Neurorehabilitation and Neural Repair
http://nnr.sagepub.com
Stroke Affects Locomotor Steering Responses to Changing Optic Flow Directions
Anouk Lamontagne, Joyce Fung, Bradford McFadyen, Jocelyn Faubert and Caroline Paquette
Neurorehabil Neural Repair 2010; 24; 457 originally published online Jan 12, 2010;
DOI: 10.1177/1545968309355985
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Research Articles
Stroke Affects Locomotor Steering
Responses to Changing Optic Flow
Directions
Neurorehabilitation and
Neural Repair
24(5) 457–468
© The Author(s) 2010
Reprints and permission: http://www.
sagepub.com/journalsPermissions.nav
DOI: 10.1177/1545968309355985
http://nnr.sagepub.com
Anouk Lamontagne, PhD,1 Joyce Fung, PhD,1 Bradford McFadyen, PhD,2
Jocelyn Faubert, PhD,3 and Caroline Paquette, PhD1
Abstract
Background. Stroke patients manifest steering difficulties during walking, which may arise from an altered perception of
visual motion. Objective.To examine the ability of stroke patients to control their heading direction while walking in a virtual
environment (VE) describing translational optic flows (OFs) expanding from different directions. Methods. The authors
evaluated 10 stroke patients and 11 healthy people while they were walking overground and visualizing a VE in a helmetmounted display. Participants were instructed to walk straight in the VE and were randomly exposed to an OF having a
focus of expansion (FOE) located in 5 possible locations (0q, r20q, and r40q to the right or left). The body’s center of mass
(CoM) trajectory, heading direction, and horizontal body reorientation were recorded with a Vicon-512 system. Results.
Healthy participants veered opposite to the FOE location in the physical world, with larger deviations occurring at the
most eccentric FOE locations. Stroke patients displayed altered steering behaviors characterized either by an absence of
CoM trajectory corrections, multiple errors in the heading direction, or systematic veering to the nonparetic side. Both
groups displayed relatively small CoM trajectory corrections that led to large virtual heading errors. Conclusions. The
control of heading of locomotion in response to different OF directions is affected by stroke. An altered perception of
heading direction and/or a poor integration of sensory and motor information are likely causes. This altered response to
OF direction while walking may contribute to steering difficulties after stroke.
Keywords
heading, hemiparesis, kinematics, virtual reality, visual motion, walking
Introduction
The control of steering, or heading direction, is a requirement for goal-directed locomotion, allowing individuals to
walk in the desired direction while avoiding obstacles along
their path. Such control depends heavily on vision that provides information about the characteristics of the surrounding
world and self-motion. Optic flow (OF) is a predictable pattern of visual motion generated at the moving eye during
self-motion.1 Together with the perceived goal direction, it
is one of the visual cues that can be used to control heading
direction while walking.2-4 When walking straight, the OF
describes a radial pattern of expansion with a focus of
expansion (FOE) located in the direction of heading.4 When
a change of direction is needed, the OF theory stipulates that
the FOE is realigned with the desired heading direction.1 In
support of this theory, it has been shown that offsetting the
FOE of OF with prisms or through virtual reality causes
healthy individuals to veer from their initial trajectory when
instructed to walk straight ahead.2-4
Individuals who sustained a stroke are especially challenged in their daily activities as they have difficulties
adapting their locomotion to environmental constraints. They
show disrupted eye and body movement coordination patterns and altered walking trajectories when executing
preplanned or cued changes of direction while walking,
suggesting disrupted steering abilities.5,6 The loss of balance from executing a sudden turn of the head or body can
result in a fall.7 Although motor deficits undoubtedly impair
1
School of Physical and Occupational Therapy, McGill University and
Jewish Rehabilitation Hospital (Feil & Oberfeld/CRIR) Research Center,
Montréal, Canada
2
Laval University and Québec Rehabilitation Research Institute (CIRRIS),
Québec, Canada
3
School of Optometry, University of Montréal, Montréal, Canada
Corresponding Author:
Anouk Lamontagne, Jewish Rehabilitation Hospital (Feil & Oberfeld/
CRIR) Research Centre, 3205 Place Alton-Goldbloom, Laval (Québec),
H7V 1R2, Canada
Email: anouk.lamontagne@mcgill.ca
458
steering abilities, sensory deficits and altered sensorimotor
integration are also likely to be involved.5,6 The ability to
process different types of visual motion was shown to be
altered by brain lesions in the occipitoparietal, parietotemporal, and posterior parietal regions possibly involving the
MT (V5) complex.8-11 It would also be affected by a lesion
of the frontal lobe.12 Whether such altered perception of OF
direction translates into poor steering abilities after stroke,
however, is not known.
The goal of this study was to examine the ability of
individuals with stroke to control their heading direction
while walking in a virtual environment (VE) describing
translational OFs expanding from different directions. It
was hypothesized that these individuals would display an
altered control of their heading direction in response to the
shifts in the foci of expansion, as reflected either by
reduced adjustments and/or directional errors in their
walking trajectories.
Methods
Participants
A convenience sample of 10 patients with stroke and 11
healthy persons participated in the study (Table 1). The 2
groups were of the same age (t test, P .12) and presented
similar anthropometric characteristics. The inclusion criteria for the patients were the following: a first unilateral
stroke in the middle cerebral artery (MCA) territory with
residual deficits, confirmed by computerized tomography;
walking independently over 10 m, with or without a walking aid, at a walking speed inferior to 1.0 m/s; and presenting
with significant motor deficits of the affected lower limb, as
reflected by a Chedoke-McMaster leg and foot impairment
inventory score of less than 7.13 Exclusion criteria for the
patients were the following: cognitive problems compromising the ability to give informed consent and to follow
instructions as well as the presence of a visual field defect,
as assessed by the Goldman visual field and/or equivalent
computerized test. Patients with stroke were also free of
visual spatial neglect, as assessed by the Bell’s Test14 or Star
Cancellation Test,15 except for 2 of them (Table 1, patients
S3 and S4) who were enrolled in the study before neglect
was confirmed. When appropriate, the behavior of these 2
patients is described separately. Both healthy participants
and those with stroke were free of visual problems not corrected by eyewear as well as of other neurological or
orthopedic conditions interfering with locomotion. All participants signed an informed consent document, and the
project was approved by the Montréal Center for Interdisciplinary Research in Rehabilitation (CRIR) establishments’
Research Ethics Board.
Neurorehabilitation and Neural Repair 24(5)
Setup and Procedures
Participants were evaluated while walking overground at
their comfortable speed in a large open space (12 m u 8 m),
with their walking aid when applicable (see walking aid
description, Table 1). They were visualizing, in a helmetmounted display (HMD) unit, a VE representing a large (40
m u 25 m) and symmetrical room created in Softimage XSI
(Figure 1A). The virtual room was created to provide a richtextured VE and had pillars at its extremities,3 which
were separated by 8 m. The HMD (Kaiser Optics ProView
XL50) had a field of view of 50q diagonal, 30q vertical by
40q horizontal. Three-dimensional body coordinates were
recorded using a 10-camera Vicon-512 motion capture
system (Denver, CO). Passive reflective markers were
located on specific body landmarks according to the PlugIn-Gait Model from Vicon, except for the head that was
represented by a 3-marker model with markers located on
the front, left side, and right side of the HMD. Location of
the body’s center of mass (CoM) was calculated based on a
15-segment kinematic model and the anthropometric characteristics of the participants. The 3D head coordinates
were tracked in real time by the Tarsus real-time engine
from Vicon and fed to the Caren-2 virtual reality system
from Motek (Motek Medical, Amsterdam). This feedback
system synchronized the virtual scene in real time with
head motions through the physical space (Figure 1B). When
applicable, a visual perturbation could also be superimposed onto the motion of the scene caused by the head
displacements of the participants. The delay in updating the
virtual reality display in the HMD is less than 10 ms. The
sampling frequency was set at 120 Hz.
As they were walking forward, participants were exposed
to a translational OF that was expanding from a FOE located
in 5 possible locations (Figure 1C): 40q and 20q to the left
or nonparetic side, 0q, as well as +20q and +40q to the right or
paretic side. A FOE angular offset (4) was obtained by translating the scene laterally (x) based on the participant’s
forward displacement (y), such that x ytan(4). Based on the
forward walking speed of the participants, this corresponds
to average rates of mediolateral translation of the scene of
0.32 m/s (r40q FOE) and 0.14 m/s (r20q FOE) for the
patients and to 0.64 m/s (r40q FOE) and 0.28 m/s (r20q
FOE) for the healthy controls. Participants were instructed to
walk straight in the VE, that is, to “walk straight with respect
to the scene they were visualizing in the HMD,” as opposed
to the physical world. For a FOE located at 20q to the right,
for instance, participants should perceive their virtual heading direction as translating forward and toward the right
(Figure 1D). In an attempt to walk straight, they should veer
to the left in the physical world, such that their walking trajectory remains around neutral (0q) in the virtual world. They
459
73
79
51
73
68
79
S5
S6
S7
S8
S9
S10
7M/4F
—
—
—
8M/2F
M
M
M
M
F
F
M
M
M
M
Gender
(F/M)
169
11
155-183
166
12
152-185
172
162
152
185
154
155
152
178
176
173
Height
(cm)
79
13
63-104
70
15
48-96
70
50
60
96
90
48
68
72
73
75
Weight
(kg)
0.73
0.18
0.50-1.00
0.44
0.23
0.20-0.80
0.20 (Quad)
0.20 (Cane)
0.60 (2 Canes)
0.66
0.34
0.3 (Cane)
—
—
—
—
1-51 Months
—
—
N
N
N
N
N
N
Y
Y
N
N
Neglect
(Y/N)
12.6
3.0 Months
2.2 Months
2.1 Months
51.0 Months
1.0 Months
2.9 Months
19.0 Months
14.0 Months
0.15 (Quad)b
0.18 (Quad)
27.7 Months
3.4 Months
Time Since
Stroke
0.35 (Cane)
0.80
Speed
(m/s)
—
—
—
—
R
R
L
R
L
L
R
L
R
L
Side of
Lesion
Intraparenchymal
hemorrhage
Ischemia
Ischemia
Ischemia
Ischemia
Ischemia
Ischemia + small
hemorrhage
Massive Ischemia
Ischemia + small
hemorrhage
Ischemia, lacunar
Etiology
1
Capsulothalamicc
2
3
2
3
3
1
None
1
2a
Groupa
Temporoparietal junction,
insular cortex
Subcortical,
postinternal capsule
Frontotemporoparietal,
basal ganglia
Frontotemporoparietal,
basal ganglia; caudate
and thalamus spared
Parietal, external capsule,
and lenticular nucleus
Parietal
Subcortical, capsulethalamic
Parietal periventricular
region, thalamus
Parietal
Location of
Cerebrovascular Accident
Abbreviation: SD, standard deviation.
a
Individuals with stroke were assigned to different groups depending on their steering behaviors, as described in the Results section. (1) Minimal Veering Group; (2) Incongruous Veering Group; and (3)
Nonparetic Veering Group.
b
The quad cane is a 4-legged cane.
c
Initial scans were negative. A subsequent report states the presence of a subcortical infarct in this patient having a contralateral sensorimotor involvement of the hemibody with mild dysarthria and
dysphagia.
63
6
50-72
66
S4
Mean
SD
Range
71
S3
69
11
50-79
79
S2
Mean
SD
Range
Controls
(n 11)
50
Age
(years)
S1
Stroke
(n 10)
Table 1. Participant Characteristics
460
Neurorehabilitation and Neural Repair 24(5)
Figure 1. This figure shows (A) the virtual room used for the experiment, (B) the control algorithm of the virtual environment (VE)
is based on real-time tracking of head coordinates, (C) the different locations of the focus of expansion (FOE) used in the present
experiment, and (D) a schematic representation of perceived, physical, and virtual walking trajectories.
were provided with 3 to 5 practice trials, with and without
perturbations, before the experiments. We also confirmed
verbally that they understood the instruction, both prior to
and after the data collection. Three trials per FOE location
were recorded, for a total of 15 walking trials. Because
of their limited endurance, participants with stroke succeeded in performing 2 to 3 trials per FOE location. An
assistant was standing next to or walking along with the
Downloaded from http://nnr.sagepub.com at MCGILL UNIVERSITY LIBRARIES on June 20, 2010
461
Lamontagne et al.
Figure 2. Individual trials representing body center-of-mass (CoM) trajectory in the physical world (left panel) as well as heading
orientation in the physical (middle panel) and virtual worlds (right panel) in (A) 1 healthy young individual and (B) 1 elderly control.
CoM trajectories are illustrated in the anteroposterior (A/P) direction as a function of the mediolateral (M/L) direction. Heading
angular orientations are illustrated as a function of CoM displacement along the A/P axis. Note that CoM and heading traces illustrated
in this figure are referred to as positive when the participants are walking to the right. Trials at r40q in the healthy young individual
were recorded only for a short distance because of large M/L deviations that were limited by the physical constraints of the room.
Because of the forward and backward oscillations in body CoM position at gait initiation that lead to inconsistent heading orientations,
the first 50 frames of each trials are not represented, so heading traces do not start at neutral position.
participants at all times, and no falls occurred during the
experiment.
Outcome variables retained for analysis included CoM
trajectory and horizontal orientations of head and feet with
respect to the physical and virtual world’s coordinates. Displacement and angular orientation toward the right (controls)
or the paretic side (stroke) are referred to as positive. In
addition, heading direction was computed as the instantaneous angular orientation of body CoM trajectory along the
mediolateral (x-axis) versus the anteroposterior (y-axis)
direction. For every trial, heading orientation in the virtual
world, also termed as virtual heading error, was estimated
as the mean heading orientation measured between 2 m and
3 m of forward walking. When 3 m of forward walking
could not be reached, the mean value between 2 m and maximal forward walking distance was used instead. Mean
virtual heading errors were thereafter averaged across trials
and participants. By convention, a negative heading error
refers to an underestimation of the correction needed to reach
a virtual heading of 0q, whereas a positive heading error
means that participants overcorrected their walking trajectory. Within- and between-participant variabilities were
obtained using standard deviation values calculated across
trials and participants, respectively. Virtual heading errors and
within-participant variability were compared across groups
(stroke vs controls) and conditions (FOE location, 5 levels)
using a 2-way analysis of variance for repeated measures.
The relationships of the virtual heading errors with gait
speed and age were assessed using Pearson correlation
coefficients. Statistics were performed in Statistica with a
level of significance accepted at P .05.
Results
Examples of CoM trajectory modulation of healthy participants in response to different FOE locations are illustrated
in Figure 2. To help understand what a typical profile of
modulation looks like, an example of a healthy elderly control is contrasted with that of a healthy young individual.
For both participants, the CoM trajectory and heading
462
Neurorehabilitation and Neural Repair 24(5)
Figure 3. Individual examples of body center-of-mass (CoM) trajectory in the physical world (left panel) as well as heading orientation
in the physical (middle panel) and virtual worlds (right panel) in participants with stroke from the (A) Minimal Veering Group, (B)
Incongruous Veering Group and (C) Nonparetic Veering Group. Axis labels and abbreviation are the same as in Figure 2, with the
exception of positive CoM and heading traces indicating a displacement to the paretic side. Participants belonging to each group
are identified as per their participant number in Table 1 (S1 to S10). Note that S2 is not shown in this figure and displayed a steering
behavior similar to healthy controls.
orientation in the physical world were characterized by a
deviation in the direction opposite to the FOE location (left
and middle panels). The amplitudes of the CoM trajectory
and the heading corrections were scaled to the magnitude of
the perturbation, being larger for the 40q than for the 20q
and 0q perturbations. The healthy young individual displayed large yet incomplete heading corrections in the
physical world (middle panel), resulting in heading errors
that were biased toward the FOE location in the virtual
world (right panel). This participant’s heading error, however, decreased in the virtual world and converged toward
the midline (0q) as he continued walking forward. In comparison, the healthy elderly control presented with much
smaller heading corrections in the physical world, resulting
in larger heading errors in the virtual world.
In comparison with healthy controls, stroke patients
presented with a variety of steering behaviors, including
heading corrections that were of the wrong magnitude and/
or in the wrong direction (Figure 3). Based on the steering
behavior, patients were classified into 3 different groups.
The Minimal Veering Group (n 3) presented with little or
no modulation of their CoM trajectory and heading orientation in the physical world when exposed to FOE shifts. As
a result, they displayed large heading errors in the virtual
world that were approaching the magnitude of the FOE
shifts. The Incongruous Veering Group (n 3) displayed
463
Lamontagne et al.
Figure 4. Individual trials representing CoM trajectory as well as head and foot horizontal orientation in the physical and virtual
worlds for 1 healthy control and 1 patient (S4) with visuospatial neglect.
multiple and inconsistent directional errors, with heading
corrections being made erratically sometimes toward the
paretic and sometimes toward the nonparetic side for similar
FOE perturbations. The Nonparetic Veering Group (n 3)
veered to their nonparetic side in the physical world for
most trials, regardless of the FOE location. This means that
when the FOE was on the paretic side, participants corrected their heading in the expected direction by veering to
their nonparetic side. When the FOE was shifted to the nonparetic side, however, they veered in the wrong direction,
that is, the ipsilateral nonparetic side. This resulted in larger
virtual heading errors for the paretic than the nonparetic
side. Note that the 2 participants with stroke who had visuospatial neglect (S3 and S4) were included in the Minimal Veering
Group and the Nonparetic Veering Group, respectively. One
remaining participant with stroke (S2), not included in the 3
groups, displayed behavior identical to that of the healthy
controls.
An example of CoM trajectory modulation as well as of
head and foot orientation is further detailed in Figure 4 for
a healthy control and a stroke patient with visuospatial
neglect. The CoM trajectory of the healthy control veered in
the direction opposite to the FOE location in the physical
world, but the correction remained incomplete, leading to
some deviation error in the virtual world. The feet were
aligned with the CoM trajectory in the physical world, but
the head showed few changes in its orientation with FOEs
of changing location. This head and foot orientation pattern
is typical of what was observed in the healthy control group
as well as in most participants with stroke. Alternatively,
the patient with visuospatial neglect represented in Figure 4
invariantly veered to the nonparetic side, irrespective of the
FOE location. As for the other patients in group 2, a directional error arose when the FOE was located toward the
nonparetic side, which did not cause the patient to veer
toward the paretic side in the physical world, as would be
expected normally. For the patient shown in Figure 4, his
head and nonparetic foot were oriented toward the nonparetic side in the physical world, whereas the paretic foot
remained in a more toes-out and widened position.
464
Neurorehabilitation and Neural Repair 24(5)
Figure 5. (A) Mean (1 SD) virtual heading errors as well as (B) mean within-participant and (C) between-participant variability
of virtual heading responses for the patients and controls across the different locations of the FOE. In A, the negative polarity of
the virtual heading errors indicates an undercorrection of the heading trajectory with respect to the virtual world’s coordinates.
Statistically significant results are indicated in A and B. No standard deviation error bars or statistical analyses can be computed for
between-participant variability in C.
Abbreviations: SD, standard deviation; FOE, focus of expansion.
The average heading orientations in the virtual world, or
heading errors, were compared between patients and healthy
participants across FOE locations (Figure 5). All participants undercorrected their heading in response to FOEs of
changing direction. Virtual heading errors increased at more
eccentric FOE locations, both for patients and healthy participants (P .01). Given the different behaviors observed
in the stroke patients, their mean virtual heading errors
465
Lamontagne et al.
were found to be similar to those of the healthy participants
(P ! .05), despite a tendency for larger heading errors in the
patients at r40q of FOE perturbation. Within-participant and
between-participant variabilities in the heading responses,
however, were larger in the patients than in the healthy group
(P .05, within-participant). Heading errors of patients and
healthy participants were not correlated with walking speed
(R2 0.00-0.07; P ! .05) or age (R2 0.00-0.19; P ! .05). A
qualitative analysis of the heading behavior of patients with
respect to the lesion site or the use of walking aids did not
reveal any identifiable relationships (Table 1).
Discussion
This study provides the first evidence that individuals who
sustained a stroke can manifest altered locomotor steering
behaviors when exposed to OFs expanding from different
locations. Such altered behaviors are reflected by abnormally small adaptations and/or by directional errors in the
participants’ walking trajectories as well as by an increased
variability across trials. The present results are consistent
with the attenuated and/or altered gait speed modulation
responses of participants with stroke when exposed to OFs
of changing speeds.16
It has been shown that healthy young individuals
exposed to an artificially shifted FOE while walking veer in
the direction opposite to the goal in the physical world so
that a virtual heading error close to zero can be reached.4
We have also shown that the larger the shift in the FOE, the
larger the walking trajectory deviation in the physical
world, and the larger the virtual heading error.3 In other
words, the corrections in the physical walking trajectory are
insufficient to lead to straight walking trajectories in the
virtual world, and the heading errors increase at more
eccentric locations of FOE. Present data collected in healthy
controls who are older than the young individuals tested
previously in other studies do support these observations.
Brain Lesion and Altered
Heading Perception
An absence of response characterized the Miminal Veering
Group, and multiple heading errors were displayed by the
Incongruous Veering Group. No qualitative relationship
could be established between the patterns of heading
responses and the localization of the brain lesion. It cannot
be excluded that the different heading behaviors (absence
of responses vs errors) may just be different expressions of
the same inability to perceive or use OFs to complete the
heading task. It is worth investigating, however, whether
the damaged brain areas of our participants could lead to an
altered discrimination of visual motion direction and heading. The intact human brain shows activation in the
occipital, parietal, and temporal cortical areas while viewing radial OFs.17 The human MT (V5) complex, and more
specifically the MST area, were shown to be highly sensitive to changes in the characteristics of the OF stimuli.17,18
Discriminating heading, depending on the nature of the
visual stimulus, would involve a complex network comprising posterior brain areas such as KO and V3a,19-21 the MT
complex,20,22 temporoparietal and occipitotemporal areas,19,20
and even frontal areas12,22 and subcortical/limbic structures.19 Altered processing of visual motion direction has
been previously reported in participants with a stroke in the
occipitoparietal, parietotemporal, or posterior parietal brain
areas, which were all believed to involve the MT complex.8-11 In the present study, the MCA territory lesions
would spare the posterior visual areas supplied by the posterior cerebral artery, but the MT complex, potentially
supplied by both the MCA and posterior cerebral artery,
could not be excluded. Some of our patients also presented
hemorrhagic events, which potentially extended the lesion
beyond the MCA territory. It is noteworthy that our patients
who displayed altered steering behaviors had lesions that
invariantly involved the parietal lobe and/or thalamus. The
parietal area is a key site for the integration of multiple
sources of sensory information,23,24 and it is involved in the
control of steering.25 The thalamus relays sensory information to different cortical areas, contributing crucially to
motor actions. It seems reasonable to assume that lesions in
such areas affect multisensory integration and can alter
heading behaviors. Some of our patients also displayed
lesion involving the frontotemporal region. There is evidence from intact or damaged brain studies that the frontal
lobe,12 and more specifically the dorsal premotor area,22,25
is involved in heading identification. Those studies involved
a ground plane or a radial OF pattern, which can resemble
the type of stimulus used in the present study. According to
Peuskens et al,22 such activation in the dorsal premotor area
could be “ . . . a final stage in a parieto-premotor visuomotor
connection, specifically related to transformation of heading information . . . into motor schemes.”(p 2460) In light of
those findings, it appears likely that our patients had brain
lesions that altered the perception and/or integration of
heading information.
Altered Sensorimotor Integration
and Visuomotor Control
The present paradigm also involved a sensory scenario in
which visual stimuli were incongruent with proprioceptive
and vestibular information. The central nervous system has
the ability to reweight relevant sources of sensory information in a context-dependent fashion to maintain postural
equilibrium.26-28 The transient aftereffect of self-motion
experienced after treadmill running29 is another indirect
466
evidence of such a sensory reweighting process. The ability
to reweight the relevant source of information appears to be
reduced in older individuals30-32 and after stroke,33 so that
those with stroke may be unable to upregulate vision and
resolve the sensory conflict to control their heading. It was
also suggested that gaze reorientation is a fundamental
component of a locomotor steering synergy while changing direction34,35 and that active gaze would contribute to
identifying heading by providing extraretinal cues.36 Passive viewing of OFs also triggers eye movements for the
purpose of image stabilization.37 This emphasizes the intimate relationship between gaze control, visual perception,
and the control of heading. In those with stroke, the coordination of gaze and posture during locomotor steering
was shown to be disrupted.5 This suggests that both perceptual and motor aspects of visuomotor control could
contribute to their altered heading responses.
Visuospatial Neglect
Perhaps one of the most unexpected findings of the present
study was the behavior observed in the Nonparetic Veering
Group, which consisted of walking trajectories consistently
deviating to the nonparetic side in the physical world.
Closer examination of present data reveals that the directional error occurred when the FOE was located on the
nonparetic side, which should have caused a turn to the
paretic side. This is not likely to be a result of biomechanical factors because those with stroke tend to walk with a
horizontal rotational bias of their body toward their paretic
side, therefore, favoring a physical turn toward the paretic
side.6 It has also been demonstrated that looking to the side
at an object causes a slight curvature in one’s walking trajectory toward the direction of gaze.38 In the absence of
reliable vision cues such as when walking blindfolded, a
walking trajectory deviation contralateral to the eye or head
rotation is observed instead.39 In the present study, head and
foot starting positions were aligned with the room’s coordinates before the participants started to walk, but the eyes
might have been oriented in one or another direction. Even
if this was the case, however, the effect would be very limited as in Jahn et al,39 for instance, a gaze rotation of 35q
leads to a small trajectory deviation of 2q to 4q. Results of
our study also show that one of the participants of the Nonparetic Veering Group had neglect, whereas the 2 others
were theoretically free of such problems. In neglect, the
paretic hemispace is less attended, and the subjective midline would be displaced to the nonparetic or ipsilesional
side.40 This predicts that those with neglect should steer
toward their paretic side in an attempt to walk straight,41 a
prediction that is not supported by the present results. In
reality, there is conflicting evidence as to whether those
with neglect veer to their paretic or nonparetic sides as
they walk.41,42 It also remains possible that some of our
Neurorehabilitation and Neural Repair 24(5)
participants might have had far extrapersonal space neglect
that was not picked up by paper-pencil tests.43
Limitations
Our results outline the within-individual and interindividual variability of behavior usually observed in stroke.
Given the exploratory nature of this study, inclusion criteria were purposely kept large, but factors such as walking
capacity, chronicity, and the extent of the brain lesion may
have contributed to the heterogeneity of behaviors. The
nature of the brain imaging tool (CT scans) and variability in the depth of the information available in the
patients’ charts also limited our interpretation of results
in terms of the lesion site and its effects on heading
behaviors. It is hoped that higher resolution imaging tools
will help shed light on the role of specific brain areas in
locomotor steering behaviors. Factors such as attention
and the sense of presence (sense of “being there,” within
the VE), which have not been quantified in this study, may
also differ between those with stroke and healthy participants and account for some of the differences between the
2 groups. It could also be argued that gait speed, which
was slower in the stroke participants, was partly responsible for their altered behavior. Indeed, walking faster or
running, as compared with walking slower, reduces the
deviations in walking trajectory when walking with shifted
OFs,44 blindfolded,45 or when presenting a vestibular
imbalance. 46 However, the fact that larger heading
errors were not associated with slower gait speeds in
the present study suggests that speed is not an explanatory variable. It was unfortunate that gaze behavior
could not be monitored in the present study. Although
this limitation does not invalidate the present results, it
also cannot reveal the presence or absence of an altered
gaze behavior associated with the identification and
control of heading direction in stroke participants.
Conclusions and Future Directions
The present results show that stroke affects the control of
heading of locomotion in response to translational OFs
expanding from different directions. An altered perception
of heading direction and/or a poor integration of sensory
and motor information are likely causes. Gaze shifts, which
help in identifying heading direction through extraretinal
cues, might also be involved, contributing in part to the
altered heading behaviors. The altered heading responses to
OF direction observed in the stroke participants may likely
contribute to their steering difficulties. Future directions for
research should include examining the effects of specific
circumscribed brain lesions on locomotor steering behaviors as well as exploring the role of oculomotor control and
the use of other sources of visual information, such as
467
Lamontagne et al.
perceived target location, in the perception and control of
locomotor heading after a brain lesion.
Acknowledgments
We would like to thank the people who participated in this study.
We are also thankful to Eric Johnston and Christian Beaudoin for
their skilful technical assistance.
Authors’ Note
Present address for Caroline Paquette: Neuroplasticity Laboratory,
Department of Neurology and Neurosurgery, McGill University at
SMBD-Jewish General Hospital and Lady Davis Institute, Montréal, Canada.
Declaration of Conflicting Interests
The authors declared no conflicts of interest with respect to the
authorship and/or publication of this article.
Funding
This study was funded by the Québec Rehabilitation Research
Network (REPAR), the Canadian Institutes of Health Research
(CIHR) and the Heart and Stroke Foundation of Canada. A.
Lamontagne is supported by a CIHR New Investigator Salary
Award. Part of the equipment used for this experiment was funded
by an infrastructure fund (New Opportunities Funds) from the
Canada Foundation for Innovation.
References
1. Gibson JJ. The visual perception of objective motion and subjective movement. 1954. Psychol Rev. 1994;101:318-323.
2. Harris JM, Bonas W. Optic flow and scene structure do not
always contribute to the control of human walking. Vision
Res. 2002;42:1619-1626.
3. Sarre G, Berard J, Fung J, Lamontagne A. Steering behaviour
can be modulated by different optic flows during walking.
Neurosci Lett. 2008;436:96-101.
4. Warren WH Jr, Kay BA, Zosh WD, Duchon AP, Sahuc S.
Optic flow is used to control human walking. Nat Neurosci.
2001;4:213-216.
5. Lamontagne A, Fung J. Gaze and postural reorientation in the
control of locomotor steering after stroke. Neurorehabil Neural Repair. 2009;23:256-266.
6. Lamontagne A, Paquette C, Fung J. Stroke affects the coordination of gaze and posture during preplanned turns while
walking. Neurorehabil Neural Repair. 2007;21:62-67.
7. Hyndman D, Ashburn A, Stack E. Fall events among people with stroke living in the community: circumstances of
falls and characteristics of fallers. Arch Phys Med Rehabil.
2002;83:165-170.
8. Plant GT, Laxer KD, Barbaro NM, Schiffman JS, Nakayama
K. Impaired visual motion perception in the contralateral
hemifield following unilateral posterior cerebral lesions in
humans. Brain. 1993;116(pt 6):1303-1335.
9. Vaina LM, Soloviev S. First-order and second-order motion:
neurological evidence for neuroanatomically distinct systems.
Prog Brain Res. 2004;144:197-212.
10. Braun D, Petersen D, Schonle P, Fahle M. Deficits and recovery of first- and second-order motion perception in patients
with unilateral cortical lesions. Eur J Neurosci. 1998;
10:2117-2128.
11. Vaina LM, Cowey A, Eskew RT Jr, LeMay M, Kemper
T. Regional cerebral correlates of global motion perception: evidence from unilateral cerebral brain damage. Brain.
2001;124(pt 2):310-321.
12. Billino J, Braun DI, Bohm KD, Bremmer F, Gegenfurtner KR.
Cortical networks for motion processing: effects of focal brain
lesions on perception of different motion types. Neuropsychologia. 2009;47:2133-2144.
13. Gowland C, Stratford P, Ward M, et al. Measuring physical
impairment and disability with the Chedoke-McMaster Stroke
Assessment. Stroke. 1993;24:58-63.
14. Gauthier L, Dehaut F, Joanette Y. The Bells test for visual
neglect: a quantitative and qualitative test for visual neglect.
Int J Clin Neuropsychol. 1989;11:49-54.
15. Halligan P, Wilson B, Cockburn J. A short screening test for
visual neglect in stroke patients. Int Disabil Stud. 1990;12:95-99.
16. Lamontagne A, Fung J, McFadyen BJ, Faubert J. Modulation of walking speed by changing optic flow in persons with
stroke. J Neuroeng Rehabil. 2007;4:22.
17. Ptito M, Kupers R, Faubert J, Gjedde A. Cortical representation of inward and outward radial motion in man. Neuroimage. 2001;14:1409-1415.
18. Morrone MC, Tosetti M, Montanaro D, Fiorentini A, Cioni
G, Burr DC. A cortical area that responds specifically to optic
flow, revealed by fMRI. Nat Neurosci. 2000;3:1322-1328.
19. Beer J, Blakemore C, Previc FH, Liotti M. Areas of the
human brain activated by ambient visual motion, indicating three kinds of self-movement. Exp Brain Res. 2002;143:
78-88.
20. Vaina LM, Soloviev S. Functional neuroanatomy of heading perception. In: Vaina LM, Beardsley SA, Rushton S, eds.
Optic Flow and Beyond. New York, NY: Kluwer Academic
Press; 2004:109-137.
21. Rutschmann RM, Schrauf M, Greenlee MW. Brain activation
during dichoptic presentation of optic flow stimuli. Exp Brain
Res. 2000;134:533-537.
22. Peuskens H, Sunaert S, Dupont P, Van Hecke P, Orban GA.
Human brain regions involved in heading estimation. J Neurosci. 2001;21:2451-2461.
23. Meehan SK, Staines WR. Task-relevance and temporal synchrony between tactile and visual stimuli modulates cortical
activity and motor performance during sensory-guided movement. Hum Brain Mapp. 2009;30:484-496.
24. Macaluso E, Driver J. Multisensory spatial interactions:
a window onto functional integration in the human brain.
Trends Neurosci. 2005;28:264-271.
Downloaded from http://nnr.sagepub.com at MCGILL UNIVERSITY LIBRARIES on June 20, 2010
468
Neurorehabilitation and Neural Repair 24(5)
25. Field DT, Wilkie RM, Wann JP. Neural systems in the visual
control of steering. J Neurosci. 2007;27:8002-8010.
26. Mergner T, Maurer C, Peterka RJ. A multisensory posture
control model of human upright stance. Prog Brain Res.
2003;142:189-201.
27. Keshner EA, Kenyon RV, Langston J. Postural responses
exhibit multisensory dependencies with discordant visual and
support surface motion. J Vestib Res. 2004;14:307-319.
28. Mergner T, Schweigart G, Maurer C, Blumle A. Human postural responses to motion of real and virtual visual environments under different support base conditions. Exp Brain Res.
2005;167:535-556.
29. Durgin FH, Pelah A, Fox LF, Lewis J, Kane R, Walley KA.
Self-motion perception during locomotor recalibration: more
than meets the eye. J Exp Psychol. 2005;31:398-419.
30. Bugnariu N, Fung J. Aging and selective sensorimotor strategies in the regulation of upright balance. J Neuroeng Rehabil.
2007;4:19.
31. Mahboobin A, Loughlin PJ, Redfern MS. A model-based
approach to attention and sensory integration in postural control of older adults. Neurosci Lett. 2007;429:147-151.
32. O’Connor KW, Loughlin PJ, Redfern MS, Sparto PJ. Postural
adaptations to repeated optic flow stimulation in older adults.
Gait Posture. 2008;28:385-391.
33. Bugnariu N, Fung J. Stroke and selective sensorimotor strategies in the regulation of upright balance. Abstr Soc Neurosci.
2006;32:353.
34. Hollands MA, Patla AE, Vickers JN. “Look where you’re going!”:
gaze behaviour associated with maintaining and changing the
direction of locomotion. Exp Brain Res. 2002;143: 221-230.
35. Reed-Jones R, Reed-Jones J, Vallis LA, Hollands M. The
effects of constraining eye movements on visually evoked
steering responses during walking in a virtual environment.
Exp Brain Res. 2009;197:357-367.
36. Wilkie R, Wann J. Controlling steering and judging heading:
retinal flow, visual direction, and extraretinal information. J
Exp Psychol. 2003;29:363-378.
37. Niemann T, Lappe M, Buscher A, Hoffmann KP. Ocular
responses to radial optic flow and single accelerated targets in
humans. Vision Res. 1999;39:1359-1371.
38. Cutting JE, Readinger WO, Wang RF. Walking, looking
to the side, and taking curved paths. Percept Psychophys.
2002;64:415-425.
39. Jahn K, Kalla R, Karg S, Strupp M, Brandt T. Eccentric eye
and head positions in darkness induce deviation from the
intended path. Exp Brain Res. 2006;174:152-157.
40. Karnath HO. Subjective body orientation in neglect and the
interactive contribution of neck muscle proprioception and
vestibular stimulation. Brain. 1994;117(pt 5):1001-1012.
41. Huitema RB, Brouwer WH, Hof AL, Dekker R, Mulder T,
Postema K. Walking trajectory in neglect patients. Gait Posture. 2006;23:200-205.
42. Robertson IH, Tegner R, Goodrich SJ, Wilson C. Walking trajectory and hand movements in unilateral left neglect: a vestibular hypothesis. Neuropsychologia. 1994;32:1495-1502.
43. Azouvi P, Bartolomeo P, Beis JM, Perennou D, PradatDiehl P, Rousseaux M. A battery of tests for the quantitative
assessment of unilateral neglect. Restor Neurol Neurosci.
2006;24:273-285.
44. Jahn K, Strupp M, Schneider E, Dieterich M, Brandt T. Visually induced gait deviations during different locomotion
speeds. Exp Brain Res. 2001;141:370-374.
45. Dickstein R, Ufaz S, Dunsky A, Nadeau S, Abulaffio N.
Speed-dependent deviations from a straight-ahead path during
forward locomotion in healthy individuals. Am J Phys Med
Rehabil. 2005;84:330-337.
46. Brandt T, Strupp M, Benson J. You are better off running than
walking with acute vestibulopathy. Lancet. 1999;354:746.
Downloaded from http://nnr.sagepub.com at MCGILL UNIVERSITY LIBRARIES on June 20, 2010