Transient Modulation of Intracortical Inhibition Following Spinal

Manipulation

HEIDI HAAVIK-TAYLOR and BERNADETTE MURPHY

ABSTRACT: Objective: To study the immediate sensorimotor neurophysiological effects of cervical spine
manipulation using transcranial magnetic stimulation (TMS). Design: Experimental design. Setting: This study
was carried out at the Human Neurophysiology Laboratory at the University of Auckland in Auckland, New
Zealand. Participants: Thirteen (13) subjects with a history of recurring neck stiffness and/or neck pain, but
no acute symptoms at the time of the study were invited to participate in the study. Intervention: Three (3)
interventions were carried out in a randomised order: a control with no intervention, a passive head move-
ment control condition, and a session of spinal manipulation of dysfunctional cervical joints. Main Outcome
Measures: Motor evoked potentials (MEP) and cortical silent periods (CSP) in the abductor pollicis brevis
(APB) muscle of the dominant hand following transcranial magnetic stimulation (TMS) over the motor cortex.
Results: The major finding of this study was that the TMS-induced CSP measured in APB was significantly
decreased for the first 20 minutes following spinal manipulation. No such changes were observed follow-
ing either control condition, i.e. following no intervention or following passive head movement. Conclusion:
Spinal manipulation of dysfunctional cervical joints can lead to transient central neural plastic changes, as
demonstrated by shortening of the TMS-induced CSP. This study suggests that cervical spine manipula-
tion may alter sensorimotor integration. These findings may help to elucidate the mechanisms responsible
for the effective relief of pain and restoration of functional ability documented following spinal manipulation
treatment.
INDEX TERMS: (MeSH): MANIPULATION, CERVICAL; PSY-
CHOMOTOR PERFORMANCE; TRANSCRANIAL MAGNETIC
STIMULATION. (Other): HUMAN; BRAIN PLASTICITY; CORTI-
CAL SILENT PERIOD. Chiropr J Aust 2007; 37: 106-116.

INTRODUCTION Spinal manipulation is used therapeutically by a number

Spinal manipulation is a commonly used conservative
treatment for neck, back and pelvic pain. The effectiveness
of spinal manipulation in the treatment of acute and chronic
low back and neck pain has been well established by
outcome-based research.1-7 Despite this, the mechanism(s)
responsible for the effective relief of pain and restoration
of functional ability after spinal manipulation are not well
understood. There is limited evidence to date regarding
the neurophysiological effects of spinal manipulation. The
evidence to date indicates that spinal manipulation can
lead to alterations in reflex excitability,8-10 altered sensory
processing,11-13 and altered motor excitability.14-16
Heidi Haavik-Taylor, PGDip(Science), BSc(Chiro)
Human Neurophysiology and Rehabilitation Laboratory
Department of Sport and Exercise Science
University of Auckland
Bernadette Murphy, PhD, DC
University of Auckland
The results presented in this paper are part of the lead author’s PhD thesis.
The paper was presented at the Chiropractors’ Association of Australia
Scientific Symposium and Policy Form, August 2006.
of health professionals, including physical medicine
specialists, physiotherapists, osteopaths and chiropractors.
The different professions have different terminology for
the “entity” or “manipulable lesion” that they manipulate.
This manipulable lesion may be called “vertebral (spinal)
lesion” by physical medical specialists or physiotherapists,
“somatic dysfunction” or “spinal lesion” by osteopaths, and
“vertebral subluxation” or “spinal fixation” by chiropractors.17
Joint dysfunction as discussed in the literature ranges from
experimentally induced joint effusion18 to pathological
joint disease such as osteoarthritis,19 as well as the more
subtle functional alterations that are commonly treated by
manipulative therapists.14,15 For the purposes of this paper,
the “manipulable lesion” will be referred to as an area of
spinal dysfunction.
There is a growing body of evidence suggesting that
the presence of spinal dysfunction of various kinds has an
effect on central neural processing. A recent study has shown
altered cortical processing for 20 minutes following spinal
manipulation of dysfunctional cervical joints in subjects with
chronic neck complaints.11 Furthermore, several authors have
suggested spinal dysfunction may lead to altered afferent
input to the CNS.9.12.13.20.21 Altering afferent input to the CNS
is well known to lead to plastic changes in the way that it
responds to any subsequent input.22-27 Neural plastic changes

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106 Volume 37 Number 3 September 2007

take place following both increased23,25 and decreased22,24,26-28
afferent input.
Altered afferent input from joints can lead to both inhibition
and facilitation of neural input to related muscles. Numerous
studies of painful joints have shown arthrogenous muscle
inhibition,29-31 however even painless experimentally induced
joint dysfunction (joint effusion) has been shown to inhibit
surrounding muscles.18 This altered motor control was also
shown to persist even after aspiration of joint effusion.18 In
the early 1980s, Steinmetz et al. demonstrated that relatively
short (15-30 min) episodes of moderately intense afferent
input to the spinal reflex pathways of rats causes increases
in neural excitability that persists for several hours.32,33 Once
these facilitated areas are established, there may be no need
for ongoing afferent input to maintain the altered output
patterns. Since these early experiments, numerous studies
have shown rapid central plastic changes after injuries and
altered sensory input from the body.34 This can explain the
findings of Shakespeare et al.18 of altered motor control
persisting even after aspiration of joint effusion. This process
provides a potential explanation for altered neural processing
as a result of joint dysfunction, and a rationale for the effects
of spinal manipulation on neural processing that have been
described in the literature.
One relatively non-invasive method to investigate such
plastic changes in humans is transcranial magnetic stimulation
(TMS). TMS has been used to demonstrate changes following
deafferentation of the CNS, such as anaesthetic nerve block35,36
or ischemic nerve block22,24,37, 38 Similarly, TMS has been
utilised to demonstrate plastic changes in humans following
hyperafferentation of the CNS, such as with a repetitive finger
typing task,39,40 or following peripheral stimulation.41
Given that spinal dysfunction would alter the balance
of afferent input to the CNS, we propose that this altered
afferent input may over time lead to potential maladaptive
neural plastic changes in the CNS. We have shown that spinal
manipulation does affect cortical processing,11 and further
propose that it should be possible to measure such changes in
human subjects non-invasively utilising TMS. Our aim with
this study is to measure any alterations in the cortical control
of a hand muscle that may occur following manipulation of
the cervical spine.
METHODS
Subjects
Thirteen (13) subjects participated in this study, including
8 females and 5 males aged 22 to 45 (mean age 30.7 ± 7.9 yr).
Twelve (12) of the subjects were deemed to be right-handed
(mean laterality quotient 96.91%, range 83.33% — 100%)
and one left-handed (laterality quotient 90.09%), using the
Edinburgh handedness questionaire.42 To be included subjects
could not have a history of neurological disease, or any known
contraindications to either spinal manipulation or magnetic
stimulation (described in more detail below). The subjects
were furthermore required to have a history of recurring
neck pain or stiffness (e.g. present during the performance
of certain tasks such as work or study). At the time of the
experiment, however, all subjects were required to be pain
free (judged by the subjects themselves). This was done in
order to assess the potential effects of spinal manipulation
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SENSORIMOTOR EFFECTS OF SMT
HAAVIK-TAYLOR • MURPHY
delivered to dysfunctional joints alone without the presence
of acute pain, as the presence of pain alone is known to
alter corticomotor measures such as utilised in the current
study.43 Table 1 contains the subjects’ details, including their
neck complaint history and known past neck (and/or head)
trauma. Informed consent was obtained, and the University
of Auckland Human Participants Ethical Committee approved
the study in accordance with the Declaration of Helsinki.
Transcranial Magnetic Stimulation (TMS)
One MagStim 200 (MagStim, Dyfed UK) magnetic
stimulator and a 55 mm diameter figure-of-eight coil was
used to deliver single-pulse magnetic stimuli over the cortical
motor strip opposite to the dominant limb at the optimal
position for eliciting motor evoked potentials (MEPs) from
the abductor pollicis brevis (APB). A purpose-made tight-
fitting cotton cap marked with a 1 cm grid over M1 was
initially positioned with reference to the vertex, and utilised to
locate the optimal site. This optimal site was then marked on
the scalp to ensure identical placement of the coil throughout
the experiment. The coil was held approximately 45o to the
midline with the handle pointing posteriorly. Active motor
threshold was determined. This was defined as the minimal
stimulus intensity at which 4 out of 8 consecutive stimuli
evoked a MEP with an amplitude of at least 100μV in APB
muscle while holding a weak isotonic background contraction
of 5-10% maximum voluntary contraction (MVC).
EMG Recording
Surface electromyographic (EMG) recordings were made
from the APB muscle. Electrodes were placed with the active
electrode over the motor point and the reference electrode
over the metacarpophalangeal joint. The ground electrode
was placed on the lateral epicondyle of the distal end of the
humerus. EMG signals were collected from 7 mm diameter
Hydrospot Ag/AgCl electrodes (Physiometrix Inc., USA),
fixed with tape 1 cm apart following standard skin preparation
to reduce electrode impedance to less than 5 kΩ. EMG signals
were amplified by a Grass Model 15 Neurodata acquisition
system via an IMEB Model Bio-potential Isolator Electrical
Board (Grass), band-pass filtered at 30 Hz-1 kHz (−6 dB
cut-off points), sampled at a rate of 2 kHz by a LabView
acquisition system and displayed using a custom made
LabView program, and stored to disk for off-line analysis.
Motor Evoked Potentials (MEPs) and Cortical Silent
Period Duration (CSP)
Blocks of 16 trials of MEPs and CSPs were recorded with
APB holding a 5-10% background contraction with 6 sec
intervals between the magnetic stimuli. Stimulus intensity
was set to 150% ATh for APB. The level of contraction
was standardised across subjects for the APB muscle by
determining the MVC for each subject. The root mean
square (RMS) level of EMG was obtained during a 3 sec
MVC obtained individually from the target muscle (best of
3). The limits for the EMG were then set at 5 and 10% of the
maximum RMS level during the MVC. The RMS level of
contraction was displayed in real time to provide feedback
and assist the subject in maintaining the appropriate level of
contraction. A stimulus was triggered by the computer only
when the RMS level was maintained by APB within their
individual range for 1.5 sec.
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Table 1

SUBJECT AGE, GENDER, HANDEDNESS AND HISTORY

No. Gender Age (yr) Handedness Subjective Neck Complaints, Known Head/Neck Injury, Previous
Spinal Manipulation History.

1 F 38 R Almost constant dull right sided neck ache. The neck pain has been recurring
regularly for 16 yr since MVA where she was thrown through windscreen. Did see
chiropractor and physiotherapist for a few sessions each many yr ago.

2 F 28 R 10 yr intermittent neck pain and tension. Minor whiplash 10 yr ago. Seeks regular
chiropractic treatment.

3 F 34 R Neck discomfort with stress and excess work for past yr. No previous known
head or neck injuries. No previous spinal manipulation treatment.

4 M 26 R Recurring neck tension and pain since head and neck injury from playing rugby 4
yr ago. Has received a few chiropractic treatments only years ago.

5 M 25 R 6 yr intermittent neck tension and neck muscle aches. Neck complaint worse
with rock climbing, when driving a car and during painting work. Receives regular
chiropractic care.

6 F 41 R 14 yr of recurring neck pain and stiffness, particularly with stress. No known

previous injuries. Receives regular chiropractic care.

7 F 45 R 28 yr recurring neck pain, stiffness and muscle tension. Worse with computer
work and sitting reading. Pain at top and base of neck. Injury to base of neck 30
yr ago, fractured right collarbone 4 yr ago. Occasionally sees a chiropractor.

8 M 40 R Occasional neck tension with prolonged computer work. No previous neck or

head injury. No previous spinal manipulation treatment.

9 F 22 L 2 yr recurring sub-occipital neck pain and general neck stiffness recurring when
working long hours in front of computer. Fell off mountain bike onto face 6 mo
ago. Was sore for weeks, had few chiropractic manipulations and pain went
away.

10 M 22 R Occasional neck tension during last few yr. Multiple minor head and neck injuries.
Regularly received chiropractic care since childhood.

11 F 27 R Right sided neck pain intermittently over last 4 yr. Minor whiplash injury 5 yr ago.
Regularly seeks chiropractic treatment past 7 yr.

12 F 27 R Recurring base of neck pain every few months past 4 yr. Two snowboarding
accidents hitting side of head and neck, 6 and 8 yr ago. No previous spinal
manipulation treatment.

13 M 24 R Recurring neck tension 3 yr duration. Worse when playing drums or working at

computer for prolonged periods. No known head or neck injuries. Occasionally
receives spinal manipulation.

F Waves Spinal Manipulation Intervention

To assess spinal motor excitability F waves were recorded
from the subjects’ relaxed APB. The median nerve was
stimulated at the wrist with a supra-maximal (1.25 Mmax)
electrical stimulation consisting of square-wave constant
current pulses with pulse width duration of 0.2 ms. Twenty
(20) trials were recorded for each subject before and after
each intervention. The F wave amplitudes were expressed
as a percent of the M wave amplitude.
This intervention consisted of spinal manipulation of the
subjects’ dysfunctional cervical joints, which was determined
by a registered chiropractor. The clinical evidence of joint
dysfunction includes tenderness to palpation of the relevant
joints, restricted intersegmental range of motion, palpable
asymmetric intervertebral muscle tension, abnormal or
blocked joint play and end-feel of a joint, and sensorimotor
changes in the upper extremity.44,45 The most reliable spinal

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108 Volume 37 Number 3 September 2007

dysfunction indicator is tenderness with palpation of the
dysfunctional joint.46,47 Cervical range of motion48,49 has also
been shown to have good inter- and intra-examiner reliability.
For the purpose of this study, spinal dysfunction was therefore
defined as the presence of both restricted intersegmental
range of motion and tenderness to palpation of the joint in
at least one cervical spine segment. This was detected in the
following manner: The examiner, a registered chiropractor
with at least 7 years of clinical experience, would passively
move the subject’s head while palpating and stabilising over
the zygapophyseal joints. For each spinal segment the head
would be gently and passively moved from neutral position
to the maximal range of lateral flexion in the coronal plane, to
both the left and right. If this movement appeared restricted,
the examiner would apply gentle pressure to the joint while
watching for signs of discomfort from the subject. The
examiner would also ask the subject if the pressure to the
joint elicited pain. Spinal segments that were deemed both
restricted in lateral flexion range of motion and elicited pain
on palpation were defined for the purpose of this study to be
dysfunctional.
The spinal manipulations carried out in this study were
high-velocity, low-amplitude thrusts to the spine held in
lateral flexion, with slight rotation and slight extension. This
is a standard manipulative technique used by manipulative
physicians, physiotherapists and chiropractors. The
mechanical properties of this type of CNS perturbation have
been investigated, and although the actual force applied to the
subject’s spine depends on the therapist, the patient, and the
spinal location of treatment, the general shape of the force-
time history of spinal manipulation is very consistent,50 and
the duration of the thrust is always less than 200 msec.51 The
high-velocity type of manipulation was chosen specifically,
since previous research 52 has shown that reflex EMG
activation observed following manipulation occurred only
following high-velocity, low-amplitude manipulation (as
compared with lower velocity mobilisations), and would
therefore be more likely to alter afferent input to the CNS
and lead to measurable TMS evoked potential changes.
Control and Passive Head Movement Intervention
The control intervention consisted of no intervention. The
passive head movement intervention was carried out by the
same chiropractor who had pre-checked the subjects for spinal
dysfunction and who performed the spinal manipulations
for the spinal manipulation experiment. The passive head
movement intervention involved the subject’s head being
passively laterally flexed, and slightly extended and rotated
to a position that the chiropractor would normally manipulate
that person’s cervical spine, and then return the subject’s head
back to neutral position. This was repeated to both the left and
the right. The experimenter was particularly careful, however,
not to put pressure on any individual cervical segment.
Loading a joint, as is done prior to spinal manipulation,
has been shown to alter paraspinal proprioceptive firing in
anaesthetised cats,53 and was therefore carefully avoided by
ending the movement prior to end-range-of-motion when
passively moving the subjects’ heads. No spinal manipulation
was performed during any passive head movement
experiment. The passive head movement experiment was
not intended to act as a sham manipulation, but to act as a
physiological control for possible changes occurring due to
Chiropractic Journal of Australia
Volume 37 Number 3 September 2007
SENSORIMOTOR EFFECTS OF SMT
HAAVIK-TAYLOR • MURPHY
the cutaneous, muscular or vestibular input that would occur
with the type of passive head movement involved in preparing
a subject/patient for a cervical manipulation.
Experimental Protocol
Subjects were first given written and verbal information,
and informed consent was obtained. All the subjects’ cervical
spines were then checked by a registered chiropractor to
determine if and where their spines would be manipulated.
If the subjects were judged to have cervical spine dysfunction,
the relevant information (including detailed medical
history) was obtained. All subjects were also screened for
evidence of vertebral artery ischemia, with the head in a
position of extension, lateral flexion and rotation, which
are neck positions shown to have the greatest mechanical
stress to the contralateral vertebral artery.54 Subjects were
also screened for other contraindications for cervical
manipulation, such as a recent history of trauma, known
conditions such as inflammatory or infectious arthropathies,
or bone malignancies. Finally, subjects were screened for
contraindications for magnetic stimulation, such as a history
of epilepsy, pregnancy, or metal implants in the brain.
Two sets (baseline 1 and 2) of the experimental measures
(MEPs and CSPs described above) were then recorded
before, and three sets (post-intervention trials 1, 2, and
3 are labelled trial 0-10 min, 10-20 min, and 20-30 min
on all tables and figures) were recorded after the control
intervention, the passive head movement intervention, or the
spinal manipulation intervention. For ATh, F wave properties
and M wave response only one set was measured before and
after the 3 interventions. The various measures were recorded
in a randomised order. The order that the 3 interventions
were carried out was also randomised. If the subject was to
receive the spinal manipulation trial before either the control
or passive head movement conditions, these were carried
out at a separate time, with at least 4 weeks in between. The
first post-intervention trial (trial 0-10 min) was recorded
within the first 10 minutes after the various interventions,
the next post-intervention trial (trial 10-20 min) was recorded
10-20 minutes after the various interventions, and the last
post-intervention trial (trial 20-30 min) was recorded 20-30
minutes after the various interventions.
Data Analysis
The effect of the 3 interventions, control with no
intervention, passive head movement and spinal manipulation,
were analysed separately. The peak-to-peak amplitudes (mV)
of the 16 MEPs per trial were averaged for statistical analysis.
For increased objectivity in the data analysis process, the CSP
duration was also determined using a LabView computer
program written to measure the time from TMS stimulation
to re-onset of EMG. Re-onset of EMG was determined using
the integrated profile method55 implemented in LabView. The
integrated profile method first integrates the non-rectified
EMG data over time. A function was created representing
the integral of the signal from the start of the data to each time
point. This function was amplitude normalised using the total
integral value. A second function was created representing
a signal with an integral equally distributed over time. The
re-onset of EMG was defined as the time at which there was
109
SENSORIMOTOR EFFECTS OF SMT
HAAVIK-TAYLOR • MURPHY
Figure 1. Graph of normalised integral and time normalised func-
tion demonstrating the time of maximal difference between the two
which will be the time chosen to represent re-onset of EMG for CSP
calculations.
Figure 3. Bar graphs showing the changes observed in the averaged
CSPs SE before (pre-intervention mean) and after (trials 0-10 min,
10-20 min and 20-30 min) no intervention (the black bar), a single
session passive head movement (the chequered bar) and cervical
spine manipulation (the grey bar). Note no significant changes were
observed following the control or passive head movement interven-
tion. The significant changes that occurred following the spinal
manipulation session are indicated with a star (*).
maximal difference between these two functions (Figure
1). To avoid the effect of the MEP peaks on the re-onset
determination, the user visually places a cursor after the
MEP peaks, and the signal from the cursor onwards is used
in the integrated profile method. As long as the cursor was
placed anywhere in the first half of the silent period, the CSP
calculations were consistent. The 16 CSPs were averaged for
each trial for statistical purposes.
The median nerve stimulation EMG traces were inspected
visually for the presence of F waves. If present, their peak-
to-peak amplitudes (mV) were determined and averaged per
subject both before and after each intervention. The peak-to-
peak amplitudes (mV) of the M wave were also determined,
and the mean F wave amplitude was expressed as a percentage
of the M wave for statistical comparisons. F wave persistence
110
Figure 2. Bar graphs showing the averaged MEPs SE before (pre-
interval mean) and after (trials 0-10 min, 10-20 min and 20-30 min) no
intervention (the black bar), a single session passive had movements
(the chequered bar) and cervical spine manipulation (the grey bar).
Note no significant changes were observed following the control, the
passive head movement, or the spinal manipulation interventions.
Figure 4. Raw non-rectified EMG traces from one representative
subject showing the MEP and CSP prior to and after the various
interventions.
was measured as a percentage of F waves present in the 20
trials recorded before and after each intervention.
All subjects’ ATh, M wave amplitudes, F wave persistence
and amplitudes were compared in each of the experiments
before and after the intervention with paired t-tests. The
averaged MEPs and CSP from the two baseline EMG
trials recorded after TMS were combined into a single pre-
intervention trial after first ensuring there was no statistical
difference between them by using paired t-tests. Averaged
MEPs and CSP were initially analysed with a one-way
analysis of variance (ANOVA) for repeated measures with
the factor “intervention”. If significant, repeated measures
ANOVAs were applied separately for each intervention
with a priori contrasts set up to compare each of the three
post-intervention data (post-control, post-passive head
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Table 2

SPINAL SEGMENTS MANIPULATED FOR EACH SUBJECT IN STUDY

Subject No. Spinal Segments Manipulated
1 C2/3 and C6/7
2 C2/3 and C5/6
3 C1/2 and C4/5
4 C0/1, C3/4 and C6/7
5 C1/2 and C5/6
6 C2/3 and C5/6
7 C2/3 and C6/7
8 C2/3 and C6/7
9 C1/2 and C6/7
10 C0/1, C3/4 and C6/7
11 C2/3 and C6/7
12 C1/2, C3/4 and C6/7
13 C2/3 and C6/7

movement and post-manipulation) with their baseline values.
Significance level was set up at p < 0.05 for all experiments.
Planned comparisons were chosen instead of post hoc analysis
to minimise Type 1 error, without reducing the sensitivity to
relevant effects.56
RESULTS
Subject Statistics
Table 1 shows the subjects’ details, including age, gender,
history of cervical pain or tension, any known neck and/or
head trauma, and previous spinal manipulation treatment
history. Table 2 shows the spinal segments manipulated for
each subject in this study. No adverse effects were reported
during this study.
Control With No Intervention
There were no statistically significant differences between
the pre-intervention baseline trials prior to the control with no
intervention. There were no significant changes observed in
any of the experimental variables following the control with
no intervention (Figures 2, 3, 4 and Tables 3 and 4).
Passive Head Movement Intervention
There were no statistically significant differences between
the pre-intervention baseline trials prior to the passive head
movement intervention. There were no significant changes
observed in any of the experimental variables following
passive head movement (Figures 2, 3, 4 and Tables 3 and
4).
Spinal Manipulation Intervention
There were no statistically significant differences between
the pre-intervention baseline trials prior to the spinal
manipulation intervention. Active motor threshold (ATh)
showed no statistically significant changes following this
intervention (Table 4). Neither were there any changes to
the M or F wave parameters measured (M wave amplitude,
F wave amplitude and persistence)(Table 4) or MEP
amplitudes following the manipulation intervention (Figure
2 and Table 3). For the CSP data, however, a significant
effect of the factor “intervention” was observed [F(2,33) =
4.5, p = 0.018]. The CSP was significantly shorter following
the spinal manipulation intervention during the first post-
manipulation trial (trial 0-10 min) [F(1,12) = 12.380, p =
0.004] and the second post-manipulation trial (trial 10-20
min) [F(1,12) + 6.278, p + 0.028] (Figure 3 and Table 3).
By the third post-manipulation trial, the CSP was no longer
significantly decreased. Figure 4 shows the raw non-rectified
EMG traces from one representative subject showing the MEP
and CSP prior to and after the various interventions. Note
that this particular subject demonstrates the greatest CSP
shortening observed in this study of about 110ms following
the spinal manipulation intervention. Table 3 contains the
mean raw MEP amplitude (mV) and CSP (ms) data with
standard deviations for the pre-intervention mean, and the
three post-intervention data (trials 0-10 min, 10-20 min, and
20-30 min) for all three interventions.
DISCUSSION
The major finding of this study was that the TMS-induced
CSP measured in APB was significantly decreased for the
first 20 minutes following spinal manipulation. No such
changes were observed following either control condition,
i.e. following no intervention or following a passive head
movement.

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Table 3

MEAN RAW MEP AMPLITUDE AND CSP DATA PRE- AND POST-INTERVENTION
MEP amplitude (mV) ± SD CSP (ms) ± SD
Control PHM SM Control PHM SM
Pre-intervention mean 4.3 ± 1.3 4.9 ± 1.9 4.35 ± 1.3 185. ± 23.8 192.7 ± 22.2 194.2 ± 26.2

Post-intervention trials

Trial 0-10 min 4.5 ± 1.4 4.7 ± 1.7 4.6 ± 1.3 186.3 ± 22.0 192.4 ± 2.3 179.5 ± 24.8*

Trial 10-20 min 4.5 ± 1.7 4.8 ± 1.9 4.5 ± 1.4 189.2 ± 25.3 198.8 ± 25.9 171.8 ± 37.7*

Trial 20-30 min 4.6 ± 1.6 4.6 ± 1.8 4.3 ± 1.3 187.0 ± 24.2 199.0 ± 24.4 184.3 ± 35.5

* p < 0.05 compared with pre-intervention mean data

Table 4

F AND M WAVE AMPLITUDES, F PERSISTENCE AND ACTIVE THRESHOLD

PRE- AND POST-INTERVENTION
Control: no intervention Passive head movement Spinal manipulation
Pre Post Pre Post Pre SM
F wave amplitude/ M
0.028 ± 0.01 0.027 ± 0.01 0.028 ± 0.01 0.028 ± 0.01 0.031 ± 0.01 0.031 ± 0.01
response ratio ± SD
F wave persistence
36.2 ± 13.9 37.3 ± 17.2 37.1 ± 11.6 35.8 ± 12.0 35.0 ± 12.6 35.8 ± 12.0
(%) ± SD

M response (mV) ± SD 17.9 ± 5.3 18.2 ± 5.3 18.0 ± 5.3 18.1 ± 5.7 16.4 ± 4.9 16.5 ± 5.1

ATh (%MSO) ± SD 39.4 ± 6.2 39.3 ± 6.1 38.8 ± 6.4 38.9 ± 6.4 39.5 ± 6.3 39.5 ± 6.3

The Cortical Silent Period this conclusion. Furthermore, no changes in F responses

The reduced CSP following cervical spine manipulation
may reflect altered intracortical inhibition. Studies suggest
that the first part of the CSP (about 50ms) after transcranial
stimulation is produced mainly by spinal mechanisms such
as after-hyperpolarization and Renshaw recurrent inhibition
of the spinal motoneurons. 57,58 Reciprocal inhibitory
effects on the target muscle may also contribute, since the
magnetic stimulation often causes simultaneous activation of
antagonists. The rest of the CSP (after about 50 ms), however,
is produced mainly by cortical inhibition.57-62
The exact mechanisms of this cortical inhibition are,
however, more difficult to establish. Most evidence suggests
that this inhibition is presynaptic to the cortico-spinal neurons,
rather than due to a decreased excitability of these cortico-
spinal neurons (which would be reflected by a decreased
MEP).58,59,63 Some argue that it results from activation of
inhibitory neurons projecting onto the pyramidal cells of the
motor cortex,58 however it may also reflect a withdrawal of
excitatory input to these cells. In any case, the shortening
of the CSP observed following spinal manipulation most
likely reflects a transient reduction in intra-cortical inhibition,
lasting on average 20 minutes following the manipulations.
The fact that some individual subjects’ CSP shortened by
over 100ms (e.g. see Figure 4) post-manipulation supports
(amplitude and persistence) were observed in this study,
also suggesting that the CSP changes observed in this study
reflect mainly changes at the supra-spinal level. It should be
noted, however, that F wave parameters (such as persistence
and amplitude) reflect the antidromic excitability of only a
portion of the entire motoneuron pool. Segmental effects can
therefore not be ruled out completely.
Neuropharmacological modulation of the CSP in healthy
subjects64-68 has also shed some light on its mechanisms.
Lengthening of the CSP has been reported with administration
of ethanol, lorazepam, gabapentin, carbamazepine, tiagabin,
and baclofen.64-68 Ethanol’s acute effect in the CNS is a
potentiation of GABA-mediated currents.69 Carbamazepine
affects the CNS by blocking sodium channels, and therefore
slowing repetitive firing of action potentials. Interestingly,
lamotrigine, a drug with a very similar mode of action to
carbamazepine, does not produce the same effect on CSP.
Glabapentin’s main mode of action is not yet fully understood.
There is, however, evidence to suggest it enhances GABA
activity.70,71 There is also evidence to suggest it interferes with
the release of the excitatory neurotransmitter glutamate.72
Furthermore, there is evidence suggesting it also binds to a
subunit of the voltage-gated calcium channels, and through
this action suppresses allodynia in neuropathic pain models.73
Lorazepam increases the frequency of openings of GABA-
activated Cl-channels by binding at the benzodiazepine

Chiropractic Journal of Australia

112 Volume 37 Number 3 September 2007

receptor (which is an integral part of the GABA-A receptor).
It therefore enhances the inhibitory effect of GABA function
in the CNS. It is puzzling, however, that not all GABAergic
drugs produce a CSP lengthening. The more recent studies64,65
suggest that the inter-neuronal inhibition that the CSP reflects
is likely due to GABAB-mediated circuits.
Due to these neuropharmacological studies, it has been
suggested that the CSP is at least in part mediated through
GABAergic activity, thus the shortened CSP observed in our
study could reflect reduced activity of intracortical inhibitory
circuits caused by a down-regulation of GABAergic
transmission.
The Motor Evoked Potential and Spinal
Manipulation
No significant changes were observed in the TMS-induced
MEP following any of the interventions, indicating there were
no excitability changes in the pyramidal tract neurons. This
is not necessarily surprising, however, as TMS generates
activation of many motoneuron pools simultaneously,
including agonists and antagonists. Consequently the
response of a single motoneuronal pool probably results
from superposition of many excitatory and inhibitory inputs.
The descending corticospinal volley resulting from a single
magnetic stimulus also consists of multiple waves, due to both
direct and indirect activation of corticospinal neurons.74-76
Therefore the descending input impinging on a motoneuron
resulting from a single transcranial magnetic stimulus is
extremely complex.
Our findings differed from a previous study that showed
changes to the MEP following spinal manipulation.16 This
contradictory finding may, however, be explained due to the
fact that in the current study we averaged 16 MEPs prior to
statistical analysis, whereas Dishman et al.16 analysed single
MEPs in their study and found only the first few MEPs
following spinal manipulation to be increased/reduced.
Potential Benefits of Spinal Manipulation in
Chronic Neck Pain
Chronic neck pain is becoming increasingly prevalent in
society. As many of 67% of individuals will suffer from some
form of neck pain at some stage in their lives.77 Impairment of
deep cervical neck flexors and significant postural disturbances
during walking and standing have been demonstrated in
both insidious-onset and trauma-induced chronic neck pain
conditions.78-84 Altered sensitivity of proprioceptors within
the neck muscles has been suggested to be related to the
postural disturbances seen in these patients.80,84 There is also
evidence to suggest that muscle impairment occurs early
in the history of onset of neck pain85 and that this muscle
impairment does not automatically resolve even when neck
pain symptoms improve.85,86 Some authors have therefore
suggested that the deficits in proprioception and motor
control, rather than neck pain itself, may be the main factors
defining the clinical picture and chronicity of different chronic
neck pain conditions.84 These deficits in proprioception and
motor control may be partly due to spinal dysfunction causing
either inhibition or facilitation of neural input to the related
muscles as discussed in the introduction. A recent study has,
for example, demonstrated a pathophysiological link between
neck muscle fatigue and impaired postural control.87 They
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SENSORIMOTOR EFFECTS OF SMT
HAAVIK-TAYLOR • MURPHY
also demonstrated that physiotherapy treatment, including
passive and active mobilisation, could relieve the symptoms
of impaired neck muscle function by reducing fatigability.87
Furthermore, it has recently been demonstrated, utilising
somatosensory evoked potentials (SEPs), that cortical
processing changes occur for at least 20 minutes following
spinal manipulation of dysfunctional cervical vertebrae in
patients with chronic neck complaints.11 It is possible that
the shortened CSP observed for 20 minutes following spinal
manipulation of dysfunction cervical vertebrae observed in
the current study reflect the same cortical changes. In the
future, if spinal manipulation can be shown to systematically
and reliably alter neural processing and abnormal motor
control, it could play an important role in the rehabilitation
of these chronic neck pain patients.
Episodes of acute pain, such as following an injury,
may initially induce plastic changes in the sensorimotor
system.34 Pain alone, without deafferentation, has been
shown to induce increased SEP peak amplitudes88,89 and
increased somatosensory evoked magnetic fields.90 Research
has also shown that the cortical silent period is prolonged
with experimentally induced tonic cutaneous pain.43 The
silent period was prolonged in a muscle underlying the
experimentally induced cutaneous pain, was not present in
two other control muscles.43 Furthermore, it was only present
as long as the subject reported the cutaneous pain.43 On the
other hand, a study has shown that a group of patients with
chronic neuropathic pain, including unilateral hand pain, have
shorter cortical silent periods bilaterally in a hand muscle
compared with healthy age-matched control subjects.91 It
has also been shown that the erector spinae muscles, close
to the site of pain in chronic low back pain patients, have
normal cortical silent periods, but higher thresholds for the
CSP compared with healthy pain-free control subjects.92
These studies demonstrate that CSP abnormalities appear
to be present with painful conditions. The various studies,
however, have shown both prolonged43 and shortened91
CSPs with different types of painful conditions. The fact
that many of the neuropathic pain subjects in Lefaucheur
et al.’s study91 also had accompanying sensory and motor
deficits may account for the differing results.
Noxious stimuli applied to the digits have also been shown
to result in MEP amplitude reduction in muscles involved in
reaching and grasping, and MEP amplitude facilitation in
muscles involved in withdrawal, suggesting a pain-induced
reflexive effect that protects the hand from harm.93 Such plastic
changes can become a “chronically progressive, functional,
structural, and neurochemical/molecular make-over of
the entire core of the somatosensory (and motor) brain.”34
Phantom limb pain is an obvious example of a maladaptive
chronic pain condition.94 As sensorimotor disturbances are
known to persist beyond the acute episode of pain,85,86 and
thought to play a defining role in the clinical picture and
chronicity of different chronic neck pain conditions,84 then
the shortened CSP observed in the current study following
spinal manipulation may reflect a normalisation of such
injury/pain-induced central plastic changes, which may
reflect one mechanism for the improvement of functional
ability reported following spinal manipulation.
113
SENSORIMOTOR EFFECTS OF SMT
HAAVIK-TAYLOR • MURPHY
Implications for Investigation of Neural Plasticity
and Spinal Manipulation
The observations in the present study suggest that spinal
manipulation of dysfunctional joints may modify transmission
in neuronal circuitries not only at a spinal level as indicated
by previous research,8-10 but at a cortical level as recently
also demonstrated with SEPs.11 Further studies are needed to
elucidate the role and mechanisms of these cortical changes,
and their relationship to a patient’s clinical presentation.
ACKNOWLEDGMENTS
The lead author was initially supported with a fellowship
from the Foundation for Chiropractic Education and Research,
and later by a Bright Futures Top Achievers Doctoral
Scholarship awarded by the New Zealand government.
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