Exp Brain Res (2003) 151:249–261DOI 10.1007/s00221-003-1452-2

R E S E A R C H A R T I C L E

Diana H. Romero · Arend W.A. Van Gemmert ·Charles H. Adler · Harold Bekkering ·George E. Stelmach

Altered aiming movements in Parkinson�s disease patientsand elderly adults as a function of delays in movement onset

Received: 8 May 2002 / Accepted: 24 February 2003 / Published online: 3 June 2003� Springer-Verlag 2003

Abstract This study investigated the effect of lengthen-ing the time the hand remains immobilized on an aimingmovement performed by Parkinson’s disease (PD) pa-tients and elderly adults, and whether visual informationcould compensate for the effects of delay. In ExperimentOne, PD patients and elderly adults kept the limb in astatic position for 1, 6, or 10 s prior to movementinitiation, both with and without vision of the initial limbposition and the movement trajectory. Compared toelderly adults, PD patients had increased movement timesand jerk scores, and exhibited shorter primary submove-ments that erred in initial movement direction. Length-ening the time delay increased movement time, decreasedmean acceleration, and decreased the distance covered inthe primary submovement for both groups. Parkinsonianpatients, however, exhibited reduced length of the

primary submovement across delay compared to elderlyadults. Occluding vision caused the movements of PDpatients to deteriorate on all measures. Although theperformance of both groups was enhanced when visionwas available, vision was not able to fully counteract theeffects of delay in either group. In Experiment Two,participants moved to a previously viewed target toexamine movement accuracy. Systematic undershootingof the target as a function of delay was found for bothgroups. Parkinsonian patients exhibited greater under-shooting of the target after the primary submovement bothwith and without vision. Visual feedback reduced theeffects of delay for both the elderly and PD patients. Itcan be inferred from the results that the decay in positionsense as a function of time produces impairments inincorporating the initial limb position in motor planningprocess.

Keywords Time delay · Proprioception · Limbimmobilization · Visual control · Basal ganglia

Introduction

Previous research has consistently shown that maintainingthe limb in a static position for a period of time prior tomovement onset results in decreased accuracy of limbposition matching or pointing to the occluded limb(Monster et al. 1973; Paillard and Brouchon 1968;Paillard and Stelmach 1996; Wann and Ibrahim 1992).While accuracy is initially quite good, systematic under-shooting occurs over time, which has been suggested tobe due to a reduction in position sense that results fromsensory receptor adaptation as a function of the timedelay. Decayed position sense has been suggested toresult in errors in judging the position of the limbs inspace, and/or errors in movement (Schneider et al. 1987).Therefore, a reduction in position sense as a function ofthe time the limb remains immobilized would inducedifficulty for the central nervous system to incorporate theinitial limb position into motor planning processes,

D. H. RomeroMotor Control Laboratory,Arizona State University,Arizona, USA

A. W. Van GemmertMotor Control Laboratory,Arizona State University,Arizona, USA

C. H. AdlerParkinson’s Disease & Movement Disorder Center,Department of Neurology,Mayo Clinic Scottsdale,Arizona, USA

H. BekkeringNijmegen Institute for Cognition and Information,University of Nijmegen,Nijmegen, The Netherlands

G. E. Stelmach ())Motor Control Laboratory, PEBE, Room 107B,Arizona State University,Tempe, AZ 85287-0404 USAe-mail: Stelmach@asu.eduTel.: +1-480-9659847Fax: +1-480-9658108

resulting in changes of movement kinematics. To date, noprevious publications have focused on the effects of delayutilizing a pointing task.

Patients with Parkinson’s disease (PD) exhibit elevatedthresholds of position discrimination compared to healthyelderly adults, indicating decreased position sense whenmatching the joint angle of one limb with the other limb(Zia et al. 2000). Although position sense has been foundto decline as a function of aging (Lord et al. 1991;Meeuwsen et al. 1993; Petrella et al. 1997), PD patientsexhibit deteriorated position sense in excess of that foundin healthy age-matched adults. The reason for decreasedproprioception with PD is not well understood, but hasbeen linked to irregular neural activity from the basalganglia into cortical sensorimotor areas, which hindersthe ability to utilize or integrate afferent information(Contreras-Vidal et al. 1995; Flash et al. 1992; Schneideret al. 1987). It has been suggested that as a consequenceof impaired sensorimotor processing, PD patients exhibitan augmented reliance on visual feedback to monitor theirmovements compared to healthy elderly adults (Denny-Brown 1962; Flash et al. 1992; Klockgether and Dichgans1994). Visual information may thus substitute for infor-mation lost as a result of reduced proprioception (Klock-gether et al. 1995). Visual compensation can be explainedby a “visual-proprioception loop” which permits for thecomparison and consequent calibration between the visualposition of the target and the proprioceptive position ofthe limb (Jeannerod and Prablanc 1983). Position sense,therefore, may be calibrated by vision so that theproprioceptive “map” that encodes limb position relativeto the body is matched to the visual “map” that encodesthe position of the limb relative to the target (Jeannerod1988). It may therefore be postulated that visual infor-mation may compensate for the effects of limb immobi-lization. To this end, Wann and Ibrahim (1992)demonstrated that providing occasional glimpses of avisually occluded limb in a static position lessened theerror of matching fingertip positions, indicating visionmay lessen the effects of time delay.

Although previous research indicates PD patients haveimpaired proprioception, to date, no study has examinedlengthening the time delay prior to execution to determinewhether a decay in position sense differentially affects themovement kinematics or pointing accuracy of PD patientsand elderly adults. Furthermore, previous studies have notexamined whether vision can limit or negate the effects ofdelay in either PD patients or elderly adults. Twoexperiments were designed to examine the effects oflengthening the time the hand remains immobilized priorto movement on the kinematics and pointing accuracy ofa point-to-point movement for PD patients and elderlyadults, and whether visual information is used tocompensate for these effects. To this end, the presentstudy investigated whether keeping the limb in a staticposition prior to movement, both with and without visionof the limb and movement trajectory, affected the abilityof participants to plan, regulate, and execute drawingmovements to a visual or previously viewed target. It is

expected that the reduced awareness of initial limbposition will primarily affect variables associated withmovement planning, causing deterioration of movementkinematics and pointing accuracy as a function of delay.

Another aspect investigated was whether vision couldupdate position sense and compensate for the effects ofimmobilization differentially between PD patients, whoare known to be heavily reliant on vision, and elderlyadults. If vision can completely update position sensedespite time delays, both PD patients and elderly adultsshould not exhibit changes in movement kinematicsacross time delay when vision is provided. Occludingvision of the limb during the time the limb remainsimmobilized, however, should impair performance due tothe reduction in position sense as a function of delay.

Experiment One

Experiment One examined the effects of delay on adrawing movement to a visual target performed by PDpatients and elderly adults. In this experiment, we wereinterested in the structure of an aiming movement; thusthe participants were instructed to terminate their move-ments within the end target and therefore accuracy couldnot be examined. To accomplish this, vision of the endtarget was provided throughout the trial so that thedrawing movement could be parsed into primary andsecondary submovements. Primary submovements arebelieved to reflect the pre-planned portion, with second-ary submovements reflecting the “homing-in” phase, of apoint-to-point movement (Meyer et al. 1988; Woodworth1899). It is predicted that the decline in afferent sensoryinformation of the initial limb position as a function ofincreasing delay prior to movement onset will be reflectedin alterations in the variables associated with movementplanning, specifically, shortened primary submovementsthat deviate in initial direction, and a greater number oftrials with secondary submovements.

Materials and methods

Participants

Ten patients with idiopathic Parkinson’s disease (four female, sixmale; mean age of 71 years, range 62–80 years) and ten healthyelderly adults (four female, six male; mean age of 68 years, range61–82 years) participated in the experiment. Parkinsonian patientswere tested in the morning while at the end of their medicationcycle. A summary of PD patients’ symptom profile and diseaseseverity is presented in Table 1. All elderly and PD participantswere right-hand dominant, and had normal or corrected-to-normalvision. The protocol was approved by the Institutional ReviewBoards of both Arizona State University and the Mayo Clinic.

Apparatus and procedure

Participants were seated comfortably in a chair in front of a WacomIntuos 12�18 digitizer tablet (sampling frequency of 200 Hz with aspatial resolution of 0.001 cm) on which they had to make point-to-

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point drawing movements with a digitizer pen between targetsdisplayed on the digitizer. The height of the chair was adjusted sothat the participant’s forearm rested comfortably on the table.Participants held the digitizer pen in a normal pen grip with thedominant hand and performed a linear drawing movement awayfrom the body midline in the horizontal plane, utilizing primarilyelbow extension. In order to make the movement amplitudeunpredictable, three start targets of varying amplitude from thesingle end target were used, resulting in amplitudes of 15 cm,20 cm, and 25 cm. Start targets were equally (five trials of eachtarget) and randomly presented within each vision � delaycondition. Data was collapsed over start targets. Start targets were1.27 cm in diameter, and the end target was 0.79 cm in diameter.

Vision of the task was manipulated by means of a shield placedover the digitizer in the no vision condition, or removal of theshield during the vision condition (see Fig. 1). The height of theshield was adjusted for each participant so that the drawingmovement could be made unobstructed under the shield. The shieldoccluded vision of the participant’s hand, forearm, start target, andmovement trajectory but allowed vision of the end target at alltimes. The shield was removed during full-vision conditions,enabling participants to completely see the start and end targets,their limb, and movement trajectory.

A 1-s, 6-s, or 10-s delay prior to movement initiation wasimposed after the participant’s pen had been positioned in the starttarget for 0.5 s. The experimenter moved the participant’s forearmback to, and placed the pen within, the designated start target in allconditions. Once the pen was placed in the start target, theparticipant was required to maintain the limb in an immobileposition until cued to begin the movement. Patients did not havedifficulty keeping the pen within the start target. If for some reasonthe pen left the start target prior to the “go” signal, the trial wasrepeated. Initiation of the movement was cued by an auditory “go”stimulus generated by the computer upon which the participantsperformed the point-to-point drawing movement as quickly aspossible terminating the movement within the end target. Eachvision (vision, no vision) by delay (1 s, 6 s, 10 s) condition wascompleted as a block of 15 trials for a total of 90 trials. The sixcondition blocks were presented in a randomized order determinedby the computer program.

Data analysis

The onset and offset of the pen tip recording was detected by afixed criterion for absolute velocity, which was 5% of the peakvelocity after low-pass filtering of the signal with a 7 Hz dual-passT

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Fig. 1 The experimental setup of Experiment One. The participantsat in front of the digitizer and held the digitizer pen in a normalpen grip. The participant moved the pen from one of three starttargets to the end target after an auditory “go” signal. During novision conditions a shield occluded vision of the participant’s hand,the start target and movement trajectory, but allowed vision of theend target. The shield was removed during vision conditions toallow full vision of the limb, movement, and targets

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Butterworth 4th order digital filter to eliminate phase shift. Thesegmentation points were fine-tuned by a search for the nearest zerocrossing in the acceleration profile for movement onset before the5% criterion, and for the movement offset after the 5% criterion,respectively.

Normalized jerk score was used to evaluate the smoothness ofthe movement, computed as:ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi

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This measure is unitless because it is normalized for bothamplitude and movement duration (Teulings et al. 1997). Index ofstraightness is a variable of path straightness indicating thedeviation from a straight line and computed as a percentage ofincreasing divergence as:

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A value of zero for the index of straightness indicates aperfectly straight line, with higher percentages indicating increaseddeviation from a straight line. Initial direction is the deviation indegrees from the best-fit line connecting the centers of the homeand end targets. A value of zero denotes a perfect center-to-centerline; positive values indicate deviation to the right; negative valuesindicate deviation to the left.

In addition to analyzing the overall movement, movements wereparsed into primary and secondary submovements. The primarysubmovement was considered from movement onset to the secondzero crossing of the acceleration profile (see Fig. 2). Vision of theend target position was available in all conditions to allow forparsing of the task into submovements as well as to control for anydifferences between participants in remembering target position.Due to the nature of the experimental paradigm, end-point accuracycould not be examined as the participant was instructed to terminatethe movement within the target in all conditions, and trials in whichthe subject overshot the target were eliminated from analysis. Acomputer program written in OASIS (De Jong et al. 1996) was usedto run the experiment and collect the data at a rate of 200 Hz.

A number of dependent variables were measured that reflectplanning and execution of the movement trajectory. The dependentvariables measured for each trial were: movement time, normalizedjerk, mean acceleration, index of straightness, initial direction,length of the primary submovement, and the number of trials withsecondary submovements. Dependent variables were analyzed by a2 (vision) � 3 (delay) within-subjects repeated-measures analysis ofvariance with group as the between-subjects factor. The number oftrials with secondary submovements was analyzed by chi-squarebecause not all trials exhibited secondary submovements. Huynh-Feldt values were used to correct for violations of sphericity, andpost hoc tests were Bonferroni corrected with significance set ata=0.05. All statistical analyses were performed using SPSS forWindows.

Results

The overall pattern of results indicates large main effectsof both the delay and vision manipulations. Means andstandard deviations of the dependent variables as afunction of group are presented in Table 2, as a functionof delay are presented in Table 3, and as a function ofvision are presented in Table 4.

Main effects of group were found for nearly all of thedependent variables (see Table 2). Parkinsonian patientsdemonstrated increased movement time compared toelderly adults (F(1,18)=14.90, p=0.001, h2=0.45). Normal-ized jerk was significantly greater for PD patientscompared to elderly adults (F(1,18)=10.67, p=0.004,h2=0.37). Mean acceleration of the PD patients was lessthan half of that demonstrated by the elderly(F(1,18)=14.81, p=0.001, h2=0.45). Group did not signifi-cantly influence the index of straightness. Initial directionof the drawing trajectory, however, indicated that thedegrees of deviation to the right of PD patients were morethan double that found for the elderly (F(1,18)=15.87,p=0.001, h2=0.47). Parkinsonian patients exhibited sig-nificantly shorter length of the primary submovement

Table 2 Means (SDs) as afunction of group

Dependent variable Elderly adults PD patients

Movement time (ms)*** 664 (152) 1191 (499)Normalized jerk (units)** 31 (14) 87 (93)Mean acceleration (cm/s2)*** 239 (98) 104 (67)Index of straightness (%) 1.4 (0.008) 1.8 (0.01)Initial direction (deg)*** 0.9 (0.4) 2.3 (1.9)Length of primary submovement (% of total amplitude)** 95 (7) 65.5 (29)Trials with secondary submovements (% of total trials

within each condition)***19 34

* p�0.05, **p�0.01, ***p�0.001

Fig. 2 Examples of raw data traces and acceleration profiles for asingle trial from a PD patient (subject #6) and an age- and gender-matched elderly adult for the 1-s delay with vision, and the 10-sdelay without vision, conditions. Data between the vertical linesindicate primary submovement distance based on the accelerationprofiles

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(F(1,18)=13.39, p=0.002, h2=0.43), and had a greaternumber of trials with secondary submovements comparedto the elderly (c2=31.60, df=1, p<0.001).

Effects of delay

Delay affected the kinematics of the drawing movement(see Table 3). Movement time significantly lengthened asthe time delay increased (F(2,36)=5.34, p=0.009, h2=0.23),with the post hoc test indicating that the movement timeafter the 10-s delay was significantly greater than after the1-s delay. No significant interactions between delay andgroup were found for movement time.

Mean acceleration was significantly influenced bydelay (F(2,36)=22.26, p<0.001, h2=0.55), with the post hoctest indicating mean acceleration was significantly lessafter a 6-s or 10-s delay compared to the 1-s delaycondition. No interactions between delay and group formean acceleration reached significance.

Neither normalized jerk nor the index of straightnessof the overall movement was significantly influenced bydelay, p>0.10; however, there was a tendency for theinitial direction angle to increase with delay (F(2,36)=3.03,p=0.061, h2=0.14), indicating an increased deviation tothe right from a best-fit line. There was a trend for a delay� group interaction for initial direction (F(2,36)=2.56,p=0.09, h2=0.13), with the elderly maintaining initialdirection across delay, whereas the PD patients increasedinitial direction angle as a function of delay (see Fig. 3).

A main effect of delay was evident for the length of theprimary submovement (F(2,36)=8.81, p=0.001, h2=0.33),with a significantly decreased length after the 10-s delaycompared to the 1-s delay. Requiring the limb to remain

immobilized for a period of time prior to movement thusresulted in decreased distance of the primary submove-ment as a function of delay. A delay � group interactionwas also significant for length of the primary submove-ment (F(2,36)=3.89, p=0.030, h2=0.18) (see Fig. 3). Where-as the difference in primary submovement length betweengroups was not significant after a 1-s delay, the distancewas significantly different between groups in the 6- and10-s delay conditions, with decreased length for PDpatients and maintained length for elderly adults, acrossdelay.

The number of trials with secondary submovementswas significantly influenced by delay (c2=12.16, df=2,p<0.001); however, the delay � group interaction was notsignificant.

Effects of vision

The majority of dependent variables exhibited robusteffects of the vision manipulation (see Table 4). Occlud-ing vision of the limb produced a significant effect onmovement time, with increased movement times acrossgroups when vision was occluded compared to whenvision was available (F(1,18)=38.15, p<0.001, h2=0.68).Movement time also exhibited a vision � group interac-tion (F(1,18)=6.76, p=0.018, h2=0.27), with a post hoc testindicating that PD patients were significantly slower thanthe elderly both with and without vision.

Normalized jerk was significantly influenced by vision(F(1,18)=15.96, p=0.001, h2=0.47), with jerk score morethan doubling when vision was occluded compared to thevision available condition, indicating movements becameless smooth when vision was blocked. A vision � group

Table 3 Means (SDs) acrossgroups as a function of timedelay

Delay (s)

Dependent variable 1 6 10Movement time (ms)** 844 (458) 951 (466) 988 (431)Normalized jerk (units) 53 (95) 59 (60) 66 (55)Mean acceleration (cm/s2)*** 196 (113) 164 (99) 155 (109)Index of straightness (%) 1.6 (1.2) 1.7 (1.3) 1.5 (0.7)Initial direction (deg) 1.3 (1.2) 1.7 (1.6) 1.8 (1.7)Length of primary submovement (% of total

amplitude)***86 (21) 80 (27) 75 (28)

Trials with secondary submovements (% of totaltrials within each condition)***

20 28 30

* p�0.05, **p�0.01, ***p�0.001

Table 4 Means (SDs) acrossgroups as a function of vision

Dependent variable Vision No vision

Movement time (ms)*** 818 (338) 1037 (523)Normalized jerk (units)*** 38 (29) 80 (93)Mean acceleration (cm/s2)*** 185 (111) 158 (103)Index of straightness (%)*** 1.2 (0.7) 2.0 (1.3)Initial direction (deg)*** 1.0 (0.8) 2.1 (1.8)Length of primary submovement (% of total amplitude) 83 (24) 77.5 (27)Trials with secondary submovements (% of total trials

within each condition)***15 38

*p�0.05, **p�0.01, ***p�0.001

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interaction was also significant for normalized jerk(F(1,18)=6.68, p=0.019, h2=0.27) (see Fig. 4). The posthoc test indicated that whereas normalized jerk was notdifferent between groups when vision was available, PDpatients had significantly greater jerk scores than theelderly when vision was occluded. Furthermore, the jerkscores of the elderly did not differ between visionconditions in contrast to the PD patients, who demon-strated a significant increase in normalized jerk when

vision was occluded compared to the vision availablecondition.

Mean acceleration exhibited a main effect of vision(F(1,18)=60.90, p<0.001, h2=0.77), with less accelerationwhen vision was not available. Mean acceleration alsoexhibited a significant vision � group interaction(F(1,18)=8.83, p=0.008, h2=0.33), which was due to PDpatients showing less mean acceleration in both visionconditions compared to elderly adults. Furthermore, avision � delay � group interaction was also significant formean acceleration (F(2,36)=3.40, p=0.044, h2=0.16). Theinteraction was due to PD patients exhibiting significantlylower mean acceleration than the elderly in both visionconditions with the 1-s delay. In the 6-s delay conditions,a significant difference in mean acceleration was ob-served between groups only when vision was occluded,whereas after the 10-s delay a significant differencebetween groups was found only when vision wasavailable.

The index of straightness of the overall movement wassignificantly affected by vision (F(1,18)=21.13, p<0.001,h2=0.54), with a greater deviation from straightness whenvision was occluded compared to when vision wasavailable. A vision � group interaction was also signif-icant for the index of straightness (F(1,18)=8.10, p=0.011,h2=0.31) (see Fig. 4). The post hoc test indicated thatwhereas the index of straightness did not differ betweengroups when vision was available, when vision wasoccluded the difference between groups approachedsignificance (p=0.07). Furthermore, the change in theindex of straightness was not different between visionconditions for the elderly, but was significantly increasedin the no vision condition compared to the visioncondition for the PD patients.

The initial direction angle deviated significantly froma best-fit line without vision (F(1,18)=22.56, p<0.001,h2=0.56), with an increased angle to the right when visionwas occluded. A vision � group interaction was alsosignificant (F(1,18)=6.80, p=0.018, h2=0.27), with PDpatients exhibiting an increased angle to the right

Fig. 3 Dependent variables exhibiting Delay � Group interactions.The interaction for Initial direction approached significance. Errorbars represent the standard error of the mean. Asterisks betweenlines represent significant differences between groups

Fig. 4 Dependent variables ex-hibiting significant Vision �Group interactions. Error barsrepresent the standard error ofthe mean. Asterisks betweenlines represent significant dif-ferences between groups; as-terisks above the line representsignificant within group differ-ences between conditions

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compared to the elderly when vision was occluded;however, no differences in angle between groups werefound when vision was available (see Fig. 4). Further-more, the change in initial direction did not differbetween vision conditions for the elderly, but wassignificantly increased when vision was occluded com-pared to available for the PD patients.

The influence of vision on the length of the primarysubmovement approached significance (F(1,18)=4.25,p=0.054, h2=0.19), with an overall decrease of approxi-mately 1.1 cm when vision was occluded compared towhen vision was available. Vision did not differentiallyaffect the length of the primary submovement for eithergroup, as the vision � group interaction was not signif-icant.

The number of trials with secondary submovementssignificantly increased in the no vision condition com-pared to the full vision condition (c2=72.8, df=1,p<0.001), with the vision � group interaction alsosignificant (c2=10.55, df=1, p<0.01) (see Fig. 4).

Conclusions from Experiment One

Experiment One investigated the effects of increasing thetime spent remaining immobile in a static posture on thekinematics of point-to-point movements performed by PDpatients and elderly adults, and whether vision of the limbcould be used to compensate for the effects of delay. Theprimary finding was that remaining immobile for longerperiods negatively influenced the ability to make aimingmovements for both PD patients and elderly adults.Increasing delay impaired the ability of PD patients toexecute the portion of the movement believed to be undercentral control. Parkinsonian patients were differentiallyimpaired when vision of the limb was occluded comparedto elderly adults. Although performance was faster andmore consistent when vision was available, visual infor-mation was able to only partially compensate for theinformation lost as a result of increasing delay.

Discussion of results from Experiment One

The majority of dependent variables showed large maineffects of delay. Compared to the 1-s vision availablecondition, which can be considered as the baselinecondition, performance deteriorated as a function of timedelay across participants. It was predicted that delaywould primarily affect variables associated with move-ment planning, namely, initial direction, length of theprimary submovement, and the number of trials necessi-tating secondary submovements. The variables of move-ment time and mean acceleration, reflecting movementexecution, were also affected by delay, suggesting thedeterioration in position sense hinders the ability to planand execute an aiming movement.

Disease affected the performance of the movementtrajectory, as evidenced by the main effects of group.

Despite proprioceptive impairments (Jobst et al. 1997;Schneider et al. 1987), the variables associated withmovement execution, specifically, movement time, nor-malized jerk, mean acceleration and index of straightness,were affected in a similar manner for PD patients andelderly adults (Tresilian et al. 1997) as delay increased.These results indicate that although the execution of themovement was degraded for PD patients compared toelderly adults, the deterioration as a function of delay inPD patients paralleled that of the elderly.

Parkinsonian patients exhibited differences in thevariables reflecting movement planning, namely, differ-entially shorter primary submovements with a tendency toerr in initial movement direction compared to elderlyadults as a function delay. The most crucial variable wasthe amplitude of the primary submovement, whichreflects pre-planning of the task and is believed to beunder feedforward or central control (Meyer et al. 1988;Woodworth 1899). When delay was minimal, PD patientsand elderly adults demonstrated similar lengths of theprimary submovement. As delay increased, however, PDpatients were unable to maintain amplitude, in contrast toelderly adults. Delay thus appeared to affect the ability ofPD patients to plan the movement.

The majority of dependent variables demonstratedlarge effects of the vision manipulation. Across groups,occluding vision of the limb resulted in increasedmovement time and jerk scores, with a greater deviationfrom straightness, decreased acceleration, and a shorterprimary submovement distance that diverged in initialdirection. Results of the current study further support theestablished reliance on vision of PD patients (Denny-Brown 1962; Flash et al. 1992; Klockgether and Dichgans1994; Teulings et al. 1997) in that the performance of PDpatients was more impaired when vision was occludedthan that of elderly adults. Without vision of their limbprior to or during the movement, PD patients exhibitedjerkier and less straight movement trajectories withincreased directional error and movement time.

The majority of dependent variables demonstrate thatthe performance of PD patients with vision was verysimilar to the performance of elderly adults without vision(see Fig. 5). Pointing movements were consistently faster,straighter, with an increased ballistic distance for elderlyadults with vision; comparatively deteriorated for PD withvision and for elderly without vision, which were similar;and most impaired for PD patients without vision. Asvision of the limb has been suggested to be able tocalibrate position sense (Jeannerod 1988), thereby reduc-ing the effects of delay (Wann and Ibrahim 1992), it wasforecast that performance would not decrease as afunction of delay when vision of the limb was available.The vision � delay interactions that were predicted,however, were not found, indicating that althoughperformance across groups was better with vision thanwithout, vision could not completely substitute for theinformation lost as a result of adaptation to a staticposition. Additionally, the vision � delay � groupinteractions that were predicted if visual information

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could be used to compensate to a large extent for thedecreased position sense of PD patients were not found. Itmay be that providing vision of the target at all timesresulted in participants adopting a strategy such that theyfocused on the end target and did not use visualinformation of the moving limb. Participants may haveplanned the movements based on knowledge of the startand end targets when vision was available. In contrast,when vision was occluded, participants may have focusedon the end target position and began to monitor theirmovement once they saw the exposed pen tip close to theend target, at which point they guided the pen into thefinal target. To test this deduction, a second experimentwas conducted in which presentation of the end target wasremoved at movement onset both with and without visionof the movement trajectory, so that participants had todraw a line to a previously viewed target after a delayperiod.

Experiment Two

Results of previous studies utilizing a delay prior tomovement onset indicate that movements systematicallyundershoot the target as a function of increasing delay(Monster et al. 1973; Paillard and Brouchon 1968;Paillard and Stelmach 1996; Wann and Ibrahim 1992).It is unknown, however, whether inflicting a delay prior tomovement onset will result in undershooting of apreviously viewed target differentially for PD patientsand elderly adults. Based on the primary submovementresults of Experiment One, it is predicted that participantswill increasingly undershoot a previously viewed target asa function of increasing delay across groups. It is furtherpredicted that although PD patients will demonstrateincreased undershooting compared to elderly adults, theincreased undershooting as a function of delay will beparallel between groups. Since vision of the targetlocation is occluded at movement onset, it is predictedthat vision of the movement trajectory will reducemovement execution error.

Materials and methods

Participants

Twelve patients with idiopathic Parkinson’s disease (five female,seven male; mean age of 65 years, range 45–77 years) and 12 age-matched healthy adults (five female, seven male; mean age ofyears, range 48–75 years) participated in the experiment. None ofthe participants in Experiment One participated in ExperimentTwo. Three Parkinsonian patients were unmedicated and twopatients were tested while at the end of their medication cycle;these patients were considered in the “off” medicated state. SevenPD patients were tested while medicated and considered in the “on”medicated state. A summary of PD patients’ symptom profile anddisease severity is presented in Table 5. All control and PDparticipants were right-hand dominant, and had normal or correct-ed-to-normal vision. The experimental protocol was approved bythe Institutional Review Boards of Arizona State University and theMayo Clinic.

Apparatus and procedure

The equipment setup of Experiment Two was slightly different thanthat of Experiment One (Fig. 6). Participants were again asked toperform a point-to-point drawing task on a digitizer tablet using adigitizer pen. The digitizer was located in front of the participant’sright shoulder so that a straight linear movement required elbowextension as well as some shoulder flexion in the horizontal plane(see Fig. 7). A flat-screen computer monitor, on which targets andfeedback of the drawing movement were presented, was placed in ahorizontal position slightly to the left of the participant’s midline.In this way participants were able to view the targets and feedbackin the same plane as their movement. Three end targets of varyingamplitude from a single start target were used, resulting inamplitudes of 12 cm, 16 cm, and 20 cm. End targets were equally(five trials of each target) and randomly presented within eachvision � delay condition. Data were collapsed over end targets. Thestart target was 1.27 cm in diameter, and the end target was 0.79 cmin diameter.

A vertical shield was placed between the monitor and digitizerthat prevented vision of the participant’s forearm, hand, digitizer,and the movement trajectory. Vision of the task was manipulatedby presenting or not presenting feedback of the trajectory trace onthe computer monitor for the vision and no vision conditions,respectively. In the vision conditions, participants saw the start andend targets on the computer monitor during the entire delay period.In the no vision condition, the participant saw only the end targetduring the delay period. Upon an auditory “go” signal, the endtarget disappeared from the monitor in both vision conditions andthe participant drew a line to the previously viewed target. A real-time trace of the participant’s trajectory was presented in the visionconditions, whereas visual feedback was not provided in the visionoccluded conditions. To summarize the vision condition, prior tomovement participants saw the start and end targets for the entiredelay period. Upon movement initiation the end target wasextinguished and a trace of the movement trajectory relative tothe still present start target was shown. In the no visual feedbackcondition, prior to movement the participants saw only the endtarget for the delay period; the start target was not presented. Uponmovement initiation the end target was extinguished and partici-pants saw nothing on the computer screen. In both conditionsparticipants were instructed to draw a line as quickly and accuratelyto the previously viewed location of the end target.

Although many of the variables in Experiment One showedeffects of delay, we decided to increase the delay periods to 1 s, 7 s,and 13 s, to make the effects more apparent. The experimentermoved the participant’s forearm back to, and placed the pen within,the start target in all conditions. Once the pen was placed in thestart target, the participant was required to maintain the limb in astatic position until cued to begin the movement. Each vision(vision, no vision) by delay (1 s, 7 s, 13 s) condition was completed

Fig. 5 Illustration of the percentage of trials with secondarysubmovements as a function of vision � delay � group demon-strating the trend of many of the dependent variables

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as a block of 15 trials for a total of 90 trials. The six conditionblocks were presented in a randomized order determined by thecomputer program.

Data analysis

Parsing of the movement data was the same as in Experiment One.The dependent variables measured for the overall movement ofeach trial were: movement time; mean acceleration; radial error,T

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Fig. 6 The experimental setup of Experiment Two. Participantsperformed the drawing task on a digitizer that was placed in front ofthe participant’s right shoulder. A computer monitor was positionedin the horizontal plane in front of the participant on which visualfeedback was provided. A shield between the monitor and digitizerblocked vision of the participant’s limb, the targets, and movementtrajectory

Fig. 7 Final end position of the pen for each group at each vision �delay condition. The large black circle represents the target, whichwas not visible during the movement. Error bars represent thestandard error of the mean

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which was partitioned into error in the y-dimension (overshoots orundershoots), and error in the x-dimension (side to side errors).Movement time of the primary submovement, in addition to radial,y-dimension, and x-dimension, errors at the end of the primarysubmovement, were also measured and included as dependentvariables. Data analysis for Experiment Two was identical to thatperformed on the dependent variables for Experiment One.

Results

Initial analysis of patients in the “off” versus “on” medicated statewere conducted. No significant differences between “off” versus“on” were found for any of the dependent variables; thus patientdata was collapsed across medication state.

Movement time of the overall drawing task exhibited asignificant main effect of group, due to the mean movement timeof PD patients (1341 ms) being significantly slower than that ofelderly adults (937 ms) (F(1,22)=9.14, p=0.006, h2=0.29). Similarly,PD patients exhibited lower mean acceleration than elderly adults(F(1,22)=5.06, p=0.035, h2=0.19), with means of 60 cm/s2 and106 cm/s2, respectively.

A main effect of group approached significance for radial error,with increased radial error in PD patients compared to elderlyadults (F(1,22)=3.99, p=0.058, h2=0.15). This result was due to thetendency of PD patients to undershoot the target more than elderlyadults (F(1,22)=3.56, p=0.07, h2=0.14). No main effects of groupwere found for errors in the x-dimension (side to side errors) (seeFig. 7).

Movement time of the primary submovement portion of thedrawing task was not significantly different between PD patients(mean of 894 ms) and elderly adults (mean of 810 ms). Radial errorof the primary submovement, however, indicated that radial errorwas significantly increased in PD patients compared to elderlyadults (F(1,22)=9.88, p=0.005, h2=0.31). The difference in radialerror was due to PD patients significantly undershooting the targetin the primary submovement compared to elderly adults(F(1,22)=12.59, p=0.002, h2=0.36), as no group effects were foundfor side to side errors at the end of the primary submovement (seeFig. 8).

Effects of delay

Movement time demonstrated a main effect of delay (F(2,44)=9.24,p<0.001, h2=0.30), with means of 1063 ms, 1130 ms, and 1224 msfor the 1-s, 7-s, and 13-s delay conditions, respectively. Pairwisecomparisons indicated movement time was significantly increasedafter the 13-s delay compared to the 1-s delay. Mean accelerationalso demonstrated large effects of delay (F(2,44)=17.79, p<0.001,h2=0.45), with pairwise comparisons indicating mean accelerationsignificantly decreased across delay periods, with means of 95 cm/s2, 84 cm/s2, and 70 cm/s2, for the 1-s, 7-s, and 13-s delays,respectively.

Radial error was also significantly influenced by delay(F(2,44)=8.30, p=0.001, h2=0.27), with increased error after the 13-s delay compared to the 1-s delay (see Fig. 7). This result was dueto significantly greater undershooting of the target after the 7-s and13-s delay compared to the 1-s delay (F(2,44)=17.53, p<0.001,h2=0.44). No significant differences were found for errors in the x-dimension across delay.

Similar results were found for the primary submovementportion of the task. Primary submovement movement timeincreased across delay (F(2,44)=3.23, p=0.049, h2=0.13). Pairwisecomparisons did not yield any significant effects between delayperiods, although the difference in movement time between the 7-sand 13-s delay approached significance (p=0.06). Mean movementtimes of the primary submovement across groups were 827 ms,852 ms, and 878 ms, for the 1-s, 7-s, and 13-s delay, respectively.

Radial error of the primary submovement exhibited a maineffect of delay (F(2,44)=19.50, p<0.001, h2=0.47), with pairwisecomparisons indicating significantly increased error after the 7-s

and 13-s delay compared to the 1-s delay condition. This result wasdue to significantly increased undershooting of the target in theprimary submovement across delay (F(2,44)=27.43, p<0.001,h2=0.56) (see Fig. 8). Errors in the x-dimension were not affectedby delay.

Effects of vision

Movement time was significantly influenced by vision(F(1,22)=48.07, p<0.001, h2=0.69). In contrast to Experiment One,movement time was increased when visual feedback was available(mean of 1317 ms) compared to when it was occluded (mean of961 ms). A significant vision � group interaction was also evidentfor movement time (F(1,22)=4.66, p=0.04, h2=0.18), which was dueto PD patients having significantly increased movement times inboth vision conditions compared to elderly adults. Additionally,both elderly adults and PD patients exhibited significantlyincreased within group movement times in the vision conditioncompared to when feedback was not available.

Mean acceleration demonstrated a significant main effect ofvision, with mean acceleration decreased when visual feedback wasavailable (77 cm/s2) compared to when it was occluded (89 cm/s2)(F(1,22)=4.57, p=0.044, h2=0.17). No interactions with mean accel-eration were evident.

Across groups, radial error was significantly increased withoutvisual feedback compared to the feedback condition (F(1,22)=51.00,p<0.001, h2=0.70). Radial error also exhibited a significant vision �delay interaction (F(2,44)=6.96, p=0.002, h2=0.24). The post hoc testrevealed that error was significantly increased without feedbackcompared to with visual feedback after the 7-s and 13-s delays (seeFig. 7). The increase in radial error was due to greater errors in boththe y-dimension (F(1,22)=95.15, p<0.001, h2=0.81) and the x-dimension (F(1,22)=12.10, p=0.002, h2=0.36) when feedback wasoccluded. Thus end position of the drawing task undershot thetarget in addition to deviating to the left in the no feedbackconditions. A vision � delay interaction proved to be significant forerrors in the y-dimension (F(12,67), p<0.001, h2=0.36) and ap-proached significance for errors in the x-dimension (F(1,22)=2.95,

Fig. 8 Pen position at the end of the primary submovement foreach group at each vision � delay condition. The large black circlerepresents the target, which was not visible during the movement.Error bars represent the standard error of the mean

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p=0.063, h2=0.12). The target was significantly undershot whenfeedback was occluded compared to when it was available at eachdelay interval. A similar trend was found for side-to-side errors, inthat without visual feedback, greater deviation to the left was foundcompared to when feedback was available.

Movement time of the primary submovement was increasedwhen vision was available (mean of 906 ms) compared to occluded(mean of 797 ms; F(1,22)=21.53, p<0.001, h2=0.50); however, nointeractions proved to be significant. Similar to the main effects ofvision found for the overall movement, radial error (F(1,22)=33.50,p<0.001, h2=0.60), y-dimension error (F(1,22)=36.99, p<0.001,h2=0.63), and x-dimension error (F(1,22)=9.18, p=0.006, h2=0.29)exhibited increased error for the position at the end of the primarysubmovement without vision. Increased undershooting and devia-tion to the left accounted for the augmented radial error when visualfeedback was occluded. A vision � delay � group interaction forerror in the y-dimension at the end of the primary submovementproved to be significant (F(2,44)=5.17, p=0.01, h2=0.19) (see Fig. 8).Post hoc analysis indicated that at the 1-s delay, elderly with visualfeedback were significantly closer to the target than the position ofPD patients without feedback. At the 7-s delay, elderly withfeedback were significantly closer to the target than the position ofPD patients both with and without visual feedback. At the 13-sdelay, elderly with visual feedback were significantly closer to thetarget than PD patients both with and without feedback, as well aselderly without feedback.

Conclusions from Experiment Two

Experiment Two extended the findings of Experiment One byinvestigating the effects of delay on the accuracy of drawingmovements to a previously viewed target performed by PD patientsand elderly adults. Consistent with the findings of Experiment Oneand previous research, the primary finding was that remainingimmobile for longer periods resulted in a systematic undershootingof the target for both PD patients and elderly adults. Increasingdelay and removing visual feedback impaired the ability of PDpatients to plan and execute the portion of the movement believedto be under central control. In contrast to the results of ExperimentOne, visual feedback of the trajectory could be used to compensatefor the information lost as a result of increasing delay acrossgroups.

Time delay hinders the ability to make accurate aiming movements

In both Experiments One and Two, movement time increased as afunction of increasing delay across participants. Parkinsonianpatients exhibited prolonged movements overall, but were notdifferentially slower as a function of delay compared to elderlyadults. In both experiments, variables reflecting movement execu-tion, namely, normalized jerk, mean acceleration, index ofstraightness, and overall radial error, also showed parallel effectsbetween groups as a function of delay. The one variable thatexhibited a three-way interaction, mean acceleration in the firstexperiment, was possibly due to PD patients exhibiting a flooreffect across delay, whereas the elderly adults were able to maintainmean acceleration from the 6-s to the 10-s delay when vision wasavailable. This result was not repeated in Experiment Two,however, in which only main effects of group and delay werefound for mean acceleration.

Accuracy exhibited large main effects of delay. The resultsreplicated previous research (Monster et al. 1973; Paillard andBrouchon 1968; Paillard and Stelmach 1996; Wann and Ibrahim1992) in that increasing the delay prior to movement onset resultedin a systematic undershooting of the target when visual feedbackwas occluded. Although PD patients exhibited greater undershoot-ing of the target overall, elderly adults demonstrated comparativelylarger undershooting of the target as a function of delay whenfeedback was blocked. These results may be considered consistentwith those of Rickards and Cody (1997), who disrupted the

proprioception of PD patients and elderly adults. Their resultsdemonstrated that the undershooting between the disrupted andnon-disrupted proprioception conditions did not differ for PDpatients as much as for elderly adults. They concluded that PDpatients do not utilize proprioceptive information to the same extentas healthy adults; thus they are not as impaired when proprioceptionis diminished or disrupted. The current results also support thisinterpretation.

Delay resulted in impairments in the variables associated withmovement planning for PD patients in both experiments. Thecrucial variable reflecting planning, amplitude of the primarysubmovement, was reduced in PD patients and became shorter withincreasing delay, suggesting that the ability to plan the portion ofthe movement under central control is impaired.

Position sense has been suggested to involve both central andperipheral components (McCloskey 1978; Monster et al. 1973). Atthe peripheral level, muscle spindles are now acknowledged to bethe sensory receptors involved in perception of position andproprioception (Clark et al. 1985; Clark and Horch 1986;McCloskey 1978; Proske et al. 2000). Muscle spindle activationhas been found to be normal in PD patients (Burke et al. 1977); thuscentral mechanisms are believed to be the source of impairedproprioception in PD patients (Moore 1987; Schneider andRoeltgen 1993). It was initially proposed that PD produces amismatch of motor (i.e., corollary discharge) and afferent sensoryinformation, although which aspect is impaired was unclear (Moore1987). More recent research disclosed that PD patients exhibithypometric amplitudes of both active and passive limb movements,suggesting corollary discharge is normal in PD patients; thus thedecreased proprioception found with PD is due to impairedintegration of sensorimotor information at the central level(Klockgether et al. 1995; Schneider and Roeltgen 1993). Support-ing this position is the suggestion that basal ganglia dysfunctionproduces impairments in integration between sensory modalities(Teuber and Proctor 1964). It was predicted that the kinematics of apointing movement would reflect the decay in position sense overtime due to reduced sensory information available for movementplanning at the central level. The current results support this notionand imply that reduced position sense impeded the ability of bothPD patients and elderly adults to construct and execute trajectoryparameters, with PD patients exhibiting impairments in planning asa function of delay.

Visual information is used to compensate for the effects of delay

Vision of the movement trajectory had opposite results onmovement time between Experiments One and Two. Whereasduration increased without vision in Experiment One, it increasedwith vision in Experiment Two. In Experiment One, vision of theend target was always available, with the requirement that themovement had to terminate within the target. In contrast, vision ofthe end target was removed in Experiment Two, with participantssignificantly undershooting the target when vision was occluded,which may account for the reduced movement times in this case.

In contrast to the results of Experiment One, visual feedback ofthe movement trajectory could be used to compensate to some extentfor the effects of delay in Experiment Two. A vision � delay � groupinteraction for the end position after the primary submovement wasdue to the highly accurate end position of the elderly when visualfeedback was available differing from the end position of PD patientsand the elderly without feedback, as delay increased. Although bothgroups continued to move toward the target after the primarysubmovement, PD patients used visual information to bring theirfinal position substantially closer to the previously viewed target,demonstrating that visual feedback was used to compensate for theeffects of delay. This outcome resulted in a vision � delay interactionfor the final end position so that when visual feedback was available,target accuracy did not differ across delay between groups, furtherconfirming the reliance of PD patients on vision. When visualfeedback was occluded, however, both groups exhibited substantialundershooting of the target as a function of delay.

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In both Experiments One and Two, vision of end target wasprovided throughout the delay period prior to movement onset.Visual representations of a target have been found to deterioraterather rapidly with delays greater than 2 s (Elliot and Madalena1987). We therefore utilized the current protocol to control for anydecay in visual representation or memory of target position betweengroups. It was proposed that when vision of the end target wasavailable, participants were focusing on the end target and notprimarily utilizing visual information of the moving limb to guidetheir movements. Although we cannot ascertain exactly whatparticipants were visually focusing on during the task, results ofExperiment Two suggest that they were using the feedback trace tomonitor their movements when end target position was not available.The results further demonstrate that as delay increased, the primarysubmovement phase (thought to be under central control) becameshorter; thus participants spent a larger part of the movement underfeedback control to compensate for the effects of delay.

General discussion

The combined results of Experiments One and Twoindicated that imposing a delay prior to movement onsetchanges the kinematics and accuracy of a point-to-pointdrawing task in a similar manner for both elderly adultsand PD patients. Although PD patients performed the taskslower and with less accuracy at all delay periods, thechanges in execution due to delay were parallel betweenthe groups.

The initial studies involving a time delay prior tomovement onset were conducted by Paillard and Brou-chon (1968), who imposed a range of delay from 0 to 12 sand found that limb position matching became increas-ingly hypometric as a function of delay. Similar resultshave been consistently demonstrated, with the mechanismof the decrease in position sense over time suggested to bedue to the decline in sensory receptor activity to amaintained, static position (Clark and Horch 1986).Muscle spindles, which provide proprioceptive informa-tion (Clark et al. 1985), have been found to reduce theirfiring activity over time when the limb remains in a staticposition, thereby reducing the information available as tothe limb’s posture (for reviews see Clark and Horch 1986;McCloskey 1978). Supporting such an interpretation,Paillard and Stelmach (1996) documented that keepingthe hand and index finger immobile for up to 12 simpaired the ability to localize it in space. Such losseswere minimized by actively stimulating the fingertip,which heightened the available afferent information. Itwas expected that as sensory receptors adapt duringimmobilization, reduced position sense informationwould result in a decreased ability to incorporate theinitial limb position into motor planning processes. Thisprediction was supported by the changes in kinematic andaccuracy measures as a function of delay; moreover, PDpatients exhibited impairments in planning the full lengthof the movement as compared to elderly adults.

In Experiment One, the final end target was alwaysvisible, which may have accounted for the inability ofvisual information to compensate for the effects of delay.Participants may have used the strategy of moving in amanner so that they were able to terminate the task as

soon as they saw the pen within the target across delayperiods. In contrast, Experiment Two demonstrated thatvisual feedback of the trajectory trace was used tocompensate for the effects of delay, and removal of allvisual information resulted in deteriorated accuracy as afunction of delay for both groups.

The importance of vision on movement control oraiming accuracy has been well established in both healthy(Gentilucci et al. 1997; Jeannerod and Prablanc 1983;Neggers and Bekkering 1999; Prablanc et al. 1979;Vercher et al. 1994) and diseased populations (Flash et al.1992; Ghez et al. 1995; Gordon et al. 1995; Klockgetherand Dichgans 1994). Previous research has demonstratedthat viewing the initial limb position significantlyimproves aiming accuracy, even when vision of themovement trajectory is blocked (Desmurget et al. 1995,1997; Jeannerod and Prablanc 1983; Rossetti et al. 1994).It has been suggested that the initial cues of body andhand position, as well as target position, are importantsources of information that allow for better motorencoding of the movement (Prablanc et al. 1979). Morespecifically, encoding of the initial hand position fromcombined visual and proprioceptive (bimodal) modalitiesenhances the ability to plan goal-directed movementscompared to proprioceptive (unimodal) encoding alone(Desmurget et al. 1997; van Beers et al. 1996, 1999).Similarly, Ghez and colleagues (1995; Gordon et al.1995) have proposed that vision of the limb is used for theformation and/or updating of the internal model of thelimb, allowing for a more precise motor plan. Supportingthis notion, results of the present experiments demonstratethat occluding vision of the hand and movement pathproduced increased trajectory irregularity and undershoot-ing of the target across groups.

Summary

The current paper is the first to investigate the effects ofimmobilization over time on the drawing performance ofPD patients and elderly adults, and to further examine theintegration of visual and proprioceptive modalities. Twoexperiments demonstrated that PD patients were similarlyaffected by delay as elderly adults. When end targetlocation was visible, visual information was not able tolimit the effects of delay. When participants had to moveto a previously viewed target, visual feedback of themovement trajectory was used to compensate for theeffects of delay. It can be inferred from the results that thereduction in position sense as a function of time createsdifficulty in incorporating the initial limb position inmotor planning process, resulting in kinematic changes inthe execution of an aiming movement.

Acknowledgements Special thanks are due to Kristy Kelly for herassistance in data collection. This research was funded by NINDS33173 and AG 14676. Portions of the results were previouslypublished in abstract form (Romero et al. 2000, 2001).

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