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Brazilian Journal of Motor Behavior
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!
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van Leeuwen,
Bruijn, van Dieën
2022
VOL.16
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Mechanisms that stabilize human walking
A. M. VAN LEEUWEN
1,2
| SJOERD M. BRUIJN
1,2
| JAAP H. VAN DIEËN
1
1
Department of Human Movement Sciences, Faculty of Behavioural and Movement Sciences, Vrije Universiteit Amsterdam, Amsterdam Movement Sciences, Amsterdam,
The Netherlands.
2
Institute of Brain and Behavior Amsterdam.
Correspondence to: Sjoerd M. Bruijn!
Email: s.m.bruijn@gmail.com
https://doi.org/10.20338/bjmb.v16i5.321
ABBREVIATIONS
α
i
Angular acceleration of the i
th
Segment
CoM Center of mass
CöM Acceleration of the COM
CoM′ Position vector of the vertical
projection of the COM on the
ground
CoP Center of pressure (position vector
of the point of application of the
ground reaction force F
g
)
com
i
Position vector of the center of
mass of the i
th
segment
com
"
i
Linear acceleration of the i
th
segment
Fg
y
Vertical component of the ground
reaction force
𝐻
$
Change of angular momentum
around the body center of mass
l
i
Moment of inertia of the i
th
segment
m Body mass
m
i
Mass of the i
th
segment
n Number of segments
r
e
Position vector of the point of the
application of an external force F
e
PUBLICATION DATA
Received 04 11 2022
Accepted 14 12 2022
Published 15 12 2022
ABSTRACT
In this paper, we review what mechanisms are used to stabilize human bipedal walking. Based on mechanical
reasoning, potential mechanisms to control the body center of mass trajectory are modulation of foot placement,
stance leg control by modulation of ankle moments and push-off forces, and modulations of the body’s angular
momentum. The first two mechanisms and especially the first are dominant in controlling center of mass
accelerations during gait, while angular momentum control plays a lesser role, but may be important to control
body alignment and orientation. The same control mechanisms stabilize both steady-state and perturbed gait in
both the mediolateral and antero-posterior directions. Control is at least in part active and is affected by
proprioceptive, visual and vestibular information. Results support that this reflects a feedback process in which
sensory information is used to obtain an estimate of the center of mass state based on which foot placement and
ankle moments are modulated. These active feedback mechanisms suggest training approaches for populations
at risk of falling, through perturbations, augmented feedback, or constraining one mechanism to train the other
mechanisms.
KEYWORDS: Gait stability | Foot placement | Stance leg control | Angular momentum | Falls
1.INTRODUCTION
Stabilizing bipedal walking to avoid falls is challenging. This is readily apparent in
toddlers who learn to walk and usually master this only after many falls have occurred. At
the other end of the age spectrum, age-related but also disease-related impairments often
also cause problems in stabilizing gait. However, then the resulting falls are much more
problematic, as they often have serious adverse consequences, such as injury, fear of
falling, loss of independence, and social isolation
1,2,3
. Training interventions have been
successful at reducing fall rates in older adults
4
and in patients at high risk of falling
5
.
However, in our opinion, new training approaches to improve gait stability and methods to
assess and understand changes in gait stability can be derived from a better understanding
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Brazilian Journal of Motor Behavior
Special issue:
Effects of aging on locomotor patterns
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van Leeuwen,
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2022
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of the mechanisms that are used to stabilize gait. In an earlier review, we covered foot
placement as the most dominant mechanism used to stabilize gait
6
. In this review, we
expand on this and provide an overview of gait stability control mechanisms and an outlook
on how insight into these mechanisms could be used to identify potential training
approaches.
For the purpose of this review, we will pragmatically define ‘stable’ gait as gait that
does not lead to falls. This requires control of the position of the body center of mass relative
to the base of support. In gait, the base of support is formed by those parts of the feet that
are in contact with the floor at any point in time. In humans, a large part of the total body
mass is located high above a small base of support, particularly in single stance.
Consequently, small deviations in body orientation result in substantial gravitational
moments that can easily move the center of mass away from the base of support. Therefore,
even the small variations in the center of mass position that occur in unperturbed gait need
to be corrected, to avoid cumulative effects over time. Thus ongoing (intermittent or
continuous) stabilization is needed. When a perturbation occurs, which can here be defined
as any external mechanical event that disturbs the relation between the center of mass and
base of support beyond the variance observed in unperturbed gait, it is evident that
stabilizing control is required. However, it is not evident that the same stabilizing
mechanisms are used for the small deviations during unperturbed gait and for the larger
deviations after perturbations.
Stabilization of gait can be achieved by passive and active mechanisms. Passive
stabilization relies on the passive mechanical properties (stiffness, damping and inertia of
the human body), whereas active mechanisms involve modulation of neural drive and
muscle activity in response to sensory information. Passive mechanisms may thus be
efficient, as in requiring low control effort and energy costs, but may not be amenable to
change for example by training. Active mechanisms are presumably more adaptive to task
requirements in the short term and may be more amenable to improvement by training in the
long term. Note that active and passive mechanisms may be used in parallel.
As mentioned above, stabilization of bipedal walking is challenging. Nevertheless,
a simple two-dimensional (sagittal plane) model of a bipedal walker can be stable without
any form of active control. In such a model, the forward fall of the center of mass is controlled
on a step-by-step basis through adequate foot placement resulting from the model’s passive
dynamics
7
. The ground contact force after foot placement creates a backward moment,
which catches the forward fall. However, these passive models cannot deal with
perturbations of realistic magnitude and also three-dimensional versions are unstable in the
mediolateral direction
8
. This indicates that additional active control must be exerted to
horizontally accelerate the center of mass in the desired direction, when the center of mass
deviates from its planned trajectory due to errors in control or external perturbations.
Modelling the human body as a system of linked rigid segments, we can write the
acceleration of the center of mass as
!"#$
%
&
!the sum of three mechanisms
9
:
(
"
!
#$%&'
)
×*
!
+,
(
$%-#$%&'
)
×*
"
#.
/
0($%& #$%& ')
' "#$
%
(1)
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in which r
e
is the position vector of the point of application of an external force F
e
,!
"#$
′ is the position vector of the vertical projection of the center of mass (CoM) on the
ground, center of pressure (CoP) is the position vector of the point of application of the
ground reaction force F
g
,
(
)
!
(
)
is the change of angular momentum around the body center
of mass, and m is the body mass. The coordinate system is according to the ISB
recommendations: X-axis forward, Y-axis vertically upward, Z-axis to the right. Note this has
effects on the sign of the contribution of each of the three terms in the numerator on the right.
The denominator of the left-hand term consists of the product of body mass and the
height of the center of mass above the ground, which we will assume to be constant for now.
This leaves us three terms to consider:
(
𝑟
#
−𝐶𝑜𝑀
$
)
×𝐹
#
*
(
𝐶𝑜𝑃−𝐶𝑜𝑀
$
)
×𝐹
%
*
𝐻
-
*
Each of these terms reflects a mechanism to horizontally accelerate the center of
mass and hence a potential mechanism to stabilize gait. We will first consider the unipedal
stance phase of steady-state gait for each of these terms and then consider what is different
in bipedal stance.
Regarding the first term, external forces can be applied by grabbing hold of for
example a handrail, but also by foot placement or stepping. We will exclude mechanisms
like grabbing a handrail and focus on the only ‘external force generation’ that is considered
part of normal walking, i.e., stepping or foot placement. R
e
can be controlled by placing the
swing leg’s foot at the desired location and F
e
can be controlled by adjusting the swing leg’s
stiffness when reaching that location. Foot placement can also be seen as changing the
base of support and center of pressure and hence part of the second mechanism, in which
case the current term does not need to be considered. From this perspective, it is obvious
that foot placement has the advantage that it allows a shift of the center of pressure beyond
the original base of support. Given that clearly different responses at the joint level underly
these two mechanisms, we prefer to keep them separate and treat foot placement as the
generation of an external force. In double support, choosing a new foot placement location
is not an option.
Considering the second term, changes in the position of the CoP and the ground
reaction force are largely determined by actions of the stance leg. We will therefore refer to
the mechanism described by this term as stance leg control, to differentiate it from the first
mechanism foot placement. The center of pressure is always underneath the stance foot,
but it can be shifted within the foot contact area by means of ankle moments. Since CoP and
CoM’ are both on the ground, the horizontal accelerations of the center of mass due to this
term are further only dependent on the vertical component of the ground reaction force (Fg
y
in equation 2).
(
𝐶𝑜𝑃−𝐶𝑜𝑀
$
)
×𝐹
%
=
/
𝑥
&'(
−𝑥
&')
0
𝑧
&'(
−𝑧
&')
3
×
4
𝐹𝑔
*
𝐹𝑔
+
𝐹𝑔
,
6
=
4
−(𝑧
&'(
−𝑧
&')
)𝐹𝑔
+
(𝑧
&'(
−𝑧
&')
)𝐹𝑔
*
−(𝑥
&'(
−𝑥
&')
)𝐹𝑔
,
(𝑥
&'(
−𝑥
&')
)𝐹𝑔
+
6
(2)
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The vertical ground reaction force can be modified to induce horizontal accelerations
as well, but this would be at the ‘cost’ of a vertical acceleration of the center of mass and
would not allow independent control of the mediolateral and anteroposterior acceleration of
the center of mass. In double support, the center of pressure can be shifted over a larger
area than in single support by modulating the ground reaction forces on both legs, e.g.,
pushing off more or less with either leg.
The third mechanism is creating a change in angular momentum of the body, which
equates to changing the moment of the ground reaction force relative to the center of mass.
The rate of change of angular momentum of a system of linked rigid segments equals:
𝐻
-
=
∑
(
𝑐𝑜𝑚
-
−𝐶𝑜𝑀
)
×𝑚
-
:
𝑐𝑜𝑚
;
-
−𝐶𝑜𝑀
;
<
+𝐼
-
𝛼
-
- ./
- .0
(3)
in which com
i
*
is the position vector of the center of mass of the i
th
segment, m
i
is the
mass of the i
th
segment, cöm
i
is the linear acceleration of the i
th
segment, I
i
is the moment of
inertia of the i
th
segment, α
i
is the angular acceleration of the i
th
segment, and n is the number
of segments to be considered.
As this equation shows, the horizontal acceleration of the center of mass can be
controlled by accelerating body segments with respect to the center of mass. Examples of
the use of this mechanism are the ‘hip strategy’
10
, involving trunk flexion for anteroposterior
stabilization after large perturbations of standing, and the arm movements used when
balancing on a slackline
11
. The use of this mechanism is in principle not different between
single and double support, except that leg segments (of the swing leg) can only be used in
single support.
In summary, horizontal acceleration of the body’s center of mass can be achieved
through three mechanisms: 1) generating an external force on the body by making contact
with the environment, 2) shifting the center of pressure of the ground reaction force within
the current base of support, 3) changing the angular momentum of body segments around
the center of mass
9
. The mechanisms described can be separated analytically, but in reality,
they will often interact. For example, changing the center of pressure without simultaneously
changing the direction of the ground reaction force will change the moment of the ground
reaction force relative to the center of mass and hence the angular momentum.
Observations from unperturbed gait can be used to assess the usage of the three
stabilizing mechanisms. In addition, perturbations of gait and changes in stabilization
demands (e.g., walking on a narrow beam versus a normal surface) have been employed to
probe their usage and the relevance of the observations for stabilization. This can provide a
first indication of whether training each mechanism could be useful. However, not only the
extent to which each mechanism plays a role, but also the extent to which this is the result
of passive dynamics or of active control is an important consideration, as only actively
controlled mechanisms would form a feasible target for training. Based on the model studies
mentioned above, this is likely to be different for control in the anteroposterior and
mediolateral directions.
In the subsequent sections of this review, we will summarize and discuss the
literature on the three mechanisms to stabilize gait identified above. For each mechanism,
we will first describe the evidence that it is actually used in the control of steady-state human
gait. We will then assess whether and how the usage of these mechanisms changes in
response to external perturbations. Next, we will discuss the sensory information and the
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actuation underlying each of the mechanisms. For each of these topics, we will compare
control in the mediolateral and anteroposterior directions. Finally, we propose and discuss
some training approaches based on these mechanisms. We will start with foot placement as
this has received more attention in the literature and is considered the dominant mechanism
to stabilize gait.
2. THE THREE MECHANISMS DURING UNPERTURBED WALKING
2.1 Foot placement
Foot placement has extensively been discussed in our previous review
6
. We will
therefore only briefly summarize the main findings here.
To stabilize gait in the mediolateral direction, foot placement should be lateral to the
extrapolated center of mass position, that is a weighted sum of the center of mass position
and its velocity
12
. By placing the foot with a lateral offset relative to the extrapolated center
of mass, the sideward movement of the body center of mass towards the lateral edge of the
base of support will be reversed. This can of course be achieved by: (1) taking such wide
steps that the feet are always placed lateral to the extrapolated center of mass position, or
(2) by regulating foot placement, so that it’s just lateral to the extrapolated center of mass
position. For the latter, both an adequate estimate of the state of the center of mass with
respect to the feet, as well as sufficient ability to control the swing leg to place it at the
appropriate position are needed.
Supporting regulation of foot placement on a step-by-step basis, Wang and
Srinivasan
13
showed that as much as 80% of the variance in deviations from average
mediolateral foot placement could be explained by deviations from average in mediolateral
pelvis position and speed at midstance, and this was much more than could be explained
from swing leg state at midstance. The pelvis state used here can be considered a
reasonable proxy for center of mass state in unperturbed walking, with an offset difference
between sacrum marker and center of mass position
14
that does not affect the model used.
Positive coefficients in the model for both state variables indicate that when the pelvis is
displaced too far lateral or moves in this direction too fast, a more lateral placed step will
follow, and vice versa. These results thus suggest a stabilizing feedback mechanism. In
terms of equation 1, r
e
is determined by foot placement and the resulting change of (r
e
-
CoM) will correct deviations in center of mass velocity or position towards the average value.
The predictive value of the model increased for center of mass states from early swing
onwards and plateaued around mid-swing
13
, suggesting that foot placement location is
selected based on information obtained until this phase of the gait cycle. For anteroposterior
foot placement, predictors of foot placement were pelvis anteroposterior velocity plus
mediolateral pelvis position and velocity. Similar to mediolateral foot placement, increased
velocity of the pelvis predicts more forward foot placement. The coefficients for mediolateral
pelvis state in this model indicate that for example rightward pelvis perturbations at right leg
mid-swing imply shorter right steps. The variance explained by this model at mid-swing was
much lower than for mediolateral foot placement, at about 40%, and increased rapidly right
after foot placement, suggesting that pelvis state is adjusted to foot placement in the early
stance phase. This indicates that in this phase other stabilizing mechanisms may be used
for anteroposterior control of the center of mass.
The models proposed by Wang & Srinivasan
13
were successfully applied to data
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from several other studies on mediolateral control
15,16,17,18,19,20,21,22,23
and to data from one
other study on anteroposterior control
13,24
. Jin et al.
24
showed that, as for mediolateral foot
placement, the anteroposterior center of mass position and velocity in the corresponding
direction only provide a good prediction of anteroposterior foot placement, supporting a more
parsimonious model for the control of foot placement than the original model
13
. In these
studies, the relative variance explained by the model and the RMS of the residual error were
used as measures for the quality of foot placement coordination and these measures were
shown to be sensitive to perturbations, ageing, pathology, fall risk and effects of enhanced
feedback
16,18,25
.
It is important to note, that foot placement also subserves other goals than
stabilization of gait, such as achieving intentional changes in velocity (speed and direction
12
) and avoiding obstacles or selecting suitable foot holds
26
. Some of these goals may
coincide. For instance, control of gait speed may well coincide with control of gait stability
27
and may in fact be inseparable from it.
2.2 Stance leg control
Stance leg control can shift the center of pressure in the mediolateral and
anteroposterior directions, respectively through ankle inversion/eversion and
plantar/dorsiflexion. Moreover, push-off can modulate the ground reaction force. In equation
1, stance leg control thus determines the following term: (CoP-CoM')×F
g
. The term (CoP-
CoM') then reflects ankle moment control to shift the center of pressure, whereas, F
g
can be
modulated through push-off.
In section 2.1, we already alluded to the use of other stabilizing mechanisms to
compensate for errors in foot placement. During steady-state walking, stance leg control is
indeed used to (partially) correct for foot placement errors, through shifting the center of
pressure and through push-off
24,28
. As the foot extends further in the anteroposterior as
compared to the mediolateral direction, more (effective) center of pressure modulation can
be achieved in the anteroposterior direction. However, despite the limited width of the foot,
mediolateral center of pressure modulation during single stance also functions as a
stabilizing mechanism during steady-state walking
28,29,30
.
During steady-state walking, ankle moment control is used in the mediolateral
direction, since the foot placement error, i.e. the residual of the foot placement model
described in section 2.1, predicts the mediolateral center of pressure shift during single
stance
28
. That these center of pressure shifts act as a stabilizing mechanism, is likely, as
they disappear when walking with external lateral stabilization
30
. So mediolateral ankle
moments correct for foot placement errors to stabilize gait during the new stance phase. In
addition, ankle moments in the previous stance phase can stabilize gait preceding placement
of the new stance leg
31
. This allows for an early correction, before foot placement can take
effect
32,33
, but might also be used to steer foot placement. Suggesting a steering role of
ankle moments, targeted stepping is preceded by an early center of pressure shift during
single stance
34
. A similar mechanism may be used during steady-state walking to steer foot
placement to comply with stability demands.
Motorized push-off, perturbations and modelling results suggest that push-off
modulation can contribute to mediolateral gait stability
35,36
. External lateral stabilization
seems to diminish active push-off modulation
37
, as the vestibulomotor coherence of the
medial gastrocnemius decreased during stabilized walking
37
. But, whether push-off
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modulation is indeed implemented to stabilize gait in the mediolateral direction remains to
be investigated.
For the anteroposterior direction, it has been shown that foot placement errors are
corrected during double stance, achieved mainly through force generated by the trailing leg,
which is in turn mainly determined by the sagittal plane ankle moment
24
. This push-off
mechanism also contributes to the trailing leg’s trajectory and hence to reaching a targeted
location
26
. It thus seems likely that during steady-state walking, push-off is used as a
corrective mechanism for anteroposterior foot placement of the leading leg as well as to
control the trajectory of the trailing leg.
Although the above-mentioned evidence shows that stance leg control contributes
to stable steady-state walking, the lower relative explained variance of steady-state ankle
moment control models, as compared to foot placement models
24,28
, reflects its lesser
importance compared to the foot placement mechanism.
2.3 Angular momentum changes
Formula 1 indicates that next to foot placement (section 2.1) and stance leg control
(section 2.2), changes in angular momentum can be used to stabilize gait. Early work on
angular momentum during unperturbed human walking has shown that it is tightly regulated,
and some authors have even suggested that the goal is to keep a near zero angular
momentum
38,39
. Indeed, angular momentum has been shown to be increased in patient
populations, and the increase in angular momentum was correlated with worse scores on
clinical balance measures
40,41
. However, as walking inherently requires movement of the
limbs which will bring about a (change in) angular momentum, it is hard to tease apart
changes in angular momentum, which are explicitly aimed at stabilizing the center of mass
trajectory, from those that happen simply due to movements necessary for progression.
One way to tease these effects apart may be to make other stabilizing mechanisms
less available, such that subjects must rely more on angular momentum control. Indeed,
angular momentum control was largely responsible for maintaining standing balance on a
beam of only 4mm width
42
. On the other hand, when standing on balance boards which
could rotate in the mediolateral
43
, or antero-posterior direction
44
, the CoP mechanism was
dominant, with contributions of angular momentum changes often in the opposite direction
of the CoP mechanism. In a recent experiment, we tested whether subjects use angular
momentum control in walking, when their other possibilities to stabilize gait are diminished
45
. Subjects walked on a treadmill in a control condition, a condition wearing shoes which
restrict the use of the ankle mechanism, and in a condition in which they both wore these
shoes and were instructed to walk with narrow steps. The idea was that these conditions
would increasingly limit use of the other stabilizing mechanisms. Results showed that indeed
changes in angular momentum contributed more to center of mass accelerations during the
harder conditions, but the effect of foot placement also remained substantial. From this, we
concluded that the use of angular momentum changes may be limited, probably because
angular accelerations ultimately need to be reversed in view of anatomical constraints and
because of interference with other task constraints, e.g., interference with the gait pattern.
Using changes in angular momentum to affect (linear) center of mass acceleration will
inevitably lead to changes in body orientation, which may also lead to altered visual and
vestibular inputs, which in and of itself may be perturbing. All in all, it seems that humans
can use angular momentum changes to stabilize steady-state gait, but that they do so to a
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limited extent.
3. PERTURBED WALKING
Above, we described how foot placement, stance leg control, and angular
momentum are used in unperturbed gait. When gait is perturbed, it could be that control is
different, because some mechanisms may be more (or less) effective for perturbed gait, or
because all available means need to be used to recover from a perturbation. In this section,
we will describe the use of the three mechanisms when gait is mechanically perturbed by for
instance a push, pull, trip, or slip. We have chosen not to describe studies studying
responses to sensory (illusory) perturbations here, and instead use these as evidence for
which sensory information is used to control the three mechanisms (see section 4).
3.1 Foot placement
Foot placement has as advantage that r
e
(equation 1) can be quite large, or in other
words, it shifts the CoP over a large distance compared to stance leg control, and this of
course also holds during perturbed walking. Hof et al
46
, showed that after mediolateral
perturbations, foot placement does require at least 300 ms (which they estimated to be about
30% of a stride), but has a range of 20 cm. They also showed that after a perturbation, if
reaction time is sufficient, the foot is placed at a more or less constant distance outward of
the extrapolated center of mass. When the available reaction time was too short, further
responses during the next step were observed. Later studies by Vlutters
47,48
showed similar
results, namely that recovery from mediolateral perturbations involved mediolateral foot
placement adjustments proportional to the mediolateral center of mass velocity
47
, and that
the adjustments in mediolateral foot placement decreased when the perturbation onset was
closer to the instant of foot contact
48
.
In the antero-posterior direction, neither forward nor backward mechanical
perturbations caused an increase in the distance between the center of pressure at foot
contact and the center of mass at foot placement
47
. While it is not clear whether this implies
no adjustment in step length relative to the stance foot, it does indicate that swing leg control
was not effectively adapted to accommodate changes in center of mass.
Like for intrinsic variations during steady-state walking
13
, foot placement responses
during perturbed walking can be predicted by a linear model with pelvis kinematic state
variables as predictors
49
. Interactions between foot placement and stance leg control (push-
off and ankle moments) to stabilize gait (i.e. when one mechanism is used more, another
mechanism is used less) also appear to generalize across steady-state and perturbed
walking contexts, at least in the mediolateral direction
31
. This suggests that similar control
strategies may underlie foot placement responses to perturbations and the intrinsic
variations of a steady-state gait pattern.
3.2 Stance leg control
Reactive center of pressure shifts and the associated ankle moments have been
reported for mechanical perturbations. For the sake of clarity, we will discuss these
responses per dimension, and only for studies distinguishing clearly between ankle moment
and foot placement control (i.e. studies that do not compute these two mechanisms as a
single center of pressure mechanism).
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Mediolateral pushes and pulls to the pelvis lead to fast ankle moment responses
before foot placement
46
. This underscores a benefit of shifting the center of pressure under
the stance foot relative to foot placement; stance leg control can take effect before foot
placement, and as such, ensure more continuous stabilizing control. Furthermore, Brough
et al
50
showed that center of pressure shifts correct for errors in foot placement in perturbed
walking
28
. When perturbing the foot to be placed too medial, this resulted in an inversion
response and vice versa. Similar ankle responses were reported in response to mediolateral
pelvis perturbations
51
.
As mentioned in section 3.1, unlike mediolateral pelvis perturbations, mechanical
perturbations in the anteroposterior direction, did not cause adjustments in foot placement
with respect to the center of mass at the first foot placement after the perturbation
47
. This
indicates that responses in the stance phase, which are partially the result of changes in
ankle moments
51
, accommodate anteroposterior perturbations more effectively than
mediolateral perturbations. Given the difference in anteroposterior and mediolateral
dimensions of the feet, this is not surprising. In response to anteroposterior perturbations at
toe-off, stance leg control responded to the perturbation during single stance
51
and during
the double stance phase
52
, to attenuate the effect on center of mass velocity. However,
when constraining such center of pressure shifts, by limiting the base of support to a point
contact, foot placement was adjusted after anteroposterior perturbations
53
. This shows that
people can switch from a stance leg to a foot placement mechanism if needed, for example
when stepping on a narrow ridge.
A recent model simulation study found that pelvis perturbations in anteroposterior
direction at toe-off could be fully recovered by shifting the center of pressure during double
stance
52
. However, humans do not appear to implement this control mechanism to its full
extent, leaving part of the perturbation’s effect to be attenuated later in the gait cycle
52
.
3.3 Angular momentum changes
The commonly observed flailing of the arms after large perturbations of walking
would suggest that angular momentum changes do play a (major?) role in stabilizing gait at
these moments. However, such arm movement may have other functions, such as reaching
for support or to break an eventual fall, or to affect body orientation rather than center of
mass position as more extensively discussed below. In a recent study on standing balance
54
, in which participants received rotational perturbations of the platform they were standing
on, we indeed found that the rate of change of angular momentum did not directly contribute
to return of the center of mass within the base of support. Instead, the changes in angular
momentum in that study seemed aimed at reorienting the body to an aligned and vertical
configuration. Our recent findings in walking seem to agree with this; after a perturbation,
changes in angular momentum contributed negatively to center of mass accelerations
55
.
Other studies also indicate limited use of angular momentum changes to correct
perturbations. For instance, in a study in which subjects wore pin shoes while undergoing
perturbations
53
, the authors reported an increased reliance on foot placement, with no
changes in trunk movements. In another study
50
, in which foot placement was perturbed by
means of a push to the foot, both medial and lateral foot placement perturbations led to a
decrease in hip abduction moments. While such a decrease could be understood as
stabilizing after a medially directed perturbation, it is harder to understand for laterally
directed perturbations. Interestingly, when angular momentum itself is perturbed directly, by
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a simultaneous push and pull perturbation, a recovery of the angular momentum was seen
directly after the perturbations
56
.
A recent study
57
showed that when the arms were bound during a slip, participants
were three times as likely to fall. During a slip, angular momentum cannot be used to create
horizontal accelerations of the center of mass (as there is no friction with the floor). Hence,
the positive effects of having arm movements during a trip most likely stem from the fact that
this limits rotation of the body, by instead rotating the arms. This would then mean that this
is a strategy with a different aim. Two studies from our own group indeed have shown such
an alternative aim for changes of angular momentum of the arms after a trip. The ongoing
movements of the arms after a trip supported lengthening of the recovery step in both young
and older adults and thus optimized foot placement
58,59
. However, the arms did not directly
contribute to acceleration of the center of mass in the desired direction. Regulating the
body’s angular momentum may thus be more important in terms of changes of the orientation
of the body. All-in all, it seems that angular momentum changes play a minor role in
controlling the center of mass after a perturbation, as we also concluded for unperturbed gait
and the same limitations may apply.
4. SENSING AND ACTUATION OF THE THREE MECHANISMS
To assess the active nature of the three mechanisms, studies have combined
kinematic and electromyography measures while changing stabilizing demands, such as
through external lateral stabilization and by applying (sensory) perturbations. The advantage
of sensory perturbations is that the first response observed is active, whilst for mechanical
perturbations early active and passive responses to the mechanical perturbations can
coincide. As such, sensory perturbations can provide additional understanding of the control
mechanisms during steady-state walking. Mechanical perturbations on the other hand may
be able to elicit larger effects, so stronger responses may be observed.
4.1 Sensing and actuation of foot placement
For steady-state walking, the correlation between center of mass state and foot
placement
13
described in section 2.1 has been interpreted as reflective of active control, but
it could also result from passive coupling of movements of the leg to the movements of the
upper body
60
. For mediolateral foot placement, it has been shown that lowering stabilization
demands, by increasing prescribed step width, decreases the strength of the coupling
between mediolateral center of mass state and foot placement
15,23
. This phenomenon is
even clearer when subjects walking on a treadmill are externally stabilized by a spring-
loaded construction, creating a force-field that corrects mediolateral deviations of the center
of mass
19
. These findings suggest that the correlation between center of mass state and
foot placement reflects a form of active control that is relaxed under less demanding
conditions.
Mechanical simulation indicates that active control over both mediolateral and
anteroposterior foot placement can be achieved by modulating activity of many muscles,
including ipsilateral swing limb gluteus medius, iliopsoas, rectus femoris and hamstrings and
the contralateral stance limb gluteus medius and ankle plantarflexors. These contributions
are not necessarily achieved by directly driving the swing leg relative to the pelvis, but also
have effect through contributions to pelvis power
61
. In strong support of active control of
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mediolateral foot placement, studies on steady-state walking have shown associations
between mediolateral foot placement and activity of stance and swing leg gluteus medius
activity and swing leg adductor longus activity
20,62,63
. The idea that active control underlies
the correlation between mediolateral center of mass state and foot placement is further
supported by studies on the effects of sensory illusions induced by proprioceptive
16
,
vestibular
33,64
, or visual stimulation
65
on this correlation. Finally, destabilizing gait by
mediolateral oscillation of the visual scenery caused increased step-to-step variance of
center of mass excursion and mediolateral foot placement in association with changes in
variance of gluteus medius muscle activity
66
. For anteroposterior foot placement, we are not
aware of studies that have assessed the relation with muscle activity. We remind the reader
that passive walker models can be stable in this direction through passive ‘adjustments’ of
foot placement
8
, which implies that humans may successfully exploit their passive dynamics
and actively intervene only when needed, for example after larger perturbations.
Work by Hof and Duysens
67
has focused on the neural underpinnings of
mediolateral foot placement control when mechanically perturbed. They found that two quick
responses in gluteus medius activity following a medial perturbation of the center of mass
trajectory can be found, one at 100 and one at 170ms after perturbation onset, as well as a
late response at 270ms after perturbation onset. These responses were all phase
dependent, and showed facilitation during swing, and suppression during stance, both
opposite to the background activity. The authors stated that this suggests premotoneural
gating of these responses, and thus, rather low-level control.
If the correlations between center of mass state and swing with foot placement
reflects active feedback control, this suggests that the center of mass state can be estimated
from sensory information. As described above, proprioceptive, vestibular and visual
information affect foot placement, and this would suggest that these sensory modalities are
used to obtain such an estimate. Additional information may be provided by pressure
sensors in the foot soles
68
. While substantial work on the integration of sensory information
for control of the center of mass in standing has been performed e.g.
69
, much less is known
on this process in walking. However, it has been suggested that proprioceptive information
from the lower extremities is weighted less in walking than in standing
70
.
4.2 Sensing and actuation of stance leg control
Ankle moments inducing center of pressure shifts during gait are at least in part
actively controlled as they are associated with peroneus longus, tibialis anterior and soleus
muscle activity, in both unperturbed
28
and perturbed
31,32,51,65,71,72
walking. In general, ankle
moment control is considered to be fast
32,65
, and, based on muscle activity latencies, it has
been attributed to phase-dependent reflexive pathways connected to visual
65
and vestibular
systems
31
, likely involving supraspinal neural connections
32,53,72,73
. Thus, ankle moment
control seems to be guided by the integration of different sensory modalities. That ankle
moment control is centrally regulated is underscored by ankle muscle activity in response to
mechanical perturbations, despite blocking of the ankle joint, which excludes spinal level
feedback-control based on local proprioceptive information alone
72
. Further evidence that
stabilizing ankle moments are not (only) determined by peripheral sensory information from
the ankle joint and surrounding muscles comes from a modelling study
73
. This study showed
that delayed feedback of ankle angles and angular velocities could not explain reactive ankle
moments, whereas delayed feedback of the center of mass kinematic state (position and
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velocity) could explain these responses. It thus seems that ankle moments are controlled
based on similar sensory information as foot placement. This is in line with visual
65
and
vestibular perturbations
31
evoking both foot placement and ankle moment responses. It is
especially noteworthy that, in response to such sensory perturbations, ankle moments show
the earliest response
65
. This is in accordance with what was observed in mechanical
perturbation studies
32,46
.
4.3 Sensing and actuation of angular momentum changes
Even though it is unclear how much angular momentum changes contribute to
controlling the center of mass, it is obvious that angular momentum must be controlled in
order to maintain an upright orientation. While the angular momentum strategy has also been
coined the “hip strategy”, there are many more joints (and muscles) that may contribute to
control angular momentum. As a matter of fact, actuation of most muscles will lead to a
change in angular momentum. Using simulations, Neptune and McGowan
74
found that in
early stance, hip and knee extensors (gluteus maximus and vastii), hamstrings and tibialis
anterior generated backward angular momentum, while the soleus and gastrocnemii
generated forward momentum. In late stance, the soleus generated primarily forward
angular momentum while the gastrocnemii generated backward angular momentum.
In a follow up study, Neptune and McGowan
75
studied which muscles contribute to
changes in angular momentum in the frontal plane. This study showed that in early stance,
the vastii, adductor magnus and gravity tended to rotate the body towards the contralateral
leg while the gluteus medius tended to rotate the body towards the ipsilateral leg. In late
stance, the gluteus medius still tended to rotate the body towards the ipsilateral leg while the
soleus and gastrocnemius tended to rotate the body towards the contralateral leg.
In both these studies, the head, arms and trunk were modelled as a HAT unit, and
hence, no statements were made about the (potential) role of arm movements. Either way,
these studies clearly shows that the angular momentum strategy entails more than simple
movements at the hip.
5. TRAINING POSSIBILITIES
We have thus far discussed how foot placement, stance leg control, and angular
momentum are used to stabilize healthy human walking, both unperturbed, and perturbed.
We have done so in view of the fact that gait stability declines with ageing and many
diseases. Thus, a better understanding of how gait is stabilized may lead to opportunities to
help those with problems. In this section, we give an outlook of how our understanding of
the three mechanisms might help to identify training targets and methods. Assuming, based
on the preceding sections, that each mechanism is a feedback-controlled process and that
the mechanisms may compensate for each other, we propose four categories of training
possibilities. In unperturbed walking, stability can be maintained without optimally exploiting
feedback control. For example, older adults coordinate their foot placement less well to their
center of mass state than young adults, but they maintain a steady-state and hence stable
gait pattern by means of a larger average step width
16
. It can thus be assumed that specific
manipulations may be needed to trigger and train the use of these stabilizing feedback
control mechanisms. The first option may be to apply perturbations of the trajectory of the
center of mass that are large enough to require an active stabilizing response, which, as
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shown above, will involve at least the two most important stabilizing mechanisms. Second,
understanding of the feedback mechanisms can be used to specifically target the outcome
of the feedback processes, e.g., perturbing foot placement away from the expected position.
Third, training approaches could constrain the use of one of the three mechanisms, such
that the other mechanisms must be used more and hence are trained. Fourth, training
methods could augment the natural feedback process, by increasing the sensory feedback
available, in the hope that subjects are then able to (re-)learn the appropriate control. Except
for general perturbation-based training, there is, as yet, limited or no evidence for
effectiveness of each of these training approaches, so this section merely aims to provide
an outlook that may be used for future work.
5.1 Perturbation-based training
Perturbation-based training is considered a promising tool to improve gait stability
and reduce fall risk, which has received rapidly growing interest in literature, for reviews on
this topic we refer to
76-78
. Studies have found effects on fall risk in daily life, with reductions
in falls up to 50%
79,80
, although such effects may depend on training dosage and differ
between treadmill and overground training
81
.
Repeated exposure to slip- and trip-like perturbations has been shown to cause
improved recovery responses in which the state of the center of mass relative to the base of
support is better controlled
82-89
. This is in part accounted for by improved foot placement, as
reflected in larger margins of stability at recovery step foot placement after training
86,88,89,90,91,92
. However, improved recovery responses were also associated with lesser
deviations in trunk movement after the perturbation
86,92-94
, which are most likely accounted
for by improved stance leg control
87,95
. After slip perturbations, the improved control was
also due to a reduced displacement of the base of support or slip severity
82,83,85,96
, which
can be accounted for by changes in pro-active control and by changes in stance leg control
to better maintain the body mass positioned above the sliding foot.
A single study explored sensory perturbations to perturb gait as a training tool
97
.
Mediolateral shifts of the visual scenery projected in front of a treadmill perturbed foot
placement, and this resulted in a decreased variability of the margins of stability in
unperturbed walking after the training. This is a clear indication of an improved coordination
of foot placement relative to the center of mass state. Transfer and retention of these effects
remains to be studied.
All in all, perturbation-based training is a promising approach for training of gait
stabilization, and its effects can be partially understood based on improvements in the
stabilizing mechanisms discussed in this paper. However, none of the studies discussed
was specifically designed with the aim of assessing changes in these mechanisms, so it is
impossible to discern which mechanisms are best targeted with which type of perturbations.
5.2 Specific perturbation training
Specific perturbation training interferes directly with the feedback mechanisms
described. This approach has been implemented by perturbing mediolateral foot placement
relative to the expected foot placement based on the predictive models described in section
3.1. Improved mediolateral foot placement control was found in healthy participants
98,99
and
in chronic stroke patients
99
. The perturbations diminished the degree of foot placement
control as an immediate effect, but with prolonged exposure, the degree of foot placement
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control increased
98,99
. Since these adaptations persisted as an after-effect, it shows that the
degree of mediolateral foot placement control in steady-state walking can indeed be
improved, but retention has not been reported.
Another study in older adults
100
used leg pulls to perturb the anteroposterior
trajectory of the swing leg, simulating a trip-like perturbation during training and testing.
Training resulted in a further forward foot placement relative to the extrapolated center of
mass at the first and second step after the perturbation. This effect was maintained after 1.5
years after only two training sessions, one at baseline and one 14 weeks later. This result
indicates that perturbation training may improve anteroposterior foot placement after
perturbations with long-term effects.
5.3 Constraint-based training
Constraining compensatory mechanisms can be seen as a potential to (re-)train the
use of a certain mechanism. For instance, walking while other stabilizing mechanisms are
constrained could be used to train foot placement. This can in part be achieved with shoes
that provide a limited base of support and hence do not allow center of pressure shifts.
Constraints on mediolateral center of pressure shifts, induced an initial decrease in the
degree of mediolateral foot placement control, followed by a gradual increase during training
22
. However, despite a trend, no significant after-effects were found. It appears that this may
in part be due to an additional constraint on foot placement, which was the result of training
and testing on a split-belt treadmill, which forces participants to take wider steps to avoid the
gap between the belts
101
.
On a single-belt treadmill, ankle moment constraints do not perturb foot placement.
Instead, in young neurologically-intact adults, the degree of foot placement immediately
increased above baseline during training
101
. For older adults, who walked during several
training sessions with shoes constraining center of pressure shifts on a single-belt treadmill,
no improvements in foot placement were seen within a session. Moreover, no consistent
after-effects were demonstrated at the end of the training sessions. However, in normal
walking, foot placement precision improved over sessions
102
. A limitation of this study was
that it did not contain a control group, and hence, it cannot be distinguished whether it was
the ankle moment constraint or the repeated treadmill walking that induced these effects.
With this in mind, we make the cautious interpretation that constraining ankle moments may
hold training potential. Furthermore, for the interventions and training interventions outlined
above, it should be investigated whether the observed training effects on a treadmill translate
towards over ground walking.
In the previous section, we discussed the possibility of training foot placement
through constraining ankle moments. In a similar vein, one might expect that constraining
foot placement would help in training center of pressure shifts. Walking on a virtual narrow
beam elicited smaller mediolateral center of mass excursions at lower speed, in young as
well as older adults, indicating that other stabilizing mechanisms than foot placement were
enhanced to compensate for constrained foot placement
103
. Unfortunately, when explicitly
testing whether constraining foot placement caused improvements in the use of center of
pressure shifts, no immediate effect was found
20
. Nonetheless, constraining foot placement
is a commonly used training tool
104,105
, which has shown positive effects on gait, but
mechanistic effects on gait stabilization have not been studied.
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5.4 Augmented feedback
Augmented feedback aims to enhance the information used in a feedback process
by providing an artificial stimulus enhancing the available sensory information. Augmented
proprioception may provide a tool to enhance the degree of foot placement control
21
.
Applying timed tendon vibration to either the stance, or the swing leg, depending on what
complied with the current center of mass kinematic state, helped to better coordinate foot
placement with respect to the center of mass kinematic state
21
. This likely entails an
increased signal-to-noise ratio of the relevant sensory information. Although this improved
the degree of foot placement control while the vibration was applied, it has not yet been
investigated whether augmented proprioception leads to beneficial training effects.
Moreover, this mechanism has thus far only been applied to improve foot placement. We
can in principle envision it working to enhance the other mechanisms as well, as all would
be dependent on correct use of sensory information to estimate the center of mass state.
6. DISCUSSION
We have discussed three gait stability mechanisms which can be distinguished
analytically. We have shown that foot placement control is dominant and is complemented
by stance leg control, either as an early response to a perturbation or to correct for foot
placement errors. Moreover, changes in angular momentum do not seem to contribute
directly to linear center of mass accelerations, and instead may be used to control the
orientation of the body, or be used only when all else fails. Both foot placement and stance
leg control are at least partly active in nature, not only in response to perturbations, but also
during steady-state walking. Actively controlled mechanisms suggest trainability, and we
proposed potential of perturbations, constraints, and sensory augmentation as training
approaches.
6.1 Control of stability is based on center of mass state
Based on the literature reviewed above, it seems likely center of mass kinematic
state information is used to control both foot placement and ankle moments. However, based
on current evidence, we are unable to conclude whether it is really the center of mass or a
related variable like pelvis state relative to the stance foot that is sensed. Responses to
visual and vestibular perturbations, as well as modelling results discussed above show gait
stabilization is not (solely) driven by local (such as hip or ankle joint angle) information. Given
that proprioceptive, visual, and vestibular information all seem to contribute, humans likely
use an estimate obtained through sensory integration, which provides a close proxy of the
center of mass. However, it may be hard to experimentally verify whether it is really the state
of the center of mass that is sensed and used to stabilize gait, or whether it is some related
state variable.
Either way, it seems that the sensory information that is obtained during gait is used
in a flexible manner, with changes in the information used at different timescales. For
instance, stretch reflexes and vestibular coupling to muscles show modulations over the gait
cycle
37,106
, and sensory down-weighing of vestibular information over the course of seconds
or minutes
107,108
. Thus, the information that is used to stabilize gait most likely comes from
multiple sensory systems, is combined in a flexible manner, and provides an estimate of the
center of mass state.
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Lastly, although sensory perturbations provide strong indications for the feedback
nature of control mechanisms during steady-state walking, they may evoke responses larger
than those required for the intrinsic variations of steady-state gait. Therefore, it is hard to
interpret whether sensory perturbations trigger responses reflecting “steady-state control” or
“reactive control”. Then again, the evidence presented here suggests that during perturbed
and unperturbed walking similar control mechanisms are employed.
6.2 Gait speed modifies contributions of stabilizing mechanisms
Walking at different speeds influences the contribution of the available stability
mechanisms. Although foot placement is dominant during walking, the degree of foot
placement control decreases with decreasing speeds
17,20
. One may argue, that given the
longer stance times during slow walking, the contribution of stance leg control may increase,
and thus foot placement control can be loosened. In a perturbation study, it was indeed
shown that ankle moment control contributed more at lower speeds
31
. Yet, in contrast,
during steady-state walking, the contribution of ankle moment control appeared higher in
normal as compared to slow walking
28
. The use of sensory information, which may
contribute to gait stabilization also appears to be speed dependent. Closing the eyes had
more effect on variability of foot placement in the anteroposterior direction at low speeds,
while effects in the mediolateral direction were similar across speeds from 20 to 80% of
maximum walking speed
109
. Effects on balance control of illusions of mediolateral movement
caused by vestibular stimulation decreased between slow (0.8 m/s) and very slow (0.4 m/s)
walking
107,110
. Some additional information can be obtained from studies on pathology. In
line with experimental work, vestibular deficits and peripheral neuropathy had more effect
on step time variability at low than high speeds
111,112
. A study on bilateral vestibular loss
was associated with a large mediolateral foot placement variability specifically at high
speeds, and with a large anteroposterior foot placement variability at low speeds
113
.
However, the latter study quantified variability by means of a coefficient of variation and
simultaneous changes in mean values make this outcome somewhat difficult to interpret.
Overall, gait stabilization appears to be more dependent on sensory feedback at low speeds.
However, the speed dependence of gait stabilization is at present incompletely described
and understood. Given the fact that individuals at risk of falling often change their gait speed,
a better understanding of the effects of speed is warranted.
6.3 Antero-posterior and mediolateral control
Although one generally looks for mediolateral responses (e.g., changes in ankle
moments) in response to mediolateral perturbations/variations and vice versa for
anteroposterior responses in response to anteroposterior perturbations/variations,
stabilization is not independent between these directions, Therefore, mediolateral and
anteroposterior mechanisms must be coordinated to stabilize gait
13,32,48
. For example, ankle
moments can speed up anteroposterior center of pressure shifts to shorten stance, allowing
foot placement control to take effect earlier in accommodating mediolateral perturbations
32
.
Although, to our knowledge, so far, this mechanism has only been reported in relation to
perturbations
32
, adaptations in stride frequency and the duration of specific stride phases
are considered stabilizing mechanism in steady-state walking as well
20,114,115
. Moreover,
push-off, a clear antero-posterior mechanism
24
, also has effects in the mediolateral
direction, due to the moment arm of the ground reaction force with respect to the center of
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mass in this direction
116
. In addition, ankle muscles causing in-/eversion (see section below),
also have a plantar/dorsiflexion component and vice versa. Thus, while we (and a lot of the
literature) have focused on control in one specific direction/plane, there are effects of these
mechanisms in other planes as well. Perhaps, future research should focus more on such
interactions.
7. CONCLUSION
We have discussed how human bipedal gait is stabilized using foot placement,
stance leg control, and angular momentum changes. The first two mechanisms and
especially the first are dominant in controlling center of mass accelerations during gait, while
angular momentum changes play a lesser role, but may be important to control body
alignment and orientation. The same control mechanisms stabilize both steady-state and
perturbed gait in both mediolateral and antero-posterior directions. Control is at least in part
active and is affected by proprioceptive, visual and vestibular information. Results support
that this reflects a feedback process in which sensory information is used to obtain an
estimate of the center of mass state based on which foot placement and ankle moments are
modulated. These mechanisms suggest training approaches for populations at risk of falling,
such as mechanically perturbing gait stability, specifically perturbing or augmenting the
effective use of the stabilizing mechanisms, or using their complementary nature to train one
mechanism by constraining the other mechanisms.
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BJMB! ! ! ! ! ! ! !
Brazilian(Journal(of(Motor(Behavior(
(
!
van Leeuwen,
Bruijn, van Dieën
2022
VOL.16
N.5
351 of 351
!
Special issue:
Effects of aging on locomotor patterns
Citation: van Leeuwen AM, Bruijn SM, van Dieën JH. (2022). Walking speed does not affect age-differences in ankle
muscle beta-band intermuscular coherence during treadmill walking. Brazilian Journal of Motor Behavior, 16(5):326-
351.
Editor-in-chief: Dr Fabio Augusto Barbieri - São Paulo State University (UNESP), Bauru, SP, Brazil. !
Associate editors: Dr José Angelo Barela - São Paulo State University (UNESP), Rio Claro, SP, Brazil; Dr Natalia
Madalena Rinaldi - Federal University of Espírito Santo (UFES), Vitória, ES, Brazil; Dr Renato de Moraes – University
of São Paulo (USP), Ribeirão Preto, SP, Brazil.
Guest editors: Dr Paulo Cezar Rocha dos Santos - Weizmann Institute of Science, Rehovot, Israel; Dr Diego Orcioli
Silva - São Paulo State University (UNESP), Rio Claro, SP, Brazil.
Copyright:© 2022 Van Leeuwen, Bruijn and van Dieën and BJMB. This is an open-access article distributed under the
terms of the Creative Commons Attribution-Non Commercial-No Derivatives 4.0 International License which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: MvL and SMB were funded by a grant from the Netherlands Organization for Scientific Research
(016.Vidi.178.014).
Competing interests: The authors have declared that no competing interests exist.
DOI:!https://doi.org/10.20338/bjmb.v16i5.321