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Ontogeny of ipsilateral corticospinal projections A developmental study with transcranial magnetic stimulation.

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Ontogeny of Ipsilateral Corticospinal
Projections: A Developmental Studv with
Transcranial Magnetic 3 timulation
K. Muller, MD, F. Kass-Iliyya, MD, a i d M. Reitz, MD
Transcranial magnetic stimulation (TMS) has been used to describe thi: maturation of the corticospinal tract in children.
Ipsilateral corticospinal connections have been demonstrated with TMS in patients with congenital mirror movements, in
patients after hemispherectomy, and in children with hemiplegic cereibral palsy. The goal of the study was to find out
whether corticospinal ipsilateral projections in children can be demonstrated during the first decade of life as part of
normal ontogeny. For this purpose, we examined 50 normal children (age range, 3-11 years) with focal TMS over the
left and right hemispheres to target muscles in proximal and distal pat$ of the upper extremity (first dorsal interosseus,
biceps brachii, and brachioradialis). To lower the stimulation threshold, we stimulated under voluntary preinnervation.
In two-thirds of the children we elicited ipsilateral motor evoked potentials (MEPs). This occurred more often in proximal than in distal muscles. The latency of the ipsilateral MEPs was about 12 to 14 msec longer than the usual contralateral response. From the age of 10, and in adults, ipsilateral MEPs could not be detected. Also considering lesion
data from adult patients, the most likely explanation for the disappearance of ipsilateral corticospinal connections after
the age of 10 years is an increasing transcallosal inhibitory influence during development. The presence of ipsilateral
corticospinal connections appears to be a normal state in ontogeny.
Miiller K, Kass-Iliyya F, Reitz M. Ontogeny of ipsilateral corticospinal projections: a developmental study
with transcranial magnetic stimulation. Ann Neurol 1997;42:705-711
Transcranial magnetic stimulation (TMS) of the motor
cortex results in contralateral motor evoked potentials
(MEPs) in the upper and lower extremities in both
adults and in children [l-31. Few studies have addressed
the occurrence of ipsilateral MEPs after cortical stimulation. Although they can be found in distal muscles [4]
of the upper extremities, they are found more regularly
in proximal and trunk muscles of adults [5-71.
Ipsilateral corticospinal connections have been demonstrated with TMS in patients with congenital mirror
movements and Kallman’s syndrome [8-121 and have
also been described in patients with cerebral palsy [13,
141 and after hemispherectomy [15-171. In patients after stroke, ipsilateral corticospinal projections appear to
become “unmasked” [ 18-201. After very early brain
damage, ipsilateral MEPs have been demonstrated with
the same latency as the contralateral responses [I3].
Clinically, these findings correspond to the presence of
mirror movements. The role of these ipsilateral projections in functional recovery aker brain damage remains
The aim of this study was to look at the ontogeny of
ipsilateral corticospinal connections in normal children.
In normal children during development, so-called associated movements, or synkinetic movements, can be
observed until the age of about 10 years [21-231. The
presence of such synkinetic movements may be related
to the existence of ipsilateral corticospinal pathways,
eg, due to uncrossed axon collaterals or transcallosal
connections. These may be gradually inhibited, or even
disappear during ontogeny. Knowledge about the ontogenetic development of ipsilateral corticospinal connections may give clues to the understanding of such
pathways in restoration of function after acquired lesions in adults. TMS has provided information about
maturational changes in the corticospinal tract. Central
conduction times (CCTs) and stimulation thresholds
reach adult values only at around the age of 10 years
[3].This trend parallels the development of the fastest
alternating voluntary movements [24].
From Department of Pediatrics, Medizinische Einrichtungen der
Heinrich-Heine-Universitat, Dusseldorf, Germany.
Address correspondence to Dr Muller, Department of Pediatrics,
Med Einrichtungen der Heinrich-Heine-Universitat, MoorenstraBe
5, D-40225 Dusseldorf, Germany.
Received Oct 15, 1996, and in revised form Apr 21, 1997. Accepted for publication Jul 6 , 1997.
Subjects and Methods
We examined 50 healthy children. All had a normal gestational and developmental record and a normal neurological
examination. The parents gave informed consent to the
Copyright 0 1997 by the American Neurological Association
study, which was approved by the Ethics Committee of the
Heinrich-Heine-University of Dusseldorf. The children were
aged between 3 and 11 years (27 boys and 23 girls). The
adult control group consisted of 8 females and 3 males aged
between 24 and 36 years.
TMS was performed using a Cadwell MES10 magnetic stimulator with a maximal output of 2 T. MEPs were recorded
with bipolar surface Ag
AgClF electrodes attached bilaterally over the first dorsal interosseus (FDI), the brachioradialis (BR), and the biceps brachii (BB). For focal stimulation, a figure-eight butterfly coil was used. For better
orientation on the scalp surface, the children wore a bathing
cap on which the reference points of the international 10/20
electroencephalography (EEG) system were marked. Stimulation was performed over the hand and arm area of the left
or right motor cortex. It was known from preliminary pilot
data that in most children the optimal stimulation area, defined as the site of the largest reproducible MEP in any of
the three muscles, was about 4 cm left or right and 1 cm
posterior to Cz (central midline for placement of electrodes)
according to the 10/20 system. Therefore, the search for the
optimal stimulation site started here. In addition, locations 1
cm anterior, posterior, and 1 cm lateral to the left and right
were also examined, and usable MEPs from these positions
were stored and analy.Led when the number of obtainable
responses was higher. To limit the number of stimuli in each
child to a minimum, no systematic approach was made to
obtain the precise topographic maps around these positions.
Therefore, inferences about subtle topographic differences
between contralateral and ipsilateral stirnulacion sites (eg, see
Wassermann and colleagues [4]) cannot be made. For the
same reason differential thresholds were not obtained.
In most children, stimulation was performed at 90%
(range, 80-100%) of the maximum of the stimulator output. Stimulator intensity was increased in steps of 10% when
responses were not present in all three recording sites for
contralateral stimulation. A minimum of 20 seconds was
kept between successive stimuli.
As stimulation thresholds are significantly higher in children than in adults [2, 31, we used a stimulation protocol
with preinnervation of the target muscles to bring stimulation thresholds to a minimum. Preinnervation was reached
by making the children lift a weight of either 500 g in
younger or 1 kg in older children in both hands. Stimulation
was performed at the very moment the weight started to be
lifted, ie, during the early phase of the flexion movement of
the elbows. Movement initiation was self-paced without preceding stimuli. Magnetic stimulation was initiated by the experimenter, when the children’s movements started. Movements were not recorded further.
Electromyelographic data were recorded in six channels simultaneously (upper cutoff, 1.5 kHz;lower cutoff, 10 Hz),
using Toennies Model 22471 amplifiers. Data were digitized
for epochs, starting 10 msec before and ending 200 msec
after stimulus onset.
Between 10 and 20 stimuli were applied for left and right
hemispheric stimulation at optimal sites. MEPs were superimposed on a computer display. The number of superim-
706 Annals of Neurology
Vol 42
5 November 1997
posed records varied between three and eight. Latencies and
amplitudes were determined from the superimposed MEPs
by an interactive cursor. Latency was defined as the point in
time where most records showed a rising curve leading directly to the maximum of the response without crossing the
baseline again (see Fig 1). Amplitude was defined as the
peak-to-peak deflection of the largest MEP.
Cervical stimulation was performed at the C-7 level.
CCTs were calculated by taking the difference between the
latency from the motor cortex to the distal muscles minus
the latency from the cervical root to the upper extremity
Age trends in the frequency of obtainable responses were
analyzed with exact
tests on data lumped into four age
groups (3-5, 6-7, 8-9, and 10-11 years) for all three muscles on both sides.
Possible differences between age groups and asymmetries
between right and left hemisphere stimulation were assessed
by analysis of variance (ANOVA) over age groups (as above)
for CCT and latency differences between ipsilateral and contralateral responses.
Figure 1A shows MEPs after left and right hemispheric
stimulation of FDI, BR, and BB muscles on either side
in a 7-year-old child. Ipsilateral responses are visible at
a somewhat longer latency compared with the contralateral responses in all three muscle groups. Figure
1B shows corresponding recordings in an adult. Here,
ipsilateral to the stimulated hemisphere no excitatory
responses can be detected; only a short silent period in
the left FDI after stimulation of the left hemisphere is
Contralateral MEPs to the FDI, the BR, and the BB
muscle could be evoked in all children. Under maximal
preinnervation, the calculated CCTs showed no significant maturational trend and were similar to the CCTs
of the adults, as revealed by insignificant group effects
in the ANOVA. The CCTs in the children were 5.9 If;0.8 msec to the FDI, 5.4 It_ 1 msec to the BR, and
5.0 t 0.8 msec to the BB muscle. The CCTs in the
adults were 5.8 -+ 0.9 msec to the FDI, 5.9 2 1 msec
to the BR, and 5.6 t 1 msec to the BB muscle.
Ipsilateral Responses
In 32 of 50 children, ipsilateral responses in at least
one muscle of the upper extremities could be elicited
after focal TMS of the motor cortex. Ipsilateral responses were found more frequently in the more proximal muscle groups (BR and BB) than in the FDI. Ipsilateral responses could not be obtained above 10 years
of age. The oldest child with ipsilateral responses was 9
years 9 months old.
Figure 2 shows a diagram of the latencies of the ipsilateral and contralateral MEPs of the FDI, the BR,
Stimulation of the left hemisphere
Stimulation of the right hemisphere
113 ms
213 mr
0.75 mV
0 7 sv.
Stimulation of the left hemisphere
Stimulation of the right hemisphere
125 m
Fig I . (A) Original motor evoked responses after lefi and right hemispheric stimulation in a 7-year-old child. Ipsilateral responses
occur at a consistently longer latency than contralateral responses. The amplitudes of the ipsilateral responses show considerable variation. (B) Motor evoked potentials after left and right hemispheric stimulation of the motor cortex in an adult; no ipsilateral responses were elicited. FDI = j r s t dorsal interosseus; BR = brachioradialis; BB = biceps brachii; R = right; L = left.
Muller et al: Ontogeny of Ipsilateral Corticospinal Projections
Stimulus: left motor cortex
Stimulus: right motor cortex
M. interosseus dorsalis I
2 '9
M. biceps brachii
M . biceps brachii
I 2 1 3
. # -
1 O I t 1 ? 1 3
1 '4
l o l l
M brachioradialis
M. brachioradialis
.,. .a':.:( - *
and the BB muscles. Ipsilateral responses always
showed longer latencies than contralateral responses.
There was, however, no significant age trend for this
difference, as determined by the ANOVA. There was
also no asymmetry between right and left cortical stimulation regarding frequency, latency, or amplitude of
the ipsilateral responses.
The Table summarizes the mean and differences and
SDs of the latencies of contralateral and ipsilateral
MEPs. The latency difference remains fairly constant at
around 12 to 14 msec. Amplitudes were higher in ipsilateral muscles in 2 cases in the FDI, in 12 cases in
the BR, and in 13 cases in the BB. This was, however,
not a consistent finding. The mean amplitudes of contralateral and ipsilateral MEPs are summarized in the
Table. In general, ipsilateral responses reached about
50% of the contralateral amplitudes.
Figure 3 sunimarizes the proportions of ipsilateral responses across age groups for the three different muscles. It is obvious that the percentage of ipsilateral responses declines until the age of 10 years, with the
presence of these responses being more pronounced in
the BB and the BR muscles. This is reflected in insig-
Vol 42
No 5
November 1997
I h
Fig 2. The diagram shows the dictribution of latencies f i r ipsilateral ( + )
and contralateral (@) responses a j e r
left and r i d t hemisoheric stimulation
$r all thr:e target k w c l e s first dorsal interosseus [FDIJ, brachioradialis
[BR], and biceps brachii [BB]) by
ape. The latencv di&rence remains
fiirly constant over age. Furthermore,
it is evident that contralateral responses are more commonly found in
vroximal comoared with distal muscles. * = addla (mean t SO).
708 Annals of Neurology
x2 tests for the FDI bilaterally (FDI left: x2 =
3 , p = 0.588; FDI right: x2 = 3.54, df=
3, p = 0.31) but highly significant x2 statistics for
both BR and BB bilaterally (BR left: x2 = 17.52, df=
3, p < 0.001; BR right: x2 = 26.58, df = 3, p <
0.001; BB left: x2 = 21.94, df = 3, p < 0.001; BB
right: x2 = 22.24, df = 3, p < 0.001).
The main finding of the study was that during development excitatory ipsilateral responses can be obtained
in upper extremity muscles after TMS of the motor
cortex in about two-thirds of children younger than 10
years. By the age of 10 years these responses disappear.
The calculated central conduction times showed no
significant maturation after the age of 3 to 5 years,
which has been shown before under a similar stimulation protocol [2]. This is in contrast to the maturation
of the CCT in relaxed muscles [3], where adult values
are not reached before the end of the first decade.
It is unlikely that the presence of ipsilateral responses
is the result of a passive stimulus spread from one to
the other hemisphere, eg, by spurious magnetic fields
Table. Latency Dzfference and Amplitudes of Ipsilateral and Contralateral MEPs
Latency Difference
Left Hemisphere
Stimulus Left Hemisphere (msec)
Right Hemisphere (msec)
14.0 +- 2.1
13.0 i 3.9
n = 9
0.9 t 0.18
n = 8
12.0 2 1.6
n = 30
11.9 t 2.9
12.0 +- 1.8
n = 27
12.7 5 1.3
n = 26
n = 32
Ipsi (mV)
Right Hemisphere
Contra (mV)
Ipsi (mV)
Contra (mV)
2.05 2 1.05
0.94 1 0 . 3 6
2.27 +- 1.05
0.98 t 0.38
1.76 +- 0.8
0.88 -C 0.43
1.69 t 0.89
0.97 t 0.39
1.95 2 0.99
0.93 t 0.48
1.88 i 0.99
The latency differences between ipsilateral and contralateral motor evoked potentials (MEPs) after left and right hemispheric stimulation are
rather consrant at around 12 to 14 msec. The amplitudes of the ipsilateral responses show considerable variation. On average, the ipsilateral
(Ipsi) responses reach about 50% of the amplitudes of the contralateral (Contra) MEPs.
first dorsal interosseus; BR = brachioradialis; BB = biceps brachii.
Frequency of ipsilateral responses
6-7 years
10-11 years
age group
Fig 3. Frequency of ipsilateral motor evoked potentials (given
as percentage of cases examined) in the target muscles of the
upper extremity lurnpedfor the left and right side. It is evident that the frequency of ipsilateral responses in proximal
muscles gradually decreases with age. (psilateral responses are
not seen ajier the age of 9 years.
as eddy currents; the significant latency difference between ipsilateral and contralateral responses makes this
very unlikely. For methodological reasons, our data do
not allow statements about relative changes in topographic localization of stimulation sites for ipsilateral
compared with contralateral responses.
That in more distal muscles fewer ipsilateral connections were obtainable corresponds well to the anatomical distribution of corticospinal fibers to the upper extremity and to studies with intracortical electrical
stimulation [25].
Multiple different routes may, however, contribute
to the presence of ipsilateral corticospinal projections.
These are illustrated schematically in Figure 4A. Ipsilateral responses can be brought about by axon collaterals from motor cortical neurons that either take a direct route to the ipsilateral motor neuron pools or
recross after the original pyramidal crossing again on
Fig 4. (A) Possible excitatory pathways for ipsilateral motor
evoked potentials (MEPs): (1) transcallosal collateral pathways,
(2) ipsilateral axon collaterals or recrossing axon collaterah at
spinal levels, or (3) a different subset of ipsilateral projecting
motor cortical neurons with lower conduction velociiy. (B)
Example of a patient with a cortical lesion of one hemisphere.
This may lead to an unmasking of ipsilateralprojections (3)
by interrupting a transcallosal inhibitovy infltence (4).
(c)This scheme represents the most like4 explanation for ipsilateral MEPs in children. During ontogeny there is an increase in transcallosal inhibitory influences (4) on ipsilateral
connections (3). In the contralateral hemisphere, additional
intrahemispheric inhibit0 y influences may also become more
active (5).
spinal levels. Such axon collaterals are very likely to be
present in normal people with congenital and remaining mirror movements and have been described in
Kallman’s syndrome [8-121. They also occur in children with congenital hemiparesis [ 131.
A second possibility to explain ipsilateral responses is
the presence of a different population of corticospinal
neurons with primarily ipsilateral projections. These
appear to have a higher density of projections to prox-
Muller et al: Ontogeny of Ipsilaceral Corticospinal Projections
imal as opposed to distal muscles. The fairly constant
latency difference between ipsilateral and contralateral
responses of about 12 to 14 msec obtained in our
study could be explained by somewhat slower conduction properties of this subset of corticospinal neurons,
eg, the corticoreticulospinal pathway [26].
Another excitatory pathway could consist of a transcallosal collateral innervation subserved by an axon collateral innervating homologous corticospinal neurons
in the contralateral hemisphere. The observed 12-msec
latency difference corresponds well to estimates of
transcallosal conduction time derived from studies
looking at interhemispheric inhibition in human motor
cortex [27, 281. In this case, however, one would expect that with increasing myelination of the corpus callosum u p to the age of 10 years, these responses should
become more pronounced. In contrast, our data show
that these responses become completely abolished or at
least masked after the age of 10 years. The key question hence remains as to by which mechanism, in the
course of ontogeny, ipsilateral responses become more
and more reduced in strength.
A possible clue to the underlying mechanism can be
derived from findings in adult patients after unilateral
cerebrovascular motor cortical lesions [ 10, 191. In these
patients, ipsilateral responses can be evoked from the
intact hemisphere at a latency of about 5 to 6 msec
longer than for the contralateral responses from this
It is likely that these responses become unmasked
due to a lack of tonic transcallosal inhibitory influence
after a hemispheric lesion (see Fig 4B). A similar mechanism can also be supposed to be present during ontogeny in the sense that these tonic transcallosal inhibitory influences between the motor cortices become
more and more active and are completely developed by
the age of about 10 years, corresponding to the time
when callosal myelination is completed [29]. This
mechanism is illustrated schematically in Figure 4C. In
addition to the increasing tonic transcallosal inhibition
during ontogeny, intrahemispheric inhibitory rnechanisms also exert an increasing inhibitory influence on
the subpopulation with ipsilateral connections, and
these may become more active gradually during the
first decade. This transcallosal tonic inhibition hypothesis does not explain directly the latency difference between contralateral and ipsilateral responses. Therefore,
in addition, it must be postulated that the ipsilaterally
projecting corticospinal neurons form a subpopulation
with somewhat slower conduction properties and probably elevated stimulation thresholds.
The “inhibition hypothesis” is further supported by
a clinical study in patients with congenital hemiparesis
[30].In this study [30],the author states that “physiological mirroring in the nonparetic hand disappears
gradually in contrast to persisting mirror movements in
Annals of Neurology
Vol 42
No 5
November 1997
the impaired hand. The most likely explanation for this
phenomenon is a one-way transcallosal inhibitory system on the tonically active uncrossed ipsilaterally projecting pyramidal tract. Another argument for a transcallosally mediated inhibition is that in patients after
cortical stroke there is a latency difference between the
contralateral and ipsilateral MEPs [ 191, whereas in patients with capsular lesions or subcortical lesions the
ipsilateral and contralateral MEPs may have the same
latencies [ 181. Nevertheless, it is very likely that several
reorganization mechanisms, in addition to a lack of
transcallosal inhibition after cortical lesions, lead to restoration of motor function [13]. Animal studies provide evidence for normal transient ipsilateral corticospinal connections [31, 321. In animals after an
experimental lesion of the pyramidal tract, axon collaterals at cortical and spinal levels and reorganization of
the motor cortex have been described [33-361. Although they are probably involved, the definite role of
ipsilateral corticospinal connections present during
early ontogeny, for restoration of motor function after
stroke or other cerebral lesions, still remains unclear.
This study was supported by the Deutsche Forschungsgemeinscha~
(DFG 90313-1).
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