Introduction

The perception of limb motion is considered part ofthe kinaesthetic or muscle sense. In general bothterms, muscle sense or kinaesthesia, refer to percep-tion of self-position and movement. The still-defini-

tive work by Goldscheider [8] distinguishes fourdifferent properties of kinaesthesia: limb positionsense, passive motion sense, active motion sense andgravito-inertial sense. This classification provides anexcellent roadmap to investigate the various aspectsof kinaesthetic function or dysfunction.

Jurgen KonczakKimberly KrawczewskiPaul TuiteMatthias Maschke

The perception of passive motionin Parkinson’s disease

Received: 21 April 2006Received in revised form: 21 September2006Accepted: 2 October 2006Published online: 10 April 2007

j Abstract The perception oflimb motion is a kinaestheticproperty that is essential for vol-untary motor control. This studyexamined the ability of patientswith Parkinson’s disease (PD) todetect the velocity of a passivelymoved limb. Eight patients withmild to moderate PD and eightage-matched healthy controlsparticipated. They placed theirforearm on a padded splint of apassive motion apparatus, whichhorizontally extended or flexed theelbow joint at velocities between1.65 and 0.075�/s (in steps of0.15�/s). Passive movement per-sisted until subjects detected armmotion and pressed a trigger heldin the hand of their non-testedarm. Time until detection andassociated arm displacement wererecorded and subsequently ad-justed for each subject’s reactiontime. We found that PD patientsneeded significantly larger limbdisplacements before they couldjudge the presence of passivemotion. With decreasing passivemotion velocity the detection timeincreased exponentially in both

groups. Yet, the mean detectiontimes of the PD group were 92–166% higher than in the controlgroup for each of the 12 testedvelocity conditions. Five of theeight patients were on Parkinso-nian medication when tested. Yet,the degree of impairment in thePD group did not correlate sig-nificantly with the patients’ levo-dopa equivalent dosage. Ourresults demonstrate that PD pa-tients were impaired in the detec-tion of passive forearmmovements. This study comple-ments a growing body of evidenceindicating that various aspects ofkinaesthesis (position sense,weight perception, passive motionsense) are affected even at earlystages of PD. The impaired pro-cessing of proprioceptive signalslikely contributes to motor symp-toms in PD.

j Key words kinaesthesis Æmotor control Æ proprioception Æperception Æ sensorimotor

ORIGINAL COMMUNICATION

J. Konczak (&) Æ K. KrawczewskiM. MaschkeHuman Sensorimotor Control LabUniversity of Minnesota400 Cooke Hall1900 University Ave. S.E.MN 55414, USATel.: +1-612/6244370Fax: +1-612/6241314E-Mail: jkonczak@umn.edu

P. Tuite Æ J. Konczak Æ K. KrawczewskiDept. of NeurologyUniversity of MinnesotaMinnesota, USA

M. MaschkeDept. of NeurologyUniversity of Duisburg-EssenDuisburg-Essen, Germany

J Neurol (2007) 254:655–663DOI 10.1007/s00415-006-0426-2

The current study is part of a series of recent workexamining kinaesthetic deficits in patients with Par-kinson’s disease (PD). For some time, it has beensuggested that PD patients have impaired limb pro-prioception. Specifically, they are believed to haveproblems integrating proprioceptive or multimodalinformation [1, 19, 21]. This could explain why PDpatients perform poorly in matching proprioceptivelyperceived limb positions to a visual reference [25].However, results from psychophysical studies indicatethat the proprioceptive dysfunction in PD may arise,because patients cannot adequately detect and dis-criminate proprioceptive stimuli. For example, recentfindings documented that the discrimination betweenneighboring forearm positions is impaired in PD [24].Results from our own work on limb position sense[15, 17] showed that PD patients have elevatedthresholds for detecting limb position. While healthycontrols reliably detected a shift in forearm positionat excursions above 1�, patients with mild to moder-ate PD required limb displacements of 2–6� beforethey detected a change in limb position. Deep brainstimulation (DBS) of the subthalamic nucleus im-proved detection thresholds in more severely affectedPD patients, but it did not fully restore kinaestheticfunction [17]. These psychophysical results corre-spond well with neurophysiological findings thatshowed altered proprioception-related EEG potentialsin PD patients during passive movements [22]. Theyare further corroborated by behavioral research,which demonstrated that in the absence of vision PDpatients consistently make hypometric pointingmovements to external targets [11].

This experiment was designed to examine whetherPD patients require larger forearm displacementsbefore detecting motion. In contrast to findingdetection thresholds for limb position, passive motionthresholds are not unique, because they depend onthe amount of limb displacement. That is, at smallexcursions (<1–2�) humans may have difficulty todetect motion, while at larger excursions the samevelocities are reliably detected. To map velocitythresholds over a range of displacements, one ideallytests various velocities at a constant displacement andthen repeats testing at other displacements. Theproblem with this approach is that it requires a largenumber of trials to fully map velocity–displacementspace. Hence, the procedure becomes tedious leadingto a deterioration of performance, which ultimatelyresults in unreliable data. Knowing that selectiveattention might be compromised in PD patients, wetherefore designed an experiment, where the dis-placement was not kept constant, but determined byeach subject’s perception of passive motion. Thisparadigm has been shown to yield-reliable and validdata in the past [7].

Methods

j Subjects

Eight PD patients (mean ± SD age 54.0 ± 6.2 years, 4 females, 4males) and eight age-matched healthy control subjects (mean ± SDage 53.6 ± 5.3 years, 5 females, 3 males) with no neurological orgeneral medical limitations participated. PD patients were recruitedfrom the movement disorders outpatient clinic at the University ofMinnesota. All were diagnosed as having idiopathic PD. No cog-nitive decline other than mild forgetfulness was observed accordingto clinical assessment and the results of each patient’s Mini MentalState Examination (MMSE) and the Unified Parkinson’s DiseaseRating Scale (UPDRS) part I. Executive function was assessed usingthe Tower of Hanoi task with three disks, which showed the PDgroup’s performance to be within the normal range (PD:mean ± SD 9.4 ± 6.3; Controls: mean ± SD 9.4 ± 2.9). Neurologi-cal examination did not show signs or symptoms of peripheralnerve disorders (vibration sense, light touch, pinprick sensation,and assessment of position sense at index finger and first toe werenormal). Five of the eight patients were tested on medication, i.e.,they took their antiparkinsonian medication in their usual dose andtime schedule. Two patients were not taking any antiparkinsonianmedication. A third patient was taking solely amantadine at thetime of testing. All patients and healthy subjects gave their in-formed consent to participate in the study. The study was approvedby the Institutional Review Board of the University of Minnesota(patient characteristics are described in Table 1).

j Apparatus

Participants placed their forearm on a padded splint that wasmoved passively by a torque engine (see Fig. 1). The apparatuscould generate movement speeds as low as 0.06�/s and as fast as8�/s. The range of angular displacement was 0.0098�–12� forextension or flexion. For the metacarpophalangeal joint it is knownthat humans can detect small excursions (<3.5�) at speeds above0.03�/s [3]. For the elbow joint, our own pilot data showed that foryoung, healthy subjects (N = 10), limb velocities below 0.075�/swere not perceptible for excursions below 0.8–1�.

j Procedure

The forearm was moved passively until subjects detected armmotion and pressed a trigger held in the hand of their non-testedarm. The trigger signal shut off the torque engine and motion ofthe apparatus ceased. Subjects then indicated verbally the per-ceived direction of limb motion by stating ‘‘away’’ or ‘‘toward’’ –indicating elbow flexion or extension, respectively. Afterwards theexperimenter recorded the angular displacement of the arm(accuracy of display: 0.001�) and the subject’s verbal judgment.The maximal possible displacement in a trial was 8�. If the subjecthad not stopped the forearm motion by 8� by using the trigger,the apparatus turned itself off. This upper displacement limit waschosen to control for a loss of concentration and frustration, ifparticipants could not detect any motion within a reasonableamount of time. Our own data [15, 17] indicated that mild tomoderately impaired PD patients reliably detect changes in limbposition at displacements beyond 6�. That is, an 8� displacementwas considered to be a conservative boundary to terminate a trialgiven the expected degree of impairment of the patient group.Starting position was at an elbow joint angle of 90� flexion.Angular velocities were presented using a staircase procedure[23]. Two staircases were employed (ascending from 0.075�/s,descending from 1.65�/s in steps of 0.15�/s). Both staircase

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procedures were intertwined meaning that trials from each stair-case were presented pseudorandomly. If a subject failed to cor-rectly detect the direction of motion, the trial was repeated toassure that the initial judgment was not due to a lack of attention.Failures to detect motion direction became an issue at lowvelocities (<0.45�/s). The additional repeated measures at theselow velocities provided information about the reliability of theirjudgments (i.e., whether they were guessing). During testingsubjects wore goggles to exclude all visual input of the arm. Theelectric motor of the apparatus did not produce any audible noiseor vibrations that could have been used as cues by the subject todetect the onset of motion. A minimum of 72 trials wereadministered. Possible myoelectric activity of the biceps and

triceps muscles was monitored online using standard surfaceelectromyography sampled at 200 Hz. If the experimenter de-tected muscle activation, the trial was repeated.

Pilot testing had revealed that healthy young subjects exhibiteda loss of concentration and made erratic judgments after prolongedtesting (>60 min). This time restraint prevented us from examiningboth arms, allowing only the testing of the patient’s more affectedarm. However, 1 out of 8 patients revealed substantial resting tre-mor in the more affected arm. In this patient, we tested the lessaffected arm. All other patients did not have moderate or severetremor that could have affected performance during testing. Eachmatched control subject was tested on the same side as therespective patient. The whole experimental procedure lastedapproximately 120 min including breaks, neuropsychological test-ing and clinical examination.

j Control experiment (reaction time measurement)

All participants were required to press a trigger switch after theydetected motion. Thus, differences in reaction time might haveinfluenced the degree of angular displacement: the torque enginedid not stop until the switch was pressed. Knowing that PD patientsmight have had longer reaction times than controls, their angulardisplacements could be larger, simply because they might takelonger to react. We therefore employed a standard simple reactiontime paradigm to obtain a measure of each participant’s reactiontime. Participants pressed a button to an auditory tone. Ten trialsfor each subject were recorded. Inter-trial intervals were between 5and 15 seconds. The analog signal from the trigger button wassampled at 200 Hz, which translates into a temporal resolution of5 ms. For each individual the average reaction time over the 10trials was computed and used for further analysis.

j Measurements

We recorded four measurements: verbal judgments about per-ceived limb motion, velocity of the passive motion apparatus (xi),angular displacement associated with the judgment (hi), and aver-age simple reaction time (RT). To achieve an accurate measure ofdisplacement, we computed the gross movement time (start to stopof engine) and subtracted each subject’s RT from it. This compu-tation insured that time-to-judgment and the associated displace-ment value were not inflated in subjects, who had longer reactiontimes. We here refer to this variable as detection time (DT) and tothe corresponding splint position as adjusted angular displacement(hadj).

Fig. 1 Experimental set-up. In patients, the more affected arm was tested.Subjects pressed a button switch in the hand of their non-tested arm to stoppassive motion as soon as they detected limb motion. Electrodes for monitoringmyoelectric activity are not shown

Table 1 Patient characteristics

ID Sex Age(years)

Disease duration(years)

Handednessa UPDRS total(max. 192)

UPDRS III(motor) (max. 108)

MMSE L-dopa equiv.Dose (mg/diem)

Medication

1 m 51 7 20 28 15 30 500 PH, C-Dp2 f 49 8 17 34 16 26 1600 C-Dp3 f 67 4 19 41 29 29 0 None4 m 54 4 20 28 19 30 0 AH5 m 47 5 20 29 21 29 100 PH6 f 58 8 20 49 29 29 1000 Dp7 f 53 6 20 18 11 28 100 Ro8 m 53 3 20 27 17 28 0 None

m = male, f = femaleaAccording to the Edinburgh Handedness Score (range 20 (right handed) to )20 (left handed)) UPDRS score = Unified Parkinson’s Disease Rating Scale (total score:range 0–192, the higher the score, the more severe the disease); Medication: C-Dp = Carbidopa/Levodopa, AH = amantadine hydrochloride, PH = pramipexolehydrochloride, Ro = ropinirole; Levodopa equivalent dose = 100 mg standard levodopa equals 125 mg sustained-release levodopa, 1.5 mg pramipexole, 6 mgropinirole, 10 mg bromocriptine or 1 mg pergolide

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j Statistical analysis

Data analysis was performed using customized algorithms based onthe MATLAB technical programming language. Since the detectiontime decreased exponentially with increasing angular speed, wefitted an exponential decay function to the DT and x data sets ofeach participant:

DT ¼Yscale � Xshift ðx�XshiftÞp

where Yscale, Xshift, and the exponent p were estimated. In essence,the Yscale factor scales the function values along the y-axis. It thusprovides a measure of the ‘‘steepness’’ of curve. With respect tomotion detection, a large Yscale value implies that the sensitivitydecreases earlier (at relatively high velocities) and that responsevariability increases at low velocities.

For the group comparisons and correlation analysis we as-sumed an initial level of significance of a = 0.05, which was ad-justed for multiple testing using the Bonferroni method.

Results

The mean reaction time for the PD patient group wassignificantly higher when compared to the controlgroup (PD: mean ± SD 288 ± 49 ms; controls:mean ± SD 213 ± 32 ms; p < 0.001). Thus, slowerreaction times could have impacted the measuredforearm displacement values as well as the totalmovement time (time-to-judgment). In order to ac-count for these group differences in RT, we here re-port only kinematic variables that were adjusted forRT. The first two parts of the analysis will focus on therelationship between movement direction, displace-ment and passive motion perception, while the thirdpart presents data on the temporal aspect of motionsense, i.e., how long it took before movement wasdetected.

j Judging the direction of motion

The ability of PD patients to detect the direction ofmotion was not impaired. The average failure rate todetect motion direction was less than 3% for bothgroups (controls: mean 2.2% – range 0.0–6.5%; PD:mean 2.5% – range 0.0–7.7%). Three PD patients andfour control participants made no errors in judgingmotion direction. The observed errors occurred pri-marily during the two lowest velocity conditions(0.075 and 0.15�/second).

j Displacement until detection

Analysis of adjusted angular displacement data (hadj)revealed that, in general, PD patients needed largerlimb displacements before they could judge thepresence of passive motion (see Figs. 2, 3). Thisimpression is corroborated by the results of a 2Groups · 12 Velocities Analysis of Variance on hadj,which yielded significant main effects for Group(p < 0.0001) and Velocity (p < 0.0002). The interac-tion term failed to reach significance (p = 0.58). Inaddition, the displacement–velocity sensitivity func-tions in Fig. 2 showed that the mean offsets in dis-placement (differences from 0�) between the twogroups were significantly different (controls:0.24� ± 0.38�; PD: 0.66� ± 0.48�; p < 0.001).

It is known that the forearm position detectionthresholds are approximately 1� for healthy controlsand 2� for mildly to moderately affected PD patients[15]. These thresholds are indicated as dashed hori-zontal lines in Fig. 2 to illustrate that values below

Fig. 2 Adjusted angular displacement as a functionof passive motion velocity. Data points representsubject means for a respective velocity condition.Dashed horizontal line indicates approximate limbposition detection threshold for each group. Anexponential decay function of the formy = A1*exp()x/t1) + y0 was fitted to each data set

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these lines were likely based on the perception of limbvelocity, while values above indicate that judgmentswere both the result of perceiving limb velocity as wellas a difference in limb position. Displacements be-yond 1� were observed in 12.5% of all trials of thecontrol group. In the PD group, 44.7% of all trials haddisplacements >1� and exceeded 2� in 15.9% of trials.The data in Fig. 3 illustrate that performance of bothgroups was essentially stable for velocities rangingfrom 1.65 to 0.9�/second and began to regress atvelocities lower than 0.9�/second. At these lowervelocities the displacement values became more var-iable and increased almost linearly in the PD group.

j Time until detection

With decreasing passive motion velocity, the detec-tion time increased exponentially in both groups.However, the mean detection times of the PD groupfor each of the 12 velocity conditions were between 92and 166% higher than in the control group (PD grouprange: 0.56–31.81 seconds; control group range: 0.29–

11.94 seconds; see Table 2 for all mean values). A 2Groups · 12 Velocities Analysis of Variance on DTyielded significant main effects for Group(p < 0.0001) and Velocity (p < 0.001), while theinteraction was not significant.

For each subject we fitted sensitivity functionsbased on their individual detection times. The per-formance of the PD patients was characterized bygenerally elevated detection times, which were ex-pressed in the sensitivity function by the higher Yscale

(the Yscale factor provides a measure of the ‘‘steep-ness’’ of the curve). For the PD group the mean Yscale

value was 4.81 (SD: 9.18), while it was 0.89 (SD: 0.62)for the control group (p < 0.0001). However, a closerlook at sensitivity functions for each patient show thatthe sensitivity functions of three patients (ID# 2, 7, 8)fell inside the range of the control group at velocitiessmaller than 0.45�/second (see Fig. 4). Patient #5exhibited the lowest sensitivity to motion (highestcurve in Fig. 4).

j Correlation with clinical scores and medication

We computed Pearson product–moment correlationsto examine the associations between L-dopa equiva-lent dosage, the UPDRS total score and the UPDRSmotor score with mean hadj. When considering thedisplacement values for the three lowest velocityconditions (0.075, 0.15, 0.3�/second), we found thatthe UPDRS motor score correlated significantly with

Fig. 3 Distribution of the adjusted angulardisplacement values as a function of passive motionvelocity. Lower whisker indicates 5th percentile, upperwhisker 95th percentile, horizontal line within boxindicates the median and the small square indicatesthe mean

Table 2 Mean detection times for each velocity condition

Velocity 0.1 0.2 0.3 0.5 0.6 0.8 0.9 1.1 1.2 1.4 1.5 1.65Control 11.9 4.96 2.88 1.7 1.07 0.78 0.58 0.48 0.36 0.30 0.27 0.29PD 31.8 11.9 5.69 3.64 2.45 1.72 1.33 0.84 0.79 0.62 0.56 0.56

Units are seconds. Velocity units are deg/s

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hadj (r = 0.63, p = 0.0026) for seven out of eight pa-tients. The respective correlation between UPDRSmotor score and hadj was computed as r = 0.56(p = 0.0083). The eighth patient (No. 3), who had oneof the largest UPDRS motor scores and the secondhighest UPDRS total score, performed within therange of controls (see Fig. 5).

We looked for reasons why this patient had per-formed so well. Since this patient had taken nomedication, we investigated whether L-dopa equiva-lent dosage correlated significantly with hadj. Thiscorrelation was computed as r = 0.41, and did notreach the level of significance. A closer look at therelationship between levodopa intake and displace-ment-until detection yielded somewhat inconsistentresults. The patient with the highest levodopa equiv-alent dosage (1600 mg) exhibited passive motionsensitivity within the normal range. In turn, two pa-tients with no or only a small levodopa equivalentdosage (100 mg) revealed the lowest sensitivity formotion detection. Two of the three patients who werenot under levodopa medication at the time of testingshowed elevated thresholds while the third patientperformed within the range of the control group.

Discussion

This study examined the ability of patients with mildto moderate Parkinson’s disease to detect the velocityof a passively moved limb. The ability to sense passivemotion is one of the four components of kinaesthesia,

next to the limb position, active motion and gravito-inertial senses [8]. Our main finding is that thedetection of passive motion is impaired in PD. Thisdeficit may affect patients even at early stages of theirdisease. To appreciate the implications of impairedkinaesthesia for motor function in PD, we will firstdiscuss the nature of the perceptual judgments thatwere required in this experiment.

j What aspects of kinaesthesia were measured?

Inherently, limb motion is associated with a change inlimb position. That is, these two aspects of kinaes-thesia, limb motion and limb position sense, arecoupled during most movements of appreciable dis-placement. While responses from Golgi tendon or-gans and dynamic muscle spindle fibres providevelocity and acceleration (tension) signals, staticmuscle spindle fibres and joint receptors encodepositional information. With respect to motionaround the elbow joint, it is known that the forearmposition detection thresholds are approximately 1� forhealthy controls and 2� for mildly to moderately af-fected PD patients [8, 15]. Below these positionthresholds, the perception of motion is primarilybased on responses from Golgi tendon organs and thedynamic muscle spindle fibres. In contrast, thedetection of motion above limb position thresholdsimplies that perceptual judgments about the move-ment of a limb can also be influenced by positionalsignals. In the extreme case one may not feel the limbmoving, but recognizes that the limb was displaced.

In this experiment, we applied movement velocitiesthat one would consider to be extremely slow (e.g., atthe slowest velocity of 0.075�/second it took 13 sec-onds to move 1�). The task required a perceptualjudgment about the direction of motion, which bothgroups judged correctly in approximately 97% oftrials. With respect to limb motion, our results showthat when both groups had to make perceptualjudgments at velocities between 1.65 and 0.9�/second,their associated limb displacements were well belowthe known position thresholds of both groups. Thisclearly indicated that positional information playedlittle to no role in perceiving forearm motion at thesevelocities (see Fig. 2). At velocities slower than 0.9�/second all subjects required more time and largerdisplacements to perceive passive limb motion. Atvery low velocities (0.075, 0.15�/second), participantsbegan to rely on limb displacements that approachedor exceeded known position thresholds to make ajudgment about motion. That is, in those cases theverbal judgment about the perception of forearmmotion was based on velocity as well as positionalsignals.

Fig. 4 Individual velocity – detection time sensitivity functions of all PDpatients. The grey zone indicates the range of the sensitivity functions of thecontrol group

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j Passive motion sense is impaired in PD

The findings from this study indicate that the con-scious perception of limb motion is impaired inParkinson’s disease. PD patients needed larger limbdisplacements and required more time before theycould judge the presence of passive motion (seeFigs. 2, 3). They consistently revealed longer detectiontimes across the range of tested velocities – the meandetection times of the PD group were 92–166% higherthan in the control group. PD patients also requiredlarger displacements during substantially more trials– in the PD group the necessary displacement fordetection exceeded a 1� displacement in 45% of trials,while only 12.5% of the control group trials showedsuch displacements. Since larger limb displacementsallow for the processing of positional as well asvelocity information, this implies that PD patientsrelied more often than controls on both sources ofinformation for their perception of motion. In otherwords, they used positional information to compen-sate for their reduced motion sensitivity.

Considering the results of this and previousexperiments, it becomes increasingly clear that PD isassociated with a loss of multiple aspects of kinaes-thetic function. Moreover, this deficit seems to in-volve early stages of proprioceptive processing, whichis underlined by the elevated thresholds for the per-ception of limb position, motion and gravitationalload [15, 16].

The observed perceptual deficit correlated posi-tively with disease severity for the majority of ourpatient sample as measured by the clinical UPDRSscores (r = 0.63; see Fig. 5). However, we also foundevidence that the time course of the impairment canbe rather different among patients. Some patientsshowed clear perceptual deficits within the first yearsof the disease, while others were still essentially nor-mal at that time. We assume that this reflects up onthe known different rates of disease progression in PDpatients [13]. At this point, it is not known, whetherthe documented perceptual deficits develop earlier inthe disease process as motor symptoms and whetherthey exhibit the same rate of decline. If they do, theycould potentially serve as pyschophysical markers forthe early detection of the disease.

Results of one previous study suggested thatdopaminergic medication might enhance kinaestheticdeficits [18]. This finding remains controversial givenearlier findings indicating that dopamine replacementtherapy might improve proprioceptive guidance ofvoluntary movements in some patients [2, 19]. Wefound a positive, yet statistically not significant cor-relation (r = 0.4) between levodopa equivalent dosageand the displacement-until-detection. This, at least,

hints that levodopa might have some adverse effect onkinaesthesia. However, based on our limited samplewe have no clear evidence that levodopa is inducingproprioceptive deficits. In fact, the patient with thehighest levodopa equivalent dosage (1600 mg) in ourstudy had a motion sensitivity within the normalrange, while patients with no or only a small levodopaequivalent dosage (100 mg) revealed the lowest sen-sitivity for motion detection. Further data from recentstudies investigating proprioceptive thresholds in PD[15, 16] were also not in support of the hypothesisthat levodopa is strongly associated with proprio-ceptive deficits. In both studies the elevated thresh-olds to perceive changes in limb position orgravitational load did not correlate significantly withPD patient’s levodopa equivalent dosages.

In summary, there is clear, increasing evidencethat PD is associated with impaired kinaesthesia.There are additional data that indicate that levodopamedication might enhance such deficits. However, noempirical evidence exists to date proving that levo-dopa is causal to these kinaesthetic deficits. In otherwords, there is no evidence that impairments in kin-aesthesia are secondary symptoms of PD and thatthese kinaesthetic deficits subside after the removal oflevodopa medication.

Fig. 5 Association between displacement-until-detection and the UPDRSmotor scores. For each patient, the mean values of the three slowest velocityconditions (0.075, 0.15, 0.3�/second) are shown. Note that one patient (No. 3;open squares) exhibited little signs of kinaesthetic impairment, despite havingthe second highest UPDRS score

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j Basal ganglia and sensorimotor integration

PD is a neurodegenerative disease affecting cerebro-basal ganglia loops. Traditionally PD has been clas-sified as a movement disorder since its main symp-toms (tremor, rigidity, bradykinesia) are related tomotor function. The transmitters, the inhibitory andexcitatory nature of the basal ganglia projections andtheir receptors are mostly known, yet the functionalrole of these loops for motor control are not preciselyunderstood [9]. Numerous research findings suggestthat a major source of the motor problems in PD is adysfunctional sensorimotor integration. For example,the performance in tasks that rely on the integrationof visual and proprioceptive stimuli are often im-paired in PD patients [1, 6]. This is consistent withresults from animal studies that demonstrated thatthe basal ganglia respond to somatosensory, auditoryand visual inputs with many neurons showing mul-timodal convergence [12]. However, in the absence ofvision, the motor problems of PD patients are oftenexaggerated. In addition, they perform poorly in tasksthat require precise kinaesthetic information such asthe estimation or the matching of limb positions [4,10, 11, 25]. This implies that the utilization of theproprioceptive and not exteroceptive inputs consti-tute a major problem for PD patients. Thus, one mayquestion whether the source of problem for PD pa-tients is not the multimodal sensory integration but isrooted in earlier stages of sensory processing –namely at the processing of proprioceptive signalsthat give rise to kinaesthetic perception.

Given the numerous research findings that docu-ment deficits in sensorimotor integration in PD, thequestion remains open whether such deficits are due

to a faulty processing of somatosensory informationor whether they constitute an additional problem.Nevertheless, all these findings support the hypothesisthat one function of the basal ganglia is to serve as asensory analyzer for movement [14].

Another important question concerns the rela-tionship between impaired kinaesthesia and brady-kinesia. It is accepted that precise proprioceptiveinformation is essential for motor planning andcontrol [5, 20]. Inaccurate information about currentlimb positions and motion very plausibly affects tra-jectory formation. It may well be that such systematicmovement errors in the spatial and time domain arerelated to coarse, skewed or distorted proprioceptivemaps. Assuming that during motor planning suchdistorted body map is matched to established, highlylearnt motor patterns, the resulting movement couldbecome hypometric (spatial error) and slowed(velocity error). In theory, the networks involved inproprioceptive-motor integration may even be intact.However, since these networks rely on faulty orimprecise proprioceptive information, the result ofsuch sensorimotor integration is necessarily an erro-neous motor output. Thus, it is plausible that dis-rupted processes of proprioceptive perception aloneor in combination with an impaired proprioceptive-motor integration ultimately lead to the observedmotor deficits in Parkinson’s disease.

j Acknowledgments We wish to thank all participants of this studyas well as Stacy Majestic who helped with coordination of thisstudy. The study was supported by grants from the AcademicHealth Center of the University of Minnesota and the MinnesotaMedical Foundation.

References

1. Adamovich SV, Berkinblit MB, HeningW, Sage J, Poizner H (2001) Theinteraction of visual and propriocep-tive inputs in pointing to actual andremembered targets in Parkinson’sdisease. Neuroscience 104:1027–1041

2. Almeida QJ, Frank JS, Roy EA, JenkinsME, Spaulding S, Patla AE, Jog MS(2005) An evaluation of sensorimotorintegration during locomotion towarda target in Parkinson’s disease. Neuro-science 134:283–293

3. Clark FJ, Burgess RC, Chapin JW,Lipscomb WT (1985) Role of intra-muscular receptors in the awareness oflimb position. J Neurophysiol 54:1529–1540

4. Contreras-Vidal JL, Gold DR (2004)Dynamic estimation of hand position isabnormal in Parkinson’s disease. Par-kinsonism Relat Disord 10:501–506

5. Cordo PJ (1990) Kinesthetic control ofa multijoint movement. J Neurophysiol63:161–172

6. Demirci M, Grill S, McShane L, HallettM (1997) A mismatch between kines-thetic and visual perception in Parkin-son’s disease. Ann Neurol 41:781–788

7. Deshpande N, Connelly DM, CulhamEG, Costigan PA (2003) Reliability andvalidity of ankle proprioceptive mea-sures. Arch Phys Med Rehabil 84:883–889

8. Goldscheider A (1898) Physiologie desMuskelsinnes. Johann AmbrosiusBarth, Leipzig

9. Kaji R, Urushihara R, Murase N,Shimazu H, Goto S (2005) Abnormalsensory gating in basal ganglia disor-ders. J Neurol 252(Suppl 4):IV13–IV16

10. Khudados E, Cody FW, O’Boyle DJ(1999) Proprioceptive regulation ofvoluntary ankle movements, demon-strated using muscle vibration, is im-paired by Parkinson’s disease. J NeurolNeurosurg Psychiatry 67:504–510

11. Klockgether T, Borutta M, Rapp H,Spieker S, Dichgans J (1995) A defect ofkinesthesia in Parkinson’s disease. MovDisord 10:460–465

12. Krauthamer GM (1979) Sensory func-tions of the neostriatum. In: Divac I(ed) The neostriatum. Pergamon Press,Oxford, p 263–289

662

13. Leenders KL, Oertel WH (2001) Par-kinson’s disease: clinical signs andsymptoms, neural mechanisms, posi-tron emission tomography, and thera-peutic interventions. Neural Plast 8:99–110

14. Lidsky TI, Manetto C, Schneider JS(1985) A consideration of sensory fac-tors involved in motor functions of thebasal ganglia. Brain Res 356:133–146

15. Maschke M, Gomez CM, Tuite PJ,Konczak J (2003) Dysfunction of thebasal ganglia, but not the cerebellum,impairs kinaesthesia. Brain 126:2312–2322

16. Maschke M, Tuite PJ, Krawczewski K,Pickett K, Konczak J (2006) The per-ception of heaviness in Parkinson’sdisease. Mov Disord 21:1013–1018

17. Maschke M, Tuite PJ, Pickett K,Wachter T, Konczak J (2005) The effectof subthalamic nucleus stimulation onkinaesthesia in Parkinson’s disease. JNeurol Neurosurg Psychiatry 76:569–571

18. O’Suilleabhain P, Bullard J, Dewey RB(2001) Proprioception in Parkinson’sdisease is acutely depressed by dopa-minergic medications. J Neurol Neu-rosurg Psychiatry 71:607–610

19. Rickards C, Cody FW (1997) Proprio-ceptive control of wrist movements inParkinson’s disease. Reduced musclevibration-induced errors. Brain 120 (Pt6):977–990

20. Scheidt RA, Conditt MA, Secco EL,Mussa-Ivaldi FA (2005) Interaction ofvisual and proprioceptive feedbackduring adaptation of human reachingmovements. J Neurophysiol 93:3200–3213

21. Schneider JS, Diamond SG, MarkhamCH (1987) Parkinson’s disease: sensoryand motor problems in arms andhands. Neurology 37:951–956

22. Seiss E, Praamstra P, Hesse CW, Ric-kards H (2003) Proprioceptive sensoryfunction in Parkinson’s disease andHuntington’s disease: evidence fromproprioception-related EEG potentials.Exp Brain Res 148:308–319

23. Treutwein B (1995) Adaptive psycho-physical procedures. Vision Res35:2503–2522

24. Zia S, Cody F, O’Boyle D (2000) Jointposition sense is impaired by Parkin-son’s disease. Ann Neurol 47:218–228

25. Zia S, Cody FW, O’Boyle DJ (2002)Identification of unilateral elbow-jointposition is impaired by Parkinson’sdisease. Clin Anat 15:23–31

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