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Central motor reorganization after anastomosis of the musculocutaneous and intercostal nerves following cervical root avulsion.

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ORIGINAL ARTICLES
Central Motor Reorganization h e r
Anastomosis of the Musculocutaneous
and Intercostal Nerves Following
Cervical Root Avulsion
Yukio Mano, MD, PhD," Takuya Nakamuro, MD," Ryuji Tamura, MD," Tetsuya Takayanagi, MD, PhD,"
Kouichi Kawanishi, MD, PhD,? Susumu Tamai, MD, PhD,t and Richard F. Mayer, MDS
In 4 patients with a complete upper limb palsy due to traumatic cervical root avulsion, surgical anastomosis of
intercostal to musculocutaneous nerves was performed to restore function in the biceps brachii muscle. Four to 6
months after the operation, motor unit discharges were recorded from the biceps muscle on the operated side during
deep breathing and by cortical magnetic stimulation. The motor unit discharges became independent from respirations
gradually over 1 to 2 years. The latencies of the motor potentials evoked by cortical and thoracic root magnetic
stimulation decreased gradually over 2 to 3 years. Motor cortex mapping of the reinnervated biceps muscle showed
a gradual change over 4 to 33 months from the area of the intercostal muscles to that of the arm area, which was
more lateral on the motor cortex. These findings suggest that reorganization of the motor cortex to arm flexor muscles
occurs following peripheral nerve anastomosis.
Mano Y , Nakamuro T, Tamura R, Takayanagi T, Kawanishi K, Tamai S, Mayer RF. Central motor
reorganization after anastomosis of the musculocutaneous and intercostal nerves
following cervical root avulsion. Ann Neurol 1775;38:15-20
Plasticity within the human central motor system occurs and has been studied with transcranial magnetic
stimulation in patients with amputations 111, spinal
cord injuries 121, and ischemic nerve block C31. These
studies have identified a pattern of motor system reorganization that results in enlarged muscle representation areas and larger motor evoked potentials (MEPs)
for muscles immediately proximal to the lesion. Some
of these changes are apparent minutes after ischemic
nerve block 131, weeks after spinal cord injury C21, and
as early as 6 months after amputation 111.
These studies motivated us to study the cortical motor reorganization after anastomosis of intercostal
nerves to the musculocutaneous nerve in young patients with cervical root avulsions due to a traumatic
motorcycle injury.
Materials and Methods
Four male patients with a complete upper limb paralysis resulting from a motorcycle accident were studied. The mean
age of the patients at the onset of the injury was 18.5 years
(range, 16-21 yr). Involvement of the upper limb was unilat-
From the Departments of *Neurology and torthopedic Surgery,
SNara Medical University, Nara, Japan; and $Department of Neurology, University of Maryland School of Medicine, Baltimore, MD.
eral; 3 cases involved the right and 1 involved the left. One
to 2 months after onset, the patients were referred for evaluation of motor function due to the lack of any recovery. An
operation to anastomose the musculocutaneous nerve to the
ipsilateral 3rd and 4th and/or 5th intercostal nerves was
planned in an attempt to restore function in the biceps brachii
muscle.The interval between the motorcycle accident and the
operation was 1 month in 2 patients and 3 and 5 months
respectively in the other 2 patients.
Before the operation, neurological examinations, electromyography (EMG), and evoked potential studies by electrical
and magnetic stimulation were performed. All patients had
a complete paralysis of one upper limb without signs of recovery. Needle EMG showed no voluntary motor unit potentials in the supraspinatus, infraspinatus, deltoid, biceps
brachii, triceps brachii, forearm, and small hand muscles. Denervation potentials were present in all of the above muscles.
No motor or sensory nerve potentials could be evoked in
the affected limbs by electrical stimulation of the axillary,
radial, median, ulnar, and musculocutaneous nerves. No motor responses were evoked in the affected hand or arm muscles by transcranial or root magnetic stimulation.Myelograms
demonstrated avulsion of the 5th and 6th cervical roots in all
4 patients. The neurological examination and EMG indicated
Received Oct 5 , 1994, and in revised form Feb 1 , 1995. Accepted
for publication Feb 2, 1995.
~ ,
of Neurology,
Address correspondence D~ M ~ Department
Nara Medical University, 840 Shijo-cho, Kashihara, Nara 634,
Japan.
Copyright 0 1995 by the American Neurological Association
15
extensive injury of the brachial plexus as well as the C5-6
roots. This was supported by the low content of choline acetyltransferase (ChAT) activity, that was measured using established techniques, in proximal nerve segments of the brachial
plexus exposed during surgery 141.
The surgical technique used to anastomose the musculocutaneous nerve to the intercostal nerves was similar to the
techniques described in the literature 15, 61. During the surgery, the brachial plexus, musculocutaneous, and 3rd through
5th intercostal nerves were explored in the affected limb. To
determine that the intercostal nerves used for the anastomosis contained an adequate number of motor fibers, the ChAT
content was measured in the sectioned intercostal nerves at
the time of surgery [4, 71. If the ChAT content was very low
in the 3rd and 4th intercostal nerves, the 5th intercostal nerve
was tested and used also in the nerve anastomosis. The musculocutaneous nerve was transectioned completely 2 to 3 cm
proximal to the motor point of the biceps brachii muscle.
This depended on the available length of the intercostal
nerves to perform an end-to-end anastomosis berween the
musculocutaneous and the intercostal nerves.
though the most excitable area was on the baseline in most
patients, 1 patient showed that the most excitable area was
slightly anterior to the base line. The cortical representation
of the biceps muscle on the scalp was expressed on the baseline, even though the center of the map was slightly anterior
to the line, which was moved and projected posteriorly in
parallel with the line in the coronal axis. The maximum amplitude of the MEP was measured in each trial and the sites
where the amplitude was 50% greater than the maximum
MEP amplitude were plotted as the excitable area. These
studies were repeated two or three times to confirm the localization of the excitable area.
Respirations were recorded by using a respiratory sensor,
which was attached to the nose and recorded the change in
temperature. Another respiratory sensor was attached
around the upper thorax and recorded the change in length.
The angle of the elbow was recorded using an electric
goniometer. Surface EMGs of the biceps and intercostal muscles were recorded using the same disc electrodes and placement as described above for the MEP recordings. Respirations and the angle of the elbow were recorded with a
polygraph simultaneously with the EMGs during voluntary
movements and various respirations.
Magnetic Stimulation Studies
For magnetic stimulation, the pulsed magnetic discharge system consisted of a high-voltage capacitor bank and coil that
discharged at a maximum of 900 V, a maximum of 8,000 A,
and 1,687 pF in condenser capacitance 18-10]. A round
magnetic coil was used to measure the latency of the evoked
potentials and a twin coil was used for cortical mapping. The
magnetic twin coil had two circular sides, each 4.5 cm in
diameter. The intersection of the sides (center) was approximately 1.5 cm long and 1 cm wide, and the current in the
center initially flowed towards the handle. The magnetic coil
was positioned on the scalp with the handle along the sagittal
axis and its center flat on the target scalp position. Thus, the
coil center was in contact with the scalp and closer to the
target neural tissues than the sides.
Magnetic stimuli were delivered to the C6 and T 4 or T5
roots just lateral to the C 6 and T4 or T 5 vertebrae to produce
MEPs in the biceps brachii or intercostal muscles.
Motor evoked potentials were recorded at rest with silver
disc surface electrodes, 5 mm in diameter, with the active
electrode overlying the belly of the biceps brachii muscle
(biceps muscle) and the indifferent over the tendon. To record from the intercostal muscles the active electrode was
placed in the 4th to 5th intercostal space at the midaxillary
line and the reference electrode was placed 3 cm anteriorly.
Signals were amplified with a Nihon Koden Neuropak 8
using a band pass of 100 to 2,000 Hz and recorded over
50 msec. The amplitude of the MEPs evoked by magnetic
stimulation was measured peak to peak.
Training after Operation
After the nerve anastomosis, passive range-of-motion training
was done in the injured upper extremity several times every
day. Visual and auditory biofeedback training, using EMG
recordings from the operated biceps muscle, was started
about 4 months after the operation. The training was started
when the EMG discharges from the biceps muscle appeared
on the oscilloscope during deep breathing.
Results
Magnetic Cervical Root Stimulation
The MEPs were evoked easily by magnetic cervical
root stimulation from t h e biceps muscle o n t h e noninjured limb and appeared normal. No MEPs could be
evoked from the biceps muscle on the injured side
either after t h e injury or following the operation.
Motor Representation of the Biceps Muscle
Magnetic Thoracic Root Stimulation
F o u r to 6 months after the nerve anastomosis, MEPs
could be evoked from t h e biceps muscle o n the operated side by magnetic thoracic root stimulation (Fig 1).
The MEP latencies were initially prolonged b u t decreased gradually over 2 to 3 years (Table). The MEP
amplitudes were initially small and gradually increased
with time. MEPs were evoked easily from intercostal
muscles on the nonoperated side at all times before
and after the operation (see Fig 1).
To map the cortical representation of the biceps muscle, the
scalp overlying the sensorimotor cortical area was stimulated
at intervals (eight sites) of 0.5 cm along the coronal axis and
1 to 2 cm (six cites) along the sagittal axis [I I}. The mapping
area was as follows: Cz was the center, and the baseline of
the coronal axis was the line between Cz and the ear. Al-
Transcranial Magnetic Stimulation
F o u r to 6 months after t h e operation, MEPs w e r e
evoked also from the biceps muscle by transcranial
magnetic stimulation at rest (see Table). T h e MEP la-
16 Annals of Neurology
Vol 38 NO 1 July 1995
- ti””
5 rns
Lv
Fig I. Motor evoked potentials recorded from the biceps brachii
mude on the operated side (A),and the intercostal muscles on
the nonoperated side (B), evoked by thoracic root magnetic stimulation 14 months after the nerve anastomosis in Patient 4.
tencies gradually decreased over 2 to 3 years and the
amplitudes increased. However, most of the decrease
in the MEP latency was due to the reduction in the
peripheral nerve conduction time. Central motor conduction time (calculated as follows: MEP latency by
transcranial stimulation minus MEP latency by thoracic
root stimulation) was constant or slightly decreased 2
to 3 years after the operation.
Relationship Between Respirations
and the Biceps Muscle
Before the operation and until 4 months after the operation, no discharges were recorded from the biceps
muscle during deep breathing. Four to 6 months after
the operation, discharges from the biceps muscle were
observed on the operated side only with deep respirations and there was no movement of the elbow. One to
3 months later discharges were observed with regular
respirations (Fig 2). At this stage, the patients could
not activate muscle discharges in the biceps muscle
without respirations, and they received intensive biofeedback training.
About 1 to 2 years after the anastomosis, the patients started to move their affected elbow voluntarily
independent of respirations, but there were some associated intercostal muscle discharges (Fig 3). Patients
were able to maintain the biceps muscle discharges
during weight bearing without disturbing respirations
and they could lift approximately 3 to 10 kg. They
could also separate flexion movements of the elbow
from respirations.
Mapping of the Cortical Motor Representation
of the Biceps Muscle
The most excitable area on the cortex where the MEP
from the nonoperated biceps muscle could be evoked
was about 4 to 5 cm from Cz on the Cz and ear line
(Fig 4). The area where the MEP from the nonoperated
intercostal muscles was most easily evoked was about
2 cm from Cz.
When the biceps muscle MEP could be evoked on
the operated side by stimulation of the cortex, the most
excitable area was about 2 to 3 cm from Cz on the line
between Cz and the ear. The area was slightly larger
than the cortical area of the intercostal muscles. The
MEP amplitudes were small, the latencies were prolonged (see Table), and the threshold of magnetic activation was increased.
The cortical areas became gradually broader from 2
to 6 cm on the line between Cz and ear 16 to 24
months after surgery. The MEP amplitudes remained
small, although the latencies gradually became shorter
(see Table).
When the contractions of the biceps muscle became
independent of respirations, the most excitable cortical
area of the biceps MEP moved laterally and was concentrated 4 to 7 cm laterally on the line between CZ
and the ear. This area was more lateral and wider than
the biceps muscle area on the nonoperated side. In 2
of the 4 patients, the most excitable cortical area of the
biceps MEP was restricted to the area about 6 cm lat-
Motor Evoked Potential Latency (meci and Amplitude (mV) Recorded from the Biceps Brachii Muscle after Anastomosij
of the Musculocutaneous and lntercostal Nerves
4-14 Months after
Operation ( 4 )
Site of Magnetic
Stimulation
16-24 Months
after Operation ( 4 )
~~
Thoracic root
Latency
Amplitude
Transcranial
Latency
Amplitude
Data are mean values
?
9.9
15.0 -+ 2.5
1.47 -+ 0.48
2.91
?
2
24.6 -+ 2.0
0.32 ? 0.20
18.4
0.47
26-33 Months
after Operation ( 3 )
~~
~
~~
2.3
1.93
8.8
3.37
2
3.5
?
0.16
17.1 ? 0.5
0.54 t 0.24
?
?
0.4
1.85
SD. Numerals in parentheses are number of cases.
Mano et al: Motor Reorganization after Root Avulsion
17
It biceps muscle
/
/
nose respiration
regular respiration
\'
u
/
deep inspiration
Fig 2. Motor unit discharges from the biceps brarhii muscle on
the operated right side during regular and deep respirations 14
months after the nerve anastomosis in Patient 4.
voluntary elbow flexion
voluntary elbow flexion
-It
biceps
musc I e
intercostal
muscle
--
r
goni
elho
Fig 3. Voluntary elbvuj flexion with motor unit discharges from
the right biceps and intercostal muscles not associated with respiration 21 m0nth.c after the nerve anastomosis in Patient 1 .
eral from Cz. The mean MEP latency, 26 to 33 months
after surgery, continued to shorten and the mean amplitude remained small.
Discussion
Paralysis of an upper extremity due to traumatic cervical root avulsion is usually permanent, since there is
minimal root regeneration 112, 131. Many operative
procedures, including nerve grafts, have been tried in
the past with limited success 112, 141. Anastomosis of
18 Annals of Neurology Vol 38 No 1 July 1995
the intercostal nerves with the musculocutaneous
nerve has been performed and reported to be one of
the most successful methods in restoring function in
the biceps brachii muscle 15, 6, 13, 151.
In this study of 4 patients, who had a complete upper
limb palsy due to traumatic cervical root avulsion and
brachial plexus injury, surgical anastomosis of the intercostal and musculocutaneous nerves was performed
and restored a moderate amount of function in the
biceps brachii muscle.
The age of the patient at the time of the neural
damage is important in regard to the ability of the nervous system to regenerate or alter its function 1161.
The neurologic dysfunction that occurs with a lesion
MEP is thought to be the cortical area of that muscle.
operated side
(12
m.)
patient 2
E
m
(4
m
m.)
(26 n . )
'
6
j
.I
J
lateral from C r i c m l
i
I
months a f t e r
2
i
+
l
2
3
middle of c o r t e x
cz
the
4
5
6
7
from c z icm)
n e r v e anastornosis
Fig 4 . Functional cortical mapping of motor evoked potentials
from the biceps brachii muscle on the nonoperated and operated
sides by transcranial magnetic stimulation from the center (Cz)
to the ear in the 4 patients 4 to 33 months after nerve anastomosis.
of one cerebral hemisphere before the age of 3 years
is known to be restored by the contralateral hemisphere 1171. However, it has been reported that cerebral hemisphere function in adults remains adaptable
and can change following peripheral events such as an
amputation, nerve block, or spinal cord injury 11-31.
In the peripheral nerve anastomosis technique used in
this study, successful cases usually occurred in patients
less than 25 years of age at the time of the injury and
the unsuccessful cases were in patients over 40 years
of age. In this study the mean age of the patients was
18.5 years and they likely had potential for neural reorganization within the central and peripheral nervous
systems. In the analysis of our unsuccessful cases, patients were older than 40 years, they were unable to
have biofeedback training, and they had medical or
psychiatric problems such as alcoholism, diabetes mellitus, or other medical diseases.
The prolonged latency of the MEPs recorded from
the reinnervated biceps muscle gradually became
shorter over 20 to 30 months due to peripheral nerve
regeneration, and there was little change in central motor conduction time. With transcranial magnetic stimulation, the most excitable area that produces the largest
After the intercostal nerves were anastomosed to the
musculocutaneous nerve innervating the biceps brachii
muscle, the cortical motor area of the biceps was located in the area of the intercostal muscles. After time
for nerve regeneration and reinnervation of the muscle, biofeedback training, and voluntary control of
flexion of the elbow, the excitable area of the biceps
motor cortex moved laterally towards the cortical area
of the arm segment of the upper limb. This suggests
that there was reorganization of the cortical motor area
to the arm flexor muscles. Initially the excitable area
was enlarged as reported in previous studies of cortical
motor reorganization 111. The excitable area of the
motor cortex to the biceps muscles became locahzed
at the time when the ability to flex the elbow and control elbow flexion without respirations occurred.
Atrophy of the motor cortex to the upper limb may
occur due to disuse and this could result in some movement of the cortical center of the intercostal muscles
laterally. However, it is unlikely that cortical atrophy
alone explains the marked lateral movement of the cortical intercostal area by about 4 cm. Brain magnetic
resonance imaging studies showed that there was no
remarkable difference between the operated and nonoperated sides of the motor cortex 2 to 3 years after
the operation in these patients. Although these changes
in the cortical motor reorganization may be due to
unmasking of preexisting connections in the motor
cortex, it is more likely that new neural connections
have been established.
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