Subjective Visual Vertical Perception Relates to Balance in Acute Stroke ORIGINAL ARTICLE

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642
ORIGINAL ARTICLE
Subjective Visual Vertical Perception Relates to Balance
in Acute Stroke
Isabelle V. Bonan, MD, Emilie Guettard, Marie C. Leman, MD, Florence M. Colle, MD, Alain P. Yelnik, MD
ABSTRACT. Bonan IV, Guettard E, Leman MC, Colle FM,
Yelnik AP. Subjective visual vertical perception relates to
balance in acute stroke. Arch Phys Med Rehabil 2006;87:
642-6.
Objective: To determine whether misperception of the subjective visual vertical (SVV) underlies balance difficulties in
hemiplegic patients.
Design: Descriptive study, using a convenience sample.
Setting: Department of physical medicine of a university
hospital.
Participants: Thirty inpatients with hemiplegia after a
hemispheric stroke during the 3 previous months.
Interventions: Not applicable.
Main Outcome Measures: The SVV was tested while subjects sat in a dark room and were asked to adjust a luminous
line to the vertical position. Mean SVV deviation and uncertainty, defined as the standard deviation, were calculated for 8
trials. Balance was assessed by the Postural Assessment Scale
for Stroke (PASS) and while patients sat on a laterally rocking
platform placed on a Satel force platform. The mean body
position and the instability score (Lx), calculated as the length
of the course of the center of pressure, were recorded. Functional outcome was also evaluated by the FIM instrument.
Results: An abnormal SVV was recorded for 20 of 30
patients. Balance (ie, PASS, Lx) and FIM correlated significantly with SVV tilt (P⬍.001, P⫽.01, and P⬍.001, respectively) and with uncertainty (PASS, P⫽.006; FIM, P⫽.003).
Conclusions: Verticality misperception was related to poor
balance and might be an important element in the assessment of
contributing factors to balance disorders after stroke. It should
probably be taken into account when establishing balance
rehabilitation programs for patients with hemiplegia.
Key Words: Balance; Hemiplegia; Rehabilitation; Stroke;
Visual perception.
© 2006 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and
Rehabilitation
FTER A STROKE, balance can be affected by various and
mixed components, including mechanical components such
A
as weakness, joint motion limitation, modification of muscle tone,
and sensory impairment. Misperception of reference frames
such as gravitational cues may constitute another component of
imbalance. Contralateral tilt of the subjective visual vertical
From the Department of Physical Medicine and Rehabilitation, Groupe Hospitalier
Lariboisiere–F. Widal, Paris, France.
No commercial party having a direct financial interest in the results of the research
supporting this article has or will confer a benefit upon the author(s) or upon any
organization with which the author(s) is/are associated.
Reprint requests to Isabelle V. Bonan, MD, Physical Medicine and Rehabilitation
Dept, G.H. Lariboisiere–F. Widal, 200 Rue du Faubourg St Denis, 75010 Paris,
France, e-mail: [email protected]
0003-9993/06/8705-10416$32.00/0
doi:10.1016/j.apmr.2006.01.019
Arch Phys Med Rehabil Vol 87, May 2006
(SVV), tested by asking subjects to adjust a luminous line to
the vertical position in a dark room, has been reported after
hemispheric lesions. This misperception is frequent after righthemispheric lesion and is closely related to visuospatial neglect.1-3
More than 50% of patients have SVV misperception after
recent cerebral hemispheric stroke.1 In addition to the tilt of the
SVV, attention has been drawn to the abnormal range of
uncertainty in the perception of the SVV, which showed the
difficulty that some patients experienced in assessing the vertical.1
The present study deals with the next stage, in which we
sought to establish whether SVV misperceptions are related to
balance difficulties in patients with hemiplegia. To our knowledge, no studies have been conducted that have determined this
relation. Poor ambulation has been related to SVV perturbations, but in that study3 ambulation was scored on a very rough
3-step scale. (Patients were classified as fully mobile, walking
up to 50m, or requiring a wheelchair.) The perception of visual
verticality after stroke has been investigated in patients with an
uncommon specific disturbance of balance called the pusher
syndrome.4,5 Discordant results were recorded in these particular patients: no SVV tilt in the study of Karnath et al4 and an
unusual tilt, ipsilateral to the lesion, in the study of Saj et al.5
Spatial abilities such as the perception of verticality can be
assumed to have a significant role in maintaining balance. We
postulated that postural imbalance in patients with hemiplegia
may be caused by a misperception of verticality. Therefore, we
conducted the present investigation to determine whether SVV
misperception correlated with balance difficulties in hemiplegic patients after recent stroke. This might be an important
element in assessing factors that contribute to balance disorders
after stroke. If a correlation exists, rehabilitation programs of
postural control for patients with hemiplegia after stroke should
take into account the possible impairment of verticality perception and include new exercises designed to improve the
sense of verticality.
METHODS
Subjects were recruited in our physical and medicine rehabilitation department. All subjects gave informed consent to
participate in the study before testing. The study received the
approval of the Clinical Investigation Unit of the Lariboisiere
University Hospital. Patients had recently experienced their
first and only cerebral hemispheric strokes, resulting at least in
initial motor and balance impairment. They were all right
handed. The time since stroke was never longer than 3 months.
Patients were excluded if they had perturbed vigilance, a history of neurologic disturbances, vertigo or vestibular dysfunction, amblyopia or diplopia, or severe aphasia. Only patients
who were able to understand the instructions for adjustments of
the SVV were included. Patients who could not keep their
balance while sitting on the laterally rocking platform were not
included. Patients with pusher syndrome, then, were not included. All patients were explored by computed tomography
scans or magnetic resonance imaging of the brain and brainstem. An ear, nose, and throat examination was conducted in
patients with poor balance. No peripheral vestibular disorder
643
VERTICAL PERCEPTION AND BALANCE AFTER STROKE, Bonan
was diagnosed. Before testing, we performed a complete neurologic examination in which the following were evaluated:
motricity using the Collin and Wade6 scale (range, 0 –200);
visual field, assessed at the bedside; and visuospatial neglect,
using the Bells Test7 and bisection test.8 Visuospatial neglect
was considered to be present when the difference between the
bells omitted on the left and right sides in the Bells Test
exceeded 3 and when the bias in line bisection exceeded 0.6cm.
Joint position sense was assessed for the big toe, ankle, knee,
and hip. Patients were then classified into 3 groups for joint
position sense: normal joint position sense (2), hyposensitivity
(1), and anesthesia (0).
rocking platform with respect to the horizontal. Two parameters were analyzed: xm (in millimeters) and length of the
course (ie, Lx) (in millimeters). A control group of 25 healthy
subjects (13 men, 12 women; median age, 50y; IQR⫽14y) was
tested on the platform. For them, the median absolute deviation
xm was 6.5mm (IQR⫽7.8mm) and the median Lx was 40.0mm
(IQR⫽13.2mm).
Procedure
SVV assessment. We conducted SVV testing in a dark
room to eliminate any visual reference cues, with subjects
sitting in a wheelchair or normal chair. The experimenter
oriented an oblique white line on a dark background, placed
directly in front of each subject at a distance of 2m, until the
subject perceived it as exactly vertical; there was no time limit.
The head was maintained in a fixed position by a supporting
chinrest. Eight trials were made in random order: for 4 of them,
the line was initially tilted 40° to the left of the vertical
objective, and patients had to adjust it with a clockwise movement; for the other 4, the rod was tilted 40° to the right of the
vertical objective for a counterclockwise adjustment. For each
trial, the deviation was evaluated in degrees (⫹, ipsilateral
deviation in relation to the lesion; ⫺, contralateral deviation in
relation to the lesion). The following parameters were analyzed: (1) the mean SVV deviation (V) value expressed as the
mean absolute deviation for the 8 SVV measurements and (2)
the uncertainty in the perception of the SVV (U), expressed as
the standard deviation (SD) for the 8 SVV measurements.
Normative control data were supplied by 20 healthy subjects,
who were age-matched with the patients (median age, 60y;
interquartile range [IQR], 19y) and underwent the same tests.
For the controls, the median V was 0.8° (IQR⫽1.4°) and the
maximum individual V was 2.8°. Consequently, the results for
each patient were considered different from control values
when V exceeded 3°, which is clearly larger than the deviation
for the controls and was similar to the normative range previously reported.9 The median U was 1.2° (IQR⫽0.7°) and the
maximum interindividual difference was 2.5°. Therefore, for
U, 3° was considered significantly abnormal.
Postural assessment. For postural assessment we used a
specific validated ordinal scale ranging from 0 to 36 called the
Postural Assessment Scale for Stroke (PASS)10 and a rocking chair paradigm derived from that proposed by Perennou
et al.11-13 Subjects sat in the center of a laterally rocking
platform placed over a force platform (Satela). Falls were
prevented by the experimenter. The height of the seat was
adjusted so that each subject’s legs could hang freely. Subjects
were asked to keep their balance while looking straight ahead
and fixing on a vertical target positioned on the visual pattern.
Subjects themselves were responsible for their imbalance and
active correction. The force platform consisted of an upper
stable support (480⫻480mm2) fixed on 3 strain-gauge force
transducers that recorded the course of each subject’s center of
pressure (COP). The platform was connected to a personal
computer with a serial connection. Dynamic balance was assessed by placing a laterally moveable rocking platform with a
radius of 55cm on the computerized force platform. First, the
course of each subject’s COP in the lateral plane was recorded
for 25 seconds, and then the mean COP deviation (xm) and the
length of the course (Lx) were recorded. The mean COP
deviation had a linear relation to the mean orientation of the
Statistical Analysis
Data were expressed as medians and IQRs, because the
parameters were not Gaussian. The relation between each patient’s characteristics (age, motricity), balance (PASS score),
mean body orientation (ie, xm), body instability (ie, Lx), FIM
score, and the variables V and U describing the SVV were
tested by the Kendall correlation test. The visual neglect and
nonvisual neglect groups and then the right (RHL) and left
hemispheric lesion (LHL) groups were compared for V and U
using the Mann-Whitney U test; the 3 sensitivity groups were
then compared using the Kruskal-Wallis test. To estimate the
role of motricity in the relation between SVV variables and
balance, partial coefficients of Kendall were calculated. To
estimate the role of joint position sense in the relation between
SVV variables and balance, the relation between V and balance
and between U and balance were tested among each group of
joint position sense with the Kendall correlation test. For all
tests, the significance level was fixed at .05 and was analyzed
using StatView software.b
Functional Outcome
The functional independence was evaluated using the FIM
instrument (range, 0 –126), used as a global indicator of stability during the activities of daily living.14
RESULTS
Patient Characteristics
Thirty patients were studied (table 1). Their median age was
59 years (IQR⫽21y), and the median time since stroke was
39.5 days (IQR⫽37d). Thirteen patients had an LHL and 17
had an RHL. Stroke was hemorrhagic in 10 patients and
ischemic in 20. Among the ischemic lesions, posterior cerebral
artery territory was never involved. Anterior cerebral artery
territory was affected in 3 patients and middle cerebral artery
territory in 19. The entire territory of middle cerebral artery
was involved in 16 patients, deep territory in 4, and superficial
territory in 5. A visual field defect was observed in 3 patients.
Visuospatial neglect was noted in 15 patients (14 RHL, 1
LHL). Median Motricity Index score was 98 (IQR⫽158). Eight
patients exhibited normal joint position sense, 12 had hyposensitivity, and 10 had anesthesia.
Table 1: Baseline Characteristics of 30 Patients With Hemiplegia
Characteristic
Median age (y)
Median time since stroke (d)
Sex (men/women)
Side of lesion (left/right)
Type of lesion
Ischemic/hemorrhagic
Median Motricity Index score
Joint position sense (group 0/group 1/group 2)
Value
59 (21)
39.5 (37)
16/14
13/17
20/10
98 (158)
10/12/8
NOTE. Values are median (IQR), n, or as otherwise indicated.
Arch Phys Med Rehabil Vol 87, May 2006
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VERTICAL PERCEPTION AND BALANCE AFTER STROKE, Bonan
Table 2: SVV Values (V, U) and Scores for Balance (xm, Lx) in
Healthy Controls and Patients With LHL or RHL
Subjects
Controls
Mean ⫾ SD
Median (IQR)
Total patients
Mean ⫾ SD
Median (IQR)
LHL patients
Mean ⫾ SD
Median (IQR)
RHL patients
Mean ⫾ SD
Median (IQR)
V (deg)
U (deg)
xm (mm)
Lx (mm)
1.1⫾1.4
0.8 (1.4)
1.4⫾0.9
1.2 (0.7)
7.8⫾6.1
6.5 (7.8)
40.4⫾9.1
40 (13.2)
3.6⫾3.4*
2.6 (3.6)
4.1⫾4.2*
2.6 (3.7)
16.2⫾9.9*
15.0 (17.0)
64.6⫾37.5*
55.0 (32.5)
3.4⫾4.0
1.6 (3.9)
1.8⫾1.0
1.2 (1.6)
13.5⫾10.8
9.3 (19.2)
55.3⫾20.9
55.0 (33.6)
3.8⫾3.1
2.8 (3.3)
5.9⫾4.9†
3.9 (5.7)
18.6⫾8.8
16.7 (13)
73.2⫾47.3
54.5 (36.0)
*Significantly different from controls.
Significantly different between LHL and RHL.
†
SVV Values
The median absolute SVV deviation (ie, V) was 2.6° (IQR⫽3.6°),
and the median uncertainty (ie, U) was 2.6° (IQR⫽3.7°). Both V
and U were higher in the patient group than in the control group
(V, P⬍.001; U, P⫽.002) (table 2). The SVV was tilted in 12
patients, and the tilt was always contralateral to the lesion. U
was abnormal in 12 patients. Values outside the normative
range were recorded for both V and U in 8 patients. Both
correlated with the Motricity Index score (P⫽.002 and
P⫽.005, respectively), and V also correlated with joint position
sense (P⫽.01). U was greater in RHL than LHL (P⫽.002) and
was greater in the neglect than in the nonneglect group
(P⬍.001).
Postural and Functional Values
The median score for the PASS was 19 out of 36 (IQR⫽19).
In the patient group, median xm was 15mm (IQR⫽17mm) and
median Lx was 55mm (IQR⫽32.5mm); both were higher than
the control values (xm, P⫽.001; Lx, P⬍.001) (see table 2). The
median FIM score was 76 out of 126 (IQR⫽48). PASS score,
Lx, and FIM score were related to Motricity Index score
(P⬍.001, P⫽.03, and P⬍.001, respectively), and PASS and
FIM scores were related to joint position sense (P⫽.003). No
relation was found between balance and age, side of lesion, or
neglect.
Correlation Between the SVV and Balance
The scores for PASS, Lx, and FIM were linked to those for
V (P⬍.001, ␶⫽⫺.47; P⫽.01, ␶⫽.32; P⬍.001, ␶⫽⫺.49, respectively) and the scores for PASS and FIM were also linked
to U (P⫽.006, ␶⫽⫺.35; P⫽.005, ␶⫽⫺.35, respectively) (table 3).
Partial coefficient scores describing the effect of motricity on
the relation between balance and V were as follows: for the
PASS, ⫺0.3; for Lx, 0.2; and for the FIM, ⫺0.31. Partial
coefficient scores describing the effect of motricity on the
relation between balance and U were as follows: for the PASS,
⫺0.1 and for the FIM, ⫺0.1. Among the group of patients with
normative joint position sense (group 2), the relations between
balance (PASS and FIM) and V were significant (P⫽.03 and
P⫽.009, respectively). Among the group of patients with intermediate joint position sense (group 1), the relation between
PASS and V was significant (P⫽.03). Among the group of
patients with anesthesia (group 0), no relation was found between balance and SVV variables.
DISCUSSION
Thirty hemiplegic patients who had recently experienced
their only stroke were studied. To evaluate balance, we chose
to use a clinical tool (PASS), fully validated for recent stroke,
and a force platform. On the platform, the sitting position was
used—first, to obtain the quickest assessment possible and
second, because sitting balance has been reported to correlate
with mobility and functional outcomes after stroke.15-17 Another advantage of this position was that it minimized the
effects of weakness and spasticity on balance. In the rocking
chair paradigm used here, as used by Perennou et al,11-13 2
complementary balance parameters were studied (COP deviation, body instability).
All our patients had hemiplegia, with various Motricity
Index scores, functional independence, and clinical balance.
The time since stroke was homogeneous and short. We found
that more than 40% of patients had an SVV tilt and that 40%
had abnormal uncertainty in the perception of verticality. The
severity of our patients’ impairments probably explains why
the SVV values were more perturbed than in some preceding
studies,2,3 but they were nevertheless similar to the SVV values
recorded in our previous study1 of patients with similarly
severe impairments.
SVV tilt after stroke has been shown to be a consequence of
lesions involving several regions. These include the central
vestibular pathways (brainstem, thalamus, cortex) on either
side,2,9,18 sensory pathways (thalamus, sensory cortex),19,20
and lesions in regions concerned with visuospatial analysis
such as parietal lesions, and, more specifically, right parietal
lesions.3 In the right parietal region, the role of the temporoparietal junction is of very great interest—first, it is a polymodal
sensory area, because it has been shown to respond to either
visual or vestibular inputs2,21 and, second, it is known to be of
crucial importance to balance.12,22
The notion of an abnormal range of uncertainty is probably
of interest. It has already been observed in hemiplegic patients,
and—as here—is very closely related to visuospatial neglect.23
Here, uncertainty was often dissociated from tilt perception. Some
patients assessed the verticality with a constant tilt, whereas
others assessed it with a great variability, as if they had lost the
sense of verticality. Therefore, such uncertainty might be induced by a disturbance different from tilt, probably located at
the level of polymodal sensory integration, which is also the
most common location of visual neglect.
Intuitively accurate perception of visual verticality seems
important to maintaining an upright stance and to walking. The
perception of visual verticality of patients with hemiplegia has
Table 3: The ␶ Statistical Correlation Between Variables Describing the SVV (V, U) and Balance (PASS, xm, Lx) and Characteristics
SVV
PASS
xm (mm)
Lx (mm)
FIM Score
Motricity
Index Score
Age (y)
V (deg)
U (deg)
⫺.47 (⬍.001)
⫺.35 (.006)
.11 (.3)
.08 (.5)
.32 (.01)
.18 (.1)
⫺.49 (⬍.001)
⫺.37 (.003)
⫺.39 (.002)
⫺.35 (.005)
⫺.07 (.5)
.05 (.6)
NOTE. Values are reported as ␶ (P value).
Arch Phys Med Rehabil Vol 87, May 2006
VERTICAL PERCEPTION AND BALANCE AFTER STROKE, Bonan
been investigated in the case of pusher syndrome.4,5 Karnath et
al4 found that this syndrome was related to a perturbed perception of the verticality of one’s own body, known as the
subjective postural vertical (SPV), but they recorded no bias in
perception of the SVV. Such results contrasted with those of
Saj et al,5 who found that patients with pusher syndrome had an
ipsilateral SVV tilt. However, these studies concerned patients
with a very specific and unusual disturbance of balance, who
were not included here because of their incapacity to keep their
balance on the unstable platform. Except in these particular
patients, to our knowledge this is the first systematic study to
find a relation between SVV misperceptions and balance difficulties. The relation between SVV values and balance is
highly significant, although correlation coefficients are relatively not impressive because of the particular distribution of
the ␶ statistics used here. Furthermore, the relation seems in
great part independent of motricity and sensory disorders. The
partial Kendall coefficients, calculated to estimate the role of
motricity in the relation between SVV values and balance, are
actually still significant when they are compared with the total
Kendall coefficients describing the relation between the SVV
misperceptions and balance. Furthermore, the link between
SVV misperception and balance difficulties is stronger when
the joint position sense is not completely impaired. However,
the independence from the joint position sense has to be interpreted cautiously because the number of patients in the 3
sensory groups was small and the confidence intervals for these
estimates were therefore large. SVV misperception might be a
component of the postural disorders occurring after stroke and
should be taken into account when establishing rehabilitation
programs.
Assessment of the SVV in the upright position needs vestibular and visual inputs. Somatosensory information is required when the head or the entire body is tilted,1,19,20,24 which
was not tested in the present study. With regard to vestibular
input, perturbation of the vestibular pathway under the thalamus could not have caused the misperception of the SVV,
because our series included no patients with peripheral vestibular or brainstem disorders. With regard to the visual input,
visual field defects do not seem to disturb SVV perception, but
perturbed visuospatial integration, like neglect, is clearly linked
to perturbed SVV.1,3 Nevertheless, neglect does not stem from
visual input alone but constitutes impairment of higher sensory
integration, because it stems from defects not only of visual but
also of vestibular and somatosensory information.13,25-27 Therefore, in our patients with hemispheric cerebral lesions, SVV misperception seemed to be caused by higher visuovestibular
integration dysfunction, resulting in perturbed construction of
the gravitational referential.
Impaired perception of the SPV has also been shown to be
related to imbalance after stroke. It may constitute another
form of higher sensory perturbation, which affects somatosensory integration more directly.4,28,29 Several researchers29,30
have argued in favor of separate pathways for the perception of
the SPV and SVV. SPV perception is mainly based on somatosensory input through sense organs in the trunk30 and projects
into the posterolateral thalamus,29 whereas SVV perception is
mainly based on visual and vestibular inputs31-33 and projects
into the vestibular cortex.2 Discordant perceptions of the SPV
and SVV have often been reported in both hemiplegic patients
and those with vestibular disorders.4,28,33 Both these perceptions of verticality are probably important in maintaining balance and must be taken into account.
645
CONCLUSIONS
SVV misperception seems, then, to be directly related to
poor balance in acute stroke. This misperception of verticality
might reflect impairment of the higher visuovestibular integration process. The results of our study give insight into balance
disorders after stroke and may change clinical practice. SVV
misperception may be an important element in the assessment
of factors that contribute to balance disorders after hemispheric
stroke. SVV assessment might be a very simple tool for appreciating central postural dysfunction. A test of verticality perception could be proposed for patients with hemiplegia, with the
aim of adapting the rehabilitation program for each person to the
possible impairment of verticality perception. Effective interventions for improving the verticality perception must, therefore, be designed. It might be of interest to test such interventions for their effectiveness in restoring balance in future
studies.
Acknowledgment: We are grateful to Eric Vicaut, MD, of the
Clinical Investigation Unit, GH Lariboisiere–F. Widal, France for
assistance with statistics.
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