[ clinical commentary ]

SIMON BRUMAGNE, PT, PhD1 • MARTIN DIERS, PhD2 • LIEVEN DANNEELS, PT, PhD3
G. LORIMER MOSELEY, PT, PhD4 • PAUL W. HODGES, PT, PhD, DSc, MedDr, BPhty (Hons)5
Downloaded from www.jospt.org at Asociación de Kinesiología del Deporte (AKD) on August 28, 2021. For personal use only. No other uses without permission.

Neuroplasticity of Sensorimotor
Control in Low Back Pain

L
ow back pain (LBP) represents an important medical (the structural and functional ab-
and socioeconomic problem.34 Current treatments normalities within the musculo-
skeletal system),67 over the past 20
provide modest and generally short-term success, which
years there has been an increasing
may be due in part to our incomplete understanding of realization that patients with LBP
the mechanisms of nonspecific LBP.12 Impaired sensorimotor might also have changes within the
control (which refers to all sensory and as one likely mechanism underlying de- central nervous system. This can be con-
motor processes that control muscles velopment and/or maintenance of pain, sidered from 2 perspectives: first, changes
and spinal alignment and movement to at least initially as a result of suboptimal in processing of nociception and pain,
Copyright © 2019 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

meet demands of healthy function and tissue loading.10,29,82 Although early work which have been observed throughout
loading of the spine) has been suggested focused on this “end-organ dysfunction” the nervous system, and second, changes
in the structure (eg, gray matter loss) and
UUSYNOPSIS: Low back pain (LBP) is an structural and functional nervous system changes function (eg, organization) of sensorimo-
important medical and socioeconomic problem. as they relate to nonspecific LBP and sensorimo- tor regions of the brain cortex. Moreover,
Impaired sensorimotor control has been suggested tor function, and (3) related clinical implications.
clinical interventions increasingly aim to
to be a likely mechanism underlying develop- Individuals with recurrent and persistent LBP
ment and/or maintenance of pain. Although early differ from those without LBP in several markers drive neuroplasticity with treatments to
work focused on the structural and functional of the nervous system’s function and structure. improve sensorimotor function and pain.
abnormalities within the musculoskeletal system, Neuroplastic changes may be addressed by This commentary aims to provide a
Journal of Orthopaedic & Sports Physical Therapy®

in the past 20 years there has been an increasing top-down cognitive-based interventions and contemporary overview of neuroplasti-
realization that patients with LBP might also have bottom-up physical interventions. An integrated
clinical approach that combines contemporary city in LBP. We specifically address (1)
extensive neuroplastic changes within the central
nervous system. These include changes related pain neuroscience education, cognition-targeted defining neuroplasticity in relation to
to both the structure (eg, gray matter changes) sensorimotor control, and physical or function- processing of pain and nociception in
and function (eg, organization of the sensory and based treatments may lead to better outcomes in LBP, sensorimotor control of the spine,
motor cortices) of the nervous system as related to patients with recurrent and persistent LBP. This
and the potential of the system to adapt;
processing of pain and nociception and to motor approach will need to consider variation among in-
dividuals, as no single finding/mechanism is pres- (2) structural and functional nervous sys-
and somatosensory systems. Moreover, clinical
interventions increasingly aim to drive neuro- ent in all individuals, and no single treatment that tem changes as they relate to nonspecific
plasticity with treatments to improve pain and targets neuroplastic changes in the sensorimotor LBP and sensorimotor function; and (3)
sensorimotor function. This commentary provides system is likely to be effective for all patients with related clinical implications.
a contemporary overview of neuroplasticity of the LBP. J Orthop Sports Phys Ther 2019;49(6):402-
pain/nociceptive and sensorimotor systems in LBP. 414. doi:10.2519/jospt.2019.8489
Neuroplasticity and LBP
This paper addresses (1) defining neuroplasticity UUKEY WORDS: brain, electrophysiology, neuroim-
in relation to control of the spine and LBP, (2) aging, rehabilitation, spine Neuroplasticity refers to the capacity of
the nervous system to undergo functional

1
Department of Rehabilitation Sciences, Katholieke Universiteit Leuven, Leuven, Belgium. 2Department of Psychiatry, Psychotherapy and Preventative Medicine, Landschaftsverband
Westfalen-Lippe University Hospital-Ruhr University Bochum, Bochum, Germany. 3Department of Physical Therapy and Rehabilitation, Ghent University, Ghent, Belgium. 4School
of Health Sciences, University of South Australia, Adelaide, Australia. 5Clinical Centre for Research Excellence in Spinal Pain, Injury and Health, School of Health and Rehabilitation
Sciences, The University of Queensland, Brisbane, Australia. In the last 5 years, Dr Moseley has received support from Pfizer Australia; Kaiser Permanente; workers’ compensation
boards in Australia, Europe, and North America; AIA Australia; the International Olympic Committee; Port Adelaide Football Club; and Arsenal Football Club. Professional and
scientific bodies have reimbursed him for travel costs related to presentation of research on pain at scientific conferences/symposia. He has received speaker fees for lectures on
pain and rehabilitation. He receives book royalties from Noigroup Publications. Dr Hodges receives book royalties from Elsevier. Professional and scientific bodies have reimbursed
him for travel costs related to presentation of research on pain, motor control, and exercise therapy at scientific conferences/symposia. He has received fees for teaching
practical courses on motor control training. He is also supported by a Senior Principal Research Fellowship from the National Health and Medical Research Council of Australia
(APP1102905). The other authors certify that they have no affiliations with or financial involvement in any organization or entity with a direct financial interest in the subject matter
or materials discussed in the article. Address correspondence to Dr Paul W. Hodges, School of Health and Rehabilitation Sciences, The University of Queensland, Level 3, Therapies
Annex (84A), St Lucia, QLD 4072 Australia. E-mail: [email protected] t Copyright ©2019 Journal of Orthopaedic & Sports Physical Therapy®

402 | june 2019 | volume 49 | number 6 | journal of orthopaedic & sports physical therapy
 and structural changes modulated by ac- as “modulation” networks (see Moseley or receptors in deep tissues, such as those
tivity and reinforcement.13 Neuroplasticity and Butler53 for extensive review). The potentially impacted by low back injury.
Downloaded from www.jospt.org at Asociación de Kinesiología del Deporte (AKD) on August 28, 2021. For personal use only. No other uses without permission.

is a concept that, in its literal sense, is so constantly varying mix of influences ex- Deep tissue nociceptive fibers primar-
broad that it is almost meaningless—it erted by modulation networks on action ily respond to noxious mechanical and
may just differentiate an alive neuron or networks allows for real-time neuroplas- chemical (eg, inflammation) stimuli.73
nervous system from a dead one.42 The ca- ticity, and shifts within those networks Increased sensitivity and ascending
pacity to learn new things, generate new allow for short-, medium-, and long- projections of neural networks in the
outputs to perform new activities, gener- term neuroplasticity by virtue of shifts spinal cord or impairment in the func-
ate new thoughts, create and remember in their influence. tion of descending inhibitory pathways11
entirely new visual scenes, and create Research into neuroplasticity within (termed central sensitization89) and in-
new links between previously unlinked the context of LBP considers the domain creased sensitivity of brain-grounded
concepts demonstrates the extraordinary spectrum (from features of pain and neural networks that encode for nocicep-
capacity of the nervous system to continue nociceptive processing to sensorimotor tion enable activation of these networks
changing, in an ongoing “online” manner. control), the time spectrum (from on- during a range of innocuous events. This
This online neuroplasticity can be line changes in function to long-term neuroplasticity is mediated by biological
conceptualized in terms of collabora- changes in function and structure), and processes that are themselves influenced
tion and competition between networks the complexity spectrum (whole-human by cognitions about pain and other psy-
of neuronal and nonneuronal cells in the research, for example, investigating how chological phenomena.74 These biological
brain or spinal cord, which collectively people with LBP seek health care). It also processes have been observed in the short
Copyright © 2019 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

exert an influence through neurobio- considers systems (eg, investigating the term and long term, and, when comor-
logical (ie, neuroneural, neuromuscular, features of neural networks that subserve bid with depressive symptoms, increased
neuroimmune, neuroendocrine) con- movement or the brain’s response to a so- sensitivity is associated with poor out-
nections.85 These networks might be matosensory stimulus) and subsystems come after an acute episode of LBP.37
more accurately termed neuroimmune (eg, in vitro studies of changes in synap- Although much research has been
networks because of the involvement of tic efficacy in spinal nociceptors, brain- conducted at the cellular level in animal
neural and immune (and immune-like) grounded neurons, or immune cells). models to understand the biological pro-
cells (see Hodges et al28 for review). Researching different targets requires cesses at multiple levels of the nervous
The influence of any given neural net- different methods and involves research- system (see Woolf88 for comprehensive
Journal of Orthopaedic & Sports Physical Therapy®

work depends on the principles thought ers from different fields, inevitably lead- review), research in humans has been
to govern its operation, including the ing to different interpretations and focused at a systems level, using meth-
number of cells involved (called neuro- terminology by which these interpreta- ods to study endogenous pain inhibi-
nal mass), the precision and efficacy of tions are articulated. FIGURE 1 aims to tory systems (often assumed to relate
the connections within the network, and capture the breadth of research targets to descending noxious inhibition) such
top-down weighting of the network by and related methods that constitute the as conditioned pain modulation,11 hy-
higher-order networks.59 Each network field of neuroplasticity research in LBP. peralgesia in areas remote to the back,38
consists of many cells, and each cell is The following sections introduce 3 do- receptive fields for spinal nociceptive re-
in many networks—the principle of mains relevant for LBP, considering how flexes,57 and temporal summation.20 Each
multitasking.66 research has explained each in the time method provides indirect evidence of the
The clinical construct of LBP involves and complexity spectra and the interac- increased sensitivity assumed to charac-
a wide range of neural networks, includ- tion between domains. terize the central sensitization processes
ing those that process pain and noci- Neuroplasticity in Processing of Pain and observed in animals.
ception (eg, regulation of descending Nociception in LBP Neuroplasticity of Importantly, enhanced sensitivity will
nociceptive modulation),61 sensorimo- processing of nociception and pain is in- likely affect processing of other sensory
tor function (eg, production of motor creasingly recognized as a major contrib- signals. Motor control is modulated by
outputs, encoding of sensory inputs21), utor to LBP, with changes having been the profound neuroplasticity of nocicep-
and cognitions and emotions (eg, en- observed throughout the nervous system. tive networks. For example, peripheral
coding beliefs and thoughts). One can Increased sensitivity of primary nocicep- sensitization means that nociceptive bar-
conceptualize neural networks that exert tive afferents, a phenomenon termed rage, which modulates motor systems at
their influence in the body (eg, a move- peripheral sensitization, is common in the spinal and supraspinal levels, can be
ment) or in consciousness (eg, a feel- many conditions, including LBP.75 This triggered by innocuous thermal and me-
ing) as “action” networks and those that can involve cutaneous receptors that re- chanical input and the presence of prod-
exert their influence inside the brain spond to a range of noxious stimuli and/ ucts of normal muscle activity (eg, lactic

journal of orthopaedic & sports physical therapy | volume 49 | number 6 | june 2019 | 403
 [ clinical commentary ]
acid). Further, sensitivity of the wide transcranial magnetic stimulation (TMS) argue that this biomechanical change is
range of modulatory neural networks over the primary motor cortex while re- the objective of motor control change,
Downloaded from www.jospt.org at Asociación de Kinesiología del Deporte (AKD) on August 28, 2021. For personal use only. No other uses without permission.

relevant to protection will expand the cording their activity78,80 (FIGURE 3), re- and that it provides advantage to the
breadth of innocuous situations that can flects neuroplasticity at a systems level. individual, this is not straightforward.
modulate the motor system to include This is also reflected by changes in TMS- While altered biomechanics may have
those beyond somatosensory inputs—a associated muscle activity in response to short-term benefit (eg, enhanced protec-
situation captured in contemporary un- an exercise program, also reflecting neu- tion from increased muscle activation29),
derstandings of central sensitization.90 roplasticity at a systems level. However, they may have long-term consequences31
Neuroplasticity in the Motor System the former relates to a medium- to long- as a result of chronic suboptimal loading
as a Modulator of Spinal Motor Con- term course and the latter to a short- to of spine tissues and consequent activa-
trol From a perspective of the motor long-term course.79 tion of nociceptors, either mechanically
aspect of sensorimotor control of the In contrast, both the altered activa- or via the sensitizing effects of inflam-
spine, neuroplasticity research has also tion patterns of the trunk muscles asso- mation.31 At the whole-person end of the
covered the complexity and time spec- ciated with the expectation of a noxious spectrum, avoidance of certain behaviors
tra. An enormous diversity of regions of stimulus54 and the avoidance of particu- or withdrawal from activity30 can lead to
the brain and spinal cord (and beyond) lar movements or behaviors because they a descending spiral of health, social, and
(FIGURE 2) is involved in the generation of are perceived to be dangerous reflect neu- personal issues.
motor output, and, although neuroplas- roplasticity at the whole-person level, in Neuroplasticity in the Somatosensory
ticity is possible at any level, research in real-time and the long term, respectively. System as a Modulator of Spinal Mo-
Copyright © 2019 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

LBP has focused on the motor cortex. For Each of these changes in the motor sys- tor Control Motor outputs generally
example, a shift in the stimulus-response tem has the potential to alter the biome- depend on sensory inputs, including
profile of the trunk muscles, revealed by chanics of the spine. Although one might somatosensory information on the po-

Example research Example research Example research Example research Example research Example research
target method target method target method
Whole person Motor performance Behavioral cross- Guarding response Cross-sectional Movement param- Cross-sectional or
during variable sectional studies after acute injury behavioral study eters associated longitudinal
Journal of Orthopaedic & Sports Physical Therapy®

demands (eg, balance during using observational with pain and pain- behavioral study
cognitive tasks) and performance related beliefs using EMG,
outcomes questionnaires,
and cognitive
manipulation
Systems Motor system MEPs using TMS over Temporal summation Behavioral experiment Altered brain volume, Cross-sectional or
stimulus-response M1 and recording of pain using repeated gray matter longitudinal study
profiles EMG in trunk noxious stimuli density, functional using cortical
muscle assessing evoked or structural volumetry, fMRI, or
pain connectivity tractography
Sensory system SEPs using somato-
stimulus-response sensory stimulus
profiles recording with EEG
Subsystems Spatial summation of In vivo animal study Short-term potentia- In vivo animal study Dendritic sprouting In vivo animal study
nociceptive inputs tion of postsynaptic in the dorsal horn;
Complexity

in the dorsal horn membrane DRG sensory-auto-

nomic coupling
Temporal summation In vivo animal study
in the dorsal horn
Online Short Term Long Term
Time

FIGURE 1. Investigations of neuroplasticity related to motor control of the trunk muscles in people with low back pain stretch along the complexity spectrum (vertical—from
subsystems to systems and whole-person studies) and along the time spectrum (horizontal—from online changes in motor output to short- and long-term neuroplasticity-
mediated effects). Example research targets are shown in blue font, and example research methods by which the target can be interrogated in black font. Abbreviations: DRG,
dorsal root ganglia; EEG, electroencephalography; EMG, electromyography; fMRI, functional magnetic resonance imaging; M1, primary motor cortex; MEP, motor-evoked
potential; SEP, somatosensory-evoked potential; TMS, transcranial magnetic stimulation.

404 | june 2019 | volume 49 | number 6 | journal of orthopaedic & sports physical therapy
 sition and movement of the body and A. TMS over scalp grid
input from nociceptive networks as out- B. Paraspinal muscle EMG
Downloaded from www.jospt.org at Asociación de Kinesiología del Deporte (AKD) on August 28, 2021. For personal use only. No other uses without permission.

recordings
lined above. As such, plasticity of the so-
matosensory system can modify motor
Motor cortex (M1)
behavior. The accuracy of interpretation
of sensory input, which may be mediat-
ed by plastic change at the dorsal horn/ Medulla
spinal cord or higher centers (eg, pri- Vertex (Cz) Corticospinal tract
mary sensory cortex excitability/organi-
zation), may change. Again, most human Spinal cord
Motoneuron
research has studied this at a systems
level. For example, there is evidence of LES
reduced proprioceptive acuity (see the
DM
review by Tong et al77), reduced weight- Vertex (Cz)
ing of proprioceptive input,7 and high-
er-level interpretation of body schema,6 E. Motor cortical map
without direct evidence of underlying
neuroplastic processes or the involved
level of the nervous system. Imaging19
Copyright © 2019 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

and electrophysiological69 studies are

currently providing additional insight.

Functional and Structural D. MEPs superimposed C. MEP recorded at each site

over scalp sites
Brain Changes and LBP
There are multiple methods to study the FIGURE 2. Mapping of the motor cortex using TMS. (A) Stimuli over the motor cortex excite intracortical neurons
function and structure of the nervous that provide synaptic input to corticospinal cells. (B) Recordings were made from the DM and LES at the L4
level. (C) The descending volley excites the spinal motoneurons and results in a MEP, mainly in the contralateral
system, and each has been used to study
muscles. (D) The MEPs were recorded in both muscles from stimuli applied at each point on the grid, placed over
changes or differences that are appar-
Journal of Orthopaedic & Sports Physical Therapy®

the scalp and aligned to the vertex (Cz). (E) A 3-D map of MEP amplitude was created for each muscle from the
ent between those individuals with and individual and then group data. Adapted with permission from Tsao et al.78 Abbreviations: DM, short/deep fibers of
without LBP. As suggested above, most the multifidus; EMG, electromyography; LES, longissimus erector spinae; M1, primary motor cortex; MEP, motor-
take a view of a small part of the com- evoked potential; TMS, transcranial magnetic stimulation.
plex whole that involves the interaction
between pain and sensorimotor control Planning and initiation of voluntary
of the spine. Each method measures dif- movement (including postural components)
ferent aspects of neural function and/or Primary somatosensory cortex Primary motor cortex
structure. The TABLE presents an overview Posterior parietal cortex Supplementary motor cortex
Premotor cortex
of the information that can and cannot Prefrontal cortex
be gleaned from each of the measures,
the pros and cons of the measures, and
Basal ganglia
some examples of findings that have been
Vestibular nuclei
reported with respect to LBP. This infor- Cerebellum Reticular formation
mation is critical to interpretation of the Basic movement
Sensory motor
findings presented below. integration and and posture
As highlighted above, it can be prob- learning
lematic and confusing to consider the evi-
dence of neuroplasticity in the different
parts of the brain and the sensorimotor Muscle
Spinal networks
control interaction separately, yet doing
Reflex
so is necessary, due to the nature of the (involuntary
studies that have been performed to date. movement)
The following sections separately discuss
FIGURE 3. Areas of the brain, spinal cord, and peripheral nervous system involved in sensorimotor control.
brain changes associated with pain and

journal of orthopaedic & sports physical therapy | volume 49 | number 6 | june 2019 | 405
 [ clinical commentary ]

TABLE Methods Used to Study Neuroplasticity in Low Back Pain

Downloaded from www.jospt.org at Asociación de Kinesiología del Deporte (AKD) on August 28, 2021. For personal use only. No other uses without permission.

Method Interpretation Pros Cons Examples in LBP

Imaging
fMRI Measure of changes in BOLD signal Good spatial resolution Relatively poor temporal resolution Reorganization of lumbar spine
related to CBF BOLD provides indirect measure of representation in the secondary
Interpreted as changes in regional neural activation somatosensory cortex is based on
brain activation fMRI requires measures made in lumbar pressure stimulus or back
Measures can be lying with a fixed head position, muscle vibration (event-related
• At rest which limits investigation of activation)23,24,33
• Event-related activation associ- functional tasks Difference in functional connectivity
ated with a stimulus or action Analysis depends on identification of between brain regions during mo-
(voluntary motor task, cognitive brain regions in separate images tor imagery of daily activities and
task, sensory input [nociceptive/ and involves substantial process- walking (task-related functional
nonnociceptive]) ing of data, which can impact connectivity)83
• Of functional and effective con- results and interpretation
nectivity between brain regions in Equipment for experimental tasks
resting state or during task needs to be fMRI safe and
compatible, which may limit
Copyright © 2019 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

possibilities
Structural MRI Measure of volume, thickness, Good spatial resolution Unclear which changes account for Decreased prefrontal and thalamic
density, and surface area of brain differences in volume (eg, cell gray matter density in chronic
regions (eg, gray matter) number, water content, etc) LBP3
Analysis can be affected by as- Increased cortical thickness in the
sumptions related to selection of primary somatosensory cortex
regions, and preprocessing can region is somatotopically associ-
affect the results ated with the lower back region in
patients with LBP39,64
Diffusion tensor Measure of white matter microstruc- … Measures can be affected by Microstructural changes in white
imaging tural changes with pathology orientation of fibers (based on matter are correlated with poor
Journal of Orthopaedic & Sports Physical Therapy®

Measure of structural connectivity the assumption that fibers have proprioception in LBP62,64
between regions by analysis of a unique orientation, which is Decreased structural connectiv-
water movement (white matter) represented by the tensor’s ity is correlated with decreased
eigenvector. However, this is not performance of a postural task
valid for crossing fibers) in LBP62,65
Functional near-infra- Measure of brain oxygenation, which Good temporal resolution Poor spatial resolution Hemodynamic changes and
red spectroscopy is interpreted to infer neural Can be measured in any position, Cannot measure brain activity more oxygenation in the somatosensory
activity allowing for more functional tasks than 4 cm deep association area and primary so-
to be studied Difficult to interpret matosensory cortex during painful
More robust against motion artifacts and nonpainful pressure stimulus:
than fMRI no significant differences between
LBP and healthy controls84
PET Measures cell activity and Good spatial resolution Must be combined with brain imag- Somatotopic organization of acti-
populations by measurement of ing (eg, MRI) to interpret location vated glial cells in chronic LBP44
radioactively labeled molecules Specificity of some molecules to the
that bind to specific cells or cells target cells varies
in specific states Invasive
Poor temporal resolution
Table continues on page 407.

nociceptive processing, the motor system, whole. It is necessary to consider the and nociceptive processing, electroen-
and the somatosensory system. Although extensive overlap between domains (eg, cephalography (EEG) studies show that
these sections provide a way to compart- impact of central sensitization on motor patients with chronic LBP have larger
mentalize information, they are not to be output), which is highlighted below. cortical responses to noxious stimuli, in-
interpreted as competing theories of the Functional and Structural Brain Chang- cluding an enhanced N80 component of
importance of neuroplasticity in pain, but es Related to Pain and Nociceptive EEG, which is thought to reflect sensory
rather as different elements of the same Processing From a perspective of pain cortex activation.14 Behavioral studies

406 | june 2019 | volume 49 | number 6 | journal of orthopaedic & sports physical therapy
 TABLE Methods Used to Study Neuroplasticity in Low Back Pain (continued)
Downloaded from www.jospt.org at Asociación de Kinesiología del Deporte (AKD) on August 28, 2021. For personal use only. No other uses without permission.

Method Interpretation Pros Cons Examples in LBP

Arterial spin labeling Measures CBF by using magneti- Noninvasive as compared to PET Regional CBF is an indirect measure Physical maneuvers that induce
magnetic resonance cally labeled arterial blood water Allows one to absolutely quantify tis- of neuronal activity pain are paralleled by changes in
perfusion protons as an endogenous tracer sue perfusion as compared to PET Highly sensitive to head motion resting-state connectivity within
• During resting state or during a Signal-to-noise ratio inherently low, default-mode network45
stimulus which increases total scan time Changes in ongoing chronic pain
• Can be used to investigate are associated with increases
functional connectivity in regional CBF in, for example,
the somatosensory, frontal, and
insular cortices87
Electrophysiology
TMS Measures excitability and organiza- Good temporal resolution Measures excitability of the Shifted location of representation of
tion (eg, motor cortex maps) of corticomotor pathway, not only the transversus abdominis on the
motor regions of the cortex the cortex. Interpretation of motor cortex in LBP80
Paired-pulse methods investigate changes at the cortex requires Changes in intracortical inhibition in
interaction between regions combination with other methods chronic LBP48
(interhemispheric) and excitability (eg, corticomedullary-evoked
Copyright © 2019 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

of intracortical networks potentials to assess changes at

the motoneuron)
Cannot detect activation
Poor spatial resolution
Interpretation of responses of legs
and trunk muscles is complicated
by location near the brain midline
EEG Provides measure of general brain ac- Good temporal resolution Interpretation of spatial location of Altered late-phase cortical process-
tivity (interpreted in relation to ac- Can be used in functional contexts/ activity is complex and requires ing of postural perturbations in
tivity in different frequency bands tasks complex mathematical processing LBP36
that are thought to subserve Analysis can be complex
Journal of Orthopaedic & Sports Physical Therapy®

different functions), event-related

potentials (change in activation
related to specific event), and
contingent negative variation
(change in brain activity after a
warning stimulus provided before
a stimulus to perform a task)
SEPs Measures excitability and processing Good temporal resolution Multiple stimuli are required to Functional reorganization in both the
of sensory inputs capture the SEP, and this may somatosensory and the motor
Different components of the affect the response to this and system in chronic LBP70
response are interpreted with other measures
respect to different brain regions
and different processing events
Abbreviations: BOLD, blood oxygenation level dependent; CBF, cerebral blood flow; EEG, electroencephalography; fMRI, functional magnetic resonance imag-
ing; LBP, low back pain; MRI, magnetic resonance imaging; PET, positron emission tomography; SEP, somatosensory-evoked potential; TMS, transcranial
magnetic stimulation.

show allodynia and hyperalgesia to stim- imaging (MRI) studies show that, in subserved by the periaqueductal gray.22
uli applied to the lumbar spine in people response to a noxious stimulus, patients Structural MRI studies suggest sys-
with LBP22 and modified nociceptive with chronic LBP have lower regional ce- tematic differences between individuals
reflexes. Further, some,11 but not all,38,47 rebral blood flow in the periaqueductal with and without LBP, for example, in
studies show impairment of conditioned gray and a higher increase in activation the dorsolateral prefrontal cortex, tem-
pain modulation in chronic or acute LBP, in the primary and secondary somatosen- poral lobes, insula, primary somato-
which suggests impaired descending in- sory cortices and the lateral orbitofrontal sensory cortex, corpus callosum, and
hibition as a feature of central sensiti- cortex. These findings suggest dysfunc- internal capsule. Results of functional
zation. Functional magnetic resonance tion in the descending inhibitory system connectivity studies during rest imply

journal of orthopaedic & sports physical therapy | volume 49 | number 6 | june 2019 | 407
 [ clinical commentary ]
enhanced activation of the medial pre- Functional and Structural Brain Changes mary motor cortex cells are involved in
frontal cortex, cingulate cortex, amygda- Related to the Motor System Some neu- the action neural networks that drive
Downloaded from www.jospt.org at Asociación de Kinesiología del Deporte (AKD) on August 28, 2021. For personal use only. No other uses without permission.

la, insula, and sensorimotor integration roplastic changes have been interpreted certain trunk muscles,80 and (2) as neu-
regions, together with disrupted func- from the perspective of motor control of ral networks that drive specific muscles
tional connectivity in the default-mode the spine, which may affect tissue loading becoming less specific to those muscles,78
network (a large-scale network of brain and motor patterns in the context of mo- a situation that implies reduced ability to
regions that maintain the brain’s resting tor output of the neural networks asso- differentially activate separate muscles.
state and are involved in neurological ciated with pain. Transcranial magnetic An association has been identified
functions that include the neural basis stimulation has been used to study the between these differences in cortical or-
of self ).1,5,26,27,41 More specifically, results organization and neural network prop- ganization and the duration and severity
of imaging studies showing functional erties of the regions of the motor cortex of pain71 and features of motor behav-
connectivity between the nucleus ac- associated with control of specific trunk ior, such as the timing of recruitment
cumbens and medial prefrontal cortex5 muscles. These studies have found that of muscles in a postural challenge80 and
and structural connectivity between in many individuals with chronic LBP, spine movement.18 These latter obser-
brain regions (white matter fractional the area of peak excitability of cortical vations have led to the hypothesis of a
anisotropy)46 suggest that such connec- inputs to the deep abdominal muscles80 link with tissue loading. An alternative
tivity patterns may be risk factors for is in a different location (more postero- view is that the changes might reflect
nonrecovery. These findings add to the lateral) and there is greater overlap of modified function of the system, which
growing evidence of the critical role the the separate representations of longer is not linked to pain by virtue of effects
Copyright © 2019 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

corticolimbic system plays in the modu- (eg, longissimus) and shorter (eg, mul- on tissue loading, but is nonetheless
lation of acute pain and mediation of tifidus) muscles of the back (FIGURE 4).71,78 relevant as an expression of changed in-
chronic pain.58 The corticolimbic sys- In terms of neural networks, one can con- teraction between modulation (such as
tem is central to reward and motivated ceptualize these differences in 2 ways: (1) those related to altered afferent input or
behavior. Although primarily linked to as a systematic difference in which pri- pain cognitions) and action networks.
modified sensory processing, this, too,
cannot be separated from sensorimotor
function, as motor behaviors will link
with reward and punishment through
Journal of Orthopaedic & Sports Physical Therapy®

relief or provocation of pain.

Furthermore, chronic pain is often Vertex
characterized by predominance of the af- (Cz)
fective/emotional dimensions of pain (its
DM fine wire LES fine wire
“unpleasantness”) over the sensory dis-
criminative dimensions of pain.53 Imag-
ing studies corroborate that observation,
Healthy

as the pattern of brain activation dur-

ing pain seems to shift toward affective/ 2 cm
emotional relevant brain areas as LBP
2 cm
persists.2,4 This can be conceptualized
in terms of increased influence of neural
networks that encode for unpleasant-
Proposed peak
ness and decreased influence of neural
1.0
networks that encode for intensity and 0.8
LBP

sensory features. 0.6

0.4
In summary, changes in function and 0.2
structure are present throughout the ner- 0
vous system and affect the processing of
FIGURE 4. Reorganization of the motor cortex in LBP. Normalized maps of the left and right motor cortex for the
nociception and pain. Each has potential DM (left panels) and LES (right panels) for healthy (top panels) and LBP groups (bottom panels). Dotted lines
to change the interpretation of pain, the denote sagittal and frontal planes, intersecting at the vertex (Cz). Note that the motor cortical map for the DM
interpretation of somatosensory inputs, overlaps that for the LES in the LBP group, whereas the DM is located posteriorly compared to the LES in the
and the motor output. This result is con- healthy group. Adapted with permission from Tsao et al.78 Abbreviations: DM, short/deep fibers of the multifidus;
LBP, low back pain; LES, longissimus erector spinae.
sidered in the following sections.

408 | june 2019 | volume 49 | number 6 | journal of orthopaedic & sports physical therapy
 Evidence of increased responsiveness ron) (FIGURE 2). For instance, changes fluence neuronal activation in multiple
of corticomotor inputs to the bracing in threshold to evoke a response in the ways. Increased activation of microglia
Downloaded from www.jospt.org at Asociación de Kinesiología del Deporte (AKD) on August 28, 2021. For personal use only. No other uses without permission.

strategy (eg, superficial abdominal mus- erector spinae in someone with LBP do in the somatotopically organized back
cles81) and decreased inputs to muscles not enable differentiation of changes at and leg areas of the motor cortex has
involved in subtle fine-tuning of spine the spinal cord, the cortex, or both.76 It been identified,44 but the functional con-
control (eg, the transversus abdomi- is possible to evaluate excitability at the sequences are not yet clear.
nis81) again raises the possibility of sub- cortex using pairs of TMS pulses. Using Functional and Structural Brain Changes
optimal tissue loading. One issue that these methods, intracortical inhibition Related to the Somatosensory System In
remains to be resolved is whether these and facilitation of corticospinal inputs LBP, numerous observations have been
effects of neuroplasticity offer behavioral to the abdominal muscles in individuals made using MRI with respect to senso-
advantage akin to a shift in strategy to with LBP suggest modification of pri- rimotor function. First, a relation between
accommodate altered demands or incur mary motor cortex synaptic function.48 reduced white matter integrity (which has
behavioral disadvantage akin to a break- These observations confirm cortical in- been interpreted to imply modified con-
down in the system.31 volvement, but do not yet provide clear nectivity) of the superior cerebellar pedun-
Changes in the response to TMS can interpretation. cle (a zone of relay for proprioceptive input
be difficult to interpret because the re- Recent work (reviewed in detail in to higher centers) and reduced utilization
sponse amplitude depends on the ex- Hodges et al28) also highlights novel of proprioceptive signals from the back
citability of the cells in the cortex and changes in glial cell activity in motor for standing postural control have been
those in the spinal cord (ie, motoneu- regions of the brain.44 Glial cells can in- observed (FIGURE 5),62,64 which may mean
Copyright © 2019 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

that information on back position/move-

ment is ignored. Second, adding further
A
support to this observation, functional
MRI of brain regions involved in higher-
order processing of muscle spindle input
(specific somatosensory input) reveals less
activity in response to back muscle vibra-
tion, and greater activation in response
to ankle muscle vibration, in those with
Journal of Orthopaedic & Sports Physical Therapy®

LBP than in those without LBP.23,25 Third,

the sensorimotor resting-state network is
B significantly reorganized, which may lead
1.5 to modified utility of sensory signals from
MD of Right Superior Cerebellar Peduncle,

1.4 the back. Functional connectivity between

brain areas related to the integration and
1.3
processing of sensory and motor signals
1.2 for movement is lower.63
10–3 mm2/s

1.1 Again, each of these differences/

changes could imply impaired capacity to
1.0
control movement (eg, lower functional
0.9 connectivity of the sensorimotor net-
0.8 work correlates with slower performance
0.7 of a dynamic sensorimotor task, such as
5-time sit-to-stand-to-sit)63 or a different
0 2 4 6 8 10 12 14 16 18
interpretation related to competition be-
CoP Displacement in Response to Ankle Muscle Vibration tween neural networks (those that serve
(Stable Support Surface), cm sensorimotor function are losing influ-
ence, whereas those that serve pain and
FIGURE 5. Association between white matter microstructure and proprioceptive weighting for postural control in
protection are gaining influence). Rele-
individuals with nonspecific low back pain. (A) Visualization of the right and left superior cerebellar peduncle. (B)
Scatter plot of the association between MD of the right superior cerebellar peduncle and the CoP displacement in vant to this is the observation that patients
response to ankle muscle vibration while standing on a stable support surface in individuals with nonspecific low with recurrent LBP show greater cortical
back pain (r = 0.65, P = .003). Adapted with permission from Pijnenburg62 andPijnenburg et al.64 Abbreviations: thickness than healthy controls in brain
CoP, center of pressure; MD, mean diffusivity. regions involved in cognitive regulation of

journal of orthopaedic & sports physical therapy | volume 49 | number 6 | june 2019 | 409
 [ clinical commentary ]
pain, and they also show a correlation be- tor actions show reduced brain activation training that targets motor skill learning
tween cortical thickening and pain inten- within the left supplementary motor area has been shown to normalize the loca-
Downloaded from www.jospt.org at Asociación de Kinesiología del Deporte (AKD) on August 28, 2021. For personal use only. No other uses without permission.

sity.8 Again demonstrating the difficulty of and the right superior temporal gyrus and tion of primary motor cortex networks
disentangling the sensory processing and sulcus (areas associated with motor imag- that are involved in activating specific
motor control aspects of neuroplasticity, ery), but diffuse and nonspecific enhance- trunk muscles, whereas general exercise
there is a relationship between impaired ment of functional connectivity between such as walking does not (FIGURE 7).79
sit-to-stand-to-sit performance and de- motor imagery–associated networks, in These interventions also improve pain
creased cortical thickness of the rostral patients with chronic LBP as compared and disability, particularly with specific
anterior cingulate cortex,8 as well as cor- to healthy controls.83 subgroups of patients.68 Noninvasive
relations between regional changes in As motor performance was not brain stimulation has been suggested as
cortical thickness and gray matter volume changed, this result may be interpreted as an option to facilitate the recovery of or-
and clinical tests of movement control, compromised sensorimotor system func- ganization of the motor cortex map, with
lumbopelvic control, and individual con- tion requiring greater neural involvement positive preliminary results.72 However,
traction of the transversus abdominis and to complete the task or as central sensi- more recent work highlights that when
multifidus muscles.40 tization characterized by hyperexcitabil- applied to people with LBP, the neural
Akin to the studies of motor cortex ity.83 Each of these differences between circuits targeted with noninvasive brain
maps, several methods have been used individuals with and without LBP might treatments do not respond in the same
to investigate the cortical organization of offer behavioral advantage akin to a re- way as they do in pain-free individuals.70
sensory cortices. Investigation of somato- vised strategy to promote protection, or Further work is required to understand
Copyright © 2019 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

sensory-evoked potentials in response to a breakdown of the system. Either could how best to utilize these approaches.
acute noxious inputs shows modification have negative consequences at a tissue- Behavioral Approaches: Extinction
of specific components of the response, loading level. Training Based on the evidence indicat-
including those interpreted to imply pro- There is clearly extensive evidence of ing modified balance between affective
cessing in the secondary somatosensory modified nervous system structure and and sensory neural networks, there are
cortex and the anterior cingulate cortex, behavior in people with LBP. Much of preliminary findings that this balance
which are thought to reflect the affec- this evidence implicates sensory and mo- can be normalized in people with LBP
tive/emotional components of the pain tor processes associated with control of by a program of extinction training.16
experience.69 Note that central sensitiza- the spine and spine loading. However, Extinction training focuses on the elimi-
Journal of Orthopaedic & Sports Physical Therapy®

tion at multiple levels of the nervous sys- this is not the only possible interpreta- nation of pain-related behaviors and the
tem would lead to increased sensitivity tion, and much can be drawn from the increase of healthy behaviors. It includes
to noxious inputs, leading to allodynia/ available literature by considering that
hyperalgesia. the processes associated with motor con-
Electroencephalography reveals a trol of the spine and sensory processing
greater area of cortical activity in asso- are parts of a whole that interact in the
ciation with postural perturbation from generation and maintenance of pain
arm movements,35 and greater ampli- through multiple mechanisms.
tude of the late positive EEG response to
unexpected postural perturbation that Clinical Implications
correlates with both the amplitude of dis- Just as neuroplasticity enables mecha-
placement of the body’s center of mass nisms that change neural function and
and the amount of catastrophizing.36 The structure to generate and maintain pain, Chronic back pain Back
location of peak primary sensory cortex it also enables the capacity to restore the Finger
response to nonnoxious and noxious tac- system to resolve or improve LBP. The in- Control group Back
Finger
tile stimulation to the back is expanded tegration of sensory and motor processes
and shifted in people with chronic LBP raises the possibility of several potential FIGURE 6. Reorganization of the somatosensory
(FIGURE 6).19 Nonpainful pressure applied targets for restoring normal conditions. cortex in low back pain. Average location of the
finger and back dipole was recorded by a 37-channel
to individual lumbar vertebrae33 evokes a The following sections highlight some
biomagnetometer from the hemisphere contralateral
secondary somatosensory cortex response innovations for treatment of LBP that to the site of stimulation in the 70-millisecond range
that is smaller in those with LBP than it is consider neuroplasticity. for patients with chronic back pain and healthy
in those without.33 Some of these changes Motor Control Training to Change Sen- controls. Locations are superimposed schematically
correlated with chronicity.19 Functional sorimotor Neuroplasticity From the on a magnetic resonance image. Adapted with
permission from Flor et al.19
MRI studies using mental imagery of mo- perspective of motor control of the spine,

410 | june 2019 | volume 49 | number 6 | journal of orthopaedic & sports physical therapy
 video feedback of expressions of pain as short term.86 Even habitual pain has been specific motor training) and bottom-up
well as training of pain-incompatible reduced by visual real-time feedback of physical interventions (such as peripheral
Downloaded from www.jospt.org at Asociación de Kinesiología del Deporte (AKD) on August 28, 2021. For personal use only. No other uses without permission.

behaviors, increase of work-related and the site of chronic pain,15 and there is sensory stimulation,49 exercise, and man-
social activities, physical therapy, and first evidence that treatments such as ual therapy). An integrated contempo-
medication management. The patients massage could be enhanced with this rary neuroscience and clinical approach
engage in role playing to reduce pain be- method.43 The next challenge will be to may combine intensive pain neuroscience
haviors and increase healthy behaviors. investigate, in larger samples, whether education with cognition-targeted senso-
Sensory Discrimination Training A pain treatment such as manual therapy rimotor control training.32,52,55,60
disrupted body image in patients with or extinction training can be boosted by
chronic LBP in the area of usual pain application of real-time feedback. Summary
suggests the need for treatment options Cognitive Training Approaches Treat- An important consideration is that, like
that focus on the reinstatement of nor- ment of patients with LBP may also fo- most clinical features in LBP, there is con-
mal body image or that strengthen body cus not on distraction and analgesia, but siderable variation among individuals,
perception.51 Until now, limited research rather on precisely encoding the painful and no single finding/mechanism revealed
has focused on treatments targeting event by reducing the influence of protec- by imaging and electrophysiological meth-
the distorted body image often seen in tive neural networks through eliminating ods is present in every case. As for other
individuals with chronic musculoskel- danger cues, differentiating safe cues, treatments, it is unlikely that any one
etal pain. However, recently it has been and increasing the influence of neural treatment that targets neuroplastic chang-
shown that when patients with LBP are networks that encode performance of es in the sensorimotor system is likely to
Copyright © 2019 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

provided with visual real-time feedback a task.56,85 These initiatives (eg, graded be effective for everyone with LBP. It is
of their own back during experimental motor imagery) are in their early days also critical to consider the importance of
painful stimulation at this site, the per- and remain to be fully tested but, impor- identifying aberrant pain mechanisms and
ceived intensity of acute painful stimuli tantly, have been developed according to choosing interventions that address the
applied to this site is reduced.17 This ap- the principles of neuroplasticity and the mechanism.9 Overall, the complexity of
proach works not only for acute experi- notion that there are many potential av- assessment methods has generally limited
mental pain, but also for the clinically enues by which to access the system. the sample size used for studies of neuro-
more relevant movement-induced pain. Neuroplastic changes may be ad- plasticity, and larger studies, perhaps with
Further, seeing the back during re- dressed by top-down cognitive-based alternative methods, are required.
Journal of Orthopaedic & Sports Physical Therapy®

peated lumbar spine movements reduces interventions (such as education, cogni-

movement-evoked pain, at least in the tive behavioral therapy, motor imagery, CONCLUSION

P
A eople with recurrent and
Before After
chronic LBP are different from those
without LBP in several markers of
the nervous system’s function and struc-
ture as they relate to sensory and motor
systems. Addressing these neuroplastic
changes in a targeted manner may lead
to better outcomes in patients with re-
current and chronic LBP, but this may
B
Before After require a combination of bottom-up and
top-down approaches. t
Proposed peak
1.0
0.8 ACKNOWLEDGMENTS: The forum on which this
0.6
0.4 body of research was based, “State-of-the-Art
0.2 in Motor Control and Low Back Pain: Inter-
0 national Clinical and Research Expert Fo-
FIGURE 7. Effect of training on organization of the motor cortex in low back pain. Normalized transcranial magnetic
rum,” was supported by the National Health
stimulation maps of the transversus abdominis representation at the motor cortex before and after (A) skilled and Medical Research Council of Australia,
motor control training and (B) walking exercise are displayed. Dotted lines represent the frontal and sagittal planes in collaboration with the North American
and intersect at the vertex. Note that skilled motor training, but not walking training, induced a shift in the motor Spine Society. The forum was chaired by Dr
cortex map toward the location observed in pain-free individuals. Adapted with permission from Tsao et al.79
Paul Hodges.

journal of orthopaedic & sports physical therapy | volume 49 | number 6 | june 2019 | 411
 [ clinical commentary ]
brain/awr039 sensorimotor impairments and functional
REFERENCES 14. D iers M, Koeppe C, Diesch E, et al. Central brain changes in patients with low back pain:
Downloaded from www.jospt.org at Asociación de Kinesiología del Deporte (AKD) on August 28, 2021. For personal use only. No other uses without permission.

processing of acute muscle pain in chronic low a critical review. Am J Phys Med Rehabil.
1. Apkarian AV, Baliki MN, Farmer MA. Predicting back pain patients: an EEG mapping study. J 2018;97:200-211. https://doi.org/10.1097/
transition to chronic pain. Curr Opin Neurol. Clin Neurophysiol. 2007;24:76-83. https://doi. PHM.0000000000000859
2013;26:360-367. https://doi.org/10.1097/ org/10.1097/01.wnp.0000241093.00844.0e 27. Hashmi JA, Baliki MN, Huang L, et al. Shape
WCO.0b013e32836336ad 15. D iers M, Löffler A, Zieglgänsberger W, Trojan shifting pain: chronification of back pain shifts
2. Apkarian AV, Hashmi JA, Baliki MN. Pain and J. Watching your pain site reduces pain inten- brain representation from nociceptive to
the brain: specificity and plasticity of the brain sity in chronic back pain patients. Eur J Pain. emotional circuits. Brain. 2013;136:2751-2768.
in clinical chronic pain. Pain. 2011;152:S49-S64. 2016;20:581-585. https://doi.org/10.1002/ejp.765 https://doi.org/10.1093/brain/awt211
https://doi.org/10.1016/j.pain.2010.11.010 16. D iers M, Yilmaz P, Rance M, et al. Treatment- 28. Hodges PW, Barbe MF, Loggia ML, Nijs J, Stone
3. Apkarian AV, Sosa Y, Sonty S, et al. Chronic back related changes in brain activation in patients LS. Diverse role of biological plasticity in low
pain is associated with decreased prefrontal with fibromyalgia syndrome. Exp Brain Res. back pain and its impact on sensorimotor
and thalamic gray matter density. J Neurosci. 2012;218:619-628. https://doi.org/10.1007/ control of the spine. J Orthop Sports Phys Ther.
2004;24:10410-10415. https://doi.org/10.1523/ s00221-012-3055-2 2019;49:389-401. https://doi.org/10.2519/
JNEUROSCI.2541-04.2004 17. D
 iers M, Zieglgänsberger W, Trojan J, Drevensek jospt.2019.8716
4. Baliki MN, Apkarian AV. Nociception, pain, nega- AM, Erhardt-Raum G, Flor H. Site-specific 29. Hodges PW, Coppieters MW, MacDonald
tive moods, and behavior selection. Neuron. visual feedback reduces pain perception. Pain. D, Cholewicki J. New insight into motor
2015;87:474-491. https://doi.org/10.1016/j. 2013;154:890-896. https://doi.org/10.1016/j. adaptation to pain revealed by a combina-
neuron.2015.06.005 pain.2013.02.022 tion of modelling and empirical approaches.
5. Baliki MN, Petre B, Torbey S, et al. Corticostriatal 18. E lgueta-Cancino E, Schabrun S, Hodges P. Is the Eur J Pain. 2013;17:1138-1146. https://doi.
functional connectivity predicts transition to organization of the primary motor cortex in low org/10.1002/j.1532-2149.2013.00286.x
chronic back pain. Nat Neurosci. 2012;15:1117- back pain related to pain, movement, and/or 30. Hodges PW, Smeets RJ. Interaction between pain,
Copyright © 2019 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

1119. https://doi.org/10.1038/nn.3153 sensation? Clin J Pain. 2018;34:207-216. movement, and physical activity: short-term
6. Bray H, Moseley GL. Disrupted working body 19. F lor H, Braun C, Elbert T, Birbaumer N. Exten- benefits, long-term consequences, and targets
schema of the trunk in people with back pain. sive reorganization of primary somatosensory for treatment. Clin J Pain. 2015;31:97-107. https://
Br J Sports Med. 2011;45:168-173. https://doi. cortex in chronic back pain patients. Neurosci doi.org/10.1097/AJP.0000000000000098
org/10.1136/bjsm.2009.061978 Lett. 1997;224:5-8. https://doi.org/10.1016/ 31. Hodges PW, Tucker K. Moving differently in
7. Brumagne S, Cordo P, Verschueren S. Proprio- S0304-3940(97)13441-3 pain: a new theory to explain the adaptation
ceptive weighting changes in persons with low 20. G eorge SZ, Wittmer VT, Fillingim RB, Robinson to pain. Pain. 2011;152:S90-S98. https://doi.
back pain and elderly persons during upright ME. Sex and pain-related psychological variables org/10.1016/j.pain.2010.10.020
standing. Neurosci Lett. 2004;366:63-66. https:// are associated with thermal pain sensitiv- 32. Hodges PW, van Dillen L, McGill S, Brumagne
doi.org/10.1016/j.neulet.2004.05.013 ity for patients with chronic low back pain. J S, Hides JA, Moseley GL. Integrated clinical ap-
8. Caeyenberghs K, Pijnenburg M, Goossens N, Pain. 2007;8:2-10. https://doi.org/10.1016/j. proach to motor control interventions in low back
Journal of Orthopaedic & Sports Physical Therapy®

Janssens L, Brumagne S. Associations between jpain.2006.05.009 and pelvic pain. In: Hodges PW, Cholewicki J, van
measures of structural morphometry and sen- 21. G etting PA. Emerging principles governing the Dieën JH, eds. Spinal Control: The Rehabilita-
sorimotor performance in individuals with non- operation of neural networks. Annu Rev Neurosci. tion of Back Pain. State of the Art and Science.
specific low back pain. AJNR Am J Neuroradiol. 1989;12:185-204. https://doi.org/10.1146/an- Edinburgh, UK: Elsevier/Churchill Livingstone;
2017;38:183-191. https://doi.org/10.3174/ajnr. nurev.ne.12.030189.001153 2013:243-310.
A5020 22. G iesecke T, Gracely RH, Grant MA, et al. Evidence 33. Hotz-Boendermaker S, Marcar VL, Meier ML,
9. Chimenti RL, Frey-Law LA, Sluka KA. A mecha- of augmented central pain processing in idio- Boendermaker B, Humphreys BK. Reorganization
nism-based approach to physical therapist man- pathic chronic low back pain. Arthritis Rheum. in secondary somatosensory cortex in chronic
agement of pain. Phys Ther. 2018;98:302-314. 2004;50:613-623. https://doi.org/10.1002/ low back pain patients. Spine (Phila Pa 1976).
https://doi.org/10.1093/ptj/pzy030 art.20063 2016;41:E667-E673. https://doi.org/10.1097/
10. Claeys K, Dankaerts W, Janssens L, Pijnenburg 23. G oossens N. Neural correlates of impairments BRS.0000000000001348
M, Goossens N, Brumagne S. Young individuals in proprioception and postural control in non- 34. Hoy D, Bain C, Williams G, et al. A systematic
with a more ankle-steered proprioceptive control specific low back pain [thesis]. Leuven, Belgium: review of the global prevalence of low back pain.
strategy may develop mild non-specific low back Katholieke Universiteit Leuven; 2018. Arthritis Rheum. 2012;64:2028-2037. https://doi.
pain. J Electromyogr Kinesiol. 2015;25:329-338. 24. G oossens N, Janssens L, Brumagne S. org/10.1002/art.34347
https://doi.org/10.1016/j.jelekin.2014.10.013 Changes in the organization of the secondary 35. Jacobs JV, Henry SM, Nagle KJ. Low back
11. Corrêa JB, Costa LO, de Oliveira NT, Sluka KA, somatosensory cortex while processing lum- pain associates with altered activity of the
Liebano RE. Central sensitization and changes bar proprioception and the relationship with cerebral cortex prior to arm movements that
in conditioned pain modulation in people with sensorimotor control in low back pain. Clin J require postural adjustment. Clin Neurophysiol.
chronic nonspecific low back pain: a case–con- Pain. 2019;35:394-406. https://doi.org/10.1097/ 2010;121:431-440. https://doi.org/10.1016/j.
trol study. Exp Brain Res. 2015;233:2391-2399. AJP.0000000000000692 clinph.2009.11.076
https://doi.org/10.1007/s00221-015-4309-6 25. G oossens N, Janssens L, Pijnenburg M, et al. An 36. Jacobs JV, Roy CL, Hitt JR, Popov RE, Henry SM.
12. Costa LCM, Koes BW, Pransky G, Borkan J, Maher exploratory study of sensorimotor brain areas Neural mechanisms and functional correlates
CG, Smeets RJ. Primary care research priorities involved in processing proprioceptive inputs from of altered postural responses to perturbed
in low back pain: an update. Spine (Phila Pa the ankle and back muscles [abstract]. 9th In- standing balance with chronic low back pain.
1976). 2013;38:148-156. https://doi.org/10.1097/ terdisciplinary World Congress on Low Back and Neuroscience. 2016;339:511-524. https://doi.
BRS.0b013e318267a92f Pelvic Girdle Pain; October 31-November 3, 2016; org/10.1016/j.neuroscience.2016.10.032
13. Cramer SC, Sur M, Dobkin BH, et al. Harnessing Singapore. 37. Klyne DM, Moseley GL, Sterling M, Barbe MF,
neuroplasticity for clinical applications. Brain. 26. G oossens N, Rummens S, Janssens L, Caey- Hodges PW. Are signs of central sensitization
2011;134:1591-1609. https://doi.org/10.1093/ enberghs K, Brumagne S. Association between in acute low back pain a precursor to poor out-

412 | june 2019 | volume 49 | number 6 | journal of orthopaedic & sports physical therapy
 come? J Pain. In press. https://doi.org/10.1016/j. 51. M
 oseley GL. I can’t find it! Distorted body image 65. Pijnenburg M, Hadi Hosseini SM, Brumagne
jpain.2019.03.001 and tactile dysfunction in patients with chronic S, Janssens L, Goossens N, Caeyenberghs K.
Downloaded from www.jospt.org at Asociación de Kinesiología del Deporte (AKD) on August 28, 2021. For personal use only. No other uses without permission.

38. Klyne DM, Moseley GL, Sterling M, Barbe back pain. Pain. 2008;140:239-243. https://doi. Structural brain connectivity and the sit-to-stand-
MF, Hodges PW. Individual variation in pain org/10.1016/j.pain.2008.08.001 to-sit performance in individuals with nonspecific
sensitivity and conditioned pain modulation 52. M
 oseley GL. A pain neuromatrix approach low back pain: a diffusion magnetic resonance
in acute low back pain: effect of stimulus type, to patients with chronic pain. Man Ther. imaging-based network analysis. Brain Con-
sleep, and psychological and lifestyle factors. 2003;8:130-140. https://doi.org/10.1016/ nect. 2016;6:795-803. https://doi.org/10.1089/
J Pain. 2018;19:942.e1-942.e18. https://doi. S1356-689X(03)00051-1 brain.2015.0401
org/10.1016/j.jpain.2018.02.017 53. M
 oseley GL, Butler DS. Explain Pain Super- 66. Raposo D, Kaufman MT, Churchland AK. A cat-
39. Kong J, Spaeth RB, Wey HY, et al. S1 is associ- charged. Adelaide, Australia: Noigroup Publica- egory-free neural population supports evolving
ated with chronic low back pain: a functional tions; 2017. demands during decision-making. Nat Neurosci.
and structural MRI study. Mol Pain. 2013;9:43. 54. M
 oseley GL, Nicholas MK, Hodges PW. Does 2014;17:1784-1792. https://doi.org/10.1038/
https://doi.org/10.1186/1744-8069-9-43 anticipation of back pain predispose to back nn.3865
40. Kregel J. Brain morphology is associated with trouble? Brain. 2004;127:2339-2347. https://doi. 67. Robinson JP, Apkarian AV. Chronic back pain.
motor control in patients with chronic low back org/10.1093/brain/awh248 In: Mayer EA, Bushnell MC, eds. Functional Pain
pain: preliminary results [abstract]. 9th Inter- 55. M
 oseley GL, Nicholas MK, Hodges PW. A ran- Syndromes: Presentation and Pathophysiology.
disciplinary World Congress on Low Back and domized controlled trial of intensive neurophysi- Seattle, WA: IASP Press; 2009:23-53.
Pelvic Girdle Pain; October 31-November 3, 2016; ology education in chronic low back pain. Clin J 68. Saragiotto BT, Maher CG, Hancock MJ, Koes
Singapore. Pain. 2004;20:324-330. BW. Subgrouping patients with nonspecific low
41. Kregel J, Meeus M, Malfliet A, et al. Structural 56. M
 oseley GL, Vlaeyen JW. Beyond nociception: back pain: hope or hype? J Orthop Sports Phys
and functional brain abnormalities in chronic the imprecision hypothesis of chronic pain. Ther. 2017;47:44-48. https://doi.org/10.2519/
low back pain: a systematic review. Semin Pain. 2015;156:35-38. https://doi.org/10.1016/j. jospt.2017.0602
Arthritis Rheum. 2015;45:229-237. https://doi. pain.0000000000000014 69. Schabrun SM, Burns E, Hodges PW. New
Copyright © 2019 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

org/10.1016/j.semarthrit.2015.05.002 57. M
 üller M, Biurrun Manresa JA, Treichel F, et al. insight into the time-course of motor and
42. Lindley EH. A study of puzzles with special Discriminative ability of reflex receptive fields to sensory system changes in pain. PLoS One.
reference to the psychology of mental adapta- distinguish patients with acute and chronic low 2015;10:e0142857. https://doi.org/10.1371/jour-
tion. Am J Psychol. 1897;8:431-493. https://doi. back pain. Pain. 2016;157:2664-2671. https://doi. nal.pone.0142857
org/10.2307/1411772 org/10.1097/j.pain.0000000000000683 70. Schabrun SM, Burns E, Thapa T, Hodges P. The
43. Löffler A, Trojan J, Zieglgänsberger W, Diers 58. N
 avratilova E, Porreca F. Reward and motiva- response of the primary motor cortex to neuro-
M. Visually induced analgesia during massage tion in pain and pain relief. Nat Neurosci. modulation is altered in chronic low back pain: a
treatment in chronic back pain patients. Eur J 2014;17:1304-1312. https://doi.org/10.1038/ preliminary study. Pain Med. 2018;19:1227-1236.
Pain. 2017;21:1623-1631. https://doi.org/10.1002/ nn.3811 https://doi.org/10.1093/pm/pnx168
ejp.1066 59. N
 icolelis MA, Lebedev MA. Principles of neural 71. Schabrun SM, Elgueta-Cancino EL, Hodges PW.
44. Loggia ML, Chonde DB, Akeju O, et al. Evidence ensemble physiology underlying the operation Smudging of the motor cortex is related to the
Journal of Orthopaedic & Sports Physical Therapy®

for brain glial activation in chronic pain pa- of brain–machine interfaces. Nat Rev Neurosci. severity of low back pain. Spine (Phila Pa 1976).
tients. Brain. 2015;138:604-615. https://doi. 2009;10:530-540. https://doi.org/10.1038/ 2017;42:1172-1178. https://doi.org/10.1097/
org/10.1093/brain/awu377 nrn2653 BRS.0000000000000938
45. Loggia ML, Kim J, Gollub RL, et al. Default mode 60. N
 ijs J, Meeus M, Cagnie B, et al. A modern 72. Schabrun SM, Jones E, Elgueta Cancino EL,
network connectivity encodes clinical pain: an neuroscience approach to chronic spinal pain: Hodges PW. Targeting chronic recurrent low back
arterial spin labeling study. Pain. 2013;154:24-33. combining pain neuroscience education with pain from the top-down and the bottom-up: a
https://doi.org/10.1016/j.pain.2012.07.029 cognition-targeted motor control training. Phys combined transcranial direct current stimulation
46. Mansour AR, Baliki MN, Huang L, et al. Brain Ther. 2014;94:730-738. https://doi.org/10.2522/ and peripheral electrical stimulation interven-
white matter structural properties predict transi- ptj.20130258 tion. Brain Stimul. 2014;7:451-459. https://doi.
tion to chronic pain. Pain. 2013;154:2160-2168. 61. O
 ssipov MH, Dussor GO, Porreca F. Central org/10.1016/j.brs.2014.01.058
https://doi.org/10.1016/j.pain.2013.06.044 modulation of pain. J Clin Invest. 2010;120:3779- 73. Schaible HG, Schmidt RF. Effects of an experi-
47. Marcuzzi A, Dean CM, Wrigley PJ, Chakiath RJ, 3787. https://doi.org/10.1172/JCI43766 mental arthritis on the sensory properties of
Hush JM. Prognostic value of quantitative sen- 62. P
 ijnenburg M. The neural basis of complex pos- fine articular afferent units. J Neurophysiol.
sory testing in low back pain: a systematic review tural tasks in individuals with and without non- 1985;54:1109-1122. https://doi.org/10.1152/
of the literature. J Pain Res. 2016;9:599-607. specific low back pain [thesis]. Leuven, Belgium: jn.1985.54.5.1109
https://doi.org/10.2147/JPR.S115659 Katholieke Universiteit Leuven; 2015. 74. Seminowicz DA, Davis KD. Cortical responses
48. Massé-Alarie H, Flamand VH, Moffet H, 63. P
 ijnenburg M, Brumagne S, Caeyenberghs K, to pain in healthy individuals depends on pain
Schneider C. Corticomotor control of deep ab- et al. Resting-state functional connectivity of catas­trophizing. Pain. 2006;120:297-306. https://
dominal muscles in chronic low back pain and the sensorimotor network in individuals with doi.org/10.1016/j.pain.2005.11.008
anticipatory postural adjustments. Exp Brain nonspecific low back pain and the association 75. Starkweather AR, Ramesh D, Lyon DE, et al.
Res. 2012;218:99-109. https://doi.org/10.1007/ with the sit-to-stand-to-sit task. Brain Con- Acute low back pain: differential somatosen-
s00221-012-3008-9 nect. 2015;5:303-311. https://doi.org/10.1089/ sory function and gene expression compared
49. Massé-Alarie H, Flamand VH, Moffet H, Schnei- brain.2014.0309 with healthy no-pain controls. Clin J Pain.
der C. Peripheral neurostimulation and specific 64. P
 ijnenburg M, Caeyenberghs K, Janssens L, et 2016;32:933-939. https://doi.org/10.1097/
motor training of deep abdominal muscles im- al. Microstructural integrity of the superior cer- AJP.0000000000000347
prove posturomotor control in chronic low back ebellar peduncle is associated with an impaired 76. Strutton PH, Catley M, McGregor AH, Davey NJ.
pain. Clin J Pain. 2013;29:814-823. https://doi. proprioceptive weighting capacity in individuals Corticospinal excitability in patients with uni-
org/10.1097/AJP.0b013e318276a058 with non-specific low back pain. PLoS One. lateral sciatica. Neurosci Lett. 2003;353:33-36.
50. Melzack R. Pain and the neuromatrix in the brain. 2014;9:e100666. https://doi.org/10.1371/journal. https://doi.org/10.1016/j.neulet.2003.09.005
J Dent Educ. 2001;65:1378-1382. pone.0100666 77. Tong MH, Mousavi SJ, Kiers H, Ferreira P, Ref-

journal of orthopaedic & sports physical therapy | volume 49 | number 6 | june 2019 | 413
 [ clinical commentary ]
shauge K, van Dieën J. Is there a relationship be- 82. v an Dieën JH, Moseley GL, Hodges PW. Motor visualization of the back during movement. Clin J
tween lumbar proprioception and low back pain? control changes and low back pain: cause or ef- Pain. 2012;28:602-608. https://doi.org/10.1097/
Downloaded from www.jospt.org at Asociación de Kinesiología del Deporte (AKD) on August 28, 2021. For personal use only. No other uses without permission.

A systematic review with meta-analysis. Arch fect? In: Hodges PW, Cholewicki J, van Dieën JH, AJP.0b013e31823d480c
Phys Med Rehabil. 2017;98:120-136.e2. https:// eds. Spinal Control: The Rehabilitation of Back 87. Wasan AD, Loggia ML, Chen LQ, Napadow V,
doi.org/10.1016/j.apmr.2016.05.016 Pain. State of the Art and Science. Edinburgh, Kong J, Gollub RL. Neural correlates of chronic
78. Tsao H, Danneels LA, Hodges PW. ISSLS Prize UK: Elsevier/Churchill Livingstone; 2013:207-217. low back pain measured by arterial spin labeling.
winner: smudging the motor brain in young 83. V rana A, Hotz-Boendermaker S, Stämpfli P, et al. Anesthesiology. 2011;115:364-374. https://doi.
adults with recurrent low back pain. Spine Differential neural processing during motor im- org/10.1097/ALN.0b013e318220e880
(Phila Pa 1976). 2011;36:1721-1727. https://doi. agery of daily activities in chronic low back pain 88. Woolf CJ. Central sensitization: implications
org/10.1097/BRS.0b013e31821c4267 patients. PLoS One. 2015;10:e0142391. https:// for the diagnosis and treatment of pain. Pain.
2011;152:S2-S15. https://doi.org/10.1016/j.
79. Tsao H, Galea MP, Hodges PW. Driving plastic- doi.org/10.1371/journal.pone.0142391
pain.2010.09.030
ity in the motor cortex in recurrent low back 84. V rana A, Meier ML, Hotz-Boendermaker S,
89. Woolf CJ. Evidence for a central component
pain. Eur J Pain. 2010;14:832-839. https://doi. Humphreys BK, Scholkmann F. Cortical sen-
of post-injury pain hypersensitivity [let-
org/10.1016/j.ejpain.2010.01.001 sorimotor processing of painful pressure in
ter]. Nature. 1983;306:686-688. https://doi.
80. Tsao H, Galea MP, Hodges PW. Reorganization patients with chronic lower back pain—an optical
org/10.1038/306686a0
of the motor cortex is associated with postural neuroimaging study using fNIRS. Front Hum 90. Woolf CJ. What to call the amplification of
control deficits in recurrent low back pain. Brain. Neurosci. 2016;10:578. https://doi.org/10.3389/ nociceptive signals in the central nervous sys-
2008;131:2161-2171. https://doi.org/10.1093/ fnhum.2016.00578 tem that contribute to widespread pain? Pain.
brain/awn154 85. W allwork SB, Bellan V, Catley MJ, Moseley GL. 2014;155:1911-1912. https://doi.org/10.1016/j.
81. Tsao H, Tucker KJ, Hodges PW. Changes Neural representations and the cortical body ma- pain.2014.07.021
in excitability of corticomotor inputs to trix: implications for sports medicine and future
the trunk muscles during experimentally- directions. Br J Sports Med. 2016;50:990-996.

@ MORE INFORMATION
induced acute low back pain. Neuroscience. https://doi.org/10.1136/bjsports-2015-095356
Copyright © 2019 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

2011;181:127-133. https://doi.org/10.1016/j. 86. W and BM, Tulloch VM, George PJ, et al. Seeing it
neuroscience.2011.02.033 helps: movement-related back pain is reduced by WWW.JOSPT.ORG
Journal of Orthopaedic & Sports Physical Therapy®

SEND Letters to the Editor-in-Chief

JOSPT welcomes letters related to professional issues or articles published
in the Journal. The Editor-in-Chief reviews and selects letters for
publication based on the topic’s relevance, importance, appropriateness,
and timeliness. Letters should include a summary statement of any conflict
of interest, including financial support related to the issue addressed.
In addition, letters are copy edited, and the correspondent is not typically
sent a version to approve. Letters to the Editor-in-Chief should be sent
electronically to [email protected]. Authors of the relevant manuscript are
given the opportunity to respond to the content of the letter.

414 | june 2019 | volume 49 | number 6 | journal of orthopaedic & sports physical therapy