Reorganization of the motor cortex is associated with postural control deficits in recurrent low back pain.
ABSTRACT Many people with recurrent low back pain (LBP) have deficits in postural control of the trunk muscles and this may contribute to the recurrence of pain episodes. However, the neural changes that underlie these motor deficits remain unclear. As the motor cortex contributes to control of postural adjustments, the current study investigated the excitability and organization of the motor cortical inputs to the trunk muscles in 11 individuals with and without recurrent LBP. EMG activity of the deep abdominal muscle, transversus abdominis (TrA), was recorded bilaterally using intramuscular fine-wire electrodes. Postural control was assessed as onset of TrA EMG during single rapid arm flexion and extension tasks. Motor thresholds (MTs) for transcranial magnetic stimulation (TMS) were determined for responses contralateral and ipsilateral to the stimulated cortex. In addition, responses of TrA to TMS over the contralateral cortex were mapped during voluntary contractions at 10% of maximum. MTs and map parameters [centre of gravity (CoG) and volume] were compared between healthy and LBP groups. The CoG of the motor cortical map of TrA in the healthy group was approximately 2 cm anterior and lateral to the vertex, but was more posterior and lateral in the LBP group. The location of the CoG and the map volume were correlated with onset of TrA EMG during rapid arm movements. Furthermore, the MT needed to evoke ipsilateral responses was lower in the LBP group, but only on the less excitable hemisphere. These findings provide preliminary evidence of reorganization of trunk muscle representation at the motor cortex in individuals with recurrent LBP, and suggest this reorganization is associated with deficits in postural control.
- SourceAvailable from: Paul W Hodges[show abstract] [hide abstract]
ABSTRACT: Experimental study of muscle changes after lumbar spinal injury. To investigate effects of intervertebral disc and nerve root lesions on cross-sectional area, histology and chemistry of porcine lumbar multifidus. The multifidus cross-sectional area is reduced in acute and chronic low back pain. Although chronic changes are widespread, acute changes at 1 segment are identified within days of injury. It is uncertain whether changes precede or follow injury, or what is the mechanism. The multifidus cross-sectional area was measured in 21 pigs from L1 to S1 with ultrasound before and 3 or 6 days after lesions: incision into L3-L4 disc, medial branch transection of the L3 dorsal ramus, and a sham procedure. Samples from L3 to L5 were studied histologically and chemically. The multifidus cross-sectional area was reduced at L4 ipsilateral to disc lesion but at L4-L6 after nerve lesion. There was no change after sham or on the opposite side. Water and lactate were reduced bilaterally after disc lesion and ipsilateral to nerve lesion. Histology revealed enlargement of adipocytes and clustering of myofibers at multiple levels after disc and nerve lesions. These data resolve the controversy that the multifidus cross-sectional area reduces rapidly after lumbar injury. Changes after disc lesion affect 1 level with a different distribution to denervation. Such changes may be due to disuse following reflex inhibitory mechanisms.Spine 01/2007; 31(25):2926-33. · 2.16 Impact Factor
- [show abstract] [hide abstract]
ABSTRACT: The TMS-mapped representations of two intrinsic hand muscles, abductor pollicis brevis (APB) and abductor digiti minimi (ADM), were quantified using a transcranial magnetic stimulation (TMS) mapping technique in 10 right handed and 6 left handed subjects. A 50 mm diameter figure eight coil was used. Stimulus sites were located using a latitude/longitude based coordinate system, stimulus intensity was threshold-adjusted and stimuli were applied during controlled low-level (10%) voluntary contraction of the target muscles. Maps of the corticomotor representation were generated by fitting a continuously defined three dimensional function to the data obtained from stimulation at specific scalp sites, and projecting this function onto a two dimensional surface using a radial projection. It was found that the mapped representations of APB and ADM were large and overlapping but that there was a statistically significant separation of the two areas, the APB area being more laterally placed than the ADM area. The TMS-mapped representations of the two muscles showed no significant interhemispheric differences and were similar in left and right handed subjects. Rotation of the magnetic coil through 90 degrees resulted in medial shift and elongation of the TMS-mapped representations but there was no change in the relative positions of the two areas. The TMS-mapped representations were found to be very reproducible when mapping was repeated after intervals of up to 181 days. The present technique of TMS mapping allows the representation of individual hand muscles in the primary motor cortex to be reliably and reproducibly mapped and should prove useful for further studies of the physiology and pathophysiology of the motor cortex in man.Journal of the Neurological Sciences 10/1993; 118(2):134-44. · 2.24 Impact Factor
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ABSTRACT: Transcranial magnetic stimulation (TMS) of the human motor cortex was used to study facilitation of motor-evoked potentials (MEPs) in the rectus abdominis (RA) muscle, a trunk flexor, during voluntary activation. MEPs could be produced in the relaxed RA muscles of all six normal subjects studied. The MEPs had short latencies (18-22 ms) which are consistent with other studies suggesting a fast corticospinal input to the trunk muscles. Marked facilitation was observed in the MEPs when subjects were asked to produce graded levels of voluntary contractions. The two tasks used to produce voluntary contractions were a forced expiration during a breath-holding task (FEBH) and bilateral trunk flexion (BTF). Maximal voluntary EMG activity during the BTF task produced around 4.2 times more integrated EMG than during the FEBH task. Similarly the MEP amplitude at MVC was 2.3 times greater during BTF than FEBH. The pattern of MEP facilitation with increasing voluntary EMG was not linear and a maximal MEP amplitude was observed at a level of voluntary contraction around 30 % MVC in both tasks. There were some subtle differences in the pattern of facilitation in the two tasks. When TMS was applied to the right cortex only, MEPs were seen in both left and right RA muscles suggesting some ipsilateral corticospinal innervation. The latency of the right (ipsilateral) response was approximately 2 ms longer than the left. Comparison with studies in hand and leg muscles suggests that the facilitation pattern in RA may reflect a substantial degree of corticospinal innervation. Experimental Physiology (2001) 86.1, 131-136.Experimental Physiology 02/2001; 86(1):131-6. · 2.79 Impact Factor
Reorganization of the motor cortex is associated
with postural control deficits in recurrent
low back pain
H.Tsao,1M. P.Galea2and P.W. Hodges1
1NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, School of Health and Rehabilitation
Sciences,The University of Queensland, Brisbane and2School of Physiotherapy,The University of Melbourne, Melbourne,
Correspondence to: Dr Paul Hodges, NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health,
School of Health and Rehabilitation Sciences,The University of Queensland, Brisbane,Qld 4072, Australia
Many people with recurrent low back pain (LBP) have deficits in postural control of the trunk muscles and this
may contribute to the recurrence of pain episodes. However, the neural changes that underlie these motor
deficits remain unclear. As the motor cortex contributes to control of postural adjustments, the current study
investigated the excitability and organization of the motor cortical inputs to the trunk muscles in 11 individuals
with and without recurrent LBP . EMG activity of the deep abdominal muscle, transversus abdominis (T rA), was
recorded bilaterally using intramuscular fine-wire electrodes. Postural control was assessed as onset of T rA
EMG during single rapid arm flexion and extension tasks. Motor thresholds (MTs) for transcranial magnetic
stimulation (TMS) were determined forresponses contralateralandipsilateralto the stimulatedcortex.In addi-
tion, responses of T rAtoTMS over the contralateral cortex were mapped during voluntary contractions at10%
of maximum. MTs and map parameters [centre of gravity (CoG) and volume] were compared between healthy
and LBP groups.The CoG of the motor cortical map of T rA in the healthy group was »2cm anterior and lateral
tothevertex, but was more posterior andlateralinthe LBP group.Thelocation ofthe CoG andthe mapvolume
were correlated with onset of T rA EMG during rapid arm movements. Furthermore, the MT needed to evoke
ipsilateral responses was lower in the LBP group, but only on the less excitable hemisphere.These findings pro-
vide preliminary evidence of reorganization of trunk muscle representation at the motor cortex in individuals
with recurrent LBP, and suggest this reorganization is associated with deficits in postural control.
Keywords: motor cortex; postural control; transcranial magnetic stimulation; abdominal muscles
Abbreviations: LBP = low back pain; MVC = maximum voluntary contraction; MT = motor thresholds;TMS = transcranial
magnetic stimulation;TrA = transversus abdominis
Received April 23, 2008. Revised June 6, 2008. Accepted June 23, 2008
Described as a ‘Western epidemic’, low back pain (LBP) is
the most common cause of work-related absence in western
society (Blyth et al., 2001). Studies show 50–80% of adults
in the general population will suffer this condition at some
stage in their lives, and 15–30% will have LBP at any given
time (Andersson, 1998). While many individuals will
recover within 1 month (Pengel et al., 2003), most people
will have recurrence of pain episodes within a 12-month
period (Cassidy et al., 2005; Wasiak et al., 2006). A possible
contributor to the persistence or recurrence of this
condition is changes in postural control of the trunk
muscles. Several studies have demonstrated delayed activa-
tion of the deep abdominal (Hodges and Richardson, 1996)
and back muscles (Leinonen et al., 2001), and increased
activity of superficial trunk muscles (Arendt-Nielsen et al.,
1996; Radebold et al., 2001) in patients with recurrent LBP.
Many of these changes persist after the resolution of
symptoms (Hodges and Richardson, 1996) and have been
argued to contribute to the recurrence of LBP episodes
(Hodges and Moseley, 2003; Cholewicki et al., 2005).
However, exactly how the organization of control of these
responses in the motor system is changed with pain
doi:10.1093/brain/awn154 Brain (2008) Page1of11
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The motor cortex provides a critical contribution to
postural control (see review Deliagina et al., 2008). For
instance, stimulation of the motor cortex in standing cats
induced both a flexion movement of the contralateral
forelimb and an anticipatory postural change in the
supporting forelimb (Gahe ´ry and Nieoullon, 1978). In
addition, data from human studies demonstrate that
inhibition of the motor cortex can reduce postural activity
of the trunk muscles associated with voluntary limb
movements (Hodges et al., 2003). As cortical regions
contribute to postural control, it could be speculated that
deficits in postural activation, such as those observed in
people with LBP, may be associated with changes in the
excitability and organization of the motor cortex.
There is a tremendous potential for areas of the brain,
such as the motor and sensory cortices, to undergo an
organizational change that was once thought only possible
during early human development (Sanes and Donoghue,
2000). For instance, the motor cortex is extensively
reorganized following stroke (Nudo and Milliken, 1996;
Bu ¨tefisch, 2004). Furthermore, changes in motor cortex
organization have been observed in conditions such as
phantom limb pain (Flor et al., 1995; Karl et al., 2001) and
complex regional pain syndrome (Krause et al., 2006;
Maiho ¨fner et al., 2007), where the central nervous system
(CNS) remains largely intact. Few studies have examined
the plasticity of the sensorimotor cortex in people with
recurrent LBP. One study showed an expansion and shift in
the representation of the lower back in the somatosensory
cortex (Flor et al., 1997). Whether there are similar changes
in the motor cortex of individuals with recurrent LBP
remains unclear. The only available data suggest higher
thresholds to evoke facilitation or inhibition of responses of
stimulation (TMS) over the motor cortex compared to
healthy individuals (Strutton et al., 2005). In that study, the
change in threshold was related to the pain and functional
disability experienced by LBP patients. However, it remains
unclear whether changes in excitability are related to
changes in organization at the motor cortex, or whether
the cortical changes are associated with changes in postural
This study investigated changes in postural activation of
the deep abdominal muscle, transversus abdominis (TrA) in
people with recurrent LBP. Feedforward postural activation
of this muscle in association with arm movement is
consistently delayed in these individuals compared to
healthy controls (Hodges and Richardson, 1996; Hodges
and Richardson, 1997). Although changes in trunk muscle
activation are not restricted to the TrA, deficits in
activation of this muscle provide an useful marker of
motor control dysfunction as they are observed relatively
consistently despite differences in LBP presentation. The
study aimed to investigate the excitability and organization
of cortical networks in the motor cortex that induce
activation of TrA when excited by TMS in healthy
individuals, and to compare these parameters to individuals
with recurrent LBP. If changes in cortical parameters were
observed, a further aim was to determine whether the
extent of cortical reorganization was associated with
changes in postural activation of the trunk muscles.
Eleven right-handed individuals with recurrent non-specific LBP
lasting longer than 3 months and 11 right-handed healthy
individuals with no history of LBP were recruited (Table 1).
Individuals were included in the LBP group if they experienced
pain in the low back region with or without accompanying
buttock pain and of sufficient intensity to have limited activities of
daily living. This group was selected as previous studies have
consistently shown delays in postural activation of TrA (Hodges
and Richardson, 1996). Subjects in the LBP group had minimal
pain at time of testing and symptoms were not aggravated by the
experimental procedures, as variability in the level of pain during
testing could increase the variability of the data. Subjects were
excluded ifthey hadany major
neurological or respiratory conditions, a history or family history
of epilepsy, recent or current pregnancies, previous surgery to the
abdomen or back, or if they had undertaken any form of
abdominal exercises in the preceding 12 months. The study
conformed to the Declaration of Helsinki and was approved by
the Institutional Medical Research Ethics Committee.
EMG activity of TrA was recorded bilaterally using intramuscular
fine-wire electrodes (Teflon-coated stainless steel wire, 75mm
diameter with 1mm of Teflon removed and tips bent back ?1 and
?2mm to form hooks). Wires were threaded into a hypodermic
needle and inserted with real-time ultrasound guidance (Hodges
and Richardson, 1997). Pairs of surface electrodes (Ag/AgCl discs,
Grass Telefactor, USA) were placed over the anterior and posterior
deltoid muscles for assessment of an arm movement task (see
below). The ground electrode was placed over the lower lateral rib
cage. EMG data were pre-amplified 2000 times, band-pass filtered
between 20 and 1000Hz, and sampled at 2000Hz using a
Power1401 Data Acquisition System with Signal2 and Spike2
software (CED, UK).
T able1 Subject demographics (mean?SD)
LBP (n=1 1)
Pain duration (years)
Oswestry Disability Index (/100)
Pain visual analogue scale (VAS) represents the worst pain
reported in the last month.
Page 2 of11Brain (2008)H.Tsao et al.
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A single-pulse monophasic MagStim 2002stimulator (Magstim
Company, UK) was used to stimulate the motor cortex. A 7-cm
figure-of-eight coil was placed with cross-over position over
respective scalp sites and the coil handle oriented at ?45?from
the mid-sagittal plane to induce currents in an anterior-medial
direction (Sakai et al., 1997). This coil orientation has been shown to
evoke consistent contralateral responses from the abdominal
muscles during submaximal voluntary contractions (Tunstill et al.,
2001; Strutton et al., 2004; Tsao et al., 2008). The figure-of-eight coil
provides better focality of stimulation compared to the standard
circular coil and is more ideal for mapping of the motor cortex
(Cohen et al., 1990; Brasil-Neto et al., 1992). However, our previous
study showed that even at maximum stimulator output with the
figure-of-eight coil, it was difficult to evoke ipsilateral responses in
TrA during submaximal contractions, or evoke contralateral
responses with the TrA muscle relaxed (Tsao et al., 2008). Thus, a
110mm double-cone coil (Magstim Company, UK) was also used as
this coil produces a stronger magnetic field and could induce
consistent contralateral and ipsilateral responses of the trunk
muscles (Davey et al., 2002; Strutton et al., 2005; Tsao et al.,
2008). The double-cone coil was positioned perpendicular to the
scalp site with induced current flowing in an anterior direction.
EMG was recorded during maximum voluntary contraction
(MVC) performed as a forced expiratory manoeuvre to determine
targets for voluntary activation of TrA. Three repetitions, each
lasting for at least 3s, were completed with verbal encouragement.
The contraction with the highest root-mean-square (RMS) EMG
amplitude was identified and the peak RMS EMG over 1s was
recorded. The target for voluntary contraction of TrA was set at
10% MVC as this was a comfortable level for subjects to maintain
and minimized the potential for fatigue. Feedback of real-time
RMS EMG of TrA (averaged online over 200ms windows on a
duplicate channel) and the target level was displayed on a
monitor. Excitability of the abdominal motoneurons is thought
to be modulated throughout the respiratory cycle as a result of
central respiratory drive potentials (Gill and Kuno, 1963; Sears,
1964), which would likely affect the amplitude of motor evoked
potentials (MEPs; Lissens et al., 1995). To standardize moto-
neuron excitability, subjects ceased breathing at the end of normal
expiration and maintained their glottis open prior to the TMS
pulse. The phase of respiration was monitored online using a
pressure cuff strapped to the chest to measure rib cage
displacement (Hodges et al., 1997).
Subjects sat comfortably in a reclined chair with arms well-
supported, hips flexed to ?70?, and knees flexed to ?45?. A tight-
fitting elastic cap was worn over the head and the location of the
vertex was identified using the International 10/20 system (Jasper,
1958). The optimal location was identified (i.e. scalp site that
induced the largest contralateral response in TrA) using the figure-
of-eight coil set at suprathreshold intensity (?70–100% maximum
stimulator output) during the activation of TrA to 10% MVC.
Four motor thresholds (MT) for TrA were identified at the
(i) Active MT for contralateral responses using the figure-
(ii) Active MT for contralateral responses using the double-cone
(iii) Active MT for ipsilateral responses using the double-cone
(iv) Resting MT for contralateral responses using the double-
MTs were defined as the minimum intensity to evoke five
consecutive MEPs in TrA, and these were to be clearly discernible
from background EMG activity (Mills and Nithi, 1997). Previous
studies from our group have shown that TMS delivered over the
optimal location (?2cm lateral to the midline in most subjects)
minimizes concurrent stimulation of both motor cortices, and
evokes contralateral responses that are faster than ipsilateral
responses from the same hemisphere (Tsao et al., 2008).
Topography of TrA responses to TMS over the contralateral
motor cortex was examined using the figure-of-eight coil
(Wassermann et al., 1992; Wilson et al., 1993). The coil intensity
was set to 120% active MT, and stimulation was delivered over
pre-marked scalp sites on a 5?5cm grid oriented in a Cartesian
system. Five stimuli were delivered at each scalp site during 10%
MVC with an inter-stimulus interval of at least 5s (Wilson et al.,
1993). Early pilot trials in individuals with recurrent LBP showed
that MEPs could also be induced when TMS was delivered at scalp
sites posterior to the inter-aural line (i.e. the line that joins the left
and right pre-auricular creases and pass through the vertex). Thus
stimulation in the LBP group was extended 2cm posterior to the
vertex. This was not possible for the control group as data for that
group were collected prior to the LBP group. This does not
compromise the data as little or no activation was achieved by
stimulation at or behind the inter-aural line in this group.
Rapid arm movements
Subjects performed single rapid arm movements during a choice
reaction time task to induce a perturbation to the trunk for
assessment of postural activation of TrA (Hodges and Richardson,
1997). Subjects stood comfortably and remained relaxed prior to
movement of the left arm into flexion or extension to ?45?‘as
fast as possible’ in response to auditory tones triggered by the
experimenter. Movement direction was indicated by distinct tones
and emphasis was placed on the speed of arm movement rather
than magnitude. Practice trials were included to familiarize
subjects to the task. To ensure arm movements were performed
in a similar manner between trials, the left arm was attached to a
potentiometer at the wrist. This device restricted motion to the
sagittal plane and measured angular displacement. Ten trials of
arm flexion and extension were completed as this number of trials
has been shown to yield sufficient repeatability of the data.
Data analysis was undertaken using MATLAB 7 (The Mathsworks,
USA). For mapping, TrA activity from individual trials was full-
wave rectified. Trials at each scalp site were averaged, and the
onset and offset of the MEP (or onset of silent period) were
visually identified from the averaged full-wave rectified traces. As
recordings were made using intramuscular electrodes, peak-
to-peak amplitude is more variable due to recordings of a small
population of motor units. Thus, the amplitude of TrA MEPs was
measured as the RMS EMG amplitude between the onset and
offset of the MEP, and background RMS EMG was removed
(55 to 5ms prior to stimulation). TrA EMG amplitudes were
superimposed over respective scalp sites to produce a topogra-
phical map of responses of the muscle and normalized to the
amplitude of the peak response. As current spread during
Motor cortex and postural controlBrain (2008)Page 3 of11
by guest on June 8, 2013
magnetic stimulation enlarges the motor cortical map, it is
difficult to define map boundaries due to small amplitude MEPs
at the map edge (Uy et al., 2002). To minimize this problem,
normalized values below 25% of the peak response were removed.
Remaining responses were rescaled from 0 to 100%.
Two parameters were calculated from the rescaled nor-
malized maps. Map volume, which is a measure of the total
excitability of cortical representation, was calculated as the sum
of normalized MEP amplitudes recorded at all scalp sites
where responses were evoked (Wassermann et al., 1992). The
centre of gravity (CoG) was calculated using the formula:
CoG ¼Pzixi=Pzi;Pziyi=Pzi; where xi and yi are medial–
(Wassermann et al., 1992). This measure gives an amplitude-
weighted indication of map position. Although map volume can
substantially change with changes in motor cortical excitability,
studies have shown that the CoG is a valid and repeatable measure
of motor cortical representation (Boroojerdi et al., 1999; Uy et al.,
2002). Shifts in map position were also examined through
calculation of the absolute distance between the location of the
averaged CoG for the healthy group, and CoG for each individual
in the healthy and LBP groups.
For rapid arm movement tasks, the onsets of TrA and deltoid
EMG were visually identified as the point at which the EMG
increased above baseline levels. Visual identification of onset of
EMG activation has been shown to be reliable and is preferred
to computer-based methods as it is less affected by factors such
as amplitude of background EMG or rate of increase in EMG
activity (Hodges and Bui, 1996). Onsets of TrA EMG relative to
that of the prime mover deltoid were calculated for the left and
right TrA muscles. In addition, as onset of trunk muscle activity
depends on the acceleration of the arm (Hodges, 2001); angular
acceleration for each trial was calculated. Data of arm displace-
ment at the shoulder were smoothed at 10Hz and twice
differentiated to yield angular acceleration. Peak acceleration was
lateral and anterior–posterior locations, and zi is amplitude
Statistica 7 (Statsoft, USA) was used for statistical analysis.
Map volume and CoG location (lateral and anterior to the vertex)
were compared between groups (healthy versus LBP) and muscles
(left versus right TrA) using a repeated-measures analysis
of variance (ANOVA). Significant interactions were further
analysed using post hoc Duncan’s multiple range test. MTs
identified using the double-cone coil were compared between
groups, muscles and conditions (contralateral, ipsilateral and
resting MT) with a repeated-measures ANOVA. MTs identified
using the figure-of-eight coil were compared between groups
and muscles. In addition, onset of TrA EMG relative to that of
the prime mover deltoid was compared between individuals
with and without recurrent LBP using repeated-measures ANOVA
with two repeated measures [group and direction (flexion versus
extension)] and one independent factor (muscle). To determine
whether CoG, map volume and MT were associated with the
relative onset of TrA EMG in the arm movement task, the
relationship between MT and map parameters, and relative
onset of TrA activation during arm movement tasks were
examined using Pearson’s correlation. Significance was set at
Figure 1 shows group data for MTs during different
stimulation conditions. For all subjects, MTs could be
identified for all conditions over at least one motor cortex.
However, contralateral responses using the figure-of-eight
coil could not be evoked over one hemisphere in five
subjects from the healthy group and four subjects from
the LBP group, even at maximum stimulator output.
Ipsilateral responses using the double-cone coil could not
be evoked over one hemisphere in four healthy and one
LBP individual. Responses evoked ipsilateral to the side
of stimulation at the optimal location were on average
3?1ms (mean?SD) slower than MEPs evoked on the
contralateral side. This confirms that ipsilateral responses
were not due to concurrent excitation of the faster contra-
lateral pathways from the opposite motor cortex, and
originated from the stimulated motor cortex (Ziemann
et al., 1999; Tsao et al., 2008).
Using the double-cone coil, the lowest MT was found for
responses contralateral to the stimulated cortex (main effect
for condition P50.001; post hoc: P50.001; Fig. 1). No
differences in MT were detected between the left and right
TrA for any condition using the double-cone coil (main
effect for muscle P=0.84), or for MT using the figure-
of-eight coil (t=0.35, P=0.98).
MT for ipsilateral responses in the LBP group was
significantly lower compared to healthy controls (interac-
tion between condition and group P=0.009; post hoc:
P=0.04). Inspection of individual data showed a tendency
for greaterasymmetry ofipsilateralMTs between
Fig.1 Active and resting MTs for contralateral (contra) and ipsi-
lateral (ipsi) responses in healthy and LBP group. Mean and 95% CI
are illustrated.For double-cone coil, lower MT for ipsilateral
responses in LBP group was observed compared to healthy con-
trols (?P50.05).No differences were detected between groups for
MT to elicit contralateral responses using the double-cone coil or
Page 4 of11Brain (2008)H.Tsao et al.
by guest on June 8, 2013
hemispheres in most healthy individuals, but the lowest
threshold was not always on the dominant or non-
dominant side. A lesser difference between hemispheres
was observed for individual data for the LBP group. To
quantify this observation, the absolute difference in MT
between left and right TrA was calculated for each subject
(Fig. 2A). There was a greater difference in MTs for
ipsilateral responses compared to contralateral responses in
the healthy group (P=0.01), but not for the LBP group
(P40.14). Furthermore, absolute difference in MTs for
ipsilateral responses was greater for the healthy group
compared to LBP participants (P=0.043), i.e. less asymme-
trical. To examine this further, ipsilateral MT for each
individual were rearranged into either a ‘lower’ or ‘higher’
MT to evoke ipsilateral responses (Fig. 2B). When analysed
in this way, the MT for the less excitable hemisphere was
higher for the control subjects compared to those with LBP
(P50.001), but there was no difference between groups in
the MT for the more excitable hemisphere (P40.066).
Together, these data suggest that the reduced MT of
ipsilateral responses in the LBP group is likely due to
reduced MT of a less excitable side.
Motor cortical map
Average maps of TrA responses to TMS for healthy and
LBP groups are illustrated in Fig. 3. The time of onset and
offset of contralateral MEPs were not different between
healthy and LBP groups [main effect for group P=0.63;
mean ? SD onset 16?1ms, mean?SD offset 35?5ms
(averaged across healthy and LBP groups)]. No differences
in map volume were detected between the left and right
hemispheres for either group (main effect for side P=0.89).
However, the volume of TMS maps for the LBP group was
greater compared to healthy controls (healthy 5.2?1.2,
Furthermore, the location of TrA CoG for LBP was located
posterior and lateral to the CoG location in healthy
main effectfor groupP50.001).
individuals (interaction for location and group P50.001;
post hoc: P50.011, Fig. 4). No difference was observed
between the left and right motor cortices (main effect for
muscle P=0.08). The TrA CoG in individuals with
Fig. 2 (A) Absolute difference in MT between the left and right TrAs.Note absolute difference in MTwas greater for ipsilateral responses
compared to that for contralateral responses in the healthy group. However, comparisons of the absolute difference between ipsilateral
and contralateral MTs were not significant (NS) for the LBP group. (B) MT for ipsilateral responses in healthy and LBP group, re-arranged
into the side with higher or lower MT . Mean and 95% CI are displayed. Note MT in LBP group on the less-excitable side is less than MT
in the control group. (?P50.05).
Fig. 3 Average normalized motor cortical maps for the healthy
and LBP groups on the left and right hemisphere. Mean and SD
of the CoG is displayed.The black cross represents the location
of vertex, horizontal dotted line denotes the inter-aural line
and vertical dotted line denotes the line that connects the nasion
and inion (Calibration ^1cm).
Motor cortex and postural controlBrain (2008) Page 5 of11
by guest on June 8, 2013
recurrent LBP were located further away from the mean
location of TrA CoG in healthy controls than the individual
data for the control group (healthy: 0.45?0.22cm; LBP:
Rapid arm movements
Figure 5 illustrates the onset of TrA EMG relative to that of
the deltoid during rapid arm flexion and extension tasks.
When LBP individuals moved their arm rapidly into flexion
or extension, activation of TrA EMG was significantly
delayed comparedto healthy
between group, muscle and direction: F=7.8, P=0.007;
post hoc: P50.001). No differences were observed between
onsets for the left and right TrA muscles (post hoc:
P40.065). There was no difference in peak arm accelera-
tion between healthy and LBP group for arm flexion
(healthy: 2411?622?/s2; LBP: 2208?938?/s2; P=0.32) or
extension (healthy: 1802?436?/s2; LBP: 1751?509?/s2;
P=0. 41). This suggests the arm was moved in a similar
manner by both groups.
The location of TrA CoG was associated with onset of
TrA EMG during rapid arm flexion and extension tasks
(r40.37, P50.033; Fig. 6). That is, slower activation of
TrA was likely when the CoG was located more posterior
and lateral. Similar correlations were found for map
volume; increased map area was associated with slower
onset of TrA EMG (r40.57, P50.001; Fig. 7). There were
no significant correlations between MTs and timing of TrA
EMG onset (all: P40.17).
This study demonstrates that LBP is associated with
reorganization of the networks in the motor cortex associated
with activation of the deep trunk muscle, TrA. Posterior and
lateral shifts in the CoG and greater map volume were
observed in individuals with recurrent episodes of LBP
compared to healthy individuals. A particularly novel finding
was that the location of the CoG and volume of the TrA map
at the motor cortex were related to the timing of onset of TrA
EMG during a functional task. There were also changes in
MT; compared to controls, threshold for ipsilateral responses
on the less excitable side was reduced. As changes in control
Fig. 4 Group (A) and individual data (B) of the CoG of TrA. Note that for group data, the location of TrA CoG in LBP group was located
posterior and lateral toTrA CoG in healthy groups (?P50.05).This was observed in most subjects.
Fig. 5 Relative onset of TrA activation (mean and 95% CI) during
rapid arm flexion and extension tasks for the healthy and LBP
groups. Dotted line represents onset of prime mover activation.
Data show slower activation of TrA in LBP group for both the left
and right TrA muscles and during both arm flexion and extension
tasks (?P50.05 between healthy and LBP group).
Page 6 of11 Brain (2008)H.Tsao et al.
by guest on June 8, 2013
of TrA are consistently observed in individuals with recurrent
LBP, these findings suggest that changes at the motor cortex
may underlie or at least contribute to alterations in postural
Reorganization of the motor cortex
in recurrent LBP
The current study confirms that topography of the
representation of the abdominal muscles on the motor
cortex can be evaluated using TMS. In healthy individuals,
TrA representation was located at scalp sites ?2cm anterior
and lateral to the vertex. This location is consistent with the
optimal location used in previous studies to evoke
responses in the more superficial abdominal muscles
recorded with surface EMG electrodes (Fujiwara et al.,
2001; Strutton et al., 2004). As expected, based on the
distribution of body representation in the motor homuncu-
lus (Penfield and Boldrey, 1937; Woolsey et al., 1952), the
representation of TrA was located medially compared to
Fig. 6 Relationship between location of the CoG; (distance anterior and lateral from the vertex) and timing of TrA activation during
arm flexion and extension. Linear regressions are shown with 95% CI.Vertical dotted line represents activation of prime mover deltoid.
Circles represent data of individuals from the healthy group (white) and LBP group (black). Data showed that individuals with slowerTrA
activation (mostly individuals from LBP group) tended to haveTrA CoG located more posterior and lateral to the vertex.
Fig. 7 Relationship between normalized map volume and timing of TrA activation during arm flexion and extension. Linear regressions
are shown with 95% confidence interval.Vertical dotted line represents activation of prime mover deltoid.Circles represent data of
individuals from the healthy group (white) and LBP group (black).There was a positive correlation between normalized map volume and
relative onset of TrA activation.
Motor cortex and postural controlBrain (2008) Page 7 of11
by guest on June 8, 2013
that of the upper limb (Wilson et al., 1993; Pascual-Leone
et al., 1994), neck (Thompson et al., 1997) and facial
muscles (McMillan et al., 1998).
The CoG of TrA at the motor cortex in individuals with
recurrent LBP was shifted posteriorly and laterally to that of
healthy individuals. Shifts in the motor cortical representa-
tion of specific muscle(s) have been reported in people with
other recurrent pain conditions. For instance, studies of
patients with phantom limb pain following upper limb
amputations demonstrated a shift in the optimal location to
evoke responses in the facial muscles on the side of the
amputation towards the representation of the missing hand
(Karl et al., 2001). The CoG is argued to be a robust
measure of motor cortical representation and corresponds
closely to the area of high excitability of corticomotor
neurons that project to the target muscle(s) (Wassermann
et al., 1992). Furthermore, TMS CoG closely approximates
the CoG identified from functional magnetic resonance
imaging (Boroojerdi et al., 1999; Lotze et al., 2003). Thus,
shifts in TrA CoG from TMS maps could imply changes in
the structural or functional organization of cortical net-
works associated with activation of TrA at the motor
cortex. As this shift was consistently observed in most
individuals with recurrent episodes of LBP, we argue that
these findings are unlikely to be related to cap displace-
ment, variability in coil placement or orientation, or
inaccurate identification of the vertex. Future studies that
utilize brain MRI and navigated brain stimulation with
TMS mapping are likely to reduce the variability of motor
cortical maps and further validate the present findings.
In addition, as evidence reveals reduced grey matter density
of the prefrontal cortex in patients with chronic LBP
(Apkarian et al., 2004), further studies are needed to
examine whether these structural changes in the brain are
associated with changes in functional organization of the
motor cortex, or how this relates to changes in motor
Map volume was also increased in the LBP group
compared to healthy individuals. This finding is similar to
expansion in area of representation at the somatosensory
cortex of patients with acute (Soros et al., 2001) and
recurrent pain (Flor et al., 1997). However, increases in
motor cortical map volume are not consistent with reduced
map areas in patients with complex regional pain syndrome
(Krause et al., 2006). This could be related to differences in
the calculation of map area, as that study measured two-
dimensional spread of representation over scalp sites
whereas we measured map volume. It is also possible that
reduced map areas detected in patients with complex
regional pain syndrome relate to the nature of injury
sustained in this group of patients, all of which involved
forearm fractures that were immobilized for a period of
time following post-fracture. As reduced motor cortex
representation has been demonstrated with immobilization
and disuse (Liepert et al., 1995), reduced map area in that
study could be associated with disuse rather than the
presence of pain and injury.
Increased map volume is difficult to interpret as
stimulation of the cortical cells/interneurons with TMS is
accompanied by current spread to produce TMS maps
which are larger than the actual area of motor cortical cells
that project to the target muscle (Roth et al., 1991; Mortifee
et al., 1994; Thickbroom et al., 1998). It could be argued
that increases in map volume in the LBP group could
correspond to an increase in the total excitability of motor
cortical cells and thus excitation by stimulation over a large
area of the cortex (Wassermann et al., 1992). However,
there were no differences in MT for contralateral MEPs at
the optimal location between the LBP and healthy groups.
Taken together, increased map volume without changes in
MT at the optimal location suggest that alteration of motor
cortical maps are not simply due to increased excitability of
cortical cells, but involve more complex neural mechanisms
that increase the area of the cortical networks involved in
the activation of TrA.
Representation at the motor cortex
is associated with postural activation
of the trunk muscles
During rapid voluntary limb movements, the CNS initiates
postural adjustments in advance of predictable perturba-
tions to the body and these involve activation of trunk and
limb muscles (Belen’kii et al., 1967). As this activation is
initiated before feedback is available, they must be pre-
programmed by the nervous system (Bouisset and Zattara,
1981). In the current study, postural activation of TrA, in
most trials, occurred either before or550ms after the onset
of deltoid EMG. Taking into account electromechanical
delay and the latency for nerve conduction, even the
shortest latency response to feedback from limb movements
cannot be initiated before 50ms after the onset of deltoid
EMG (Aruin and Latash, 1995). Thus, the current study
confirms previous findings that feedforward activation of
TrA is associated with voluntary limb movements in
healthy individuals (Hodges and Richardson, 1997), and
that activation of TrA is delayed in individuals with
recurrent LBP (Hodges and Richardson, 1996).
A novel finding was that the cortical reorganization of
inputs to TrA was associated with onset of TrA EMG
during rapid limb movements. This relationship is con-
contributes, at least in part, to postural activation associated
with limb movements (Gahe ´ry and Nieoullon, 1978;
Hodges et al., 2003). The present data provide evidence
that changes in its organization at the motor cortex may
contribute to deficits in feedforward postural control. As
similar deficits in feedforward control have been demon-
strated in other trunk muscles [for instance, the lumbar
multifidus muscles (MacDonald et al., 2004)], the current
findings suggest the potential for similar reorganization of
Page 8 of11 Brain (2008)H.Tsao et al.
by guest on June 8, 2013
neural networks at the motor cortex that contribute to the
control of these muscles.
Exactly how changes in motor cortical representation are
associated with deficits in postural control remains spec-
ulative. One possibility is that reorganization in motor
cortical map of TrA and potentially other muscles in
patients with recurrent LBP could distort the coordination
between muscles. Data from people with focal hand
dystonia provide evidence that reduced ability to isolate
finger movements is associated with reorganization (i.e.
reduce differentiation of individual finger representations)
of the sensorimotor cortex (Byl et al., 1996). Although TMS
maps of other trunk or limb muscles were not evaluated in
the current study, similar mechanisms may contribute to
Furthermore, several studies have reported atrophy of the
paraspinal muscles in human and animal studies of pain
and injury to the low back (Hides et al., 1994; Hodges
et al., 2006). Thus, it is reasonable to speculate that these
morphological changes may be associated with reorganiza-
tion at the sensorimotor cortex. This warrants further
In addition, the trunk muscles receive multiple projec-
tions from other supraspinal and spinal centres (see review
Iscoe, 1998). For example, the reticulospinal and vestibu-
lospinal neurons, which are intricately involved in postural
control, have descending projections to the abdominal
motoneurons (Miller et al., 1985; Miller et al., 1989).
Changes in the excitability and/or organization of these
regions of the CNS are also likely to contribute to changes
in postural control of the trunk muscles in patients with
ofthe trunk muscles.
Reduced MT for ipsilateral corticospinal
projections to the abdominal muscles
There was greater asymmetry in MT between the left and
right hemispheres for ipsilateral responses compared to
contralateral responses in control subjects. The lateraliza-
tion of ipsilateral MT to one side is consistent with findings
from other proximal (MacKinnon et al., 2004) and axial
muscles (Strutton et al., 2004), and was unrelated to
handedness. Interestingly, individuals with recurrent LBP
did not demonstrate this asymmetry in ipsilateral MT. The
MT to evoke responses in the left and right TrA in people
with recurrent LBP was similar to the more excitable side in
healthy individuals. One interpretation of this finding could
be that coordination of the activation of the right and left
abdominal muscles in healthy individuals is mediated
by contralateral and ipsilateral projections from a single
hemisphere, that is, the cortex with the lower threshold
ipsilateral projections. In contrast, in people with recurrent
pain the symmetrical excitability of ipsilateral projections
suggests no preference for control by a single hemisphere.
Although changes in MT for ipsilateral responses did not
correlate with changes in timing of TrA activation, this does
not exclude a contribution of ipsilateral projections to
postural control of the trunk muscles. It has been argued
that responses evoked ipsilateral to the stimulated cortex
using TMS are likely to be mediated via slower conducting
uncrossed polysynaptic corticospinal pathways that project
via regions in the brain stem (Ziemann et al., 1999). These
brainstem pathways are also intricately involved in the
coordinationof timing and
responses (Inglis and Macpherson, 1995; Prentice and
Drew, 2001). Changes in excitability of these pathways
may contribute to alterations in activation of the trunk
muscles for postural control. However, whether the earliest
component of postural responses is related to ipsilateral
projections, or how changes in excitability are related to
coordination of muscle activation remains unclear.
The present findings suggest that deficits in postural control
in a patient population are associated with reorganization
of the motor cortex. In patients with recurrent LBP, these
deficits in postural activity can be trained by skilled motor
training that involves voluntary contractions of muscle(s)
(Tsao and Hodges, 2007, 2008), and is associated with
improvements in clinical outcomes (see review Ferreira
et al., 2006). Skilled motor training induces greater plastic
change at the motor cortex than strength training (see
review Adkins et al., 2006). Thus it is reasonable to predict
that reorganization of the motor cortex following skilled
motor training may be associated with improved postural
activity in patients with deficits in postural control. This
requires further investigation.
Financial support was provided by the National Health and
Medical Research Council of Australia (ID351656 to HT
and ID401599 to PH) and the Physiotherapy Research
Foundation (Grant No: 007/06).
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