jaw movement dysfunction related to parkinson's disease ... · treatment improves specific...

Journal ofNeurology, Neurosurgery, and Psychiatry 1996;60:41-50

Jaw movement dysfunction related to Parkinson'sdisease and partially modified by levodopaLee T Robertson, John P Hammerstad

AbstractObjectives-To test the hypotheses thatParkinson's disease can differentiallyproduce deficits in voluntary and rhyth-mic jaw movements, which involve differ-ent neuronal circuits, and that levodopatreatment improves specific componentsof the motor deficit.Methods-Patients with idiopathicParkinson's disease and control subjectswere tested on a series of jaw motor tasksthat included simple voluntary move-ment, isometric clenching, and naturaland paced rhythmic movements. Jawmovements were measured by changes inelectromagnetic fields and EMG activity.Patients with Parkinson's disease withfluctuations in motor responses to lev-odopa were tested while offand on.Results-During the off state, patientswith Parkinson's disease were signifi-cantly worse than the control subjects onmost tasks. The deficits included adecrease in amplitude and velocity duringjaw opening and closing, aberrant pat-terns and low amplitude ofEMG activityduring clenching, and low vertical ampli-tude and prolonged durations of occlusionduring rhythmic movements. No decre-ments were found in the amplitude ofvoluntary lateral jaw movements or thefrequency of rhythmic movements.During the on state, improvementsoccurred in the patterns and level ofEMGactivity during clenching and in the verti-cal amplitude and duration of occlusionduring rhythmic movements, although asignificant decrement occurred in the lat-eral excursion ofthe jaw.Conclusions-Parkinson's disease affectsthe central programming of functionallyrelated muscles involved in voluntary andrhythmic jaw movements and levodopareplacement influences only certainaspects of jaw movement, most likelythose requiring sensory feedback.

CT Neurol Neurosurg Psychiatry 1996;60:41-50)

Keywords: mastication; Parkinson's disease; levodopa

Orofacial motor abnormalities have long beenrecognised in Parkinson's disease. -3 Includedin most textbook descriptions of Parkinson'sdisease is hypokinesia of the muscles of facialexpression and a reduced eye blink rate,resulting in a mask-like face.4 Many patients

also have difficulties in the production of clearspeech5 and with the automatic clearing of thethroat or swallowing.3 Although the sameperipheral structures are involved in variousoral motor acts, such as speaking, swallowing,or chewing, distinct basal ganglia circuits maybe used to generate the various motor pat-terns.6 The neural circuits involved in volun-tary movement of the mandible may bedifferent from those used for force productionwhereas those circuits regulating chewing mayinclude portions of circuits for voluntarymovement and force as well as additional cir-cuits to process specific sensory input. A majorbasal ganglia circuit is the projection from theglobus pallidus and substantia nigra reticulata,via the thalamus, to the primary motor cortex,the supplementary motor cortex, and the pre-motor area. Animal studies suggest that thesecortical areas help to control the initiation,direction, force, and internal guidance of vol-untary movements.68 A circuit that may influ-ence rhythmic jaw movements is a small directprojection from the substantia nigra reticulatato brain stem neurons, which have connec-tions with the trigeminal motor complex.9 10

Little information is available on howParkinson's disease affects the motor controlof the jaw. Connor and Abbs" showed thatpatients with Parkinson's disease haddecreased peak velocities and increased dura-tions in a visually guided vertical jaw move-ment task. Abbs and associates3 reported thatpatients with Parkinson's disease were unableto sustain a steady four to five second isometricforce using jaw closing muscles. However, thechanges in velocity and force occurred inpatients receiving dopamine replacement,which may have produced a motor deficitbecause of dyskinesia.4 Karlsson and cowork-ers'2 studied patients both on and off levodopatreatment and showed that levodopa increasedthe duration of the chewing cycle and theopening and closing velocities during peanutchewing.The present study examines the effects of

Parkinson's disease and the effect of dopaminereplacement on voluntary jaw movements, jawclenching, and rhythmic jaw movements. Abattery of jaw motor tasks was used to discernpossible involvement of different neural cir-cuits (for example, voluntary jaw movementsthat likely involve connections with the motorcortical areas versus rhythmic movements thatmay include connections with brain stem neu-rons), differences among various variables ofmovement (for example, velocity, amplitude,or force), and differences between internal and

Department ofBiological Structureand Function, Schoolof Dentistry, OregonHealth SciencesUniversity, Pordand,OR, USAL T RobertsonDepartment ofNeurology, School ofMedicine, OregonHealth SciencesUniversity, Portland,OR, USAJ P HammerstadCorrespondence to:Dr Lee Robertson,Department of BiologicalStructure and Function,Oregon Health SciencesUniversity, 611 S W CampusDrive, Portland, OR 97201,USA.Received 30 March 1995and in revised form28 June 1995Accepted 7 September 1995

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external signals to organise rhythmic jawmovements. By testing patients withParkinson's disease with major fluctuations intheir motor response to levodopa (the on-offphenomenon), we could determine whetherParkinson's disease, as manifested during theoff state, affects particular types of jaw motorcontrol and whether acute levodopa treat-ment, during the on state, is useful for all typesor only specific classes of jaw motor deficits.

Subjects and methodsSUBJECTSWe tested eight patients (six men and twowomen with a mean age of 53-7 years) withidiopathic Parkinson's disease (average dura-tion nine years) and 11 control subjects (ninemen and two women with a mean age of 54-4years) who were free of signs of neurologicaldisease. Routine examinations of the orofacialregion were made and included an examina-tion of intraoral structures; palpation of thetemporomandibular joints, muscles of mastica-tion, and associated muscles and tissues; andan assessment of the range of movement of themandible and any accompanying pain or jointsounds. All subjects had most of their normaldentition and no signs of malocclusion. Twocontrols and two patients with Parkinson's dis-ease had condyle displacement during theopening phase of the movement, but no evi-dence of pain and tenderness in the region ofthe jaw muscles and joints. All patients withParkinson's disease showed some reduction inthe range of normal jaw movement.

Patients were specifically selected becausethey displayed an on-off oscillating clinicalresponse to levodopa and did not show signs oforal-buccal-lingual dyskinesia. For the data col-lection, the patients with Parkinson's diseasehad refrained from all medication for 10 to 12hours and showed posture and locomotion dis-turbances when they entered the laboratory.During their off state, the patients withParkinson's disease reported that they had con-siderable difficulty with activities of daily living,were unable or barely able to walk, and severalreported having difficulty chewing or eating anentire meal. Their motor disability during theoff state ranged from stage 2 5 to 5 0 on theHoehn and Yahr scale.'3 After being tested inthe off state, the patients took their usual morn-ing oral dose of carbidopa-levodopa (Sinemet).Within one hour, they were independent inambulation and most other activities; their dis-ability according to the Hoehn and Yahr scaleranged from stage 2 0 to 2 5, with an averageimprovement of 1 4 from the off state. At theend of the test session, the patients took theirroutine doses of other medications (includingSinemet-CR, selegiline hydrochloride, per-golide mesylate, and bromocriptine mesylate).All subjects gave informed consent for the pro-cedures used in this study.

JAW POSITION AND MUSCLE ACTIVITYThree dimensional measurement of mandibu-lar movement was achieved with a model K6Kinesiograph (MyoTronics, Seattle, WA). A

small magnet was glued to a point below thelower central incisors and changes in the elec-tromagnetic fields were detected by magne-tometers mounted on a lightweight set ofeyeglass frames worn by the subject. The kine-siograph was interfaced with a microcomputerfor data display and analyses.

Recordings of the EMG activity of the rightand left temporalis and masseter muscles wereobtained with bipolar, silver-silver chlorideEMG electrodes placed in standardised posi-tions on the skin over each pair of muscles.For the jaw clenching task, the EMG activitywas differentially amplified, bandpass filtered(30 to 500 Hz), and full wave rectified.

EXPERIMENTAL DESIGN AND PROCEDURESPatients with Parkinson's disease were evalu-ated in two one-hour test sessions. The firsttest session was done while the patients werein the off state and the second test sessionbegan one hour after the patients took theirusual oral dose of carbidopa-levodopa (the onstate). A single test session was used for mostcontrol subjects because no difference wasfound between the first and second test sessionfor three subjects who were tested in two one-hour sessions with an hour of rest between ses-sions and because the performance of thecontrol subjects was not significantly differentfrom the results of a pilot study, which showedno difference between two separate one-hoursessions.The jaw motor tasks were performed while

the subject sat upright on a chair. Three typesof jaw motor tasks were given simple volun-tary jaw movements, brief isometric molarclenching, and natural and paced rhythmicmovements and were done in the samesequence for all subjects. All tasks began andended with intercuspal contact. The subjectswere given simple verbal instructions andallowed to practice the tasks two to threetimes. Each task involved several trials withabout 30 to 60 seconds of rest between trials;no information was given to the subjectregarding their performance.The voluntary jaw movements included

normal vertical opening and closing of themouth, opening the mouth as wide as possible,vertically opening and closing the mouth asfast as possible, and right to left horizontal jawmovements. Changing the conditions of thetask for example, from normal opening toopening wide or fast differentially activatesvarious muscle groups.'4 Measurements weremade on the amplitude, velocity, and variabilityof the jaw trajectory. For the isometric jawclenching task, the subjects were required tobite on a piece of gauze using their molarteeth. Due to the wide range in age and clinicalstatus of the patients with Parkinson's disease,the level of force during clenching was notspecified. Each subject performed a series ofthree two second maximal effort jaw clenches,with one second of rest between each clench.The series was repeated three times with oneminute of rest between each series. Measure-ments were made of the pattern, sequence,and amplitude of muscle activity.

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The natural and paced rhythmic jaw move-ments were evaluated by unilateral gum chew-ing. The cadence of the natural versus thepaced chewing provided information on inter-nal timing regulation versus the ability of thesubject to follow a rhythmic external signal.For the natural chewing, the subjects wereinstructed to first soften a piece of gum bychewing and then to chew the gum in theirhabitual manner on the right side for 60 sec-onds and, after a one minute rest, to repeat thetask for another minute. Paced rhythmic jawmovements at various frequencies wereincluded to disclose differences in jaw kine-matics and velocity.'5 The paced rhythmic jawmovement task involved making vertical jawmovements with tooth contact in time with aone, two, or three second auditory signal.Increasing the frequency of the paced move-ment also provided an indication of fatigue, asmore work was done at the higher frequenciesthan at 1/s. The paced rhythmic movementswere done for one minute and then repeatedafter a one minute rest. About 10 seconds afterthe subject began chewing, 10 seconds of data

were collected and another set of data was col-lected during the last 10 seconds of each oneminute trial for both the natural and pacedchewing tasks. A comparison between the firstand last 10 seconds of data provided anothermeasure of fatigue. Data were collected on therate and variability of the rhythmic move-ments, the vertical amplitude, and the dura-tion of occlusion, although accuratemeasurements of occlusion could not be madefor the 2/s and 3/s paced conditions.

STATISTICAL ANALYSISStatistical analyses were performed separatelyfor the results from each task. Student's t testwas used to the compare the differencesbetween the control subjects and patients withParkinson's disease. Differences in the perfor-mance between the off state (non-drug condi-tion) and the on state (dopamine replacementcondition) for each task were analysed using arepeated measures analysis of variance(ANOVA), followed by post hoc Student's ttests. The criterion for significance was set atP < 0 05.

Figure 1 Kinematics ofthree normal opening andclosingjaw movements for acontrol subject (A) and twopatients with Parkinson'sdisease (B). The controlsubject's traces were fromtwo test sessions separatedby one hour of rest; the datafor the patients withParkinson's disease werecollected during the off andon states. The verticalplane represents themaximal vertical openingbetween the start positionand the change betweenopening and closing phasesof the cycle; the horizontalplane represents velocityduring opening (traces onthe right side) and closing(left side) of the cycle. Theclosing phase begins whenthe opening velocity returnsto zero. During both offand on states, the patientshad lower verticalamplitude and decreasedvelocity than the controls.During the on state, theopening amplitudeincreased for one patient(P03) and the openingvelocities increasedfor bothpatients (P03 and P05).The midline is indicated bythe small vertical arrow.

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Figure 2 Means (SD)(error bars) of verticalamplitude (A) duringniornal opening and zwideopening, anid of the velocity(B) dur'ng nominal andfastopeninlg and closing.During off and onl states,the patienits zvithParkinson 's disease had areduced vertical amplitudefor both normnal openingand wide opening tasks andslozver velocities dur'ngnormnal anzdfast openinganid closing than thecontrols. *P < 0Q05;**P < o.oJ; ***P < 0*001v controls.

ResultsDuring the off state, patients with Parkinson'sdisease experienced some difficulty doingmost of the jaw motor tasks, including onepatient who was unable to move his jaw later-ally and two who were unable or declined todo the paced chewing at 3/s In the on state,the degree of improvement or decrement var-ied among the patients and the tasks. Six ofthe eight patients with Parkinson's diseaseimproved their performance on rhythmic jawmovements and improved or showed nochange in jaw clenching, and two of thesepatients also improved their vertical voluntaryjaw movements. However, one of the eightpatients only improved his voluntary verticaljaw movements and one had performancedeficits on all the behavioural tasks.Unexpectedly, most patients reduced theirability to move the jaw laterally during the onstate. In this section, we describe for each taskthe differences between the patients withParkinson's disease during the off state andthe control subjects and then the differencesbetween the off and on states.

VOLUNTARY JAW MOVEMENTSEven for the simplest voluntary movement ofopening and closing the mouth, patients withParkinson's disease had restricted movement,both in amplitude and opening and closingvelocities, although the amplitudes and veloci-ties were generally consistent from trial totrial. Figure 1 shows examples of the ampli-tudes and velocities of three normal openingand closing cycles for a representative controland two representative patients withParkinson's disease. During the off state, thepatients showed a reduced maximal verticalamplitude and opening velocity in comparisonwith the control subjects, one patient (P03)also had a slow closing velocity, and one (P05)had some trial to trial variability in his closingvelocities (fig iB). Comparing the on statewith the off state, one patient (P03) increasedhis maximal vertical opening and the openingand closing velocities, although they were still

worse than the control's performance. Theother patient (P05) slightly reduced his maxi-mal vertical opening and closing velocity, butslightly increased his opening velocity.

Patients with Parkinson's disease were sig-nificantly worse than the control subjects formaximum vertical amplitudes and velocitiesfor normal opening and closing, opening wide,and opening fast tasks (fig 2). During the offstate, the maximal vertical amplitude duringnormal opening by patients was about 30%lower than the amplitude of the control sub-jects. During the on state, four patients had a5% to 15% increase in vertical amplitudecompared with the off state but three had a30% to 61% decrease in amplitude. The aver-age vertical amplitude during the on state wassignificantly (P < 0-001) lower than the con-trol condition but was not significantly differ-ent from the off state. For the opening widetask, there was little change between the offand on states, with the vertical amplitudes forboth off and on states being significantly less(P < 0 01) than the controls.The maximum velocities during normal

opening and closing were significantly(P < 0-05) slower for patients with Parkinson'sdisease during the off state than for the controlsubjects (fig 2B). The average opening and clos-ing velocities did not change during the on statecompared with the off state. When making fastvertical jaw movements, the control subjectsincreased their opening and closing velocities byabout 50% in comparison with the normal situa-tion. The patients with Parkinson's disease alsoincreased their velocity by about 42% but theywere still significantly (P < 0 001) slower thanthe control subjects for both the opening andclosing phases. No significant differences werefound between the off and on states for theopening and closing velocities or for the normalversus the fast conditions.The lateral movement of the jaw was

included in the test battery because it was amovement that the subject did not make rou-tinely, so it required conscious control. Thetask required several practice trials by both

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Figure 3 Fronital planevi'ew of the ki'nemtati.cs Oflateralljaw movements Ofseveni pati'ents wi'thParkinson's di'sease (oniewas unable to mtove hi's jawlaterally during the offstate) and tworepresentative conitrolsubjects. For the pati'ents,the first and seconid trialsare shown for both off andon states; for the controls,the first and second trialsare shown for each subject.Although the ki'nemiaticsbetween trials were simtilar,considerable variabilityoccurred between patients.Five patients with.Parkinison's di'sease (P07,P01, P06, P03, and P05)had less total right to leftlateral excursion during theon state than during the offstate. Some subj'ectsrequi'red a final lateralmnovemtent to achi'evei.ntercuspal occlusion(arrow).

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On

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P05

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Controls

2nd trial

groups and one patient was unable to make

lateral jaw movements during the off state

(this patient's data were not included in the

statistical computations). Variability in the

vertical and the right to left horizontal ampli-

tudes of the movement was evident among the

controls and patients with Parkinson's disease

(fig 3). However, all except one patient (P06)

had consistent trial to trial kinematics, and all

except two patients (P06 and P08) had sym-

metric right to left movements, The right to

left distances averaged 18-7 mm for the con-

trols and 15S4 mm for patients and were not

significantly different.

During the on state, the total right to left

excursions decreased by about 6 1 mm, which

resulted in a significant (P < 0-05) difference

between off and on states. Six patients with

Parkinson's disease were worse during the on

state than during the off state, including two

with reduced total lateral excursions of more

than 70% (for example, the average for patientP07 went from 15 mm to 6-6 mm total excur-

sions). For several patients, the kinematics of

the lateral movement during the on state were

also more complex than during the off state

and often included difficulties in achieving

final intercuspal occlusion (fig 3: P01, P06,

P03, and P02).

ISOMETRIC JAW CLENCHING

During the off state, none of the patients with

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Figurc 4 Rectified EMGactivity of the lefttemnporalis (LT) andiniasseter (LM) musclesduring three isomzetric jawcleniches for a representativeconitrol subject (A) andthree patienits withParkinson 's disease duringthe off (B) and On (C)states. In the representativeconitrol subject (A), the leftmnasseter muscle had greateractivity than the lefttemporalis muscle, whichwas similar for half of thecontrol subjects whereas thereverse was true for the restof the controls. During theoff state, none of thepatients had a nornalpattern ofEMG activity(subject P01 had an EMGpattern that zwas m1ostsi7nilar to the controlpatteni, zwhereas P06 wasthe least simnilar). Duringthe on state, an imnprovedpattern ofEMG activity isrepresented by patients P01and P06, whereas subjectP05 represents little change.

A Control

C09

B Off state

LT

P01

C On state

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P05 LS_ - - -------i-

------------------------------------ ------ -------~~~~~~~~~~~~~~~~~~~~~~~~~~~~

P06

-------------r-------t-- -------r-------o--------t-------- r--- ----t------- ---------

-----------------J ---t-----W ------- ----------X ------- ---l-- L

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..i1i. Li_

Parkinson's disease had a pattern of EMGactivity to clenching that completely resembledthe EMG pattern of control subjects, althoughtwo patients had activity in one of the fourmuscles recorded that resembled the controlcondition (fig 4B, P01). The pattern of EMGactivity for each two second episode of clench-ing by the control subjects consisted of a sharponset of activity for each muscle that quicklyreached peak amplitude and then graduallydecayed until the verbal signal to relax, afterwhich there was sharp, synchronous termina-tion of activity, followed by an absence ofactivity during the rest phase (fig 4A). Duringthe off state, patients with Parkinson's diseaseexhibited a variety of patterns ofEMG activityto clenching (fig 4B). The abnormal EMG pat-terns included no clear onset or offset of activ-ity, very low amplitude of activity in one ormore of the muscles, a slow rise to peak ampli-tude, a rapid decay of activity, brief (< 1 s) sus-tained activity, and failure to return to baselineduring the rest period.

During the on state, five of the eightpatients showed improvements in the patternof EMG activity, two had minimal change,and one was worse. Although no consistentpattern of improvement was evident amongthe patients with Parkinson's disease,improvements included an absence of inap-propriate activity during the rest phase (fig 4C,P01), an increased duration of activity (fig 4C,P05), and a more well defined onset and ter-

1 s

mination of activity (fig 4C, P06). Theabsence ofEMG activity during the rest phasecorresponds with the absence of involuntaryjaw movements (mandibular dyskinesia) dur-ing the on state. The average peak amplitudeof EMG activity (120 (SD 34) ,V) of the jawclosing muscles during clenching for patientswith Parkinson's disease while in the off statewas lower than the average (215 (SD 102) pV)for control subjects, but they were not signifi-cantly different. During the on state, the aver-

age peak EMG activity increased by about28% but was not significantly different fromthe off state.

RHYTHMIC JAW MOVEMENTSAll subjects were easily able to chew the gumfor one minute and to make the paced move-ments at 1/s and 2/s. Several controls andpatients with Parkinson's disease reported thatthe movements at 3/s were fatiguing and thatthey had problems maintaining the frequency;two patients declined to preform the 3/s pacedmovement. However, no significant differ-ences were found in the cycle frequency or thevertical amplitude of the opening cyclesbetween the first and last 10 seconds of theone minute trial of normal chewing or for anyof the paced movements. Consequently, thefirst and last 10 seconds of data were com-bined for the present analysis.The mean vertical amplitude of the opening

phase was significantly less (P < 0-05) for

LT

LM

LM -

LT

LM

LT

LM

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Figure 5 Mean (SD) ofthe vertical amplitude (A)and the duration ofocclusion (B) duringnormal chewing and pacedjaw movements (nomeasurements of occlusionwere made for the 2 and 3/spaced tasks). During theoff state, the verticalamplitude was significantlyreduced during normalchewing and the 1/s pacedcondition and the durationof occlusion weresignificantly increasedduring the 1/s paced task.*P< 0-05.

Patients with Parkinson's disease during the offstate than for the control subjects for normalchewing and the 1/s paced movement (fig 5A).The average vertical amplitudes during the 2/sand 3/s paced movement were also lower thanthe controls but were not significantly differ-ent. During the off state, the duration of theocclusal phase during normal chewing wassimilar to the control subjects, but was signifi-cantly (P < 0 05) longer than the controlcondition during the 1/s paced movement(fig 5B).The vertical amplitude during the normal

chewing and the 1/s paced movementincreased slightly more than 4 mm betweenthe off and on states. This resulted in a signifi-

Figure 6 Percentagedifference between thecontrol subjects and thepatients with Parkinson'sdisease during the off stateand between the off and onstates for variables of thejaw motor tasks.Parkinson's disease wasassociated with deficits inall categories except thefrequency of rhythmicaljaw movements. Levodopatreatment (on state)produced improvement inthe amplitude ofEMGactivity during clenchingand in the openingamplitude and duration ofocclusion during therhythmicaljawmovements, but caused adecrease in the amplitudeof the lateraljawmovement and, in a fewpatients, a decrease ofvertical amplitude duringnormal opening.

cant (P < 0 05) difference between the off andon states but no significant difference betweenthe on state and the controls (fig 5A). Theduration of occlusion for the 1/s paced move-ment during the on state was also similar tothe control condition. In addition, the twopatients who were unable to do the 3/s pacedmovement during the off state, had an appro-priate frequency and vertical amplitudes dur-ing the on state.

DiscussionThe present study shows that Parkinson's dis-ease affects more variables of motor control ofthe jaw than indicated by previous reports3 11 12

Voluntirv jawaN vemen'etS

Clench .X119

Rhythm-iic jaw movements

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and that dopamine replacement seems to tar-get only specific jaw motor deficits (fig 6).During the off state, Parkinson's disease isassociated with large deficits in several vari-ables of voluntary jaw control, jaw clenching,and rhythmic jaw movements. Most of the vol-untary jaw movements were of low amplitudeand slowly executed, similar to the characteris-tic bradykinesia of voluntary limb move-ments,4 the EMG activity was abnormal in allpatients with Parkinson's disease during iso-metric jaw clenching, and the vertical ampli-tude during chewing was low. However,Parkinson's disease had little influence oncycle frequency during either normal chewingor paced movements during the off state andonly a few patients had difficulties making lat-eral jaw movements or had prolonged occlusaldurations during rhythmic jaw movements. Anoral dose of levodopa (the on state) producedimprovements, in comparison with the offstate, in the jaw clenching and in the verticalamplitude and duration of occlusion duringrhythmic movements. A few patients alsoimproved the velocity of their fast voluntaryjaw movements. However, levodopa treatmentalso resulted in a decreased amplitude of lat-eral jaw movements and, in a few patients, thevertical amplitude during normal jaw opening.A limitation of the present study was the

variability between patients of the motorimpairments, which was most likely related tothe unique features of the disease process andthe variability of the therapeutic benefits ofdopamine replacement. Patients withParkinson's disease displayed a wide range ofperformance on each task during both the offand on states. For example, most patients hadnormal lateral jaw movements during the offstate but one patient was completely unable tomove his jaw laterally. The changes in perfor-mance related to levodopa ranged from onepatient who achieved improvements on alltasks to another who was worse on all tasks.The individual differences were not correlatedwith the severity or duration of the disease, thedegree of improvement of the Hoehn andYahr scores between the off and on states, orthe patients' age.Some performance deficits of the patients

with Parkinson's disease may be related totemporomandibular disorders (TMDs)because of their limited range of vertical andlateral movements and the abnormal patternofEMG activity. Miller4 described neuromus-cular changes of TMD, including decreasedEMG activity during clenching, increasedduration of the masticatory discharge, andspastic discharges. Although the EMG activityof the patients with Parkinson's diseaseincluded some EMG characteristics of TMD,none of the patients showed symptoms of ten-derness and pain to palpation of theirmandibular and cervical muscles, which ismost often the initial symptom of the TMD.'6Further, there is little evidence to support theidea that variables of jaw movement and EMGactivity are good predictors of TMDs inasymptomatic subjects.7

Peak dose dyskinesia can account for per-

formance decrements.4 Because the patientswith Parkinson's disease were specificallyselected to be free of cranial-cervical dyskine-siae, they did not show any oral-buccal-lingualdyskinesia during the on state. Further, duringthe on state of isometric jaw clenching, theabsence of masseter and temporalis EMGactivity during the rest phase corresponds withthe absence of involuntary jaw movements.Even the patient with decrements on all thejaw motor tasks had no obvious dyskinesia. Inthis patient, levodopa resulted in considerableimprovement in posture and locomotion, buthindered her fine hand movements, such aswriting, which may correspond to her deficitsin jaw motor control. In this discussion, weevaluate the influence of Parkinson's diseaseand levodopa on the various jaw motor tasksand then consider how levodopa treatmentmay affect jaw motor control, while acknowl-edging that for a few patients other unknownmechanisms may be operating.

Disease or drug induced alterations of spe-cific neural circuits may account for perfor-mance decrements during the off state orbetween off and on states. The voluntary jawmovement tasks used in the present studywere designed to test the pallidothalamocorticalconnections with different cortical motorareas,(-) which then project to interneurons ofthe gigantocellar reticular formation near thetrigeminal motor nucleus.'8I'9 In the presentstudy, Parkinson's disease resulted in deficitsin the velocity and vertical amplitude of volun-tary jaw movements made on command,movements that are likely regulated by motorareas of the cortex. Connor and Abbs" alsohave noted that Parkinson's disease results indecrements in the velocity:amplitude ratios ofvisually guided jaw movements, but not forsimilar movements made during speech.These investigators" suggested that the decre-ment during the visually controlled task wasbecause the task was unfamiliar or unnatural,whereas the jaw movements made duringspeech were embedded in a natural sequence.The simple task of voluntary opening and clos-ing of the mouth, used in the present study,was obviously a familiar task, which suggeststhat the deficit was probably in the corticalcontrol of voluntary movement. This idea issupported by the similar deficits for normalopening versus wide opening and for normalversus fast opening and closing, though thedifferent tasks activated different combina-tions of muscles and sensory feedback.'4Although patients with Parkinson's diseasecould increase their amplitude and velocity ofjaw opening, their level was consistently belowthat achieved by control subjects. Theseresults are consistent with the recent findingsfor arm movements2' and postural adjust-ments21 of an inability of patients withParkinson's disease to scale up the magnitudeof a movement when increased speed or force isrequired.Not all voluntary jaw movements were

affected by Parkinson's disease or unaffectedby levodopa. The amplitudes of the lateral jawmovements during the off state were not dif-

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Jaw movement dysfunvction related to Parkinson 's disease anid partially modified by levodopa

ferent from control subjects, but during the onstate, were significantly reduced. This was justthe opposite of the levodopa effects on verticaljaw movements. We initially expected that allvoluntary jaw movements would have reducedamplitudes and that less practiced movementswould have a greater deficit than the familiarmovements. The lateral jaw movement taskwas initially not easy for the patients to exe-cute, as they all required several practice trials.Consequently, the lateral jaw movement taskmay have involved learning whereas the verti-cal movement tasks were already well learnedmotor patterns. If the basal ganglia provide amechanism to suppress unwanted movementsduring the acquisition of a movement," thenperformance of the lateral movement shouldhave been worse during the off state than thatof the control subjects, which was not the case.Another possible explanation is that the lateraland vertical jaw movements involve differentneural circuits. For example, lateral jaw move-ments have a different cortical representationthan the jaw closing representation in themotor cortex,2324 which may also occur for theother motor cortical areas.The negative effects of levodopa were also

not expected. During the on state, patientswith Parkinson's disease showed mild to severereductions in the amplitude of the lateral jawmovements, even though levodopa was associ-ated in these patients with improvements invarious aspects of rhythmic movements andjaw clenching. The negative effect of levodopaon a specific task is consistent with negativeeffects of levodopa for lateral head move-ments23 and postural adjustments.2' Furtherinvestigation will be required to decidewhether the deficit induced by levodopa in lat-eral jaw movements is related to variables inthe acquisition of the motor task, particularitiesof the neuronal circuits, or other reasons.The isometric jaw clenching task was

included as another task involving the pallido-thalamocortical circuit, particularly those con-nections with the primary motor cortex, whichanimal studies have shown to be important inregulating force.26 A deficit in force productionand maintenance is suggested by the low levelof EMG activity during isometric jaw clench-ing by patients with Parkinson's disease, as theEMG activity during isometric clenching islinearly related to the total tension force devel-oped by the muscles.2 Reduced force produc-tion by patients with Parkinson's disease hasbeen noted in tasks involving the upperextremities28 and the orofacial muscles of thelip, tongue, and jaw.3 In the present study, allpatients showed some abnormal EMG activityduring isometric clenching, although the peakamplitude of EMG activity in patients withParkinson's disease was not significantly dif-ferent from the controls due to the high vari-ability between patients. Some of thisvariability may have occurred because theinstructions did not specify the amount offorce to be reached, slight differences in theEMG electrode placement, and variations infacial dimensions and size of the jaw closingmuscles.4 However, these factors were min-

imised by comparing the same patient duringthe off and on states, which showed thatParkinson's disease influenced both the pat-tern and amplitude of EMG activity duringclenching. Levodopa treatment producedmixed effects, including improved onset andoffset of EMG activity and large increases inEMG amplitude, although a few patients haddecreases in amplitude. Although single unitactivity of neurons in the basal ganglia ispoorly correlated with EMG activity, ' areduction in thalamocortical activation mayprevent the motor cortex from generatingappropriate commands.

Rhythmic jaw movements that occur duringmastication are mainly controlled by brainstem neurons. The basal ganglia can influencerhythmic jaw movements through direct pro-jections from the substantia nigra reticulata toparvicellular reticular neurons of the brainstem,"3" which form direct connections withneurons controlling the jaw closing muscles.'Parkinson's disease influenced the verticalamplitude and the durations of occlusion ofinternally (self induced) and externally pacedrhythmic movements, suggesting either thatthe tasks involved similar circuits for internaland external control or that Parkinson's dis-ease does not influence the internal versus theexternal control of a movement. Althoughinternal control versus synchronisation with anexternal signal may involve separate neuronalcircuits,8 there is also evidence from animalexperiments that parts of the striatum, outsidethe motor region, are activated by both inter-nal and external stimuli before a motorresponse.3' 32

Levodopa increased the vertical amplitudeand decreased the occlusion duration enoughthat there was no significant differencebetween the on state and the control subjects.Karlsson et al ' noted similar findings forpeanut chewing during off and on states. Thesimilarity of the results between gum chewing,vertical paced movements, and chewingpeanuts is remarkable, as the size, shape, andhardness of the food are known to influencethe pattern of chewing movements, theaccompanying EMG activity, and the force-time curves."33 4

Because both the jaw clenching and therhythmic movements tasks benefited from lev-odopa, they may share important commonfeatures, such as access to sensory stimuli.Achieving appropriate force levels duringclenching or chewing depends on feedbackfrom receptors in the periodontal region of thedentition, the temporal-mandibular joint, andthe muscles and ligaments,"1 although animalstudies have shown that muscle spindles ortemporal-mandibular joint receptor afferentsdo not influence the frequency of rhythmic jawmovements.35 The dopaminergic circuits mayparticipate in the processing of sensory infor-mation or in the regulation of access of sensoryinput to appropriate motor centres.2 Patientswith Parkinson's disease show deficits in testsof orofacial sensory function and sensorimotorintegration,2 although they also exhibit hyper-sensitivity to cutaneous stimuli as part of a

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perioral reflex3' and alterations of varioustrigemotrigeminal or trigemofacial reflexes.37Thus the dopamine induced improvements ofclenching may result from better processing ofsomatosensory stimuli within the brain stemreticular formation.The results of this study support the idea

that Parkinsonism does not alter just one typeof jaw movement but affects several variablesof voluntary and automatic movement, con-firming the conclusions of animal studies.sxParkinson's disease seems to affect behavioursthat are probably controlled by ascending con-nections with various cortical areas anddescending projections to the brain stem.However, the present data support a limitedrole for dopamine replacement in motor con-trol of the jaw. The dopaminergic system mayimpact the general motor control of the limbsand posture in various ways but, for jaw motortasks, the dopaminergic influence seemsrestricted to a few tasks, possibly those involv-ing a particular type of sensory feedback.

We thank Dr Hiroshi Ueno for assistance with the oral exami-nation and the use of the kinesiograph. We also appreciate theexcellent technical assistance of Mary Dennis and CharellMelfi. This work was supported by NIDR grant DE10395.

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