The Relation Between EMG Activity and Kinematic ParametersStrongly Supports a Role of the Action Tremor in

Parkinsonian Bradykinesia

M.C. Carboncini,1* D. Manzoni,2 S. Strambi,1 U. Bonuccelli,1 N. Pavese,1 P. Andre,1 and B. Rossi1

1Department of Neuroscience, University of Pisa, Pisa, Italy2Department of Physiology and Biochemistry, University of Pisa, Pisa, Italy

Abstract: The kinematics characteristics of an upper arm ex-tension of large amplitude (90°) performed in the horizontalplane and the simultaneous activity of the shoulder muscleswere recorded in 12 parkinsonian patients and in six normalcontrol subjects. The movement, triggered by an acoustic “go”signal, was preceded by an isometric adduction.

Within the whole population of individuals (n4 18) astrong, positive correlation was observed between the rootmean square value of agonist EMG activity, evaluated duringthe acceleration phase of the movement, and both peak velocityand acceleration.

In six patients tremor bursts at the frequency of 8–14 Hz(action tremor) were observed during the movement phase inthe anterior, middle, and posterior deltoid: all these patients

showed low root mean square values and were bradykineticwith respect to the control subjects.

The remaining six patients did not show this action tremorduring the movement phase. All but one had an agonist acti-vation of normal duration and amplitude, showed high rootmean square values, and performed well in the range of controlsubjects. We conclude that the inability to suppress the activityof pathological oscillator(s) responsible for the action tremorplays a fundamental role in the bradykinesia associated withParkinson’s disease.

Key words: Parkinson’s disease; action tremor; bradykine-sia. Mov. Disord. 16:47–57, 2001. © 2001 Movement DisorderSociety.

Akinesia, bradykinesia, and hypokinesia are wellknown symptoms of Parkinson’s disease, which corre-spond to the difficulty or inability to start a movementand to its reduced velocity and angular excursion, re-spectively. They are commonly attributed to an impairedcontrol of the agonist muscles.1,2

It is known that in normal subjects rapid movementsare performed by a triphasic muscle activation consistingof an initial burst of the agonists (AG1),3 followed by aburst of the antagonists (ANT),4 and finally by a secondburst of the agonists (AG2).3 Preliminary inhibitory phe-nomena are also present in the agonists (premotor si-lence)5 and in the antagonists.6

While premotor silence can be lost in Parkinson’s dis-ease patients,7 the inhibition of the antagonist musclesproved to be normal in some of them.8 Moreover the

agonist activation may be anomalous: often, when fastdisplacements1 have to be performed, several cycles ofalternating agonist-antagonist activity are generated toperform the movement.1,8This peculiar EMG pattern canbe differentiated from the bursting activity observed atrest on the basis of several physiological criteria.8 Thereare two possible explanations for this repeated muscleactivation. The first is that the weakness of the initialAG1 burst makes necessary further muscle recruitmentsto perform the movement; alternatively a pathologicaloscillator could be released during the movement, thusleading to an “action” tremor9 that constrains the expres-sion of the triphasic pattern and generates bradykine-sia.10 It should be possible to differentiate between thesehypotheses by increasing the amplitude of the move-ment. In this instance the duration of the AG1 shouldalso increase,11 making this motor pattern distinguish-able from the action tremor.

The aim of the present study was to investigate, in

*Correspondence to: Dr. Maria Chiara Carboncini, Department ofNeuroscience, University of Pisa, Via Roma, 67, 56124 Pisa, Italy.

Received 10 August 1999; Accepted 20 July 2000

Movement DisordersVol. 16, No. 1, 2001, pp. 47–57© 2001 Movement Disorder Society

47

Parkinson’s disease patients, the relation existing be-tween agonist activation and kinematic characteristics offast voluntary displacements. These data were then com-pared with those obtained in a control group of healthy,age-matched subjects, in order to clarify the extent of themotor deficits of Parkinson’s disease patients and to un-derstand whether they depend upon the weakness of ago-nist activation, the recruitment of a pathological oscilla-tor, or both factors. For this purpose all the subjects wereasked to perform a movement of large amplitude to in-crease the period of the AG1 above that of the actiontremor.

MATERIALS AND METHODS

We have analyzed 12 patients with Parkinson’s dis-ease (six males and six females, age 48–75 years), diag-nosed by the criteria of the UK Parkinson’s Disease So-ciety Brain Bank (see Table 1), and six control, age-matched (range 52–75 years), healthy subjects (threemales and three females). The clinical conditions, illus-trated in Table 1, were stable in the two months preced-ing the present investigation. Both control subjects andpatients were right-handed. All subjects gave their in-formed consent for the procedure, which had previouslybeen approved by the Ethics Committee of the Univer-sity of Pisa.

Experimental Protocol

All subjects were asked to sit in a chair with their armsunsupported, unrestrained, and free to move. They wereinstructed to keep the right arm straight, with the elbowextended and the forearm in the midprone position (seeFig. 1), while grasping the handle of a strap that wasconnected to a strain gauge. An isometric flexion atabout 70% of the maximum voluntary effort (isometricphase of the task) had to be exerted for about 3 seconds.The generated force could be monitored on an oscillo-scope screen. Following an acoustic “go” signal the sub-jects had to extend the forearm as quickly as possible,reaching the largest excursion they could. The final po-sition had to be kept for a few seconds (holding phase ofthe task). In this way it was possible to study severalaspects of muscle activation: the relaxation of the an-tagonist before the beginning of the movement, the tri-phasic pattern associated with the fast limb displacement,and finally, the postural activity necessary to maintainthe arm extended in the horizontal plane. This sequencewas repeated ten times at regular intervals of 30–120seconds. Data recording started only when the subjectshad practiced the movement, i.e. when it appeared to beas rapid as possible. Both electromyographic (EMG) andkinematic analysis were carried out using an integrated

TABLE 1. Clinical features of the different Parkinson’s disease patients

Case AgeIllness

duration H.Y.UPDRSsub II

Tremorsub III

Rigiditysub III

Akinesiasub III

Dopaminergictreatment

1 49 3 years 2.5 14 0 2 2 Y0

2 73 6 months 2.5 12 1 2 4 N0

3 53 8 years 2.5 15 0 2 5 Y1

4 66 8 months 2.5 4 1 1 2 N1

5 47 9 years 2 9 1 2 5 Y1

6 74 5 years 2.5 9 2 1 4 Y1

7 48 1 year 2 10 1 1 2 N0

8 62 2 years 2.5 12 1 1 4 Y0

9 75 2.5 years 2 8 1 1 1 Y1

10 66 8 years 2 14 1 1 2 Y0

11 64 9 years 2.5 15 1 1 2 Y0

12 70 4 years 1.5 9 0 1 0 N0

H.Y., Hoehn Yahr rating scale. U.P.D.R.S.; Unified Parkinson Disease Rating Scale. Upper and lowernumbers in the Tremor column refer to “resting” and “postural” tremor (see text for further explanations). Y, Nindicate respectively patients treated or not with dopaminergic drugs.

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system (Elite-BTS), composed of an eight-channelelettromyograph and two telecameras, all connected tothe main computer.

The EMG activity was measured by surface elec-trodes, spaced 1 cm, placed longitudinally with respect tothe muscle fibers. EMG recordings were differentiallyamplified, analogic-to-digital converted at 500 Hz with12-bit resolution and stored on a computer. The activityof the following muscles was recorded: pectoralis major,deltoid (anterior, middle, posterior), trapezius (superior,middle), triceps, and biceps brachii. The present report isfocused on the pectoralis major (Pm) and the anterior(aD), middle (mD), and posterior (pD) deltoid: due totheir mechanical moment these muscles act respectivelyas agonists (mD and pD) and antagonist (Pm and aD) forextension movements of the upper arm in the horizontalplane.12

The kinematic of the upper arm movement was re-corded using four semispheric skin markers (1 cm diam-eter), covered with reflecting material, which were pre-liminarily placed on the following points: sterno-clavicolaris joint, acromion, elbow and wrist (see filledand open circles in Fig. 1). The position of the markerswas recorded by the two television cameras and utilizedto determine the angle (a, Fig. 1) included between theupper arm (A, Fig. 1) and the shoulder (B, Fig. 1). BothEMG and kinematic signals were stored on disk for off-line analysis.

Data Recording

The kinematic analysis gave objective information onthe angular position of the arm at rest and during themovement, as well as on its angular velocity and accel-

eration. The beginning and the end of the movement(arrow heads in Figs. 2, 3) were evaluated from the an-gular velocity trace and corresponded to the points ofzero velocity that encompassed the largest bell-shapedcomponent of the movement velocity. In a few task rep-etitions the subjects performed small limb displacementsthat preceeded the beginning of the movement or a sec-ondary adjustment in order to reach the aimed position.These earlier and later components were included in theevaluation of movement duration. The amount of activa-tion of pD, mD, and aD was evaluated during the periodof time from the beginning of AG1 to the peak of angularvelocity by calculating the root mean square (RMS) ofthe EMG. The rationale for this procedure was to com-pare Parkinson’s disease patients who did not show clearAG1 burst with the remaining subjects. Data obtained forpD and mD were averaged to characterize the overallagonist activation with a single parameter.

The amount of cocontraction of aD with pD-mD ob-served during the movement was quantified by a cocon-tration index (CI), calculated as the ratio of the corre-sponding RMS values (aD/pD-mD). In control subjects,as well as in Parkinson’s disease patients showing clearAG1, we also evaluated the duration of the correspond-ing bursts. Even in this instance data relative to pD andmD were averaged. Although the occurrence of cross-talk between adjacent muscles can never be eliminated,we estimated the amount of this effect by recording si-multaneously their activity during different movementsand isometric efforts. When a muscle can be stronglyrecruited while the adjacent one is poorly active, it isreasonable to assume that the effect of cross-talk is poorand cannot account for the recording of simultaneouslarge-size bursts from the two muscles. In control sub-jects it was observed that, during the development of aflexor torque, the aD could be strongly activated, whilethe mD and pD were poorly recruited.

To quantitatively assess the presence of physiologicaland pathological tremor, the rectified EMG traces weresubmitted to a spectral analysis. Blocks of equal duration(512 ms), corresponding to the isometric movement, andholding phases of the task were submitted to a Fast Fou-rier Transform performed by a statistical package. Eachbin in the power spectra was indicated by its upper limit.

In particular we selected the harmonics showing anamplitude that rose above a value corresponding to themean amplitude plus twice the standard deviation of allthe frequency components included between 2 and 100Hz. The amplitude of these peaks was expressed in per-centage of the total spectral power included in the above-mentioned range.

FIG. 1. Schematic representation of the movement performed by nor-mal subjects and Pd patients. Open and filled circles represent theposition of the markers utilized for kinematic recordings. The anglea,included between segmentsA andB, measures the relative position ofthe upper arm with respect to the shoulder.

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Statistical analysis

ANOVA was used to compare EMG and kinematicdata between different experimental groups. Post-hoccomparisons were performed by the Newman Keuls test.A linear regression analysis was used to assess the cor-relation between the different parameters. The signifi-cance level was set atP < 0.05.

RESULTS

Emg and kinematic analysis in control subjects

During the isometric phase of the task, the Pm and aDwere always strongly activated, while the mD and pDshowed a very slight background activity.

In general, the EMG background of normal subjectswas not characterized by a clear periodic bursting activ-

ity during this phase of the task, although a similar phe-nomenon could occur during isolated task repetition.

The spectral analysis performed during this phase re-vealed that the power of the EMG signal, recorded fromall the tonically active muscles, was scattered between 2Hz and 100 Hz (Fig. 5A, lower row). Sizeable spectralpeaks, rising above the significance level, at frequencyranging from 5.9 to 60.5 Hz, could be observed in one ormore of the muscles recorded from a given subject. Theamplitude of these peaks corresponded on the mean to10.3 ± 4.3% of the whole signal power. During the“holding” phase, a tonic EMG activity could be detectedin all the three parts of deltoid muscle, but not in thePm. The FFT analysis revealed spectral profiles qualita-tively similar to those observed during the isometricphase (Fig. 5C, lower row). The amplitude of the signifi-

FIG. 2. Kinematic characteristcs of upper limb movementsperformed by a control subject (A) and by a Parkinson’sdisease patient (B) that did not show alternating EMG burstsduring limb displacement. In both instances the movementswere normokinetic. Head arrows indicate the beginning andthe end of the movement.

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cant peaks corresponded to 11.6 ± 4.6 % of the totalsignal power. The corresponding frequencies rangedfrom 7.8 to 60.5 Hz.

All the control subjects showed similar features in thepattern of muscle activation during the task (Fig. 4A).The EMG background of Pm was suppressed before theonset of the extension and an ANT burst was usuallypresent (see asterisk in Fig. 4A), rising near to the peakof movement velocity. During the extension both mDand pD showed the classical AG1 and AG2 bursts. Theaverage RMS and duration values relative to AG1 (pD-mD) are given in Table 2.

The activation pattern of aD did not corresponded tothat expected for a flexor muscle. In 5 out of the 6 controlsubjects the aD fired AG1 and AG2 bursts time-locked tothose observed in the pD and mD. In the remaining case

the high aD activity observed during the isometric phasewas also present during the first half of the movement,with a transient suppression that preceded the beginningof limb displacement. This suppression was synchronouswith that occurring in Pm.

In conclusion, during the accelerative phase of themovement, the aD was always active together with thephysiological extensors pD and mD. The average CI val-ues evaluated in the individual subjects ranged from 0.13to 0.46 (mean 0.27 ± 0.13 SD). When the FFT analysiswas applied to the movement phase, the occurrence ofEMG bursts (AG1-ANT-AG2) gave rise to significantspectral peaks at about 2 Hz (Fig. 5B, lower row). Theanalysis of kinematic data indicated that the angular ve-locity profiles of the controls were generally unimodaland bell shaped (Fig. 2A). The average values of angular

FIG. 3. A,B: Kinematic characteristics of the movement per-formed by two different Parkinson’s disease patients withbradykinesia of different severity. Only the patient illustratedin A showed alternating EMG bursts during the movement.Head arrows indicated the beginning and the end of themovement.

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excursion, peak velocity, peak acceleration, and execu-tion time obtained from control subjects are given inTable 2.

Emg and kinematic analysis in Parkinson’s disease

Parkinsonian patients often showed clear alternatingEMG bursts in some or all of the active muscles duringeither phase of the task. In particular they could be di-vided in two groups according to their behavior duringthe movement phase.

In six patients (group I patients) a sequence of shortlasting bursts of activity in mD and pD was observedduring limb displacement (Fig. 4B). This bursting activ-ity could also involve the aD. Due to the presence ofthese EMG bursts these patients showed RMS valuessignificantly lower (ANOVAP < 0.05) than the controls(see Table 2). It is remarkable that, in spite of the burst-ing activity occuring in the shoulder muscles, the upperarm of these patients did not show evident oscillationsduring the movement. The alternating bursts mentionedabove were not necessarily associated with the presenceof the classical parkinsonian tremor, i.e. with the oscilla-tions of the hanging hand observed when the patientskept their upper arm adducted to the body with the elbowflexed (“resting” tremor), or else when the arm was ad-

ducted on the midline at 90° with respect to the bodywith the elbow fully extended (“postural” tremor). Thepresence of these classical symptoms in the differentpatients is indicated in Table 1. A peculiar feature of thealternating bursts observed in the shoulder muscle wasthat they tended to be synchronous in the flexor aD andin the extensors mD-pD, rather than out-of-phase. It isunlikely that this finding could be merely due to a fallingconduction for the reasons explained in the methods.Moreover, synchronous bursts could be seen in distantmuscles, as Pm and mD, during the isometric phase ofthe task.

The duration of the individual bursts ranged from 60to 80 msec in the individual patients, with an average of73.3 ± 10.3, which was significantly lower with respectto the duration of AG1 observed in control subjects(ANOVA P < 0.001, see Table 2). An interesting pointwas that for all the group I patients, the duration of thebursts observed during the movement was not correlatedto the amplitude of the latter, in spite of the fact thatthis parameter could vary up to 35° in different taskrepetitions of the same subject. The spectral analysis ofthe EMG traces obtained during the movement phaseof these patients (see Fig. 5B, upper row), showed thepresence of particularly large peaks in the range 3.9–15.6

FIG. 4. Patterns of EMG activity observed during the task in a control subject (A) and in three Parkinson’s disease patients (B–D). While the patientillustrated in D showed normal kinematic characteristics of the perfomed movement, those illustrated in B and C were bradykinetic. Note that tremorbursts were present during the movement phase in B but not in C and D. Pm, pectoralis major; aD, anterior deltoid; mD, medial deltoid; pD, posteriordeltoid. The dashed lines included the movement phase of the task. The asterisk indicates the ANT burst of Pm.

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Hz (average frequency 10.4 ± 2.5), with an average am-plitude of 22.2 ± 8.3% of the total power signal (seeTable 3).

In the remaining six patients (group II patients) clearAG1 and AG2 bursts were observed during the move-ment, while at least in some of them a bursting activitycould be present during the isometric and holding phases.The power spectra of the EMG traces recorded duringthe movement phases of these patients were similar tothose of normal controls, with large, significant peaks atabout 2 Hz. It is of interest that, in five out of six of them,the duration of AG1, as well as the RMS values obtainedfor pD-mD, were within the range observed for controlsubjects (Table 2). In the remaining patient (patient 7,see Table 2) the duration of AG1 was nearly normal (Fig.4C), but the amount of associated EMG activity waspoor, leading to an abnormally low RMS value. With thisexception, the absence of bursting activity during themovement was associated to a normal recruitment of theagonist muscles.

It is of interest that, in both group I and II patients, anANT burst was seldom observed among Parkinson’s dis-ease patients (see Fig. 4B–D). Moreover, the degree ofcocontraction of aD together with pD/mD was higherthan that observed in controls. The average CI valuesobtained for group I (0.52 ± 0.17 SD) and group II (0.46± 0.13 SD) were in fact significantly higher (ANOVA,P

< 0.02 andP < 0.04, respectively) than that obtained forcontrol subjects (0.27 ± 0.13).

During the isometric phase of the task clear alternatingbursts could be observed not only in group I, but also ingroup II patients. These bursts led to particularly large,significant peaks in the power spectrum (Fig. 5A) at afrequency ranging from 3.9 to 15.6 Hz (average 11.5 ± 3SD) (see Table 3 for details). The average amplitude ofthese peaks corresponded to 18.8 ± 12.2 for all the pa-tients.

When, at the end of the movement, the arm was keptstill in the final position, a bursting activity could be stillobserved in the pD, mD, and aD of all the group I andseveral group II patients (Table 3 for details). This ac-tivity led to significant peaks (Fig. 5C, upper row) in thepower spectrum within the same frequency range (3.9–15.6 Hz) mentioned above (average frequency 10.5 ± 2.3Hz). The amplitude of these peaks corresponded on theaverage to 17.5 ± 10.9 for all the patients. It is worthnoting that in both the isometric and holding phases thebursting activity did not give rise to appreciable oscilla-tion of the forearm.

The kinematics of the movement could be distorted ingroup I patients (see Fig. 3A). Occasionally more thanone movement component could be observed in the ve-locity and acceleration profiles. Average values of move-ment amplitude and peak velocity of group I patients

FIG. 5. Power spectra relative to the EMG activity recorded from the mD of a control subject (lower row) and a Parkinsonian patient (upper row)during the three different phases of the task.A: Isometric phase;B: movement phase;C: holding phase.

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were significantly lower, while their execution timewas longer with respect to the corresponding values ob-tained for both group II patients and healthy controls(see Table 2). On the other hand all the average kine-matic characteristics of group II patients were similar tothose of control subjects (Table 2). In particular theirvelocity traces were bell shaped, while accelerationtraces biphasic (see Fig. 2B). The only group II patientshowing an abnormally low RMS value for the agonistsdid not show gross alterations in the shape of the kine-matic profiles (see Fig. 3B), but was hypometric andbradykinetic.

An attempt was made to correlate, in Parkinson’s dis-ease patients, the kinematics of arm movement to theamount of agonist activation. For this purpose the angu-lar excursion, peak velocity and peak acceleration wereplotted as a function of the corresponding RMS values(Fig. 6). Larger RMS values were associated with largerpeak velocities (Fig. 6B) and accelerations (Fig. 6D). Inboth istances the coefficient of correlation was very high(velocity: r 4 0.9,P < 0.0005; acceleration: r4 0.83,P< 0.001). It is remarkable that the regression lines ob-tained for the plotted data were virtually unchanged byadding those points relative to the six control subjects.These findings indicate that the RMS values of the ago-nists, which increase progressively from group I patients

to group II patients and control subjects, largely deter-mine the kinematic characteristics of the movement. Thecorrelation between movement amplitude and RMSvalue of the agonists, however, was less striking (see Fig.6A: r 4 0.79,P < 0.002). This finding was due to thefact that the weakest patients tended to increase themovement time up to about one second, as indicated inFigure 6C. In this way they were able to increase theangular excursion, so that their hypometry was lessmarked than their bradykinesia.

DISCUSSION

General considerations

Although limb displacements of large amplitude areseverely impaired in Parkinson’s disease,13,14half of ourpatients (group II) were normokinetic. This finding isprobably related to the triggering “go” stimulus, whichspeeds up the beginning of the movement in Parkinson’sdisease,15 but also to interindividual differences in theextent of the pathological process, in the pharmacologi-cal treatment and in the susceptibility of the patients to it.Among both normo and bradykinetic patients there weresubjects either treated with dopaminergic agents or not.Although a small overlap existed between these twogroups, the normokinetic patients tended to show lower

TABLE 2. Electromiographic (RMS values) and kinematic characteristics of the movements performed by Parkinson’s diseasepatients and control subjects

Patient RMS mVDuration

AG1Movement amplitude

degreesMovementtime msec.

Maximal velocitydegrees/sec

Maximal accelerationdegrees/sec2

Parkinson’s disease patients (Group I)1 0.27 — 77 967 107 3442 0.38 — 63 932 121 5453 0.25 — 65 864 174 9794 0.21 — 63 631 140 5755 0.53 — 56 591 241 12876 0.69 — 65 549 218 1699

Mean ± SD *°0.39 ± 0.18 — *°64.8 ± 6 *°755 ± 187 *°167 ± 53 *°904 ± 516N.6

Parkinson’s disease patients (Group II)7 0.51 300 74 635 194 10338 1.31 266 83 456 318 22639 1.10 276 83 454 427 3350

10 1.30 215 89 393 404 222011 1.11 220 90 466 304 150112 1.12 227 83 433 305 1960

Mean ± SD 1.08 ± 0.29 259 ± 34 83.7 ± 6 472 ± 87 325 ± 83 2054.5 ± 788N.6

Control subjectsMean ± SD 1.02 ± 0.11 220 ± 38 75.3 ± 5 476 ± 97 297 ± 80 1955 ± 818

The values relative to the individual patients are the average of ten task repetitions. RMS values are relative to the period from the beginning ofAG1 to the peak of angular velocity. Both RMS values and AG1 duration values corresponded to the average of the data obtained for pD and mD.

*: Significant difference (at leastP < 0.05) with respect to Parkinson’s disease patients without tremor (Group II).°: Significant difference (at leastP < 0.05) with respect to control subjects.The numeration of patients corresponds to that of Table 1.

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tremor, rigidity, and akinesia scores with respect to thebradykinetic ones. A larger overlap between the twogroups of patients was indicated by U.P.D.R.S. sub IIand Hoehn Yahr scale.

The kinematics characteristics of the movement aredetermined by the pattern of muscle activation. In thepresent study the activation of the agonist muscles pD

and mD was impaired in half of the patients, while theantagonist muscle Pm was never used to brake the move-ment. The latter finding is in agreement with previousobservations of fast arm extensions in Parkinsonian pa-tients.16

Relation between kinematic characteristics andpattern of muscle activation

Bradykinetic patients were those who failed to pro-duce AG1 bursts of the appropriate size and duration.This point is clearly indicated by the fact that, in ourpatients, both velocity and acceleration were stronglycorrelated to the RMS values of the agonists. Since thecorresponding regression lines were virtually unmodifiedby adding control subjects data, the degree of agonistactivation accounts for most of the kinematic variability.This observation indicates that, in our experiments, in-terindividual differences in electrode placement and/orskin resistance do not greatly affect the amplitude ofEMG recordings.

As mentioned in the result section, an EMG burstingactivity, not associated to evident oscillation of the fore-arm, could be observed in most of the subjects, not onlyduring the isometric and holding phases of the task, butalso during the movement phase. A bursting activity ofthe agonist, similar to that observed in the present study,has been previously described to the level of both el-bow1,8 and shoulder16 muscles in Parkinson’s diseasepatients that performed small amplitude, rapid move-ments. These EMG bursts have been interpreted1,8 as arepeated running of the same motor pattern (AG1), madenecessary by the fact that the initial agonist activationwas of small amplitude and inefficient to drive the move-ment. It seems unlikely that, in the present experiments,the repeated activity observed during limb displacementis merely a sequence of agonist bursts,1 since a normalAG1 would show a larger duration (see Table 2), and itsduration would scale with the movement amplitude. Ob-viously we cannot ignore the possibility that these Par-kinsonian patients were unable to modify the duration oftheir agonist burst and were obliged to a repeated acti-vation of these muscles in order to perform the move-ment. However, the fact that this bursting activity couldalso be present with the same average frequency (10–11Hz) during the isometric and holding phases, would fa-vor the hypothesis that these patients recruited a “tremorrather than a ballistic” generator during the movement.Given the value of the average frequency, and the ten-dency to a synchronous activation of agonist and antago-nist it is likely that the EMG bursts observed correspondto an action tremor9,17,18that did not result in appreciableforearm oscillations, due to synchronous activation of

TABLE 3. Presence of tremor bursts in the EMG activityrecorded from the shoulder muscles of Parkinson’s disease

patients during the different phases of the task

Patient Premovement Hz Movement Hz Holding Hz

1 Pm 14aD 14 aD 14mD 14pD 14 pD 8 pD 8

2 Pm 14aD 16 aD 10 aD 12mD 16 mD 8 mD 12

pD 10 pD 83 Pm 12

aD 12 aD 12 aD 12mD 12 mD 12 mD 10pD 12 pD 12 pD 10

4 Pm 10aD 14 aD 12mD 14 mD 12pD 10 pD 10

5 Pm 12aD 10 aD 12

mD 6 mD 10pD 8 pD 12

6 Pm 14aD 6 aD 8 aD 12mD 6 mD 8 mD 6

pD 8 pD 87 Pm 14

aD 14mD 16pD 8

8 Pm 16aD 14 aD 10mD 12 mD 10

pD 109

aD 8 aD 12mD 6 mD 8

pD 810 Pm 12

aD 8 aD 8mD 8 mD 8pD 8 pD 8

11aD 12 aD 10mD 14

12 Pm 10aD 10 aD 8

pD 8

The numeration of patients correspond to that of Table 1. The num-bers indicate the frequency value corresponding to the largest spectralpeaks observed within the frequency range 3.9–15.6 Hz, as calculatedby the Fourier analysis. Pm, pectoralis major; aD, anterior deltoid; mD,middle deltoid; pD, posterior deltoid.

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the antagonist muscles and to the dampening effect oflimb inertia. This tremor could be present independentlyupon the 4–6 Hz resting tremor, which is easily recog-nized at sight (compare Tables 1 and 3). It is known thatthe presence of action tremor is associated with a reduc-tion in the force development,18 due to the incompletefusion of muscle contraction that is observed when themotor units are locked to an approximately 10-Hzrhythm.

The results of the present investigation show that dueto the presence of EMG bursting during the movementphase (group I patients), the agonist recruitment was con-strained to a restricted time window and resulted in aninability to drive the movement appropriately. They areconsistent with kinematic observations suggesting thatthe action tremor is related to bradykinesia in Parkinso-nian patients.19 Further experiments are necessary toverify to what extent, in different experimental condi-tions, other factors may account for bradykinesia. It mustalso be stressed that one patient without bursting activityduring the movement was bradykinetic, due to a reducedamplitude of the AG1. This finding indicates that thedifficulty in “infusing energy”2 in the muscles and therecruitment of a pathological oscillator during the move-ment can be considered as separate pathogenetic mecha-nisms of the bradykinesia.

Temporal organization of motor behavior inParkinson’s disease: relation to motor deficits

The temporal organization of motor behavior is dis-rupted in Parkinson’s disease. Freund20 and Logigian10

suggested that, in Parkinson’s disease, the slowing ofrepetitive voluntary alternating movements may derivefrom synchronization of the voluntary movement patterngenerators with pathological oscillators. Moreover, dur-ing repetitive movements,21,22 Parkinson’s disease pa-tients show a variability of the corresponding periodlarger than normal.23

In the present experiments a 10–11 Hz EMG burstingimpairs the agonist activation leading to bradykinesia.Similar results have been obtained by Te¨ravainen andCalne9 during rapid pronation-supination movements ofthe forearm, as well by Brown et al.18 and Brown24 dur-ing tonic contractions and movement. It is possible thatthis pathological tremor, as well as the classical 4–6 Hz“resting” tremor are induced by the disruption of specificoscillating circuits related to the activation of both ago-nist and antagonist during fast voluntary movements.

It is of interest that in Parkinsonian patients significantcoherence values were found between the magneto-EEGtraces and the EMG activity of finger flexor and extensormuscles in the 4–5 and 8–10 Hz frequency bands.25 This

FIG. 6. The kinematic characteris-tics of the movements performed byall the patients have been plotted as afunction of the corresponding RMSvalues evaluated for posterior andmiddle deltoid from the beginning ofmuscle activation up to the peak ofangular velocity. Each point is theaverage of 10 repetitions (see text forfurther explanation).A: Movementamplitude;B: peak movement veloc-ity; C: movement duration;D: peakmovement acceleration. The lines arethe regression evaluated for the plot-ted points. Black squares: Parkin-son’s disease patients without EMGbursting. Open symbols: Parkinson’sdisease patients with EMG burstingduring the movement phase.

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synchronized magnetic activity was localized in the re-gions involved in the control of voluntary movements,which also shows an increase in blood flow during rest-ing Parkinsonian tremor. Based on this evidence Volk-mann et al.25 proposed that “slowing of movement inParkinson’s disease patients results at least in part fromcoupling of voluntary motor activity into abnormallyslow and synchronised neuronal activity within the thala-mocortical motor loop”. It has to be mentioned, thatmore recently, Wang et al.26 and Brown and Marsden27

showed that in Parkinson’s disease patients the levodopaenhance the EEG desynchronisation observed before andduring movement. This finding was correlated to a re-duction in bradykinesia and was attributed to a proposedrole of the basal ganglia in releasing the motor circuitsfrom an idling rhythm, which is abnormally enhanced inParkinson’s disease. As recently proposed on the basis ofexperiments of unit recording in Parkinsonian mon-keys,28 this abnormal rhythm could arise from the ab-normal firing of pallidal neurons that is processed at thelevel of the thalamic cells. The persistence of an 8–12 Hzaction tremor following thalamotomy17 indicates thatpallidal neurons may drive the spinal circuits by meansof efferent projections to mesencephalic and medullarystructures.

CONCLUSIONSThe results of the present experiments that allow a

direct measurement of EMG agonist bursts together withtheir kinematics consequence, suggest that the criticalfactor in the impairment of fast movements observed inParkinson’s disease patients is the action tremor that de-velops during the movement.

It appears, therefore, that the neuronal circuits thatcontrol the movement may undergo an abnormal oscil-latory state when driven by voluntary motor commands,8

independently upon their condition at rest. We proposethat in the context of Parkinson’s disease, the classicalview of a resting tremor that disappears with the move-ment must be replaced by the concept of pathologicaloscillators that can be differentially recruited accordingto the behavioral condition.

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