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Neural representations and the cortical body matrix:
implications for sports medicine and future directions
Sarah B Wallwork,
1
Valeria Bellan,
1
Mark J Catley,
1
G Lorimer Moseley
1,2
1
Sansom Institute for Health
Research and PainAdelaide,
University of South Australia,
Adelaide, South Australia,
Australia
2
Neuroscience Research
Australia, Sydney, New South
Wales, Australia
Correspondence t o
Professor G Lorimer Moseley,
Sansom Institute for Health
Research and PainAdelaide,
University of South Australia,
G.P.O. Box 2471, Adelaide
5001, Australia;
lorimer.moseley@gmail.com
Accepted 8 November 2015
To cite: Wallwork SB,
Bellan V, Catley MJ, et al. Br
J Sports Med Published
Online First: [ please include
Day Month Year]
doi:10.1136/bjsports-2015-
095356
ABSTRACT
Neural representations, or neurotags, refer to the idea
that networks of brain cells, distributed across multiple
brain areas, work in synergy to produce outputs. The
brain can be considered then, a complex array of
neurotags, each influencing and being influenced by
each other. The output of some neurotags act on other
systems, for example, movement, or on consciousness,
for example, pain. This concept of neurotags has
sparked a new body of research into pain and
rehabilitation. We draw on this research and the concept
of a cortical body matrix—a network of representations
that subserves the regulation and protection of the body
and the space around it—to suggest important
implications for rehabilitation of sports injury and for
sports performance. Protective behaviours associated
with pain have been reinterpreted in light of these
conceptual models. With a particular focus on
rehabilitation of the injured athlete, this review presents
the theoretical underpinnings of the cortical body matrix
and its application within the sporting context.
Therapeutic approaches based on these ideas are
discussed and the efficacy of the most tested approaches
is addressed. By integrating current thought in pain and
cognitive neuroscience related to sports rehabilitation,
recommendations for clinical practice and future research
are suggested.
INTRODUCTION
Sports injuries and the pain associated with them
often lead to reduced movement and reduced par-
ticipation in sporting activity. A reduction in move-
ment might occur because of a physiological
impairment (eg, reduced range of motion or
muscle strength), external immobilisation (such as
splinting or bracing), for fear of pain provocation,
because of implicit instruction from a health pro-
fessional or because of fear of further injury or
re-injury. Usually, rehabilitation involves gradually
increasing movement, strength, endurance and skill,
until the athlete is able to fulfil all the requirements
of their chosen activities. The focus of sports
rehabilitation is, understandably, on loading the
tissues in a graded fashion until the athlete and
their sports medicine team, are satisfied that they
can withstand the requirements of recommencing
sport. Another effect of sports injury that is less
readily considered in sports rehabilitation, is the
state of the various cortical representations that
subserve proprioception, movement, the body and
peripersonal space. That is, the role of the brain in
movement planning, preparation and execution,
and the graded exposure of such neural mechan-
isms when returning to sport after injury. Here we
discuss the potential application of current concepts
in cognitive and behavioural neuroscience related
to pain, movement and bodily awareness, to sports
rehabilitation.
THE COMPLEXITIES OF MOTOR PERFORMANCE
Movement and motor performance involve highly
complex interactions between the neural networks
in the brain that represent our body and the space
around us.
1
For example, skilled motor perform-
ance utilises neural representations from visual,
proprioceptive, spatial and tactile domains, enab-
ling us to establish body position and alignment in
relation to the external environment. Such informa-
tion gets continually fed into sensory-motor loops
that constantly update internal predictions about
the outcome of a motor command. This continu-
ous updating promotes smooth, efficient and accur-
ate motor performance
2
as well as optimal
protection and functionality.
1
Both a wide reper-
toire of possible motor strategies, and a precise and
efficient cortical predictive modelling capacity, are
considered important for high level motor com-
mands such as those required in sport.
3
Finely
tuning such a system after injury or inactivity
involves reinstating the capacity of the brain to
integrate these multiple representations and rapidly
run them in a constantly changing and updating
sensory-motor environment. The implications of
this neurological component to sports rehabilita-
tion depends on fundamental matters of neural
representations and their governance.
NEURAL REPRESENTATIONS OR ‘ NEUROTAGS ’
Neural representations, networks or ‘neurotags’
4
are large groups of brain cells that are distributed
across multiple brain areas and that are thought to
evoke a given output. The concept of neural repre-
sentations is a theoretical one, but the theory is
informed by a very large body of empirical data
from fundamental neuroscience research using
brain computer interface, for example,
5
in vivo
animal studies and modelling.
6
Available human
neuroimaging research is also supportive.
7
Conventionally, a neurotag is labelled according to
its output.
6
Each neurotag consists of numerous
brain cells, which can be called member brain cells;
each member brain cell is part of multiple neuro-
tags. A useful analogy for the concept of neurotags
is that of an orchestra—member musicians contrib-
ute to many pieces (outputs) and each piece
(output) involves a group of musicians distributed
across the orchestra (see ref. 4 for a comprehensive
account of this metaphorical conceptualisation).
A primary neurotag effects an action at the end
organ such that its output results in a tangible
Wallwork SB, et al. Br J Sports Med 2015;0:1–8. doi:10.1136/bjsports-2015-095356 1
Rev i ew
outcome. For example, the primary neurotag acts on motor
units and thereby muscles, or evokes a perception such as pain,
or a belief such as ‘my hamstring is weak’ (see also ref. 8 for
extensive review). A secondary neurotag effects an action by
modulating the neuronal mass and precision of primary neuro-
tags and therefore influences the likelihood of that neurotag
being activated (figure 1). Skills required for sport can be con-
ceptualised as the result of activation of primary neurotags,
themselves influenced by activation of secondary neurotags. It is
therefore important to consider the principles that govern the
operation of neurotags, in particular those principles of neur-
onal mass, neuronal precision and neuroplasticity.
5
Neuronal
mass refers to the number of member brain cells in a given neu-
rotag and the synaptic efficacy between them. Neuronal preci-
sion refers to the inhibition of non-member brain cells (see also
ref. 8). The strength of a neurotag determines its influence and
depends on both its neuronal mass and its neuronal precision.
Larger neurotags will predominate over smaller ones; precise
neurotags will predominate over imprecise ones (see also ref. 9
for specific discussion of visual neurotags). The third principle
of neurotags that is very relevant here is that of neuroplasticity
—that property of the nervous system to undergo functional
and structural change in response to activity and
reinforcement.
10
THE CORTICAL BODY MATRIX
A very large number of empirical studies have led to the pro-
posal of a cortical body matrix—a network of neurotags that
subserves the regulation, control and protection of the body and
the space around it, on both a physiological and a perceptual
level
1
(see also refs 11 12 for relevant reviews). Extensive
review of the original experimental and clinical data that under-
pin the cortical body matrix theory is beyond the scope of this
paper, but the theory is captured to some extent by several key
findings. For example, (1) people with pathological arm pain
and the feeling that the arm was swollen performed painful
movements of their hand under four conditions: watching the
arm through a magnifying lens so that the arm looked more
swollen, watching it through a ‘minimising lens’ so that it
looked less swollen and two control conditions.
13
The pain and
swelling evoked by movement was greatest in the magnified con-
dition and least in the minified condition even though the move-
ments themselves were identical; (2) when healthy volunteers
experience a cognitive illusion in which one hand seems to have
been replaced by an artificial counterpart, then the hand that
has been ‘replaced’ becomes cooler
14
and hyper-reactive to his-
tamine in a limb-specific manner that is positively related to the
vividness of the illusion;
15
when the limb is first cooled, the illu-
sion is made stronger;
16
(3) when amputees with an intact
phantom limb learn how to perform a biomechanically impos-
sible movement with their phantom limb, they report simultan-
eous shifts in the internal structure of their phantom and the
ability to perform the movement. What is more, some physio-
logical movements are rendered more difficult in line with the
new structure of the phantom;
17
when people with pathological
arm pain and an associated cold arm cross their hands over the
body midline, then the painful hand warms up and the healthy
hand cools down relative to the healthy one and this effect
depends not on where the limbs actually are, but where they are
perceived to be.
18 19 20
Each of these findings demonstrate a
tight connection between our bodily feelings, for example pain,
swelling, location and ownership, and physiological regulation,
for example, movement, swelling, temperature control and
inflammatory responses.
The pertinence of the cortical body matrix theory to return
to sport after injury is threefold: (1) it provides a working
model that integrates the complex proprioceptive, motor and
spatial representations that are involved in sport, particularly
those sports involving equipment (eg, balls) or athlete-to-athlete
interaction; (2) it stipulates that neurotags, the outputs of which
act on end organs (eg, muscles or blood vessels) are closely
integrated with neurotags, the outputs of which are feelings
(eg, a feeling of warmth, or pain); (3) it implies that both exter-
nal and internal events or situations, including the location of
body parts, are mapped spatially according to a frame of refer-
ence centred about oneself (‘egocentric’),
18 19 20
and according
to a frame of reference centred on an external object or limb
(‘allocentric’).
21
This implies that spatial tasks that interrogate
both frames of reference should be incorporated into
rehabilitation.
Proprioception provides an excellent model with which to
understand the idea of secondary neurotags influencing primary
neurotags. For example, proprioceptive awareness (where you
feel a body part to be) can be considered the output of a
primary neurotag. There are many influences on this primary
neurotag, for example, that from visual input, somatosensory
Figure 1 Secondary neurotags are
those that exert their influence over
primary neurotags. Primary neurotags
are those that evoke an output, for
example, a motor command, a feeling
or a conscious belief.
2 Wallwork SB, et al. Br J Sports Med 2015;0:1–8. doi:10.1136/bjsports-2015-095356
Rev i ew
input (that detected by mechanoreceptors and propriocep-
tive organs in the peripheral nervous system) and internally
generated inputs related to effort and force.
22
Each of these
inputs onto the primary neurotag is generated by secondary
neurotags.
These ideas have been explored previously in the body local-
isation and motor control literature where the terms ‘stability’
or ‘reliability’ of the modality are reasonably analogous to the
neuronal mass and precision of the subserving neurotags. In par-
ticular the Maximum Likelihood Estimation theory
23
states that
the nervous system combines the information coming from the
different sensory modalities in a statistically optimal fashion.
Generally speaking, when both vision and proprioception are
available at the same time, vision dominates the output, suggest-
ing that the vision-specific neurotag carries much greater influ-
ence than the somatosensory-specific neurotag, according to
their relative neuronal mass and precision. This predominance
of visually encoded neurotags over somatosensory encoded neu-
rotags can be readily observed in illusions that exploit the usual
strength of vision to render the perceived location of a limb
inaccurate. For example, in the Disappearing Hand Trick
24
par-
ticipants are encouraged to look at their hands and maintain
their position relative to a visual cue, but are naïve to the
experimental trick that means their hands are actually moving
such that the felt location of one hand is rendered completely
inaccurate. In this scenario, the neuronal mass and precision of
the visually encoded secondary proprioceptive neurotag far out-
weighs that of the somatosensory encoded one, such that the
hand is felt to be in the location the visual system suggests it to
be, even though it is not (figure 2).
The third principle of neurotags—neuroplasticity—imparts its
effects by modulating both the strength and precision of neuro-
tags. This is a critical consideration during rehabilitation
because neuroplasticity ‘works both ways ’ on neurotags—to
increase or decrease the likelihood of their activation. According
to the principle of neuroplasticity, changes in the movement and
behaviour repertoire lead to motor learning such that the ease
with which different motor outputs are generated is altered in
a use-dependent manner. The less active a particular neurotag,
the weaker and less precise it becomes; the more active a par-
ticular neurotag, the stronger and more precise it becomes (up
to a point, at which member brain cells appear to become
‘disinhibited’
25
or imprecise, which has potentially profound
implications when considered within the cortical body matrix
framework—see below).
These fundamental matters—of neurotags and the cortical
body matrix—present three important implications for sports
rehabilitation: that by remaining cognisant of the principles that
govern neurotags, we can appreciate how (secondary) neurotags
related to actual or implied danger can influence (primary) neu-
rotags of motor output; that by exploiting these principles we
can more effectively find the optimal balance between protec-
tion and rapid return to full performance and we can ensure
that the neuroplastic effects of altered activity can be limited by
integrating ‘virtual rehabilitation’ into physical rehabilitation;
that by remaining cognisant of the tight and bidirectional link
between neurotags that produce body-related outputs and those
that produce feeling-related outputs, we can use one to modu-
late the other.
To appreciate the potential importance of these implications,
let us consider the relationship between pain and motor output.
The dominant paradigm is that pain causes altered motor
control. We contend that this paradigm implants a false hier-
archy in which pain is considered a lower order event that
occurs to an individual, and that motor control will normalise if
pain is eradicated. That motor control changes might also cause
pain depends on nociceptive stimulation and the completion of
a ‘ vicious cycle’. We suggest instead that pain and motor control
are outputs of primary neurotags, intimately linked but not hier-
archically differentiated. We contend that both are modulated
by a range of secondary neurotags (figure 3A). The common
experimental paradigm that underpins the dominant model
involves nociceptive stimulation, which evokes both pain and
altered motor output.
26 27
We are among those who have
naively attributed alterations in motor output to pain, when the
design does not allow us to differentiate pain from nociceptive
stimulation. That is, we mistake association for causation. There
is now a compelling body of literature that points to the pro-
blems with the dominant model at a theoretical and empirical
level
28 29 30
(also see ref. 31 for the theoretical underpinnings
of this contention). Nociception is neither sufficient nor neces-
sary for pain. That is, activity in primary nociceptors—high
threshold free nerve endings located in the tissues of the body—
and their projections, which are collectively responsible for
Figure 2 Localisation of a limb and performing a task, as conceptualised according to neurotags and the principle of neuronal mass and precision,
together constituting the strength of the neurotag and its resultant influence over the primary neurotag. Here, the weight of the lines denotes
neuronal strength, itself a reflection of the number of neurones in the neurotag and its synaptic efficacy, which determines its influence over the
subsequent primary neurotag or end output. During localisation of the limb and task performance, the neurotag that represents the visually
identified location of the limb is very strong and exerts a greater influence than the neurotag that represents the somatosensory or proprioceptively
identified location of the limb, over both the feeling neurotag (where does it feel to be?) and the movement neurotag (what motor command will
achieve the correct trajectory from the limb’s current location).
Wallwork SB, et al. Br J Sports Med 2015;0:1–8. doi:10.1136/bjsports-2015-095356 3
Rev i ew
detecting, transforming and transmitting a danger message to
the brain, is now considered just one contributor to pain. We
suggest that the same applies for protective motor outputs—
nociception is just one contributor, albeit an influential one, to
protective motor outputs (figure 3B).
That movement prioritises protection is reflective of a highly
complex and multifactorial process that promotes self-survival.
Enhanced protective movement and behaviour has been demon-
strated in a range of clinical pain disorders, where people in
pain have upregulated defensive reflexes. In a recent
meta-analytical systematic review ( personal communication,
2015, Wallwork et al), we showed that the threshold at which
reflex responses are triggered is lower in people with pain than
it is in healthy controls, but that this augmentation could not be
explained by tissue-based sensitivity, peripheral sensitisation or
spinal sensitisation. Rather, the augmentation of these thresh-
olds, appears to be driven by online descending facilitation.
That is, it seems that the immediate and current evaluation of
threat to body tissue modulates fine tuning of motor output
right down to the level of short-loop reflexes. Moreover, the
hand blink reflex is upregulated when the hand is closer to the
face. This upregulation occurs in real time and indeed in a feed-
forward manner if the hand is moving (personal communica-
tion, 2015, Wallwork et al), but the upregulation is absent if a
physical barrier is placed between the hand and the face.
32
These results clearly show that a complex evaluative process
associated with the perception of danger to body tissues modu-
lates sensitivity of supposedly ‘automatic’ reflex motor
responses. Applying the neurotag model to these discoveries, we
can see that each of the cues, for example, the presence of a
physical barrier, is represented by a secondary neurotag that
influences the primary descending modulation neurotag.
THE EFFECT OF INJURY A ND INACTIVITY O N THE
CORTICAL BODY MATRIX
The effects of injury and inactivity on the cortical body matrix
can be considered in terms of both the change in secondary neu-
rotags that influence motor output and perception, and the
effects of neuroplasticity. The idea that pain is simply a reflec-
tion of tissue state was elegantly dismantled several decades
ago
33
and there is now widespread endorsement of a truly biop-
sychosocial conceptualisation of pain in the scientific,
34
clinical
4
and lay
35 36 37
literature outside of the sports rehabilitation
field. A modern conceptualisation of pain emphasises its multi-
factorial nature—a protective conscious feeling that compels the
sufferer to protect their body from danger.
38
As such, any infor-
mation that implies danger to body tissue will be represented by
secondary neurotags that influence the primary ( pain) neurotag,
making it more likely to fire. Any information that implies
safety to body tissue will also be represented by secondary
Figure 3 (A) The dominant, but we
contend less accurate
conceptualisation of the relationship
between pain and motor control using
the model of neurotags. Here,
movements are considered a
consequence of pain, instead of a
closely related but independent output
of the cortical body matrix. Line
weights denote the differential
influence of different secondary
neurotags on the primary neurotag.
(B) Conceptualisation of pain and
motor control according to the
influence of secondary neurotags. Line
weights denote the differential
influence of different secondary
neurotags on the primary neurotag.
Here, secondary neurotags driven by
nociception have greatest influence
over both the pain and movement
neurotags. Note that perceived current
body position/location exerts a strong
influence over the movement neurotag
but not the pain neurotag.
4 Wallwork SB, et al. Br J Sports Med 2015;0:1–8. doi:10.1136/bjsports-2015-095356
Rev i ew
neurotags that also influence the primary (pain) neurotag,
making the pain neurotag less likely to fire.
35
This is conceptu-
ally simple even though the biological processes underpinning it
are very complex and far from completely understood. The con-
ceptual shift from the previous structural-pathology model to
the current biopsychosocial protection-based model, is now seen
as a therapeutic target, most obviously by explaining pain, a
range of educational strategies that teach people about pain
biology.
4353839
Indeed, reconceptualisation of pain is now
considered a fundamental objective of chronic pain rehabilita-
tion.
38
We contend that it should also be integral to sports
rehabilitation. These principles extend beyond pain, however, to
other protective outputs of the cortical body matrix, for
example, fatigue, anxiety, fear, dyspnoea, stiffness and weakness,
all of which can be conceptualised as protective feelings,
40
and
upregulated inflammatory response, increased cortisol produc-
tion, elevated heart rate, all of which can be conceptualised as
protective regulatory responses.
Neuroplasticity
The principle of neuroplasticity can be applied to sports
rehabilitation in several ways. For example, repeated activation
of secondary neurotags that represent danger to body tissue will
increase their neuronal mass and precision, thereby increasing
their influence on pain and the other protective outputs includ-
ing motor output; decreased activation of primary performance-
dedicated motor neurotags will decrease their neuronal mass
and precision, reducing the likelihood that they will be acti-
vated. That is, the potentially broad range of neurotags that are
associated with most sports, becomes less broad, and certain
neurotags become less easily accessible when sought for a quick
and efficient motor execution. According to Bayesian theory,
this shift in propensity to engage the optimal motor outputs is
conceptualised as reflecting fine tuning of the relevant neurotag
based on previous experiences.
41
We also make predictions
about external environmental factors based on the probabilities
of events that have occurred in the past, also called ‘priors’, and
these probabilities are based on experience of such events.
Therefore, the less often these movements are performed, the
less efficient and less precise these movements become, by
virtue of the reduced neuronal mass and precision of their sub-
servant neurotags. The predictable consequence then, would be
greater error in motor performance and an increased risk for
further injury.
ASSESSMENTS
Motor assessments
Although these concepts are not new, their clinical application is
only just gaining ground. One objective of the research in this
area is the development of clinical assessments that target the
integrity of the neurotags of the cortical body matrix. The most
advanced of these research streams involves motor imagery,
8
with deficits in performance being clearly related to clinical phe-
nomena such as pain and training being clearly related to
improvement in those clinical phenomena. Imagining movement
of one’s own body is a form of explicit motor imagery. That is,
the person imagining the movement is aware that that is what
they are doing. Implicit motor imagery, on the other hand,
involves cortical motor processing or the activation of motor
neurotags, but without awareness.
8
Implicit motor imagery can
be assessed using choice reaction time tasks, most commonly a
judgement as to whether a pictured body part belongs to the left
or right side of the body.
42
Left/right judgements, such as of
hands, involves two stages—an initial ‘automatic’ judgement,
followed by mentally manoeuvring one’s own hand from its
current position into the position of the target hand—a process
called ‘confirmation’.
42
In terms of cortical representation
theory, the confirmation process engages secondary propriocep-
tive and spatial neurotags, which exert an infl uence on the
primary motor neurotag, but do not activate it—thus, there is
no movement.
43
Left/right judgements like this have been
widely studied in healthy participants
42 44 45
and in people with
pain. As a general rule, performance is reduced for implicit
motor imagery of the affected body part, but not unaffected
body parts. For example, people with low back pain perform
badly on the left/right trunk rotation task but not a left/right
hand judgement task;
45 46
people with complex regional pain
syndrome (CRPS) of the hand perform badly on left/right hand
judgement task but not the left/right knee judgement
task.
47 48 49
Similar segment-specificdeficits have been reported
in people with neck pain,
50
painful knee osteoarthritis
20
and leg
pain.
51
Implicit motor imagery interrogates secondary neurotags, so
deficits in motor imagery reflect problems upstream to move-
ment execution—in movement preparation processes, for
example. These reaction time tests provide two metrics—accur-
acy and reaction time—which are thought to reflect different
aspects of the task, and therefore different sets of neurotags.
Accuracy deficits are interpreted as reflecting disruption
(decreased neuronal mass or precision) of proprioceptive neuro-
tags that are then used for movement, and reaction time deficits
are interpreted as reflecting disruption of spatial neurotags,
whereby the neurotags that represent one side or area of space
have greater neuronal strength than those representing another
area and therefore exert a greater influence on the automatic
decision stage of the task (see refs 852).
Implicit motor imagery is easily assessed using commercially
available software (eg, ‘Recognise’—noigroup.com, Adelaide,
Australia) on computers, tablets or smart phones. Users can
obtain immediate data on both accuracy and reaction time and
keep online records to track performance over time. Clinicians
can monitor patient practice and performance remotely.
Tactile acuity
Tactile neurotags—those that represent our feeling of touch on
the body—are also implicated in many pain disorders and train-
ing tactile performance has been associated with pain reduc-
tion.
53 54
Tactile acuity depends on the integrity of tactile
transducers—specialised receptors on the terminals of Aβ neu-
rones,
55
—transmission of the sensory signal to the brain and
activation of the appropriate secondary neurotag (see ref. 56 for
comprehensive review). Body part-specificdeficits in tactile
acuity have been documented in people with CRPS,
57 58 59 60
non-specific chronic low back pain,
61 62 63
facial pain
64
and
arthritis.
65
These deficits cannot be explained by detection of
the signal, transduction or transmission, but are instead attribu-
ted to disruption (decreased neuronal mass or precision) of the
subserving neurotag.
66
We would like to raise the possibility that the evidence
obtained from clinical populations, and outside the sporting
context, may be relevant to those with sporting injuries. Our
own clinical observations seem to uphold this possibility and
preliminary empirical studies are corroborative.
67 68
Perhaps sur-
prisingly, there are no systematic differences in motor imagery
performance between those who do and do not participate in
sport.
69
In fact, that regular participation in yoga does not
appear to enhance performance
70
and that people who experi-
ence regular bouts of dizziness do not appear to have disrupted
Wallwork SB, et al. Br J Sports Med 2015;0:1–8. doi:10.1136/bjsports-2015-095356 5
Rev i ew
performance,
71
strengthens the implication that disrupted per-
formance is reasonably specific for disrupted body-part specific
representations. ‘Sporting injuries’ are clearly not a homogenous
group—the implications of the body of literature in this field are
probably different for those with chronic or recurrent sports-
related pain as compared to those with, for example, an acute
cruciate ligament tear. Implications may exist for both, however.
That is, the commonalities between chronic and recurrent pain
problems experienced by professional, recreational or indeed
‘industrial’ athletes, suggests generalisability of findings across
these groups. However, consideration of cortical representations
in acute sporting injury rehabilitation is a relatively unexplored
field. One might propose a role in the maintenance of coherent
neurotags even when movement is not possible, but this idea
has not, to our knowledge, been investigated. Nonetheless, we
would contend that representation theory and the cortical body
matrix theory, insofar as they relate to human behaviour and
function, should be equally applicable to humans who are
engaged in sport as they are to humans who are not. Clearly
until empirical data are obtained, these contentions remain
theoretical.
THE POTENTIAL ROLE OF NEUROTAG REHABILITATION IN
RETURN TO SPORT
As mentioned above, treatments that target secondary motor or
tactile neurotags promote clinical recovery in those with chronic
pain. Evidence is most established for graded motor imagery
(GMI)
72
(see ref. 8 for a comprehensive review) and tactile dis-
crimination training
53 54 73 74
(see refs 11 and 12 for relevant
reviews) but other approaches are confined at this stage to case
studies and observational accounts.
The proposed mechanism behind GMI is that it uses a graded
exposure paradigm to reinstate normal (non-protective) motor
neurotags. GMI involves a three-step process; implicit motor
imagery, explicit motor imagery (imagined movements) and
mirror therapy.
8
The sequence of steps appears to be important,
at least for the severely disabling and painful condition of
CRPS.
75
Recommendations for GMI include performance
during exposure to cues that signal danger to body tissue. Such
cues are individually-specific but may include time of day, loca-
tion, noise, competition, stress, fatigue, cognitive load, all of
which may be addressed by simply modifying the context of
GMI training. Importantly, GMI can be undertaken well in
advance of physical rehabilitation. This is a key implication of
this emerging field—that the normal decrease in neuronal
strength and precision that occurs when a neurotag is taken ‘off
line’ might be avoided by regular and varied ‘virtual ’ training.
GMI forms an empirically tested subset of imagery applications,
but we contend that the principles captured by GMI should
apply to less formalised application of motor imagery. That is,
‘neurotag maintenance’ might be as simple as motor imagery in
the presence of performance-related cues. A thorough subjective
examination about the injury and associations related to the
injury could shed light on potentially threatening cues that
could be integrated into neurotag rehabilitation well in advance
of physical rehabilitation. For example, the extent and the
context of the injury, the time of day the injury was sustained,
the mood the athlete was in, weather conditions, background
noise, other team players involved, might all constitute ‘cues of
danger to body tissue’. To appreciate the potential importance
of these considerations, one must only appreciate that each of
these sensory and contextual cues are transformed into neural
activity and therefore exert some kind of influence over lower
level neurotags within the cortical body matrix. It is worth
reiterating here that the influence of neurotags on other neuro-
tags, and ultimately on outputs such as movement, immune
responses and feelings, is determined by neuronal mass and pre-
cision and that both are open to modification via the principle
of neuroplasticity.
Tactile discrimination training can also be undertaken well in
advance of physical and sporting rehabilitation. Such training
involves a forced choice between at least two different tactile
stimuli, relying only on somatosensory information to make that
choice. The most tested protocol is to first identify several
potential locations at which the participant might receive a
tactile stimulus, stimulate at one location and ask the patient to
identify which location was stimulated.
53 54 74 76
According to
the principles of neurotags, the nature of the stimulus is not
important but the requirement to differentiate it from similar
stimuli is. That spatial neurotags can also be disrupted implies
that training spatial acuity will also offer benefits, although evi-
dence for this is lacking and it remains, for now, conjecture.
Perhaps surprisingly, there is a dearth of research on the use
of such interventions for acute sporting injuries, despite known
motor performance disruptions in association with such condi-
tions. Those treatments could be delivered and tailored accord-
ing to the outcome of assessments and according to the array of
neurotags normally involved in the chosen sport; motor
imagery tasks could be modified to interrogate sport-specific
neurotags, for example, including context-relevant and
equipment-relevant images.
IMPORTANT CAVEATS AND FUTURE DIRECTIONS
We have proposed that the principles that govern neural repre-
sentations, or neurotags, are of fundamental importance to
sports rehabilitation. We contend that incorporating neurotag
assessment and retraining as a component of sport rehabilita-
tion, in the light of tight inter-relationships between how our
body is regulated and how it feels, will limit the deleterious
effects of inactivity on neurotags, and hasten and optimise
reinstatement of performance-related neurotags. We also
contend that motor output and other protective outputs might
be modulated by any credible evidence of danger regardless of
whether or not the individual is in pain. If so, in situations
where performance quality is key and executing a precise move-
ment is vital, identifying and eliminating potential danger-
related cues may be critical. Notably, the patient’s understanding
of the biological reasons to take this approach would also seem
critical.
Our contentions are based on a very large body of empirical
work outside of the sporting context, but, as it is applied to the
sporting context, it is limited to personal experience and anec-
dotal evidence. This is an important caveat and, in light of it,
this review primarily serves to provide a provocative account of
What are the findings?
▸ Recent advances in theoretical models of pain and
rehabilitation are relevant to sporting injuries.
▸ The brain’s representation of movements and skills is a
viable target for rehabilitation.
▸ Movements and skills can be thought of as outputs of
‘neurotags’.
▸ Recognised paradigms for understanding pain are applicable
for understanding movements and skills.
6 Wallwork SB, et al. Br J Sports Med 2015;0:1–8. doi:10.1136/bjsports-2015-095356
Rev i ew
current thought in pain and cognitive neuroscience and possibil-
ities for the sports medicine field. That some of the assessments
and treatments that are based on these ideas are becoming more
common in the sporting context does not constitute evidence of
their prognostic or therapeutic value. Nonetheless, perhaps this
review will spark a new conversation and line of research
enquiry.
Contributors SBW and GLM contributed to the conceptualisation, planning,
literature review and writing of this manuscript. VB and MC contributed to the
literature review and writing of this manuscript. GLM is responsible for the overall
content of this manuscript.
Funding SBW is supported by an Australian Postgraduate Award from the
Australian Government. GLM is supported by a Principal Research Fellowship from
the National Health & Medical Research Council of Australia ID 1061279. This work
draws on findings from projects supported by the National Health & Medical
Research Council of Australia IDs 630431, 1008017, 1047317.
Competing interests GLM receives royalties for books that are directly related to
the material presented here and payments for the delivery of professional
development courses. He consults to Pfizer and to Workers' Compensation Boards in
Australia, Europe and North America.
Provenance and peer review Not commissioned; externally peer reviewed.
REFERENCES
1 Moseley GL, Gallace A, Spence C. Bodily illusions in health and disease:
physiological and clinical perspectives and the concept of a cortical ‘body matrix’.
Neurosci Biobehav Rev 2012;36:34–46.
2 Wolpert DM, Ghahramani Z. Computational principles of movement neuroscience.
Nat Neurosci 2000;3:1212–17.
3 Classen J, Liepert J, Wise SP, et al. Rapid plasticity of human cortical movement
representation induced by practice. J Neurophysiol 1998;79:1117–23.
4 Butler DS, Moseley GL. Explain pain. 2nd edn. Adelaide: Noigroup Publications,
2013.
5 Nicolelis MAL, Lebedev MA. Principles of neural ensemble physiology underlying the
operation of brain-machine interfaces. Nat Rev Neurosci 2009;10:530–40.
6 deCharms RC, Zador A. Neural representation and the cortical code. Annu Rev
Neurosci 2000;23:613–47.
7 Bushnell MC, Villemure C, Strigo I, et al. Imaging pain in the brain: the role of the
cerebral cortex in pain perception and modulation. J Musculoskelet Pain
2002;10:59–72.
8 Moseley G, Butler D, Beames T, et al. The graded motor imagery handbook.
Adelaide: NOIgroup publishing, 2012.
9 Desimone R, Duncan J. Neural mechanisms of selective visual attention. Annu Rev
Neurosci 1995;18:193–222.
10 Chang Y. Reorganization and plastic changes of the human brain associated with
skill learning and expertise. Front Hum Neurosci 2014;8:35.
11 Moseley GL, Flor H. Targeting cortical representations in the treatment of chronic
pain: a review. Neurorehabil Neural Repair 2012;26:646–52.
12 Wand BM, Parkitny L, O’Connell NE, et al. Cortical changes in chronic low back
pain: current state of the art and implications for clinical practice. Man Ther
2011;16:15–20.
13 Moseley GL, Parsons TJ, Spence C. Visual distortion of a limb modulates the pain
and swelling evoked by movement. Curr Biol 2008;18:R1047–8.
14 Moseley GL, Olthof N, Venema A, et al. Psychologically induced cooling of a
specific body part caused by the illusory ownership of an artificial counterpart. Proc
Natl Acad Sci USA 2008;105:13169–73.
15 Barnsley N, McAuley J, Mohan R, et al. The rubber hand illusion increases
histamine reactivity in the real arm. Curr Biol 2011;21:R945–6.
16 Kammers MPM, Rose K, Haggard P. Feeling numb: temperature, but not thermal
pain, modulates feeling of body ownership. Neurospychologia 2011;49:1316–21.
17 Moseley G, Brugger P. Interdependence of movement and anatomy persists when
amputees learn a physiologically impossible movement of their phantom limb. Proc
Natl Acad Sci USA 2009;106:18798–802.
18 Moseley GL, Gallace A, Spence C. Space-based, but not arm-based, shift in tactile
processing in complex regional pain syndrome and its relationship to cooling of the
affected limb. Brain 2009;132:3142–51.
19 Moseley GL, Gallace A, Iannetti GD. Spatially defined modulation of skin
temperature and hand ownership of both hands in patients with unilateral complex
regional pain syndrome. Brain 2012;135(Pt 12):3676–86.
20 Stanton T, Lin C, Smeets R, et al . Spatially defined disruption of motor imagery
performance in people with osteoarthritis. Rheumatology (Oxford)
2012;51:1455–64.
21 Behrmann M, Tipper SP. Attention accesses multiple reference frames: evidence
from visual neglect. J Exp Psychol Hum Percept Perform 1999;25:83–101.
22 Proske U, Gandevia SC. The proprioceptive senses: their roles in signaling body
shape, body position and movement, and muscle force. Physiol Rev
2012;92:1651–97.
23 Ernst MO, Banks MS. Humans integrate visual and haptic information in a
statistically optimal fashion. Nature 2002;415:429–33.
24 Newport R, Gilpin HR. Multisensory disintegration and the disappearing hand trick.
Curr Biol 2011;21:R804–5.
25 Di Pietro F, McAuley JH, Parkitny L, et al. Primary motor cortex function in complex
regional pain syndrome: a systemtic review and meta-analysis. J Pain
2013;14:1270–88.
26 Arendt-Nielsen L, Graven-Nielsen T, Svarrer H, et al. The influence of low back pain
on muscle activity and coordination during gait: a clinical and experimental study.
Pain 1996;64:231–40.
27 Graven-Nielsen T, Svensson P, Arendt-Nielsen L. Effects of experimental muscle pain
on muscle activity and co-ordination during static and dynamic motor function.
Electroencephalogr Clin Neurophysiol 1997;105:156–64.
28 Moseley GL, Hodges PW. Are the changes in postural control associated with low
back pain caused by pain interference? Clin J Pain 2005;21:323–9.
29 Moseley GL, Hodges PW. Reduced variability of postural strategy prevents
normalization of motor changes induced by back pain: a risk factor for chronic
trouble? Behav Neurosci 2006;120:474–
6.
30 Moseley GL, Nicholas MK, Hodges PW. Does anticipation of back pain predispose
to back trouble? Brain 2004;127:2339–47.
31 Moseley GL. Trunk muscle control and back pain: chicken, egg, neither or both?
In: Hodges PW, Cholewicki J, van Dieen JH, eds. Spinal control: the rehabilitation of
back pain. Oxford, UK: Churchill Livingstone Elsevier, 2013:123–31.
32 Sambo CF, Forster B, Williams SC, et al . To blink or not to blink: fine cognitive
tuning of the defensive peripersonal space. J Neurosci 2012;32:12921–7.
33 Wall PD, McMahon SB. The relationship of perceived pain to afferent nerve
impulses. Trends Neurosci 1986;9:254–5.
34 Wiech K, Vandekerckhove J, Zaman J, et al.Influence of prior information on
pain involves biased perceptual decision-making. Curr Biol 2014;24:
R679–81.
35 Moseley GL, Butler DS. The explain pain handbook: protectometer. 1st edn.
Adelaide, Australia: Noigroup Publications, 2015.
36 Moseley GL. Painful yarns. Metaphors and stories to help understand the biology of
pain. Canberra: Dancing Giraffe Press, 2007.
37 Wall P. Pain. The science of suffering. London: Orion Publishing, 1999.
38 Moseley GL, Butler DS. Fifteen years of explaining pain: the past, present and
future. J Pain 2015;16:807–13.
39 Lotze M, Moseley GL. Theoretical considerations for chronic pain rehabilitation.
Phys Ther 2015;95:1316–20.
40 Williams MT, Gerlach Y, Moseley L. The ‘survival perceptions’: time to put some
Bacon on our plates? J Physiother 2012;58:73–5.
41 Kölding KP, Wolpert DM. Bayesian decision theory in sensorimotor control. Trends
Cogn Sci 2006;10:319–26.
42 Parsons LM. Imagined spatial transformations of one’s hands and feet. Cogn
Psychol 1987;19:178–241.
43 Parsons LM. Integrating cognitive psychology, neurology and neuroimaging. Acta
Psychol (Amst) 2001;107:155–81.
44 Wallwork SB, Butler DS, Fulton I, et al. Left/right neck rotation judgments are
affected by age, gender, handedness and image rotation. Man Ther
2013;18:225–30.
45 Bowering KJ, Butler DS, Fulton IJ, et al. Motor imagery in people with a history of
back pain, current pain, both, or neither. Clin J Pain 2014;30:1070–5.
46 Bray H, Moseley GL. Disrupted working body schema of the trunk in people with
back pain. Br J Sports Med 2011;45:168–73.
47 Schwoebel J, Coslett HB, Bradt J, et al. Pain and the body schema: effects of pain
severity on mental representations of movement. Neurology 2002;59:775–7.
48 Schwoebel J, Friedman R, Duda N, et al. Pain and the body schema: evidence for
peripheral effects on mental representations of movement. Brain
2001;124:2098–104.
How might it impact on clinical practice in the future?
▸ Broaden the assessment of those in pain to include domains
implicated in modern pain-related theory.
▸ Broaden intervention, for example:
– Training neurotags to prevent deleterious impact of
neuroplasticity after sporting injuries
– Training neurotags to optimise rehabilitation after
sporting injuries
Wallwork SB, et al. Br J Sports Med 2015;0:1–8. doi:10.1136/bjsports-2015-095356 7
Rev i ew
49 Moseley GL. Why do people with complex regional pain syndrome take longer to
recognize their affected hand? Neurology 2004;62:2182–6.
50 Elsig S, Luomajoki H, Sattelmayer M, et al. Sensorimotor tests, such as movement
control and laterality judgment accuracy, in persons with recurrent neck pain and
controls. A case-control study. Man Ther 2014;19:555–61.
51 Coslett HB, Medina J, Kliot D, et al. Mental motor imagery and chronic pain: the
foot laterality task. J Int Neuropsychol Soc 2010;16:603–12.
52 Bellan V, Gilpin HR, Stanton TR, et al. Untangling visual and proprioceptive
contributions to hand localisation over time. Exp Brain Res 2015;233:1689–701.
53 Moseley GL, Wiech K. The effect of tactile discrimination training is enhanced when
patients watch the reflected image of their unaffected limb during training. Pain
2009;144:314–19.
54 Moseley GL, Zalucki NM, Wiech K. Tactile discrimination, but not tactile stimulation
alone, reduces chronic limb pain. Pain 2008;137:600–8.
55 Johnson KO, Yoshioka T, Vega-Bermudez F. Tactile functions of mechanoreceptive
afferents innervating the hand. J Clin Neurophysiol 2000;17:539–58.
56 Gallace A, Spence C. In touch with the future: the sense of touch from cognitive
neuroscience to virtual reality. Oxford: Oxford University Press, 2014.
57 Pleger B, Ragert P, Schwenkreis P, et al. Patterns of cortical reorganization parallel
impaired tactile discrimination and pain intensity in complex regional pain
syndrome. Neuroimage 2006;32:503–10.
58 Lewis JS, Schweinhardt P. Perceptions of the painful body: the relationship between
body perception disturbance, pain and tactile discrimination in complex regional
pain syndrome. Eur J Pain 2012;16:1320–30.
59 Maihofner C, DeCol R. Decreased perceptual learning ability in complex regional
pain syndrome. Eur J Pain 2007;11:903–9.
60 Reiswich J, Krumova EK, David M, et al. Intact 2D-form recognition despite
impaired tactile spatial acuity in complex regional pain syndrome type I. Pain
2012;153:1484–94.
61 Luomajoki H, Moseley GL. Tactile acuity and lumbopelvic motor control in patients
with back pain and healthy controls. Br J Sports Med 2011;45:437–40.
62 Moseley GL. I can’t find it! Distorted body image and tactile dysfunction in patients
with chronic back pain. Pain 2008;140:239–43.
63 Wand BM, Di Pietro F, George P, et al
. Tactile thresholds are preserved yet
complex sensory function is impaired over the lumbar spine of chronic
non-specific low back pain patients: a preliminary investigation. Physiotherapy
2010;96:317–23.
64 von Piekartz H, Wallwork SB, Mohr G, et al. People with chronic facial pain perform
worse than controls at a facial emotion recognition task, but it is not all about the
emotion. J Oral Rehabil 2015;42:243–50.
65 Stanton TR, Lin CW, Bray H, et al. Tactile acuity is disrupted in osteoarthritis but is
unrelated to disruptions in motor imagery performance. Rheumatology (Oxford)
2013;52:1509–19.
66 Catley MJ, O’Connell NE, Berryman C, et al. Is tactile acuity altered in people with
chronic pain? A systematic review and meta-analysis. J Pain 2014;15:985–1000.
67 Rio E, Moseley GL, Purdam C, et al. The pain of tendinopathy: physiological or
pathophysiological? Sports Med 2014;44:9–23.
68 Debenham JR, Krummanacher SA, Skinner AW, et al., eds. Motor imagery training
decreases pain on loading in people with chronic achilles tendinopathy: a
preliminary rendomised cross-over experiment. Australian Pain Society 35th Annual
Scientific Meeting, 2015.
69 Dey A, Barnsley N, Mohan R, et al. Are children who play a sport or a musical
instrument better at motor imagery than children who do not? Br J Sports Med
2012;46:923–6.
70 Wallwork SB, Butler DS, Wilson DJ, et al. Are people who do yoga any better
at a motor imagery task than those who do not? Br J Sports Med
2015;49:123–7.
71 Wallwork SB, Butler DS, Moseley GL. Dizzy people perform no worse at a motor
imagery task requiring whole body mental rotation; a case-control comparison.
Front Hum Neurosci 2013;7:258.
72 Bowering KJ, O’Connell NE, Tabor A, et al. The effects of Granded Motor Imagery
and its components on chronic pain: a systematic review and meta-analysis. J Pain
2013;14:3–13.
73 Flor H. The modification of cortical reorganization and chronic pain by sensory
feedback. Appl Psychophysiol Biofeedback 2002;27:215–27.
74 Flor H, Denke C, Schaefer M, et al. Effect of sensory discrimination training on
cortical reorganisation and phantom limb pain. Lancet 2001;357:1763–4.
75 Moseley GL. Is successful rehabilitation of complex regional pain syndrome due to
sustained attention to the affected limb? A randomised clinical trial.
Pain
2005;114:54–61.
76 Wand BM, Abbaszadeh S, Smith AJ, et al. Acupuncture applied as a sensory
discrimination training tool decreases movement-related pain in patients with
chronic low back pain more than acupuncture alone: a randomised cross-over
experiment. Br J Sports Med 2013;47:1085–9.
8 Wallwork SB, et al. Br J Sports Med 2015;0:1–8. doi:10.1136/bjsports-2015-095356
Rev i ew