See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/11640428

Coordination of coupled hand and foot movements during childhood

Article  in  Experimental Brain Research · December 2001

DOI: 10.1007/s00221-001-0898-3 · Source: PubMed

CITATIONS READS

26 218

3 authors:

Paolo Cavallari Gabriella Cerri

University of Milan University of Milan
117 PUBLICATIONS   3,159 CITATIONS    60 PUBLICATIONS   2,082 CITATIONS   

SEE PROFILE SEE PROFILE

Fausto Giacomo Baldissera

University of Milan
122 PUBLICATIONS   3,761 CITATIONS   

SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Brain networks in cognitive control View project

Bionic repair of facial palsy View project

All content following this page was uploaded by Paolo Cavallari on 31 May 2014.

The user has requested enhancement of the downloaded file.

  6SULQJHU

'HDU$XWKRU

3OHDVHILQGDWWDFKHGWKHILQDOSGIILOHRI\RXUFRQWULEXWLRQZKLFKFDQEHYLHZHGXVLQJWKH
$FUREDW5HDGHUYHUVLRQRUKLJKHU:HZRXOGNLQGO\OLNHWRGUDZ\RXUDWWHQWLRQWRWKH
IDFWWKDWFRS\ULJKWODZLVDOVRYDOLGIRUHOHFWURQLFSURGXFWV7KLVPHDQVHVSHFLDOO\WKDW

• <RXPD\QRWDOWHUWKHSGIILOHDVFKDQJHVWRWKHSXEOLVKHGFRQWULEXWLRQDUH
SURKLELWHGE\FRS\ULJKWODZ

• <RXPD\SULQWWKHILOHDQGGLVWULEXWHLWDPRQJVW\RXUFROOHDJXHVLQWKHVFLHQWLILF
FRPPXQLW\IRUVFLHQWLILFDQGRUSHUVRQDOXVH

• <RXPD\PDNHDQDUWLFOHSXEOLVKHGE\6SULQJHU9HUODJDYDLODEOHRQ\RXUSHUVRQDO
KRPHSDJHSURYLGHGWKHVRXUFHRIWKHSXEOLVKHGDUWLFOHLVFLWHGDQG6SULQJHU9HUODJLV
PHQWLRQHGDVFRS\ULJKWKROGHU<RXDUHUHTXHVWHGWRFUHDWHDOLQNWRWKHSXEOLVKHG
DUWLFOHLQ/,1.6SULQJHU
VLQWHUQHWVHUYLFH7KHOLQNPXVWEHDFFRPSDQLHGE\WKH
IROORZLQJWH[W7KHRULJLQDOSXEOLFDWLRQLVDYDLODEOHRQ/,1.KWWSOLQNVSULQJHUGH
3OHDVHXVHWKHDSSURSULDWH85/DQGRU'2,IRUWKHDUWLFOHLQ/,1.$UWLFOHV
GLVVHPLQDWHGYLD/,1.DUHLQGH[HGDEVWUDFWHGDQGUHIHUHQFHGE\PDQ\DEVWUDFWLQJDQG
LQIRUPDWLRQVHUYLFHVELEOLRJUDSKLFQHWZRUNVVXEVFULSWLRQDJHQFLHVOLEUDU\QHWZRUNV
DQGFRQVRUWLD

• <RXDUHQRWDOORZHGWRPDNHWKHSGIILOHDFFHVVLEOHWRWKHJHQHUDOSXEOLFHJ\RXU
LQVWLWXWH\RXUFRPSDQ\LVQRWDOORZHGWRSODFHWKLVILOHRQLWVKRPHSDJH

• 3OHDVHDGGUHVVDQ\TXHULHVWRWKHSURGXFWLRQHGLWRURIWKHMRXUQDOLQTXHVWLRQJLYLQJ
\RXUQDPHWKHMRXUQDOWLWOHYROXPHDQGILUVWSDJHQXPEHU

<RXUVVLQFHUHO\

6SULQJHU9HUODJ%HUOLQ+HLGHOEHUJ
Exp Brain Res (2001) 141:398–409
DOI 10.1007/s00221-001-0898-3
R E S E A R C H A RT I C L E
Paolo Cavallari · Gabriella Cerri · Fausto Baldissera
Coordination of coupled hand and foot movements during childhood
Received: 12 February 2001 / Accepted: 1 September 2001 / Published online: 17 October 2001
© Springer-Verlag 2001
Abstract To acquire further insight into the neural
mechanisms governing the association of voluntary os-
cillations of ipsilateral hand and foot we investigated
when and how coordination of such coupling develops in
children 7–10 years old. Sixty-six children were asked to
rhythmically oscillate their right hand and foot, paired
in-phase or anti-phase (i.e. rotating in the same or in the
opposite angular direction). Angular displacement was
monitored by a potentiometric technique, and EMGs
from extensor carpi radialis (ECR) and tibialis anterior
(TA) were recorded. All subjects were able to couple in-
phase oscillations, but 13 of them failed to perform the
anti-phase task. Maximal frequency of oscillation was
found to be positively correlated with age. Phase-rela-
tions between hand and foot oscillations and between on-
sets of the EMG activity in hand and foot movers were
measured in 37 of the children. During in-phase coupling
limb oscillations were kept in an almost perfect synchro-
ny by three different modalities of muscle recruitment.
Ten of the youngest children activated TA before ECR,
while 13 of the oldest subjects activated ECR before TA,
as do adults. The remaining 14 children (7–8 years old)
activated the two muscles almost synchronously. During
anti-phase coupling, most of the younger children (20)
showed a strict phase-opposition between both EMG on-
sets and movements. The remaining 10 (9–10 years old)
activated the ECR first. The hand frequency-response
(i.e. the phase-relation between the onset of the EMG
and the related movement) showed age-related changes,
corresponding to the behaviour of a mass-spring model
(with lumped parameters) decreasing its resonant fre-
quency. Instead, the foot frequency-response remained
P. Cavallari (✉)
Dipartimento di Scienze Precliniche, LITA-Vialba,
Università degli Studi di Milano, Via GB Grassi 74,
20157 Milan, Italy
e-mail: paolo.cavallari@unimi.it
Tel.: +39-02-70601087/38210621
G. Cerri · F. Baldissera
Istituto di Fisiologia Umana II, Università degli Studi,
Milan, Italy
unchanged. The age-related modifications of the hand
frequency-response adequately explain the changes of
the interlimb relations described above. These results
show that central structures controlling hand and foot
coupling are still immature before 10 years of age and
reinforce the view that in-phase and anti-phase coupling
require separate neural controls.
Keywords Associated movements · Phase coupling ·
Hand · Foot · Children
Introduction
Voluntary limb movements can be organised in a variety
of associations, but anyone can readily perceive that
some of the couplings are promptly and easily performed
while others require dexterity and close attention (Meige
1901; Baldissera et al. 1982; Kelso 1984; Carson et al.
1995; Swinnen et al. 1995). In particular, cyclic flexion-
extensions of one hand and the ipsilateral foot are easily
associated when the two segments oscillate with the
same angular direction (i.e. in-phase), while great con-
centration is required when they are moved in opposite
directions (i.e. anti-phase; Baldissera et al. 1982, 1990).
It has also been pointed out that kinesthetic signals pro-
duced by the ongoing movement are critical in control-
ling the synchrony between the two oscillating segments
(Baldissera et al. 1990, 1994; Baldissera and Cavallari
2001).
The frequency-responses of the hand and the foot (i.e.
the phase-relations between the muscular drive and the
related movement) during voluntary oscillations of the
two segments have been recently analysed in adult sub-
jects (Baldissera et al. 2000). By comparing the hand fre-
quency-response to that of a second-order model with
lumped parameters, it was argued that in adults males the
ratio between stiffness (K) and inertia (M) is lower in the
hand than in the foot, while in adult females the two ex-
tremities have similar K/M ratios. To synchronise two
oscillating segments displaying different mechanical

properties, such as the hand and foot, a “neural control-
ler” should be added to a common rhythm generator so
as to compensate for their physical differences. The con-
troller may operate either by desynchronising hand from
foot activation or by changing the physical properties of
one or both limbs. In adults, these two mechanisms seem
to coexist, although each of them is applied to a different
extent by males and females (Baldissera et al. 2000).
It is well known that during childhood body morphol-
ogy and the biomechanical properties of the upper and
the lower limbs undergo large transformations (Jensen
and Nassas 1988; Jensen 1993). Moreover, several neuro-
anatomical (Yakovlev and Lecours 1967; Pujol et al.
1993) and electrophysiological studies (Lauffer and Wen-
zel 1986; Eyre et al. 1991; Müller et al. 1991a, 1994;
Müller and Hömberg 1992) indicate that some motor and
sensory components of the human nervous system are
still developing at the end of the first decade of life, as
also suggested by the late maturation of cutaneous reflex-
es (Rowlandson and Stephens 1985), of the short and the
long latency responses of the stretch reflex (Bawa 1981)
and of various postural reflexes (Haas et al. 1986; Berger
et al. 1987; Müller et al. 1991b). It was thus of interest to
investigate when and how the coordination of coupled
limb movements develops during childhood, in order to
acquire further insight into the nature and the functional
organisation of neural mechanisms which govern move-
ment coupling of the hand and foot.
Materials and methods
Experiments, authorised by the children’s parents and approved by
the local ethics committee, in accordance with the ethical stan-
dards laid down in the 1964 Declaration of Helsinki, were per-
formed on 30 boys and 36 girls, aged 7–10 years (15 of age 7, 36
of age 8, 9 of age 9 and 6 of age 10). Children were informed
about the test and were never forced to take part in it. Subjects had
no history of neurological disease and no pathological signs at the
moment of the test; all of them showed a normal growth develop-
ment and an academic level appropriate to their age. All the chil-
dren were tested on the right side. To make the children more
comfortable with the experimental procedure, 1 week before the
session they were instructed about the task and asked to practice at
home under parental control.
During the experimental session the subject was sitting on an
armchair with forearms resting in a prone horizontal position and
legs hanging. The right hand and the right foot were free to per-
form full-range flexion-extension movements in a parasagittal
plane. Wrist and ankle angular displacements were recorded by a
potentiometric device positioned coaxially to the joint centre of
rotation. Electromyogram (EMG) from extensor carpi radialis
(ECR) and tibialis anterior (TA) muscles was recorded by surface
silver electrodes. Both goniometric and EMG signals were ampli-
fied, digitised (DAQcard 700; National Instruments; sampling rate
of 250 Hz per channel), visualised and stored on a computer.
In the first part of the experiment, the subject was asked to
couple cyclic flexion-extensions of the hand and the ipsilateral
foot. This task was achieved by associating hand extension to foot
dorsal flexion and hand flexion to foot plantar flexion, so that the
two segments moved isodirectionally (in-phase coupling). In the
second part of the experiment, subjects were asked to oscillate the
two segments in opposite directions, i.e. now associating hand ex-
tension to foot plantar flexion and hand flexion to foot dorsal flex-
ion (anti-phase coupling). Oscillation frequency was paced by a
399
metronome from 0.8 Hz up to each subject’s maximal frequency,
in steps of 0.2 Hz. The trial duration was of at least 10 s. If during
this period a coupling error occurred, the trial was interrupted and
repeated after a short rest. Trials performed at frequencies lower
than 0.8 Hz and for less than 10 s were not considered. The move-
ment amplitude was spontaneously chosen by the subject in a
range between 20° and 40°.
Interlimb phase-relation between hand and foot movements
The phase-relation between hand and foot oscillations was auto-
matically calculated from the goniometric signal. For each move-
ment cycle, the timing of the half-excursion points, where speed is
maximal and the measurement error minimal, was determined. To
reduce the influence of possible asymmetries of the movement cy-
cles, the difference in time between each hand and foot cycle was
calculated by comparing the midpoint of the hand period to the re-
spective midpoint of the foot period. The phase-relation between
the hand and the foot movement was expressed in degrees, taking
each hand period as a reference. For each trial the average phase-
relation and standard deviation were computed. Phase 0° indicates
that the task was executed with the required synchrony (0° for in-
phase coupling and 180° for the anti-phase). Conventionally, posi-
tive values indicate a phase-advance of the hand cycle.
Interlimb phase-relation between ECR and TA EMG activation
The EMG signal from ECR and TA muscles was rectified and in-
tegrated (time constant 5 ms). The onset of each EMG burst was
determined by automatically selecting the point where the EMG
signal crossed a threshold voltage. Threshold value was visually
chosen so as to detect the very beginning of the EMG bursts. Then
periods between the successive EMG bursts were measured. The
mean phase difference between hand and foot EMG bursts was
calculated by comparing the midpoints of each ECR and TA peri-
od, and expressed in degrees. For each trial, the average phase-
relation and its standard deviation were computed. Phase 0° indi-
cates that ECR activated synchronously with TA during in-phase
coupling and at 180° with respect to TA during anti-phase cou-
pling. Conventionally, positive values indicate a phase-advance of
the ECR on TA burst.
Frequency-response of the hand and the foot:
phase-relations between the EMG onset and the ensuing movement
On the assumption that the hand and the foot behave like two os-
cillating pendula forced by sinusoidal inputs (see Baldissera et al.
2000), the input-output phase-relation of each segment was mea-
sured with the aim of estimating the mechanical characteristics of
the hand and the foot systems during voluntary oscillations. For
each limb, the EMG periods of a single trial were summed and av-
eraged. Movement periods underwent the same mathematical
treatment. The mean phase-relation was then calculated between
the onset of the EMG burst and the onset of the related movement.
Mean phase values were then plotted against the movement fre-
quency to give a frequency-response plot.
Adult population
The maximal frequency of oscillation was tested both during in-
phase and anti-phase coupling in 18 adult volunteers (9 males,
9 females) aged 22 to 35 years. Hand and foot movements were
monitored as in children.
Statistical analysis
Maximal frequency data were treated by a two-way ANOVA test
(between factor: age, in steps of 1 year; within factor: coordination
400
mode). Values of F, degrees of freedom and the related probability
(P) are given in the text. Post hoc comparisons were performed by
the Tukey HSD for unequal n test.
The dependence of the mean maximal frequency value on chil-
dren’s age, both during in-phase and anti-phase movements, was
also confirmed by regression analysis. The coefficient of determi-
nation (r2) and coefficient of regression (slope) are given. Com-
parison between the mean maximal frequencies performed by the
oldest children with data from adults was validated by the un-
paired Student t-test. Values of t, degrees of freedom and the relat-
ed probability are given in the text.
Since the grouping procedure, based on the pattern of muscular
activation (see Results), divided the children in three groups (TA,
SYNCH and ECR) for the in-phase coupling and in two groups
(SYNCH and ECR) for the anti-phase, data collected during the
two modes of coordination have been treated separately. Also in-
terlimb phase-differences (between hand and foot EMGs and be-
tween hand and foot movements) were analysed separately from
the intralimb phase-responses (phase-differences between EMG
and movement in the hand or the foot). Thus, comparisons be-
tween groups of children and between children and adults (inter-
limb or intralimb relations) were validated by two-way ANOVA
tests (between factor: behavioural group; within factor: frequen-
cy). Comparisons within the same group of children (hand and
foot phase responses) were validated by two-way ANOVA tests
(between factor: hand and foot; within factor: frequency). Values
of F, degrees of freedom and the related probability (P) are given
in the text.
A comparisons was considered not significant when P>0.05.
For each comparison only values covering the common frequency
range were included in the analysis. In the comparison between
the oldest children and adults, the data match was between 0.8 and
2.8 Hz for the in-phase association, and between 0.8 and 2.0 Hz
for the anti-phase association. The number of subjects considered
in each comparison will be indicated in the text. Children unable
to perform the anti-phase coupling were excluded from statistical
evaluation.
Results
Maximal frequencies of the hand and foot oscillations
Each of the 66 subjects was required to perform, as fast
as possible, 10 s of rhythmic oscillations of the right hand
and foot, paired first in-phase and then anti-phase. The
maximal frequency of the in-phase coupling was equal or
higher than 1.2 Hz in 63 children (95.5%), while 3 sub-
jects (4.5%) could not do better than 0.8 Hz. During such
coupling 22 children (33%) were able to reach frequen-
cies higher than 2.0 Hz. In contrast, during anti-phase
coupling maximal frequency was lower than or equal to
1.2 Hz in 59 children (89.4%) including those (13) who
could not to perform the task at all. Of the remaining pop-
ulation (10.6%), 4 children could reach 1.4 Hz and 3 at-
tained frequencies equal to or higher than 2.0 Hz.
Maximal frequency of the in-phase coupling was
higher than that of the anti-phase in 64 subjects (97%)
and equal in two cases (3%), however the difference
between in- and anti-phase values displayed a great
intersubject variability, ranging from 0 to 1.8 Hz
(mean 0.92±0.47 Hz). In the population performing both
in-phase and anti-phase coupling mean maximal fre-
quency in the two modalities was significantly different
[in-phase: 1.76±0.56 Hz; anti-phase: 1.00±0.38 Hz;
t(104)=8.16; P<0.001].
Fig. 1 Maximal frequency of oscillation attained during in-phase
(filled circles) and anti-phase coupling (open circles) in 53 chil-
dren. Children were grouped by age: 12 aged 7 years, 29 aged
8 years, 6 aged 9 years and 6 aged 10 years. For comparison, the
maximal values attained by 18 adults are plotted on the right side
of the figure. Vertical bars ±1 SD
The frequency limit of in-phase and anti-phase cou-
pling varied with subject age. To better visualise this cor-
relation, data were ranked in four groups, each collecting
children born in the same year and the mean maximal
frequency of each group calculated. Children unable to
perform anti-phase coupling (13) were excluded from
this calculation. As shown in Fig. 1, the mean maximal
frequency of in-phase movements (filled circles) was
close at ages 7 and 8 years (1.5 and 1.6 Hz, respectively)
while it increased to 2.2 Hz at 9 years and to 2.6 Hz at
10 years. During anti-phase movements (open circles)
the mean maximal frequency was 0.8 Hz at 7 years,
0.9 Hz at 8 years, 1.3 Hz at 9 years and 1.5 Hz at
10 years. Two-way ANOVA showed a significant effect
of both age [F(3,49)=16.42; P<0.0001] and coordination
mode [F(1,49)=167.05; P<0.0001] on maximal frequen-
cy. The comparison between contiguous age groups, per-
formed by a Tukey HSD for unequal n test, showed that
the mean maximal frequency changed significantly
(P<0.005) only in the step between 8 and 9 years. Com-
parisons between non-contiguous groups were always
highly significant (P<0.0001). Instead, interaction of the
two factors showed no significant effect, indicating that
during the considered age span maximal frequency under-
went parallel changes in the two movement conditions.
The dependence of the mean maximal frequency values
on children’s age, both during in-phase and anti-phase
movements, was confirmed by regression analysis (in-
phase: slope 0.41, r2 0.95; anti-phase: slope 0.25, r2 0.98)
The mean maximal frequency value attained by
18 adults is plotted, for comparison, on the right side of
the figure. In this sample maximal frequency ranged
between 2.6 and 3.4 Hz (mean: 3±0.2 Hz) during in-
phase movements, and between 1.6 and 2.2 Hz (mean:
2±0.2 Hz) during anti-phase movements. The mean
maximal frequency attained by the six oldest children
(10 years) was significantly lower then that attained
by adults in both movement conditions [in-phase:
t(22)=3.37; P<0.005; anti-phase: t(22)=5.49; P<0.005],
indicating that maturation is still incomplete at the end
of the first decade.

Interlimb phase-relations
and limb frequency-responses during in-phase coupling
Rhythmic oscillations of the right hand and ipsilateral
foot, coupled in-phase, were performed in steps of
0.2 Hz, from 0.8 Hz to the maximal frequency. Children,
as adults, appeared to be very comfortable when initiat-
ing and performing the in-phase task, the coupling being
only limited by muscle fatigue or by the sporadic appear-
ance, at frequencies above 2.5 Hz, of multiple rhythms
(1:2, 1:3).
These trials aimed at analysing the effect of the oscil-
lation frequency on both the interlimb phase-relations and
the frequency-responses of the hand and the foot. This
analysis, requiring detection of the timing of EMG bursts,
was fulfilled in 37 children only (8 of age 7, 19 of age 8,
4 of age 9 and 6 of age 10), since the presence of a strong
tonic background activity in one or both muscles did
not allow a correct measurement of the EMG onsets in
the remaining 29 children. Differently from adults (see
Baldisssera et al. 2000), data from boys and girls over-
lapped and were thus pooled together (see Discussion).
Interlimb phase-relations
The synchrony between hand and foot movements was
evaluated by measuring the phase-relation between the
oscillation of the two limbs. Although children were un-
able to reach frequencies as high as adults (see above),
they displayed a good synchrony between hand and foot
movements at all frequencies. In fact, in the whole sam-
ple, the hand movement lagged the foot one by only
1±9° (standard deviation).
As already stated in the Introduction, in adults the
movement synchrony is achieved by anticipating the
command forwarded to the hand movers so as to com-
pensate for the lower K/M ratio in the hand than in the
foot. In particular, in adult males the onset of the ECR
EMG always anticipates the TA EMG and the phase-
advance increases with frequency, while in females this
advance becomes evident only above 1.4 Hz. Differently
from adults, children adopted three different patterns of
muscular activation to achieve synchrony between hand
and foot movements. Some of them activated the TA
muscle earlier than ECR (Fig. 2a) and some displayed a
simultaneous activation of both muscles (Fig. 2b), while
others activated the ECR earlier than TA (Fig. 2c), as
adults do. Recall that hand and foot movements were al-
most synchronous in all three groups. On the basis of
this observation, children were divided in three groups
(TA, SYNCH and ECR) each collecting those subjects
who showed a similar pattern of muscular activation.
Figure 3 illustrates, for each group, the mean phase-rela-
tions between hand and foot movements (Fig. 3a–c open
circles) and the mean phase-relation between ECR and
TA onsets (Fig. 3a–c filled circles).
The TA group included 10 children (aged 7–8 years)
who obtained an almost perfect movement synchrony
401
Fig. 2a–c In-phase coupling of rhythmical oscillations of the hand
and the ipsilateral foot in three children, at the frequency of
1.2 Hz. Cycle plot of the angular displacement of the hand and
foot (two uppermost traces in each panel) are displayed together
with the integrated EMG from the extensor carpi radialis (ECR)
and tibialis anterior (TA) muscles (two lowermost traces in each
panel). Each trace is the average of 10 cycles. Note that in all sub-
jects the hand and foot oscillations are almost synchronous, while
the timing of the EMG onset is different in each of them: in a the
onset of the TA EMG precedes (arrow) that of the ECR; in b the two
EMG onsets are synchronous; in c the ECR leads (arrow) the TA
(mean phase-difference –1±2°; open circles in Fig. 3a)
by an earlier activation of the TA with respect to the
ECR (mean phase-difference –16±5°, filled circles in
Fig. 3a). All of them but one reached the frequency of
1.4 Hz. Conversely, the 13 children included in the ECR
group (10 aged 9–10, three aged 7–8) exhibited a net ad-
vance of the ECR onset with respect to the TA. The
mean ECR advance progressively increased from 0.8 to
2.4 Hz, reaching a maximum of 43° at 2.4 Hz. In the
range between 0.8 and 1.4 Hz, in common with the TA
group, the mean ECR-TA advance was 17±7°. The ad-
vance of the hand on foot movers led to a good move-
ment synchrony (Fig. 3c open circles, mean phase-differ-
ence –6±4°). Eleven of these children reached the fre-
quency of 2.0 Hz, eight 2.4 Hz and five 2.8 Hz. Finally,
the 14 children of the SYNCH group (aged 7–8 years)
achieved synchrony between hand and foot movements
(Fig. 3b open circles) by a simultaneous activation of the
ECR and TA muscles (Fig. 3b filled circles). All were
able to oscillate their limbs up to 1.4 Hz, 9 up to 1.6 Hz,
6 up to 1.8 Hz and 3 attained 2.0 Hz. In the common fre-
quency range, between 0.8 and 1.4 Hz, the mean phase-
difference between ECR and TA onset was 1±2°, and the
lag of the hand movement was 4±1°.
Statistical analysis showed that in the frequency range
common to the whole children population the mean
phase-difference between hand and foot movements was
almost equal in the three groups [F(2,34)=0.32; P<0.72],
while the mean phase-difference between activation of
muscles was significantly different in the TA vs the
402
Fig. 3a–h Interlimb phase-relations and limb frequency-responses
during in-phase coupling. a–d The mean phase-difference between
hand and foot movements (open circles) and between ECR and TA
EMG onsets (filled circles) at various frequencies, are plotted for
each of the three groups of children. Children of the TA group
(a; 10 subjects) show an earlier activation of the TA with respect
to the ECR (negative values of the ordinate); children of the
SYNCH group (b; 14 subjects) display an almost simultaneous
activation of ECR and TA muscles; while in the ECR group
(c; 13 subjects) the hand mover largely anticipates the foot mover.
Ordinate Deviation from the task-related relation (0°); negative
values signal a phase-lag of the hand cycle. e–g Frequency-
responses (i.e. phase-difference between the EMG onset and the
onset of the related movement) of the hand (filled circles) and the
foot (open circles). Positive values when the EMG onset lags the
movement. For comparison, data from five adult males (continu-
ous lines) and from five adult females (dashed lines) are plotted in
d and h (from Baldissera and Cavallari 2001). Vertical bars ±1 SD
SYNCH group [F(1,22)=7.20; P<0.01], as well as in the
SYNCH vs the ECR group [F(1,25)=5.20; P<0.03].
Frequency-response of the hand and foot
For each limb, the phase-difference between the EMG
onset and the onset of the related movement was plotted
against the oscillation frequency to draw frequency-
response curves as those illustrated in Fig. 3e–g for the
hand (filled circles) and the foot (open circles).
In children belonging to the TA group the onset of the
TA EMG followed the onset of the foot dorsal flexion
(Fig. 3e open circles), as happens in adults (Fig. 3h). The
phase-difference between the onset of the TA EMG and
the related movement was about 29° at 0.8 Hz but rapid-
ly decreased to about –1° at 1.4 Hz (mean value
15±14°), indicating that the children’s foot is relatively
“heavier” then that of adults (compare Fig. 3e and h).
Differently from adults, the children’s hand curve
showed positive values, i.e. children activated hand ex-
tensors after the onset of extension phase. The lag of the
ECR onset was about 43° at 0.8 Hz and progressively
decreased to 23° at 1.4 Hz (mean lag 36±10°; Fig. 3e
filled circles). Since a similar course of the phase curve
was observed in adults when their hand was connected to
an elastic load (Baldissera and Cavallari 2001), this re-
sult suggests that in children the first phase of hand ex-
tension may be sustained by the elastic recoil of tissues
which have been stretched during the flexion phase.
When comparing the frequency-responses of the two
limbs, one observes that the hand curve remains above
that of the foot over the whole frequency range. This dif-
ference is confirmed by statistical analysis [F(1,18)=
24.48; P<0.01] and indicates that the ratio K/M should
be larger in the hand than in the foot. It also accounts for
the earlier activation of the TA muscle with respect to
ECR, necessary to synchronise hand to foot oscillations
(Fig. 3a).
Children of the SYNCH group showed a perfect over-
lapping [F(1,26)=0; P<0.96] of the hand and foot fre-
quency-responses (mean 19±16° for the hand curve,
17±17° for the foot curve; Fig. 3f). Identical mechanical
properties of hand and foot could explain why synchro-
nous muscle activation resulted in a synchronous oscilla-
tion of the two limb segments (Fig. 3b). In children be-
longing to the ECR group (Fig. 3g) the ECR onset
lagged the hand extension by about 29° at 0.8 Hz, antici-
pated it by –10° at 1.4 Hz, reaching a maximum of –56°
at 2.6 Hz (mean value –21±29°; filled circles). The TA
activation lagged the foot dorsal flexion by 48° at
0.8 Hz, anticipated it by –3° at 2.2 Hz and by –27° at
2.8 Hz (mean value 11±23°; open circles). The frequen-
cy-response of the hand lay below that of the foot over
the whole frequency range and was statistically different

from it [F(1,24)=13.93; P<0.01]. Thus, hand and foot
mechanical properties are inverted in children of the
ECR group with respect to the TA group. In fact, due to
the relatively higher elastic recoil of the foot, children of
the ECR group synchronised hand and foot oscillations
by an earlier activation of the hand flexor (Fig. 3c).
When comparing the hand frequency-responses of the
three groups over the common frequency range, it is ap-
parent that the curves were similar in the TA and
SYNCH groups (on average 36±10° vs 30±10°; no sig-
nificant difference), while it significantly rotated clock-
wise in the ECR group [on average 19±16° vs –10±26°;
F(1,25)=10.52; P<0.04]. In contrast, the foot frequency-
response significantly shifted upwards when passing
from the TA to the SYNCH group [15±14° vs 30±9°;
F(1,22)=14.09; P<0.01], but it remained unchanged
from the SYNCH to the ECR group (17±17° vs 21±18°;
no significant difference).
Comparison between children and adults
Only children of the ECR group adopted the pattern of
muscle activation which is characteristic of adults (com-
pare the EMG curves in Fig. 3c and d), since both share
similar mechanical properties (i.e. a lower K/M ratio in
the hand than in the foot, compare Fig. 3g and h). How-
ever, the biomechanical characteristics of the hand and
foot are not identical in adults and in children of the
ECR group. For instance, the frequency-response of the
children’s hand lies above that of adults (males and fe-
males) over the entire common frequency range. The
mean phase-difference between the ECR onset and the
hand extension was –21±29° in children, –38±39° in
adult females and –50±42° in adult males. The children’s
curve was significantly different from that of females
[F(1,16)=4.83; P<0.04], as well as from that of males
[F(1,16)=13.85; P<0.02]. As far as the foot curve is con-
cerned, the phase-difference between the TA onset and
the foot dorsal flexion was, on average, 11±23° in the
children, 0±28° in adult females and –8±24° in adult
males. The children’s curve differed significantly only
from that of adult males [F(1,16)=6.27; P<0.02].
Correlation between pattern of muscle activation,
maximal frequency of oscillation and age of the children
Having classified children according to the temporal pat-
tern of activation of hand and foot movers, it was of in-
terest to verify whether this subdivision would correlate
with maximal frequency and age. When considering the
maximal frequency of oscillation (Fig. 4a), it was found
that mean maximal frequency was 1.4 Hz in children of
the TA group, 1.8 Hz in the SYNCH group and 2.4 Hz in
the ECR group. Although only the improvement from
the SYNCH group to the ECR group was significant
[F(1,25)=8.95; P<0.01], statistical analysis confirmed
the progressive growth of this parameter when crossing
403
Fig. 4 Distribution of the mean value of the maximal frequency of
oscillation (a, c) and of the children’s ages (b, d) across the three
different groups of children (TA, SYNCH and ECR). Filled col-
umns In-phase coupling, open columns anti-phase coupling. Verti-
cal bars ±1 SD
all three groups [F(2,34)=12.14; P<0.01]. Age was on
average 8.1 years in the TA group, 8.2 years in the
SYNCH group and 9.7 years in the ECR group (Fig. 4b).
As for maximal frequency, only the difference between
SYNCH and ECR groups was statistically significant
[F(1,25)=22.51; P<0.01]. However, although the mean
children’s age was similar in TA and SYNCH groups,
the gradual improvement in maximal frequency suggests
a progressive functional maturation of the structures
which control the coordination of the in-phase pattern,
which is not evident when comparing the subject’s age.
In the sample of 37 children the relation between age
and mean maximal frequency was similar to that of the
whole children’s population (66), as indicated by the
first-order linear regression of the two curves (slope 0.37
and 0.39, r2 0.84 and 0.92, respectively).
Interlimb phase-relations and limb frequency-responses
during anti-phase coupling
Subjects were asked to perform cyclic oscillations of the
right hand and ipsilateral foot coupled in phase-opposi-
tion, at different frequencies. Children showed great dif-
ficulty in starting the anti-phase coupling and hesitations
and errors when executing this task. The most frequent
error was an abrupt phase transition leading to a sponta-
neous reversal to the in-phase pattern. As in adults, the
error probability grew with the oscillation frequency and
with the duration of the performance. Seven of the
37 subjects (2 from the TA group, 4 from the SYCH
group and 1 from the ECR group) were just not able to
accomplish the task. Since data obtained at frequencies
404
Fig. 5a, b Anti-phase coupling of rhythmical oscillations of the
hand and ipsilateral foot in two subjects, at the frequency of
1.2 Hz. Cycle plot of the angular displacement of the hand and
foot (two uppermost traces in each panel) are displayed together
with the integrated EMG from the ECR and TA muscles (two low-
ermost traces in each panel). Each trace is the average of 10 cy-
cles. Note that the hand and foot oscillations are almost perfectly
out of phase (180° difference) in both subjects, but while in a the
ECR EMG onset precedes the TA just by a half-cycle, in b the on-
set of the ECR is anticipated (arrow) with respect to the phase-op-
position
above 1.2 Hz comprise only part of the population, they
were not included in the statistical analysis, albeit they
remain valuable in characterising the frequency depen-
dence of the results.
Interlimb phase-relations
As shown by the two individual cases of Fig. 5, children
adopted two patterns of muscular activation to perform
anti-phase coupling. Most of them (20; 5 of age 7, 12 of
age 8 and 3 of age 10) managed to keep the movements
in phase-opposition by shifting the ECR and the TA on-
set by about 180° (Fig. 5a). These individuals, who
maintained the task-required synchrony (180°) between
movements and between EMG onsets, will be referred to
as the SYNCH group, similarly to those who showed
synchronous muscle activation during in-phase coupling.
The remaining 10 children (1 of age 7, 2 of age 8, 4 of
age 9 and 3 of age 10) achieved the requested synchrony
of movements by anticipating the ECR onset with re-
spect to the reference phase (ECR group; Fig. 5b). The
mean phase-relation between ECR and TA onsets was
–4±3° in the SYNCH group (Fig. 6a filled circles) and
19±6° in the ECR group (Fig. 6b filled circles). Over the
common frequency-range the two means are significant-
ly different [F(1,18)=10.79; P<0.01]. Note, however,
that in the last group the ECR advance progressively de-
creased at frequencies higher than 1.4 Hz and reversed to
a lag of about 12° in the 3 subjects who reached 2 Hz.
As far as movements are concerned (Fig. 6a, b open
circles), no significant difference between the two
groups was found over the common frequency range
(0.8–1.2 Hz). However, in the ECR group movement
synchrony deteriorated at frequencies higher than 1.4 Hz
Fig. 6a–f Interlimb phase-relations and limb frequency-responses
during in-phase coupling. a, b The mean phase-difference between
hand and foot movements (open circles) and the mean phase-dif-
ference between the onsets of ECR and TA EMG (filled circles), at
different frequencies, are plotted for each of the two groups of
children. Children of the SYNCH group (a; 20 subjects) display
an activation of ECR and TA muscles with a perfect anti-phase
synchrony while those of the ECR group (b; 10 subjects) antici-
pate activation of the hand mover with respect to phase-opposition
(positive values of the ordinate). Ordinate Deviation from the
task-required relation (180°). d, e Frequency-responses (i.e. phase-
difference between the EMG onset and the related movement) of
the hand (filled circles) and the foot (open circles). Positive values
when the EMG onset lags the movement. For comparison, data
from five adult males (continuous lines) and from five adult fe-
males (dashed lines) are plotted in c and f (from Baldissera and
Cavallari 2001). Vertical bars ±1 SD
so that the hand progressively lagged the foot, up to 37°
at 2 Hz.
Thus grouping of children based on to the pattern of
muscular activation did not coincide when comparing in-
phase with anti-phase coupling. Out of the 20 subjects
included in the anti-phase SYNCH group, only 10
showed synchronous muscle activation when performing
in-phase oscillations, while 6 anticipated the TA muscle
and 4 the ECR contraction. Out of the 10 subjects in-
cluded in the anti-phase ECR group, 8 used the same
pattern during in-phase coupling, while 2 anticipated the
TA contraction.
Frequency-response of the hand and foot
The frequency-responses of the hand and foot measured
during anti-phase movements are displayed in Fig. 6d, e.
Children of the SYNCH group activated the ECR after
the onset of wrist extension at all frequencies, producing

positive values in the frequency-response of the hand
(Fig. 6d filled circles). The mean lag of the ECR onset,
with respect to the onset of the extension movement, was
41° at 0.8 Hz, and progressively decreased to 26° at
1.4 Hz (mean EMG lag 34±6°). Similarly, the onset of
the TA EMG followed the onset of the foot dorsal flex-
ion (Fig. 6d open circles). The lag was 38° at 0.8 Hz and
decreased to 26° at 1.4 Hz (mean 34±7°). The curves of
the two limbs overlapped over the whole course (no sig-
nificant difference). Thus, the hand and foot of the chil-
dren belonging to the SYNCH group displayed identical
mechanical properties when performing the anti-phase
coupling. This is in agreement with the fact that synchro-
nous oscillations of hand and foot in anti-phase were
produced by synchronous muscle activation (Fig. 6a). In
children of the ECR group, activation of the wrist exten-
sor followed the onset of the hand movement by about
37° at 0.8 Hz. This delay progressively decreased until
the ECR onset preceded the hand movement by about 5°
at 2 Hz (Fig. 6e filled circles). Also the TA onset lagged
the foot dorsal flexion of 48° at 0.8 Hz, but differently
from the hand, this lag remained almost constant over
the whole frequency range (Fig. 6e open circles). Thus,
the frequency-response of the hand progressively di-
verged from that of the foot reaching a significant differ-
ence at 2.0 Hz [F(1,4)=63.9; P<0.01].
Comparison between children and adults
The almost perfect phase-opposition between ECR and
TA activation displayed by children of the SYNCH
group was also observed in adult females (compare
Fig. 6a and c), whose hand frequency-response (i.e. its
biomechanical properties) overlapped the foot frequen-
cy-response (Fig. 6d, f). On the other hand, children of
the ECR group adopted a pattern of muscle activation
more similar to that of adult males (no statistical differ-
ence between the two curves) than to that of adult fe-
males [F(1,11)=7.38; P<0.02], at least up to 1.2 Hz.
Above that frequency they progressively lost their limb
synchrony and the hand ended up lagging the foot move-
ment (Fig. 6b open circles). In adults of both genders, in-
stead, a further anticipation of the ECR onset maintained
a constant phase-delay between the limb oscillations (see
movement lines in Fig. 6c).
Adults and children of the ECR group also differed in
their limb frequency-responses (Fig. 6e, f). In children
the mean phase-delay between the ECR onset and the
hand extension was 23±15°, while it measured 6±16° in
adult females and –3±25° in adult males. The children’s
hand curve lay above both adult curves, but no statistical
difference was found. As far as the foot curve is con-
cerned, the phase-difference between the TA onset and
the foot dorsal flexion was, on average, 45±3° in chil-
dren, 37±10° in adult males and 8±15° in adult females.
The children’s curve ran above both adult curves but was
significantly different only from that of adults females
[F(1,6)=25.25; P<0.01].
405
Correlation between pattern of muscle activation,
maximal frequency of oscillation and age of the children
On average, children of the SYNCH group reached a
maximal frequency of 1.1±0.2 Hz while those of the
ECR group attained 1.4±0.5 Hz (Fig. 4c). A significant
difference was found between the two groups [F(1,29)=
6.72; P<0.01]. However, the average age of the SYNCH
group (8.6 years) was not significantly different from
that of the ECR group (9.2 years).
The significant improvement of the maximal frequen-
cy from the SYNCH to the ECR group suggests the oc-
currence of a functional maturation of the structures con-
trolling the coordination of the anti-phase pattern, not
evident when considering the subject’s age. Also in the
case of anti-phase coupling the relation between age and
maximal frequency of oscillation in the sample of
37 children was similar to that of the whole population
(66). First-order linear regression of the two sets of data
resulted with a slope of 0.37 and an r2 value of 0.84 in
the reduced sample and a slope of 0.39 and an r2 value of
0.92 in the whole sample.
Discussion
Our data suggest that the neural network processing the
coupling of hand and foot movements is not completely
mature by the end of the first decade of life. Two pieces
of evidence support this conclusion: (1) during in-phase
and anti-phase coupling the maximal frequency of oscil-
lation is lower in children than in adults and (2) a large
number of the youngest children were unable to perform
the anti-phase task. However, it should be noted that de-
spite the intergroup differences in limb mechanical prop-
erties, synchrony of limb movements was quite good in
all groups of children, at least at low frequencies. This
should indicate that the mechanism that controls syn-
chronisation of hand and foot movements is already op-
erating the appropriate compensations by the age of sev-
en.
Three further aspects will be discussed: (1) the maxi-
mal frequency of oscillation, (2) the movement synchro-
ny and (3) the absence of gender differences.
Maximal frequency of oscillation
None of the children was able to reach frequencies of os-
cillation comparable to those attained by adults; never-
theless, as in adults, maximal frequency of in-phase
movements was higher than that of anti-phase move-
ments. It should also be underlined that some of them,
who reached relatively high frequencies during in-phase
coupling, failed to associate the hand and foot anti-
phase. In particular, this was common below the age of
8 years.
All these results seem to indicate that structures con-
trolling anti-phase coupling develop later than those con-
406
trolling in-phase coupling and strengthen the hypothesis
that different parts of the nervous system may process
the two kind of movements. This conclusion appears to
be in contrast with a recent PET study (Ehrsson et al.
2000) in which no substantial difference in brain imag-
ing was observed when adults oscillated their wrist and
the ipsilateral ankle, in-phase or anti-phase. It should,
however, be stressed that an unchanged PET signal dur-
ing opposite tasks indicates that a certain brain region
keeps identical levels of blood flow, not identical neural
activity. In the present case, the opposite alternation of
excitation and inhibition is a main feature distinguishing
in-phase from anti-phase coupling. Thus it is not surpris-
ing that PET, which cannot discriminate between the ac-
tivation of excitatory vs inhibitory neurones, would give
the same result for the two coordination modes. Alterna-
tively, in-phase and anti-phase couplings could be
achieved by activating different neuronal populations in-
termingled in the same volume, which would also be
hardly detected by PET imaging. We cannot but agree
with Ehrsson’s statement “the direction of the movement
seems to be of little importance in terms of increases in
rCBF”, but we disagree with his further statement that
“there is no difference in the pattern of cortical activi-
ty...”.
In both associations, maximal frequency was positive-
ly correlated with the children’s age. Several authors in-
vestigated the maturation profile of the central and the
peripheral nervous system. Despite some methodological
controversies, it seems well established that maturation
of the corticospinal system, as estimated by measuring
the conduction velocity of the fastest corticospinal neu-
rones, is completed after the 10th year (Eyre et al. 1991;
Müller et al. 1991a, 1994; Nezu et al. 1997; Fietzek et al.
2000). Instead, the conduction velocity of spinal moto-
neurones has a much faster maturation, nearing adult
values by about the age of 3 years (Eyre et al. 1991;
Müller et al. 1991a, 1994; Cai and Zhang 1997; Nezu et
al. 1997). Factors that could determine the increase in
conduction velocity during development of the nervous
system are thought to be both an increase of axon diame-
ter and a higher degree of myelinisation in corticospinal
fibres.
Finally, it should also be considered that the low fre-
quencies of oscillation might result from the mechanical
limits of muscle contraction. Is known in fact that mus-
cle relaxation time shortens with the children’s age and,
in consequence, the maximal frequency of alternating
movements of the wrist and ankle doubles between the
3rd and the 10th year (Lin et al. 1996).
Movement synchrony during in-phase coupling
Biomechanical characteristics of the hand and the foot
The maintenance of an almost perfect phase-relation be-
tween hand and foot movements (mean phase-difference
ca 1°) indicates that children, favoured by an advanta-
geous biomechanical situation, can accomplish the in-
phase task with a higher synchrony than adults (mean
phase-difference ca 20°; see Baldissera et al. 2000). To
achieve this result, three different motor strategies were
adopted, which well compensated for three different bio-
mechanical situations. The frequency-responses of the
children belonging to TA, SYNCH and ECR groups wit-
ness that the mechanical properties of both the hand and
foot change from one group to another. In children of the
TA group the hand curve lies above that of the foot over
the whole frequency range, i.e. stiffness is relatively
higher (than inertia) in the hand than in the foot, a situa-
tion that justifies the earlier activation of the TA on the
ECR muscle. In the SYNCH group the two segments
display almost identical mechanical properties (the hand
and the foot curves overlapped) and synchronous oscilla-
tions of the two limb segments was obtained by synchro-
nous activation of muscles. Finally, in the ECR group the
hand curve lies, as in adults, below the foot curve, indi-
cating that the effect of mass (with respect to elasticity)
is relatively higher in the hand than in the foot. Thus,
children belonging to the ECR group synchronised hand
and foot oscillations by anticipating the onset of ECR
activation, as adults do.
As a matter of fact, the mechanical properties of the
two limbs change progressively from one group to an-
other as if the three groups may represent three different
stages of development. Though this can only be ascer-
tained with a longitudinal study, it was of interest to ana-
lyse the relationship between groups and age. It turned
out that the direct correlation between these two parame-
ters is low: for example, the TA and SYNCH groups in-
clude children of about the same age. Instead, the maxi-
mal frequency of the oscillations significantly increased
when changing from TA to SYNCH and from SYNCH
to ECR groups, i.e. it changed in parallel with the me-
chanical properties of the limbs. Now, since maximal
frequency seems correlated with children’s age (see Re-
sults), it is reasonable to deduce that during childhood
the mechanical properties of the limbs change from those
displayed by the TA group to those exhibited by the ECR
group, passing throughout a transition phase which is
represented by the SYNCH group. In particular, around
the age of seven the stiffness appears to be higher, rela-
tive to inertia, in the hand than in the foot. Later, the two
limbs become biomechanically equivalent, mainly be-
cause of an increase in the foot elasticity (the foot fre-
quency-response lifts towards that of the hand). Finally,
when reaching 9–10 years, the hand becomes relatively
“heavier” and its frequency-response steeper. At this
stage, the hand curve falls below that of the foot and as-
sumes a shape similar to that displayed by adults.
The neural controller
The most economical way to synchronise rhythmical os-
cillations of two limb segments that share identical me-
chanical properties (for example the two hands) is to uti-

lise a common rhythm generator which sends a synchro-
nous command to the muscles that move each segment.
If, instead, the two segments have different mechanical
properties (as the hand and the foot do), an additional
neural controller is needed which monitors the ongoing
movement and compensates for the phase-shift due to
the mechanical differences between the two segments.
When an adult subject is asked to perform in-phase
rhythmical flexion-extensions of the hand and foot on
one side, synchrony is achieved by two contrivances
which are intended to compensate for the relatively high
inertial resistance of the hand (Baldissera et al. 2000). A
first one is to generate a time delay between the com-
mands reaching the two limbs, i.e. to anticipate the acti-
vation of the “heavier” of the two segments, while the
second is to modify the viscoelastic properties of one (or
both) segment, thus reducing the mechanical differences
between them.
Our results suggest that the neural mechanism that
compensates for the mechanical difference between seg-
ments is already present since the age of seven, allowing
children to couple the limb movements in-phase. The
limb frequency-responses observed in children of the TA
group indicate that their hand is more elastic than that of
adults, while their foot is relatively heavier. These in-
verted biomechanical properties seems to be well detect-
ed by the in-phase neural controller since it provides to
anticipate the EMG onset in the TA with respect to that
in the ECR. Note that the TA advance was never ob-
served in adults.
Given this ability to compensate, one may wonder
why those children are not able to couple movements at
frequencies as high as adults do. As a matter of fact they
can easily oscillate the wrist alone at frequencies well
above 3 Hz (Müller and Homberg 1992; Lin et al. 1996;
Blank et al. 1999) and even granting that the maximal
frequency of foot oscillations has not yet been deter-
mined, it seems improbable that the rhythm generator is
responsible for the frequency limits. This limit may rath-
er depend on the immaturity of the in-phase control
system. Hypothetically, this control system should be fed
by both the rhythm generator and the feedback kinesthet-
ic signals from the moving limbs. If during infancy the
processing velocity of the controller is lower than in
adults, then compensation may become insufficient at a
rhythm lower than in adults, and association disrupts.
However, this would not explain the low maximal fre-
quency values displayed by children of the SYNCH
group, where intervention of a phase controller should
not be necessary because of the identical frequency-
responses of the hand and foot.
Movement synchrony during anti-phase coupling
Biomechanical characteristics of the hand and the foot
When moving the two segments in opposite directions
all children produced an upward shift of the frequency-
407
response of one segment (i.e. an increase of its elastic
properties) that minimised the difference between the
two segments.
This modification had important consequences on the
strategy of muscular activation and, therefore, on chil-
dren’s grouping. For instance, when performing anti-
phase coupling, all subjects of the TA group switched to
the synchronous ECR-TA activation (SYNCH group) by
stiffening the foot (see Fig 6d). Also three children from
the ECR group switched to the SYNCH group, but in
this case by stiffening the hand (Fig. 6e). In all other
subjects of the ECR group stiffening was insufficient to
equalise the biomechanical properties of the hand to
those of the foot. Thus they continued to advance the ECR
activation also during anti-phase coupling. The same be-
haviour was found in normal adults (see Baldissera et al.
2000 and cf. Fig. 6f).
The neural controller
Most of the children easily performed the in-phase cou-
pling but it was very hard for them, or even impossible,
to accomplish the anti-phase task. Similarly to what hap-
pens in children, both hemiplegic patients tested on the
unaffected side (Baldissera et al. 1994) and a split-brain
subject (Baldissera et al. 1995) showed great difficulty,
or inability, in performing anti-phase movements. How-
ever, differently from patients, children were able to de-
velop, both during in-phase and anti-phase coupling, a
proper EMG anticipation so to compensate for the differ-
ent mechanical properties of the two segments and thus
maintain their oscillation in a tight synchronism. These
findings indicate that integrity of both hemispheres and
completeness of their interconnections is needed to con-
trol the movement in phase-opposition.
When comparing these last results with the children’s
behaviour, it may be argued that the children’s difficul-
ties in performing anti-phase coupling may be related to
the incomplete maturation of the interhemispheric con-
nections. This view is supported by several anatomical
studies showing that growth and myelinisation of the
corpus callosum is not completed until the end of the
second decade of life (Yakovlev and Lecours 1967; Pujol
et al. 1993) and that the number of fibres of the hemi-
spheric white matter, and their diameter, continue to in-
crease beyond the first decade of life (Scammon 1933),
but this conclusion does not exclude that other brain
structures take part in the phase-control of hand-foot
coupling. For instance, it was found that cerebellar le-
sions disrupt both in-phase and anti-phase coupling of
the hand and the foot (Cavallari 2001) and patients suf-
fering from Parkinson’s disease show difficulties in con-
trolling anti-phase movements of the upper and lower
limb (Serrien et al. 2000).
Although the present results do not allow any firm
conclusion about the identity, the characteristics and the
mechanism of action of the anti-phase neural controller,
the fact that some of the youngest children can easily
408
synchronise in-phase oscillations up to 1.8 Hz, while
they are unable to perform anti-phase oscillations, indi-
cates that the two types of coupling are controlled by dif-
ferent neural structures with different maturation times.
Absence of gender differences
Adult subjects showed a clear-cut gender difference in
the pattern of activation of hand and foot movers when
performing coupled movements of the hand and foot
(Baldissera et al. 2000). In particular, the limbs frequen-
cy-responses showed that during in-phase oscillations
the masculine and feminine feet shared similar mechani-
cal properties, while in the hand the K/M ratio was sig-
nificantly lower in males than in females. Correspond-
ingly, movement synchrony was obtained by a larger
phase advance of ECR on TA EMGs in males than in fe-
males. During anti-phase coupling, a change in the vis-
coelastic properties of the hand occurred in both genders,
which reduced the differences between the hand and foot
frequency-responses as well as between the EMG onsets
of the hand and foot movers. In males, however, the
ECR-TA anticipation still remained large.
When the present population of children was divided
according to gender, no significant difference was ob-
served either in the maximal frequency of oscillations or
in the movement synchrony. This suggests that before
puberty the biomechanical characteristics of the hand
and the foot are similar and change in parallel in the two
genders. However, this point cannot be further discussed
since studies on the development of the biomechanical
characteristics of hand and foot are scanty and data un-
certain (see Jensen 1993).
Acknowledgements This study was supported by grants from the
“Ministero della Università e della Ricerca Scientifica e Tecnolo-
gica” and from the “Università degli Studi di Milano”.
References
Baldissera F, Cavallari P (2001) Neural compensation for mechan-
ical loading of the hand during coupled oscillations of the
hand and foot. Exp Brain Res 139:18–29
Baldissera F, Cavallari P, Civaschi P (1982) Preferential coupling
between voluntary movements of ipsilateral limbs. Neurosci
Lett 34:95–100
Baldissera F, Cavallari P, Marini G, Tassone G (1990) Differential
control of in-phase and anti-phase coupling of rhythmic move-
ments of ipsilateral hand and foot. Exp Brain Res 83:375–380
Baldissera F, Cavallari P, Tesio L (1994) Coordination of cyclic
coupled movements of hand and foot in normal subjects and
on the healthy side of hemiplegic patients. In: Swinnen S,
Heuer H, Massion J, Casaer P (eds) Interlimb coordination:
neural, dynamical and cognitive constraints. Academic Press,
San Diego, pp 229–242
Baldissera F, Cavallari P, Locatelli M (1995) Associated move-
ments of ipsilateral hand and foot in a split-brain subject. Eur J
Physiol Pflügers Arch 431:R58
Baldissera F, Cavallari P, Borroni P (2000) Neural compensation for
mechanical differences between hand and foot during coupled
oscillations of the two segments. Exp Brain Res 133:165–177
Bawa P (1981) Neural development in children: a neurophysiolog-
ical study. Elecroenceph Clin Neurophysiol 52:249–256
Berger W, Quintern J, Dietz W (1987) Afferent and efferent con-
trol of stance and gait: developmental changes in children.
Elecroencephalogr Clin Neurophysiol 66:244–252
Blank R, Miller V, Hoss H von, Kries R von (1999) Effects of age
on distally and proximally generated drawing movements: a
kinematic analysis of school children and adults. Dev Med
Child Neurol 41:592–596
Cai F, Zhang J (1997) Study on nerve conduction and late respons-
es in normal Chinese infants, children and adults. J Child Neu-
rol 12:13–18
Carson RG, Goodman D, Kelso JAS, Elliott D (1995) Phase tran-
sitions and critical fluctuations in rhythmic coordination of ip-
silateral hand and foot. J Motor Behav 27:211–224
Cavallari P (2001) Cerebellar control of associated movements in
man. Eur J Physiol 442:R7
Ehrsson HH, Naito E, Geyer S, Amounts K, Zilles K, Forssberg
H, Roland PE (2000) Simultaneous movements of upper and
lower limbs are coordinated by motor representations that are
shared by both limbs: a PET study. Eur J Neurosci 12:3385–
3398
Eyre JA, Miller S, Ramesh V (1991) Constancy of central conduc-
tion delay during development in man: investigation of motor
and somatosensory pathways. J Physiol 434:441–452
Fietzek UM, Heinen F, Berweck S, Maute S, Hufschmidt A,
Schulte-Monting J, Lucking CH, Korinthenberg R (2000) De-
velopment of the corticospinal system and hand motor func-
tion: central conduction times and motor performance tests.
Dev Med Child Neurol 42:220–227
Haas G, Diener HC, Backer M, Dichgans J (1986) Development
of postural control in children: short-, medium-, and long-
latency EMG responses of leg muscles after perturbation of
stance. Exp Brain Res 64:127–132
Jensen RK (1993) Human morphology: its role in the mechanics
of movement. J Biomech 26:81–94
Jensen RK, Nassas G (1988) Growth of segment principal mo-
ments of inertia between four and twenty years. Med Sci
Sports Exer 20:594–604
Kelso JAS (1984) Phase transitions and critical behaviour in hu-
man bimanual coordination. Am J Physiol 246: R1000–R1004
Lauffer H, Wenzel D (1986) Maturation of central somatosensory
conduction time in infancy and childhood. Neuropediatrics
17:72–74
Lin JP, Brown JK, Walsh EG (1996) The maturation of motor dex-
terity: or why Johnny can’t go any faster. Dev Med Child Neu-
rol 38:244–254
Meige H (1901) Les mouvements en mirroir: leurs applications
pratiques et thérapeutiques. Rev Neurol 19:780
Müller K, Hömberg V (1992) Development of speed of repetitive
movements in children is determined by structural changes in
corticospinal efferents. Neurosci Lett 144:57–60
Müller K, Hömberg V, Lenard HG (1991a) Magnetic stimulation
of motor cortex and nerve roots in children. Maturation of cor-
tico-motoneuronal projections. Elecroencephalogr Clin Neuro-
physiol 81:63–70
Müller K, Hömberg V, Coppenrath P, Lenard HG (1991b) Matura-
tion of lower extremity EMG responses to postural perturba-
tion: relationship of response-latencies to development of fast-
est central and peripheral efferents. Exp Brain Res 84:444–452
Müller K, Ebner B, Hömberg V (1994) Maturation of fastest affer-
ent and efferent central and peripheral pathways: no evidence
for a constancy of central conduction delays. Neurosci Lett
166:9–12
Nezu A, Kimura S, Uehara S, Kobayashi T, Miyabi T, Saito K
(1997) Magnetic stimulation of the motor cortex in children:
maturity of corticospinal pathway and problem of clinical ap-
plication. Brain Dev 19:176–180
Pujol J, Vendrell P, Junqué C, Martí-Vilalta JL, Capdevila A
(1993) When does human brain development end? Evidence
of corpus callosum growth up to adulthood. Ann Neurol 34:
71–75

Rowlandson PH, Stephens JA (1985) Maturation of cutaneous re-
flex responses recorded in the lower limb in man. Dev Med
Child Neurol 27:425–433
Scammon RE (1933) Growth and development of the child. Part
II: anatomy and physiology. The central nervous system. In:
White House conference on child health and protection. Cen-
tury, New York, pp 176–190
Serrien DJ, Steyvers M, Debaere F, Stelmach GE, Swinnen SP
(2000) Bimanual coordination and limb-specific parametrizat-
ion in patients with Parkinson’s disease. Neuropsychologia
38:1714–1722
View publication stats
409
Swinnen SP, Dounskaia N, Verschueren S, Serrien DJ, Daelman A
(1995) Relative phase destabilisation during interlimb coordi-
nation: The disruptive role of kinaesthetic afferences induced
by passive movement. Exp Brain Res 105:439–454
Yacovlev PI, Lecours AR (1967) The myelogenetic cycles of re-
gional maturation of the brain. In: Minkovski A (ed) Regional
development of the brain in early life. Blackwell Scientific
Publication, Oxford, pp 3–70