Foot anatomy specialization for postural sensation and

control
W. G. Wright, Y. P. Ivanenko and V. S. Gurfinkel
J Neurophysiol 107:1513-1521, 2012. First published 7 December 2011; doi:10.1152/jn.00256.2011

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Foot anatomy specialization for postural sensation and control
W. G. Wright,1 Y. P. Ivanenko,2 and V. S. Gurfinkel3
1
Temple University, Philadelphia, Pennsylvania; 2IRCCS Fondazione Santa Lucia, Rome, Italy; and 3Oregon Health
& Science University, Portland, Oregon
Submitted 22 March 2011; accepted in final form 4 December 2011
Wright WG, Ivanenko YP, Gurfinkel VS. Foot anatomy specializa-
tion for postural sensation and control. J Neurophysiol 107: 1513–1521,
2012. First published December 7, 2011; doi:10.1152/jn.00256.2011.—An-
thropological and biomechanical research suggests that the human
foot evolved a unique design for propulsion and support. In theory, the
arch and toes must play an important role, however, many postural
studies tend to focus on the simple hinge action of the ankle joint. To
investigate further the role of foot anatomy and sensorimotor control
of posture, we quantified the deformation of the foot arch and studied
the effects of local perturbations applied to the toes (TOE) or 1st/2nd
metatarsals (MT) while standing. In sitting position, loading and
lifting a 10-kg weight on the knee respectively lowered and raised the
foot arch between 1 and 1.5 mm. Less than 50% of this change could
be accounted for by plantar surface skin compression. During quiet
standing, the foot arch probe and shin sway revealed a significant
correlation, which shows that as the tibia tilts forward, the foot arch
flattens and vice versa. During TOE and MT perturbations (a 2- to
6-mm upward shift of an appropriate part of the foot at 2.5 mm/s),
electromyogram (EMG) measures of the tibialis anterior and gastroc-
nemius revealed notable changes, and the root-mean-square (RMS)
variability of shin sway increased significantly, these increments
being greater in the MT condition. The slow return of RMS to baseline
level (⬎30 s) suggested that a very small perturbation changes the
surface reference frame, which then takes time to reestablish. These
findings show that rather than serving as a rigid base of support,
the foot is compliant, in an active state, and sensitive to minute
deformations. In conclusion, the architecture and physiology of the
foot appear to contribute to the task of bipedal postural control
with great sensitivity.
foot deformation; proprioception; human posture control
THE HUMAN FOOT IS A UNIQUE structure, formed by numerous
bones and joints and fastened by the three layers of ligaments.
Human foot bones are arranged to form three strong arches:
two length ways and one across the foot. Ligaments bind the
foot bones together along with the tendons of foot muscles.
This helps to hold our foot bones firmly in the arched position
but still allows some give and springiness. It is known that
during locomotion (especially in running), the foot arch is
subjected to considerable deformations, resulting in elastic
energy storage in the longitudinal foot arch for propulsion.
From the biomechanical viewpoint, the foot is typically con-
sidered as a “functional unit” with two important aims: to
support the body weight (static foot) and to serve as a lever to
propel the body forward in walking and running (dynamic foot;
Bramble and Lieberman 2004; Ker et al. 1987; Morton 1935;
Ridola and Palma 2001). However, support of the body weight
in the erect posture involves not only the counterbalancing of
Address for reprint requests and other correspondence: W. G. Wright, PT
Dept., College of Health Professions, ME Dept., College of Engineering, 3307
N. Broad St., Philadelphia, PA 19140 (e-mail: wrightw@temple.edu).
www.jn.org 0022-3077/12 Copyright © 2012 the American Physiological Society
J Neurophysiol 107: 1513–1521, 2012.
First published December 7, 2011; doi:10.1152/jn.00256.2011.
the gravitational load, but also equilibrium maintenance, which
is dynamic in nature.
The inverted pendulum is often used as a model of bipedal
human posture (Clifford and Holder-Powell 2010; Fitzpatrick
et al. 1994; Gatev et al. 1999; Maurer et al. 2006; Morasso and
Schieppati 1999; Vette et al. 2010; Winter et al. 2001). A
multijoint plant for posture control also typically implies a
rigid foot body (Kiemel et al. 2008). Yet, the two areas, arch
structure and toes, which have been identified as critical in gait
because of the large range of motion displayed in the ankle and
proximal interphalangeal joint, are also involved in posture.
Furthermore, there are additional sources of deformation that
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are of similar magnitude as in the ankle and toes during quiet
standing (QS). For example, there are the longitudinal and
transverse arches as well as the soft tissue on the plantar
surface both under forefoot and calcaneus (Hicks 1955; Scott
and Winter 1993). Accordingly, somatosensory information on
local foot deformations can be provided from numerous recep-
tors in the foot arch ligaments, joint capsules, intrinsic foot
muscles, and cutaneous mechanoreceptors on the plantar soles
(Fallon et al. 2005; Gimmon et al. 2011; Kavounoudias et al.
1998; Magnusson et al. 1990; Meyer et al. 2004; Schieppati et
al. 1995).
What is the role of the vaulted configuration of the foot in
the equilibrium maintenance? In a previous study (Gurfinkel et
al. 1994), we showed that support surface or body inclinations
by approximately 1–1.5° relative to the vertical were accom-
panied by not only the changes in the ankle joint angle, but also
a noticeable plantar surface skin compression. The vertical
displacements of the calcaneus recorded by means of a clamp
rigidly fixed at the heel were 0.5 ⫾ 0.3 mm/° during body tilt
in the anterior-posterior (A/P) direction, and the corresponding
foot compliance was 0.04 ⫾ 0.03°/Nm (foot pitch tilt per unit
torque change in the ankle joint), so that the actual changes in
the ankle joint angle were estimated to be only half of those
expected when considering the foot as a rigid body firmly
attached to the ground (Gurfinkel et al. 1994).
It is also known that under limb loading, the height of the
longitudinal foot arch decreases. In young adults, a navicular
drop and medial longitudinal arch deformation during QS were
5.0 ⫾ 2.2 mm and 3.5 ⫾ 2.6°, respectively (Bandholm et al.
2008). The height of the dorsum changes by ⬃4 mm during
changes in load from 10 to 90% body wt. In the study of
McPoil et al. (2008), the mean difference in dorsal arch height
between nonweight bearing and weight bearing was even 10
mm. These values characterize foot arch deformations under
significant changes in limb loading. However, it might be that
during QS, the foot is also subjected to some deformations due
to the center-of-body-mass (COM) displacements. The extent
of deformations may, in fact, turn out to be not so negligible
1513
1514 FOOT SPECIALIZATION FOR POSTURAL CONTROL
when taking into account the large body weight and, conse-
quently, the large load on the feet. By visual observation alone,
flattening of the foot arch during QS has been reported (Di
Giulio et al. 2009). Therefore, even a small deformation could
yield relatively large errors in the measured changes of the
ankle joint angle. If so, what could be the functional signifi-
cance of such deformations and their consequences?
To answer to these questions, it is important to ascertain the
presence or absence of foot deformations under normal pos-
tural conditions. This was our first goal. In the case of the
positive result and knowing the parameters of deformations,
one might further question what the postural consequences of
specially evoked deformations of the foot arch could be. To
this end, in our study, we 1) quantified foot deformations in the
sitting position under stationary foot loading corresponding
approximately to the amplitude of postural foot pressure oscil-
lations (protocol 1), 2) quantified foot deformations during QS
(protocol 2), and 3) applied very small perturbations of the foot
arch by elevating the metatarsals (MT) or toes during QS
(protocol 3). The results are discussed in context of the con-
tribution of foot deformations to the actual changes of the ankle
joint angle and body sway during QS and their role in the
posture control mechanisms.
METHODS
Subjects
Twelve healthy subjects (8 women and 4 men) between the ages of
26 and 44 (33 ⫾ 5) yr, with an average height of 171.6 ⫾ 7.9 cm, an
average weight of 75.0 ⫾ 15.5 kg, and no known neurological,
vestibular, or neuromuscular impairments participated in this study.
All subjects gave informed written consent to participate in the
institutional review board-approved protocols conducted in this study,
in accordance with local ethical regulations for human subjects studies
and the Declaration of Helsinki.
Equipment and Experimental Paradigm
Protocol 1: quantification of foot arch deformation. To quantify
foot arch deformation under stationary loading (Fig. 1A), subjects
(n ⫽ 7) were seated on a stable armless chair. Its height was adjusted
to keep the thigh approximately horizontal with knees and ankle
slightly flexed past 90° so that the shank vertical orientation was about
the same as that during normal upright standing. The subject was fully
seated without back support with the feet in a natural, relaxed state,
flat on a stable, fixed, horizontal surface (AMTI force plate, Water-
town, MA). A linear displacement transducer (Series 200; Trans-Tek,
Ellington, CT) was placed either on left foot dorsum (Fig. 1A)
approximately over the cuneiform bones but avoiding dorsiflexor
tendons (e.g., extensor hallucis longus) or at the head of the 1st MT
(MT1; in separate trials). The force applied by the transducer was
⬍0.1 N, and no subject was aware of changes in the skin pressure of
the probe on the foot dorsum. This device was placed to measure
changes in the height of the foot arch when loaded and unloaded with
10-kg weight on the knee. The rationale for using a 10-kg weight was
that this load imitates approximately the amplitude of natural oscil-
lations in the forefoot and heel loading during QS. We were interested
here not in the deformations of the foot that occur due to large foot
loadings (Bandholm et al. 2008; McPoil et al. 2008) but rather the
deformations due to a redistribution of loading between anterior and
posterior foot parts caused by displacements of the COM. Given that
the center of pressure (COP) is located 4 –5 cm in front of the ankle
joint axis, redistribution of pressure does not exceed 4 – 8% body wt
during QS. During loading, the weight was slowly placed (within ⬃1 s;
J Neurophysiol • doi:10.1152/jn.00256.2011 • www.jn.org
Fig. 2A) on the knee by the experimenter (W. G. Wright). The subject
was allowed to guide manually lateral stabilization of the weight
during the load and hold period, but the full 10 kg was vertically
loaded on the knee. The weight was then lifted off the knee. Loading
and lifting was repeated at least three times. The mean value of the
dorsum displacement in the vertical direction for the last 2 s of the trial was
used to estimate foot deformations. Trials in which the transducer was
placed over MT1, so that compression of the plantar surface could be
measured during passive 10-kg knee loading, employed a similar
measurement technique. The mean height change of the dorsum was
significantly greater than at MT1 (P ⬍ 0.01; Fig. 2B).
Protocol 2: correlating foot arch deformation and postural sway.
To test the relation between A/P body sway and foot arch deformation
during QS, subjects (n ⫽ 7) stood with eyes closed for 60 s on a fixed,
horizontal AMTI force plate (Fig. 1, B and C) on which COP was
measured. The onset of recording started 5–10 s after the subject
closed his or her eyes in preparation for trial. A linear displacement
transducer was placed on the dorsum of the left foot approximately
over cuneiform bones but avoiding dorsiflexor tendons (e.g., extensor
hallucis longus or in separate trials either at the head of MT1 or on the
toe nail of the hallux). This device was used to measure changes in
foot arch height during active postural control. An angular potenti-
ometer attached to anterior tibia of the left leg was used to detect A/P
change in tibial orientation (i.e., shin tilt). The shin tilt measurement
device included a rigid metal arm (40 cm) connected to a sensitive
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CP-2UK-R250 potentiometer (Midori America, Fullerton, CA). The
metal arm was linked to the lower leg using nonelastic thread attached
to a flat mounting piece (6 ⫻ 1.5 cm) that was strapped around the
lower leg. The lower leg attachment site was at the medial surface of
the tibial shaft, 5–7 cm below the patella (planum tibia). The tibia at
this site has a flat surface, and the thickness of a subcutaneous layer
is small and thus minimizes unwanted shifting of the mounting piece,
which therefore gives accurate measure of the tibia orientation. The
thread linking the metal arm to the tibia was kept taut using the low
restoring force of very thin elastic cords (0.5 mm) connected to the
metal arm in a manner similar to symmetrical guy wires. The sensi-
tivity of this sensor was found to be on the order of the force plate.
Additionally, kinematic data using reflective markers attached to the
skin overlying the ankle and knee joints were collected at 120 Hz
using Motion Analysis (Santa Clara, CA) system cameras during QS
trials to verify the accuracy of the shin tilt measurement device (Fig.
1B). Because of some intrinsic noise, the optoelectronic (Motion
Analysis) system loses sensitivity below 0.2 mm, whereas the linear
transducer was able to detect the correlation of foot dorsum motion
with shin tilt at well below 0.1 mm. Although the shin tilt potenti-
ometer was more sensitive than the camera system, the two devices
showed highly significant correlation with each (r ⫽ 0.88 – 0.98, SD
0.049). Therefore, the data presented in RESULTS refer to those mea-
sures using the angular potentiometer.
Protocol 3: postural response to phalange and metatarsal
perturbations. To examine postural effects after small perturbations to
different parts of the forefoot (Fig. 1D), subjects (n ⫽ 12) stood with
eyes closed with a majority of the posterior part of each foot on a
stably fixed horizontal surface while a small part of the anterior
portion of each foot was on a moveable platform. Specifically, in the
MT condition, heads of the 1st and 2nd MT and the phalanges were
placed on a flat moveable surface that delivered small upward trans-
lations while the posterior part of the foot remained on a stable, fixed
platform. In the TOE condition, only the 1st 3 phalanges were on the
anterior moveable platform, while the 1st and 2nd MT as well as the
rest of the mid- and hind foot were on the fixed platform. It is worth
noting that all our subjects had a classic (non-Morton) form of the
foot, i.e., MT1 was equal or longer than the 2nd MT (Morton 1927).
The anterior moveable platform and the posterior fixed platform
abutted each other with no gap between the two. The surfaces were
level with one another before upward displacements of the anterior
platform. A motorized, torque-driven surface (Neurocom, Clackamas,
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Fig. 1. Experimental setup. A: an analog linear displacement transducer measured foot dorsum changes in height during 10-kg loading and unloading of the knee
while seated (protocol 1). A force plate measures loading force. B: during quiet standing (protocol 2), an angular potentiometer measures anterior
(ANT.)-posterior (POST.; A/P) shin tilt, a force plate measures center of pressure (COP), and the linear transducer measures changes in the height of the foot
dorsum. C: the displacement transducer accurately shows no error when measuring fixed surface height (top trace), whereas the optoelectronic motion analysis
camera system shows up to 0.2 mm of variability when measuring an earth-fixed ground marker (2nd trace). The camera system (3rd trace) and angular pot
(bottom trace) both reliably measured A/P shin tilt, but the former less so because of reduced sensitivity as well as potential skin movement artifacts of the markers
at the ankle and knee joints. deg, Degrees. D, top: a top view of foot placement on moveable and stationary surfaces (protocol 3). In the TOE condition (dashed
line), only 1st through 3rd phalanges are perturbed. In the metatarsals (MT) condition (solid line), the 1st and 2nd MT and all toes are perturbed by a moveable
surface that can move the forefoot upward. A greater portion of the forefoot is positioned on the moveable surface in the MT condition than the TOE condition.
Medial view of TOE condition shows placement of the linear transducer on the hallux toenail, which measures the onset of the upward surface displacement
(bottom left). Similarly, the linear transducer placed on the foot dorsum over the head of the 1st MT (MT1) measures the onset of the surface displacement in
MT conditions (bottom right). In protocol 3, subjects are standing with eyes closed while shin tilt is measured as depicted in B.

OR) was used to deliver the small linear displacements upward such
that the left and right feet received a symmetrical stimulus. In other
words, subjects were perturbed along the A/P direction to induce
sagittal plane postural responses while no stimulus asymmetry existed
along the mediolateral (M/L) axis. To validate the absence of any
systematic response asymmetry along the M/L axis, we performed
analyses of the M/L COP as well. Full trials lasted 60 s, divided into
10 s of eyes-closed QS followed by 50 s of eyes-closed standing
postperturbation. The preperturbation period was a variable length
with 10 s before perturbation used as a baseline for comparison with
the postperturbation period. Four displacement magnitudes of the
anterior platform were 1.5, 3.0, 4.5, and 6.0 mm, which were ran-
domly delivered at 2.5 mm/s. The 2.5 mm/s speed was chosen because
it is in the range of normal COP velocity during QS. Although no
earphones were used, ambient noise made it impossible to hear the
perturbation since the perturbations were so small and the system is
driven by very-low-noise motors. Often, the subject reported no
conscious awareness that the stimulus had occurred.
The shin tilt measurement device described in protocol 2 was used
to measure A/P postural responses. Because the majority of the foot
was on the posterior fixed platform with only the forefeet on the
moveable platform (Fig. 1D), during displacement of the anterior

J Neurophysiol • doi:10.1152/jn.00256.2011 • www.jn.org

1516 FOOT SPECIALIZATION FOR POSTURAL CONTROL

RESULTS

Foot Arch Deformation Measures

Fig. 2. A: static weight loading of the knee deforms the foot arch as measured
by a linear displacement transducer placed on foot dorsum (top trace). A force
plate measuring 10-kg weight loading onto the seated subject’s knee (bottom
trace) shows high correlation with the foot arch deformation. B: the average
height change (⫾ SD) across subjects as measured by the linear transducer
placed on the head of the MT1 (black) or on the foot dorsum (white) was
significantly less at the MT1 compared with the dorsum (P ⬍ 0.01) during
static loading.
platform the part of the subject’s weight was lifted off the posterior
AMTI force plate. As a result, the COP showed an obvious posterior
shift, since the AMTI force plate uses body weight (FZ) to calculate
In protocols 1 and 2, the measures from the linear displace-
ment transducer showed changes in the foot arch height with
weight loading in a passive state (sitting posture) and their
correlation with changes in kinetic (COP) and kinematic (shin
tilt) measures during active postural control. Specifically, in
protocol 1, loading and unloading a 10-kg weight on the knee
lowered and raised the foot arch, respectively, on average
1.3 ⫾ 0.47 mm. Placement of the transducer on the foot
dorsum at the head of MT1 allowed measurements to be taken
at this location to rule out plantar skin compression as the cause
for the change in foot arch height (Fig. 2B). Loading of the
knee would presumably compress the plantar pads under the
extra weight, however, our measures revealed that ⬍50% of
the magnitude of the foot arch height change could be ac-
counted for by skin compression.
In protocol 2, we characterized natural foot arch deforma-
tions during QS. The amplitude (peak-to-peak) of foot dorsum

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COP. An analysis of FZ revealed that 9.2 ⫾ 2.1% in MT or 4.5 ⫾
1.5% in TOE was lifted off the AMTI force plate after the moveable
platform lifted up the forefoot. In this case, COP is not representa-
tive of a postural response, rather it indicates the mechanical conse-
quence of removing part of the FZ load from the posterior force plate
onto the anterior force plate. Therefore, in this protocol, shin tilt was
used as the kinematic measure of A/P postural response rather than
COP. Analysis of these two variables conducted in protocol 2 showed
significant correlation between A/P COP and shin sway (r ⫽ 0.84 ⫾
0.09, P ⬍ 0.00001), and thus this measure of A/P sway was highly
reliable (Fig. 3).
A linear displacement transducer was placed on the hallux toenail
in the TOE condition or on the foot dorsum on the head of MT1 in the
MT condition. This was used to measure how much of the upward
surface displacement was transferred through the fat padding on the
plantar surface of the foot to the supporting musculoskeletal structure.
Electromyogram (EMG) of tibialis anterior (TA) and lateral gastroc-
nemius (GAST) of the same leg as transducer and shin tilt were
collected during perturbation trials. Surface electrodes were placed 5
cm apart to collect a differential EMG signal that was amplified
2,000 –5,000 times, low-pass filtered below 30 Hz, and full-wave-
rectified. All measurement devices were controlled by one central
computer, which synchronized and collected the force plate, dorsum
displacement, and shin tilt data at 120 Hz and EMG data at 1,000-Hz
sampling rate.

Data Analysis
The shin tilt, displacement transducer, and COP data were
filtered using a low-pass 4th order Butterworth filter with a 5-Hz
cutoff frequency. Changes in TA and GAST activity were analyzed
both relative to the baseline measure (before perturbation) and with
regard to those in the antagonist muscle (see RESULTS). Descriptive
statistics included means ⫾ SD. Statistical comparisons included
repeated-measures general linear models multivariate analysis of
variance, paired t-tests, and Pearson correlation coefficients. The
nonparametric Fisher exact test was used to make binomial com-
parisons. Significance was set at ␣ ⱕ 0.05, with Bonferroni cor-
rections applied when multiple comparisons with the same time
series were made.
Fig. 3. A: raw data from 2 different subjects showing that longitudinal foot arch
displacement, as measured by linear transducer placed over the foot dorsum
(top trace), is highly correlated with A/P shin tilt, as measured by angular
potentiometer attached (2nd trace). A/P COP (3rd trace) is also highly
correlated with foot arch and shin tilt, but mediolateral (M/L) COP (bottom
trace) is not. B: overall subject averages of the trial-by-trial correlation of shin
tilt with height displacement of the hallux toenail (gray), head of the MT1
(black), and the foot dorsum (white) all have high negative correlations with
shin tilt (left plot). Overall subject averages (⫾ SD) of the height change
(peak-to-peak amplitude of vertical oscillations) of the TOE, MT1, and dorsum
during eyes-closed quiet standing (right plot) are shown. Corr. coeff., corre-
lation coefficient.

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 FOOT SPECIALIZATION FOR POSTURAL CONTROL 1517

displacements was approximately 0.2– 0.9 mm across subjects

(Fig. 3B) and that of the shin tilt was 1.5– 4.1°. Analysis of the
foot arch deformation and the shin sway revealed a significant
correlation between the two measures ranging from r ⫽ 0.70 to
0.90, with an average r ⫽ 0.81 ⫾ 0.07 (P ⬍ 0.0001) during QS
with eyes closed. Anterior shin tilt correlated with flattening of
the foot arch and posterior tilt with the foot arch rising (Fig. 3).
Correlations with similarly high significance were found be-
tween foot arch displacements and A/P COP (r ⫽ 0.70 ⫾ 0.09,
P ⬍ 0.0001; Fig. 3). Correlations of M/L COP with foot arch
displacements were weak ranging from r ⫽ ⫺0.36 to 0.04 with
an average of r ⫽ ⫺0.14 (Fig. 3A, bottom curves).

Postural Response to Surface Perturbations of the Foot

In protocol 3, perturbed standing showed measurable
changes in the shin tilt and EMG (TA and GAST), correspond-
ing to the displacement onset of the anterior platform. Overall,
the lift of the platform resulted in greater mean values of the lift
of the phalanges in the TOE condition than the phalanges and
MT in the MT condition. For instance, a 3-mm perturbation
resulted in 1.84 ⫾ 0.27- and 2.46 ⫾ 0.29-mm vertical displace-

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ments in the MT and TOE condition, respectively. Thus more
compression of the plantar surface skin occurred in MT than in
TOE, which means on average the toes were displaced by the
stimulus more during TOE than MT perturbations. Despite
this, however, postural responses were significantly more pro-
nounced in the MT compared with the TOE conditions. The
postural response occurred ⬍600 ms after perturbation onset
on average. A 3-s window was chosen that represents a period
greater than long-latency postural phasic responses and 1 s
greater than the slowest responses observed across trials (la-
tencies ranged from 0.3 to 2.1 s). The 10 s of QS preceding the
perturbation was divided into three 3-s windows excluding the
first second and then averaged to ensure that variability mea-
sures were not biased by the length of the window. The average
shin tilt variability during the 9 s of QS preceding the pertur-
bation was 0.31°. The average shin tilt variability during 3 s
immediately after the perturbation was 0.50 ⫾ 0.45° in MT and
0.24 ⫾ 0.29° in TOE. As perturbation magnitude increased
from 1.5 to 6 mm, the magnitude of the shin tilt response also
increased, however, this change was not significant in either
the MT (P ⬎ 0.10) or TOE conditions (P ⬎ 0.5; Fig. 4B).
The shin tilt measure showed different outputs depending on
the foot perturbation condition, MT or TOE. In the MT
conditions, an initial passive response to surface perturbation
was typically evident whereby the shin tilted backward as MT1
was pushed upward. This was considered to be a passive,
mechanical response and was evident in the 87% of the trials,
whereas in the TOE condition a clear passive response was
evident in only 33% of the trials. After the initial passive
response, the subject either responded with a compensatory
anterior shin tilt or continued backward typically at a different
rate than during the passive response. In the MT condition,
30% of the responses resulted in posterior shin tilt, and 59%
were anterior compensatory responses, whereas 11% showed
no clear directional shin tilt. In the TOE condition, 30% were
posteriorly directed responses, 49% were anterior compensa-
tory responses, and 35% showed no clear shin tilt response.
Many of the trials showing no response in shin tilt occurred
J Neurophysiol • doi:10.1152/jn.00256.2011 • www.jn.org
Fig. 4. Shin tilt changes with surface perturbation. A: dark solid traces show
mean shin tilt (solid line) in the posterior direction, which occurs after the
upward surface displacement (vertical dashed line). Note that the postural
response has a latency often ⬎500 ms after the surface perturbation. The 95%
confidence envelopes are shown by light dotted lines. MT condition (left
column) and TOE condition (right column) shin tilt responses at 3 displace-
ment amplitudes show increasing response with increasing surface displace-
ment amplitude. MT condition responses are larger than TOE condition
responses. All postural responses show a delay. B: group means for each
condition shows significantly larger means of absolute shin tilt in MT com-
pared with TOE at all surface displacement amplitudes. Error bars show 95%
confidence interval (CI).
during low amplitude surface perturbations (i.e., 1.5 and 3 mm)
in the TOE condition.
Another measure of postural response that showed clear
changes was the root-mean-square (RMS) of shin tilt, pre- and
postperturbation. The shin tilt RMS increased significantly in
both the TOE (F3,25 ⫽ 20.5, P ⬍ 0.0002) and the MT
conditions (F3,25 ⫽ 39.8, P ⬍ 0.00001) compared with base-
line variability during QS. However, the increase in RMS was
significantly greater in the MT condition (P ⬍ 0.009). Further-
more, on average, shin tilt RMS did not return to baseline level
for at least 30 s (Fig. 5, shin tilt traces).
EMG Response to Surface Perturbations of the Foot
EMG measures of the TA and GAST revealed measurable
changes in muscle activity corresponding to the perturbation
1518 FOOT SPECIALIZATION FOR POSTURAL CONTROL

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Fig. 5. Electromyogram (EMG) responses to foot perturbation. A: small perturbation (⬍4 mm) at 10 s (dotted line) lifts MT. EMGs of tibialis anterior (TA) or
gastrocnemius (GAST) and A/P shin tilt data from 3 representative subjects reveal that even if the majority of the foot is supported on a stable, fixed surface,
a postural response to small toe or MT perturbation occurs. Root-mean-square (RMS) shin tilt postperturbation is greater than quiet stance preperturbation.
B: during surface perturbations, subjects either responded with an increase in GAST and decrease in TA muscle activity typically during forward lean (Œ), an
increase in TA and decrease in GAST muscle activity typically during backward lean (□), or no clear change in muscle activity (⽧). C: the absolute change in
EMG activity (AbsEMG) in TA and GAST was significantly greater in the MT than in the TOE condition.

onset, which significantly correlated with A/P sway direction
(Fig. 5A). On average, the absolute change in EMG activity
was 43.1% relative to the 10-s baseline measure of EMG
activity before surface perturbation in each trial. For each
muscle, this percentage change was normalized as a ratio of the
mean EMG activity (␮emg) during the 3-s (t1 ⫽ 10 s to t2 ⫽ 13
s) postperturbation minus the mean activity during the 10-s (t0
to t1) baseline QS before perturbation and then divided by the
baseline QS activity. The ratio was multiplied by 100 to give
the outcome as a percentage (Eq. 1).
change in EMG (i.e., ␦muscle) of the GAST (␦GAST) and the TA
(␦TA) with each other (Fig. 5B). A highly significant difference
in EMG activity was apparent between the GAST and TA
when these trials were divided into their respective response
types (F2,37 ⫽ 13.7, P ⬍ 0.00005). The no-response trials,
however, did not show a difference between the muscle activ-
ity of the GAST and TA. We used this as further justification
that the no-response trials could not be classified as a clear
muscle response to the perturbation. Specifically, the Diffemg
between GAST and TA muscle activity (Eq. 2) in the no-

ⱍ ⱍ t1 response trials could have reached a maximum of 50% if one

␮emg t2
t1 ⫺ ␮emg t0
␦emg ⫽ 100 ⴱ
ⱍ
(1)
␮emg t1
t0
With the median absolute change in EMG activity found to
equal 25%, this was used as a threshold for a reliable leg
muscle response to the surface perturbation. Among the trials
that showed a clear EMG response, the anterior and posterior
leg muscles sometimes worked reciprocally, i.e., when the TA
increased, GAST decreased or vice versa, however (see also Di
Giulio et al. 2009), we also observed trials with little or no
response in the agonist as well as coactivation resulting in a net
increase in leg muscle activity. An analysis of A/P shin tilt
response relative to the difference in GAST and TA (Diffemg)
revealed a highly significant correlation (r ⫽ 0.65, P ⬍
0.00001) with forward shin tilt corresponding to increasing
Diffemg (Eq. 2), i.e., increasing GAST and/or decreasing TA.
Since the majority of trials could be clearly divided into TA or
GAST responses, an analysis of the signed activity (Eq. 1) in
each of these response types was performed that compared the
J Neurophysiol • doi:10.1152/jn.00256.2011 • www.jn.org
muscle increased by 25%, whereas the other decreased by
25%. However, the average of the absolute differences
៮ , Eq. 3) was only 13% for no-response trials
(AbsDiff emg
compared with 160% in the GAST and TA response trials
(where n equals either the number of trials found with
significant TA and GAST responses or the number of
no-response trials).
Diffemg ⫽ ␦GAST ⫺ ␦TA (2)
兺 ⱍ␦GAST ⫺ ␦TAⱍ
n
៮ i⫽1
AbsDiffemg ⫽ (3)
n
The above evidence suggests that small surface perturba-
tions elicited an EMG response in the legs in both MT and
TOE conditions. Further analysis of the two surface conditions,
MT and TOE, revealed significant differences in their EMG
responses. First, as mentioned above, a significant correlation
(r ⫽ 0.65) exists between A/P sway and leg muscle activity,
 FOOT SPECIALIZATION FOR POSTURAL CONTROL
Diffemg (Eq. 2), however, in the MT condition, this correlation
was r ⫽ 0.75 (P ⬍ 0.0000), whereas in the TOE condition, a
weaker correlation of r ⫽ 0.31 (P ⫽ 0.02) was observed. A
comparison of the absolute change in EMG activity revealed
significantly more activity following MT perturbation than
TOE perturbation (F1,23 ⫽ 7.73, P ⫽ 0.01). In other words, the
sum of absolute EMG change (|␦GAST| ⫹ |␦TA|) was greater in
MT than TOE trials. Finally, using the 25% threshold for
no-response trials and performing a nonparametric analysis of
the number of above threshold responses vs. no-response trials
showed that 33% were above threshold in the TOE condition
trials, whereas in the MT condition, 56% were above threshold,
a significantly higher EMG response rate (Fisher exact test,
P ⫽ 0.01, 1-tailed).
DISCUSSION
Overall, the results confirmed our hypothesis with respect to
the presence of significant foot deformations (Figs. 2–3). Tak-
ing into account very small body oscillations during QS, these
deformations are remarkable (⬃0.5–1 mm) and might signifi-
cantly affect the afferent outflow from the foot mechanorecep-
tors (and about the ankle joint angle in particular) during
maintenance of orthograde posture. Furthermore, a very small
perturbation to either the phalanges or MT evoked noticeable
changes in the EMG activity and postural sway (Figs. 3–5).
Interestingly, these changes could exceed the duration of per-
turbation by tens of seconds (see Fig. 5, shin tilt traces),
suggesting a potential disturbance of the postural reference.
Postural Foot Deformations
Under full limb loading, the height of the foot dorsum
decreases by a few millimeters (Bandholm et al. 2008; McPoil
et al. 2008). It is worth emphasizing, however, that during
normal standing, a relatively small redistribution of loading
between forefoot and heel occurs due to A/P COM displace-
ments. Here, we quantified variations in the height of the foot
dorsum under relatively small changes in limb loading com-
parable with postural adjustments. In sitting position, loading
the 10-kg weight on the knee lowered the foot arch by about
1–1.5 mm (Fig. 2). More than 50% of this change could be
accounted for by the foot arch deformation and the rest by
plantar surface skin compression (by skin compression, we
imply pressing out and changing the shape of the foot soft
tissues, since the body liquid per se is incompressible). Also,
although we assumed that the foot behaves as an elastic body,
it could not be ruled out that a part of the foot deformation was
due to its plasticity (e.g., that of the soft tissues of the sole).
During standing, the foot arch probe and shin sway revealed
a significant correlation, which shows that as the tibia tilts
forward, the foot arch flattens and vice versa (Fig. 3). It is
unlikely that changes in the linear displacement transducer
height were simply due to compression of dermal padding on
plantar surface of the feet (Gurfinkel et al. 1994), for a few
reasons. The transducer was placed at a point between the
anterior and posterior parts of the foot (i.e., the cuneiform
bones). Thus, when the A/P COP shifts from front to back, this
will compress the calcaneal fat pad while reducing compres-
sion of the forefoot fat pad, so measurement at the fulcrum of
this lever-like action would not show a change at the midfoot
dorsum. However, if the foot height changes were due to
J Neurophysiol • doi:10.1152/jn.00256.2011 • www.jn.org
1519
conformational changes of the foot arch as A/P sway occurs,
then a net change in foot dorsum height would be expected.
Most work uses ankle joint angles determined from opto-
electronic systems. Our findings clearly show that, depending
on the marker position, the drop in the foot arch or deformation
of soft tissues may have significant influence on the actual
measured ankle angle. Moreover, taking into account very
small changes in the ankle joint angle and a distributed or
nonuniform deformation of different parts of the foot during
standing (see Fig. 6 with a schematic foot model), one cannot
be sure that the actual ankle joint angle is being measured.
Furthermore, different muscles of the ankle joint or even
different compartments of the same muscle may show coun-
terintuitive changes in muscle length during postural body tilts
due to the different attachment geometry and flattening of the
foot (Di Giulio et al. 2009). There might also be large inter-
individual differences in the degree of deformation of the soft
tissues of the foot (Gurfinkel et al. 1994). Moreover, such
interindividual differences in foot compliance may affect pos-
tural responses to support surface perturbations (Gurfinkel et
al. 1994). Further investigations are needed to determine the
exact mechanism of these differences and the extent of foot
compliance changes in different populations as well as adap-
Downloaded from on August 26, 2014
tations throughout development (for instance, due to soft tissue
distribution and foot shape in infants; Bertsch et al. 2004;
Hallemans et al. 2006).
The observed foot dorsum displacements (⬃0.5 mm; Fig. 3)
are not negligible. Taking into consideration a short distance
between the transducer and the ankle joint (5–7 cm; Fig. 1B),
the estimated errors in the ankle joint angle due to foot
deformations (⬃0.5/50 mm ⫽ 0.01 rad or 0.6°) are in fact of
the same order as angular oscillations of an inverted pendulum
(about 0.5–1°) that is often used as a model representing
bipedal posture (Fitzpatrick et al. 1994; Gatev et al. 1999;
Maurer et al. 2006; Morasso and Schieppati 1999; Winter et al.
2001). Given also a plantar surface skin compression that
further attenuates the actual changes in the ankle joint angle by
Fig. 6. Schematic representation of distributed foot deformations during
standing. A: the axes of all the foot joints (except for those of the middle 3 rays)
adapted from radiographs of the experimental foot. Original figure by W. G.
Wright, Y. P. Ivanenko, and V. S. Gurfinkel, adapted from Hicks (1953).
B: simplistic model of the foot (sagittal plane) composed of several parts
behaving as an elastic beam.
1520 FOOT SPECIALIZATION FOR POSTURAL CONTROL
a factor of almost two (Gurfinkel et al. 1994), the hypothetical
ankle joint angle oscillations and the corresponding changes in
the calf muscle length may be minute if any (or even opposite
in sign) during natural A/P postural body displacements. Fur-
thermore, high tendon compliance (Rack et al. 1983) and
“paradoxical” calf muscle lengthening/shortening during un-
disturbed human standing (Loram et al. 2007, 2009) also
question the usage of a simple control scheme of human
standing based on the stretch reflex in the ankle joint muscles.
Therefore, sensory input arising from notable deformations of
the foot arch and soft tissues may provide important (or at least
complimentary) information about postural body sway and/or
postural reference.
Postural Responses to TOE and MT Perturbations
It is worth stressing that the foot represents an important
receptive field, formed by numerous skin, joint, tendon, and
muscular receptors (including intrinsic foot muscles), and it
has long been recognized that damage to the foot, be it either
by sensorineural loss or physical damage to the muscles, bones,
or supporting tissues, changes posture and gait stability. A
number of cutaneous and load-related reflexes may participate
in the fine control of posture or foot positioning during walking
(Abbruzzese et al. 1996; Aniss et al. 1992; Duysens et al. 2000;
Ivanenko et al. 2002; Kavounoudias et al. 1998; Nardone et al.
2000; van Wezel et al. 1997; Yang and Stein 1990). For
instance, loss of cutaneous sensation may lead to less stable
posture and locomotion (Courtemanche et al. 1996; Dingwell
and Cavanagh 2001; Meyer et al. 2004; Perry et al. 2000;
Taylor et al. 2004). In addition, support surface may also be
included as a component of our ego space in a similar way as
external objects and tools can be included in our body scheme
(Iriki et al. 1996; Ivanenko et al. 1997; Pearson and Gramlich
2010; Solopova et al. 2003; Wright and Horak 2007). The
tactile information from the main supporting areas of the foot
is also used by the brain for perceptual purposes and can evoke
strong kinesthetic illusions (Roll et al. 2002), vibrotactile
thresholds being lower in the ball and arch of the sole than in
the heel and toe regions (Gravano et al. 2011; Inglis et al.
2002).
Here, we found that perturbing MT or toes affects human
posture (Fig. 4), consistent with the previous studies that input
from the foot helps in the control of upright human balance
(Fujiwara et al. 2003; Ivanenko et al. 1997; Kavounoudias et
al. 2001; Priplata et al. 2006). Perturbing MT affected posture
more than perturbing toes. It is interesting that these small
perturbations evoked both immediate (with a latency of 0.3–2.1
s; Fig. 4) and long-lasting (tens of seconds; Fig. 5) effects. The
slow return to baseline state (Fig. 5, shin tilt traces) might be
due to a change in the foot-related reference frame similar to
what we observed previously in postural responses to very
slow support inclinations (Gurfinkel et al. 1995; Wright and
Horak 2007). Compensations in the reference perturbation
seem to take more time than compensations of postural devi-
ations from a reference position (see also Bove et al. 2009).
These data support the hypothesis that, besides operative con-
trol assigned to compensate quickly for deviations from a
reference position, the system of postural control includes at
least one additional level, which elaborates this reference using
information about mutual position of body links, muscular
J Neurophysiol • doi:10.1152/jn.00256.2011 • www.jn.org
torques, and interaction with the support (Fujiwara et al. 2003;
Gurfinkel et al. 1995; Wright 2011).
Conclusions
With over 100 muscles, tendons, and ligaments, 26 separate
bones, and 33 joints, the foot and specifically the arch likely
evolved for a role as specialized as the thumb and fingers did
for fine manual control (Rolian et al. 2010). Despite this, many
postural studies tend to focus on the simple hinge action of the
ankle joint without taking into account the distributive nature
of foot deformations. Here, we show that the foot, rather than
serving as rigid base of support, is in an active, flexible state
and is sensitive to minute perturbations even if the entire hind
and midfoot is stably supported and the ankle joint is unper-
turbed. We also found that perturbing MT affects posture more
than perturbing toes. The slow return to baseline posture after
a very small perturbation to the phalanges or the 1st and 2nd
MT may be due to a change in the surface reference frame.
Subsequent to a change in the surface reference frame, it takes
time to reestablish the new frame of reference. These findings
suggest that the entire neurophysiology and anatomic architec-
ture of the foot are uniquely designed for and integral to
Downloaded from on August 26, 2014
performing the complex task of bipedal postural control, a fact
overlooked by some ankle-axis inverted pendulum models and
postural control theories that focus suprapedally.
GRANTS
This research was supported, in part, by National Institute of Neurological
Disorders and Stroke Grant NS-45553 and the European Union Seventh
Framework Programme (FP7)-Information and Communication Technologies
(ICT) Programs (AMARSi Grant no. 248311).
DISCLOSURES
No conflicts of interest, financial or otherwise, are declared by the author(s).
AUTHOR CONTRIBUTIONS
W.G.W., Y.P.I., and V.S.G. conception and design of research; W.G.W.,
Y.P.I., and V.S.G. performed experiments; W.G.W. analyzed data; W.G.W.,
Y.P.I., and V.S.G. interpreted results of experiments; W.G.W. and Y.P.I.
prepared figures; W.G.W. and Y.P.I. drafted manuscript; W.G.W., Y.P.I., and
V.S.G. edited and revised manuscript; W.G.W., Y.P.I., and V.S.G. approved
final version of manuscript.
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