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Acta Physiol 2011, 202, 119–140

REVIEW
Neural adaptations to strength training: Moving beyond
transcranial magnetic stimulation and reflex studies

T. J. Carroll,1 V. S. Selvanayagam,1,2 S. Riek1 and J. G. Semmler3

1 School of Human Movement Studies, The University of Queensland, Brisbane, Queensland, Australia
2 Sports Centre, University of Malaya, Kuala Lumpur, Malaysia
3 Discipline of Physiology, School of Medical Sciences, The University of Adelaide, Adelaide, South Australia, Australia

Received 4 October 2010, Abstract

revision requested 16 December
2010,
revision received 12 January 2011,
accepted 2 March 2011
Correspondence: Dr T. J. Carroll,
Faculty of Health Sciences, School
of Human Movement Studies, The
University of Queensland, Qld
4072, Australia.
E-mail: timothy.carroll@uq.edu.au
It has long been believed that training for increased strength not only affects
muscle tissue, but also results in adaptive changes in the central nervous
system. However, only in the last 10 years has the use of methods to study
the neurophysiological details of putative neural adaptations to training
become widespread. There are now many published reports that have used
single motor unit recordings, electrical stimulation of peripheral nerves, and
non-invasive stimulation of the human brain [i.e. transcranial magnetic
stimulation (TMS)] to study neural responses to strength training. In this
review, we aim to summarize what has been learned from single motor unit,
reflex and TMS studies, and identify the most promising avenues to advance
our conceptual understanding with these methods. We also consider the few
strength training studies that have employed alternative neurophysiological
techniques such as functional magnetic resonance imaging and electroen-
cephalography. The nature of the information that these techniques can
provide, as well as their major technical and conceptual pitfalls, are briefly
described. The overall conclusion of the review is that the current evidence
regarding neural adaptations to strength training is inconsistent and
incomplete. In order to move forward in our understanding, it will be nec-
essary to design studies that are based on a rigorous consideration of the
limitations of the available techniques, and that are specifically targeted to
address important conceptual questions.
Keywords H-reflex, muscle strength, single motor unit, transcranial
magnetic stimulation, V-wave.

There is a long history of research aimed at identifying
the nervous system responses to repetitive muscle
actions against high loads (i.e. strength training). As
an illustration, at least 25 systematic reviews have been
published in the last 30 years that have neural adapta-
tions to strength training as a major focus. Until
relatively recently, most of the evidence on the topic
was indirect, such as the well-known mismatch between
the time course of strength increases versus muscle
hypertrophy. In the last 10 years or so, however, there
has been a relative explosion in the use of neurophys-
iological methods to assess the effects of strength
training on various aspects of neural function. This
has occurred due the widespread availability of tech-
niques for non-invasive stimulation of the human brain
[i.e. transcranial magnetic stimulation (TMS)], as well
as electrical stimulators, amplifiers and associated
devices for the capture and storage of electrical and

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Acta Physiologica  2011 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2011.02271.x 119
Neural adaptations to strength training Æ T J Carroll et al.
twitch responses of muscle. The purpose of this review
is to critically evaluate evidence about the neural
responses to strength training obtained from single
motor unit, reflex, and TMS studies. The physiological
and technical principles that underlie these techniques,
and their limitations and complications, are emphasized
in order to make the point that care is required when
interpreting data from these electrophysiological meth-
ods in humans. We also consider the potential of some
alternate applications of these techniques to provide
new information regarding the neural adaptations to
strength training. Subsequently, methods to assess
nervous system functions that have only very recently
been applied to strength training will be considered.
These include techniques for studying brain function
through functional magnetic resonance imaging (fMRI)
and electroencephalography (EEG). The overall goals
are to summarize the current evidence regarding neural
adaptations to strength training, and to identify the
most promising avenues to address the key conceptual
questions that remain.
Single motor unit studies
Since its introduction in the late 1920s (Adrian & Bronk
1929), intramuscular recording of single motor unit
activity has provided valuable insight into the neural
control of movement in humans. The key advantage of
recording single motor unit activity is that the discharge
properties of the motoneuron, whose cell body origi-
nates in the spinal cord, can be obtained from the
discharge of the single motor unit. This is achieved
because every action potential generated in the moto-
neuron will result in an action potential in all muscle
fibres innervated by the parent motoneuron, because of
the high safety factor for action potential transmission
at the neuromuscular junction (Bigland-Ritchie et al.
1979). Accordingly, single motor unit recording is one
of only a few neurophysiological techniques that can
provide unambiguous information about the behaviour
of motoneurons during voluntary contractions in
humans.
Technical considerations
The conventional approach to record single motor unit
activity is to insert an electrode into the muscle of
interest to record the extracellular action potentials
from a group of muscle fibres associated with one motor
unit. An intramuscular electrode commonly consists of
a set of flexible fine wires or a needle. A fine wire
electrode is usually custom made and can consist of
several (2–4) insulated wires that are inserted into the
muscle with a hypodermic needle (Milner-Brown et al.
1973). With this technique the needle is withdrawn
120 Acta Physiologica  2011 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2011.02271.x
Acta Physiol 2011, 202, 119–140
leaving the fine wires within the muscle, with the cut
ends of the wires representing the exposed recording
surface. More recently, concentric needle electrodes
have been used to record single motor unit activity,
which usually consist of a stiff needle (250 lm in
diameter) that remains within the muscle during the
voluntary contraction (Stalberg et al. 1996). One
advantage of this technique is that the needle can be
advanced (as opposed to only withdrawn) to optimize
the motor unit recording, or manipulated to record
from other locations within the muscle, which can allow
recordings at high forces under some circumstances.
The obvious drawback is that the needle can generate
some discomfort within the muscle during a voluntary
contraction, and it is not suitable for recording action
potentials when there is a change in muscle length.
Furthermore, recordings at high forces with this tech-
nique are often limited by the inability to identify the
recruitment threshold or to obtain a sufficient number
of action potentials for each motor unit, because the
location of the electrode is often manipulated through-
out the contraction. Nonetheless, it seems that measur-
ing motor unit activity with a concentric needle
electrode has become more commonplace over recent
years, with a growing number of studies utilizing this
technique during isometric contractions.
In addition to intramuscular electrodes, motor unit
potentials can be recorded with subcutaneous electrodes
or with surface electrode arrays. Subcutaneous elec-
trodes comprise a branched bipolar configuration that is
positioned under the skin but over the muscle (Gydikov
et al. 1986, Enoka et al. 1988). Although more techni-
cally difficult to fabricate and use compared with
conventional fine-wire electrodes, these electrodes are
capable of providing selective recordings of single
motor unit potentials up to maximal contractions
(Oya et al. 2009), and provide the necessary stability
to isolate and identify the same motor unit during
different fatiguing tasks (Miller et al. 1996, Mottram
et al. 2005). Electrode arrays consist of a grid of
electrodes placed on the skin above the muscle, and
were originally used to provide a non-invasive assess-
ment of the conduction velocity of motor unit potentials
along the muscle fibres (Schneider et al. 1989, see
Merletti et al. 2003 for review). However, the develop-
ment of more advanced processing methods has
expanded the utility of this technique through decom-
position of the surface electromyogram (EMG) to
identify the discharge times of individual motor units
(De Luca et al. 2006, see Merletti et al. 2008 for
review), which can be accurate up to maximal contrac-
tions (Nawab et al. 2010). While these techniques are
limited to superficial motor units (Farina et al. 2010),
they offer a promising alternative to more invasive
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Acta Physiol 2011, 202, 119–140
procedures where interpretations are constrained
because of a low motor unit yield.
Despite the emergence of some new hardware and
software, longitudinal strength training studies pose an
additional challenge for reliable assessment of motor
unit activity in humans. The main problem is that it is
not yet possible to identify the same motor unit before
and after the training program, in order to clearly
demonstrate an effect of the intervention. Longitudinal
tracking of the same motor unit is possible under some
circumstances (Doherty & Brown 1994), but the
usefulness of the technique is likely to be limited to
patient populations with substantial motoneuron loss
(Gooch & Harati 1997), and does not provide infor-
mation on motor unit discharge behaviour during
voluntary contractions. Therefore, with current motor
unit recording techniques, studies that involve strength
training require a large sample of motor units in each
subject, with a sufficient number of subjects, to
adequately characterize the change with training.
Because of these technical constraints, coupled with
the time consuming nature of the experiments, there are
only a few studies that have adequately addressed the
effect of strength training on motor unit activity in
humans.
Single motor unit activity
One possible neural mechanism to increase muscle
strength with training is an increase in motor unit
discharge rate during maximal contractions. Because
these measures are technically challenging, only a
limited number of studies have examined maximal
motor unit discharge rates after a strength training
intervention. Specific details of these studies are pro-
vided in Table 1. Using both isometric and dynamic
training protocols that produced significant increases in
strength, these studies have demonstrated an increase in
maximal motor unit discharge rates in upper and lower
limb muscles after training, although this is not always
a consistent finding (e.g. Pucci et al. 2006). The greatest
changes in maximal discharge rates with training (up to
49% increase) have been observed in older adults
(Kamen & Knight 2004). This may be because maximal
discharge rates are lower in the untrained state (Kamen
et al. 1995), reflecting a greater potential for change in
the elderly. However, there is a poor association
between increases in muscle strength and maximal
motor unit discharge rates after training (r2 = 0.15 for
studies in Table 1), presumably because it is only
possible to sample from a small proportion of the
active motor units, and several muscles are likely to
contribute to the mechanical action at the relevant joint.
Nonetheless, these findings suggest that other factors
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Acta Physiologica  2011 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2011.02271.x
T J Carroll et al. Æ Neural adaptations to strength training
must also be contributing to the early gains in strength
with training.
Experimental evidence suggests that more subtle
changes in single motor unit activity, such as an
increased incidence of brief interspike intervals (known
as double discharges or doublets), may have the
potential to influence the neural control of force with
strength training. When present at the beginning of a
voluntary contraction, double discharges have been
shown to substantially increase low-frequency (unfused)
motor unit force (Macefield et al. 1996), which may be
important in the maintenance of force during a
submaximal fatiguing contraction (see Garland &
Griffin 1999). After rapid force development training
of the ankle dorsiflexors, Van Cutsem et al. (1998) has
shown that an increase in the rate of force development
(RFD) was associated with an increased incidence of
double discharges from 5% before training to 33% after
training. This finding suggests that it may be an
appropriate neural strategy to utilize when performing
rapid muscle contractions. However, other evidence
suggests that the implementation of double discharges
may not be a strategy used to improve the functional
outcome, but represent a byproduct of a change in the
intrinsic properties of the motoneurons. For example,
the incidence of double discharges is not associated with
the speed of the voluntary contraction (Bawa &
Calancie 1983, Christie & Kamen 2010), is reduced in
older adults (Klass et al. 2008, Christie & Kamen
2010), and is greater in patients with neuromuscular
disorders (see Thomas et al. 2002). The lack of any
consistent finding on the functional significance of
double discharges may be caused by sampling from
only a small number of motor units in each contraction,
and may depend on the muscle investigated, the
contraction intensity, or the type of motor unit (low
vs. high threshold) examined (see Garland & Griffin
1999, Christie & Kamen 2006).
Along with the gain in maximal strength, several
lines of evidence suggest that training alters the activity
of single motor units and improves performance of
submaximal tasks. In particular, after several weeks of
strength training, the variability of motor output
(referred to as steadiness) is reduced during isometric
(Keen et al. 1994) and slow lengthening contractions
(Laidlaw et al. 1999). Although multiple factors are
likely to be responsible (Taylor et al. 2003), one
candidate mechanism for improved steady motor
performance after training is a reduction in the
variability of motor unit discharge rate (Moritz et al.
2005, Tracy et al. 2005). This hypothesis was exam-
ined following a training intervention (Kornatz et al.
2005) that involved 2 weeks of practicing a steadiness
task with a light load (10% of maximum) followed by
4 weeks of strength training with a heavy load (70% of
121
122
Table 1 Summary of studies examining the effect of strength training on motor unit discharge rate during maximal contractions

Recording Training Training

Study Muscle Subject details technique duration frequency Training intensity Strength gain Discharge rate

Christie & Kamen Tibialis anterior 30 young 4-wire needle 2 weeks 3· week)1 3 sets of 10 isometric › 17% young › 7% young
Neural adaptations to strength training

(2010) 30 old (15 controls/ (quadrifillar) MVCs › 20% old › 24% old
group)
Kamen & Knight Vastus lateralis 8 young 4-wire needle 6 weeks 3· week)1 3 sets of 10 dynamic › 29% young › 15% young
(2004) 7 old (quadrifillar) contractions (85% › 36% old › 49% old
1RM)
Patten et al. Abductor digiti 6 young 4-wire needle 6 weeks 5· week)1 2 sets of 10 isometric › 25% young › 11% young
Æ T J Carroll et al.

(2001) minimi 6 old (quadrifillar) MVCs › 33% old › 23% old

Pucci et al. Vastus lateralis 10 training Tungsten 3 weeks 3· week)1 3 sets of 10 isometric › 35% training › 3% training
(2006) 10 controls microelectrode MVCs group (n.s.)
(All young males)
Van Cutsem et al. Tibialis anterior 5 training Fine-wire needle 12 weeks 5· week)1 10 sets of 10 rapid › 30% training › 29% training*
(1998) 5 controls electrode shortening
(all young subjects) contractions
(30–40% 1RM)
MVC, maximal voluntary contraction; 1RM, one-repetition maximum; n.s., non-significant difference after training.
*This value was calculated without the presence of double discharges (<5 ms).

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Acta Physiol 2011, 202, 119–140
Acta Physiol 2011, 202, 119–140
maximum). After the first 2 weeks of practice, there
were parallel declines in motor unit discharge rate
variability in the first dorsal interosseous muscle and
the steadiness of slow shortening and lengthening
contractions performed by the index finger. No further
changes in motor unit discharge rate variability or
steadiness were evident after 4 weeks of strength
training, suggesting that practice of the task was
largely responsible for the changes in motor unit
discharge rate variability and improvements in motor
performance. Similarly, 6-weeks of strength training
the knee extensor muscles resulted in an increase in
mean motor unit discharge rates and a decrease in
motor unit discharge rate variability during submaxi-
mal contractions (Vila-Cha et al. 2010). Furthermore,
Knight & Kamen (2004) examined the modulation of
motor unit discharge rate during isometric force
tracking tasks requiring skill acquisition. The target
force comprised an average of 20% maximal voluntary
contraction (MVC) that was modulated by 2% MVC
with sine waves of 0.15 and 0.5 Hz. Throughout the
performance of 15 trials, they found that an improved
precision of force matching was accompanied by
decreased motor unit discharge rate modulation at
the higher of the two modulating frequencies. Taken
together, these studies suggest that training to increase
maximal strength may have implications for motor unit
activity during submaximal tasks that may improve
skilled motor performance.
Correlated motor unit activity
The correlated activity of motor units is now regarded
as an important physiological principle for the neural
control of movement. Computer simulation studies
have shown that correlated motor unit activity can
have a substantial influence on EMG and force fluctu-
ations (Yao et al. 2000, Zhou & Rymer 2004), and
experimental studies suggest that it can vary depending
on the details of the task that is performed (see Semmler
et al. 2002). The correlated discharge of action poten-
tials by motoneurons is caused by common branched
pre-synaptic inputs or independent inputs that are
themselves synchronized. The effect on motor unit
activity can be quantified in the time domain as motor
unit synchronization or in the frequency domain as
motor unit coherence (Farmer et al. 1997). There is a
strong association between motor unit synchronization
and high-frequency coherence (10–30 Hz), indicating
that similar mechanisms contribute to these two fea-
tures of correlated motor unit activity (Farmer et al.
1993, Semmler et al. 2004). Furthermore, low-fre-
quency (1–2 Hz) motor unit coherence is equivalent
to the common fluctuations in mean motor unit
discharge rates, which is referred to as common drive
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Acta Physiologica  2011 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2011.02271.x
T J Carroll et al. Æ Neural adaptations to strength training
(De Luca et al. 1982). As a coherence analysis is able to
detect these multiple features of correlated motor unit
activity over a range of frequencies, it is now considered
the most sensitive approach when examining the
discharge patterns from a population of active motor
units.
One of the most appealing mechanisms for an
increase in strength with training is an increase in
correlated motor unit activity. This has largely been
driven by an original investigation from Milner-Brown
et al. (1975), which found a 128% increase in motor
unit synchronization after 6 weeks of isometric strength
training that involved the index finger. However, this
study used a surface EMG based population index of
motor unit synchronization, which has been shown to
be an unreliable estimate of correlated motor unit
activity (Yue et al. 1995). Nonetheless, this seminal
study by Milner-Brown et al. (1975) has been widely
cited as one of only a few examples of a chronic neural
adaptation induced by strength training. Using the more
robust cross-correlation procedure between pairs of
concurrently active motor units (see Farmer et al.
1997), several studies have shown that habitual physical
activity patterns may influence motor unit synchroni-
zation. For example, motor unit synchronization is
greatest in strength-trained subjects (weightlifters),
intermediate in untrained control subjects, and least in
skill-trained musicians (Semmler & Nordstrom 1998).
More recently, motor unit synchronization has been
shown to be greater in strength-trained males, but only
for the biceps brachii muscle at high forces (80% MVC)
and not for the first dorsal interosseous muscle at low
(30% MVC) or high (80% MVC) force levels (Fling
et al. 2009). However, these cross-sectional studies are
difficult to interpret because no training intervention
was performed, and therefore they do not account for
other genetic or lifestyle factors that may contribute to
alterations in motor unit synchronization. In contrast, a
4-week training intervention that resulted in a 54%
increase in index finger strength showed no change in
motor unit synchronization in the first dorsal interos-
seous muscle (Kidgell et al. 2006). This definitive
interventional study using cross-correlation from pairs
of concurrently active motor units indicates that corre-
lated motor unit activity is unlikely to be important for
the expression of muscle strength with training.
An alternative explanation for differences in the
strength of correlated motor unit activity in skill and
strength-trained individuals (Semmler & Nordstrom
1998, Semmler et al. 2004) might be that practice of a
task results in reduced motor unit synchronization,
which may be beneficial in performing fine motor tasks
at low force levels. This hypothesis was addressed in a
recent study which examined motor unit synchroniza-
tion in hand muscles during a pinching task following
123
Neural adaptations to strength training Æ T J Carroll et al.
training with light loads to improve force steadiness in
older adults (Griffin et al. 2009). After 4 weeks of light-
load isometric training (2 and 4% MVC), they found no
change in motor unit synchronization both within and
between hand muscles despite significant improvements
in isometric steadiness at these low force levels. In
contrast, there were significant declines in motor unit
discharge rate variability in the first dorsal interosseous
muscle with training. Thus, it appears that improve-
ments in motor performance with skill training or
practice may occur through altered motor unit dis-
charge rate variability, rather than a change in corre-
lated motor unit activity.
Finally, evidence from lengthening (eccentric) muscle
contractions has provided new insight into the task-
related adjustments of correlated motor unit activity.
Lengthening contractions are performed regularly in
everyday lives, and are important considerations for
training because of their potential to produce large
forces with low metabolic cost. Several studies have
shown altered motor unit behaviour during lengthening
contractions (Del Valle & Thomas 2005, Pasquet et al.
2006), supporting the proposal that lengthening con-
tractions require unique neural activation strategies
(Enoka 1996). Interestingly, the modulation of corre-
lated motor unit activity also appears to be an impor-
tant feature of lengthening contractions. For example,
cross-correlation analysis from the same pairs of con-
currently active motor units in the first dorsal interos-
seous muscle has shown an increase in motor unit
synchronization during lengthening, compared with
postural or shortening muscle contractions (Semmler
et al. 2002). This increased motor unit synchronization
during lengthening contractions may act as a protective
mechanism by distributing the load over a greater
number of motor units to reduce the extent of muscle
damage that can occur after these types of contractions
(see McHugh 2003 for review). This suggestion is
supported by recent work showing that motor unit
synchronization is increased in biceps brachii motor
units for at least 24 h after the muscle has been
damaged with repetitive lengthening contractions
(Dartnall et al. 2008). These data suggest that length-
ening muscle contractions, including the involvement of
naturally occurring movements such as the stretch-
shortening cycle (see Nicol et al. 2006), may be impor-
tant in the neural adaptation and the modulation of
correlated motor unit activity with training.
Moving forward with human motor units
Over the last 3 decades, evidence has accumulated to
suggest that certain types of strength or resistance
training can alter the discharge properties of human
motor units. However, the progress in this field at the
124 Acta Physiologica  2011 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2011.02271.x
Acta Physiol 2011, 202, 119–140
single motor unit level has not accelerated markedly
over the last 10 years. This can largely be attributed to
technical difficulties associated with recording single
motor units, particularly at high forces. This limitation
has been detrimental to studies specifically designed to
increase strength, as it is the behaviour of high threshold
motor units that are most likely to contribute to the
strength gains, but are least amenable to study with
invasive motor unit recording techniques. The contin-
ued development of hardware and software for use with
surface electrode arrays offers many promising avenues
for advancing knowledge in this field, as they provide a
means of obtaining a high motor unit yield, even during
strong contractions (Farina et al. 2010, Nawab et al.
2010). Furthermore, these techniques may also shed
new light on the coordination of multiple muscle
synergists and antagonists, by facilitating comparisons
of common drive between muscles and how this may
contribute to changes in muscle strength with training.
Finally, for practical reasons, many training studies
have been restricted to isometric contractions, but the
involvement of lengthening contractions may enhance
the changes with training and offer further insight into
the proposed neural adaptations.
Spinal reflex studies
Technical considerations
Reflex responses produced by electrical stimulation of
peripheral nerves have the potential to contribute
information regarding the sites and mechanisms of
neural adaptation to strength training. The two reflexes
that have been applied most commonly in strength
training studies are the H-reflex (Magladery & McDo-
ugal 1950) and the V-wave (Upton et al. 1971), both of
which rely to a large extent on the monosynaptic circuit
from Ia afferent fibres to motoneurons. Both reflexes are
produced by electrical stimulation of a mixed nerve (i.e.
containing axons of motoneurons and afferents of
various origin). The afferent volley generated ultimately
causes a relatively synchronous discharge of motoneu-
rons, and the earliest part of the response is probably
due purely to the monosynaptic connection between Ia
afferents and motoneurons (Magladery et al. 1951).
With H-reflexes, the response initially grows with
stimulation intensity as the afferent volley increases in
size, but then progressively falls to zero as the intensity
approaches levels supramaximal for activating motor
axons (i.e. to produce a maximal M-wave). It is
generally accepted that this is because of collision
between orthodromic action potentials produced by the
reflex with antidromic action potentials generated
directly in the motor axons by the electrical stimulus.
In contrast, the V-wave is produced by supramaximal
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Acta Physiol 2011, 202, 119–140
stimulation during voluntary contraction (typically
MVC). The cancellation of action potentials that
abolishes the H-reflex at high stimulus intensities is
prevented in some motoneurons by action potentials
produced via volition. That is, in some motoneurons, a
voluntary action potential will collide with the
antidromic action potential produced by the stimulus,
and ‘clear’ the pathway for subsequent reflex activation.
The number of motoneurons that are free to respond to
the afferent volley will depend on the number and firing
rate of the motoneurons involved in the voluntary
contraction, and the conduction time from the stimu-
lation site to the spinal cord. The ultimate size of the
reflex will also depend on motoneuron responsiveness
and the efficacy of synaptic transmission between
afferents and motoneurons. Although these two reflexes
can provide information regarding the efficacy of the Ia
afferent reflex pathway and the output from the
motoneuron pool during voluntary contraction, there
are a number of technical issues that complicate their
interpretation. Because many of the complications with
H-reflex interpretation are often neglected, some of the
key points will be summarized in the following sections.
The reader is referred to Burke & Gandevia (1999) for
detailed coverage.
The first complication in interpreting changes in
H-reflex amplitude because of an intervention such as
strength training is the difficulty in ensuring an identical
size of the afferent volley elicited by the stimulation
pulse. One way of attempting to control this is by
matching the amplitude of a small M-wave between
conditions, and thereby ensuring a similar number of
motoneurons are excited by the stimulus (e.g. Zehr
2002, Misiaszek 2003). However, this procedure does
not account for potential changes in axonal excitability
(e.g. Bostock & Grafe 1985). This is a critical consid-
eration because axonal excitability is susceptible to
change in ways that differ for large diameter afferents
versus motoneurons (e.g. Mogyoros et al. 1996, Vagg
et al. 1998). If strength training were to alter axonal
excitability of afferents or motoneurons, this could
produce a change in H-reflex amplitude in the absence
of central effects [i.e. effects within the central nervous
system (CNS)]. However, measures of H-reflex
responses provided by H-reflex recruitment curves
(i.e. recording the reflex size at a range of stimulus
strengths from below threshold to supramaximal levels)
should be less susceptible to this potential confound.
The issue is also less likely to be of concern for V-waves
provided that the stimulus intensity was sufficiently
supramaximal to account for activity dependent reduc-
tions in axonal excitability (see Burke & Gandevia 1999
for details).
The second complication for interpreting the size of
H-reflexes is that there are almost certainly considerable
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T J Carroll et al. Æ Neural adaptations to strength training
non-monosynaptic contributions to the reflex (e.g.
Burke et al. 1984, Marchand-Pauvert et al. 2002, see
Burke & Gandevia 1999 for review). While the earliest
part of the response is via monosynaptic Ia inputs, this
initial excitation is curtailed by disynaptic inhibition
(i.e. produced via Ia or Ib afferent activation of an
inhibitory interneuron; Marchand-Pauvert et al. 2002).
Thus, as pointed out by Burke & Gandevia (1999), the
size of the H-reflex is determined by the balance
between monosynaptic Ia excitation and disynaptic
inhibition. A change in H-reflex or V-wave size could be
brought about by an alteration in transmission efficacy
in either of these circuits. Clearly, as pointed out
previously by many authors (e.g. Burke & Gandevia
1999, Zehr 2002, Misiaszek 2003), the H-reflex does
not provide a measure of ‘motoneuron excitability’.
Finally, if one considers only monosynaptic Ia con-
tributions, changes in the size of the H-reflex could be
because of changes in the responsiveness of the moto-
neurons or alterations in the synaptic transmission
efficacy at the Ia afferent terminals (see Zehr 2002,
Misiaszek 2003 for reviews). With respect to moto-
neuron responsiveness, intrinsic membrane properties,
firing rate and the effects of neuromodulators such as
serotonin could contribute (Capaday 1997, Matthews
1999). Alterations to the synaptic transmission efficacy
can occur because of pre-synaptic inhibition of Ia
afferent terminals and homosynaptic post-activation
depression (see Hultborn & Nielsen 1998, Pierrot-
Deseilligny & Burke 2005 for extensive review).
H-reflex and V-wave studies
Since the earliest cross-sectional (Milner-Brown et al.
1975), and longitudinal studies (Sale et al. 1982, 1983),
there have been many reports of H-reflex and V-wave
responses to strength training (summarized in Table 2).
With the exception of the earliest studies (Sale et al.
1982, 1983), all of these investigations have involved
muscles that act at the ankle joint. There have been no
reports of an increase in H-reflex amplitude at rest as a
consequence of strength training (Aagaard et al. 2002,
Scaglioni et al. 2002, Del Balso & Cafarelli 2007,
Holtermann et al. 2007, Duclay et al. 2008, Schubert
et al. 2008, Fimland et al. 2009a, Ekblom 2010) or
tetanic electrical stimulation of muscles (Maffiuletti
et al. 2003, Gondin et al. 2006). In contrast, strength
training was reported to increase the amplitude of
V-waves in all studies involving plantar flexors (Sale
et al. 1983, Aagaard et al. 2002, Gondin et al. 2006,
Del Balso & Cafarelli 2007, Holtermann et al. 2007,
Duclay et al. 2008, Fimland et al. 2009a,b, Ekblom
2010) but not for the thumb abductors (Sale et al.
1982). Thus, for the Soleus muscle, there is clear
evidence that resting H-reflexes are unaffected, and
125
 Table 2 Summary of studies examining the effect of strength training on H-reflex and V-wave size

126
Training Training
Study Muscle group Subject details Methods schedule intensity Strength gain Results

Sale et al. (1982) Thumb abductors 11 trained V-wave, MVC 18 weeks Dynamic › 41% MVC M V-wave
74 sessions 5–6 sets up to 1RM
Isometric
2 sets 10 MVC
Sale et al. (1983) Plantar flexors 14 trained V-Wave, MVC 9–21 weeks Dynamic Not reported › 50% V-wave. Pooled
toe extensors F-wave 5–6 sets up to 1RM across muscles
elbow flexors Isometric M F-wave
finger flexors 2 sets 10 MVC
Aagaard et al. Plantar flexors 14 trained H-reflex, rest and 90% 14 weeks Dynamic › 20% MVC M H-reflex at rest
Neural adaptations to strength training

(2002) MVC 38 sessions 3–10RM › 23% concentric › 55% V-wave,

V-Wave, 90% MVC multiple exercises 4–5 › 19% H-reflex 90%
sets each MVC
Scaglioni et al. Plantar flexors 14 trained H-reflex, rest 16 weeks Dynamic › 18% MVC M H-reflex
(2002) (65–85 years) 48 sessions 50–80% 1RM › 24% 1RM
Æ T J Carroll et al.

1 set of 10
Maffiuletti et al. Plantar flexors 8 trained H-reflex, rest 4 weeks 45 electrical Not reported M H-reflex
(2003) 6 control 16 sessions stimulations (max
tolerable)
50–70% MVC
Lagerquist et al. Plantar flexors 10 trained H-reflex, 10% MVC 5 weeks Isometric › 15% MVC › H-reflex during 10%
(2006) 6 control 15 sessions MVC MVC
5 sets of 8
Gondin et al. Plantar flexors 12 trained H-reflex, rest and MVC 5 weeks 40 electrical › 22% MVC M H-reflex
(2006) 7 Control V-Wave, MVC 15 sessions stimulations › 80% V-wave
(max. tolerable)
60% MVC
Del Balso & Cafar- Plantar flexors 10 trained H-reflex, rest, 10% 4 weeks Isometric › 20% MVC M H-reflex
elli (2007) 10 control MVC 12 sessions 6 sets of 10 MVC › 54% V-wave
V-Wave, 50, 75, 100%
MVC
Beck et al. (2007) Dorsiflexors, 8 trained H reflex during fast 4 weeks Dynamic ballistic Not reported M H-reflex
Plantar flexors 10 control contraction 16 sessions 30–40% 1RM
4–6 sets of 10
Holtermann et al. Plantar flexors 12 trained H-reflex at rest and 3 weeks Isometric › 18% MVC M H-reflex at rest
(2007) 12 control during 20 and 60% 9 sessions MVC › H-reflex, 20, 60%
MVC 5 sets of 10 MVC

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Acta Physiol 2011, 202, 119–140
 Table 2 Continued

Training Training

 2011 The Authors

Study Muscle group Subject details Methods schedule intensity Strength gain Results

Duclay et al. (2008) Plantar flexors 10 trained H-reflex at rest & 7 weeks Dynamic eccentric, › 22% MVC M H-reflex at rest
8 control during passive 18 sessions 120% 1RM › 31% max › V-wave in MVC and
Acta Physiol 2011, 202, 119–140

movement 6 sets of 6 eccentric max eccentric

H-reflex and V-wave › 28% max › H-reflex in MVC, max
during max isometric, concentric eccentric and concentric
concentric and
eccentric contractions
Schubert et al. Plantar flexors 12 trained H-reflex and 4 weeks Dynamic ballistic › RFD M H-reflex
(2008) 11 control TMS-conditioning of 16 sessions 30–40% 1RM MVC not reported › conditioned H-reflex
H reflex during rest and 4–6 sets of 10 size in ballistic task but
ballistic tasks not rest
Geertsen et al. Dorsiflexors 12 trained Disynaptic reciprocal 4 weeks Isometric › 20% MVC › reciprocal inhibition
(2008) 6 control inhibition of plantar 12 sessions MVC ballistic
flexors at onset ballistic 3 sets of 16
dorsiflexion
Fimland et al. Plantar flexors 10 trained H-reflex at rest 8 weeks Dynamic ballistic › 20% MVC › 50% V-wave in MVC
(2009a) 9 control H-reflex and V-wave 24 sessions multi-joint extension › 44% 1RM leg M H-reflexes
during MVC 85–90% 1RM press
T J Carroll et al.

4 sets of 4
Fimland et al. Plantar flexors 15 trained H-reflex and V-wave 4 weeks Isometric › 44% MVC › 72% V-wave in MVC
(2009b) 11 control during MVC 16 sessions MVC M H-reflexes
6 sets of 6
Ekblom (2010) Plantar flexors 9 trained H-reflex and V-wave 5 weeks Dynamic › 19% mean M H-reflex
11 control during max concentric 15 sessions eccentric focused for concentric/eccentric › 77% V-wave during

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and eccentric PF maximal eccentric and
H-reflex at rest 5–6 sets of 5RM concentric actions

max, maximal; MVC, maximal voluntary contraction; RM, repetition maximum.

127
Æ Neural adaptations to strength training
Neural adaptations to strength training Æ T J Carroll et al.
V-wave amplitudes are enhanced, by strength training.
The results for H-reflexes elicited during voluntary
contractions are less consistent. There have been reports
both that strength training increases H-reflex size
(Aagaard et al. 2002, Lagerquist et al. 2006, Holter-
mann et al. 2007, Duclay et al. 2008) and does not
change H-reflex size (Gondin et al. 2006, Beck et al.
2007, Del Balso & Cafarelli 2007, Fimland et al.
2009a,b, Ekblom 2010), when evoked during contrac-
tions ranging in strength from 10 to 100% of MVC.
The discrepancies could be due partly to differences in
the details of how the reflexes were elicited and
measured. For example, some studies determined the
maximal H-reflex amplitude, whereas others assessed
H-reflex size at matched M-wave amplitudes, or calcu-
lated the slope of the stimulus intensity versus response
curve. Each of these methods might be differentially
affected by methodological factors that can influence
H-reflex amplitude such as axonal excitability.
When a change in H-reflex was detected, the result
was taken as evidence of neural adaptation to strength
training mediated at a spinal level. Whether this is
entirely accurate depends on one’s perspective on
defining a ‘site’ of adaptation. While it is accepted
that the H-reflex is subject to modulation within the
spinal cord, it is quite possible that changes in
supraspinal inputs to the spinal circuitry could increase
H-reflex size (i.e. by modulating pre-synaptic inhibition
or the responsiveness of inhibitory interneurons).
Increases in V-wave amplitude have frequently been
cited as evidence of increased motoneuron activation.
There has also been a strong tendency to ascribe the
putative increased motoneuron activation to adapta-
tions at supraspinal levels, particularly when V-wave
changes were observed in parallel with H-reflexes (e.g.
Aagaard et al. 2002, Del Balso & Cafarelli 2007).
While an increased supraspinal drive to motoneurons is
certainly a plausible explanation for increased V-wave
amplitudes, there are numerous alternative possibilities
that cannot be discounted. More generally, the notion
that comparisons between V-wave and H-reflex allow
dissociation between spinal and supraspinal adapta-
tions is ill-founded. For example, the different stimulus
intensities associated with the two methods will acti-
vate of different populations of afferents and moto-
neurons (i.e. antidromically), which might also result in
different oligosynaptic influences on the reflex ampli-
tude (e.g. greater antidromic activation of motoneurons
produced by supramaximal stimulation to generate the
V-wave might activate more Renshaw cells), and the
reflexes might be differentially influenced by activity
dependent changes in axonal excitability. Furthermore,
even if an increase in V-wave amplitude could be
ascribed entirely to an increase in the number of
voluntarily recruited motoneurons (i.e. if one could be
128 Acta Physiologica  2011 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2011.02271.x
Acta Physiol 2011, 202, 119–140
sure of an identical reflex excitation of motoneurons),
then there is no basis for determining the origin of the
extra motoneuronal drive. For example, spinal reflex
pathways are known to contribute considerably to the
activation of motoneurons during voluntary contrac-
tion (e.g. Macefield et al. 1993).
Conditioning-test reflex approaches
Given the difficulty in identifying the specific spinal
circuits responsible for any changes that might occur in
H-reflex (or V-wave) size, it is worth considering the
potential of related methods that might provide more
specific information about the nature of neural adap-
tation to strength training. By careful application of
conditioning stimulation to various homonymous and
heteronymous muscle afferents or skin afferents, it is
possible to draw inferences about the efficacy of
specific spinal reflex pathways (see Pierrot-Deseilligny
& Burke 2005 for extensive review). For example,
Geertsen et al. (2008) used conditioning stimulation of
the peroneal nerve to suppress the soleus H-reflex in
order to study the effect of explosive strength training
on disynaptic reciprocal inhibition (i.e. via Ia inhibi-
tory interneurons that reduce coactivation of antago-
nist muscles). They found that 4 weeks of ballistic
strength training for the dorsiflexors increased disy-
naptic reciprocal inhibition from peroneal afferents to
the antagonist soleus when assessed at the onset of
ballistic dorsiflexion contraction, but not at rest. The
lack of change in disynaptic reciprocal inhibition at
rest implies that there was no change in the default
properties of the pathway per se, and that the
increased inhibition prior to ballistic contraction might
reflect a training-induced descending modulation of
spinal interneuronal responsiveness that is tailored to
the functional requirements of the training task (i.e. to
ensure that antagonist muscles do not contribute
plantar flexion torque at the onset of intended dorsi-
flexion).
Moving forward with reflex studies
Despite the many complications with interpreting
H-reflex and V-wave results, it appears that for the
plantar flexors, resting H-reflexes are unaffected by
strength training and V-waves during MVC are
increased. The physiological implications of these
results are not definitive, but it is likely that there is
little ‘baseline’ alteration to the Ia-afferent-motoneu-
ronal circuit, and an increase in motoneuronal output
during MVC. An understanding of spinal responses to
strength training might be advanced by the applica-
tion of conditioning-test approaches to study modu-
lation in specific reflex circuits. While these
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Acta Physiol 2011, 202, 119–140
approaches are powerful in the sense that they have
potential to provide specific information about par-
ticular afferent and interneuronal pathways, it is
important to note that they provide only indirect
evidence (i.e. inferences obtained require confirmation
from more than one method) and can be technically
challenging.
TMS studies
Technical considerations
Transcranial magnetic stimulation can painlessly acti-
vate neurons in the human cerebral cortex through the
scalp (Barker et al. 1985), and has been used to study
neural transmission from the motor cortex to the
muscles in many behavioural contexts. An index of
the responsiveness of the entire pathway from brain to
muscle (often termed ‘corticospinal excitability’) can be
obtained from the size of the compound muscle action
potentials (CMAP) recorded at the muscle via electro-
myography. These responses are known as motor
evoked potentials (MEPs). Given that MEPs are gener-
ated in response to stimulation of the brain, it can be
tempting to interpret alterations in MEP size as being
caused by a change in the properties of the motor
cortex. This is not appropriate, however, as the size of
TMS responses is subject to potential modulation at
each point in the pathway from brain to muscle. Thus,
in order to properly interpret the effects of an interven-
tion on MEP size, consideration of all of the biophysical
and physiological factors that determine muscle
responses to TMS is required. This is particularly
important for longitudinal studies involving strength
training where there might be substantial changes in
spinal cord circuitry (see Spinal reflex studies above).
Transcranial magnetic stimulation can activate cort-
icospinal cells (i.e. output cells from the motor cortex
that project to the spinal cord) both directly and
indirectly, depending on the magnitude and orientation
of the induced electric field to the cortical network (i.e.
which are influenced by coil size, shape and orientation,
stimulus intensity, and the anatomy of the skull and
cortex; e.g. Barker 1991, Ruohonen & Ilmoniemi
1999). Direct activation of corticospinal cells results in
a descending corticospinal volley termed a ‘D-wave’,
that can be recorded by electrodes implanted in the
cervical epidural space (e.g. Di Lazzaro et al. 1998a),
and inferred from peri-stimulus time histograms from
single motor unit recordings (e.g. Day et al. 1989).
Indirect activation of corticospinal cells results in one or
more ‘I-waves’ (n.b. numbered in order of appearance
latency), the earliest of which (i.e. the I1 wave) appears
approximately 1.5–2 ms after the D-wave (Day et al.
1989, Di Lazzaro et al. 2004, Brocke et al. 2005). The
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Acta Physiologica  2011 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2011.02271.x
T J Carroll et al. Æ Neural adaptations to strength training
size of D-waves produced some distance from the
corticospinal cell soma is little influenced by the state of
the cortical network (see Di Lazzaro et al. 2004 for
review), but the size of I-waves is determined by the net
result of multiple synaptic inputs to the corticospinal
cells. These inputs could arise both from local cortical
interneurons and projections from distant cortical and
subcortical sites, are transmitted from the site of (TMS)
activation to the corticospinal cells via mono- and
oligosynaptic circuits, and contain both excitatory and
inhibitory elements (see Reis et al. 2008 for recent
review). Thus, the net descending volley produced in the
corticospinal tract by a TMS pulse is potentially
influenced by the intrinsic responsiveness of the corti-
cospinal cells (i.e. which is influenced by firing rate and
membrane properties), the synaptic efficacy of local and
distant connections onto corticospinal cells and local
interneurons, and the axonal excitability of the cells
initially responsive to the TMS pulse. Given the
complexity of the system between the sites of stimula-
tion and measurement of the response, the conception
that alterations in ‘cortical excitability’, as suggested by
TMS studies, might provide a mechanism of strength
gains produced by training represents a somewhat
superficial consideration of the physiological changes
that might be involved.
In addition to the anatomical organization and
functional state of cortical circuits (which modulate
the descending volley), the size of the MEP induced by
TMS is also influenced by factors within the spinal cord.
The fact that there are numerous monosynaptic corti-
cospinal connections to distal limb motoneurons in
primates (see Porter & Lemon 1993 for review), has
perhaps led to excessive focus on the corticospinal cell –
motoneuronal connection as a potential site of MEP
modulation. It is correct that the responsiveness of
motoneurons (i.e. influenced by firing rate and
membrane properties) and the efficacy of the cortico-
spinal-motoneuronal synapse can affect the MEP size.
However, because many corticospinal cells terminate on
interneurons in the spinal cord (see Porter & Lemon
1993 for review), the net motoneuronal output pro-
duced by a TMS pulse can be affected by the synaptic
efficacy and intrinsic responsiveness of the components
of spinal interneuronal circuits. It is quite possible that
MEP size might change despite an identical output from
the cortex (i.e. due entirely to spinal factors), and this is
true even if the level of background EMG does not
change. Comparisons of MEP size with H-reflex size,
often erroneously interpreted as an index of ‘motoneu-
ronal excitability’ (see Spinal reflex studies section), do
not allow dissociation of spinal from cortical effects
because the afferent and descending volleys might
activate different interneuronal circuits, and because
the monosynaptic components of the responses traverse
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Neural adaptations to strength training Æ T J Carroll et al.
different synapses (i.e. the corticospinal-motoneuronal
synapse versus the Ia-afferent-motoneuronal synapse;
both of which are subject to modulation with voluntary
muscle activation; Hultborn & Nielsen 1998, Petersen
et al. 2003). Only the response to a descending volley
that travels in the same corticospinal axons as those
activated by TMS, such as transmastoid electrical or
magnetic stimulation, can provide unambiguous
evidence about the spinal or cortical location of MEP
modulation.
Finally, since the MEP is recorded from the muscles
via electromyography, its size is subject to all of the
factors that can affect the amplitude of a CMAP. These
include electrode impedance and the location of elec-
trodes relative to the muscle architecture and innerva-
tion zones (which can be influenced, for example, by
muscle length and contractile status; Lee & Carroll
2005, Frigon et al. 2007), the characteristics of tissue
between the muscle and the skin, the number and
functional state of ion channels in the muscle mem-
brane, the relative timing of action potential firing in
different muscle fibres, and synaptic transmission at the
neuromuscular junction. Thus, it is conceivable that
MEP size might change despite an identical motoneu-
ronal output in response to a TMS pulse (i.e. due
entirely to peripheral factors). In order to properly
interpret MEP size, it is essential to normalize the
responses to a standardized CMAP such as the maximal
M-wave (i.e. which is elicited by supramaximal stimu-
lation of the motor nerve).
MEP studies
The details of studies that have examined the effect of
strength training protocols on EMG responses to TMS
are summarized in Table 3. These studies show that
there is no clear pattern of change in MEP size after
short-term strength training (i.e. 4 weeks). It is pos-
sible that the inconsistent results might be because of
variations in testing and training protocols, and in the
muscle groups studied. For example, the size of MEPs
recorded from muscles at rest was unchanged after
training of finger (Carroll et al. 2002, Hortobagyi et al.
2009), wrist (Carroll et al. 2009) or leg muscles (Griffin
& Cafarelli 2007, Schubert et al. 2008), but was
decreased by training of proximal arm muscles (Jensen
et al. 2005). Resting MEP size has been used to provide
an index of ‘baseline’ corticospinal responsiveness that
represents the default characteristics of the pathway
from motor cortex to muscle. From this perspective,
changes in resting MEP size might reflect training-
induced adaptations in the efficacy of synapses and
axonal and/or cellular excitability at cortical sites, or in
synaptic efficacy or cellular excitability at subcortical
sites (n.b. as responses are normalized to the maximal
130 Acta Physiologica  2011 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2011.02271.x
Acta Physiol 2011, 202, 119–140
M-wave in most studies, the possibility that the results
could be because of muscular factors alone can gener-
ally be excluded). However, it is important to consider
carefully what conditions represent ‘rest’. MEPs are
typically considered to be elicited at rest if the target
muscle exhibits EMG silence. However, even in the
absence of overt motoneuron activity, contextual fac-
tors such as muscle history (Stuart et al. 2002) and
motor imagery (e.g. Hashimoto & Rothwell 1999) can
influence MEP size. As it is difficult to control all
relevant (i.e. especially cognitive) factors, there is likely
to be some ‘noise’ in the assessment of corticospinal
responsiveness at rest. If strength training induces
corticospinal adaptations that are subtle, resting MEPs
may lack the precision to detect them.
The variability of the results across studies is even
more apparent for assessments of MEP size during
muscle activation. The majority of studies have assessed
MEP size during weak isometric contraction of the
trained muscles. Under these conditions MEPs have
been shown to increase in the plantar flexor muscles
(Griffin & Cafarelli 2007), be unchanged in finger
muscles (Carroll et al. 2002, Kidgell & Pearce 2010) or
trend lower in arm muscles (Jensen et al. 2005, Carroll
et al. 2009). Changes in MEP size during contractions
of matched strength could potentially be mediated by all
of the factors outlined for resting responses, but are
likely to be affected to a relatively greater extent by
motoneuron firing rate and intrinsic motoneuron firing
properties (Matthews 1999). Only Carroll et al. (2002,
2009) considered MEP amplitudes during strong iso-
metric contractions, and reported reductions in MEP
size for contraction strengths over about 50% MVC in
both finger and wrist muscles. These reductions in
corticospinal responsiveness were likely mediated
largely at the spinal level, as similar results were
obtained when the descending tracts were activated by
transcranial electric stimulation (Carroll et al. 2002)
and stimulation of the corticospinal tract via stimula-
tion at the cevicomedullary junction (Carroll et al.
2009). Although both of these techniques are less
affected by the state of cortical circuits than TMS (see
Di Lazzaro et al. 1998a,b for evidence in relation to
transcranial electrical stimulation), stimulation at the
cervicomedullary junction is the superior method of
dissociating cortical from subcortical effects (Taylor &
Gandevia 2004). This is because corticospinal axons are
activated well caudal to the cortical circuits (excluding
direct influence of cortical excitability to the responses),
and peripheral responses to both TMS and cervicome-
dullary stimulation arise from at least some identical
corticospinal axons (Ugawa et al. 1991, Gandevia et al.
1999, Taylor et al. 2002). Unfortunately, the technique
is painful (particularly if responses at rest are sought),
and it will probably be difficult to recruit large samples
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 Table 3 Summary of studies examining the effect of strength training on MEP size

Muscle Subject Training

Study group details Methods schedule Training intensity Strength gain Results

 2011 The Authors

Carroll et al. 2002 Finger abductors 8 trained TMS at rest 4 weeks Dynamic › 30% MVC M Resting MEPs
8 control TMS and TES during 12 sessions 70–85% initial 1RM fl TES and TMS MEPs
0–60% MVC 4 sets of 8 at >50% MVC
Jensen et al. 2005 Elbow flexors 8 trained TMS at rest 4 weeks Dynamic › 31% 1RM fl Resting MEP max size
Acta Physiol 2011, 202, 119–140

8 control TMS during 10% MVC 12 sessions 10–6RM › 12% MVC and slope
5 sets of 10–6 n.s. trend for same at
10% MVC
Griffin & Cafarelli Dorsiflexors 10 trained TMS at rest 4 weeks Isometric › 18% MVC › MEP size at 10%
2007 10 control TMS during 10% MVC 13 sessions MVC MVC
6 sets of 10 M at rest
Beck et al. 2007 Dorsiflexors 8 trained TMS and H reflex during 4 weeks Ballistic, dynamic Not reported M H-reflex
plantar flexors 10 control fast contraction 16 sessions 30–40% 1RM M SICI or ICF
SICI and ICF at rest 4–6 sets of 10 › TMS during
dorsiflexion in TA
Schubert et al. 2008 Plantar flexors 12 trained TMS-conditioning of H 4 weeks Ballistic, dynamic › Rate of force fl conditioned H-reflex
11 control reflex during rest and 16 sessions 30–40% 1RM development, size in ballistic task but
ballistic tasks 4–6 sets of 10 MVC not not rest
reported
Carroll et al. 2009 Wrist abductors 8 trained TMS and CMEPs during 4 weeks Dynamic › 11% MVC fl MEP and CMEP at
9 control 0–75% MVC 12 sessions 70–85% initial 1RM high contraction
T J Carroll et al.

4 sets of 8 strength
M MEP at rest
Hortobagyi et al. Finger abductors 8 trained TMS at rest 4 weeks Isometric › 38% MVC M MEPs
2009 8 control 10 sessions 70–80% MVC
5 sets of 10
Kidgell & Pearce Finger abductors 8 trained TMS during 5 and 20% 4 weeks Isometric › 34% MVC M MEPs

Acta Physiologica  2011 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2011.02271.x

2010 8 control MVC 12 sessions MVC
6 sets of 10
TMS, transcranial magnetic stimulation; TES, transcranial electrical stimulation; SICI, short-interval intracortical inhibition; ICF, intracortical facilitation; CMEPs, cervico-meduallary evoked
potentials; MVC, maximal voluntary contraction; RM, repetition maximum; n.s., non-significant; TA, tibialis anterior.

131
Æ Neural adaptations to strength training
Neural adaptations to strength training Æ T J Carroll et al.
for studies involving this technique. Carroll et al. (2002)
speculated that the decreases in MEP size after strength
training at high forces could be explained by changes in
the firing rate of the motoneurons or an increase in the
amplitude or duration of motoneuronal after-hyperpo-
larisation potential.
The group of Beck et al. (2007) and Schubert et al.
(2008) assessed TMS responses after a form of strength
training involving ballistic contractions. The size of
MEPs was greater after training when elicited during
the execution of dynamic contractions that resembled
the training task, but not at rest (Beck et al. 2007). The
data indicate a context-specific increase in corticospinal
responsiveness after training. In contrast, the size of
H-reflexes conditioned by subthreshold TMS pulses
was reduced in a task-dependent manner (Schubert
et al. 2008). The H-reflex conditioning technique
involves assessing the degree to which a TMS pulse
(conditioning pulse), that is subthreshold for producing
an MEP on its own, increases the size of an H-reflex
(test pulse) that is elicited near simultaneously (see
Nielsen et al. 1993). As the precise conditioning-test
interval is specified so that the H-reflex is facilitated
only by the earliest (monosynaptic) component of the
descending volley, the conditioned H-reflex results of
Schubert et al. (2008) are consistent with a decrease in
the size of the motor cortical output in response to
TMS. Although adaptations at the cortico-motoneuro-
nal synapse (see Petersen et al. 2003) could also explain
a change in conditioned H-reflex amplitude, the lack of
change in this variable at rest argues against this
possibility. It is difficult to draw general conclusions
from the conflicting results; that is, task-specific
increase in corticospinal excitability revealed by MEPs
versus task-specific decrease in cortical excitability
revealed by TMS conditioning of H-reflexes. However,
the studies illustrate the importance of considering task
context when attempting to categorize the neural
responses to training.
Given the inconsistent results from studies that have
focused on the effect of strength training on MEP size in
muscles directly targeted during training, progress
toward an understanding of the neural responses to
training might be facilitated by reflecting on putative
mechanisms that have been proposed on conceptual
grounds. If a change in the CNS is to enhance strength,
it must act by increasing the activation of motoneurons
that contribute to torque in the desired direction (i.e. by
recruiting additional motoneurons or increasing the
firing rate of motoneurons that innervate agonist and
synergist muscles), or by reducing the activation of
motoneurons that oppose torque in the desired direction
(i.e. antagonist muscles). Since the ability of the CNS to
activate many muscles (i.e. when acting as agonists) is
near maximal (see Gandevia 2001 for review), one
132 Acta Physiologica  2011 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2011.02271.x
Acta Physiol 2011, 202, 119–140
might speculate that the predominant component of the
neural adaptation to strength training should be asso-
ciated with refining circuitry to facilitate activation of
synergists and suppress activation of antagonists. This
reasoning reinforces the notion that MEPs recorded
from agonist muscles may lack the sensitivity to detect
corticospinal adaptations in many contexts. How then
could TMS be used to identify the neural mechanisms
that underlie putative changes in coordination between
agonist, synergist and antagonist muscles?
Use of TMS-induced twitch responses
One obvious approach to studying possible changes in
coordination between muscles after strength training is
to measure MEPs in antagonist and synergist muscles.
However, a major impediment to experiments of this
kind would be the difficulty in obtaining selective
recordings from all of the individual muscles that might
be relevant. At most joints, there are many muscles that
can contribute non-negligible moments, and it is pos-
sible that important functional effects might be brought
about by the combined effect of small changes (i.e. that
are difficult to measure) in multiple muscles. Some of
these muscles will be in close proximity to one-another
(i.e. making selective recording difficult), and some will
be deep (i.e. making detection with surface electrodes
difficult). Another approach is to record the twitch
torque evoked by TMS, which will reflect the net
response in all agonist, synergist and antagonist mus-
cles. The major difficulty here is to ensure that
contractile factors do not contribute to any change in
the responses. Carroll et al. (2009) found that TMS-
evoked twitches were larger during weak background
contraction in the wrist muscles after 4 weeks of
strength training involving wrist abduction. Spinal
factors were likely dominant, since similar results were
obtained for twitches evoked by cervico-medullary
stimulation. There were no differences in twitch ampli-
tudes evoked by supramaximal nerve stimulation
(at rest or during identical voluntary contractions),
suggesting that muscular factors did not underlie the
results. Similarly, Lee et al. (2009) reported increased
TMS-evoked twitch size during high force contractions
in a larger study with an overlapping subject cohort.
They also found that the direction of evoked twitches
shifted toward the training direction. The differences in
the results between the two studies (i.e. no effect on
TMS-evoked twitches at high forces in the Carroll et al.
2009 study), despite identical training parameters, is
probably because of subtle differences in TMS intensity
and the contractile conditions (i.e. whether subjects
matched EMG or torque as a percentage of MVC).
Although the results are consistent with the hypothesis
that strength training causes corticospinal adaptations
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Acta Physiol 2011, 202, 119–140
that facilitate coordination between the muscles
involved in training, many questions remain about the
precise mechanisms involved.
Cortical voluntary activation
Although the technique of twitch interpolation (Merton
1954) is not the focus of this review, it is worth noting
that a version of the method that involves TMS might
have some benefits over ‘traditional’ nerve stimulation
methods for identifying changes in the ability of the
CNS to activate muscles after strength training (see
Todd et al. 2003). Twitch interpolation with nerve
stimulation is limited to assessing voluntary activation
in a single muscle (with motor point stimulation) or in a
group of muscles innervated by a single peripheral
nerve. The nerve stimulation technique also provides no
information about the site of any failure in the capacity
of the CNS to drive the muscles maximally. In contrast,
if TMS can elicit extra force during an MVC, it
indicates that the output from the motor cortex was
suboptimal for driving the motoneurons (see Gandevia
et al. 1996, Todd et al. 2003). Furthermore, given the
relatively poor spatial resolution of TMS, the proximity
of cortical representations of functionally related mus-
cles, and the fact that the corticospinal responsiveness
of muscles activated voluntarily is considerably higher
than resting muscles, the TMS twitch interpolation
method can, in many cases, provide information about
the ability of the motor cortex to drive all of the relevant
agonist and synergist muscles in any given contraction.
It is important to note that for TMS methods of twitch
interpolation to be valid, it is essential that the stimulus
produces a near maximal response in the relevant
muscles. Any degree to which the stimulus is submax-
imal will introduce variability into the measurements,
and substantially submaximal stimulations would result
in invalid results. Nevertheless, the validity and reli-
ability of the method has been demonstrated in the wrist
extensors (Lee et al. 2008), elbow flexors (Todd et al.
2003, 2004) and knee extensors (Sidhu et al. 2009).
Lee and colleagues used twitch interpolation with
TMS to study the influence of strength training on the
ability of the motor cortex to drive wrist muscles after
4 weeks of strength training (Lee et al. 2009). They
found that cortical voluntary activation of the wrist
abductors was high at baseline (94%), and did not
change as a consequence of strength training. However,
the dynamic training was not specific to the isometric
conditions under which voluntary activation was
assessed, and the improvement in MVC was relatively
small (11%). Lee et al. (2010) subsequently showed
that cortical voluntary activation increased for the wrist
extensors in the limb contralateral to the trained
muscles when there was a 30% increase in MVC in
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Acta Physiologica  2011 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2011.02271.x
T J Carroll et al. Æ Neural adaptations to strength training
the trained limb (i.e. produced by isometric training).
These results suggest that the motor cortex is better able
to drive motoneurons during MVC of the untrained,
homologous muscles after strength training. This could
be due to adaptations at any point upstream of the
motor cortical output cells; that is, in the circuitry of the
primary motor cortex, or at any of the secondary motor
cortical areas or subcortical areas that shape the output
of the primary motor cortex. It seems likely that similar
mechanisms might contribute to strength gains in the
trained limb, which might only be detectible when
training causes a considerable increase in MVC.
Use of repetitive TMS (rTMS)
In the studies described above, TMS was used to probe
the responsiveness of the pathway from motor cortex to
muscle. However, in repetitive mode, TMS can also be
used to transiently disrupt ongoing cortical processing,
or to induce persistent (i.e. that outlast the stimulation
by a few minutes to an hour) changes in the respon-
siveness of cortical (n.b. and/or spinal) circuits (see
Fitzgerald et al. 2006, Ziemann et al. 2008 for recent
review). In the only strength training study to date to
use rTMS in this way, Hortobagyi et al. (2009) applied
a low-frequency protocol that is known to induce
lasting corticospinal inhibition (1 Hz for 15 min at
110% of resting motor threshold; Chen et al. 1997) to
the motor cortex after every session in a 4 week
strength training program. The participants who
received rTMS showed impaired strength gains relative
to control subjects by the end of training, which implies
that the cortical or spinal circuits activated by the rTMS
were important substrates for the adaptations that
increased strength. It is important to note that although
rTMS effects are commonly attributed to cortical
factors by default, a spinal origin for effects cannot be
discounted when the stimulus is above the threshold for
a descending volley (n.b. there will be a descending
volley from the brain to the spinal cord at stimulus
intensities well below resting motor threshold; e.g.
Di Lazzaro et al. 1998b).
Although they have yet to be applied to the context of
strength training per se, rTMS protocols that induce
effects that resemble synaptic plasticity in the motor
cortex might allow insights into the nature of corti-
cospinal responses to training. If strength training does
cause cortical adaptations, it seems likely that short-
term changes might be mediated by synaptic processes
similar to those thought to be involved in motor
learning, (e.g. Carroll et al. 2001, Carson 2006, c.f.
Adkins et al. 2006). Long-term potentiation (LTP) is a
likely candidate for the cortical reorganization that
underlies some forms of motor learning (Rioult-Pedotti
et al. 1998, 2000), and inferences about the induction
133
Neural adaptations to strength training Æ T J Carroll et al.
of LTP can be drawn in humans through rTMS
protocols that mimic LTP and long-term depression
(LTD). The principle that allows rTMS approaches to
provide inferences about the induction of LTP- or LTD-
like changes in synaptic efficacy is that of ‘metaplastic-
ity’, or ‘plasticity of plasticity’ (see Abraham & Bear
1996). This principle holds that the effects of any given
plasticity inducing protocol will be regulated depending
on the prior history of synaptic activity. The functional
effect of this process is to maintain synaptic efficacy
within an appropriate range. Thus, the effect of a
protocol that typically enhances corticospinal respon-
siveness will be reduced if it is applied when the targeted
circuits have experienced prior LTP (Ziemann et al.
2004, 2006). Accordingly, the effects of a protocol that
typically suppresses corticospinal excitability will be
enhanced by prior induction of LTP. A series of studies
have used this general approach to argue that a motor
learning training protocol that is not dissimilar to
strength training (i.e. multiple ballistic contractions that
increase peak joint acceleration) causes LTP-like adap-
tations in the motor cortex (Ziemann et al. 2004, Stefan
et al. 2006, Rosenkranz et al. 2007). These studies used
a technique known as paired associative stimulation
(PAS), which involves the application of peripheral
nerve stimulation (to activate muscle afferents) such
that the afferent volley arrives near simultaneously at
the motor cortex with TMS (Stefan et al. 2000).
Approximately 100 stimuli pairs are needed to modu-
late the synaptic efficacy of cortical synapses for an
extended period (see Ziemann et al. 2008 for review). If
the afferent volley arrives at the cortex prior to TMS
[i.e. inter-stimulus interval (ISI) of 10 ms for hand
muscles; PAS10], long lasting depression occurs. If the
afferent volley arrives coincident with, or just subse-
quent to the TMS (i.e. ISI of 25 ms for hand muscles;
PAS25), long lasting facilitation results. PAS protocols
induce effects that share many characteristics with LTP/
LTD; the changes in excitability last for a similar
duration (30–60 min), they are dependent on normal
N-methyl-D-aspartate receptor function, they are spe-
cific to the circuits targeted by stimulation, and are
reversible by protocols that have opposite effects on
synaptic efficacy (see Ziemann et al. 2008 for review).
Although there are many technical challenges in apply-
ing PAS and other rTMS techniques that can induce
synaptic plasticity to strength training studies, the
potential to establish whether strength training induces
LTP-like changes in the motor cortex dictate that the
experiments should be attempted.
Moving forward with TMS studies
There is a lack of consistency in the results of studies
that assessed the effect of strength training on MEPs at
134 Acta Physiologica  2011 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2011.02271.x
Acta Physiol 2011, 202, 119–140
rest or during weak contractions. This suggests that if
training changes the properties of cortical and spinal
circuits projecting to agonist muscles, then the changes
may be too subtle to be detected with MEP approaches
in many contexts. Despite this, there is some evidence
from TMS studies that the responsiveness of motoneu-
rons during high force contractions is reduced after
strength training, that disruption of normal corticosp-
inal processing after training reduces strength gains, and
that training increases the capacity of the motor cortex
to drive the motoneurons during maximal effort. In
order to advance our understanding of the neural
adaptations to strength training, studies that target
specific sites of modulation via converging techniques
(e.g. TMS vs. cervico-medullary stimulation) or condi-
tioning-test approaches are required. Close attention to
the functional context under which the methods are
applied will also be essential. Finally, rTMS protocols
have potential to provide information regarding the
nature of any synaptic plasticity that might be induced
by strength training.
Imaging and EEG studies
Functional magnetic resonance imaging is a non-inva-
sive technique that detects regional changes in cortical
blood flow in response to a task measured as the blood
oxygenation level dependent (BOLD) contrast or ratio
of oxygenated to deoxygenate haemoglobin (see Logo-
thetis 2003 for review). Changes in BOLD response are
interpreted as changes in ‘neural activation’ in fMRI
studies but are not direct measures of synaptic activity
or neuronal action potentials. While the spatial resolu-
tion of fMRI is in the order of a few millimetres,
because the signal is sensitive to vascular changes and
not neuronal activity, the temporal resolution is in the
order of a few seconds.
Using fMRI, Farthing et al. (2007) examined changes
in brain activation following 6 weeks of unilateral
strength training consisting of a maximum isometric
ulnar deviation task. The authors reported widespread
changes in the activation profile in both the contralat-
eral (trained) and ipsilateral (untrained) cortices in
parallel with increased strength in both the trained
(right) and untrained (left) limb. There are, however,
several limitations to the interpretation of changes in
brain activation from fMRI (see Poldrack 2000, Kelly
& Garavan 2005 for review). Firstly, it is not possible to
determine the extent to which areas of activation
detected by fMRI are functionally related to and share
a causal relationship with behaviour, or merely repre-
sent correlated activity associated with task-irrelevant
processing. For example, changes in behavioural output
or cognitive awareness of the imaging process can
influence brain activation measured with fMRI. Infor-
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Acta Physiol 2011, 202, 119–140
mation regarding the mechanisms of cortical changes
associated with strength training might be best achieved
by testing specific predictions regarding changes in brain
activity, based on the known functional roles of cortical
areas and likely time course of the hypothesized effects,
rather than simply documenting changes in cortical
activity in response to training. For example, in assess-
ing transfer of motor skill from one limb to the other,
Perez et al. (2007) found that the level of pre-training
fMRI activity specific to the ventrolateral posterior
thalamic (VLp) nucleus predicted successful future
intermanual transfer. These observations are consistent
with what is known about the associated connections
between VLp, cerebellum and supplementary motor
area, which are all implicated in error prediction and
correction (Butler et al. 2000, Sakai et al. 2002, Died-
richsen et al. 2005). Secondly, using fMRI, it is not
possible to dissociate activity that is excitatory in nature
from that which is inhibitory. Therefore, the overall
activation profiles observed in fMRI studies are a
combination of excitatory and inhibitory neural pro-
cesses and their associated BOLD signal. As such, it is
often unclear how to interpret increases in ‘activity’
based on fMRI.
Another important consideration in interpreting stud-
ies that examine the cortical changes associated with
strength training is the time course of the changes. For
example, observed changes in M1 representation with
motor learning (Pascual-Leone et al. 1994, Karni et al.
1995) are dependent on the time course of measure-
ment. Xiong et al. (2009) found increases in M1 activity
after 2 weeks of motor practice, but activity levels
returned to baseline by week four. It is likely that, if
there are cortical changes associated with strength
training, they are also time dependent. As mentioned
in an earlier section, alterations in cortical activation
which might contribute to early increases in strength
might be associated with generating an increase in
agonist and synergist activation while inhibiting antag-
onist activation. Alternatively, strength training that is
sufficient to result in enhancements in peripheral force
generating capacity, might be expected to result in less
cortical activation to produce a given level of force (i.e.
because fewer motor units would be require activation).
It remains uncertain whether fMRI has sufficient
resolution to detect potentially subtle changes in brain
organization underlying enhanced muscular coordina-
tion in the presence of peripheral changes.
Another technique for monitoring brain activity is
EEG, a non-invasive technique that records electrical
activity in the brain. Surface EEG electrodes measure
voltage changes on the scalp that reflect ion flow caused
by excitatory and inhibitory post-synaptic potentials. As
EEG is derived from post-synaptic potentials in cortical
neurons, it has the advantage of excellent temporal
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Acta Physiologica  2011 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2011.02271.x
T J Carroll et al. Æ Neural adaptations to strength training
resolution (i.e. over fMRI, for example). However, the
spatial resolution of EEG is much lower than most
imaging techniques, such as fMRI. Surface negative
potentials detected at the scalp around the time of
voluntary movement are referred to as movement-
related cortical potentials (MRCP). MRCPs reflect the
summed excitatory post-synaptic potentials of apical
dendrites and are related to the preparation and
execution of self-initiated movement (see Shibasaki &
Hallett 2006 for review). The MRCP waveform has an
onset 1–2 s prior to movement onset and can be divided
into three consecutive phases referred to as (1) the
Bereitschaftspotential (preparation), (2) motor execu-
tion and (3) movement-monitoring potentials. The
amplitude of each component is a function of the
number of active neurons, their synchrony and rate of
discharge (Siemionow et al. 2000). The later MRCP
components have been correlated with force, RFD, and
associated EMG amplitude for both elbow flexion
(Siemionow et al. 2000), and plantar flexion move-
ments (do Nascimento et al. 2005) suggesting that
MRCP is indicative of the level of muscle activation.
A 3-week resistance training program, with increases
in MVC, RFD and EMG in the trained leg extensor
muscles, resulted in changes in MRCP amplitude at
several motor electrode sites (Falvo et al. 2010).
For repetitive submaximal leg extensions, Falvo et al.
(2010) observed an attenuation of MRCP amplitude.
These findings support the hypothesis that by increasing
muscle strength, comparable motor tasks can be
performed with a lower level of neural activation (e.g.
Carroll et al. 2001, Carson 2006). As the force gener-
ating capacity of individual motor units increases with
training, fewer motor neurons are required in order to
accomplish a given submaximal task. Such a reduction
in motor unit recruitment might be reflected in dimin-
ished cortical activation.
Finally, frequency-domain coupling between cortical
activity and spinal motoneuron firing can be captured in
the EEG–EMG coherence signal (see Conway et al.
1995). It has recently been shown that corticomuscular
coherence is lower for strength trained than for non-
trained individuals (Ushiyama et al. 2010), which sug-
gests that the method may have potential for studying
the corticospinal responses to strength training.
General summary and conclusions
In this review, we summarized the available research in
which neurophysiological methods were applied to
study neural adaptations to strength training. Despite
a considerable body of work spanning over 30 years,
there remain many inconsistencies in the data and many
gaps in our understanding. One possible interpretation
of the inconsistent results is that variations in the
135
Neural adaptations to strength training Æ T J Carroll et al.
training task and muscle groups targeted fundamentally
alter the nature of the neural adaptations produced.
However, we do not favour this interpretation. In our
opinion, although there is likely to be a continuum of
changes that will depend upon the precise details of the
training and the characteristics of the involved neuro-
muscular components, we expect that it should ulti-
mately be possible to identify some general principles of
neural adaptation that are applicable to all forms of
strength training that involve systematic repetition of
actions requiring strong neural drive. Clearly, if these
general principles exist, they cannot be identified on the
basis of current data. We conclude that in order to
advance knowledge in this field, studies should be
designed to rigorously account for the limitations of the
available techniques, and be specifically targeted to
address important conceptual questions. Careful con-
sideration of the likely time course of mechanisms to be
studied, and the functional context in which they are
investigated will be critical.
Conflict of interest
None.
This work was supported by the Australian Research Council
(TJC, SR) and the National Health and Medical Research
Council (JGS). The authors thank Dr Michael Lee and
Professors Simon Gandevia and Richard Carson for discussions
that helped shape many of the ideas in this paper.
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