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Training the brain and its connections to muscles

Article in Journal of Applied Physiology · May 2013

DOI: 10.1152/japplphysiol.00503.2013 · Source: PubMed

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Training the brain and its connections to muscles
C. Rae, R. G. Henry and S. C. Gandevia
J Appl Physiol 115:155-156, 2013. First published 2 May 2013; doi:10.1152/japplphysiol.00503.2013

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J Appl Physiol 115: 155–156, 2013;
doi:10.1152/japplphysiol.00503.2013.
Training the brain and its connections to muscles
C. Rae,1 R. G. Henry,2 and S. C. Gandevia1
1
Neuroscience Research Australia and University of New South Wales, Sydney, New South Wales, Australia;
and 2Department of Neurology, University of California, San Francisco, California
Submitted 25 April 2013; accepted in final form 25 April 2013
THERE IS NO DOUBT THAT EXERCISING limb muscles can enhance
their strength and endurance. However, while some obvious
changes occur within the muscles, changes also occur within
the central nervous system. For most muscle groups, there is an
obvious avenue to increase muscle strength, and that is to
increase the level of voluntary activation that accompanies
maximal contractions. Levels of voluntary activation are usu-
ally above 80%, but rarely 100%, with attempted maximal
isometric efforts for most muscle groups (6), and this can be
documented with motor nerve or motor cortical stimulation
(11). Hence, an increase in effective descending drive to
motoneuron pools should increase voluntary muscle force
output, provided that it was not already maximal. This in-
creased drive would recruit more motoneurons or increase their
discharge rate.
A paper in this issue (8) attempts to demonstrate, with the
use of neuroimaging, a change in the corticospinal tract linking
the motor cortex and the spinal cord. Note such a neuroanat-
omical approach cannot provide information about synaptic
properties of the physiological connections with motoneurons.
One group of subjects trained the plantar flexors of the ankle on
their dominant side with 4 wk of maximal voluntary contrac-
tions (16 sessions, each with 36 maximal efforts of 4-s dura-
tion), while the control group had no training. After training,
strength increased by a mean of 39% on the trained side and
30% on the untrained side. The latter change represents a large
cross-training effect and is likely to reflect a learned enhance-
ment of output to motoneurons (2).
Using diffusion tensor imaging (DTI), there was a small but
significant reduction (2%; P ⫽ 0.021) in mean diffusivity
(MD) of the left corticospinal tract between the foot area of the
motor cortex and the cerebral peduncle. Fractional anisotropy
(FA) increased by 1.7%, although this was not significant (P ⫽
0.7). No such changes occurred for the contralateral cortico-
spinal tract in the trained group or for either tract in the control
group. Although the group size for these analyses was small
(ⱕ10), there was a correlation between the improvement in
strength and the reduction in mean diffusivity. Additional
studies examined functional MRI using blood oxygenation
level-dependent imaging during attempted maximal plantar
flexion contractions performed supine in the scanner before
and after training. No changes were observed in activation of
the primary motor cortex for the lower limb.
While the effects of motor learning in the brain have been
studied with neuroimaging, there are much less data on the
effects of strength training. Strength training has been investi-
gated using transcranial stimulation, but the results are contra-
dictory and difficult to unravel (3). Different paradigms have
Address for reprint requests and other correspondence: S. C. Gandevia,
Neuroscience Research Australia, PO Box 1165, Randwick, NSW 2031,
Australia (e-mail: s.gandevia@neura.edu.au).
http://www.jappl.org 8750-7587/13 Copyright © 2013 the American Physiological Society
Invited Editorial
been used, and it is clear that any task focused on strength
training must minimize the effects of confounding complexi-
ties, such as motor learning. This is further complicated by the
motor system itself, which has many levels (e.g., cortical,
subcortical, and spinal) at which direct and indirect changes
can occur. Some of this complexity is depicted in Fig. 1.
The work of Palmer and colleagues (8) does provide a
tantalizing suggestion that strength training may have ramifi-
cations for brain plasticity and, furthermore, that it may affect
a major corticofugal tract involved in force production. While
the new study will generate an interesting hypothesis and is
likely to engender further studies by others, it is probable that,
statistically, the result is marginal. In general, one must ques-
tion the utility of the role of small studies (with low N and
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hence borderline statistical value) to the literature and be
mindful that they can exert undue influence on the field. The
recent report of Button and colleagues (1) highlights the point
that the likelihood of obtaining reliable outcomes from small-N
studies is low, and this is reflected in the contradictory out-
comes of strength training studies already in the literature.
The authors point out, wisely, in their conclusion that further
work is essential. We suggest that such work requires a
carefully designed and controlled strength training paradigm
coupled with a larger sample size (at least 20 subjects). The
work should also include test-retest reliability of the DTI
BRAIN
Motor
‘strength’ ‘learning’ etc
feedback
A1 B1 C1 D1 A2 B2 C2 D2
SPINAL
CORD
A3 B3 C3 D3
MUSCLE
strength
co-ordination
other
Fig. 1. The flow chart shows an abstraction of some possible effects and
observables associated with understanding tissue and functional changes and
their relationships. Experiments that aim to elucidate the associations between,
say, strength training and changes in brain tissue would need to establish that
the paradigm under consideration can properly differentiate them, and that any
observed effects are truly associated with the task. For example, does the task
really reflect only strength and not other activity that may be the cause of
observed tissue changes? What other elements covary with the task? As with
work involved in functional MRI paradigms, appropriate control tasks may
need to be developed so that direct inferences between task activity and
observed changes in neural tissue can be made.
155
Invited Editorial
156
metrics, coupled with measures of confidence in the structural
changes, verified for example, by the bootstrap method (4), so
as to avoid potentially systematic changes due to technical
factors.
Further inspection of the data in the present study reveal that
the DTI metrics varied among the trained group, and, with a
small cohort, the true variability of these metrics is not known.
The changes in MD and FA are driven by data from 3 of the 10
subjects. Is there a decrease in FA associated with a decrease
in MD in one subject? The directional diffusion coefficients
were not presented and may provide some sense of uniformity
in the changes observed in MD and FA. Previous studies
suggest that, in some scenarios, radial diffusivity may be
associated with myelin and axial diffusivity with axonal
changes (7, 9, 10). Decreased MD and increased FA may be
driven by reduction in the radial diffusion. Although not
conclusive, the directional coefficients may provide better
clues about the physiological changes. A priori, physiological
changes in myelin would not be expected to change the MD
value by much, and 2% changes would already be very large;
compared for example to MD changes during maturation (5).
Improved statistical power and investigation of directional
diffusion coefficients could bring these data to the point of
suggesting that new myelination is a good hypothesis that
would need to be further tested with more specific measures
that indicate myelin changes.
The large improvement in maximal voluntary force on the
nontrained side is interesting but not discussed. Results are
given for the mean and standard deviation for the change, but
these do not seem normally distributed. Looking at the median
increase (near zero percent for the untrained group), there is a
larger increase of ⬃40% in the untrained leg compared with
⬃30% in the trained leg. Furthermore, if the untrained side
exhibited a larger (median) change in maximum voluntary
contraction, it is intriguing why are there are no correlations
with the DTI metrics. It may have been instructive to consider
nonparametric approaches to some of the comparisons and
correlations.
In the fields of study of muscle strength, endurance, and
fatigue, there is the ever-present specter of what is cause, what
is effect, and what is an epiphenomenon! So, how should we
view the new study? Our position is that we should be skeptical
but interested to see larger and more detailed studies. Regard-
less of the level of the evidence in this study, it will be cited as
supporting evidence in any future study with similar results,
J Appl Physiol • doi:10.1152/japplphysiol.00503.2013 • www.jappl.org
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and, for this reason alone, it is imperative that overconfident
conclusions or partial views of the data are not presented. If
(and it’s a big if) about 1/2 hr of intense neural activity spread
over 1 mo can alter the cellular properties of the major motor
tract connecting the brain and spinal cord, then we need to
understand the process and its implications.
DISCLOSURES
No conflicts of interest, financial or otherwise, are declared by the author(s).
AUTHOR CONTRIBUTIONS
Author contributions: all authors drafted the manuscript, revised it, and
approved the final version.
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