Impact of optic flow perception and egocentric
coordinates on veering in Parkinson’s disease
Sigurros Davidsdottir,1Robert Wagenaar,2Daniel Y oung2and Alice Cronin-Golomb1
1Department of Psychology and2Department of Physical Therapy and AthleticTraining Rehabilitation Sciences,
Boston University, Boston, MA 02215,USA
Correspondence to: Alice Cronin-Golomb,PhD,Departmentof Psychology, Boston University, 648 Beacon Street, 2nd floor,
Boston, MA 02215,USA
Spatial navigation is a complex process requiring integration of visuoperceptual information.The present study
examined how visuospatial function relates to navigational veering in Parkinson’s disease, a movement disorder
in which visuospatial cognition is affected by the degeneration of the basal ganglia and resulting dysfunction of
the parietal lobes.We hypothesized that patients whose initial motor symptoms start on the left versus right
side of the body (LPD, predominant right-hemisphere dysfunction; RPD, predominant left-hemisphere dysfunc-
tion) would display distinct patterns of navigational veering associated with the groups’ dissimilar visuospatial
profiles. Of particular interest was to examine the association of navigational veering (lateral deviation along
the medio-lateral axis) with perception of egocentric coordinates and of radial optic flow patterns, both of
which are mediated by the parietal lobes. Thirty-one non-demented Parkinson’s disease patients (16 LPD,
15 RPD) and18 healthy control (HC) adults received visuospatial tests, of whom 23 Parkinson’s disease patients
and 17 HC also underwent veering assessment.The participants were examined on three visual-feedback navi-
gation conditions: none (eyes closed), natural, and optic flow supplied by a virtual-reality headset. All groups
veered to the left when walking with eyes closed, women with Parkinson’s disease more so than the other par-
ticipants. On the navigation assessments with visual feedback, only LPD patients deviated right of centre.
Ontests of visuospatial function, the perceivedmidlinewas shiftedrightwardin LPD (men andwomen), increas-
ingly so with the addition of visual input. In contrast, men with RPD showed leftward deviation. RPD patients
and HC perceived optic flow in the left hemifield as faster than in the right hemifield, with a trend for the oppo-
site pattern for LPD. Navigational veering in LPD was associated with deviation of the perceived egocentric
midline and not with perception of optic flow speed asymmetries, and in RPD it was also associated with
visual dependence, though in fact LPD subjects were more visually dependent than those with RPD.Our results
indicate that (i) parietal-mediated perception of visual space is affected in Parkinson’s disease, with both side
of motor symptom onset and gender affecting spatial performance, and (ii) visual input affects veering.
Keywords: Parkinson’s disease; navigation; optic flow; visuospatial
Abbreviations: cpd=cycles per degree; ECRP=egocentric reference point; HC=healthy control; LPD=Left-onset
Parkinson’s disease; NVF=natural visual feedback; PSE=point of subjective equality; RPD=Right-onset Parkinson’s disease;
Received January 28, 2008. Revised August14, 2008. Accepted September 2, 2008
Spatial navigation is a complex set of behaviours that
includes the processing of incoming sensory information
and the continuous updating of one’s position relative to
spatial landmarks. Systematic biases in processing of
incomingperceptualinformation may contributeto
abnormalities in spatial navigation, including lateral drift,
or veering. The present study examined how vision and
visuospatial function relates to navigational veering in
Parkinson’s disease, a movement disorder that is increas-
ingly recognized as causing alterations in cognition and
perception. Impairments in basic vision as well as in
doi:10.1093/brain/awn237 Brain (2008),131, 2882^2893
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higher-order visuospatial function are well documented
in Parkinson’s disease (Bodis-Wollner et al., 1987; Cronin-
Golomb and Braun, 1997; Lee et al., 1998, 2001a, b;
Amick et al., 2003, 2006; Davidsdottir et al., 2005; Schendan
et al., in press), and may well underlie patients’ difficulty
with spatial navigation beyond the effects of motoric
Information about heading during navigation may be
gained from either perception of optic flow patterns or
perceived location of a goal (Harris and Carre, 2001;
Warren et al., 2001; Kearns et al., 2002; Fajen and Warren,
2004; Turano et al., 2005). Asymmetries in optic flow bias
the perceived heading towards the hemifield in which there
is slower flow speed (Dyre and Andersen, 1996); a strategy
for steering down a corridor is to equalize the speed of
optic flow across the left and right hemifields (Srinivasan
et al., 1991; Duchon and Warren, 2002). Besides optic flow,
the perceived location of a goal may influence one’s path of
movement (Rushton et al., 1998; Harris and Bonas, 2002).
The egocentric reference point (ECRP) divides space into
two lateral hemifields with respect to the midline of the
trunk (Karnath et al., 1991), providing a framework for
spatial orientation and goal-directed actions, including
walking (Hasselbach-Heitzeg and Reuter-Lorenz, 2002).
Functional neuroimaging has demonstrated that parietal
areas are recruited both in perception of optic flow patterns
(Peuskens et al., 2001) and computation of the midline
(Vallar et al., 1999). Shifting of the perception of the
egocentric midline may be seen in patients with spatial
neglect associated with extensive right parietal lesions
(Karnath, 1994; Hasselbach and Butter, 1997), together
estimates, such as is observed on line bisection tests (e.g.
Rorden et al., 2006). While shifting in extrapersonal
midpoint estimates has been reported in Parkinson’s
disease, consistent with a neglect-like pattern (Lee et al.,
2001a), neither egocentric midline shifting nor optic flow
perception has been examined
Impairments in these functions may be expected because
of dysfunction of basal ganglia-thalamocortical circuitry
that extends to the parietal lobe (Middleton and Strick,
2000a; Clower et al, 2005; Bartels et al., 2006).
A factor of potential importance in investigating the
association between deficits in visuospatial perception and
veering in Parkinson’s disease is the hemispheric side of
disease onset. Parkinson’s disease patients who initially
experience motor symptoms on the left side of their body
(LPD), reflecting predominantly right-hemisphere dysfunc-
tion, generally present with more pronounced disturbance
on tests of spatial perception than do patients whose motor
symptoms start on the right side of their body (RPD,
predominantly left-hemisphere dysfunction) (Blonder et al.,
1989; Lee et al., 2001a, b; Harris et al., 2003). There is
evidence that the representation of external space (particu-
larly left hemispace) in LPD patients is compressed (Lee
et al., 2001a, b). These findings are consistent with LPD
having a shift of midline perception to the right. It is also
relevant that parietal activation in the perception of optic
flow patterns is predominantly in the right hemisphere
(Peuskens et al., 2001) and therefore optic flow perception
as well as egocentric midline alignment may be particularly
deficient in LPD patients.
When the integrity of optic flow perception is compro-
mised, such that optic flow speed perception is asymmet-
rically affected, or the midline is misaligned, systematic
heading errors in navigation (veering) may be expected.
The aim of the present study was to examine navigational
veering in Parkinson’s disease and the contributions of
disturbances in the perception of optic flow and the
egocentric midline to biases in this behaviour. It was
predicted that persons with Parkinson’s disease, who have
experience an imbalanced optic flow pattern, in which
motion in the non-compressed side of space is perceived to
be faster than in the compressed space, wherein points of
texture appear to travel a shorter distance in the same
amount of time. Such inaccuracy in visual perception
during navigation would result in a biased path of
locomotion. In the case of LPD, with greater right than
left parietal dysfunction, perceived compression of the left
hemispace would translate into the perception of slowed
optic flow speed on that side. Because individuals move
away from the side of faster-moving flow, LPD should veer
to the left. In contrast to the results predicted for optic flow
perception, if LPD have a rightward shift of the egocentric
midline, one would expect rightward veering. Predictions in
both cases are less clear for RPD, for whom there is less
evidence of spatial distortion. As Lee and colleagues (2001b)
provided some evidence that spatial perception is expanded
rather than compressed in RPD, one might expect these
individuals to show a pattern of veering opposite that
of LPD. Investigation of the direction of veering would
provide evidence of the preferential use of optic flow
perception or midline reference to update position during
spatial navigation in Parkinson’s disease. To this purpose
we manipulated optic flow speed during an open-field test
of spatial navigation and assessed the role of midline
estimation as well as vision and other visuospatial function
There were 49 individuals in the study: 31 patients with idiopathic
Parkinson’s disease (15 men, 16 women) and 18 healthy control
(HC) adults (nine men, nine women). Consent was obtained
according to the Declaration of Helsinki. The study protocol was
approved by the Institute Review Board of Boston University. All
participants were native speakers of English. Exclusion criteria
included co-existing serious chronic medical illnesses (including
psychiatric or neurological), use of psychoactive medications
besides antidepressants and anxiolytics in the Parkinson’s disease
Veering in Parkinson’s diseaseBrain (2008),131, 2882^28932883
group, use of any psychoactive medications in the HC group,
history of intracranial surgery, traumatic brain injury, alcoholism
or other drug abuse, or eye disease or abnormalities as noted on a
neuro-ophthalmological examination. Individuals who had a
physical disability that prevented them from moving freely in
the open-field spatial navigation task (such as past knee or hip
surgeries or lower back pain) were excluded from the study.
Participants were not demented as indicated by scores of 26 or
above on the Mini-Mental State Examination (MMSE; Folstein
et al., 1975) and 135 or above on the Mattis Dementia Rating
Scale (DRS; Mattis, 1976, 1988).
The Parkinson’s disease patients included 16 with LPD (nine
men, seven women) and 15 with RPD (six men, nine women).
Only Parkinson’s disease patients with clear asymmetric onset of
motor symptoms were enrolled in the study. Initial side of motor
symptom onset was affirmed with a review of neurology records.
Although most individuals were experiencing motor symptoms on
both sides of their body at the time of the study, this was accept-
able because hemispheric brain disease asymmetry is maintained
after motor symptoms have progressed from unilateral to bilateral
(Rinne et al., 1993). Motor disability as indexed by Hoehn and
Yahr stage (H & Y; Hoehn and Yahr, 1967) was similar for the
LPD andRPD groups,Kolmogorov-Smith
P=0.96. The median stage of H&Y was 2 (off medications).
Only one patient was stage 1.5 (unilateral), 25 were stage 2 (mild
bilateral), four were stage 3 (moderate bilateral with postural
instability) and one was stage 4 (considerable disability but able to
walk independently). Age and education were matched for LPD,
RPD and HC, F(2, 46)=0.43, P=0.65 and F(2, 46)=0.34,
P=0.72, respectively. Mean age in years for LPD was 60.0
(SD=8.6); RPD 62.8 (SD=7.8); HC 61.2 (SD=8.8). Mean
education in years for LPD was 16.6 (SD=2.6); RPD 17.0
(SD=2.9); HC 16.2 (SD=2.6). The three groups performed
similarly on the MMSE and the DRS, F(2, 46)=0.38, P=0.69 and
F(2, 46)=0.74, P=0.48, respectively. All participants were right-
handed except for one LPD and one HC. Mean Parkinson’s
disease duration was 5.9 years (SD=3.4, range 1–15) with no
difference between LPD and RPD, t(29)=1.51, P=0.14 (LPD:
M=6.8 years; SD=3.6, range: 1–15; RPD: M=4.9 years, SD=3.1,
Mood functioning was assessed with the Beck Depression
Inventory-2 (BDI-2; Beck, 1987). A one-way analysis of variance
(ANOVA) demonstrated that
differences, F(2, 46)=8.44, P=0.001. Post hoc Scheffe ´ t-tests
showed that LPD and RPD scored higher on the BDI-2 than did
HC (P=0.002 and P=0.009, respectively) and that LPD and RPD
did not differ (P=0.91). Thirty-seven participants scored within
the normal range on the BDI-2 (range 0–9), including all HC and
19 Parkinson’s disease patients. Depression scores were used as a
covariate in the main experimental analyses. There was no
difference in the level of Parkinson’s disease-related disability for
LPD and RPD as measured with the Parkinson’s Disease Quality
of LifeInventory-39 (Jenkinson
The majority of patients reported using dopamine agonists
(24, or 77%) and/or levodopa (27, or 87%). Six (19%) used
monoamine oxidase inhibitors and catechol-O-methyltransferase
inhibitors and ten (32%) used amantadine or anticholinergic
agents. Nine (29%) reported using antidepressant or antianxiety
there weresignificant group
medications. LPD and RPD did not differ significantly in
Characteristics of participants who completed the
Of the 31 Parkinson’s disease patients and 18 HC who volunteered
to participate in the study, 23 Parkinson’s disease patients and 17
HC completed the assessment of veering during walking. There
were eight individuals for whom we were unable to schedule the
walking assessment within a short enough time of the visuospatial
testing, or who declined the opportunity to schedule a session to
walk in the optic flow virtual reality (VR) condition after
introduction to the optic flow environment on a perceptual
measure. The majority of these individuals were RPD (seven of
eight). Demographics, disease variables (duration and motor
disability) and basic visual functioning were similar between
Parkinson’s disease patients who did and who did not complete
the walking session. Additionally, veering data from the two left-
handed individuals (1 LPD, 1 HC) were not included in the
analyses, because both individuals demonstrated an exaggerated
degree of veering compared with their group counterparts,
consistent with reports that handedness affects lateralized motor
preference (Mohr et al., 2003). This was a conservative decision, as
it is likely that failure to exclude the LPD patient would have
produced larger statistical effects for the deviation of the LPD
group. Both of these individuals demonstrated rightwards veering;
the left-handed LPD veered 202mm rightward (12 times that of
right-handed LPDs) and the left-handed HC veered 106mm
rightward, which is a shift both in magnitude and direction of
veering compared to other HC. In sum, veering data from
14 LPD, 8 RPD and 16 HC are reported, with groups matched for
age and education, F(2, 38)=0.20, P=0.82 and F(2, 38)=0.38,
P=0.69, respectively, and with equal numbers of men and women
in each group. There were no significant differences between LPD
and RPD for disease duration, t(20)=1.58, P=0.13; extent of
motor disability as measured by the H&Y scale, K-S Z=0.48,
P=0.97, or for participant characteristics or vision assessments
(described in the Results section).
Assessment of veeringin an open-field environment
Navigation with natural visual feedback and eyes closed. Prior to
data collection, participants were trained to walk a 15m long
pathway with eyes open at 0.8?0.1m/s and to maintain this
walking speed throughout the session. There were five trials
conducted with eyes open, then five with eyes closed. The
participant was then fitted with a headset (head-mounted display),
which was connected to a VR system. Five additional training
trials were conducted in which the participant wore the head-
mounted display and was instructed to walk at the target speed
with eyes open. Three-dimensional kinematic data were collected
through anOptotrak/3020 System
Waterloo, ON, Canada). An Optotrak bank was placed on each
side of the walkway and a third bank was located at the end of the
walkway in order to capture bilateral movements for at least eight
strides. Calibrations among the three banks were accepted when
the mean error was 1.5mm or less. Infrared light emitting diodes
(LEDs) were placed bilaterally on ankles, knees (patella), hips
2884Brain (2008),131, 2882^2893S. Davidsdottir et al.
(anterior superior iliac spine), wrists (radiocarpal joint), shoulders
(humeral head), cheeks (2cm below zygomatic arch) and chin.
Small adjustments from these positions were made to increase
LED visibility when necessary. The instantaneous position of each
LED was sampled at a rate of 100Hz and stored to disk for further
analysis. The average between left and right hip position data in
the Z-axis (medio-lateral axis) was used to estimate heading drift
during walking. The measure of drift was the signed distance
between Z1 and Zn (Drift=Zn?Z1). Zn was the maximum
positive value in the Z-direction of the last stride cycle and Z1was
the maximum positive medio-lateral deviation of the first stride
Navigation in a VR corridor with symmetrical optic flow. The
procedure was similar to the open-field natural visual feedback
(NVF) condition, except that VR input was applied. The VR input
consisted of a virtual hallway, which was composed of two
sidewalls of white random dots on a black background, with a
black floor and ceiling devoid of texture. There was one condition
in which the white dots on the black backgrounds were stationary
(0.0m/s), and four in which optic flow speed was symmetric
across hemifields (0.4, 0.8, 1.2 and 1.6m/s). This perceived scene
was consistent with self-motion through a three-dimensional
corridor. Across VR trials, participants always walked down the
hallway at a speed of 0.8m/s while optic flow speed was varied.
There were five training trials followed by the experimental
conditions, each of which consisted of five walking trials.
The virtual hallway was created using World ToolKit Release 9
(Sense8, San Francisco, CA, USA) on an Onyx2 Reality graphics
work station (Silicon Graphics Inc., Mountain View, CA, USA). The
scene was displayed on a ProView 60 head mounted display (Kaiser
Opto-Electronics Inc, Mountain View, CA, USA) weighing 1.75lbs.
This display contained two active LCD panels (640 ?480 resolution,
true color, 60Hz) and had a 60?field of view (diagonal) with 100%
overlap to allow for true stereo viewing. Field of view was restricted
to the VR environment by an additional mask that occluded vision
outside the LCD panels. Head coordinates (except for the anterio-
posterior axis) were tracked in real time, using an IS 900 LAT
system (InterSense, Burlington, MA, USA) and the information was
used to update the visual scene. The dots disappeared off the edges
of the LCD panels and reappeared at the open end of the hallway.
The depth of the hallway ahead of the participants remained
constant regardless of the position of the participants—that is, an
infinite hallway was created in which the participants could not
move closer to the end of the hallway, but they were still able to
experience motion parallax and move closer to the right or left wall.
We assessed acuity, contrast sensitivity and planar motion
perception. Participants used their own refractive correction.
Most participants (24/31 Parkinson’s disease and 13/18 HC)
underwent a neuro-ophthalmological examination to ensure eye
integrity, ruling out any ocular disease or other abnormalities; the
rest experienced scheduling difficulties. There was no significant
difference in the basic visual functioning of individuals who
underwent this exam and those who did not (e.g. letter-
identification contrast sensitivity, t(6.47)=?0.65, P=0.54).
Acuity. Snellen eye charts (Lighthouse Company, New York,
NY, USA) were used to measure near binocular visual acuity
at 16 in.
Contrast sensitivity. was assessed binocularly with near (16 in.)
and far (10ft) Functional Acuity Contrast Test charts (FACT:
Stereo Optical, Chicago, IL, USA) and
letter-identification measure. The FACT determined contrast
sensitivity level for five spatial frequencies: 1.5, 3, 6, 12 and 18
cycles per degree (cpd). The computer-based letter-identification
measure is a genuine threshold test, similar to one used to
demonstrate contrast sensitivity deficits in Parkinson’s disease
(Amick et al., 2003). This task uses a ZEST procedure that permits
the reliable determination of a threshold in relatively few trials.
Further details of both contrast sensitivity tests are available in
Gilmore et al. (2005).
Planar motion perception. Participants
centrally presented field in which coherent motion appeared to
move either up or down. The task was to state the direction of
coherent dot motion (up or down). The window of motion was
200?200 pixels subtending 6.9?
subtended ?0.069?of visual angle and was displayed for 24ms.
Noise dots were randomly replotted. Coherent dot motion varied
from 0% to 100%. Responses were recorded on computer by the
examiner. Threshold was determined using a staircase procedure
with a stopping criterion of 25% standard error of the estimate.
Further details of this test are available in Amick et al. (2003).
of visual angle. Each dot
We assessed visual dependence and line bisection, the latter of
which is sensitive to spatial neglect, in addition to optic flow
perception and egocentric reference.
Visual dependence. We used large-screen presentation of a
1.5m horizontal line (53.1?of visual angle) that was tilted at the
outset of each trial (initial tilt ranging from 9?to 12?). Azulay
et al. (2002) reported increased visual dependence in Parkinson’s
disease using a similar test. Participants indicated when the rod
was horizontal. There were 10 trials, with equal number of trials in
which the left end of the line was initially tilted upwards and
downwards. The angle of the line was gradually altered to become
more horizontal by1?
horizontal reflected the level of visual dependence.
Line bisection. The Landmark test of line bisection has been
used to demonstrate lateral biases in allocentric spatial perception
in Parkinson’s disease (Lee et al., 2001a). This version of the test
did not require use of motor skills and did not have time limits.
Participants sat in front of a projection screen, trunk aligned with
a predetermined midpoint. A 2.2m horizontal line and a vertical
cursor were projected on the screen (72.5?of visual angle). The
cursor was initially presented on the left or the right of the line’s
true center, at a starting point of 8–12% deviation (of the total
length of the horizontal line). Cursor adjustments were made in
increments of 0.5% of the total line length. There were 10 trials,
with equal number of trials in which the cursor initially appeared
on right and left. The examiner moved the cursor towards the
line’s center and the task was to state when the cursor fell in the
center of the horizontal line. Lateral deviation of the judgment of
the center of the horizontal line was analysed.
Optic flow perception. Perception of expansive optic flow
patterns was measured by manipulating optic flow speeds in the
two hemifields. Participants sat in front of a large projection
screen using a headrest to align them with a predetermined
Veering in Parkinson’s diseaseBrain (2008),131, 2882^28932885
midpoint. Two mirror-symmetrical stimulus fields were presented
simultaneously on both sides of fixation, each extending 41?to the
periphery. The symmetrical fields resembled the hallway in the VR
walking trials, in that they were composed of two sidewalls of
white random dots on a black background with a black floor and
ceiling devoid of texture. On the optic flow task, differences in
motion speed for the dots were introduced by gradually varying
the temporal frequency in one of the two stimulus fields, starting
from either a very slow (0.0–0.15m/s) or fast (1.45–1.60m/s)
speed compared to the fixed-speed visual field for that set of trials
(0.80m/s). Speed adjustments were made in increments or
decrements of 0.05m/s. This perceived scene was consistent with
self-motion through a three-dimensional corridor. On trials in
which one hemifield speed was held constant, the participant was
asked to determine whether movement in the other hemifield was
faster, slower or the same speed as in the first hemifield. There
were 20 trial sets, 10 for each fixed-speed visual field, for a total of
636 judgments about the relative hemifield speeds. The point of
subjective equality (PSE) was obtained when the participant
judged the speed of optic flow in the two hemifields as equal. The
PSE indicated whether there was a hemifield imbalance that
distorted the perceived symmetry of the optic flow.
Egocentric reference point. ECRP, which divides space into
two hemifields by way of perception of the spatial midline, was
measured by means of a pointing task (Heilman et al., 1983).
Participants sat with the sternum aligned to a predetermined
point, using a headrest. They placed the index finger on the
sternum for a reference, then pointed straight ahead, then lowered
the arm to place the index finger on the desk. There were two
conditions for this test, one with eyes open (five trials each with
right and left hands) and one with eyes closed (five trials each
with right and left hands). There was a large sheet on the desk, on
which the experimenter marked the placement of the index finger.
Responses were analysed for lateral deviation in estimates of the
Notes on statisticalanalyses
Analyses were corrected for multiple comparisons (Bonferroni
method). Analysis of covariance was used to account for variables
that could affect the dependent measures (e.g. age disease
onset; disease duration). In all cases, gender was examined as a
variable but is mentioned in results only if there was a significant
Veering during open-field spatial navigation
Statistical results of the veering assessments appear in
Eyes-closed condition. All groups veered leftward. While
women demonstrated greater leftward veering than men in
the Parkinson’s disease group, there was no signifi-
cant difference between men and women in the HC
group (Fig. 1).
Natural visual feedback condition (eyes open). Veering was
affected by group but not by gender or trial order. The LPD
group veered rightward, and differed significantly from the
other two groups, whereas RPD and HD veered leftward
and did not differ from each other (P=0.61) (Tukey post
hoc tests) (Fig. 2).
Virtual reality condition. As in the NVF condition, LPD
veered rightward and RPD and HC veered leftward. LPD
differed significantly from RPD and HC, and HC and RPD
differed significantly from each other (Games-Howell post
Figure 3 comparesveering
conditions (eyes-closed, NVF and VR visual feedback).
Because there was no effect of optic flow speed, veering on
VR walking trials was averaged across the five speed
conditions. Whereas all participants veered leftward in the
absence of visual information, decreased leftward deviation
was observed upon walking with visual feedback, indepen-
dent of whether the feedback was natural or synthetic (VR),
on the three walking
T able1 Results of ANOVA for veering and sources of
variance for eyes-closed, NVF and VR conditions
NVF condition (eyes open)
Optic flow speed
Fig.1 Veering during a walking trial without visual feedback
(eyes closed). HC: eight women, eight men, LPD: seven women,
seven men, RPD: four women, four men. Negative signs represent
leftward deviation from the true centre.Horizontal lines represent
standard error of the mean.
2886Brain (2008),131, 2882^2893S. Davidsdottir et al.
with LPD demonstrating absolute rightward deviation
(343.7mm shift), and RPD and HC remaining left of
center (RPD=171.4mm shift, HC 77.2mm shift). Paired
t-tests demonstrated that veering of LPD and RPD was
significantly altered by visual input (P50.001, P=0.01,
respectively), and that veering of HC did not change across
Statistical findings are presented in Table 1. As there were
no significant interaction effects for the various conditions
(P40.10 in each case), those P-values are not shown.
Acuity and contrast sensitivity. Median near acuity for
each group was 20/16 (–0.1 LogMar). The groups (LPD,
RPD and HC) performed similarly on the FACT charts.
The computerized test that identified contrast threshold for
letter identification elicited performance differences between
the groups. HC required less contrast than RPD in order to
perform at an 80% accuracy level, there was a trend for
LPD to perform more poorly than HC and there was no
significant difference between RPD and LPD performance
on this test (P=0.004, 0.05 and 1.00, respectively)
(Bonferroni post hoc tests). These findings are in accord
with Amick et al. (2003) who found normal Parkinson’s
disease performance on the FACT but impaired contrast
sensitivity using the more sensitive letter-identification test.
Accordingly, data from the latter test only are included in
subsequent correlational analyses.
Planar motion perception. Whereas men with Parkinson’s
disease performed better than women with Parkinson’s
disease, the opposite occurred for HC participants, as HC
women outperformed HC men. There was no difference
between men and women (such as age or corrected visual
acuity) that explained this finding. The results for the
Parkinson’s disease groups were similar in Amick et al.
(2003), but in that study, the HC men outperformed HC
sensitivity and motion perception measures appear in
Table 2. The statistical findings appear in Table 3.
Statistical findings for the visuospatial tests are provided in
−200 20 4060
Fig. 2 Veering during a walking trial with NVF condition (eyes
open). HC: N = 16, LPD: N = 14, RPD: N = 8. Negative signs
represent leftward deviation from the true center. Positive signs
represent rightward deviation from the true center. Horizontal
lines represent standard error of the mean.
−2000 200 400
Fig. 3 Comparison of veering on three walking conditions: eyes
closed, NVF,VR. HC: N = 16, LPD: N = 14, RPD: N = 8. Negative
signs represent leftward deviation from the true center. Positive
signs represent rightward deviation from the true center.
Horizontal lines represent standard error of the mean.
T able 2 Performance by group on tests of visual
functioning, mean (SD)
FACT log contrast sensitivity: far
FACT log contrast sensitivity: near
Michelson contrast at
criterion error rate of 20%
46.5 (20.7) 52.8 (20.7) 30.9 (12.6)
Planar motion perception:
percent coherent dot
motion at threshold.
W (women), M (men)
W: 9.3 (3.9)
M: 5.7 (2.8)
W: 9.1 (3.0)
M: 5.6 (2.8)
W: 5.0 (2.8)
M: 7 .2 (3.6)
Veering in Parkinson’s diseaseBrain (2008),131, 2882^28932887
Visual dependence. The three groups performed differ-
ently on this task. LPD were more visually dependent than
either RPD or HC, and RPD were more visually dependent
than HC (Games-Howell post hoc tests).
Line bisection: Landmark test. Whereas men in the LPD
group deviated towards the right, men in the HC group
estimated the midline to be close to its true midpoint and
men in the RPD group demonstrated a relatively large
leftward deviation. In contrast, women in the LPD group
deviated towards the left, women in the HC group deviated
to the right, and performance of women in the RPD group
was close to the true midpoint. These findings are depicted
in Fig. 4.
asymmetries. LPD performed differently on this test than
either HC or RPD (P=0.016 and 0.024), but there was no
significant difference between HC and RPD (P=0.096).
Paired t-tests were used to assess the perception of the two
hemifields for PSEs for each group. When optic flow speeds
were equal in the two hemifields, RPD and HC perceived
the optic flow speed in the left hemifield as faster than in
the right hemifield (P=0.007 and 0.005, respectively). On
average, RPD estimated optic flow speed in the left
hemifield as 0.024m/s faster, and HC estimated it as
0.020m/s faster. There was an opposite trend for LPD to
evaluate the left hemifield optic flow speed as slower than
optic flow speed in the right hemifield, on average by
Egocentric reference point estimation. The HC participants
(who were tested first) did not use a headrest; Parkinson’s
disease patients required that support to maintain their
position during this test. Because the groups differed on
this procedure, performance of Parkinson’s disease patients
only was analysed. Across visual input conditions, on
average, women with LPD exhibited a relatively large
deviation toward the right side but men with LPD deviated
minimally leftward. A different pattern was observed for
RPD, with women displaying a small leftward and men a
small rightward deviation (Fig. 5).
There was a trend for an interaction between group,
gender and condition. On average, women with LPD
showed rightward bias with eyes closed that was exagger-
ated with visual input. Men with LPD showed leftward bias
with eyes closed that changed to rightward bias with visual
input. Women with RPD, like men with LPD, moved from
leftward bias with eyes closed to rightward bias with visual
input. Hence, in these three groups, addition of visual input
of hemispheric speed
T able 3 Results of ANOVA of tests of visual functioning
FACT contrast sensitivity
Letter-identification contrast sensitivity
Planar motion perception
Sources of variance for fact contrast sensitivity, letter-identifica-
tion contrast sensitivity and planar motion perception.
T able 4 Results of ANOVA on tests of visuospatial function
Landmark test (line bisection)
Initial location of the bisection cursor
Sources of variance for visual dependence, Landmark test (line
bisection), optic flow and ECRP.Constant side: Hemispace side
in which optic flow speed was held constant.
DEVIATION (PERCENT OF LINE LENGTH)
Fig. 4 Performance by group and gender on the Landmark test.
Horizontal lines represent standard error of the mean. HC men
and RPD women estimated the midpoint to be close to the true
2888Brain (2008),131, 2882^2893 S. Davidsdottir et al.
resulted in rightward bias, which constituted a change of
direction from leftward deviation or an exaggeration of a
preexisting rightward deviation. Men with RPD performed
opposite the other groups, moving from rightward bias
with eyes closed to leftward bias with visual input.
Correlations between tests of vision and visuospatial
function, and between tests of visuospatial function. There
was a significant correlation between visual dependence and
contrast sensitivity impairment on the letter-identification
measure, r=0.54, P=0.001 for the Parkinson’s disease
participants. There was no correlation between motion
perception and any of the other visuospatial function tests
in any of the experimental groups.
We also examined correlation of performance on tests of
visuospatial function pertaining to asymmetries in percep-
tion of the two hemispaces. Analyses were split across
group and gender, with Bonferroni corrections for multiple
comparisons (a 0.05/6=0.0083). There were no significant
correlations between performance on the Landmark test,
ECRP deviation or optic flow asymmetries for men or
women in any of the groups.
Correlations between perceptual variables and veering
without visual feedback and with NVF. There were no
significant correlations for any group between veering
under these conditions and any participant characteristic
or measure of vision or visuospatial ability including optic
flow PSE, deviation on the Landmark test, or deviation on
the ECRP estimate test.
Correlations between visual and visuospatial variables and
veering under VR condition. Visual dependence was corre-
lated with VR veering for RPD (P=0.004), with RPD who
were more visually dependent veering to a greater extent to
their left. For RPD, there was a significant correlation
between VR veering (at 0.0m/s, stationary walls) and ECRP
deviation (on the eyes-closed trial), such that they veered in
the direction of the ECRP shift (r=0.91, P50.01). For
LPD, there was a significant correlation between VR veering
(at 1.6m/s) and ECRP deviation (on the eyes-open trial)
such that patients veered in the direction of shifted ECRP
(r=0.67, P=0.01). There were no other correlations
between VR veering and performance on measures of
basic visual or visuospatial function, including optic flow
PSE and the Landmark Test.
The present study provides evidence for the existence of
distinct patterns of veering in Parkinson’s disease that are
associated with side of motor symptom onset, gender and
the level of visual input available. It further documents
impairments in optic flow perception and the perception of
the egocentric midline that vary with side of disease onset
When participants were instructed to walk straight ahead
with eyes closed, all groups veered leftward (women with
Parkinson’s disease more so than other participants). Upon
addition of visual feedback (either natural or virtual-reality
input), LPD demonstrated a rightward shift in veering
(across the medio-lateral axis), whereas HC participants
and RPD continued to veer leftward (RPD more than HC).
In healthy individuals, veering, or direction of heading,
may be influenced by optic flow asymmetries (e.g. Duchon
and Warren, 2002), by information gained from the
egocentric reference system (Rushton et al., 1998; Harris
and Bonas, 2002), or by both types of information (Warren
et al., 2001). In Parkinson’s disease patients, we expected
that reliance on information provided by optic flow
asymmetries would be perturbed by abnormal perception
of the size of the visual hemifields. Specifically, use of optic
flow equalization strategies to maintain heading would lead
to leftward deviation in LPD (on the basis of the prediction
of perceived spatial compression of the left visual hemifield)
and possibly rightward deviation in RPD (on the basis of
the prediction of perceived spatial expansion). In contrast,
based on the findings of Rushton and colleagues (1998),
who reported that a lateral shift of the perceived egocentric
midline is associated with veering toward the corresponding
side, and on the study by Bracha et al. (1987), who found
spontaneous whole-body rotational behavior towards the
ipsilesional hemisphere in patients with Parkinson’s disease,
one might predict that navigation based on egocentric
midline perception would follow a pattern opposite to that
predicted by optic-flow reliance. That is, patients with LPD
would veer rightward and patients with RPD would veer
leftward. Our data mainly bore out the latter prediction.
We found that veering corresponded to the shifting of the
perceived midline rather than to optic flow perception (PSE
of speed in the two hemifields) and, for the RPD group,
also corresponded to increased visual dependence.
ECRP DEVIATION (DEGREES)
Fig. 5 Performance by group and gender on the ECRP task.
Horizontal lines represent standard error of the mean.
Veering in Parkinson’s diseaseBrain (2008),131, 2882^28932889
Leftward navigational bias under visual feedback in the
HC group is consistent with the findings of Mohr et al.
(2004), who reported leftward rotational bias. These
investigators suggested that visually directed left-sided
rotational preference arises from greater activation of the
right- than the left-hemispheric dopaminergic system, a
consequence of relatively great right-hemisphere processing
of visuospatial information. In our HC group, leftward bias
occurred under the eyes-closed as well as the visual
feedback (natural and virtual-reality) conditions. In our
sample, there were two left-handed individuals, one in the
LPD group and one in the HC group, who exhibited
veering patterns that were shifted both in magnitude and
direction. This finding underscores the importance of
controlling for handedness in studies of veering.
The LPD results are consistent with the overall effects of
increased visual feedback on walking in Parkinson’s disease
patients that was reported by Almeida et al. (2005) as well
as with the idea of Mohr et al. (2004) that in LPD, there
would be decreased dopamine available to the right-
hemisphere system during visuospatial processing and
therefore there would be no ‘normal’ leftward bias. In the
present study, the extent of veering in the RPD group
correlated with the extent of visual dependence and shifting
of the egocentric midline. In contrast, veering in the LPD
group was primarily associated with ECRP deviation and
not with visual dependence. This result suggests that visual
dependence in the LPD group (which was larger in extent
than was that of the RPD group) may have already exerted
its maximal influence. Because the veering pattern for
Parkinson’s disease patients changed with visual feedback,
the results of these experiments cannot be attributed simply
to directional hypokinesia.
In regard to visual dependence, Parkinson’s disease
patients rely more than healthy adults on visual guidance
or feedback on tasks of simple perception and postural
manipulations, and when walking (Cooke et al., 1978;
Bronstein et al., 1990; Azulay et al., 1999, 2002; Morris et al.,
2005). Our new finding is that the extent of visual
dependence varies as a function of laterality of motor
symptom onset. Patients with LPD were more visually
dependent than were patients with RPD, and those with RPD
were more visually dependent than were HC. Only for RPD
was visual dependence associated with veering, suggesting
that in the LPD group there were more salient influences
on veering, correlated with associated shifting of the ECRP.
This is the first study to present evidence for impaired optic
flow perception in Parkinson’s disease, although there are
studies on the effects of modulation of speed of artificial
optic flow on gait parameters in Parkinson’s disease
(Schubert et al., 2004; van Wegen et al., 2006). As
predicted, we found that RPD and HC perceived flow
in their left hemifield as moving faster than the right
hemifield, as indicated by their PSE of flow speed in the
two hemifields, whereas an opposite trend was observed in
LPD, in which there is evidence for compressed perception
of left hemispace (e.g. Harris et al., 2003). The evidence
that parietal-mediated optic flow perception is impaired in
Parkinson’s disease lends support to the notion of parietal-
lobe dysfunction in Parkinson’s disease (Cronin-Golomb
and Braun, 1997; Amick et al., 2006; Schendan et al., in
press). It appears likely that parietal areas that are recruited
in optic flow perception may be functionally affected in
Parkinson’s disease through disruption of the basal ganglia-
thalamocortical loops (Clower et al., 2005).
While disruption of egocentric midpoint estimation may
certainly be seen in patients with spatial neglect (Hasselback
and Butter, 1997; Karnath, 1994), not all researchers have
found a correlationbetween
traditional neglect measures (e.g. allocentric line bisection
tasks) (Chokron and Bartolomeo, 1997; Hasselbach and
Butter, 1997; Pizzamiglio et al., 2000; Chokron et al., 2002;
Pisella et al., 2002), and accordingly the possibility has been
raised that these phenomena
(Chokron, 2003). In light of this possibility, we used a
traditional line bisection measure (the Landmark test) in
addition to the egocentric midline estimation task. On both
tasks, patients’ gender, as well as which hemisphere was
predominantly affected, played a role in determing the
direction of the shift. Overall, on the egocentric midline
estimation task, patients showed shifts in opposite direc-
tions depending on which hemisphere was predominantly
affected (LPD: rightward, RPD: leftward). On the Landmark
measure, men with Parkinson’s disease showed a similar
pattern, but not women; LPD women showed a slight
leftward deviation and RPD women remained close to the
center in their estimates. In the overall direction of effect,
the results are primarily in accord with findings from
neglect patients who demonstrate shifting of the midline
towards the ipsilesional hemispace (Karnath et al., 1991;
Chokron and Bartolomeo, 1997; Karnath, 1997; Richard
et al., 2004), though the intertask correlations were not
significant in our study. As we expected, the observed
Parkinson’s disease deviations were small (largest 52?)
compared to those reported in neglect patients (commonly
10–15?). We interpret our findings as suggestive that
Parkinson’s disease affects the integrity of the ability to
estimate the midline.
On the egocentric midpoint estimation task, there was a
trend for LPD to demonstrate an increased deviation
towards the right side when they performed the task with
eyes open compared to eyes closed. RPD patients showed
less deviation upon performing the task with their eyes
open, and their estimates approached the true reference
point. The finding that Parkinson’s disease patients’ midline
deviation was dependent on visual input provides evidence
shifting ofECRP and
2890Brain (2008),131, 2882^2893S. Davidsdottir et al.
for the impact of visuoperceptual biases on the perception
of the ECRP in Parkinson’s disease, with deviation
increasing for LPD and decreasing for RPD. Richard et al.
(2005) reported that neglect patients demonstrated greater
deviation of the ECRP when they had access to visual input.
Because the midline deviation of LPD patients became
more pronounced with added visual feedback, it appears
that behavioural biases in these individuals reflect genuine
visuoperceptual biases rather than being due solely to
motor biases (hemispatial akinesia), as has in the past
been suggested for Parkinson’s disease (e.g. Brown and
Marsden, 1986; Garcia-Larrea et al., 1996; Heilman et al.,
Despite some gender differences in group performances,
there was an overall similarity in direction of deviation on
the egocentric and allocentric midpoint measures, possibly
reflecting to some extent a common neural substrate.
This common substrate likely involves parietal areas, as
functional neuroimaging studies on healthy individuals
have shown increased activation in the right posterior
parietal lobe with line bisection (Fink et al., 2000) and with
computation of the mid-sagittal egocentric reference plane
(Vallar et al., 1999). As technology develops, more fine-
grained analysis of the within-parietal substrates may be
possible, accounting for behavioral evidence of a distinction
between egocentricand allocentric
(Chokron, 2003). Lesion studies have demonstrated that
shifting of the egocentric midline is predominantly seen
in patients with spatial neglect due to extensive right
parietal lesions (Hasselbach and Butter, 1997; Karnath,
1994). Deviation of this type has also, however, been
documented in idiopathic cervical dystonia (Muller et al.,
2005), which is associated with gray matter increase in the
putamen (Black et al., 1998) and in the globus pallidus in
addition to changes in the metabolism of cortical areas of
the basal ganglia-thalamocortical circuit (e.g. right supple-
mental motor area, dorsolateral prefrontal and visual
cortex) (Dragansky et al., 2003). These observations,
together with those of the present study of Parkinson’s
disease, suggest a central role of the basal ganglia-
thalamocortical system, which includes the parietal lobes,
of egocentric midline
Gender effects in the Parkinson’s disease group were noted
on several tasks, including the navigation assessment,
motion perception, ECRP deviation and the Landmark
test. This is an area that clearly requires more investigation,
with larger samples, in light of Parkinson’s disease gender
(Davidsdottir et al., 2005), disease prevalence rate (Van
den Eeden et al., 2003) and constellation of motor
symptoms (Bordelon and Fahn, 2006).
The present study provided evidence that parietal-mediated
perception of visual space is affected in Parkinson’s disease,
including perception of optic flow speed and egocentric
midline coordinates. Side of motor-symptom onset and
gender affected spatial performance. The walking assess-
ment demonstrated that visual input affects veering, that
veering corresponds to the shifting of the egocentric
midline rather than to abnormal perception of optic flow
speed in the two hemifields and, although LPD were more
visually dependent than RPD, only in RPD was visual
dependence associated with veering.
We thank all of the individuals who participated in this
study. Our recruitment efforts were supported, with our
gratitude, by Marie Saint-Hilaire, MD, and Cathi Thomas
RN, MS, of Boston University Medical Center Neurology
Associates, and by Boston area Parkinson Disease support
groups. We thank Sandy Neargarder, PhD, for consulting
on statistical analyses and for reviewing the manuscript.
Melissa Amick, PhD, Tom Laudate, MA, and Bruce Reese,
MA, provided expert technical support.
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