behaviour in the human first dorsal interosseous
muscle. J. Physiol. 2009; 587:917–25.
5. Binder MD, Heckman CJ, Powers RK. The physiological control of mo-
toneuron activity. In: Rowell LB, Shepherd JT, editors. Handbook of
Physiology, Section 12, Exercise: Regulation and Integration of Multiple Systems.
Bethesda (MD): American Physiological Society; 1996. p. 3–53.
6. Cope TC, Sokoloff AJ. Orderly recruitment among motoneurons supplying
different muscles. J. Physiol. Paris. 1999; 93:81–5.
7. Somjen G, Carpenter DO, Henneman E. Responses of motoneurons of
different sizes to graded stimulation of supraspinal centers of the brain.
J. Neurophysiol. 1965; 28:958–65.
8. Milner-Brown HS, Stein RB, Yemm R. The orderly recruitment of hu-
man motor units during voluntary isometric contractions. J. Physiol.
1973; 230:359–70.
9. Thomas CK, Ross BH, Calancie B. Human motor-unit recruitment during
isometric contractions and repeated dynamic movements. J. Neurophysiol.
1987; 57:311–24.
10. Thomas CK, Ross BH, Stein RB. Motor-unit recruitment in human first
dorsal interosseous muscle for static contractions in three different direc-
tions. J. Neurophysiol. 1986; 55:1017–29.
11. Loeb GE. Motoneurone task groups: coping with kinematic heterogeneity.
J. Exp. Biol. 1985; 115:137–46.
12. Chanaud CM, Pratt CA, Loeb GE. Functionally complex muscles of the cat
hindlimb. V. The roles of histochemical fiber-type regionalization and me-
chanical heterogeneity in differential muscle activation. Exp. Brain Res.
1991; 85:300–13.
13. ter Haar Romeny BM, Denier van der Gon JJ, Gielen CC. Changes in re-
cruitment order of motor units in the human biceps muscle. Exp. Neurol.
1982; 78:360–8.
14. van Zuylen EJ, Gielen CC, Denier van der Gon JJ. Coordination and inho-
mogeneous activation of human arm muscles during isometric torques. J.
Neurophysiol. 1988; 60:1523–48.
15. Riek S, Bawa P. Recruitment of motor units in human forearm extensors. J.
Neurophysiol. 1992; 68:100–8.
16. Puckree T, Cerny F, Bishop B. Abdominal motor unit activity during respi-
ratory and nonrespiratory tasks. J. Appl. Physiol. 1998; 84:1707–15.
17. Sokoloff AJ, Siegel SG, Cope TC. Recruitment order among motoneurons
from different motor nuclei. J. Neurophysiol. 1999; 81:2485–92.
18. Butler JE, McKenzie DK, Gandevia SC. Discharge properties and recruit-
ment of human diaphragmatic motor units during voluntary inspiratory
tasks. J. Physiol. 1999; 518(Pt 3):907–20.
19. Watson TW, Whitelaw WA. Voluntary hyperventilation changes recruit-
ment order of parasternal intercostal motor units. J. Appl. Physiol. 1987;
62:187–93.
20. Kernell D, Hultborn H. Synaptic effects on recruitment gain: a mechanism
of importance for the input–output relations of motoneurone pools? Brain
Res. 1990; 507:176–9.
21. De Troyer A, Boriek AM. Mechanics of the respiratory muscles. Compr.
Physiol. 2011; 1:1273–300.
22. Hudson AL, Gandevia SC, Butler JE. Control of human inspiratory
motoneurones during voluntary and involuntary contractions. Respir. Phys-
iol. Neurobiol. 2011; 179:23–33.
23. Butler JE, Hudson AL, Gandevia SC. The neural control of human inspira-
tory muscles. Prog. Brain Res. 2014; 209:295–308.
24. Gandevia SC, Hudson AL, Gorman RB, Butler JE, De Troyer A. Spatial
distribution of inspiratory drive to the parasternal intercostal muscles in
humans. J. Physiol. 2006; 573:263–75.
Volume 47 • Number 3 • July 2019
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
25. De Troyer A, Gorman RB, Gandevia SC. Distribution of inspiratory
drive to the external intercostal muscles in humans. J. Physiol. 2003;
546:943–54.
26. Zhan WZ, Mantilla CB, Zhan P, et al. Regional differences in serotonergic
input to canine parasternal intercostal motoneurons. J. Appl. Physiol. 2000;
88:1581–9.
27. Hudson AL, Gandevia SC, Butler JE. Common rostrocaudal gradient of
output from human intercostal motoneurones during voluntary and au-
tomatic breathing. Respir. Physiol. Neurobiol. 2011; 175:20–8.
28. De Troyer A, Kirkwood PA, Wilson TA. Respiratory action of the intercos-
tal muscles. Physiol. Rev. 2005; 85:717–56.
29. Butler JE, Gandevia SC. The output from human inspiratory motoneurone
pools. J. Physiol. 2008; 586:1257–64.
30. Hudson AL, Gandevia SC, Butler JE. Task-dependent output of human
parasternal intercostal motor units across spinal levels. J. Physiol. 2017;
595:7081–92.
31. Hudson AL, Gandevia SC, Butler JE. The effect of lung volume on the co-
ordinated recruitment of scalene and sternomastoid muscles in humans. J.
Physiol. 2007; 584:261–70.
32. Hudson AL, Butler JE, Gandevia SC, De Troyer A. Interplay between the
inspiratory and postural functions of the human parasternal intercostal mus-
cles. J. Neurophysiol. 2010; 103:1622–9.
33. Hudson AL, Joulia F, Butler AA, Fitzpatrick RC, Gandevia SC, Butler JE.
Activation of human inspiratory muscles in an upside-down posture. Respir.
Physiol. Neurobiol. 2016; 226:152–9.
34. Larnicol N, Rose D, Marlot D, Duron B. Spinal localization of the intercos-
tal motoneurones innervating the upper thoracic spaces. Neurosci. Lett.
1982; 31:13–8.
35. Greer JJ, Martin TP. Distribution of muscle fibre types and EMG activity in
cat intercostal muscles. J. Appl. Physiol. 1990; 69:1208–11.
36. Burke RE, Jankowska E, ten Bruggencate G. A comparison of peripheral
and rubrospinal synaptic input to slow and fast twitch motor units of triceps
surae. J. Physiol. 1970; 207:709–32.
37. Garnett R, Stephens JA. The reflex responses of single motor units in hu-
man first dorsal interosseous muscle following cutaneous afferent stimula-
tion. J. Physiol. 1980; 303:351–64.
38. Kanda K, Desmedt JE. Cutaneous facilitation of large motor units and motor
control of human fingers in precision grip. In: Desmedt JE, editor. Motor
Control Mechanisms in Health and Disease. New York: Raven Press; 1983.
p. 253–61.
39. Davies JG, Kirkwood PA, Sears TA. The distribution of monosynaptic con-
nexions from inspiratory bulbospinal neurones to inspiratory motoneurones
in the cat. J. Physiol. 1985; 368:63–87.
40. DiMarco AF, Kowalski KE. Activation of inspiratory muscles via spinal cord
stimulation. Respir. Physiol. Neurobiol. 2013; 189:438–49.
41. Gandevia SC, Kirkwood PA. Spinal breathing: stimulation and surprises. J.
Physiol. 2011; 589:2661–2.
42. Lane MA. Spinal respiratory motoneurons and interneurons. Respir. Physiol.
Neurobiol. 2011; 179:3–13.
43. Enriquez Denton M, Wienecke J, Zhang M, Hultborn H, Kirkwood PA.
Voltage-dependent amplification of synaptic inputs in respiratory
motoneurones. J. Physiol. 2012; 590:3067–90.
44. Kennedy PM, Cresswell AG. The effect of muscle length on motor-unit re-
cruitment during isometric plantar flexion in humans. Exp. Brain Res. 2001;
137:58–64.
45. Kawakami Y, Ichinose Y, Fukunaga T. Architectural and functional features
of human triceps surae muscles during contraction. J. Appl. Physiol. 1998;
85:398–404.
46. Desmedt JE, Godaux E. Spinal motoneuron recruitment in man: rank
deordering with direction but not with speed of voluntary movement. Sci-
ence. 1981; 214:933–6.
47. Heroux ME, Dakin CJ, Luu BL, Inglis JT, Blouin JS. Absence of lateral
gastrocnemius activity and differential motor unit behavior in soleus
and medial gastrocnemius during standing balance. J. Appl. Physiol. (1985).
2014; 116:140–8.
48. Falla D, Farina D. Motor units in cranial and caudal regions of the upper tra-
pezius muscle have different discharge rates during brief static contractions.
Acta Physiol. 2008; 192:551–8.
49. Bhutada MK, Phanachet I, Whittle T, Peck CC, Murray GM. Regional
properties of the superior head of human lateral pterygoid muscle. Eur. J.
Oral Sci. 2008; 116:518–24.
Motor Units and Neuromechanical Matching 167
50. Park RJ, Tsao H, Cresswell AG, Hodges PW. Anticipatory postural activity
of the deep trunk muscles differs between anatomical regions based on
their mechanical advantage. Neuroscience. 2014; 261:161–72.
51. Herzog W, Schappacher G, DuVall M, Leonard TR, Herzog JA. Residual
force enhancement following eccentric contractions: a new mechanism
involving titin. Physiology (Bethesda). 2016; 31:300–12.
52. McKeon B, Gandevia S, Burke D. Absence of somatotopic projection of
muscle afferents onto motoneurons of same muscle. J. Neurophysiol. 1984;
51:185–94.
168 Exercise and Sport Sciences Reviews
Copyright © 2019 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
53. Gallina A, Blouin JS, Ivanova TD, Garland SJ. Regionalization of
the stretch reflex in the human vastus medialis. J. Physiol. 2017; 595:
4991–5001.
54. Heroux ME, Brown HJ, Inglis JT, Siegmund GP, Blouin JS. Motor units in
the human medial gastrocnemius muscle are not spatially localized or
functionally grouped. J. Physiol. 2015; 593:3711–26.
55. Hodson-Tole EF, Wakeling JM. Motor unit recruitment patterns 1: re-
sponses to changes in locomotor velocity and incline. J. Exp. Biol. 2008;
211:1882–92.
www.acsm-essr.org