Control of Foot Trajectory in Walking Toddlers:

Adaptation to Load Changes

Nadia Dominici, Yuri P. Ivanenko and Francesco Lacquaniti

J Neurophysiol 97:2790-2801, 2007. First published 24 January 2007; doi:10.1152/jn.00262.2006

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J Neurophysiol 97: 2790 2801, 2007.

First published January 24, 2007; doi:10.1152/jn.00262.2006.

Control of Foot Trajectory in Walking Toddlers: Adaptation to Load Changes

Nadia Dominici,1,2 Yuri P. Ivanenko,1 and Francesco Lacquaniti1,2,3
1
3

Department of Neuromotor Physiology, Santa Lucia Foundation; and 2Department of Neuroscience and
Centre of Space Bio-medicine, University of Rome Tor Vergata, Rome, Italy

Submitted 10 March 2006; accepted in final form 20 January 2007

What is the role of body weight for the control of locomotion? Footsupport interactions and load-regulating mechanisms play a crucial role in shaping patterned motor output
during stepping (Duysens et al. 2000). Transient loading of the
limb enhances the activity in antigravity muscles during stance
and delays the onset of the next flexion (Duysens and Pearson
1980). Furthermore, the safe trajectory of the foot with minimal toe clearance at midswing is a precise endpoint control
task that is under multisegmental motor control in both the
stance and swing limbs (Bernstein 1967; Winter 1992). In
adults, minimal contact forces are sufficient for accurate foot
trajectory control because the required variation of the parameters that describe shape and variability of the foot path is very
limited despite drastic changes in limb kinetics with body
unloading (Ivanenko et al. 2002). These findings argue against
a simple controller that commands a fixed change of limb
kinematics for a fixed change of force. Thus the basic kinematic control mechanisms operating in normal walking (Lac-

quaniti et al. 1999, 2002) also apply to walking with a high

level of body weight support (BWS) in adults, suggesting that
the kinematic locomotor program compensates well for body
weight.
Previous studies have shown that infants have the ability to
adapt to environmental changes. Infants, when supported, can
step with a variety of speeds, in different directions, and with
appropriate response to external perturbations long before the
time of the onset of independent walking (Forssberg 1985;
Lam et al. 2003a; Lamb and Yang 2000; Pang and Yang 2001;
Thelen 1986; Thelen and Cooke 1987; Thelen et al. 1987;
Yang et al. 1998, 2005; Zelazo 1983), suggesting that the
pattern generation network and ability to adapt to environmental changes are present in the human locomotor system before
independent walking. Nevertheless, initial stepping in toddlers
has also some specific features. For instance, global gait
features, such as the planar law of intersegmental coordination
(Cheron et al. 2001a,b) and the pendulum mechanism of
walking (Holt et al. 2006; Ivanenko et al. 2004), are still
immature at the beginning of independent walking. A toddlers
ability to walk on uneven terrain or slopes is very limited
(Adolph 1997) and an appropriate control of foot motion is also
lacking: infants show a larger foot clearance, an unusual single
peak trajectory (Ivanenko et al. 2005), and flat-footed contact
with the ground (Forssberg 1985).
Young infants (2 mo) can support only 20 40% of their
body weight on one limb (Forssberg 1985). In addition, slimmer babies with smaller bones and smaller muscle mass are
believed to begin crawling and walking sooner than chubbier,
more top-heavy infants (Adolph 1997; Garn 1966; Jensen
2005; Payne and Isaacs 2005; Shirley 1931; Thelen et al.
1984). In toddlers, given limited muscle strength and limited
experience with their body weight and leg movements in an
upright posture against gravity, body heaviness may represent
a challenging factor for stepping. To obtain further insights
into the footsupport interactions and the intrinsic dynamics of
the neuromotor system at the walking onset, we examined how
toddlers adapt to a change in the amount of load on their legs.
Trunk support represents a common experimental strategy to
provide equilibrium and thus facilitate locomotor movements
in infants. Moreover, one might expect that infants are well
adapted to trunk support and body unloading before the onset
of independent walking, but unsupported stepping represents a
new condition for them. However, other than the occasional
stick-diagram or individual trajectory plots at uncontrolled
BWS levels, a comprehensive study of limb kinematics in
toddlers walking at different gravitational loads has not yet

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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0022-3077/07 $8.00 Copyright 2007 The American Physiological Society

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Dominici N, Ivanenko YP, Lacquaniti F. Control of foot trajectory in walking toddlers: adaptation to load changes. J Neurophysiol 97: 2790 2801, 2007. First published January 24, 2007;
doi:10.1152/jn.00262.2006. On earth, body weight is an inherent
constraint, and accordingly, load-regulating mechanisms play an
important role in terrestrial locomotion. How do toddlers deal with
the effects of their full body weight when faced with the task of
independent upright locomotion for the first time? Here we studied
the effect of load variation on walking in 12 toddlers during their
first unsupported steps, 15 older children (1.35 yr), and 10 adults.
To simulate various levels of body weight, an experimenter held
the trunk of the subject with both hands and supplied an approximately constant vertical force during stepping on a force platform.
During unsupported stepping, the shape of the foot path in toddlers
(typically single-peak toe trajectory) was different from that of
adults and older children (double-peak trajectory). In contrast to
adults and older children, who showed only limited changes in
kinematic coordination, the reduced-gravity condition considerably affected the shape of the foot path in toddlers: they tended to
make a high lift and forward foot overshoot at the end of swing. In
addition, stepping at high levels of body unloading was characterized by a significant change in the initial direction of foot motion
during early swing. Intermediate walkers (1.55 mo after walking
onset) showed only partial improvement in foot trajectory characteristics. The results suggest that, at the onset of walking, changes
in vertical body loads are not compensated accurately by the
kinematic controllers; compensation necessitates a few months of
independent walking experience.

FOOT TRAJECTORY IN TODDLERS

TABLE

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1. Developmental group characteristics

Toddlers (within 1 wk
of unaided walking
experience)
Intermediate walkers
(1.55 mo after
onset of walking)
Children 25 yr
(between 9 and 50
mo walking experience)
Adults

Age, Months

Limb Length, cm

Mass. kg

Number of Recorded
Unsupported Steps

Number of Steps
With BWS

12

12.9 1.2

32.1 4.1

10.4 1.0

32 19

34 18

17.4 1.1

37.2 2.5

11.7 0.6

16 11

11 3

9
10 (5)*

46.7 16.9
31 7 (yrs) (34 6)

43.7 7.6
83.7 3.5 (81.1 2.2)

15.6 3.6
64.6 15.0 (53.5 6.1)

29 14
26 6 (12 3)

21 10
76 17 (11 5)

Values are means SD. The length of the lower limb was measured as thigh plus shank length. *Overground walking with manual body weight support.

METHODS

Subjects
We recorded surface locomotion in 12 toddlers (6 males, 6 females,
1115 mo of age), 6 intermediate walkers (4 males, 2 females, 1.55
mo after the walking onset), 9 children 25 yr old (7 males, 2 females,
9 50 mo after the walking onset), and 10 healthy adults [5 females
and 5 males, 31 7 (SD) yr; Table 1]). We used the same developmental groups (Table 1) as in our previous paper (Ivanenko et al.
2004). Five of our toddlers were recorded a second time 0.12 yr after
the first recording session (3 of our toddlers were the same as in our
J Neurophysiol VOL

previous paper about the effect of posture stabilization, Ivanenko et al.

2005; but now we report their locomotor response to a full range of
BWS levels). Informed consent was obtained from all the adults and
from the parents of the children. The experimental procedures were
approved by the ethics committee of the Santa Lucia Institute and
conformed with the Declaration of Helsinki. The laboratory setting
and experimental procedures were adapted to the children such that
the minimal risks were equal or lower to that of walking at home. Both
a parent and an experimenter remained astride 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 toddlers hand and encouraging
her or him to walk unsupported on the floor. For each subject, about
10 trials were recorded under similar conditions. Short trials (3 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 retained
to avoid initiation and braking phases and head movements caused by
looking in other directions. Older children and adults were monitored
while they walked at natural, freely chosen speeds. Typically, we
analyzed two to five consecutive step cycles in each trial, for toddlers,
older children, and adults.

WALKING WITHOUT SUPPORT.

WALKING AT DIFFERENT LEVELS OF BODY WEIGHT SUPPORT. In the

toddlers we studied the effect of changing the load on the lower limb
kinematics. To this end, after recording gait under standard conditions, some trials were recorded while an experimenter (or a parent)
held the trunk of the child under his/her arms with both hands and
supplied an approximately constant vertical force during stepping
attempts (Fig. 1, A and B). The amount of the external BWS was
varied from trial to trial to cover a wide range of values. The same
procedure of body unloading was performed in older children during
overground walking.
In adults, the experiments with different BWS levels (0, 35, 50, 75,
and 95% of body weight) were carried out on a treadmill at 3 km/h.
BWS was obtained by suspending the subjects in a parachute harness
(Reha, BONMED) connected to a pneumatic device that applied a
controlled upward force at the waist (WARD system, Gazzani et al.
2000). As a result, each supporting limb experienced a simulated
reduction of gravity proportional to the applied force, while the
swinging limb experienced 1g. The overall constant error in the
applied force and dynamic force fluctuations monitored by a load cell

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appeared in the literature. Few previous studies have dealt with

adaptation to limb loading (Schmuckler 1993; Thelen et al.
1984) and unexpected unloading (e.g., removal of the extra
weight strapped around the lower limb, Lam et al. 2003b) to
the additional body mass (Adolph and Avolio 2000), or with
spontaneous leg movements in different postures (supine, angled and vertical), i.e., in different gravitational contexts in
infants (Jensen et al. 1994). Such studies have reported mainly
local or transient modifications in muscle activity, joint rotations, or step length characteristics.
In our previous work (Ivanenko et al. 2005), we used trunk
support as a means toward reducing the effects of postural
instability in walking toddlers and found no significant changes
in lower limb kinematics. In that study, we reported only the
effect of postural instability, and to this end, we supplied
limited vertical force (typically 20% of the body weight).
However, trunk stabilization (postural stability) and trunk unloading (weight bearing) may have separate consequences on
stepping. Here, we report stepping with and without trunk
support in toddlers who were just beginning to walk independently, and the amount of body weight support was varied from
trial to trial to cover a wide range of values (0 90% of full
body weight). Gait improvements during the first 13 mo show
a very high rate of change, which is followed by a less steep
curve of maturation (Adolph et al. 2003; Hallemans et al. 2005,
2006; Holt et al. 2006; Ivanenko et al. 2007; Sutherland et al.
1988). We hypothesized that appropriate adaptation to body
weight changes may also occur within the first several months
after the onset of independent walking. To this end, we also
compared toddlers gaits with walking in older children and in
adults at different levels of BWS. To analyze kinematic patterns, we used methods developed earlier for adult gait (Bianchi et al. 1998; Borghese et al. 1996; Ivanenko et al. 2002).

2792

N. DOMINICI, Y. P. IVANENKO, AND F. LACQUANITI

Data analysis

was 5% of the body weight. All adults were also recorded during
oveground walking at a natural speed. In addition, five smaller-weight
(4358 kg) adults were recorded using the same manual unloading
protocol during overground walking as in children.

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). Particular care was taken to place the VM marker in
the same position (on the lateral aspect of the 5th metatarso-phalangeal joint) in all subjects. Individual deviations of the VM marker
position relative to the actual fifth metatarso-phalangeal joint (because
the diameter of the marker was 1.4 cm and it was attached to the skin
on a short 1-cm height stem) were measured before the recordings and
corrected afterward with software.
The ground reaction forces under both feet (Fig. 1B) 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.
J Neurophysiol VOL

Intersegmental coordination
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 covary during walking. When these angles are plotted
in three dimensions (3D), they describe a path that can be leastsquares fitted to a plane over each gait cycle. In adults, changing BWS
results in limited changes of the kinematic coordination (Ivanenko et
al. 2002). Here, we studied this issue of intersegmental coordination
(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 u1u3, 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 and u2 lie on the best-fitting
plane of angular covariation. The third eigenvector (u3) is the normal
to the plane and thus defines the plane orientation. To quantify the
rotation of the plane with BWS, we analyzed the u3t parameter (the
direction cosine of the normal to the plane with the axis of thigh
elevation), which was found to vary systematically with BWS in
toddlers (see RESULTS).

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FIG. 1. An example of unsupported and supported walking. A: unilateral

sagittal stick diagrams (of a single step) when the toddler walked unsupported
(left) and when an experimenter held the trunk of the child with both hands and
supplied an approximately constant vertical force during stepping attempts
(middle and right). B: ground reaction forces under both feet were recorded
with a force platform. Dotted horizontal lines indicate body weight. Amount of
external body weight support was estimated as percent reduction of mean
vertical force on the platform (Fy).

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).
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.
In adults, 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 children 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).
The amount of the external body weight support in children and
adults during overground walking was estimated as the percent
reduction of the mean vertical force on the platform (Fig. 1B).
To verify whether the trunk angle in the sagittal plane varied with
weight support, we measured the mean angle of the long axis of the
trunk with respect to the vertical axis. 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.

FOOT TRAJECTORY IN TODDLERS

2793

Foot trajectory

Age-related changes

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 (using Pearson
correlation coefficient). VM trajectories were time-normalized over
the swing phase duration. They were analyzed both in space and
relative to the instantaneous hip (GT marker) position. To show the
dynamics of foot motion during swing, we also calculated the instantaneous pitch angle of the VM velocity vector in the sagittal plane. In
each gait cycle, the foot moves back and forth relative to the body. To
emphasize the differences in the initial direction of foot motion during
early swing across subjects, we computed the mean pitch angle of VM
motion during the first 30% of swing (beginning from the moment
when the VM marker reversed direction from backward to forward).

The time-course of changes of kinematic and kinetic parameters as

a function of age was fitted by an exponential function, y aet/
b, where y is the specific parameter under study, t is the time since
onset of unsupported walking, is the time constant, and a and b are
two weighting constants.

Foot trajectory variability

Statistical analyses (Students t-test) were used when appropriate.

Reported results were considered significant for P 0.05. Statistics
on correlation coefficients was performed on the normally distributed,
Z-transformed values. The algebra of angles (circular variables) is
somewhat different from the rules governing other (linear) quantities.
Circular statistics (Watsons U2 test) were used to compare the initial
directions of foot motion during swing across subjects. Spherical
statistics on directional data (Batschelet 1981) were used to characterize the mean orientation of the normal to the covariation plane (see
above) and its variability across steps. To assess the variability
directly, we calculated the angular SD (called spherical angular
dispersion) of the normal to the plane.
RESULTS

General characteristics of foot trajectory in children

During unsupported walking, foot trajectory characteristics
differed systematically in toddlers compared with those in
adults and older children. The dominant template of foot
motion is shown in Fig. 2A (left). All toddlers typically moved
the leg in such a way that foot lift (VMy) had only one
maximum at midswing. This behavior was entirely in contrast
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 in the
end of swing. 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 (0.51 0.19). The spatial variability of the endpoint
(foot) path in the sagittal plane was considerably greater than
in the adults (see also Ivanenko et al. 2005): the normalized
tolerance area (scaled to the mean limb length of adults) was

FIG. 2. Changes of the foot trajectory

characteristics (shape and variability) with
age. A: stick diagrams (of a single step) and
corresponding foot trajectories in 1 toddler, 2
older children, and in 1 representative adult.
B: correlation coefficient between VMy data in
children and corresponding ensemble average
in adults during swing. C: normalized 5th
metatarso-phalangeal joint (VM) tolerance
area during swing. All data refer to overground walking at natural speed. Values for
adult group were obtained by computing mean
(SD) from pooled data obtained for walking
at natural, freely chosen speed (on average,
3.8 0.4 km/h). Time-course of changes with
age was fitted by an exponential function (r
0.92 and 0.86 in B and C, respectively). is
corresponding time constant.

J Neurophysiol VOL

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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, 2005). These
indices describe the integrated variability of foot path, including
variability in 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 resampled 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 715) 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. 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 2D 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

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N. DOMINICI, Y. P. IVANENKO, AND F. LACQUANITI

20.5 6.5 cm2/cm in toddlers and 3.8 1.9 cm2/cm in adults

(P 0.0001, Students unpaired t-test).
Age-related changes of the kinematic parameters related to
the foot trajectory control are presented in Fig. 2, B and C, for
the whole group of subjects during overground walking at a
natural speed. Both the correlation coefficient between VMy in
children and VMy in adults (Fig. 2B) and the foot path variability
(normalized VM tolerance area; Fig.2C) changed rapidly over the
first few months of independent walking experience. Changes
with age were fitted by an exponential function (see METHODS).
The time constant was fast both for the correlation with the
ensemble average in adults ( 2.5 mo) and for the changes of
the VM spatial variability across steps ( 1.9 mo).
Stepping at different BWS levels

J Neurophysiol VOL

Effect of BWS on intersegmental coordination

Figure 3A plots averaged thigh, shank, and foot elevation
angles and corresponding gait loops in toddlers, older children
(25 yr), and adults at two levels of BWS. In adults and older
children, temporal changes of the elevation angles of lower
limb segments covaried along a plane, describing a characteristic loop over each stride. Paths progress in time in the
counter-clockwise direction, lift-off and touch-down corresponding approximately to the top and bottom of the loop,
respectively (Fig. 3A). 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. Planar covariation was obeyed at
all tested BWS levels (on average, PV3 was 1.0 0.2%),
although the 3D gait loop became slightly narrower with
increasing BWS (e.g., at 95% BWS, in 4 of the 10 adults PV2
was 3%), consistent with our previous study; (Ivanenko et al.
2002; PV1 increase and PV2 decrease; Fig. 3B, right). The first
two eigenvectors u1 and u2 of the covariance matrix lie on the
best-fitting plane of angular covariance, whereas the third
eigenvector (u3) is the normal to the plane and is characterized
by the direction cosines plotted in Fig. 3B (bottom panels).
The gait loop and its associated plane depend both on the
amplitude and phase of the limb segment oscillations. The
plots of Fig. 3A show the basic stereotypy of the patterns of
intersegmental covariations obtained at different BWS levels,
but they hide subtle yet important trends with BWS changes. In
all subjects, the plane of angular covariation rotated with
increasing BWS (U3t monotonic decrement; Fig. 3B).
In toddlers, at 0 BWS, the gait loop departed significantly
from planarity and the mature pattern. Although the plane
(PV1 PV2 PV3) resembled that of the adults, PV3 was
significantly higher in toddlers (3.1 0.8%) than in adults
(0.9 0.2%, P 0.001 Students unpaired t-test), in agreement with previous findings (Cheron et al. 2001b; Ivanenko et
al. 2004). Moreover, the step-by-step variability of plane orientation (estimated as the angular dispersion of the plane
normal) was considerably higher in toddlers (15.8 7.3) than
in adults (2.9 1.0). In addition, because the amplitude of
thigh movements was relatively higher with respect to that of
shank and foot movements in toddlers (Fig. 3A), the gait loop
was less elongated than in adults, as shown by the larger
contribution of the second eigenvector (PV2), although with
increasing BWS, the gait loop in toddlers (Fig. 3A) tended to be
more elongated (PV2 decreased; Fig. 3B, left).
Effect of BWS on foot trajectory
BWS did not influence appreciably the shape of the endpoint
path in adults (Fig. 4) in agreement with our previous study
(Ivanenko et al. 2002). At 95% BWS (nearly complete unloading), adult subjects were still able to step on the treadmill,
typically with only forefoot loading during stance (no heel
contact). However, the correlation coefficient between the time
series of the VMy during swing at 0 and 95% BWS was still
very high (0.94 0.03). The path and its variability were
relatively conserved from 0 to 95% BWS. Finally, the addi-

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To study the effect of BWS, an experimenter or a parent

firmly held the trunk of the child with both hands providing an
approximately constant vertical force while the child stepped.
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
toddlers forward motion. Nevertheless, during supported stepping, the mean walking speed and stride length (1.6 0.5
km/h and 0.44 0.08 m at 40 90% BWS) were similar to
those during unsupported stepping (1.5 0.4 km/h and 0.35
0.06 m; P 0.05, paired t-test). The position of the arms was
also similar because the upper extremities in newly walking
toddlers are typically held away from the body (Sutherland et
al. 1980). The mean walking speed in nine older children (25
yr), supported in the same way as the toddlers, also did not
change significantly (3.0 0.5 km/h at 0 BWS and 3.1 0.4
km/h at 40 90% BWS).
The walking speed freely chosen by toddlers was in general
lower than in adults or in older children when expressed in
dynamically equivalent terms using the Froude number
(Fr V2/gL, where V is the average speed of locomotion, g is
the acceleration of gravity, and L is 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 0.07 0.04 in our toddlers (across all conditions) versus
0.18 0.05 in older children and 0.19 0.04 in adults during
overground walking. The mean walking speed in toddlers
(1.5 km/h) corresponds to 2.5 km/h in adults when normalized using the Froude number (i.e., to the square root of L).
Therefore, although the general characteristics of foot motion
in adults do not depend significantly on the walking speed
(Ivanenko et al. 2002), for the sake of comparison, we recorded
treadmill locomotion with BWS in adults at a comparable
equivalent speed (3 km/h).
It is worth noting that the general characteristics of the foot
path in adults did not differ significantly during overground
walking and walking on the treadmill at 0 BWS except that the
foot path variability was slightly larger during overground
walking: VM tolerance area was 3.8 1.9 cm2/cm during
overground walking and 2.7 1.1 cm2/cm during treadmill
walking at 3 km/h. This difference was likely caused by some

variability in the walking speed (and consequently in the stride

length) across overground trials.

FOOT TRAJECTORY IN TODDLERS

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tional kinematic data from smaller-weight adults (n 5, Table

1) during overground walking with manual unloading were not
significantly different from those obtained during walking on a
treadmill when suspending the subjects in a parachute harness
connected to a pneumatic device that applied a controlled
upward force. The correlation coefficient between the time
series of the VMy during treadmill and overground walking was
very high (0.97 0.02 at 0 BWS and 0.95 0.03 at 40 90%
BWS), and the maximal foot lift during swing and the relative
position of the main peak were also similar at all BWS levels,
independent of the unloading procedure (Fig. 4, bottom).
In contrast, the reduced gravity considerably affected the
shape of the foot path in toddlers: all toddlers tended to make
J Neurophysiol VOL

an unusual high foot lift and forward foot overshoot (a kickinglike movement) at the end of swing at high levels of body
unloading (Fig. 4A, right). For instance, at 0 BWS, the mean
peak position of the VMy was at midswing, whereas at 40 90%
BWS, it was significantly shifted forward (Fig. 4B; P 0.001,
paired t-test). This behavior (forward foot overshoot) persisted
over all consecutive steps performed at high BWS levels in
one trial (typically 25 steps). It is worth noting that the
same unloading procedure that was used in toddlers did not
change significantly the shape of the foot path in older
children (Fig. 4).
Variability inherent in the toddlers stepping pattern may
have limited our ability to draw definitive conclusions about

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FIG. 3. Effect of body weight support (BWS) on intersegmental coordination. A: averaged thigh, shank, and foot elevation angles and corresponding gait loops
plotted in 3D in toddlers, older children (25 yr), and adults at 2 levels of BWS (0 and 75%). Data are plotted vs. normalized gait cycle. Data for adults refer
to treadmill walking at 3 km/h. A loop is obtained by plotting thigh waveform vs. shank and foot waveforms (after mean values subtraction). Paths progress in
time in counter-clockwise direction, foot strike and lift-off corresponding approximately to the top and bottom of the loop, respectively. B: characteristics of gait
loops in toddlers, older children, and adults. Interpolation planes result from orthogonal planar regression. First eigenvector (u1) is aligned with the long axis
of gait loops, 2nd eigenvector (u2) is aligned with the short axis, and 3rd eigenvector (u3) is normal to the plane. Planar covariance for thigh-shank-foot loops
is assessed by percentage of variance accounted for by eigenvectors u1, u2, and u3 (PV1, PV2, and PV3, respectively). PV1 and PV2 are related to the global form
of 3D gait loop, and PV3 provides an index of planarity of the loop (0% corresponds to an ideal plane). Normal to covariance plane is characterized by direction
cosines of plane normal (u3) with positive semi-axis of thigh, shank, and foot angular coordinates, respectively (u3t, u3s, and u3f). Each point corresponds to 1
individual stride. Changes with BWS are fitted by a linear function.

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N. DOMINICI, Y. P. IVANENKO, AND F. LACQUANITI

the exact dependence of the foot trajectory on the BWS level

(Fig. 4). To estimate the level at which changes in the forward
foot overshoot become significant, we compared the relative
peak position (Fig. 4B) obtained at 0 BWS and under weight
supported conditions within each 20% interval of BWS: we
moved the BWS window every 10% (10 30%, then 20 40%,
etc.) until the difference with the 0 BWS condition became
significant (using t-test). Such procedure revealed significant
changes with respect to the unsupported walking condition
beginning from the 30% BWS values.
Figure 5A shows the average template of the foot trajectory
and the dynamics of the pitch () angle in toddlers, older
children (25 yr), and adults. In the time domain (Fig. 5B), at
all levels of BWS, the vertical excursion of the foot in toddlers
J Neurophysiol VOL

tended to have only one maximum at midswing, and the

correlation coefficient between the time-series of the VMy
during swing in toddlers and the corresponding ensemble
average in adults remained negative at 40 90% BWS
(0.72 0.10). However, there were significant changes in
the hip angle during swing initiation at high levels of BWS
(Fig. 5C): the hip tended to be slightly extended (by 7) in
toddlers, whereas it was similar in older children and adults
during body unloading. The knee angle tended to be somewhat
flexed during stance-to-swing transition in toddlers at high
levels of BWS (Fig. 5C).
The amplitude of the vertical hip (GTy) oscillations throughout the gait cycle did not change significantly with BWS
(2.8 0.6 cm at 0 BWS and 3.2 0.8 cm at 40 90% BWS,

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FIG. 4. Effect of BWS on shape of foot

path. A: examples in 3 toddlers, 1 older child,
and 1 adult. Trajectories over 6 10 steps were
superimposed in space relative to mean VMx
position during each stride; adult data were
also corrected for treadmill belt speed. Note
that path shapes are roughly comparable in all
support conditions in the adult and in the older
child, whereas these both differ from those for
the toddlers. B: maximal foot (VM) lift and
relative position of main peak. In adults, we
analyzed the 1st peak of VM path (just after
lift-off) because it was usually higher than the
2nd peak at the end of swing. Changes with
BWS are fitted by a linear function in adults
and older children and by a 2nd-order polynomial function in toddlers. Values for adult
group were obtained both for overground
walking and for walking on a treadmill at 3
km/h. L, limb length.

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FIG. 5. A: average VM trajectories in space in toddlers, older children, and adults during walking at 0 and at high levels of BWS. Plots are anisotropic, vertical
scale being expanded relative to horizontal scale. Data for the adult group were obtained from smaller-weight adults (n 5, Table 1) during overground walking
with manual BWS. Bottom panels show instantaneous pitch angle of VM path. LO, lift off; TD, touch down. B: time-course of average vertical foot (VMy)
displacement and average hip, knee, and ankle angles. Black line corresponds to walking at high levels of BWS. Solid line surrounded by gray shading represents
unsupported stepping curve and SE, respectively. Vertical dotted lines correspond to stance-to-swing transition. C: changes in joint angles (SD) at moment of
lift off at high levels of BWS with respect to unsupported stepping. Asterisks denote significant differences (P 0.05).

P 0.05) making it unlikely that the increased trunk oscillations could govern larger foot movements in space. In addition,
the mean trunk orientation in toddlers tended to tilt forward
during body unloading (BWS 40%; by 3.1 5.6, P 0.05,
one-tailed t-test), although in older children (25 yr) the
amount of forward tilt was similar (6.1 4.8). We also
analyzed the foot path relative to the instantaneous hip position. Again, the distinctive forward foot overshoot was present
in toddlers at high levels of BWS (Fig. 6A), and stepping at
these levels was characterized by an apparent change in the
initial VM direction during early swing. The VM tolerance
area also remained high (19.8 3.7 cm2/cm with 40 90%
body support and 20.5 6.5 cm2/cm without). In toddlers, the
J Neurophysiol VOL

pitch angle of this directional vector (mean circular SD,

relative to the horizontal) was 32 9 at 0 BWS and 0 4
at 40 90% BWS, whereas in older children it was 0 7 and
5 6 and in adults it was 4 6 and 1 6, respectively.
At 0 BWS, this angle (32 9) was significantly different
from that of adults and older children (P 0.001, Watsons U2
test), indicating a high initial foot elevation during swing in
toddlers, whereas at high levels of BWS, the difference was
minor (Fig. 6B).
Figure 7 shows the effect of BWS on the shape of the foot
path in all groups of subjects (Table 1). Older children (25 yr)
displayed quite mature foot trajectory characteristics, whereas
intermediate walkers (1.55 mo after the onset of walking)

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N. DOMINICI, Y. P. IVANENKO, AND F. LACQUANITI

showed only partial improvement, supporting the conclusion

that a few months of walking experience is the minimum
practice duration for the beginning of an effective (adult-like)
foot trajectory control.
DISCUSSION

Our study supports the common notion that toddlers are able
to adapt to environmental changes and they can step at different levels of BWS. The intersegmental coordination (rotation

of the covariance plane; Fig. 3B) showed similar monotonic

changes with BWS in all subjects, suggesting similar amplitude and phase regulation of segment motion with body unloading. We also confirmed our previous findings (Ivanenko et
al. 2005) that trunk stabilization (low BWS levels) did not
affect significantly limb motion. Our main finding in this study,
however, was that, in contrast to adults and older children, foot
trajectory characteristics in toddlers showed systematic
changes with limb unloading. This difference was exemplified
by the higher foot lift, forward foot overshoot (Figs. 4 and 5A)

FIG. 7. Effect of BWS on the shape of foot path (swing phase) in all groups of subjects. A: correlation coefficient between VMy data in children and
corresponding ensemble average in adults. B: relative position of main peak of VMy (same parameter as in Fig. 4B). C: mean initial directions of VM path. IWK,
intermediate walkers (see Table 1). Asterisks denote significant differences (P 0.05).

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FIG. 6. Foot trajectories relative to instantaneous hip position (swing phase). A: example of 1 toddler, the same child recorded 3 yr later, and 1 representative
adult. Top to bottom: stick diagrams of 1 cycle relative to instantaneous hip position and VM spatial density plots. Initial direction of VM path (1st 30% of swing)
is indicated by an arrow. Spatial density of VM path was integrated over swing phase (across 10 15 steps) performed at different BWS. Density of each cell
was depicted graphically by means of a color scale (empty cells were excluded): the lower the density (toward blue in color-cued scale), the greater the variability.
Plots are anisotropic, vertical scale being expanded relative to horizontal scale. B: mean initial directions of VM path for toddlers, older children, and adults for
stepping at 0 and high levels of BWS.

FOOT TRAJECTORY IN TODDLERS

and remarkable change in the initial foot direction (Fig. 6) with

body weight unloading. These performance changes with level
of unloading were observed in all toddlers who were just
beginning to walk independently. Intermediate walkers (1.55
mo after walking onset) showed only partial improvement in
foot trajectory characteristics (Fig. 7).
Methodological considerations

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Effect of body weight unloading on foot trajectory control

in toddlers
What is special in toddler gait? When children start to walk
independently, their gait is characterized by considerable trunk
oscillations revealing postural instability (Assaiante et al.
1993; Bril and Brenie`re 1993; Roncesvalles et al. 2001), wide
swinging arms (Sutherland et al. 1980), high interstep variability (Clark et al. 1988), and immature foot trajectory characteristics and intersegmental coordination (Cheron et al. 2001a,b;
Ivanenko et al. 2004, 2005). In particular, early stepping
typically manifests itself in shorter step lengths, disordered
vertical hip displacements, nonplantigrade gait (lack of the
heel-to-toe roll-over pattern), and a single peak foot lift during
swing. One may argue that this evolutionary adopted pattern
(nonplantigrade gait with a high foot lift) is beneficial for
toddlers as an optimal starting point strategy (Ivanenko et al.
2007) to avoid stumbling and falls and for reducing the effect
of involuntary foot drag and the lack of dorsiflexor activity,
which has been observed at the stance-to-swing transition
during treadmill stepping in young infants (Yang et al. 2004).
The phenomenon may possibly reflect flexor-biased pattern
generation (Yakovenko et al. 2005) in infants that is replaced
by mature control with walking experience. For instance, the
flexion reflex and the placing reflex seem to be important
components of infants stepping (Forssberg 1985; Zelazo et al.
1972). An early form of locomotor-like alternating kicking and
stepping movements is present at birth and even prenatally in
humans (Thelen 1981; Zelazo 1983). Hip flexion dominates in
an early period of infancy during supported neonatal stepping
(4 wk after birth), throughout the first year up to the beginning of independent walking (Forssberg 1985; Lamb and Yang
2000; Okamoto et al. 2003; Pang and Yang 2001; Thelen 1981;
Yang et al. 1998). The relative hyperflexion in hip and knee is
slightly reduced compared with the neonatal stepping but it is
still present before the onset of independent walking (Forssberg 1985). Indeed, the amplitude of thigh movements is
relatively higher with respect to that of shank and foot movements, resulting in the wider gait loop in toddlers and by the
larger contribution of the second eigenvector (PV2 in Fig. 4)
(see also Cheron et al. 2001a,b). Moreover, several aspects of
infant stepping, including 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 (Ivanenko et al.
2005). This hypothesis is also consonant with the finding that
toddlers had not yet learned to use transverse pelvic rotation in
leg-pelvis coordination to increase speed of walking (Holt et al.
2006).
In addition to the idiosyncratic foot trajectory characteristics
during unsupported stepping, our data indicate that toddlers
adapt differently than adults and older children to variations in
load (Figs. 5A, 6, and 7). At low levels of BWS (30%), foot
trajectory characteristics were similar to those during unaided
stepping, in agreement with our previous results (Ivanenko et
al. 2005). However, at higher levels of BWS, the flexorbiased (or stepping-in-place) component of swing initiation
(Figs. 5A and 6) decreased significantly with limb unloading
resulting in alternating swing movements of the legs with an
overshoot at the end of swing. If one accepts the terminology

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Sensory signals interact with central rhythm-generating centers in a complex manner (Pearson 1995). Afferent activity
helps to shape the motor patterns, control phase-transitions,
and reinforce ongoing activity. In stance, load-detecting afferents, both from muscles and skin, facilitate the center for the
generation of extension and inhibit that for flexion. In toddlers,
the foot shape and ossification of the soft bones of the feet are
still immature at the age of 1 yr (Bertsch et al. 2004). During
limb loading, a variety of receptors can be activated, such as
Golgi tendon organs, cutaneous receptors of the foot, and
spindles from stretched muscles (Duysens et al. 2000). A
number of cutaneous reflexes participate in the fine control of
foot positioning in animals (Guertin et al. 1995; Schouenborg
and Weng 1994) and humans (Aniss et al. 1992; Van Wezel et
al. 1997; Yang and Stein 1990; Zehr and Stein 1999). Even
though the spatio-temporal distribution of load on the soles of
the feet may be generally important in the regulation
of locomotion, we have previously found that it does not
appreciably affect the endpoint trajectory constraints in adults
(Ivanenko et al. 2002): in the limit cases of 95% BWS and
100% BWS with surrogate contact, detection of ground contact
at the forefoot was sufficient to trigger the central program for
accurate endpoint control in adults. These findings suggest that
an idiosyncratic distribution of load on the soles (Bertsch et al.
2004; Hallemans et al. 2004) and nonplantigrade stepping in
toddlers were not the primary reason for the observed adaptive
difference between toddlers and adults (Fig. 5).
One could argue that the enlarged vertical foot displacements at high levels of BWS in toddlers (Fig. 4) were a simple
result of changes in the trunk motion influenced by an experimenter who supported the child. However, this is unlikely
because of the following reasons. First, the same unloading
procedure in older children and adults did not affect significantly the foot path (e.g., Figs. 4 6). Second, the amplitude of
the vertical hip oscillations in toddlers throughout the gait
cycle did not change significantly with BWS. Also, the mean
trunk angle varied similarly with weight support between the
groups of children. Finally, the foot path relative to the instantaneous hip position showed similar behavior (Fig. 6) as in
space (Fig. 5A). In addition, when holding the trunk under the
arms, i.e., at low levels of trunk support (BWS 20%), leg
and foot movements were similar to those during unsupported
stepping (Ivanenko et al. 2005), making unlikely the contribution of simple sensory contact of the hands with the childs
trunk. As a final point, the observed phenomenon (Figs. 4 and
6) was not caused by the aftereffect of transient load changes
(Lam et al. 2003b) because it persisted over all (from 2 to 5)
consecutive steps performed at high levels of BWS. Therefore
we believe that the unusual forward foot overshoot in toddlers
was caused by the nonspecific reduction of gravitational load
during stance.

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Holt et al. 2006; Ivanenko et al. 2004, 2005; Roncesvalles et al.

2001; Sundermier et al. 2001; Sutherland et al. 1988).
ACKNOWLEDGMENTS

We thank Dr. W. Miller for helpful comments on the manuscript and V.

Sabia for the toddler drawing (Fig. 1A).
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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of motor primitives or stereotypies in infants (Thelen 1981),

there was a switch from the stepping-in-place motor component during unsupported walking to the kicking component
during walking at high levels of BWS.
We do not know the exact nature or transmission mechanisms of the information that shapes the foot trajectory and its
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1999) and in the elderly (Winter et al. 1990). In toddlers,
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after a swim or bath, one perceives the body as being very
heavy, and it can be initially very difficult to walk, even though
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interactions and a lack of the appropriate pendulum behavior of
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underdevelopment. The transition to a pendulum pattern occurs
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(Ivanenko et al. 2007). In fact, walking practice is a much
stronger predictor of posture and gait improvement in newly
walking toddlers than age or body size (Adolph et al. 2003;

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