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Neuropsychologia, Vol. 36, No. I, pp.

109-114, 1998
~/ 1998 Elsevier Science Ltd. All rights reserved
~ Pergamon PII: S0028 3932(97)00017-1 Printed in Great Britain
0028 3932/98 $19.00+0.00

Impairments of mental rotation in Parkinson's


disease
A. C. LEE,*t J. P. HARRIS* and J. E. CALVERT~

*Department of Psychology, University of Reading, Whiteknights, Reading RG6 6AL, U.K.;


SDepartment of Psychology, University of Bristol, 8 Woodland Road, Bristol BS8 ITN, U.K.

(Received 17 June 1996; accepted 7 January 1997)

Abstract--It is controversial whether parkinsonian patients are impaired on visuospatial tasks. In the present study, patients and
normal control subjects judged whether pairs of wire-frame figures in different orientations were the same or different. The orientation
difference between the figures was either in the picture plane (around the z-axis, or two-dimensional) or in depth (around the y-axis,
or three-dimensional). Reaction times and error rates were measured. For the two-dimensional task, there were no significant
differences in errors between the two groups, though Parkinsonian subjects were significantly slower to respond than the control
group. In the three-dimensional task, patients had a different pattern of reaction times from the controls and made significantly
more errors, which were systematic at large angular differences. The results suggest a visuospatial deficit in Parkinson's disease,
which reflects problems in some aspect of the perception of extra-personal space. © 1998 Elsevier Science Ltd. All rights reserved

Key Words: visuospatial tasks; object-centred processing; image-centred processing; extra-personal space.

Introduction was on their left or right. When the arrow pointed up, no
mental reorientation was required; when it was hori-
One of the more controversial questions about possible zontal, re-orientation through 90 ° was required; when it
cognitive changes in Parkinson's disease (PD) has been pointed down, re-orientation through 180 ° was required.
whether or not there is impairment of visuospatial pro- PD subjects, although slower than controls in all
cessing in the illness. Early studies have generally con- conditions, were not differentially worse in the conditions
cluded that there is evidence for such a deficit. For that required greater amounts of re-orientation. Brown
example, patients are impaired on visuospatial subtests and Marsden concluded that these results did not provide
of the WAIS [7] and in route-finding tasks [3]. However, evidence for an impairment of mental manipulation and
there are several problems with such studies [4, 5]. If the so for a general visuospatial deficit in the illness.
dependent variable is time, patients will be at a dis- However, it can be argued that this task is not a strong
advantage because of the accepted effects of the illness on test of mental manipulation, for two reasons. First, it
the motor system. Again, many tests require a sequence of requires the subject to change the relationship between
operations, and it may be in the organization or execution themselves and the stimulus, rather than the relationship
of such a sequence that the patients' difficulties lie, rather between two stimuli. The latter may put greater demands
than in visuospatial processing per se. on visuospatial mechanisms. Secondly, and perhaps more
In Brown and Marsden's study [4], a mental rotation importantly, even if the subjects were mentally man-
task [11] was employed. A Maltese cross was presented ipulating the stimulus as Brown and Marsden suggest,
on a computer screen, with an arrow in one arm and a this could be done as a two-dimensional rotation of
dot in one of the adjacent arms. The subjects' task was an image-based representation, rather than a three-
to align themselves mentally with the arrow, and to press dimensional rotation of an object-based representation.
one of two push-buttons, depending on whether the dot Other studies (e.g., [8]) have used other tasks to explore
the ability of the parkinsonian to mentally manipulate
objects in three dimensions. Ogden and co-workers used
t Address for correspondence: Department of Psychology,
University of Reading, Whiteknights, Reading RG6 6AL, a subsection of the Differential Aptitude Tests [1], in
U.K.; e-mail: a.c.lee@reading.ac.uk; tel: + 1189 318522; fax: which the subject was shown a drawing of a two-dimen-
+ 1189 316604. sional shape and was asked to decide which of four pic-

109
110 A.C. Lee et al./Mental rotation in Parkinson's disease

tures of various three-dimensional shapes represented the by Brown and Marsden, whereas, in the other, rotation
target shape if it were to be folded along specific lines. The in depth (around the y-axis) is required.
authors suggest that this task requires quite sophisticated
visuospatial abilities, as the subject has to both form and
manipulate mental images, without having to sequence Method
behaviour. Although the patient group were significantly
slower than the controls, both groups made a similar Stimufi
amount of errors (between 33% and 35%). Ogden et al.
concluded that performance on this task demonstrated Images based upon the Shepard and Metzler [12] figures
that the patients did not have a visuospatial deficit. How- were used. Eight perspective line drawings of unfamiliar three-
ever, it could be argued that the task can be done in an dimensional figures were used (see Fig. 1). Each figure com-
prised 10 individual wire-frame cubes laid end-to-end.
image-centred way, using local two-dimensional rather
After the third, the fifth and the eighth blocks, the next cube
than global three-dimensional information. For example, was attached to one of the sides, rather than to the end, of the
if the local two-dimensional shape defined by the specified last cube, thus creating a 90 ° angle in the figure. The shapes
line and the edges of the paper were a triangle, this would were chosen for their ability to be rotated around the y-axis,
immediately rule out a cube as a possible candidate three- without one part of the figure occluding most of another part.
Thus, whatever the viewpoint, most of the figure was always in
dimensional shape. Given the high error rates in the task,
view. The stimuli were presented in pairs, one on each side of a
in both patients and controls, such a strategy seems to computer monitor screen, in a range of orientations. Examples
give a possible account of the data. of the stimuli are shown in Fig. 1.
In this paper, we compare performance on two tasks
involving the kind of wire-frame figures introduced by
Shepard and Metzler [12]. Both tasks involve same/ Apparatus
different judgements of two such figures which vary in
orientation. Thus, subjects cannot perform the task by The test stimuli were generated by a Pluto 11 graphics system,
mentally re-orientating themselves with respect to one or (spatial resolution 768H x 288V pixels), and displayed on a
Digivision CD 14 RGB monitor. The stimuli were white against
both stimuli, but must re-orientate one stimulus with a black background. The Pluto was programmed by an IBM
respect to the other. In one experiment, the task involves PC AT clone, to which two response buttons were connected
rotation in the picture plane (around the z-axis), as used via an I/O card.

i
Fig. 1. Examples of stimuli shown at 20 ° separations.
A. C. Lee et al./Mental rotation in Parkinson's disease 111

Procedure that reaction times (RTs) increase with angular discrep-


ancy. Figure 2 shows that such a trend was generally
E x p e r i m e n t I: t h r e e - d i m e n s i o n a l r o t a t i o n . The subjects were
found in the present data when the figures were the same,
seated 1 m from the screen so that the display subtended a
horizontal visual angle of 10°. They were shown a dem- both for patients and controls, though the control data
onstration of the principles of mental rotation, using models. are the m o r e variable, once the angular difference exceeds
Then the subjects were shown examples of the stimuli on the 140 r~. The graph of the RTs of parkinsonian subjects has
screen. In this experiment, one of the figures was rotated with an apparently shallower slope for the 'same' stimuli than
respect to the other (by a variable amount) around the y-axis. that of the controls, though this difference was not sig-
Subjects were told that they had to decide if the figure on the
right was the same in shape (but globally rotated) as the figure nificant because o f the scatter in the data at the higher
on the left. They were to press either of two buttons ('same' or angular discrepancies (t--0.03; P > 0 . 0 5 ) . The slopes of
'different') to indicate their choice. The figures would remain the graphs of RTs for the 'different' stimuli are very
on screen until their decision was made, so there were no time shallow, though slightly steeper for patients than
limits. They were to signal that they were ready for the next controls.
trial by pressing one of the response buttons, when the next
stimulus would appear on screen. RTs to respond to the same images were significantly
Each subject was given a practice session of 15 trials, to slower [F(1,12) = 35.18; P = 0.0001] than those to different
familiarize them with the task and the response box. In the images. This m a y reflect a difference in the way that the
experimental sessions, there were 80 trials. On 50% of them, two tasks can be solved. It can be obvious, on 'different'
the figures were the same, and on 50% they were different. trials, that the stimuli are different, from a c o m p a r i s o n
It was stressed to the subjects that they should try to be as
accurate, rather than as fast, as possible. Testing occurred of individual limbs of the figures, which can occur early
30 min after the PD subjects had taken a therapeutic dose of in the presentation. However, if no incongruent limb is
L-DOPA. immediately apparent, as on the ~same' trials, the subject
E x p e r i m e n t 2." t w o - d i m e n s i o n a l r o t a t i o n . The procedure of must continue the rotation of the images before being
this experiment was identical to that of Experiment 1, except sure that the figures are indeed the same. It appears that
that the demonstration and explanation of the principles of
mental rotation referred to two, rather than three, dimensions. the control group did indeed use this strategy, but the
That is, rotation was around the z-axis (in the plane of the PD group did not. Instead, they responded m o r e quickly
screen). than the controls, but at the cost of systematic errors (see
below).
Overall, there was no significant difference in the reac-
Subjects. tion times of the two subject groups [F(1,12)=0.07;
P > 0 . 7 ] , because of an interaction between group and
Parkinsonian subjects. Experiment l: three-dimensional image type. Thus, for the 'same' stimuli, the P D group
rotation. Seven volunteer patients (six male, one female), were faster (for most angular differences) but for 'differ-
diagnosed by a consultant neurologist as having idiopathic PD,
ent' stimuli they were slower than the control group.
were recruited from the regional Parkinson's Disease Society
[mean age 66.6 years (S.D. 5.4years), L-DOPA daily 878.3 mg Although this interaction just missed significance
(S.D. 357.8 mg)]. These patients were selected because they all [F(1,12) = 4.14; P = 0.06], analysis of the simple effects in
had little or no akinesia in their dominant hand after medi- the interaction showed that they were all significant at
cation, which might have affected their ability to use the the 2 % level at least, except for the difference between
response box. Subjects scored between Stages II and III on the
the P D and control group R T s for the 'same' images.
Hoehn and Yahr scale.
Experiment 2: two-dimensional rotation. Two of the patients Errors. Figure 3 shows the mean percentage error
who took part in Experiment 1 were unavailable for this experi- scores for P D subjects and controls. As the angular
ment. Testing of the remaining five subjects ensured that medi-
cation, duration of illness and symptoms were similar in the
two experiments. SAME
Controlsubjects. Experiment 1: three-dimensional rotation.
Seven age- and sex-matched control subjects (six male, one
female) were used [mean age 63.6 years (S.D. 4.6 years)].
Experiment 2: two-dimensional rotation. The same five con-
24 [--
22 f
2018 _•PD PD DIFF
CO SAME
CO DIFF , , ,~t/"
/~
XX A

trols who had been matched to these PD subjects in Experiment


1 were used.

Results bl , ~ U].. . "53 412. . . . [5- " - - "C3- " - "~


41 . . . . [ 2 , . . _ . q D - - " ----E-'--"
2~ ~ o ~ & ~ o
Experiment l: three-dimensional rotation I I 1 [ I t I I I
20 40 60 80 100 120 140 160 180
ANGULAR DISCREPANCY
Reaction t i m e s . The three-way analysis of variance (in degrees)
( A N O V A ) showed a highly significant main effect of Fig. 2. Mean reaction times for judgements of the same and
angular discrepancy [F(9,108)=7.82; P < 0 . 0 0 0 1 ] , as different pairs of images for parkinsonian and control subjects
expected f r o m the finding of Shepard and C o o p e r [11] in Experiment 1.
112 A.C. Lee et al./Mental rotation in Parkinson's disease

PD SAME 14 "-0-" PD SAME


100 - ,--c]-- PD DIFF - C ~ PD DIFF i
90 - ~ CO SAME
12 .
CO SAME
_ Q _ ~
/\
•-O-- CO DIFF A
80
70- 10
~. 60
s
50
~ 40
30
4[
20

2~_

0 20 40 60 80 100 120 140 160 180


o I 1 I I r J I I I
ANGULAR DISCREPANCY 20 40 60 80 100 120 140 t 60 180
(in degrees) ANGULAR DISCREPANCY
Fig. 3. Mean percentage errors for judgements on the same and (in degrees)
different pairs of images for parkinsonian and control subjects Fig. 4. Mean reaction times for judgements on the same and
in Experiment 1. different pairs of images for parkinsonian and control subjects
in Experiment 2.

difference between the stimuli was increased, PD patients


became relatively less accurate compared to controls. The
heavy black line indicates the level at which the subjects although the slopes of the graphs for the control group
would be performing if they were responding at chance. are much flatter.
As Fig. 3 shows, the PD subjects performed at worse than It can be seen that the pattern of results is quite differ-
chance on the 'same' stimuli once the angular discrepancy ent from that found in Experiment 1, as both patients
exceeded about 140 ° . and controls show similar reaction times to the 'same'
Analysis of variance of the data shows a significant and 'different' stimuli. The PD group are always at least
main effect of angular discrepancy [F(9,108)=10.27; 2 sec slower than the control group, a difference which
P < 0.00001] and for whether the figures were the 'same' was significant [from the ANOVA F(1,8)=10.86;
or 'different' [F(1,12)= 10.44; P = 0.007]. There is also a P < 0.02], but performed faster than they did in Experi-
highly significant interaction between angular dis- ment 1. The group × angles interaction is also highly sig-
crepancy and image type [F(9,108) = 5.32; P < 0.00001 ]. nificant [F(9,72)= 3.28; P = 0.02], reflecting the fact that
Overall, there was a significant difference in the error the difference between the two groups gets larger with
rates of the two subject groups [F(1,12) = 6.74; P < 0.02], increasing angular discrepancy.
with the patients making more errors. There were also The differences in response times within both groups
significant interactions which can be best understood by of subjects for the 'same' and 'different' images are less
analysis of the underlying simple effects. The PD group apparent in this experiment than in Experiment 1, and
made significantly more errors than the controls for the neither reached significance at the 5% level.
'same' images (at the 2% level), but not for the 'different' Errors.. The mean percentage errors are plotted in Fig.
images. In addition, the patients had significantly higher 5. There is a large difference between the pattern of errors
error rates (at the 0.5% level) in recognizing the 'same' found in Experiment 1 and that in this experiment. There
images than the 'different' images, whereas the control is a ceiling effect for smaller angular discrepancies, with
group had similar error rates for both types of stimulus. both the PD and control subjects making no or very few
For the last three angles of the sequence (140 °, 160 °, errors. Even at large angular discrepancies, the mean
180°), it can be seen that the parkinsonian subjects are percentage of errors did not exceed 15 %. Non-parametric
performing worse than would be expected if they were analysis using the Friedman test (the data were not con-
responding randomly, i.e. at chance. This suggests that sidered suitable for analysis with ANOVA because of a
the patients were making systematic errors, perhaps lack of homogeneity) showed no significant differences
through the use of an inappropriate strategy. between the groups at any angular discrepancy for both
targets and distracters.
The graphs show that the number of errors made by
Experiment 2: two-dimensional rotation both groups increases with angular discrepancy, but not
as steeply as in Experiment 1. Above about 140 ° angular
Reaction times.. Figure 4 shows the mean RTs for the discrepancy, the error rates for the PD group are slightly
PD and control groups in Experiment 2. The charac- higher than those for the control group. However, the
teristic increase in the time taken to respond with angular PD group shows no signs of the systematic errors at large
discrepancy is still apparent for both subject groups, angular discrepancies found in the first experiment.
A. C. Lee et al./Mental rotation in Parkinson's disease 113

discrepancies in three-dimensional rotation, on the other


PDDIFF [ hand, strongly suggest that there is a qualitative, not
CO SAME simply a quantitative, difference between patients and
CO DIFF
controls on this task. This finding suggests a positive
answer to the question (answered negatively by Brown
~- 15 1 and Marsden [4]) of the existence of a visuospatial impair-
ment in PD. The discrepancy between Brown and
~ 10 Marsden's finding that there was no differential slowing
with increased angular difference in a two-dimensional
rotation task and the present data could have arisen
5 because the tasks were subtly different. Our task required
subjects to rotate one stimulus with respect to another,
whereas that of Brown and Marsden required rotation
of the stimulus with respect to the subject. The latter task
20 40 60 80 100 120 140 160 180 may not allow any visuospatial impairment to become
ANGULAR DISCREPANCY apparent.
(in degrees)
The nature of the patients' visuospatial problems is
Fig. 5. Mean percentage errors for judgements on the same and
different pairs of images for parkinsonian and control subjects less clear. One relevant piece of evidence comes from the
in Experiment 2. systematic errors made at large angular discrepancies in
the three-dimensional task. These errors imply that stim-
uli which were in fact the same but rotated close to 180°
Discussion with respect to each other were judged to be different.
One possible explanation for this effect is that patients
The results of these experiments may be summarized relied too heavily on local instead of global matching.
as follows. In two-dimensional mental rotation of one For example, they could select, say, the lowest vertical
wire-frame stimulus with respect to another, the patterns segment of the figures (note that this was in the same
of response times and errors are similar in parkinsonian orientation in both figures), then compare the orien-
and in control subjects. The error rates are similar in both tations of the angles between those segments and the
groups, and, though slower, the PD response times show adjoining segments. For rotations close to 180"~,the orien-
similar increases with angular discrepancy to those of the tations of the segments would be similar, but the upper
controls. In three-dimensional mental rotation, on the segments would be pointing in opposite directions in the
other hand, though the response times show similar pat- two figures. This would be taken (incorrectly) by the
terns in both groups, there are large differences in error patients as evidence for a difference, whereas the controls,
rates. In particular, at large angular discrepancies, pat- who (we assume) would perform the task with a more
ients perform worse than chance, suggesting that their global comparison, would make less errors of this kind.
errors are systematic. The results suggest that the patients This notion of local processing could also be an expla-
may be performing the two-dimensional rotation task in nation for the results of Ogden et al. [8] on a mental paper
a similar way to the controls, even though their responses folding task [1]. For example, a subject may make one
are slower, but that for three-dimensional rotation, at fold along a specified line, and on this basis may be able
large angular discrepancies, patients are using a different to eliminate some of the four response options.
strategy to that of the controls. Visuospatial functions can be evaluated by tasks that
The findings raise a number of issues: involve three components: the understanding of relative
positions of stimulus objects in space; the integration
1. What light do the findings throw on the nature of
of the stimuli into a simple spatial framework; and the
visuospatial processing in PD?
performance of mental tasks involving that spatial frame-
2. What is the strategy used by the patients in the three-
work, (e.g., [2]). Many parkinsonian patients report that
dimensional task?
they experience a sense of constriction of visual space. In
3. How do the findings relate to broader PD symp-
Sacks' [10] evocative words: "what we observe, however,
tomatology?
is that all his space-time judgements are pushed out of
On the first issue, the patients are clearly worse than shape, that his entire co-ordinate system is subject to
controls on two-dimensional mental rotation as indicated expansions, contractions, torsions and warps...". Ano-
by the significantly higher intercepts and steeper slope ther of Sacks' parkinsonian patients suffered with a deficit
RT functions, and slightly worse in terms of error rates. in proprioception which made him unaware that he
However, it could be argued that this is not strong evi- walked with a 10Utilt [9]. This observation is in line with
dence for a major visuospatial impairment in the illness, the results of laboratory studies showing that patients
but rather for a slowing of visuospatial processing which may mis-perceive visual vertical and/or horizontal [6]. In
is comparable to the slowing of other cognitive processes a very different letter cancellation task, Villardita et
in the illness. The PD error data from the large angular al. [13] demonstrated peripheral visual neglect in the
114 A.C. Lee et al./Mental rotation in Parkinson's disease

disease, another result consistent with a constriction mined by a route walking test. Neuropsychologia 10,
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1986.
We suggest that it is this global distortion of their 5. Brown, R. G. and Marsden, C. D. Cognitive function
spatial frame of reference which affects three-dimensional in Parkinson's disease: from description to theory.
mental rotation in PD. The local feature-matching strat- Trends in Neuroscience 131, 21-29, 1990.
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three-dimensional, rotation tasks. insonism. Neurology 25, 43-47, 1975.
7. Loranger, A. W., Goodell, H., McDowell, F. H.,
Lee, J. E. and Sweet, R. D. Intellectual impairment
in Parkinson's syndrome. Brain 95, 405-412, 1972.
Acknowledgements--This work was supported by an MRC 8. Ogden, J. A., Growden, J. H. and Corkin, S. Deficits
studentship (A.C.L.) and grants from the Parkinson's Disease on visuospatial tests involving forward planning in
Society (J.P.H.) and the Lord Dowding Fund (J.E.C.). We high-functioning parkinsonians. Neuropsychiatry,
thank Dr Gavin Brelstaff for help with programming. Neuropsycholoyy and Behavioural Neurology 3, 125-
139, 1990.
9. Sacks, O., The Man Who Mistook His Wife For A
Hat. Pan, London, 1985.
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