J Neurophysiol 94: 754 –763, 2005.
First published February 23, 2005; doi:10.1152/jn.00088.2005.
Kinematics in Newly Walking Toddlers Does Not Depend Upon
Postural Stability
Yuri P. Ivanenko,1 Nadia Dominici,1,2 Germana Cappellini,1 and Francesco Lacquaniti1,2,3
1
Department of Neuromotor Physiology, IRCCS Fondazione Santa Lucia, Rome; 2Department of Neuroscience, University of Rome Tor
Vergata; and 3Centre of Space Biomedicine, University of Rome Tor Vergata, Rome, Italy
Submitted 24 January 2005; accepted in final form 17 February 2005
Ivanenko, Yuri P., Nadia Dominici, Germana Cappellini, and
Francesco Lacquaniti. Kinematics in newly walking toddlers does
not depend upon postural stability. J Neurophysiol 94: 754 –763,
2005. First published February 23, 2005; doi:10.1152/jn.00088.2005.
When a toddler starts to walk without support, gait kinematics and
electromyographic (EMG) activity differ from those of older children
and the body displays considerable oscillations due to poor equilibrium. Postural instability clearly affects motor patterns in adults, but
does instability explain why toddlers walk with a different gait? Here
we addressed this question by comparing kinematics and EMGs in
toddlers performing their first independent steps with or without hand
or trunk support. Hand support significantly improved postural stability and some general gait parameters, reducing percent of falls, step
width, lateral hip deviations and trunk oscillations. However, the
kinematic and EMG patterns were unaffected by increased postural
stability. In particular, the co-variance of the angular motion of the
lower limb segments, the pattern of bilateral coordination of the
vertical movement of the two hip joints, high variability of the foot
path, the elliptic or single peak trajectory of the foot in the swing
phase, and characteristic EMG bursts at foot contact remained idiosyncratic of toddler locomotion. Instead the toddler pattern shared
fundamental features with adult stepping in place, suggesting that
toddlers implement a mixed locomotor strategy, combining forward
progression with elements of stepping in place. Furthermore, gait
kinematics remained basically unchanged until the occurrence of the
first unsupported steps and rapidly matured thereafter. We conclude
that idiosyncratic features in newly walking toddlers do not simply
result from undeveloped balance control but may represent an innate
kinematic template of stepping.
In contrast with humans, many animal species can stand and
walk within hours after birth. To deal with an inherently
unstable upright posture, bipedal human locomotion involves a
significant dependence on descending pathways (Capaday
2002; Ivanenko et al. 2000; Orlovsky et al. 1999) that are not
mature in infants at the age of 1 yr (Paus et al. 1999). One
oft-cited hypothesis is that “what allows the infant to begin to
walk independently at the end of the first year is not necessarily
maturation of the stepping pattern but instead maturation of the
system that enables successful balance control” (Pearson and
Gordon 2000). Indeed, when supported, infants can step long
before the time of the onset of independent walking (Forssberg
1985; Thelen and Cooke 1987; Yang et al. 1998; Zelazo 1983)
at a speed modulated by peripheral sensory inputs, in different
directions (forward, backward, sideways), and with appropriate
coordinated behavior in response to external perturbations
(Lam et al. 2003; Lamb and Yang 2000; Pang and Yang 2001).
Nevertheless, the question remains as to what extent immaturity of gait kinematics in toddlers is due to postural instability
as opposed to immaturity of the generating networks. Few
previous studies have dealt with the effects of postural stability
on the development of walking and these have reported mainly
the degree of variability in joint rotations or various phase
characteristics (Clark et al. 1988; Lasko-McCarthey et al.
1990). However, direct quantitative demonstration of the effect
of posture-stabilizing maneuvers on the global aspects of the
toddler’s gait, such as the inverted pendulum mechanism of
walking (Cavagna et al. 1983), planar co-variance of the
angular motion of the lower limb segments (Lacquaniti et al.
1999, 2002) or foot trajectory control (Ivanenko et al. 2002), is
lacking.
When children start to walk without support, their bodies
display considerable oscillations in different directions revealing postural instability (Assaiante et al. 1993; Bril and Brenière
1993; Yaguramaki and Kimura 2002). Postural instability in
turn might affect the state of the control system, change
reliance on vestibular (Fitzpatrick et al. 1994) or proprioceptive (Ivanenko et al. 1999) sensory cues, and strengthen participation of the cortical motor areas in equilibrium maintenance (Ouchi et al. 1999; Solopova et al. 2003). Therefore
equilibrium instabilities could reorganize a coordination pattern and augment kinematic variability in walking toddlers as
occurs in adults under unstable walking conditions (Cham and
Redfern 2002; Lejeune et al. 1998; Menz et al. 2003). Subjects
with a high risk of falling typically exhibit reduced temporospatial gait parameters and increased step timing variability,
the features typical for toddlers. Moreover, drastic changes in
lower extremity behavior might occur even when there is a
perceived potential risk of falls (Cham and Redfern 2002).
Therefore one can expect that postural instability represents a
perturbing factor that changes the state of the control system
and prevents the expression of the mature coordination pattern
in toddlers.
Here we tested this hypothesis by attempting to stabilize the
child’s body and thus give the toddlers greater confidence in
walking. In adults, hand contact with an external surface results
in a significant decrease of trunk and limb segment oscillations
when posture is unstable (Dickstein and Laufer 2004; Ivanenko
et al. 1999; Jeka and Lackner 1994). In toddlers, hand support
represents a common strategy used by the parent to prevent the
Address for reprint requests and other correspondence: Y. P. Ivanenko,
Dept. of Neuromotor Physiology, IRCCS Fondazione Santa Lucia, via
Ardeatina 306, 00179 Rome, Italy (E-mail: y.ivanenko@hsantalucia.it).
The costs of publication of this article were defrayed in part by the payment
of page charges. The article must therefore be hereby marked “advertisement”
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
INTRODUCTION
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FIRST STEPS IN TODDLERS
child’s falls. We used a similar approach to increase postural
stability in toddlers who were just beginning to walk independently. We also recorded walking at different speeds in adults
(including stepping in place) and older children to highlight
common kinematic principles that might be responsible for
shaping the toddler’s gait. To compare kinematic patterns, we
used the methods developed earlier for adult’s gait (Bianchi et
al. 1998; Borghese et al. 1996; Ivanenko et al. 2002). The
results show that at the moment of transition to independent
walking, immaturity of inter-segmental coordination and high
foot trajectory variability do not depend on postural imbalance.
Instead, our data suggest that a few months of unsupported
locomotion experience are apparently necessary for calibration
of the innate stepping mechanics to the unconstrained walking
conditions. We also argue that the precursor of the mature
kinematic pattern consists of a locomotor strategy combining
forward progression with elements of stepping in place.
METHODS
Subjects
We recorded surface locomotion in 7 toddlers (3 males, 4 females,
12–15 mo of age), 7 older children (2–7 yr old), and 10 healthy adults
[5 females and 5 males, 28 ⫾ 7 (SD) years old]. Informed consent was
obtained from all the adults and from the parents of the children. The
procedures were approved by the ethics committee of the Santa Lucia
Institute and conformed with the Declaration of Helsinki. The laboratory setting and the experimental procedures were adapted to the
children so as to result in absent or minimal risk, equal or lower to that
of walking at home. Both a parent and an experimenter remained
along side the younger children to prevent them from hurting themselves during falls. For the toddlers, daily recording sessions were
programmed around the parents’ expectation of the very first day of
independent walking until unsupported locomotion was recorded.
Walking conditions
For the recording of the very first
steps, one parent initially held the toddler by hand. Then the parent
started to move forward, leaving the toddler’s hand and encouraging
her or him to walk unsupported on the floor. For each subject, ⬃10
trials were recorded under similar conditions. Short trials (ⱕ3 min,
depending on endurance and tolerance) were recorded with rest breaks
in between. Only sequences of steps executed naturally by the toddler
(e.g., no stop between steps) and while looking forward, were considered to avoid initiation and braking phases and head movements
due to looking in other directions. The mean walking speed in toddlers
was 1.4 ⫾ 0.7 km/h. Adult subjects were asked to walk at a natural,
freely chosen speed (on average, 3.8 ⫾ 0.4 km/h) and at lower speeds
in additional trials and to step in place. Typically, we analyzed two to
five consecutive step cycles in each trial for toddlers, older children,
and adults.
WALKING WITHOUT SUPPORT.
One hand of the child was held in
the hand of a parent, while the other parent (or an experimenter)
encouraged the child to walk straight ahead. This condition was
recorded in all seven toddlers and older children.
WALKING WITH HAND CONTACT.
As an alternative way to reduce
the effects of postural instability on lower limb kinematics, in four
toddlers, additional trials were recorded while an experimenter (or a
parent) firmly held the trunk of the child with both hands and supplied
only limited vertical force (typically ⬍20 –30% of the body weight, as
estimated from the mean vertical force on the platform) during
stepping attempts.
WALKING WITH TRUNK SUPPORT.
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Supported steps of four toddlers (2 males and 2 females) were also
recorded between 1.5 and 4 mo before the onset of unsupported
walking as well as after this event to follow the early gait maturation.
The infants walked firmly supported by one or both hands of one of
their parents.
WALKING BEFORE THE ONSET OF UNSUPPORTED LOCOMOTION.
Data recording
Bilateral kinematics of locomotion was recorded at a digitizing rate
of 100 Hz by means of the VICON-612 motion analysis system
(Oxford, UK). The positions of selected points on the body were
recorded by attaching passive infrared reflective markers (diameter:
1.4 cm) to the skin overlying the following bony landmarks on both
sides of the body: gleno-humeral joint (GH), the tubercle of the
anterosuperior iliac crest (IL), greater trochanter (GT), lateral femur
epicondyle (LE), lateral malleolus (LM), and fifth metatarso-phalangeal joint (VM).
In children and in adults at low speeds, the ground reaction forces
under both feet were recorded at 1,000 Hz by a force platform (0.9 ⫻
0.6 m, Kistler 9287B, Zurich, Switzerland). Toddlers generally performed two to three steps on the force platform in each trial. At
natural, higher speeds in adults, the ground reaction forces under each
foot were recorded separately by means of two force platforms (0.6 ⫻
0.4 m, Kistler 9281B), spaced by 0.2 m between each other in both the
longitudinal and the lateral direction.
Electromyographic (EMG) activity was recorded by means of
surface electrodes from the rectus femoris (RF), hamstring (HS),
tibialis anterior (TA), and soleus-gastrocnemius (GC) muscles. EMG
signals were preconditioned at the recording site (active electrodes
from BTS, Milan, Italy or DelSys, Boston, MA), transmitted to the
remote amplifier (bandwidth was 20 –200 Hz), and sampled at 1,000
Hz. Some crosstalk from nearby muscles is inevitable in tiny limbs of
young infants. Nevertheless, due to the low skin impedance and
preconditioning at the recording site, no artifacts appeared due to
movement of electrode cables and cross talk from the antagonistic
muscles seems to be limited (Forssberg 1985; Okamoto et al. 2003;
Sundermier et al. 2001). Sampling of kinematic, kinetic, and EMG
data was synchronized.
Data analysis
We analyzed and separately presented the effect of support on
postural stability and general gait characteristics (such as walking
speed, percent of falls, step length and width, trunk oscillations) and
on the kinematic patterns of walking (intersegmental coordination,
EMG patterns, and foot trajectory control).
Deviations of gait trajectory relative to the x direction of the
recording system were corrected by rotating the xz axes by the angle
of drift computed between start and end of the trajectory. The body
was modeled as an interconnected chain of rigid segments: GH-IL for
the trunk, IL-GT for the pelvis, GT-LE for the thigh, LE-LM for the
shank, and LM-VM for the foot. The main limb axis was defined as
GT-LM. The elevation angle of each segment corresponds to the angle
between the segment projected on the sagittal plane and the vertical
(positive in the forward direction, i.e., when the distal marker falls
anterior to the proximal one).
To evaluate trunk stability with respect to the vertical axis, we
measured the peak-to-peak angular deviation of the long axis of the
trunk in both sagittal and frontal planes. The long axis of the trunk was
defined by connecting the midpoint of the two (left and right) IL
markers with the midpoint of the two GH markers. Percent of falls
was computed as the number of trials in which the toddlers fell
divided by the total number of recording trials. Walking speed was
measured by computing the mean velocity of the horizontal IL marker
movement. The length of the lower limb (L) was measured as thigh
(GT-LE) plus shank (LE-LM) length.
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Y. P. IVANENKO, N. DOMINICI, G. CAPPELLINI, AND F. LACQUANITI
Gait cycle duration was defined as the time interval between two
successive maxima of the elevation angle of the main limb axis of the
same limb and stance phase as the time interval between the maximum and minimum values of the same angle (Borghese et al. 1996).
Thus a gait cycle (stride) referred to a cyclic movement of one leg and
equaled two steps. When subjects stepped on the force platforms,
these kinematic criteria were verified by comparison with foot strike
and lift-off measured from the changes of the vertical force around a
fixed threshold. In general, the difference between the time events
measured from kinematics and kinetics was ⬍3%. However, the
kinematic criterion sometimes produced a significant error in the
identification of stance onset in toddlers if there was an unusual
forward foot overshoot at the end of swing (cf. Forssberg 1985). In
such cases, foot contact was determined using a relative amplitude
criterion for the vertical displacement of the VM marker (when it was
elevated to 7% of the limb length from the floor).
Raw EMG data were numerically high-pass filtered (cutoff: 30 Hz)
to remove motion artifacts, rectified and then low-pass filtered with a
zero-lag Butterworth filter (cutoff: 15 Hz). Data from several steps
were ensemble-averaged after time-interpolation over individual gait
cycles to a normalized 200-point time base.
The time-varying coordinates of the center of pressure (CoP) were
derived from the force plate measurements. Step length (variation of
CoPx between 2 foot contacts with the floor) and width (variation of
CoPy) were calculated from the force plate data (Ledebt and Bril
2000) and normalized to the limb length. Duration of the single
support phase (i.e., time of the step spent with only 1 foot on the
ground) was normalized with respect to the duration of the step.
Ensemble averages with SD of kinematic variables were computed
at each point of the normalized time base. The mean SD values were
computed to characterize deviations of the individual step traces from
the ensemble average.
Intersegmental coordination
The intersegmental coordination was evaluated in position space as
previously described (Bianchi et al. 1998; Borghese et al. 1996). In
adults, the temporal changes of the elevation angles at the thigh,
shank, and foot co-vary during walking. When these angles are plotted
one versus the others in a three-dimensional graph, they describe a
path that can be fitted (in the least-square sense) by a plane over each
gait cycle. Here, we studied the development of the gait loop and its
associated plane in children. To this end, we computed the covariance
matrix of the ensemble of time-varying elevation angles (after subtraction of their mean value) over each gait cycle. The three eigenvectors u1– u3, rank ordered on the basis of the corresponding eigenvalues, correspond to the orthogonal directions of maximum variance
in the sample scatter. For each eigenvector, the parameters uit, uis, and
uif correspond to the direction cosines with the positive semi-axis of
the thigh, shank, and foot angular coordinates, respectively. The first
two eigenvectors u1–u2 lie on the best-fitting plane of angular covariation. The third eigenvector (u3) is the normal to the plane and
defines the plane orientation.
Foot trajectory
The shape of the endpoint path was compared by computing the
vertical excursion of the VM marker (during swing) and correlating it
with the corresponding ensemble average in adults. VM trajectories
were time-normalized over the swing phase duration.
Foot-trajectory variability
Foot-trajectory spatial variability in the sagittal plane was quantified in terms of spatial density and normalized tolerance area of VM,
computed over the swing phase (Ivanenko et al. 2002). These indices
describe the integrated variability of foot path, including variability in
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both the vertical and horizontal directions. To compare subjects of
different heights, VM trajectories (relative to the instantaneous position of GT) were first scaled by the limb length (in proportion to the
mean limb length of adults) and then re-sampled in the space domain
by means of linear interpolation of the x,y time series (1.5-mm steps)
over all gait cycles. All steps (typically 7–15) from different trials
under the same walking conditions were pooled together for this
analysis.
Spatial density was calculated as the number of points falling in
1 ⫻ 1 cm2 cells of the spatial grid divided by the number of step
cycles. The density of each cell was depicted graphically by means of
a color scale (empty cells were excluded): the lower the density
(toward the blue in the color-cued scale), the greater the variability.
Normalized tolerance area was derived as follows. The mean length of
foot trajectory over the swing phase across all steps was calculated
from the corresponding path integral. For every interval corresponding to 10% of the maximal horizontal excursion, we computed the
two-dimensional 95%-tolerance ellipsis of the points within the interval. The typical number of points in each interval ranged from 500 to
1,200 (depending on the number of gait cycles). The areas of all
tolerance ellipses were summed and normalized by the mean length of
foot trajectory. This normalized area provides an estimate of the mean
area covered by the points along 1 cm of path. A greater tolerance area
indicates greater variability.
Statistics
Statistical analyses (Student’s t-test) were used when appropriate.
Reported results are considered significant for P ⬍ 0.05. Statistics on
correlation coefficients was performed on the normally distributed,
Z-transformed values. Spherical statistics on directional data were
used to characterize the mean orientation of the normal to the
co-variation plane (see preceding text) and its variability across steps.
To assess the variability, we calculated the angular SD (called spherical angular dispersion) of the normal to the plane.
RESULTS
Effect of hand contact on postural stability and general
gait characteristics
When children start to walk without support, their bodies
display considerable oscillations due to postural instability:
peak-to-peak sway of the trunk was 14.1 ⫾ 3.4° in the sagittal
plane and 9.5 ⫾ 1.9° in the frontal plane, both values being
significantly (P ⬍ 10⫺5) higher than in adults (6.2 ⫾ 0.8 and
2.7 ⫾ 0.6°, respectively). As a rule, toddlers take relatively few
steps and readily fall. Percent of falls in the children was
relatively large (37 ⫾ 23% in the recording trials).
At the onset of unaided walking, general gait parameters
display high variability. There are considerable variable lateral
trunk displacements (both GT and GH markers, Fig. 1B, left).
To minimize disequilibrium, toddlers take short steps with a
wide base of support and a prolonged time in double support
(Fig. 2A) (see also Bril and Brenière 1993). The walking speed
freely chosen by toddlers was considerably lower than in adults
or in older children when expressed in dynamically equivalent
terms—Froude number (Fr ⫽ V2g⫺1L⫺1, where V is the
average speed of locomotion, g the acceleration of gravity, and
L the limb length). The Froude number is a dimension-less
parameter suitable for the comparison of locomotion in subjects of different size walking at different speeds, under the
assumption of the gravity-related pendulum mechanism of
movement (Cavagna et al. 1983). Fr was 0.04 ⫾ 0.03 in
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FIRST STEPS IN TODDLERS
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without, where L is the limb length; Fig. 2A, right). Finally,
percent of falls in these supported trials decreased drastically
(7 ⫾ 6%, Fig. 2A, left).
In summary, hand contact had a strong impact on general
characteristics of infant’s stepping (Fig. 2A). The same hand
holding procedure in older children did not show any significant influence on these parameters (Fig. 2B).
Kinematic patterns of walking with and without hand contact
FIG. 1. An example of unsupported and supported walking. A: unilateral
sagittal stick diagrams when the toddler walked unsupported (left) and with the
hand held in the hand of a parent (right). B: superimposed trajectories of the
right gleno-humeral (GH) and greater trochanter (GT) markers across 10 steps
(after subtracting the mean values) in the horizontal plane for unsupported
(left) and supported walking (right).
toddlers versus 0.21 ⫾ 0.08 in adults and 0.23 ⫾ 0.03 in older
children (Fig. 2, A and B).
To improve postural stability, in a series of trials the child
walked with a hand lightly held by the hand of one parent. The
procedure resulted in minimal additional contact forces but
gave the toddlers greater confidence in walking than without
hand contact (as shown by their increased willingness to walk
in the laboratory). In contrast to older children (Fig. 2B), the
step length and the walking speed increased significantly and
the step width decreased when walking with hand contact (Fig.
2A). The relative duration of the single support phase increased
slightly but significantly in all toddlers. Trunk oscillations were
significantly reduced: the reduction of sway in the sagittal
plane amounted to 25% on average (Fig. 2A). Variability in the
mediolateral GT oscillations, estimated as the mean SD from
the ensemble averaged GTz waveform, was also reduced (being 0.041 ⫾ 0.005 L with hand contact and 0.052 ⫾ 0.009 L
One question addressed in this study is whether postural
instability represents a major factor inhibiting the expression of
the mature stepping pattern in toddlers. To this end, we
compared the kinematics of unaided unstable stepping with
that of supported walking. Figure 3 shows a typical example of
a stepping pattern in one adult and one toddler at the beginning
of independent walking. Various general gait features are
described in this figure.
First, in adults, the temporal changes of the elevation angles
of lower limb segments co-vary along a plane, describing a
characteristic loop over each stride (Fig. 3A, far right). In
toddlers, the gait loop departed significantly from planarity and
the mature pattern. Planarity was quantified by the percentage
of variance accounted for by the third eigenvector (PV3) of the
data covariance matrix: the closer PV3 is to 0, the smaller the
deviation from planarity. PV3 was significantly higher in toddlers (3.1 ⫾ 0.7%) than in adults (0.8 ⫾ 0.3%, P ⬍ 0.001
Student’s unpaired t-test), in agreement with previous findings
(Cheron et al. 2001b). Also because the amplitude of thigh
movements was relatively higher with respect to that of shank
and foot movements in toddlers, the gait loop was less elongated than in adults, as shown by the smaller contribution of
the first eigenvector (PV1). Moreover, the step-by-step variability of plane orientation (estimated as the angular dispersion
of the plane normal) was considerably higher in toddlers
(16.1 ⫾ 2.4°) than in adults (2.9 ⫾ 1.0). In toddlers, neither the
percent of variance PV1, PV2, and PV3, nor the orientation of
the co-variation plane changed significantly across the two
postural support conditions (Fig. 4A, right). Furthermore, the
2 ⫺1 ⫺1
FIG. 2. Effect of hand contact on global gait parameters. Left to right: percent of falls, normalized walking speed (Froude number ⫽ V g L ), step length,
step width, relative single support phase duration, peak-to-peak pitch trunk oscillations, and variability in the lateral displacement of GT across 10 steps
(estimated as the mean SD from the ensemble average). Step length, step width, and GTz lateral variability were normalized by the limb length to provide
comparisons between children of different sizes. All parameters were significantly different in toddlers during walking with hand contact vs. unsupported
walking. Older children (B) never fell during the test.
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Y. P. IVANENKO, N. DOMINICI, G. CAPPELLINI, AND F. LACQUANITI
FIG. 3. An example of lower limb kinematics and
electromyographic (EMG) activity in 1 toddler and in a
representative adult. A, top to bottom: stick diagrams of 1
cycle (swing phase is in red), stick diagrams during swing
relative to the instantaneous hip position, ensemble averages (⫾SD, n ⫽ 5 steps) of vertical hip displacement
(GTy), vertical foot displacement (VMy), thigh, shank,
and foot elevation angles and corresponding 3-dimensional gait loops. Data are plotted vs. the normalized gait
cycle. GTy and VMy are expressed in relative units
(normalized by the limb length L). A loop is obtained by
plotting the thigh waveform vs. shank and foot waveforms (after subtracting mean values). Paths progress in
time in the counter-clockwise direction, foot strike and
lift-off corresponding approximately to the top and bottom of the loop, respectively. The interpolation planes
result from orthogonal planar regression. B: ensemble
averaged (across 5 steps) EMG activity. C: plots of spatial
density of VM path. Spatial density was integrated over
the swing phase (across 10 –15 steps): the lower the
density (toward the blue in the color-cued scale), the
greater the variability. Plots are anisotropic, vertical scale
being expanded relative to horizontal scale. Note that
density is roughly comparable in all support conditions in
the toddler, whereas it is much higher in the adult.
step-by-step variability of plane orientation remained unchanged (15.0 ⫾ 2.8° with hand contact and 16.1 ⫾ 2.4°
without) reflecting a high degree of instability in the phase
relationship between limb segments.
Second, in walking adults, the hip vaults over the stance
leg as an inverted pendulum. As a result, we found two
peaks in the temporal profile of vertical hip position (GTy
and ILy) over each gait cycle, in coincidence with midstance of the right and left leg, respectively (Fig. 3A, right).
Fourier series expansion of GTy revealed a clear dominance
of the second harmonic: the percent of GTy variance explained was 13 ⫾ 7 and 80 ⫾ 7% for the first and second
harmonic, respectively. In toddlers, GTy oscillations were
variable from step to step. Their mean profile systematically
differed from that of the adults. Thus independent of support
conditions, the first peak in the adult GTy (corresponding to
the stance phase of the ipsilateral leg) was often absent in
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toddlers (Fig. 3A). Instead, toddler GTy activity typically
exhibited a peak corresponding to the second peak of the
adult GTy profile, and reflected a lift of the hip joint during
swing relative to the contra-lateral hip joint of the loadbearing leg. This behavior was observed both during bilateral kinematic recordings and in the motion of the IL
markers. Therefore we can exclude the possibility that the
toddler GTy peak originates from a misplacement of the GT
marker relative to the center of joint rotation. In toddlers,
the percent of GTy variance explained by the first and
second harmonic was 56 ⫾ 9 and 23 ⫾ 5%, respectively,
indicating a dominance of the first harmonic (Fig. 4B). A
lack of the pendulum behavior of the hip in toddlers was
conserved across support conditions. Thus over the 0.07–
0.20 range of Fr values, the percent of variance explained
by the second harmonic of GTy was 27 ⫾ 7% with hand
contact and 23 ⫾ 5% without (P ⬎ 0.7 in all cases).
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FIRST STEPS IN TODDLERS
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FIG. 4. Effect of hand contact on lower
limb kinematics in toddlers and older children.
Left: percent of variance (⫾SD) of GTy data
explained by the 2nd Fourier harmonic. The
values for the adult group were obtained by
computing the mean (⫾SD) from the pooled
data obtained for walking at natural, freely
chosen speed (on average, 3.8 ⫾ 0.4 km/h).
Second panel: correlation coefficient between
VMy data in toddlers and the corresponding
ensemble average in adults during swing.
Third panel: normalized VM tolerance area
during swing. Fourth panel: planar co-variance for the thigh-shank-foot loops: percentage
of variance accounted for by eigenvectors
u1–u3 (PV1, PV2, PV3 respectively). The 1st
eigenvector (u1) is aligned with the long axis
of the gait loops of Fig. 3, the 2nd eigenvector
(u2) is aligned with the short axis, and the 3rd
eigenvector (u3) is the normal to the plane.
Right: direction cosines of the plane normal
with the positive semi-axis of the thigh, shank,
and foot angular coordinates (u3t, u3s, and u3f).
All parameters presented in this figure were
not significantly different in toddlers during
walking with hand contact.
Third, foot trajectory characteristics differed systematically
in toddlers as compared with those in adults. The dominant
template of the foot motion is illustrated in the stick diagram of
Fig. 3A (left). All toddlers moved the leg in such a way that the
foot lift had only one maximum at midswing. Often, the toe
reached its maximal height in front of the body at the end of
swing. This behavior was entirely opposite to that observed in
the typical adult gait, which was characterized by prominent
foot lift in early swing, a minimum foot clearance during
midswing, and another separate toe lift at the end of swing
(Fig. 3A, right). As a result, the correlation coefficient between
the time series of the VMy during swing in toddlers and the
corresponding ensemble average in adults was typically negative (⫺0.59 ⫾ 0.22). The spatial variability of the endpoint
(foot) path in the sagittal plane was considerably greater than
in the adults (Fig. 3C): the normalized tolerance area (scaled to
the mean limb length of adults) was 20.7 ⫾ 3.1 cm2/cm in
toddlers and 4.8 ⫾ 1.9 cm2/cm in adults (P ⬍ 0.0001, Student’s unpaired t-test). Hand contact did not influence appreciably the shape (Fig. 3A) and spatial variability (Fig. 3C) of
the endpoint path. The correlation coefficient between VMy in
toddlers and adults remained negative (⫺0.55 ⫾ 0.20). The
VM tolerance area remained high (17.9 ⫾ 4.6 cm2/cm).
Finally, EMG activity in toddlers was variable across steps
due to augmented step-by-step variability in the kinematics and
in the speed of progression, though it comprised many features
of adult gait. Nonplantigrade gait and foot placements were
often accompanied by an atypical burst of activity in the
gastrocnemius muscle at foot touchdown (Fig. 3B) (see also
Forssberg et al. 1985; Okamoto et al. 2003), this burst was
never observed in adults. The mean level of activation of leg
muscles did not change significantly with hand contact. In the
hand contact condition, the TA, GC, HS, and RF activity was
22 ⫾ 10, 33 ⫾ 11, 21 ⫾ 10, and 18 ⫾ 14 V; in the
unsupported condition, it was 20 ⫾ 11, 27 ⫾ 10, 20 ⫾ 9, and
16 ⫾ 15 V, respectively. Characteristic EMG bursts at foot
contact were also observed during supported stepping.
J Neurophysiol • VOL
In summary, experimental interventions leading to increased
postural stability and reduced trunk oscillations did not result
in significant amelioration of the kinematic dis-coordination
and EMG patterns in toddlers. Walking with hand contact also
did not affect the kinematics of stepping movements in older
children (Fig. 4B), which remained similar to that of adults
across support conditions.
Effect of trunk support
In four toddlers, we also performed a more drastic maneuver
to stabilize the body during walking. In some trials, an experimenter (or a parent) firmly held the trunk of the child with
both hands while the child stepped. The mean walking speed
(1.3 ⫾ 0.6 km/h) was similar to that during unsupported
stepping (1.4 ⫾ 0.7 km/h). Supporters were instructed to avoid
influencing the toddlers’ forward motion. However, we were
unable to completely control for the possibility that some
aspects of stepping were influenced by external forces generated by the supporter on the toddler’s forward motion. Thus the
movement of the trunk (and in particular the vertical displacement of the hip joint) could not be analyzed reliably due to the
presence of the external support. Nevertheless, leg movements
and EMG activity were comparable to those during unsupported stepping (Fig. 3). The gait loop departed from planarity
and from mature pattern in the two support conditions. The
percent of variance accounted for by the third eigenvector
(planarity, PV3) was 2.5 ⫾ 0.5% during walking with trunk
support and 2.7 ⫾ 0.3° without (sf. 0.8 ⫾ 0.3% in adults). The
step-by-step variability of plane orientation remained high
(13.6 ⫾ 3.6° with trunk support and 15.7 ⫾ 3.2° without). The
correlation coefficient between the time series of the VMy
during swing in toddlers and the corresponding ensemble
average in adults remained negative (⫺0.51 ⫾ 0.15) and the
VM tolerance area remained high (19.2 ⫾ 3.9 cm2/cm with
trunk support and 17.0 ⫾ 5.5 cm2/cm without). In summary,
neither inter-step kinematic variability, nor the index of planarity (PV3), nor the orientation of the plane of angular
co-variation changed significantly (P ⬎ 0.05 in all cases).
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Y. P. IVANENKO, N. DOMINICI, G. CAPPELLINI, AND F. LACQUANITI
Similarities between toddler stepping and marching in place
in adults
Behavior before and after the onset of
unsupported locomotion
Interestingly, the shape of the foot path, bilateral coordination of the two hip joints and EMG patterns in the toddlers
were reminiscent of those observed for stepping in place in the
adults (Fig. 5). The correlation coefficient between the time
series of the vertical foot (VM) displacements during swing in
the toddlers and the ensemble average in the adults for stepping
in place was typically very high and positive (0.92 ⫾ 0.09),
while it was typically negative (⫺0.59 ⫾ 0.22) when comparing with normal adult walking. As in the case of the toddler
gait, GTy oscillations during stepping in place in adults displayed a prominent peak during swing and a tiny peak during
stance (Fig. 5); as a consequence, the percent of GTy variance
explained by the first and second harmonic was 52 ⫾ 22 and
31 ⫾ 13%, respectively.
In additional trials, adults were asked simultaneously to
perform stepping-in-place-like vertical leg movements while
moving slowly forward. The adults executed this task easily
and the kinematics were very similar across adults. Again, in
this task, the VMy and GTy behavior was similar to that of the
toddlers (Fig. 5). Moreover, during stepping in place in adults,
we detected bursts of EMG activity in the calf muscles at foot
touchdown similar to those often observed in toddlers (Fig. 5),
and the HS muscle regularly exhibited activity in the middle of
swing phase. Furthermore, the gait loop during adult stepping
in place dwindled to a line because all three segments moved
in phase. However, when the adults were asked to simultaneously step in place and to move forward, this manipulation
created phase shifts between segment rotations, and the shape of
the gait loop became very similar to that of the toddlers (Fig. 5).
Four infants were tested repeatedly over a period between 4
mo before and 13 mo after the onset of independent walking
(Fig. 6). During the experiments, the infants walked firmly
supported by the hand of one of their parents before they could
walk independently. In all recording sessions performed before
the onset of unsupported locomotion, the pattern of intersegmental coordination, the pendulum-related pattern of vertical hip displacement and foot trajectory characteristics all did
not differ significantly from those recorded at the onset of
unsupported locomotion. The percentage of variance accounted for by the second Fourier harmonic of the vertical GT
displacement (denoting the double-peaked profile of pendular
oscillations of COM) exhibited inter-step variability but did not
change systematically as a function of age up to the time of
onset of unsupported locomotion, when it started to increase
rapidly over the first few months of independent walking
experience (Fig. 6B). A similar trend was exhibited by the time
course of the VMy (Fig. 6D), by the endpoint (VM) spatial
variability (Fig. 6E), by the index of planarity of the gait loop
(PV3, Fig. 6C) and by the step-by-step variability of plane
orientation (angular dispersion of the plane normal, not
shown).
DISCUSSION
There are three main findings in this study: immaturity of
global gait parameters did not depend on postural stability, the
toddler pattern shared fundamental features with adult stepping
in place, and idiosyncratic gait parameters remained basically
FIG. 5. Similarities between the toddler’s gait and steppingin-place in adults. From left to right: normal walking in the
adult, stepping in place in the adult, stepping in place ⫹ linear
translation in the adult, unsupported stepping in the toddler
(swing phase is in red).
J Neurophysiol • VOL
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FIRST STEPS IN TODDLERS
FIG. 6. Behavior before and after the onset of independent walking. A: stick
diagrams of 1 child for experimental sessions performed at different times
before and after the 1st unsupported steps. B: percentage of variance of GTy
data explained by the 2nd Fourier harmonic. C: percentage of variance
accounted for by the 3rd eigen vector u3 of the thigh-shank-foot gait loop. D:
correlation coefficient between VMy data in toddlers and the corresponding
ensemble average in adults during swing. E: normalized VM tolerance area
during swing. The time course of changes with age was fitted by an exponential
function for experimental sessions performed after the onset of unsupported
walk and by a linear function for experimental sessions performed before the
onset of unsupported walk. Œ, data from subject R. D.C; F, data from subject
G.M.; E, data from subject M.M.; 䊐, data from subject L.B:
unchanged until the occurrence of the first unsupported steps
and rapidly matured thereafter, suggesting that unsupported
locomotion experience may act as a functional trigger for
maturation of the innate kinematic pattern.
Idiosyncratic kinematic features of a toddler’s gait
Prewalking children are typically able to stand up and
maintain static equilibrium from ⬃10 mo of age (Zernicke et
al. 1982). At the age of ⬃1 yr, maturation of central neuronal
pathways arrives at a point whereby the necessary integrative
capacity for balance and rhythmic leg activity allows unaided
walking to take place even though the posture is unstable.
Equilibrium instabilities, however, could reorganize a coordination pattern and augment kinematic variability in walking
toddlers as occurs in adults under unstable walking conditions
(Cham and Redfern 2002; Menz et al. 2003). However, our
results show that even when supported through hand contact,
which reduced balance difficulties and thereby increased confidence of stepping, toddlers still exhibited their idiosyncratic
gait pattern, characterized by undeveloped phase coupling of
limb segment motion, bilateral hip discoordination, lack of the
pendulum behavior of the COM, characteristic EMG bursts at
foot contact, high kinematic variability, and distinctive ellipticJ Neurophysiol • VOL
761
like or single-peak trajectories of the foot during swing. Trunk
support also did not significantly improve gait kinematics (Fig.
3), although one can never be sure of having totally removed
the problem of postural instability because translational and
rotational trunk oscillations are inertially coupled with leg
motion. However, if we take a realistic operational approach to
the problem, we are confident that our results do reveal the
absence of a strong relationship between postural instability
and gait immaturity at the onset of independent walking.
Clearly, the task of maintaining stability when walking is
considerably different from that of standing because the former
necessitates an appropriate lower limb coordination pattern. Furthermore, the residual trunk oscillations during walking with hand
support (Fig. 2, right) may likely be a result of the immature
intersegmental coordination. The planar co-variance of the elevation angles of the lower limb segments is weak and variable at the
time of the first unsupported steps (Cheron et al. 2001a,b). The
maturation of the planar co-variance is functionally significant for
the mechanics of walking (Bianchi et al. 1998) and is likely
important for higher postural stability. The parallel development
(similar time constants) of trunk stabilization, planar co-variance
of the elevation angles (Cheron et al. 2001b), and the gravityrelated pendulum mechanism of walking (Ivanenko et al. 2004)
suggests that a dynamic integration of a gravity-centered reference
emerges for equilibrium and forward propulsion.
An optimal cadence in walking roughly corresponds to the
eigen (resonance) frequency of the swinging limbs coupled
with inverted pendulum motion of the stance limb, as predicted
by the pendulum mechanism of walking (Cavagna et al. 1983)
and by the “ballistic walking” model proposed by Mochon and
McMahon (1980), in which the swing limb behaves like a
compound pendulum. Therefore matching of neural and mechanical oscillators might be essential both for minimization of
energy consumption and for a higher dynamic stability because
one of the benefits of pendular rhythmic movements is cycleto-cycle stability and reproducibility (Goodman et al. 2000). In
adults, the minimum variability of the foot trajectory and of the
elevation angles occurs ⬃3– 4 km/h and defines the optimal
kinematic walking speed from the point of view of minimization of positional variance (Ivanenko et al. 2002) and ⬃4.5
km/h from the point of view of minimization of energy consumption (Cavagna et al. 1983). Optimal speed cannot be
easily determined in newly walking toddlers as they usually
walk over a limited range of speeds and steps. However, the
kinematic pattern differed from the adult pendulum behavior
and the kinematic variability was always considerably higher
in the toddlers than in the adults, independent of speed or
support conditions, suggesting that toddlers do not properly use
the gravity-related properties of limb mechanics (transfer between potential and kinetic energies). In addition, the upper
extremities in newly walking toddlers are held away from the
body, whereas, as a child grows older, reciprocal arm swinging
emerges (Sutherland et al. 1980).
Similarities between toddler stepping and stepping in place
in adults
The basic invariance of the characteristic kinematic pattern
in toddlers across different support conditions leads to the
question: does this kinematic invariance reflect motor primitives for the control of stepping? Several aspects of infant
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Y. P. IVANENKO, N. DOMINICI, G. CAPPELLINI, AND F. LACQUANITI
stepping, in particular, the vertical movement of the hip joint
and of the foot, the shape of the gait loop, and the bursts of
EMG activity on foot placements, all suggest that toddlers
implement a mixed locomotor strategy, combining forward
progression with elements of stepping in place. In fact, as noted
in RESULTS, this toddler pattern is highly reminiscent of adult
stepping in place accompanied by supplementary slow forward
translation (see Fig. 5). It is also worth noting that stepping in
place usually precedes independent walking because infants
spend time stepping on the spot, when supported by an adult or
while holding onto an object. Obviously, the linear component
is fundamental for sustaining the locomotor pattern because
unsupported toddlers do not typically step in place. Illustrations of the simple integration of stepping movements with
forward translation can be found in the typical strategy of gait
initiation in toddlers, whereby gait is initiated by letting the
body fall forward, and in a form of early walking, whereby the
toddler puts the swing foot forward to break the fall and bring
the body back to the original stance foot (McCollum et al.
1995). Often, the “faller” cannot stop without something to
bump into, such as a wall or friendly adult (McCollum et al.
1995). The linear component of foot motion in supported
infants can also be evoked when stepping on a moving treadmill belt (Lamb and Yang 2000; Pang and Yang 2001; Yang et
al. 1998). However, the behavior of the body as a compound
inverted pendulum appears later with walking experience.
In infant stepping, several leg muscles emit short-latency
EMG bursts when the foot contacts the ground (Fig. 3B). These
bursts were attributed to hypersensitive stretch reflexes distributed to several muscles (Forssberg 1985, 1999; Okamoto et al.
2003). In contrast, our findings suggest that this characteristic
EMG activity might be a result of nonplantigrade gait rather
than hyperactivity of stretch reflexes because these bursts are
always observed during adult stepping in place accompanied
by supplementary linear translation (Fig. 5).
The occurrence of the prominent single-peak foot lift during
swing corroborates Sherrington’s views on the involvement of
the spinal flexion reflex in step generation (Sherrington 1910).
A similar form of locomotor-like alternating kicking and stepping movements is present at birth and even during the prenatal
period in humans (Forssberg 1985; Zelazo 1983). Thus one can
recognize the above-mentioned features of toddler stepping in
the stick diagrams, video recordings and EMG traces documented by others during supported neonatal stepping (ⱕ4 wk
after birth) and throughout the first year of life (1–12 mo after
birth) (Forssberg 1985; Lamb and Yang 2000; Okamoto et al.
2003; Pang and Yang 2001; Yang et al. 1998), namely: high
single-peak foot lift, short step length, disordered vertical hip
displacements, and characteristic EMG bursts at foot contact.
Role of walking experience in gait maturation
Progressive changes of gait kinematics and kinetics depend
on musculoskeletal growth (including foot shape modifications
and ossification of the soft bones of the feet) (Bertsch et al.
2004), development of the vestibular system (Wiener-Vacher
et al. 1996), central conduction delays (Eyre et al. 1991), and
maturation of central neuronal pathways that are important for
postural and locomotor control, the latter resulting in part from
myelination of descending tracts (Paus et al. 1999). In addition
to these factors, however, walking experience under unsupJ Neurophysiol • VOL
ported conditions may act as a functional trigger of gait
maturation because characteristic gait parameters were basically conserved until independent walking and then rapidly
mature (Fig. 6). Thus the most dramatic phase of maturation
takes place during the first months of independent walking
(Sundermier et al. 2001), though anthropometrical changes and
developmental tunings go on for many years. It is also worth
noting that infants undergoing daily stepping exercise exhibit
an earlier onset of independent walking than untrained infants
(Zelazo et al. 1972). Consistent with learning of other motor
skills, rapid maturation of the infant’s gait is accompanied by
a similar rapid reduction in kinematic variability (e.g., Fig. 6E).
In a computational context, high variability may reflect the
attempts of the CNS to explore a wide range of different
kinematic solutions during development (Forssberg 1999;
Konczak and Dichgans 1997; McCollum et al. 1995; Thelen
and Smith 1994), and walking experience may act to accelerate
the motor system’s ability to identify the optimal solution.
Underlying changes in information accessibility due to the
enhanced freedom to explore the world beyond the territory at
hand, coupled with improved cognitive capacity to generate
complex associations (Butterworth 1998), may also be important for fully unaided walking to develop (Zelazo 1983). For
instance, at the onset of independent walking, appropriate
control of foot placement is greatly lacking: infants often
neglect obstacles (e.g., toys located on the floor) when walking
in a play area and a toddler’s ability to walk on uneven terrain
or slopes is very limited (Adolph 1997). Although postural
control constitutes a necessary ingredient of independent walking, our results clearly show that the onset of walking itself
leads rapidly to stabilization of the locomotor pattern.
ACKNOWLEDGMENTS
We thank Dr. W. Miller for comments on the manuscript and V. Sabia for
the toddler drawing (Fig. 3).
GRANTS
The financial support of Italian Health Ministry, Italian University Ministry
(PRIN and FIRB projects), and Italian Space Agency is gratefully acknowledged.
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