Journal of Neurology, Neurosurgery, and Psychiatry 1983 ;46:145-151

Perceptual motor dysfunction in Parkinson's disease:a deficit in sequential and predictive voluntarymovement

YAAKOV STERN,*t RICHARD MAYEUX,t JEFFREY ROSEN,* JOYCE ILSONt

From the Departments of Psychology, City University of New York* and Neurology, Columbia UniversityCollege ofPhysicians and Surgeons, t New York, USA

SUMMARY We studied the ability of Parkinsonian patients and controls to generate voluntarymovements on a tracing task. Subjects were videotaped while tracing designs of increasingcomplexity, presented on a vertical, transparent screen. Some designs were presented in adegraded form and subjects filled in their missing sections. Subjects also received a constructionaltask and a test of general intellectual ability. The quality of errors on the tracing task differed in theParkinsonian and control groups. Parkinsonian patients made two distinct types of errors. Oneprobably related to the motor disorders of the disease, but another seemed to be related to a higherlevel of control over sequential and predictive movements. The latter correlated with performanceon the constructional and general intellectual tasks. These results suggest that Parkinson's diseasemay affect basal ganglia structures that are necessary for voluntary movements which requiresequencing or planning. Clinically this may be observed in perceptual motor tasks since theyrequire both voluntary movement and sequential organisation of behaviour.

Impairments in perceptual motor or visuospatialtasks are among the most frequently encounteredabnormalities in neuropsychological studies ofParkinson's disease.5 Many of these tasks requirevoluntary movements, so these deficits could reflectnothing more than the disordered movement ofParkinson's disease. Alternatively, this disturbancein perceptual motor tasks suggests that there mayalso be a loss of higher order motor control that isdistinct from the characteristic motor disorders ofParkinson's disease. Certain deficits on trackingtasks in Parkinson's disease can be characterised asan inability to generate and sequence predictivemovements, that is movements that must be accom-plished without external feedback to guide them. Forexample, Flowers6 demonstrated that while Park-insonian patients could successfully track a targetmoving on an oscilloscope screen in a regular patternat a sufficiently slow speed, tracking performancedegenerated when the target was momentarily re-moved from the screen. This perceptual motor deficit

Address for reprint requests: Dr Mayeux, The NeurologicalInstitute, 710 West 168th Street, New York, New York 10032, USA.

Received 8 April 1982 and in revised form 27 September 1982Accepted 4 October 1982

may be a result of impaired generation of control ofsequential and predictive voluntary movements.To examine this hypothesis, we tested patients

with a simplified version of Flowers' tracking task,6and with a constructional task. In addition, generalintellectual function and the severity of symptomswere assessed. We expected that certain errors intracing would relate to the severity of patients'Parkinsonism, that is tremor, rigidity orbradykinesia. However, we anticipated that othererrors in tracing, particularly those demandingpredictive movement, might be related to perfor-mance on the constructional and general intelligencetests and not to the severity of the Parkinsonism. Thiswork was presented in part at the 33rd annualmeeting of the American Academy of Neurology.'

Methods

SubjectsEighteen patients with Parkinson's disease and 14 healthy,elderly adult controls volunteered and gave informedconsent. We excluded people with a history or overt signs ofdementia as defined by the DSM 111.8 Fourteen of the 18patients were on levodopa therapy (table 1). All subjectswere examined by the same neurologist. For the patients,we used a standardised evaluation form rating 21 signs and

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Table 1 Subjects: descriptive information. Values inparentheses are standard deviations

Parkinson's disease Control

N 18 14Age 62-3 (12-8) 72-0 (38)Education (years) 13.0 (4-5) 9-7 (26)Mini-Mental State 51-3 (6.6) 50-3 (4.6)Parkinson's disease

evaluationTotal 28-8 (12-8)Tremor 18 (24)Bradykinesia 1-5 (0.9)Rigidity 4-6 (2-7)

Duration of illness 9-6 (82)N on levodopa (Sinemet) 14Levodopa dosage 1-4 gms/day

1

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4

5 A - w

6

/77

3.

Fig 1 Paths used in tracing task.

symptoms of Parkinson's disease from 0-4 (0 indicating theabsence and 4 indicating the highest severity); higher totalParkinson's disease evaluation scores indicated higherParkinson's disease severity. Rigidity and tremor ratingswere the sum of ratings of each of the four limbs and theneck or head. Controls were examined to ensure theabsence of any neurological disorder.

Neuropsychological testingWe used a brief but thorough measure of intellectualfunction, a modified version of Mini-Mental State examina-tion (MMS).9 Previously, we have found this measure to bea useful indication of intellectual function in Parkinson'sdisease.5 The maximum possible score on the modifiedMMS is 57. In addition, all subjects completed the RosenDrawing Test;10 the subject copied 15 designs ranging incomplexity from those testing simple concepts of topologi-cal space to 3-dimensional figures.

Tracing taskPaths drawn in black ink (approximately 6 mm thick) onclear plastic sheets were affixed to a 60 x 60 cm plexiglassscreen mounted perpendicular to a table (fig 1). Basic pathsconsisted of a straight line in horizontal and verticalorientation and a saw-tooth pattern. Further paths wereconstructed by deleting segments of the original ones; twoendpoints represented the straight line and the sawtoothpattern was modified by the removal of a straight linesegment, or one or two angular segments. Subjects tracedthe mounted paths with their index finger and a felt padreduced friction between the finger and plexiglass. Tracingperformance was recorded using a video camera mountedon the other side of the plexiglass screen. Subjects sat at theedge of a table within comfortable reach of the tracingscreen. Paths were administered in the sequence shown infig 1. Subjects were instructed to trace each path with theirindex finger, moving at their own pace. At the end of eachpath they turned and continued tracing for a total of threetimes back and forth. Subjects were cautioned to stay on thepath. Left hand performance followed right. For thepartially deleted paths (Paths 3, and 5-7), there wereadditional instructions. For Path 3, subjects were instructedto move between the endpoints in a straight line. Beforetracing Paths 5, 6 and 7, Path 4 was superimposed todemonstrate that the current path was similar but that a

segment had been deleted. Subjects were permitted tocompare the two paths until they were satisfied that theycould perceive the shape of the missing segment. They thentraced the partially deleted path, filling in the missingsegment. Path 4 was removed during tracing. When severeerrors occurred on Path 7 (according to the criteriadescribed below), Path 4 was redisplayed, subjects werepermitted to study the missing segment and trace it withtheir finger, and Path 7 was then readministered.

Rating. Videotaped tracing performance was rated by twoneurologists who did not know the results ofneuropsychological testing. In pilot work, we identified fourtypes of errors in Parkinson's disease patient tracingperformance. These errors were rated from 0 to 2 with 0indicating absence of error, 1, slight error and 2, severeerror: (1) loss-of-form: distortion of missing segments.Displacement of the relative position of portions of thepattern or the rounding of angles was related as a slight error(rating = 1). Grosser distortions were rated as severe(rating = 2) (see fig 2). (2) tracing error: slight (rating = 1)or severe (rating = 2) deviation from the displayed portions

a b4

5

6

7

,II

/'I/1 )," I,',

7" '

Fig 2 Selected examples ofslight (a) and severe (b) loss-of-form errors on paths 5-7. Path 4 is included forcomparison.

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of the path. (3) tracing hesitation: a one (rating = 1) or two(rating = 2) second hesitation during tracing but not at anend point. (4) endpoint hesitation: hesitation at endpointsscored as in tracing hesitation. Before rating subjects'performance, the raters reviewed tapes to establish concor-dance on rating criteria. During rating, any disagreementwas settled by reviewing taped performance until concensuswas reached. Tracing and hesitation errors were scored eachtime they occurred and were summed for each cycle ofmovement from the starting point of a path back to thestarting point. Loss of form errors could occur only twice ineach cycle.

Results

Parkinsonian patients were comparable in age,intellectual evaluation scores, and disease severity tothose we have studied previously (table 1).1 Controlswere significantly older and less educated than ourParkinsonian patients (p = 0-05; table 1). For controland Parkinson's disease groups respectively, meanMMS scores were 50-2 (SD = 4.6) and 51-2 (SD =

6.6) and Rosen Drawing test scores were 10-3 (SD =

2-2) and 10-9 (SD = 2-7). No significant differenceexisted between groups on these measures.No difference was found between performance on

successive tracing cycles of a particular path orbetween left and right hand. Therefore ratings foreach type of error were summed across thesedimensions for each path.

Loss-of-form-errors. The frequency and severity ofloss-of-form errors, as well as the qualitativecharacteristics of errors differed in the Parkinson'sdisease and control groups. In the Parkinson'sdisease group, loss-of-form errors occurred in allpaths with increased frequency and severity of errorsin Paths 6 and 7 (table 2). Patients often made errorsconsisting of the displacement of the relative positionof missing segments or distortion and rounding off ofangles (see fig 2). In Path 7, only one of the patientsexpressed an awareness of making an error and onlyone of the four patients who made severe errors on

Table 2 Loss-of-form errors. Number ofsubjects makingloss ofform errors on each path and median severity oferrorfor these subjects

Path Parkinson's disease Control(N= 18) (N= 14)

No Median No Medianseverity severity

3 4 2 0 -

5 4 1 0 -

6 10 2 2 *

7 15 4 7 *

* See text for explanation of missing values.

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Path 7 improved after redemonstration. In somecases several redemonstrations were added with noimprovement noted. Loss-of-form errors in theParkinson's disease group did not correlate with anyfacet of the symptom severity rating. Only twocontrol subjects made loss-of-form errors prior toPath 7 (one slight and one severe error on Path 6). OnPath 7, seven of the control subjects did not initiallyreproduce the missing segment. Ratings for thecontrols' performance are not included in table 2because, rather than making errors, controls oftenrefused to attempt performance prior toredemonstration of Path 4. While this would be ratedas maximal error in our rating system, it would not betruly descriptive of the controls' performance. Six ofthe seven controls were aware of their inability tocomplete the missing segment; redemonstration ofPath 4 led to improvement in performance of five ofthe control subjects.

Tracing errors. In the Parkinson's disease group, tensubjects made tracing errors on at least one designand five made severe errors (table 3). It was notpossible to relate tracing error ratings to specific signsof Parkinson's disease. Tracing error was also notrelated to the complexity of the paths, occurring withcomparable frequency in each. No correlation wasfound with any cognitive measure. In the controlgroup, tracing errors were infrequent and of slightseverity (table 3). For Path 7, control's tracing errorratings are taken from the first attempt they made attracing the path. In some cases, this occurred afterredemonstration of Path 4.

Hesitation errors. In the Parkinson's disease group,hesitation errors occurred in the tracing of all paths(table 4), but were not related to severity ofParkinson's disease, the complexity of the paths, orto any of the cognitive measures. In the controlgroup, hesitation errors occurred only in degradedpaths (table 4). These were typically pauses duringwhich the subject attempted to determine the

Table 3 Tracing errors: number ofsubjects making tracingerrors on each path and median error severityfor thosesubjects

Path Parkinson's disease Control(N = 18) (N = 14)No Median No Median

severity severity

1 6 1 0 -2 4 2 2 1-54 5 3 0 -5 6 2 0 -6 3 4 0 -7 4 3 1 1

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Table 4 Hesitation errors. Number ofsubjects making hesitation errors on each form and median error for these subjects

Form Endpoint hesitation Tracking hesitation

Parkinson's disease Control Parkinson's disease Control

No Median No Median No Median No Medianseverity severity severity severity

1 4 4 0 - 4 1 0 -2 3 2 0 - 5 2 0 -3 3 2 0 - 4 2 0 -4 2 1 0 - 3 1 1 15 5 1 0 - 5 2 0 -6 3 1 1 4 9 3 5 17 2 4 3 1 8 2 5 4

50 .

40 -

11. 30- -

o 0

' 20O 0

0'-1 * 3

5 10 15Rosen

Fig 3 Scatter ofcorrelation between Parkinson's diseasepatients' scores on Rosen Drawing Test and total loss-of-form errors.

C-

a

ILU-

0

15-10~~~~~~~~

20:

5 .S5 ~~~~~0 S0 0

0 3I.. .I

.I, , , , I , . .45 50 55

MMS

Fig 4 Scatter of correlation between Parkinson's diseasepatients' scores on the modified Mini-Mental Stateexamination and loss-of-form errors on Path 7.

ratings on all paths correlated with performance onthe Rosen Drawing Test (r = 0*50, p = 0.048) (fig 3).The sum of loss-of-form errors did not correlatesignificantly with the modified MMS scores, but totalloss-of-form errors on Paths 3, 6 and 7 did (r = -0-84,-0*63, and -0*51 respectively; p = 0.05) (fig 4).Tracing and hesitation errors did not correlate withmodified MMS, Rosen Drawing Test, or loss-of-formerrors.

Correlation of loss-of-form errors withneuropsychological variables was not possible in thecontrol group because of the lack of variance in theerror ratings (that is error ratings were either at theminimum or maximum). T tests comparing controlswho were successful and not successful on Path 7 ofthe tracing task revealed no differences betweenthese groups in modified MMS or Rosen DrawingTest scores.

60

continuation of the pattern into the degraded por-tion. Again, ratings for Path 7 in the controls are

based on the first performance attempt.

Relation of errors to cognitive tasks. In the Parkin-son's disease group, the sum of loss-of-form error

Discussion

The generation of tracing and hesitation errors by theParkinson's disease group, and the paucity of theseerrors in the controls, suggests that the abnormalitiesmay be specifically related to Parkinson's disease.These errors could be related to the motor symptomsof Parkinson's disease, although we found no correla-tion of errors with any specific rating of Parkinson'sdisease. Correlations between visual tracking perfor-mance and bradykinesia have been described byothers but were not found in this study." Mortimer etall2 used a random tracking test to measurebradykinesia; their findings related this measure toimpaired performance on tests of visual-spatialreasoning. Others have also described a relationshipbetween bradykinesia and visuospatial perfor-mance.5 13

Loss-of-form (errors in filling in missing seg-ments), occurred in both Parkinsonian patients andcontrols, but performance in the two groups wasquantitatively and qualitatively different. First, in theParkinson's disease group, these errors occurred on

Stem, Mayeux, Rosen, Ilson148

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all degraded paths and increased in frequency andseverity as the complexity of the paths increased.Controls made fewer errors and only on the morecomplex designs. Second, controls tended to makeerrors of omission; most would not trace the missingsegment until redemonstration. Patients made errorsof commission, generating inaccurate movementswithout apparent insight. Third, the controls, unlikethe patients, eliminated their errors with additionalpractice. Finally, loss-of-form errors correlated withperformance on the construction and general intel-lectual tasks only in the Parkinson's disease group.Although control's errors were minor, they none-

theless occurred on what appears to be a relativelysimple task. It is possible that their greater age andlower level of education played a role in theirperformance on the tracing and constructional tasks.Age and level of education have both been found tocorrelate with performance on intellectual tasks inParkinsonians as well as controls.5 Despite thisrelationship, patients still performed more poorly onthe tracing task than controls.The relation between patients' loss-of-form errors

and performance on the constructional task suggeststhat these tasks are mediated by a similar process.Poor performance on similar tasks has been encoun-tered frequently in Parkinson's disease and havebeen variously described with such terms asvisuomotor,14 sensorimotor,'5 and motor planningdeficits."3 16 It is possible that these terms are allattempts to characterise a perceptual motor deficitwhich is not related to the specific motor problems inParkinson's disease such as tremor or rigidity. Thisdeficit could represent an inability to coordinateperception with certain motor functions in order togenerate movements based on an internal concept ofspace (or a motor plan). Perception refers to theability to discriminate external sensory information,in this case visual. The motor functions consist of aseries of movements which are sequentially per-formed. The coordination of these two activities inorder to fulfil a motor plan may represent a higherorder of motor control.The tracing task in this study required both

sequential and predictive movements. Specific move-ments had to be accomplished in the absence of visualfeedback, forcing the subject to generate predictivemovements based on an internal spatial percept.Flowers and others have also demonstrated thisdeficit in the generation of movement in the absenceof visual guidance in both Parkinson's disease andnon-human primates with lesions in the basalganglia.6 14 17-19 The tracing task also demands thatthe movements be generated in their propersequence, beginning and terminating at their propertime. Deficits in the sequencing of movement have

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often been demonstrated in Parkinson's dis-ease. 5 20 21

In the constructional task, the subjects again wererequired to generate sequences of movements thatsatisfied set spatial demands. In this case visualguidance was present in the form of the designs, butthe designs were often complex enough to challengethe subject's ability to organise the movementsnecessary to reproduce them. Other investigatorshave demonstrated constructional deficits in Parkin-son's disease which may also reflect this inability toorganise or sequence the movements necessary forsuccessful performance.'3 2 Other tracking studiesdemonstrate that even when patients are informedthat a target is moving in a specific sequence theycannot use this information to improve their trackingaccuracy.6 16

According to Marsden'6 the basal ganglia may beresponsible for the automatic execution of learnedmotor plans; that is, they take part in sequencing themotor programs needed to accomplish a motor plan.The mechanism through which the basal ganglia mayaid in this activity is unknown.

Angel's20 hypothetical efference copy system mayexplain how perceptual motor coordination takesplace. In a tracking study, he induced subjects tomake incorrect movements. Subjects could correctthese movements even when there was no externalfeedback to inform them that they were incorrect. Hesuggested that subjects corrected errors usingefference copy, which he defined as a centralrepresentation of efferent motor activity. Theserepresentations of motor commands are evaluatedfor their appropriateness or effectiveness. Incorrector ineffective movements are corrected either beforeor as they occur, with or without external feedback.Angel observed this error correction mechanism inParkinson's disease but it was slowed, suggesting thatthe basal ganglia were involved in an efference copysystem.2" 25 Furthermore, this may imply that thebasal ganglia aid in the monitoring of ongoingmovement and may even determine when to movefrom one portion of a motor plan to the next.

In single unit studies of basal ganglia areas inprimates, the animals also made tracking movementswhich were disrupted and then had to be corrected.Cells fired more frequently after the correctivemovements had been initiated, suggesting that thebasal ganglia are involved in monitoring as opposedto initiating the movements.2508 Prism adaptation,another task which requires the coordination ofattempted movements with an internal percept, isdisrupted with lesions to the basal ganglia in primatesand man. Again this suggests that the basal gangliaare critical in perceptual motor coordination.23'Similar monitoring systems involving the basal

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ganglia have been suggested by others32 33 and areanatomically feasible.34The deficit in the coordination of perceptual and

motor activity could be viewed as purely motor innature.16 On the other hand, this process may have anintellectual component for the following reasons: (1)Loss-of-form errors in this study correlated withperformance on the mental status examination, (2)Investigators have reported deficits in purely intellec-tual tasks which require Parkinsonian subjects tomonitor test responses and use this information tomodify later performance. (An example of this is theWisconsin card sort),3 (3) Poor performance onconstruction tasks, block design and puzzle assemblytasks have been observed in Parkinson's disease 12 13 22as well as lower scores on the Performance subtests ofthe Wechsler Adult Intelligence Scale,4 all of whichare measures of intellectual ability, (4) Spatialrepresentation, which is dependent on perceptualmotor coordination,3 is also defective in Parkinson'sdisease; for example, patients perform poorly on theAubert task, a test of horizontal orientation.3"Potegal has also demonstrated that the basal gangliamay be necessary for locating objects in spacerelative to the observer."3Our data may suggest that perceptual motor

impairment in Parkinson's disease is a form ofintellectual impairment associated with higher-ordermotor control of sequential and predictive voluntarymovements. This may reflect a disturbance in basalganglia participation in a hypothetical efference copysystem. It is a subtle deficit that appears in mostParkinsonian patients and does not appear to simplybe related to motor symptoms of Parkinson's disease.

We thank the staff and members of the South EastQueens Multi-Service Senior Citizens Center fortheir aid and participation in this study, and Drs Coteand Fahn for their assistance.

This work was supported by the Parkinson's DiseaseFoundation and the Epply Foundation (Mr Stem)and in part by a grant to Dr Mayeux (AG02802).

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