Bradykinesia and Impairment of EEG Desynchronization inParkinson’s Disease

Peter Brown, MD, and *C. David Marsden, DSc

MRC Human Movement and Balance Unit, Institute of Neurology and National Hospital for Neurology and Neurosurgery,Queen Square, London, U.K.

Summary: It has been suggested that the basal ganglia controlthe release of cortical elements from low-frequency rhythmicidling activity during voluntary movement.1 This hypothesiswas tested by recording the local idling rhythms of the motorcortex, the alpha and beta rhythms, in 12 untreated and treatedpatients with Parkinson’s disease as they moved a wrist. Re-cordings were made after overnight withdrawal of medicationand again 1 hr after levodopa. The treatment-related attenuationof the alpha and beta rhythms picked up over the cortical motor

areas contralateral to the active arm correlated with the im-provement in size and speed of movement effected by levodo-pa. The distribution and degree of attenuation depended on thecomplexity of the task. These results demonstrate for the firsttime a specific effect of levodopa on the organization of motorcortical activity in the frequency domain, an effect that corre-lates with improvements in bradykinesia.Key Words: Parkin-son’s disease—Alpha rhythm—Beta rhythm—Desynchro-nization—Bradykinesia.

The cerebral cortical activity during the waking stateis characterized by two major modes of rhythmicity, thealpha and gamma rhythms. The former is a pervasive,high-amplitude oscillation at approximately 10 Hz. It isgenerally considered a feature of the resting cerebral cor-tex, and its attenuation a measure of activity and, par-ticularly, attention related to the function of that cor-tex.2,3 Thus, oscillations at approximately 10 Hz over theoccipital cortex disappear when an interesting subject isviewed or, perhaps more importantly, when a subjecttries to see in the dark.3 Similar oscillations may bepicked up over the sensorimotor cortex where they aresometimes termed the mu rhythm. Related to this is aslightly faster rhythm in the low beta range (12–22 Hz).Both are attenuated by the preparation and execution ofa voluntary movement.4–7 These electroencephalo-graphic (EEG) changes are related to the mechanismsunderlying the movement rather than consequences ofthe movement itself because similar attenuation may beseen when the same action is imagined.8,9

The high-amplitude alpha activity contrasts with themultiple activities in the gamma band recorded duringactivation of the cortex.10–15 Intracerebral recordings inanimals demonstrate that these are often synchronizedacross the cortex, albeit on a smaller scale than the syn-chronization in the alpha or beta rhythms.10–15 Compa-rable fast oscillations have been identified in the activehuman motor cortex where they can be picked up asmagnetoencephalographic signals mirroring the Piperrhythm of contracting muscle.16 Coherence betweenmultiple, often distributed gamma activities in the motorareas of the cortex may provide a means whereby spe-cific channels of motor processing can be favored, lead-ing to the effective selection and execution of a givenmotor act.1

It has recently been suggested that during action it isthe basal ganglia that are primarily responsible for re-leasing selected cortical elements from pervasive low-frequency idling rhythms so that these elements maybecome coherent in the gamma range.1 This hypothesiswould predict a correlation between the attenuation ofidling rhythms and movement performance in disease ofthe basal ganglia. This was tested in 12 patients withidiopathic Parkinson’s disease in whom the surface EEGand motor performance were recorded during a trackingtask.

* Deceased.Received September 11, 1998; revision received December 7, 1998.

Accepted January 25, 1999.Address correspondence and reprint requests to Peter Brown, MD,

MRC Human Movement and Balance Unit, Institute of Neurology,Queen Square, London WC1N 3BG, U.K.

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METHODS

We studied 12 patients with Parkinson’s disease(mean age 60 yrs, range 45–70 yrs; three women; twoleft-handed subjects). Three, six, and three patients wereHoehn and Yahr stage I, II, and III, respectively, whenoff medication. All patients were taking levodopa prepa-rations (mean daily dosage 550 mg, range 300–1000mg). In addition, three were taking selegeline, three per-golide, and one each apomorphine, lithium carbonate,and amitriptyline. Patients met criteria for the diagnosisof idiopathic Parkinson’s disease17 and had no clinicalevidence of other neurologic disease. All improved by atleast 50% on their Unified Parkinson’s Disease RatingScale motor score when treated with levodopa (meanscore on treatment 10, range 4–20; untreated mean score29, range 9–52) and demonstrated no electromyographicactivity (EMG) in scalp electrodes resulting from resttremor or dyskinesia in the untreated and treated condi-tions. The worst affected hand was determined clinicallyand tested in each case (left hand in five patients). Re-cords were made 12–18 hrs after withdrawal of antipar-kinsonian medication and again 1–2 hrs after treatmentwas restarted on the same day. All studies were per-formed with the approval of the local ethics committeeand the informed consent of each subject obtained ac-cording to the declaration of Helsinki.

Scalp EEG was recorded with 9-mm diameter silver–silver chloride electrodes fixed with collodion. F3, FC3,C3, P3, O1, F4, FC4, C3, P4, and O2 were referenced tolinked ears (O1 and O2 were not available in two pa-tients). Wrist position in the anterior–posterior plane wasrecorded with a goniometer. The EEG and positionalsignal were amplified and bandpass filtered between 0.5Hz and 300 Hz, and DC and 300 Hz, respectively. Theywere digitized with 12-bit resolution, and collected andanalyzed on a PC by a software package (C.E.D. Spike 2,Cambridge, U.K.). The sampling rate was 640 Hz. Datawith artifact as a result of EMG or eye movement wererejected. The fast Fourier transform was used to computethe discrete Fourier transform of blocks of data. Blockswere of equal duration (512 data points), and spectrawere estimated by averaging across blocks. The non-cycling nature of data blocks was dealt with by applyinga raised cosine window to each block and then compen-sating for the resultant loss of power.

Subjects tracked the predictable movement of a targeton an oscilloscope screen using the wrist. They wereseated with the forearm supported in a pronated positionfacing an oscilloscope screen in a quiet and darkenedroom. They were unable to see the tracking hand. Pa-tients were first asked to spend two 70-second periods

practicing following a target as accurately as possiblewith visual feedback. The screen target moved sinusoi-dally with a frequency of 0.2 Hz. The wrist had to beflexed and extended through a 40° arc to match the ex-cursion of the target spot. Pilot studies showed no sig-nificant improvement in performance with longer train-ing periods so that subsequent measurements were es-sentially independent of further training effects. Flowersmade similar observations.18

During data collection the subjects were asked to re-main relaxed for 60 sec while following the moving tar-get with their eyes (rest–pursuit) followed by a further 60sec tracking the target (tracking). This was repeatedtwice. Movement of both target and feedback spots thenceased and subjects were recorded while they fixated thestationary target while at rest for 60 sec (rest–fixation)and then again while they copied the same wrist move-ments from memory, trying to match both the size andrate of the movement to that demanded earlier (nontrack-ing). Three such rest–fixation and nontracking move-ment runs were completed, with a further rest–pursuitand tracking run interposed between the second and thirdof these. The first 50 sec at rest and during wrist move-ment were analyzed in each case. EEG prior to the move-ment was excluded from analysis to avoid changes re-lated to the preparation for movement. Amplitude spectrafrom the rest–pursuit and tracking runs were averaged ineach subject and percentage change in the alpha (6.25–12Hz) and low beta (12–22 Hz) bands calculated from thearea below the curves in the respective frequency bandsaccording to the formula [(rest − pursuit − tracking/rest–pursuit) × 100]. Similar calculations were performed forthe rest–fixation and nontracking tasks. Movement per-formance was assessed in terms of percentage relativemovement amplitude (RMA), that is, [(mean amplitudeof wrist movement/target amplitude) × 100]. Off-lineanalysis confirmed that the frequency of wrist movementremained more-or-less fixed in both the tracking andnontracking tasks. Thus, increases in the amplitude ofwrist excursion also entailed an increase in the speed ofmovement. Correlation coefficients (r) for [% change inalpha band treated − % change in alpha band untreated]versus [RMA treated − RMA untreated] were for eachelectrode site. A p <0.05 (one-tailedt test) was taken assignificant whenever correlation was positive (con-strained to our a priori hypothesis that levodopa-relatedimprovement in EEG desynchronization would correlatewith improvement in bradykinesia).

RESULTS

Figure 1 gives examples of the attenuation of alphaand beta activities during the tracking task in a parkin-

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sonian patient after drug withdrawal (Fig. 1A) and rein-troduction of levodopa (Fig. 1B) and in a healthy subjectfor comparison (Fig. 1C). The EEG has been bandpassfiltered in the alpha (6–12 Hz) and beta (12–22 Hz)bands. The attenuation of the slow idling rhythms duringmovement was diminished in the untreated state. Treat-ment with levodopa in this patient restored the normalattenuation of the idling rhythms and was successful inreversing the bradykinesia evident when the task wasperformed without medication.

Such a dramatic response to levodopa was not uni-formly the case, and performance on the tracking taskactually deteriorated with treatment in two cases. As pre-dicted, however, changes in movement performance cor-related with drug-induced changes in the degree ofmovement-related attenuation of alpha and beta activitiesas measured from Fourier-transformed amplitude spectraof EEG. Thus, the change in attenuation of both activitiesrecorded over the sensorimotor, premotor, and prefrontal

cortices contralateral to the tracking hand correlated withthe change in relative movement amplitude (RMA) ef-fected by levodopa (Fig. 2A). In addition, the change inthe attenuation of the 10 Hz activity recorded over bothsuperior parietal areas also correlated with the drug-induced improvement in RMA. The latter areas, particu-larly the superior parietal lobule, participate in the con-trol of arm and hand movements and are frequently ac-tivated in positron emission tomography studies ofvoluntary movement.19–21

Previous studies of desynchronization in sensory areashave suggested that the attenuation of idling rhythmsmay have more to do with high-level attentional mecha-nisms than the computation necessary in response to af-ferent input.3 In the above, we chose a challenging taskthat drew heavily on attentional mechanisms. We there-fore requested subjects to fixate a stationary target andthen repeat the previously performed movements of thewrist from memory without visual feedback. Subjects

FIG. 1. Examples of the attenuation of alpha and beta activities during the tracking task in a single parkinsonian patient after drug withdrawal (A)and re-introduction of levodopa (B), and, for comparison, in a healthy 69-year-old subject (C). The attenuation of the slow idling rhythms duringmovement is diminished in the untreated state (A). Treatment with levodopa (B) restores the normal attenuation of the idling rhythms and reversesthe bradykinesia evident inA. The EEG recorded at C3 during the rest–pursuit period and the third cycle of tracking are displayed in each case. Theposition of the right wrist (bold line) has been superimposed over that of the target (grey line). EEG has been digitally bandpass filtered in the alpha(6–12 Hz) and beta (12–22 Hz) bands. The gains inC also apply toA andB. (D) Movement performance (mean RMA + SEM) in the 12 parkinsonianpatients during the tracking and nontracking tasks. Overall, movement size is increased with drug treatment regardless of task (p <0.01, pairedt test).In addition, movements made with and without antiparkinsonian treatment are bigger if made from memory (p <0.01, pairedt test). RMA 4percentage relative movement amplitude.

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found this easier, and in the untreated state, movementswere substantially bigger than when performed with vi-sual feedback (Fig. 1D). The correlations betweenchanges in percentage attenuation of the alpha and betarhythms and changes in RMA seen with treatment were

smaller than in the tracking task and only reached sig-nificance for the change in alpha band activity over thecontralateral sensorimotor and premotor areas (Fig. 2B).The regression coefficient linking changes in the alphaband with improvement in RMA over these areas was

FIG. 2. Correlation coefficients (r)for (% change in alpha band treated −% change in alpha band untreated)and (% change in beta band treated −% change in beta band untreated)versus the change in relative move-ment amplitude (RMA treated −RMA untreated) at each electrodesite in 12 patients with Parkinson’sdisease. The change in EEG ampli-tude in the alpha and beta bands (asmeasured from Fourier-transformedamplitude spectra) and the change inRMA were calculated from valuesobtained after overnight withdrawalof medication and, subsequently, 1–2hours after a single therapeutic doseof levodopa. (A) Tracking task. Thechange in percentage attenuation inboth the alpha and beta bands oversuperior parietal, sensorimotor, pre-motor, and prefrontal areas contralat-eral to the tracking wrist is signifi-cantly correlated with the change inRMA effected by levodopa. A simi-lar correlation is only seen ipsilateralto the moved hand for the change inalpha activity over the superior pari-etal region. (B) Nontracking task.Overall, correlations between thechange in percentage attenuation inthe alpha and beta bands and move-ment performance are less than in thetracking task and are only significantfor the contralateral sensorimotor andpremotor areas. The data have beennormalized to right hand movement(EEG records from left and rightsides of the head were reversed be-fore analysis in the five patients inwhom the left hand was tested.). Theposition of the electrodes with re-spect to the central sulcus is indicatedon the schematic head. 01/2, P3/4,C3/4, FC3/4, and F3/4 overlie the oc-cipital lobe, superior parietal lobule,and sensorimotor, premotor, and pre-frontal cortices, respectively.35,36

RMA 4 percentage relative move-ment amplitude.

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smaller than that seen during the tracking task (Fig. 3).Note that because movements performed in the untreatedstate were substantially bigger when copied frommemory than under visual feedback, similar increases inRMA in the two tasks entailed greater absolute increasesin movement amplitude in the nontracking task. How-ever, EEG desynchronization was still less in the non-tracking task.

DISCUSSION

Patients with Parkinson’s disease may have abnormalpatterns of movement-related attenuation of the alphaand beta rhythms.22,23 The major conclusion from thepresent study is that dopaminergic stimulation in Parkin-son’s disease restores the movement-related attenuationof the alpha and beta rhythms in a way that correlateswith improvements in motor performance. The levodo-pa-induced change in the EEG varied between tasks andspared both occipital areas even though visual input wasa critical element in the tracking experiment. The varia-tion between tasks was not related to the absolute move-ment amplitude, because EEG desynchronization wasless for a given increase in movement size when the wristmovement was repeated from memory. Thus, the levo-dopa-induced attenuation of idling rhythms was not sim-ply a reflection of the general level of cortical activity,the absolute amplitude of the movement, or the result ofa direct pharmacologic effect on the cortex. Instead, itseemed to be specific and restricted to those areas of thecerebral cortex involved in the motor task and receivingdirect or indirect projections from the basal ganglia.Wang et al. came to a similar conclusion in their studyof simple and complex arm movements in Parkinson’sdisease.24

The converse of the attenuation of the slow idlingrhythms during movement is the appearance of multiplecortical oscillations in the gamma band.11,12,15Such os-cillations are poorly recorded with scalp electrodes andwere not measured here. However, recent findings sug-gest that the normal Piper rhythm of muscle is dimin-ished in untreated parkinsonian patients, and the infer-ence is that the parallel gamma activity in the motorcortex that can be demonstrated magnetoencephalo-graphically is also lost.16,25Treatment with levodopa re-stores the Piper rhythm in muscle, just as it disruptslow-frequency oscillatory activity within the cortex.Thus, the present EEG findings and past EMG studiesare consistent with a role for the basal ganglia in releas-ing selected cortical elements from idling rhythms so thatthey may become coherent in the gamma range therebyfavoring those often distributed cortical activities neces-

sary for the selection and execution of a given motoract.1

Can this putative function of the basal ganglia be de-scribed in psychophysical terms? The attenuation of thealpha and beta rhythms bore only a superficial (propor-tional) relationship to the more basic aspects of move-ment organization, and instead seemed to vary in ampli-tude and distribution with the attentional demands of thetask. Thus, with treatment, the attenuation of idlingrhythms during movement performed from memory wasless marked and less extensive than that during visualtracking despite the greater movement amplitude seen inthe memory task. The influence of attention seemed in-dependent of voluntary or central effort. Five of the par-kinsonian patients spontaneously volunteered that thetracking task had been more taxing and demanding whenwithdrawn from medication compared with whentreated. The attenuation of idling rhythms off medica-

FIG. 3. Correlation between change in percentage attenuation in thealpha band and change in RMA on treatment in 12 patients with Par-kinson’s disease. The results from those two sites showing significantcorrelation in both tracking and nontracking tasks (contralateral senso-rimotor [C3/4] and premotor [FC3/4] areas) have been pooled becausethere was no difference in the regression coefficients between thesesites. During tracking (A) and nontracking (B), the correlation coeffi-cients for the pooled data were 0.733 and 0.600, respectively. Theregression coefficient during tracking (0.356) was larger than duringthe nontracking task (0.161, p <0.05), although the y axis intercept wassimilar. Note that the RMA declined with treatment in a minority ofpatients. Two subjects developed a disorganized and dyspraxic re-sponse to the tasks following treatment. Three more subjects consid-erably overestimated the size of the target movement when trackingfrom memory in the untreated state. Wrist movement in these subjectswas scaled more appropriately following treatment. RMA4 percent-age relative movement amplitude.

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tion, however, remained inadequate despite this extraeffort.

Mechanisms by Which Motor Idling Rhythms Maybe Modulated by the Basal Ganglia

Current theories of parkinsonism suggest that an ex-aggeration of pallidal output is a critical element in thepathophysiology of bradykinesia.26 The overactivity ofneurons in globus pallidus interna (GPi) in parkinsonismconsists of two elements: an increase in the firing rateand a change in the pattern of firing.27,28Normally, GPineurons tend to fire evenly and independently, with thevast majority of the remaining 5% or so oscillatory neu-rons bursting with a frequency greater than 20 Hz.27,29

GPi neurons in parkinsonian monkeys and patients havea greater tendency for burst discharge and synchroniza-tion, and this can be reversed by dopamine agonists.27,29

The frequency of the abnormal synchronous and oscilla-tory activity is approximately 4–10 Hz,28 and this is therange of stimulation rates in the inner division of thepallidum of animals which leads to synchronization ofthe EEG over cortical motor areas and to the gradual slow-ing and eventual cessation of spontaneous movements.30,31

Could this abnormal low-frequency synchronous andoscillatory activity in GPi act to hold the motor cortex inthe idling state in Parkinson’s disease? Such an effect oncortical rhythmicity could be mediated through the clas-sic projection of the basal ganglia to the motor areas ofthe cortex through the ventrolateral thalamus and theequally abundant connections to the more-or-less non-specific nuclei of the thalamus, particularly the ventro-anterior, mediodorsal, and centromedian nuclei.32 Neu-ronal activity in the specific and nonspecific nuclei tendsto oscillate with a frequency of approximately 40 Hz ondepolarization,33 and the effect of GPi overactivity andlow-frequency bursting in Parkinson’s disease might beto diminish these fast oscillations and their action on thecortex. This could be brought about by GABA-inducedhyperpolarization of thalamocortical neurons and dein-activation of low-threshold calcium channels triggeringshort bursts of high-frequency action potentials synchro-nized by and phase-locked to the pallidal bursts in muchthe same way as phasic GABAergic inputs from nucleusreticularis thalami may drive sleep spindles.34 The resultwould be a pervasive synchronization of cortical activityat frequencies of approximately 10 Hz.

The EEG findings reported here support a role for thebasal ganglia in controlling the release of cortical ele-ments from idling rhythms during voluntary movement.1

Thus, levodopa seems to have a specific effect on theorganization of motor cortical activity in the frequency

domain, an effect that correlates with improvements inbradykinesia.

Acknowledgments: The authors thank Dr. R. Brown forstatistical advice, Mr. P. Asselman for technical assistance, andDr. A. J. Lees and Prof. N. Quinn for permission to study theirpatients.

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