Journal ofNeurology, Neurosurgery, and Psychiatry 1990;53:862-868

Temporal movement control in patients withParkinson's disease

Normand Teasdale, Jim Phillips, George E Stelmach

AbstractPatients with Parkinson's disease (PD)have been reported to be unable tomodify their movement velocity to adaptto changing environmental demands.For example, when movement ampli-tude is varied, PD patients usuallyexhibit a nearly constant peak velocity,whereas elderly subjects show an in-crease of their peak velocity with in-creased amplitude. The experimentexamined the ability of PD patients tovary the duration of their movement(four different percentages of theirmaximum) under conditions wheretemporal, but not spatial, control was

emphasised. PD patients had longermovement times than control subjects,but were able to vary the duration oftheir movement with comparable tem-poral accuracy to that of elderlysubjects. For both groups, the agonistEMG activity increased with decreasedmovement duration. For the PDpatients, the number of agonist burstsincreased with increased movementduration.

Clinical HealthScience Center/Department ofRehabilitationMedicine and MotorBehavior Laboratory,University ofWisconsin-Madison,United StatesN Teasdale*J PhillipsG E Stelmach*Present address:Universite Laval, Labatoirede Perfermance NotriceHumaine PEPS, Quebec,CanadaCorrespondence to:Dr G E Stelmach, Universityof Wisconsin-Madison,Motor Behavior Laboratory,2000 Observatory Drive,Madison, Wisconsin 53706,United States.Received 31 May 1988 and infinal revised fornr16 January 1990.Accepted 31January 1990

A cardinal manifestation of Parkinson's dis-ease (PD) is slowness in the execution of a

movement.`q Experiments suggest that PDpatients are not only slow, but that they are

also seriously limited in their ability to modifymovement velocity to meet changing environ-mental demands.39 10 For example, Draperand Johns3 reported that, contrary to elderlysubjects who showed an increase in their peakvelocity with increased movement amplitude,PD patients exhibited a nearly constant peakvelocity across movements of different ampli-tudes. When under drug therapy, PD patientsincreased their peak velocity, but it was stillsmaller than that of elderly subjects by a more

than five-fold difference. Flowers'0 also re-

ported that PD patients made movements ofdifferent amplitudes with constant velocity so

that longer movements took more time. Somestudies'1112 have also suggested that PDpatients are often unable to move faster whencued to do so. Thus there seems to be a

general consensus that PD patients can onlyexecute movements of different amplitudes ata single, slow velocity and cannot increasetheir movement velocity when they are cuedto do so.These experiments provide valuable infor-

mation on how movement amplitude affectsPD patients' control of movements. It is also

of interest to determine whether and how PDpatients can vary the duration of a movementwhen amplitude is kept constant. Indeed,movement time is an important parameter inmovement behaviour"'-6 and an inability tomodify the temporal structure of a movementwould suggest fundamental underlying de-ficits in movement organisation. Thus it isuseful to determine the mechanisms by whichPD patients vary the duration of theirmovements.The underlying mechanisms of bradykin-

esia has been addressed by Hallett et al.17-19They attempted to understand bradykinesiaby examining abnormalities in PD patients'EMG during voluntary movements. In nor-mal individuals, simple arm movements areusually initiated by a burst of EMG in theagonist muscles and decelerated by a burst inthe antagonist muscles; the movement issometimes concluded by a second and smallerburst in the agonist muscles.20 For brady-kinetic patients, additional cycles of alter-nating bursts in the agonist and antagonistmuscles have been observed.'8 19 Hallettt7 18suggested that this is because the amount ofEMG activity that can be put into a burst islimited in PD patients and that bradykinesia isa saturation problem, that is, a failure toappropriately "energise" the agonist muscle.Subsequently, Berardelli et al.2" showed thatthe first agonist burst does not saturate andsuggested that in PD there is a breakdown ofthe link between "perceptual appreciation" ofthe goal and "delivery of the appropriate in-structions" to the motor cortex. It followsfrom these two experiments that PD patientsrequire more bursts ofEMG to produce bothfaster and longer movements.'7 1822

In previous experiments, however, move-ment amplitude covaried with movementduration so that movements of longer ampli-tudes were also of longer durations. Hence, itis not known whether the additional cycles ofEMG activity previously observed in PDpatients were the results of the longermovement amplitudes or of the longer dura-tions associated with the movements of longeramplitudes. A resolution of this question isessential to a better understanding of thephysiological mechanisms underlying theproduction of multiple cycles ofEMG activityin PD. The aim of this experiment was thustwofold: 1) to examine the degree to whichPD patients can vary the duration of theirmovements, and 2) to determine whether theincreased cycles of EMG activity observed inPD patients are associated with the produc-tion of slow or fast movements.

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Temporal movement control in patients with Parkinson's disease

Materials and methodsEight patients with idiopathic PD (mean age= 66-2 years) and eight age- and sex-matchedelderly subjects (mean age = 68-7 years) wereexamined. The clinical features of the patientsare presented in table 1. Patients followedtheir normal schedule of medication duringthe day of testing, but an attempt was made tomanage the effects of medication by testingthe patients within the same relative temporalperiod of their drug cycle. Control subjectswere free from any signs or symptoms ofneurological disease. All subjects gave in-formed consent for the procedures used.The apparatus consisted of a horizontal

aluminium manipulandum; a force transducerwas attached to the handle and reflected theforce necessary to overcome the inertia of themass-lever system. In the initial position, thelever was electrically connected with a rigidstarting plate; moving the lever from theinitial position opened the circuit. Movementonset was defined as this initial drop in thevoltage signal, and all the recorded data weresynchronised with this event. Because almostno movement is required to deactivate thecircuit, such a procedure allows for a moreprecise determination of movement onset thanwhen it is determined from a displacementsignal or its derivatives. Moving through amicroswitch located at 200 closed the electricalcircuit, and movement time was determined asthe time interval for which the voltage signalwas low.Muscle discharge patterns from the biceps

brachii and triceps lateralis were recordedusing physiological amplifiers having a com-mon mode rejection of 87 dB at 60 Hz(Therapeutics Unlimited). Pre-spaced (2-5cm) Ag-AgCl surface electrodes were placedover the muscle bellies. The electromyogra-phical (EMG) signals were pre-amplified atthe source, full wave rectified, band-passlimited from 40 Hz-4 KHz, and filtered with a

2-5 ms time constant. All signals were digi-tised at 500 Hz.The movement examined was a horizontal

elbow flexion, with the shoulder abducted 900.A display panel with two vertically alignedlight-emitting diodes (LED) faced thesubjects. The top light indicated a ready sig-nal and was labelled as such, and the bottomlight signified that subjects were to initiate themovement. A target indicated 200 but therewas no spatial accuracy constraint. Subjectswere instructed to follow-through theirmovement and encouraged to plan theirmovement in advance and to perform it with-out making on-line corrections. Thus the goalwas to perform the initial 200 of movement ina pre-determined duration without stoppingat that spatial location; in fact, for all temporalconditions, the instructions resulted in thelimb stopping when the elbow was near

hyperflexion (about 1500). There are manyreal life analogues to this task: for example,when throwing an object, one often needs tocontrol the time interval between movementinitiation and object release without actuallystopping the throwing arm at the point of

release. All patients were able to follow theseinstructions as no hypometric movementswere observed.

In a baseline condition, subjects were in-structed to produce ten maximum speedmovements upon presentation of the visualstimulus. Temporal feedback was providedafter every trial and subjects were encouragedto move fast; average movement duration wascalculated from those trials. In subsequentconditions, subjects were trained to producemovements of similar duration, 30% slower,and 60% slower. To ensure that subjectswould perform movements as fast as theycould, we added a "speed-plus" condition. Inthis condition, the goal duration was 10%faster than the Movement Time (MT) ob-tained for the baseline condition; subjectswere unaware of this procedure. All subjectsproduced shorter average MTs for the"speed-plus" condition than for the "as fastas possible" condition (on average, 34 msshorter for the PD patients and 15 ms shorterfor the elderly). All conditions were presentedby block. There were 10 practice trials fol-lowed by 25 experimental trials for each of themovement durations. Movement time feed-back was presented verbally when it exceeded± 10% of the goal duration. EMG activity inthe biceps and triceps muscles were alsomonitored on-line via an oscilloscope (Tek-tronix 5113) and background activity wasminimised before the initiation of a trial.Each trial started with a ready signal (the topLED was turned on for is), and a variableforeperiod (0-5s to 1 5s) preceded the stimulus(bottom LED) to initiate a movement.

Data AnalysisThe trials obtained for the "speed-plus" condi-tion and the slowest movement time conditionwere selected to evaluate whether additionalbursts of EMG activity were used to producefaster movements. An arbitrary temporalbandwidth from 100 ms before the initiation ofthe movement to 100 ms after the 200 dis-placement was first established. The number ofagonist bursts included in the temporal band-width was determined by visually identifying(on a computer display) the onset and offset ofthe bursts for the background activity. Becauseof the procedure used to minimise backgroundactivity before trial initiation, there was littleresting EMG activity preceding the movement,thereby providing a sensitive initial detection.The criterion for offset was when the EMGreturned to baseline or near baseline activity(no higher than 20% of the peak EMG). Burstsinitiated before the movement reached the 200target, but which finished after it, were in-cluded in the analysis; bursts that started afterthe 20° target was reached were, however, notincluded. To determine- whether the agonistburst was saturated and whether there was anyextraneous activity in the antagonist muscle inPD subjects, theEMG envelope for the agonistand antagonist muscles was also calculated.TheEMG activity obtained for the speed-plus,slowest and baseline conditions was integratedin four temporal bandwidths of 50 ms from the

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Teasdale, Phillips, Stelmach

Table 1 Profile of Parkinson's disease subjects

Subject Age Duration Hoehn andnumber (years) of disease Yahr Predominant symptoms Medication

1 70 3 I Mild tremor Artane2 68 23 III Moderate bradykinesia, Sinemet,

mild rigidity Amantadine3 61 7 III Severe bradykinesia, Sinemet,

moderate rigidity, akinesia Artane4 72 17 II Mild tremor, Sinemet

moderate rigidity5 66 9 III Moderate bradykinesia, Sinemet

mild tremor6 64 5 II Mild rigidity, Sinemet

moderate tremor7 68 7 III Moderate to severe rigidity Sinemet8 61 19 III Moderate rigidity, Sinemet,

severe akinesia Pergalide, Imiprine

onset of the agonist muscle.* The values ob-tained for each subject were normalised to theintegrated EMG values obtained for the base-line condition. Analysis of variance was used todetermine group and temporal requirementeffects.

ResultsTemporal characteristics of the movementsThe data demonstrate that PD patients havethe ability to vary the duration with which amovement is produced. The movement timesobtained for the four temporal requirementsare presented in table 2. PD patients producedslower baseline maximum movement times andas a result had slower movements at the fourtemporal requirements (on average, 249 msversus 191 ms). The difference, however, wasmodest (F(1,14) = 4-03, p < 0-06). PDpatients were able to vary their movement timewhen required to do so (191, 225, 272, and 309ms for the four temporal requirements;(F(3,42) = 273-35,p < 0001),fortheeffectoftemporal requirement). When the movementtimes were transformed relative to each sub-ject's maximum (movement time x 100/meanmovement time of the baseline condition),there were no group differences (p > 0-05).Hence, both groups showed a similar ability tovary movement duration.

Table 2 Summary of movement production resultsforPD patients and elderly subjects

Slowest Slow Fast Speed-plus

Mean Movement TimePD 309 (79) 272 (82) 225 (75) 191(62)Eld 247 (49) 200 (37) 166 (27) 151 (31)

Mean Time to peakforcePD 213 (54) 176 (46) 131(40) 118 (30)Eld 136 (35) 111 (29) 77 (18) 76 (17)

Mean Temporal variabilityPD 51(36) 42 (18) 34 (13) 25 (14)Eld 36 (8) 30 (9) 24 (12) 21(7)

Values in brackets are the between-subject standard devi-ations.

*Burst offsets are usually easily identifiable. The exact tenporallocation of the endpoint, however, is often arbitrary. Thetemporal requirements in the present experiment accentuatedthis problem. For this reason, we arbitrarily determined tem-poral bandwidth of 50 ms from the agonist onset. The selectionof a 50 ms bandwidth was based on previous experiments thathave estimated the first agonist burst duration to be in the 50-80ms range."2'

The temporal variability of both groups wascomputed (within-subject standard deviationof movement times at a given temporal re-quirement) to determine if PD patients weremore variable than elderly subjects at achievinga given goal movement time. The data presen-ted in fig 1 show that PD patients were slightlymore variable than elderly subjects. For bothgroups, the variability increased with an in-creased movement time (from 16 ms to 31 msfor the elderly subjects and from 25 ms to 58 msfor the PD patients; F(3,42) = 6-58,p < 0-001). Temporal variability, however,increases with increased movement time,23implying that the increased temporal vari-ability for PD patients is not the result ofdifferent control processes but simply a reflec-tion of longer movement times. Thus PDpatients were slower than elderly subjects, butthe overall linear relationship obtained be-tween temporal variability and movement timeimplies that both groups were affected similarlyby the different temporal requirements.The temporal structure of the force-time

curves was also analysed to determine ifchanges in movement duration affect theunderlying temporal movement organisation.PD patients needed more time to achieve peakforce than elderly subjects (on average, 160 msversus 100 ms; F(1,14) = 14-26, p < 0 005).Peak force also occurred relatively later in time(ratio time-to-peak force/MT) for the PDpatients than for the elderly subjects. On

- 5O.

D 40-3-

'o 30-

20-v-

125 175 225 275Mean movement time (ms)

325

Figure I Movement-temporal variabiltty (within-subject standard deviation of the movement times at agiven temporal condition) for the PD patients and theelderly subjects.

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average, time-to-peak force occurred at 65% of (fig 2) shows that our PD patients did notthe total MT for the PD patients, whereas it exhibit this saturation problem (p > 0 05 foroccurred at 52% for the elderly (F(1,14) = the group effect). As in elderly subjects, PD4-61, p < 005). Thus peak force occurred patients modulated the amount of EMGabsolutely and relatively later in time for the activity produced so that faster movementsPD patients. Nevertheless, PD patients modu- were produced with much larger initial EMGlated their time-to-peak force, as did the elderly activity than slower movements (F(1,14) =subjects. For the four temporal requirements, 14-33,p < 0005, for the movement time effect.PD patients needed 118, 131, 176, and 213 ms Despite the ability to produce more EMGto achieve peak force whereas elderly subjects activity when faster movements were required,needed 76, 77, 111, and 136 ms (F(3,42) = most of our PD patients (seven out of eight)51 87, p < 0-001, for the main effect of showed multiple bursts of EMG. However,temporal requirement). multiple bursts of EMG were not observed

when faster movements were produced, butEMG rather when slower movements were produced.Hallett and Khoshbin'5 suggested that PD Figure 3 has representative raw EMG agonistpatients can put a limited amount of EMG and antagonist records for the speed-plus andactivity in a burst and as a result they need the slowest movement time conditions. Frommultiple bursts of EMG to produce move- these records, it is clear that the number ofments of greater amplitude.t An examination bursts increased with an increased MT for theof the integrated agonist EMG activity for the PD patient. On the average, elderly subjects"speed-plus" and the slowest MT conditions had a constant number of bursts across the two

conditions of movement time (1I 2 and 1I5 forthe speed-plus and the slowest movement timeconditions), whereas PD patients needed more

* * PD speed-plus bursts and showed significantly more "burst-_- - _O PD slowest ing" over longer movement durations (2-0 and0 n0 Elderly speed-plus 3 51 for the speed-plus and the slowest MT).O- -O-0Elderly slowest Both the group effect (F(1,14) = 15-06, p <

0-001) and the interaction of temporal1-30 Agonist requirement by group (F(1,14) = 6-44, p <115 0-05) were statistically significant. Hence, not

\\_ only did PD patients require more bursts than( 1X00\* elderly subjects to produce a movement, but

085 they also showed an increased number ofburstsa)/ tC82 ug with increased movement time. There was also

Q' 0.70 / / a strong relationship between bradykinesia andC 055 / _/ the multiple bursts ofEMG activity. Figure 4

-055e shows the individual relationships between the0.40 ____ I_ I_ I__ _ number of bursts produced and movement

0 50 100 150 200 time for the PD patients and the elderly1 60 Antagonist subjects. For seven out of eight PD patients, an

A1-40 n i 0 increased movement time yielded a significantincrease in the number of bursts which ex-E 1 20 ~ _ ceeded the "normal" two bursts of agonist seen

in the triphasic pattern of EMG activity of100 0 normal individuals.

C 080 .os It does not appear that the additional cyclesp ,.- N_ s of EMG were the result of extraneous activity

E 060 'U -NO in the antagonist muscle as might occur if there_ *-4 - were problems of reciprocal inhibition. For

0.40 '5 both groups (p > 0-05, for the group effect), the0 50 100 150 200

Time (ms) antagonist EMG activity, presented in fig 2,was larger for the speed-plus movements than

Figure 2 IntegratedEMGfor the agonist and for the slowest movements (F(1,14) = 15.51,antagonist muscles for the slowest and speed-plus p < 0-005). There was a tendency for thetemporal conditions. The labels on the abscissa correspond ed< to Thereas acteneny for thto the integrated EMGfrom agonist onset to 50 ms, 51 to elderly to show an increased activity 150 ms100 ms, 101 to 150 ms, and 151 to 200 ms after agonist after agonist onset, but this effect was notonset, respectively. significant (p > 0-05). This supports

Delwaide's24 findings, using H-reflex tech-tIn this experiment, the temporal location of the antagonist niques, that reciprocal inhibition is not(when present) to the agonist activity was quite varied for both impaired in PD.g us.- rr "l. -5l W_ W51 ISULr..,r;II tU a p'A lnegroups. ror tnus reason, we wiii not rexer to a specinc locuscausing "multiple cycles oftri-phasic patterns" (that is, agonist-antagonist-agonist) as Hallett and Khoshbin'5 did, but simply tothe mechanism of producing multiple bursts or cycles ofEMGwithout reference to the activity in the antagonist muscle. Theexact role and function of the antagonist burst in the control ofsimple movements is still a matter of debate. Nevertheless, thereis a general consensus that it is involved in the deceleration ofthelimb. The task used in the present experiment did not have anyspecific deceleration requirements and as such was certainlydifferent than the one used in previous experiments, suggesting a

task-dependent role for the antagonist muscle.4'

DiscussionWhereas previous experiments have focusedupon the effects ofmovement amplitude on PDpatients' movement control, this experimentexamined the extent to which PD patientscould control their movement duration and

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PD speed-plus0-4.

w3

PD slowest

0-3 T

0-21

Antagonist

0-14

0

-0-1 t

_0'3 I

Agonist

S_~~~~~~~~Atgnsw~~~~~~~' r..

0:6 0:8 i-b 1-2Time (s)

Elderly slowest

Agonist

Antagonist

0-2 0-4 0-6 0-8Time (s)

Figure 3 Representative raw EMG records for the agonist and antagonist musclesfor the slowest and the speed-plus conditions. The arrows indicatemovement onset and the point at which 200 was reached. Clearly, the number of agonist bursts increases with an increased MTfor the PD patient (2bursts versus 6 bursts), while it stays normalfor the elderly subject.

how their pattern ofEMG activity waby variations in movement durationslower minimum movement duratipatients were able to vary movementwith comparable temporal accuracy rthat of elderly subjects. The temporalof their movements, however, wasfrom that of elderly subjects. Peoccurred both absolutely and relative]time for the PD patients, implyingincreased slowness in PD cannot be afor by a simple overall slowing of t]programme. Rather, the results suggefundamental problem, because PDgenerated forces at rates that were albeyond a simple proportional slowijwas the case for each of the fourconditions studied.

Figure 4 Relationshipbetween the mean numberof agonist bursts and meanmovement timefor the PDpatients and the elderlysubjects. Each linerepresents the meannumber of burstsfor theslowest and speed-plusmovement time conditionsfor each subject.

6-

5-

4

o 3z

2 2-

0100 200 300 400

Mean movement time (ms)

5S affected Contrary to previous experiments in whichL. Despite PD patients, even when under drug treatment,ions, PD were unable to speed up their movements,' 3 11 12duration PD patients in this experiment were able to

-elative to produce movements that were 15% faster thanstructure during an initial "as fast as possible" condition.different Obviously, this result implies that sub-maxi-ak force mal movements were initially produced despitely later in the specific instructions to produce movementsthat the that were as fast as possible. This result,ccounted however, may also be interpreted as an impor-he motor tant aspect ofPD movement control. Indeed, itst a more is possible that a portion of the slowness inpatients movement, as well as the limited ability tobove and modify movement velocity (hence, movementng. This duration when amplitude is constant), showntemporal in previous experiments, was the result of a

reluctance among the PD patients to emphasisemovement speed at the expense of movementaccuracy. According to this suggestion, a por-tion of the slowness observed in PD is not areflection of the disease itself but is insteada necessary adaptation of the sensory-motorsystem to cope with the realities of an environ-ment that requires movement precision andaccuracy.4Because of the specific task requirements

previously used, however, this aspect of PDmotor control might have been overlooked.Indeed, previous experiments that haveexamined the velocity control problem in PDhave used very similar tasks in which spatial

500 accuracy was always emphasised (either im-posed by the task or perceived by the patients).

0-3Elderly speed-plus

0-2-

01 *+w

0-

-0-1 +

- 0:2 04

0- I

Agonist

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Temporal movement control in patients with Parkinson's disease

For example, in the Berardelli et al"experiment, subjects were required to jointhree or four small dots in order to draw atriangle or a square. PD patients, in thisexperiment, were slower but were actuallymore spatially accurate than elderly subjects.In our experiment the task did not have anyspatial accuracy requirements and agrees withour suggestion that PD patients showed asignificant decrease in their movement time(thus increased velocity) when they wererequired to reduce it (15% decrease versus 9%for the elderly). Also, Sanes25 26 recentlyshowed that, for an alternating tapping task(Fitts-task), PD patients performed as quicklyand accurately as elderly subjects when the taskhad a low index of difficulty (that is, largetargets, small amplitude). Movement impair-ments were induced only when spatial accuracyand/or movement amplitude were increased.Thus, task requirements appear to be an im-portant determinant of the movement perfor-mance and control of PD patients. Similarly,there is an increasing amount of evidencesuggesting that, for normal subjects, the con-text in which a movement is performed is amajor determinant of movement organisa-tion.27-This context-dependent hypothesis suggests

that the expression ofthe velocity and temporalcontrol deficits in PD varies as a function oftask requirements. Thus it is important thatfuture research needs to vary systematically thecontext in which a movement is performed todetermine where and how the performance ofPD patients breaks down. The determinationof these breakdowns along the varying con-tinuum of movement constraints should yieldinsights into the underlying neuro-controlprinciples in PD.32

Multiple cycles ofEMG activity in Parkinson's,.diseaseWhile some studies'7 18 21 22 have suggested thatPD patients require more cycles of EMG toproduce movements of short durations, wefound that PD patients required more bursts toproduce those movements. Rather than pro-ducing movements of longer durations byincreasing the duration of their first agonistEMG burst, 1920303336 seven out of eight PDpatients required additional cycles of EMGactivity. Further, there was no indication thatPD patients had problems appropriately"energising" the agonist muscle; indeed, theintegrated EMG data showed that the firstagonist burst did not saturate in PD patients.As in elderly subjects, PD patients modulatedthe EMG activity so that faster movementsrequired more EMG activity that did slowermovements. Berardelli et al 2' also reported thatthe duration and amplitude of the first agonistburst in a wrist fiexion task does not saturate inPD but increases with increased movementamplitude.The question remains as to why multiple

cycles of EMG activity are observed in PDpatients. To explain some of the slowness inPD, Berardelli et ale raised the possibility that

patients underestimate the muscle activityrequired for a particular movement because ofa"breakdown of the link between the perceptualappreciation of the task requirements and theappropriate instructions to the motor cortex".This suggestion cannot explain why slowerrather than faster movements were character-ised by an increased number of EMG cycles.Because of their larger EMG requirements,faster rather than slower movements shouldhave yielded an underestimation of the muscleactivity and an increased number of EMGcycles. In our experiment, there was also astrong relationship between bradykinesia andmultiple cycles of EMG activity so that themost bradykinetic patients were also thepatients who exhibited the most cycles ofEMG. Clearly, tremor is a likely explanationfor these results. Action tremor has in fact beenshown to be in the 6 to 9 Hz range, and higherfrequencies (10-11 Hz) have also been ob-served.37 Nevertheless, the results shed morelight on the physiological mechanism of pro-ducing multiple cycles of EMG. Because wefound in a previous experiment'8 thatmovement time covaried with movementamplitude, the results suggest that the multiplecycles of activity were not the result ofmovements of longer amplitudes but of longermovement times associated with the move-ments of longer amplitudes. Thus ratherthan having a problem calculating necessaryforces" 3 or. appropriately "energising" theagonist muscle,4 PD patients may experienceproblems controlling muscle activation. Whilethe cortico-motor neuron connection has beenshown to be intact in bradykinetic patients39and the recruitment order of motor neurons islittle affected,"' there are, however, motor unitabnormalities.Milner-Brown et al"' reported that, even

when PD patients made an effort to maintainvoluntary force, some motor units stoppedfiring for prolonged periods; some of the unitsalso fired at abnormally low frequencies (2-3per second). Further, in agreement with ourresults showing greater EMG abnormalitiesfor slower movements, their patients haddifficulty in the recruitment of motor units atlow threshold levels. Dietz et al42 also reporteda prolonged postexcitatory inhibition betweenspike bursts for tremorous patients. Thus themechanism of producing multiple cycles ofEMG might be associated with an inability tomaintain and regulate the EMG activity overtime rather than with a "perceptual break-down" or an inability to appropriately "ener-gise" the agonist muscle

Slowness of movement, on the other hand,might be induced by increasing the spatialaccuracy requirements. In our experiment, thelack of spatial accuracy constraints resulted inseven out of eight patients being as fast ornearly as fast as elderly subjects. As previouslymentioned, Sanes2526 also suggested that PDpatients can produce nearly normal perform-ance and that it is increased movement accu-racy which induces movement impairments.This may be the case because increasing accu-racy requirements creates a different control

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problem.4"5 For example, Waters and Strick4s

have shown that the antagonistic activity is

nearly abolished when subjects are allowed to

terminate their movement by hitting a mechan-

ical stop as opposed to when they must de-

celerate precisely. Hence, it could be that

impaired agonist-antagonist synergies induce

slowness of movement.Overall, the data demonstrate that when

temporal control is emphasised, PD patients

are able to vary movement duration with com-

parable temporal accuracy to that of elderly

subjects. The movements were, nevertheless,characterised by more irregularities in the

force-time and EMG patterns, implying that

while PD patients have an accurate internal

model of the forces required to produce

movements, they have problems regulating and

sustaining EMG activity. Indeed, slower (not

faster) movements were characterised by a

greater number of EMG bursts. It is possible

that changes occur in the excitability of certain

interneurons24 or that the impulse to the cor-

tico-spinal system is impaired in PD.33

This research was supported by a grant from the National

Institute of Neurological Disease and Stroke (NS 17421)

awarded to George E Stelmach.

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