kuropsrrhoiq,ro. Vol. 27. No 4. pp. 485.493, Printed in Great Brtta~n.

VISUO-SPATIAL

1989.

c

PROCESSING

0(12X-393? x9 $3.00+ I1 00 19x9 Prrpmon Prers plc

IN PARKINSONIANS*

GEORGE E. STELMACH,JIM G. PHILLIPS and ALBERT W. CHAU Motor

Behavior

Laboratory,

2000 Observatory

Drive, University U.S.A.

(Rrceiued 2 February

of Wisconsin-Madison.

Madison,

WI 53706.

1988: uccepted 4 July 1988)

Abstract-It has been suggested that patients with Parkinson’s disease (PDs) may have problems processing visuo-spatial information and that this deficiency may contribute to the motor control problems observed in PD. However, most studies reporting visuo-spatial deficits are equivocal; they confound perceptual and motor processes. To address this issue. the present experiment systematically compared the relative contributions of several cognitive processes to performance: perception, stimulus-response translation, movement preparation and execution. Seven nondemented PDs and seven age-matched controls performed visual RT tasks, based upon judgements of spatial displacements. Both the RT and MT data suggested that PDs do not prepare movements as adequately as normals, and that PD deficits are associated with problems controlling movement execution. On the other hand, PDs were not slower in judging distances and linking perceptlon to action, suggesting that previous findings of visuo-spatial deficits may be due in part to motor impairments.

INTRODUCTION THE PRESENT experiment assessed factors that may contribute to movement problems observed in patients with Parkinson’s disease (PDs). It has been suggested that PDs are deficient in their ability to process visuo-spatial information and this deficiency contributes to their known problems of motor control. However, visuo-spatial ability tends to be inferred from patients’ motor performance during visuo-spatial tasks. A systematic assessment of the relative contributions ofperceptual and motor processes is necessary to establish whether the motor problems in PDs are indeed due to deficits in visuo-spatial processing abilities or due to other processes. Successful goal-oriented movements require accurate appreciation of the environmental constraints, and the location of goals in space. The ability to judge distances, angles, left from right, and other spatial relationships are therefore important for movement. Deficits in some form of visuo-spatial information processing could thus contribute to PDs’ defective motor control [8,12,20]. Indeed, while Parkinson’s disease (PD) has traditionally been linked with movement control problems, researchers have also associated it with deficits in higher cognitive processes [17, IS]. Moreover, some have suggested that Parkinson’s disease involves defective visuo-spatial processing [3, 12, 13, 16, 211. Table 1 summarizes a number of relevant studies which have examined defective spatial ability in PDs. Although some studies [3, 4, 12, 211 have found PDs had impaired spatial

* This work was supported

by grant NS17421

from the National 485

Institute

of Health

486

GEOKC;~ E. STELMA~H. Jlhl G.

PHILLIPS

and ALBIXT W. CHAI.

ability, these tasks contained a substantial motor component. for example route-walking [3], copying figures 1211, and pointing to body parts 141. In contrast, in tasks which have a minimal motor component, there is a disagreement among reported findings. For example, DELLA SALA rt ~1. [8] used non-speeded tasks with minimal movement to examine non-demented PDs’ ability to extrapolate and predict where one line would intersect with another. No difference was found between PDs and normal controls in their ability to predict where the two lines intersected, and it was suggested that, at least in the early stages of PD, there is no visuo-spatial deficit. Moreover, BROWN and MARSDEN [S] examined PDs’ ability to discriminate whether a target stimulus appeared to the left or right of a cue stimulus. They also considered whether the observed deficits in spatial ability were due to an inability of PDs to alter their spatial perspective, given that PDs have problems in shifting their cognitive and motor set 161. Although the PDs were found to be slower than controls, there was no evidence that PDs were differentially impaired in making left-right discriminations, or in shifting their spatial perspective. Performance is the end product of a number of cognitive-motor processes such as perception, response selection and response organization 1223. It is thus difficult to assess high level cognitive impairments in such a way that they are independent of associated motor deficits [ 151. Since cognitive abilities are inferred from speed and accuracy of responses, any slowness in movement can lead to the incorrect interpretation that there arc deficits in cognitive abilities. Experiments should thus assess how each process contributes to overall task performance. For example, experiments testing visuo-spatial abilities should minimize [ 131 or assess the effects of motor impairment [S, 111 before concluding that PDs have visuospatial deficits. While there are a variety of processes contributing to visuo-spatial judgements (e.g. left-right discrimination, mental rotations of spatial relationships, judgements of distance and angles), PDs’ ability to judge distances is of particular interest considering that Parkinsonian movements characteristically fall short of the intended target [ 141. Similarly, PDs’ ability to alter the relationships between stimulus and required response is of interest since PDs have problems shifting their cognitive set [6]. The present experiment therefore manipulated a number of cognitive-motor factors contributing to performance in a visuo-spatial task, to establish whether PDs are deficient in certain visuospatial processing abilities and whether such abilities could affect their movement problems. The relative contributions of perceptual processes, stimulus%response translation, movement preparation and movement execution were assessed in comparisons of tasks that systematically differed in difficulty. The subject was required to judge distances, relate these perceptions to action, as well as to prepare and execute movements. It was anticipated that PDs would have deficits in motor processes, rather than in visuo-spatial processing abilities.

METHOD Seven non-demented patients and seven aged-matched controls were tested. Patients were screened on the basis of their Mini-Mental-Status scores. All control subjects had no history of neurological disease. The mean age of the Parkinsonians was 69 (range 61 82) and the mean age of the control group was 70 (range from 66 to 80). Patient characteristics are shown ii Table 2

VISUO-SPATIAL

Table 1. Studies of visuospatial

Authors

Stern ef a/. (1984) Goldenberg et ul. (1986) Villardita et (I/. Boller et al. (1984)

function

in Parkinsonian

(I 982)

Brown and Marsden (1986) Della Sala et al. (1986) Goldenberg et al. (1986)

patients

Substantial motor components involved

Test

Bowen et al. (1972) Bowen et ul. (1976) Villardita et al. (1982) Boller ef al. (1984)

487

PROCESSING

Visuo-spatial abilities

Yes Yes Yes Yes Yes Yes Yes Yes

Impaired Impaired Impaired Impaired Impaired Impaired Impaired Impaired

WAIS figure assembly Visual perception tests Spatial orientation memory Benton visual retention Multiple choice Visual discrimination (Matching figures) Hooper visual organization Angle perception (Visuoperceptual part) Judgement of spatial relationship

Yes No No

Impaired Impaired Unimpaired

No

Unimpaired Impaired

Spatial forecast test Judgement of line orientation Ratcliffs mannekin test of mental

Route-walking Body schema Benton visual retention (copymg Purdue pegboard Benton visual retention (copying Angle perception Pattern tracing Assembly of geometric figures

figures) figures)

No

No

Unimpaired Unimpaired

No

Unimpaired

No No No

Unimpaired Impaired Unimpaired

No

rotation

Apparatus and task Two response keys were used in conjunction with the visual display terminal ofan IBM XT personal computer. In all tasks, subjects were required to respond to visual stimuli presented on the visual display terminal by pressing a response key. Each trial commenced with the presentation of both a visual fixation point in the center of the screen, and an auditory warning signal. This was followed by a randomized delay of 0.5, 1.0, or 1.5 set before the presentation of the stimulus to be judged. The stimuli consisted of two 1 x 1 cm squares, one on the left and one on the right of the terminal screen. For the experimental trials, either the left or right stimulus could deviate vertically from the horizontal mid-line (Fig. 1). The subject’s task was to judge on which side of the screen did the square show a vertical displacement from the screen’s mid-line. Responses were made upon the two response keys. After each trial, subjects were informed by the computer about the correctness of their response. Procedure PD subjects initially received a test of their visual simple reaction time. They were also given a bradykinesia test in which subjects tapped for 20 set with either their left or right hand between two targets separated by 6 cm. Three factors were systematically manipulated in the experiment. The first variable manipulated was perceptual judqemrnt dificulty. This was accomplished by varying the vertical distance a square could deviate from the horizontal mid-line of the screen. For the difficult condition, the distance between the center of the square and the mid-line ofthe screen was 3 cm; for the easy condition, it was 9 cm. Secondly, to assess subjects’ability to shift spatial perspective, the linkage between judged stimulus and required response was varied so that subjects performed under compatible and incompatible conditions. For the compatible condition subjects pressed the response key on the same body side as that of the square which deviated from the mid-line of the screen. For the incompatible condition, subjects responded with the response key on the opposite body side to that of the square that deviated from the midline. The third factor manipulated was response complexity. Subjects were required to respond to a judged stimulus with either one or two taps of the response key. Varying each level of the 2 x 2 x 2 Judgement Difficulty by Compatibility by Response Complexity design produced eight experimental tasks. The order ofpresentation of the experimental tasks were randomized for each subject. For each task, subjects received 12 practice trials and 24 experimental trials.

Age 68 61 69 82 66 62 72

Subject

WD

JP

WJ RS JH

BD RC

6 2 20 11 9 3 1

III III II III II I

Duration of disease (yr)

II

Hoehn and Yahr stage Sinemet Bromocriptine Sinemet Bromocriptine Sinemet Sinemet Sinemet Bromocriptine Sinemet Sinemet

subjects

Tremor Tremor Tremor, rigidity Tremor Tremor, rigidity

Rigidity, tremor Rigidity

Main symptom

of the Parkinsonian

Medication

Table 2. Characteristics

34 40 40 32 20 39 35

30 29 27 29 30 30

40 31

50 40 32

45

40

401 307

381 327 324

291

324

245 230

474 307 385

293

363

Simple Bradykinesia RT L R L R

30

Minimental status

VISUO-SPATIAL

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PROCESSING

Time COUi32 Display

I Fixation point and beep sound

FIG. 1. Warning

Delay of 0.5s. 1s or 1.5s

and response

Response Signal

signals sequence

for a trial.

RESULTS Reaction

times

Reaction time (RT) was defined as the interval from the appearance of the visual stimuli to the initiation of the tapping movement. Reaction times were submitted to a Group by Judgement Difficulty by Compatibility by Response Complexity ANOVA. It was found that responses were initiated faster in easy spatial judgements (904 msec) than in difficult spatial judgements (1091 msec) [F (1, 12) = 19.09, P < 0.051. The size of these RTs reflects the amount of complex cognitive processing required in these tasks. Further, the compatible conditions (883 msec) were easier than the incompatible conditions (1112 msec) [F (1, 12) = 34.62, P-c 0.051. There was no main effect of the number of taps [F (1, 12) = 2.54, P>O.O5]. These effects can be seen in Table 3 which shows the means and standard deviations of the RT data. There was a significant three-way interaction between Group, Compatibility and Response Complexity [F (1, 12) = 9.30, PC 0.051. Analysis of the simple main effects showed that PDs required more time to initiate two taps (960 msec) than the controls (858 msec) under the compatible condition (Fig. 2). Table 3. Reaction

Normals Parkinsonians

time means and SD for controls

and Parkinsonians

Condition

EC1

EC2

El1

E12

DC1

DC2

DIl

DI2

Mean SD Mean SD

704 165 776 182

743 168 857 233

965 294 1117 341

1036 296 1041 262

934 241 1016 259

972 254 IO64 254

1128 287 1172 257

1237 283 1204 252

Ahhruc ialions,for condition: The first letter denotes Judgement Difficulty (E for Easy, n for Difficult), the second letter is for compatibility (Cfor Compatible. lfor Incompatible); and the number at the third position represents the number of taps in the task.

The relative difficulty of each factor was assessed by comparisons of the additional processing time required for each manipulation of task difficulty. The effects of judgement difficulty were thus estimated by averaging the RT differences between difficult and easy tasks. The effects of stimulus-response translation were assessed by calculating the mean difference between incompatible tasks and compatible tasks; and, finally, an estimate of the effects of response complexity was obtained by taking the mean difference between two-tap tasks and one-tap tasks. As seen in Table 4, PDs required shorter additional processing time for all three manipulations. Moreover, the percentage contribution by each factor to the total additional processing time provides an indication of the relative difficulty of the

GEORW E. ST~LMACH, JIM G. PHILLIPS and ALBERT W. CHAI.

490

.

E

.P

z

x

cc

950 900

850

I

0-e

Normals,

I

A-A

Normals,

2 taps

c

M

PDS,

.

,m

PDs,

I

top

tap

2 taps

fi

.

Compatible

Incompatible

FK. 2.

manipulations to the subjects. As seen in Table 4, Compatibility was the most effective manipulation (the one which accounted for the highest percentage of the additional RT) for controls (49%) and Parkinsonian subjects (52%) respectively. For both groups performing a stimulus-response translation of the spatial concepts was the most difficult for PDs. Furthermore, the percentage additional time explained by increased response complexity was lower in the PD subjects, showing that PD subjects allocated proportionally less time to response preparation as the response complexity increased. Table 4. Reaction

Factor Normals Parkinsonians

Inter-tap

Mean (msec) % Mean (msec) %

time accounted

Judgement difficulty 205 39 167 42

for by each factor

Compatibility 253 39 205 52

Response complexity 64 12 21 6

Total 522 100 393 IO0

interval

The RT data suggested that the problem of PD does not lie in spatial judgement or mental manipulation of spatial concepts, and that PD patients spend proportionally less time preparing for a movement. This result is in keeping with the view that PD involves a shift from programmed to visually guided control ofmovement [9]. To assess the motor aspects of the task, the time for movement execution was analyzed. The time interval between the two tapping responses in the two-tap tasks (inter-tap interval), was examined. Table 5 shows the means and SD of the intertap interval. Parkinsonian patients (440 msec) were found to be significantly slower than the elderly (359 msec) [F(l, 12)= 5.49, PcO.051, as would be expected. Error

rates

Error rates were analyzed to see whether PDs were differentially affected by task difficulty. Four error types were defined and recorded during data acquisition. Reaction times shorter than 50 msec were considered anticipation errors. Pushing the wrong key was a decision

VISUO-SPATIAL

PROCESSING

Table 5. Mean and SD of intertap Condition Normals

intervals

EC2*

EI2

DC2

D12

373 35 441 97

368 55 428 90

343 61 431 84

352 47 462 75

Mean SD Mean SD

Parkinsonians

491

* Refer to Table 3 for abbreviations

error. An akinetic error was committed when the reaction time was longer than 2000 msec or the total time (reaction time plus inter-tap interval) was longer than 4000 msec. A movement error was defined as a wrong number of taps and/or pushing both keys. Rates and patterns for the four types of errors are shown in Table 6. Table 6. Error rates of normals and Parkinsonians the total number of trials)

Error type Anticipation Akinesic Movement Decision Total

Normals (%)

(in % of

Parkinsonians (%)

0.30 3.87 2.38 4.09

1.27 8.33 6.32 6.77

10.64

22.69

Overall error rates are analyzed in a Group by Judgement Difficulty by Compatibility by Response Complexity ANOVA. The error rates for the elderly controls and the PDs were 10.64 and 22.69% respectively, and this difference approached significance [F (1, 12) = 3.41, P-cO.091. Main effects for Task and Compatibility were significant. It was found that the error rate was larger for difficult tasks [F (1, 12) = 14.71, P< 0.051 (mean for difficult tasks=20.65%; mean for easy tasks= 10.68%) and incompatible tasks (mean for incompatible tasks=21.17%; mean for compatible tasks= 10.16%) [F(l, 12)= 19.84,

P-cO.051. From the above data, it can be seen that Parkinsonian patients tended to make more errors of all types. Akinetic and movement errors were the main source of differences; again, this suggests that PDs’ have difficulty with the motor components of the task.

DISCUSSION It had been suggested that motor control problems in PD patients could be due to deficits in the processing of visuo-spatial information. To examine this hypothesis, the present experiment assessed the relative contributions of perception, stimulus-response translation, movement preparation and movement execution to PDs’ performance in a visuo-spatial judgement task. Taken together, the results of RT and error rates do not support the hypothesis that patients with Parkinson’s disease have deficits in judging distances and in mentally linking these perceptions to action. In contrast, the inter-tap interval showed that the observed slowing of performance was localized in movement execution processes.

492

GEORGEE. STELMACH, JIM G. PHILLIPSand ALHEKTW. CHAI:

Previous studies which have used experimental tasks in which motor components were minimized have concluded that PDs are unimpaired in their visuo-spatial function [S, 81. The present experiment elaborated on them, by systematically examining contributions of different factors. Both groups required the same relative amount of time to perceive a small difference in the spatial displacement of two visual stimuli. This suggests that PDs are not impaired in their appreciation of the relative positions of stimulus objects in the visual space. In the manipulation of stimulussresponse translations, the subject had to relate a particular perception to a particular response. PDs, compared to normal controls, were not impaired in performing stimulus-response translations. However, as this manipulation constituted the largest portion of the additional reaction time in PDs, it suggests that this processing component is the most difficult one during PDs’ preparation for movements. Indeed, some experiments have suggested that PDs have a diminished ability to reorganize their behavior in accordance with task requirements [6]. While the present experiment found no differences between normal and PD subjects in the visuo-spatial processes examined (distance judgements), the data suggested that the observed deficits in PDs’ performance in visuo-spatial tasks could be due to motor processes. Our data provide evidence that PDs have problems in movement preparation and execution. The literature has suggested that PDs alter their movement strategy such that PDs shift from open loop control to closed loop control [9, IO]; that is, PDs control movements during execution rather than preparing them in advance. In keeping with these suggestions, PDs showed smaller proportional increases in RT when they were supposed to be preparing more complex movements, and they took longer in executing their movements. This suggests that PDs did not prepare the whole movement sequence in advance. PDs probably initiated the first tap producing a direct response to the stimulus in any condition, while the subsequent tap would be prepared during the execution of the first tap, producing a longer inter-tap interval. Indeed, STELMACH et al. [ 191 also found evidence that PDs only prepare the early components of the movement, the subsequent movements being controlled through ongoing monitoring of the movements as they are actually produced. This finding does not necessarily mean that PDs cannot prepare their movements. Indeed, our data suggest that there is a partial switch from open loop control to closed control: advance programming as well as ongoing monitoring are used by PDs to control more complicated movements. One possible reason for the compatible condition being the only condition in which the effect of response complexity was manifested is its relatively low demand in processing. There was a direct association between the stimulus and the response. The subject was thus given a chance to devote some of his resources to movement preparation. Under such a condition, the PD subjects did program both taps and showed a ionger response latency than the controls. This data is in keeping with studies examining predictive control in PDs [l, 71. When the findings of the present experiment arc compared to those studies which did not minimize movement, there is a disagreement in the findings. Studies not minimizing movement found impairments in visuospatial function in PDs. The discrepancy can be explained by the nature of the tests used. To study visuospatial function, one must eliminate or control the contribution of the motor components as well as other cognitive processes like memory and cognitive set. Previously used tests like route walking 131, copying figures [21] involve substantial motor components. Other tests like body schema test 147 and spatial orientation memory test [Z] involve additional factors like cognitive set and memory. It is difficult to disentangle the effect of such factors in these studies and the present study shows

VISUO-SPATIALPROCESSING

493

that some of the reported

deficits in PDs’ performance in visuo-spatial tasks may be due, not to deficits in visuo-spatial abilities, but may be due to deficits in cognitive-motor processes which are not in themselves visuospatial functions: movement preparation and execution.

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