ORIGINAL ARTICLE

Steven Morrison á Karl M. Newell

Bilateral organization of physiological tremor in the upper limb

Accepted: 22 May 1999

Abstract The bilateral patterns of physiological tremorin the upper limb of adults were examined under con-ditions where eight combinations of the elbow, wrist andindex-®nger joints of the right arm were braced usingindividually molded splints. The hypotheses tested werethat: (a) coordination of upper-limb tremor involves(compensatory) coupling of intra- but not inter-limbsegments, (b) splinting the respective joints of the rightarm changes the organization of this synergy in bothlimbs, and (c) reducing the involvement of joint-spacedegrees of freedom through restricting their motion (bysplinting) results in increased tremor in the distalsegments. Under no-splinting conditions, signi®cant re-lationships were only observed between adjacent (intra-limb) e�ector units, with the strength of the correlationincreasing from proximal to distal. Splinting the rightlimb resulted in an increase in the strength and numberof signi®cant intra-limb relationships in both limbs. Nointer-limb tremor relationships were found between anysegment during this task, irrespective of the splintingcondition. The frequency pro®le for the tremor in eachlimb segment showed two prominent frequency peaks(at 2±4 Hz and 8±12 Hz). A third, higher frequency peak(18±22 Hz) was observed in the index ®ngers only.Splinting the right limb produced a general increase inthe amplitude and variability of tremor in the ®ngertipof both arms. This e�ect was particularly strong underconditions where the more proximal joints were splinted.The lack of any between-limb relationships, coupledwith the fact that splinting one limb in¯uenced bothlimbs, suggests that some form of linkage does exist

between the limbs. It is unlikely that mechanical linkagescan explain fully these relationships. It is proposed thatthe tremor observed in either limb represents the outputof a central oscillatory mechanism(s), but that this out-put is subsequently independently ®ltered in a parallelfashion on its way to each respective limb. A commonbilateral (compensatory) strategy is employed to mini-mize the tremor in either limb during this multiple-de-grees-of-freedom task.

Key words Posture á Physiological tremor á Bilateral áCompensatory synergy

Introduction

The sustained maintenance of a postural position ischaracterized by periodic, involuntary oscillation in theoutstretched limbs; a feature that is referred to asphysiological tremor (Marsden 1984; Elble and Koller1990). Obviously, minimization of these oscillations isone goal of the motor system, although our under-standing of how this is achieved is complicated by thefact that tremor changes across di�erent limb segmentsand body positions. Furthermore, the tremor in anygiven limb represents the combined output of a numberof di�erent oscillatory sources, including the naturalresonant properties of the limb segment and neural in-puts of central and peripheral origin (Marsden 1984;Elble and Koller 1990; Elble 1996; Britton 1997).

Various approaches have been employed to examinethe contribution of neural and/or mechanical factors tolimb tremor in human subjects. One approach for ex-amining tremor characteristics has been to apply externalconstraints, such as loads, to alter limb inertia (Stilesand Randall 1967; Joyce and Rack 1974; Elble 1986;HoÈ mberg et al. 1987), or to block neural and/or cardiacinput through temporary dea�erentation (Marsdenet al. 1969a,b). While changing external constraints doesprovide some appreciation of the relative contribution ofmechanical and neural factors to tremor, these studies

Eur J Appl Physiol (1999) 80: 564±574 Ó Springer-Verlag 1999

S. Morrison (&)School of Physiotherapy and Exercise Science,Gold Coast Campus, Gri�th University,PMB 50, Gold Coast Mail Centre,Queensland 9276, Australiae-mail: s.morrison@mailbox.gu.edu.auTel.: +61-7-55948917; Fax: +61-7-55948674

K.M. NewellThe Pennsylvania State University, Pennsylvania, USA

have, by design, been limited to examining oscillations ina single e�ector within a single limb.

An alternative means to examine the nature of tremoris to investigate tremor between limbs. Bilateral studiesof tremor have reported a symmetrical nature to thedegree of tremor in either wrist (Arblaster et al. 1990;Lakie et al. 1994), although the tremor in any segmentappears to be unrelated to that observed in any con-tralateral e�ector (Marsden et al. 1969a,b; Morrisonand Newell 1996; Newell and Sprague 1996).

The proposed symmetry of tremor between homo-lateral limb segments, coupled with the lack of any inter-limb relationships poses an interesting question as to thegeneration and control of this tremor. Two di�erentperspectives have been proposed to answer this question.One is that the pattern of linked tremor relationships isderived primarily from mechanical coupling betweensegments, with the resultant tremor output being inde-pendent of any signi®cant neural or voluntary coordi-nation. Thus, tremor similarities between limbs merelyrepresent the fact that each limb has similar biome-chanical properties (Stiles and Randall 1967; Elble andRandall 1978; Walsh 1992; Lakie et al. 1994).

The converse perspective is that a signi®cant pro-portion of tremor is derived from a centrally drivenneural oscillatory mechanism(s) (Lippold 1970; Llinas1984; Elble 1996; Britton 1997; Llinas and Pare 1997).The lack of any inter-limb relationships indicates thatthe tremor in each limb is derived from two (or more)independent oscillatory mechanisms, with the neuraloutput to a single limb being generated in a parallelfashion, independent of the neural signals that are re-layed to the other limb (Marsden et al. 1969a,b; Steinand Lee 1981). It should be noted that such an oscillatoris almost certainly not con®ned to a single neuralstructure, but is spread over a number of structuresthroughout the neuroaxis (Bernstein 1967; Llinas 1984;Elble and Koller 1990; Elble 1996).

One concern regarding the aforementioned studies ofbilateral tremor is that they have only compared oscil-lations within a single e�ector unit of each limb. Thus, itmay be that a clearer understanding of the contralateraltremor relationships can be gained from examining thetremor from more than one limb segment within a singlelimb. This would provide a means with which to in-vestigate the organization of tremor both between- andwithin-limb from a multiple-degrees-of-freedom per-spective. Furthermore, constraining the motion (tremor)of a single limb would permit an indirect examination ofthe assumption that the tremor in each limb is inde-pendent of oscillations in the contralateral limb.

We investigated the question of the intra- and inter-limb tremor relationships by manipulating the dynamicproperties of a single limb through the application oflightweight splints, which constrain two or more adja-cent limb segments to operate as a single unit (Trombley1989; Canelon 1995). If there is a strong central commoncomponent to the tremor in each limb, it would be hy-pothesized that the splinting in one limb would lead to a

new common pattern of organization in both thesplinted and unsplinted limbs that is distinct from thecompensatory organization found in the natural armtremor task (Morrison and Newell 1996). Alternatively,if the tremor in each limb is unrelated, then the e�ect ofsplinting one limb on the tremor in the contralaterallimb segments should be negligible.

The splinting manipulation also allows the examina-tion of how the tremor is controlled in multiple upper-limb degrees of freedom. Presumably, the goal of themotor system in any postural task is to minimize the in-trinsic oscillations of a limb, a goal that begs the question;how does the motor system achieve this? At least tworelated motor problems can be identi®ed when consid-ering this question in relation to postural pointing tasks.The ®rst is the conceptual and fundamental problem ofcoordinating the many degrees-of-freedom that need tobe controlled during movement (Bernstein 1967). Thesecond is the more local problem of controlling thetremor in each limb segment. This local problem is con-founded by the di�erent oscillatory sources underlyingthe tremor, which combine to constrain the more generaldegrees-of-freedom problem of realizing an adaptive co-ordination solution to the demands of the task.

In summary, this study was designed to examine thebilateral organization of physiological tremor and toestablish what form the changes in tremor each limbsegment take following splinting of a single limb. Cur-rent thinking dictates that little or no alteration in intra-limb relationships in the unsplinted limb should befound as a result of splinting the other limb. In addition,the Bernstein (1967) degrees-of-freedom perspective(and basic mechanical principles) anticipate that thegeneral amount of activity at the distal ®nger segmentwould increase due to the progressive splinting of moreproximal arm segments (reduced degrees of freedom),but that this e�ect should not translate to the unsplintedlimb. These issues were examined in this study, wherebythe e�ect of selected splinting of joints within one armon the organization of within- and between-limb tremorwas investigated.

Methods

Subjects

Nine neurologically normal male adult student subjects (meanage = 24.7 years; range 20±32years)withnoknownhealthproblemsparticipated in this study.Of the nine subjects tested, four reported tobe left-hand dominant. All subjects volunteered to participate in thisstudy and all provided informed consent prior to testing. The O�ceofRegulatoryCompliance, Pennsylvania StateUniversity, approvedall of the experimental procedures used in this study.

Apparatus

Eight uniaxial Coulbourn (T45-10) accelerometers were positionedon the right and left upper limbs, on the following anatomicallandmarks (from proximal to distal): on the upper portion of theupper arms ± approximately 3 cm lateral to the belly of the biceps

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brachialis muscle; on the forearms ± the belly of the brachioradialismuscle; on the hands ± midway down the shaft of the third meta-carpal bone; and on the dorsal distal aspect of the index ®nger. Allaccelerometers were attached securely to the underlying tissue.These accelerometers measured the oscillations of the limb seg-ments in the vertical plane of motion.

Absolute acceleration levels were obtained by zero-balancingeach accelerometer in DC mode in a horizontal position on a levelsurface. Each accelerometer signal was ampli®ed through a Co-ulbourn transducer coupler (S72-25) with an excitation voltage of5 V and a gain of 1000. All acceleration data were sampled at90 Hz and collected on a 386 IBM-compatible computer through a12-bit analog-to-digital converter. A signal-to-noise ratio of ap-proximately 10:1 was observed for all accelerometers. The accel-eration data were ®ltered using a Digital Butterworth low-pass®lter with a cuto� frequency of 30 Hz. This cuto� frequency wasselected since there was little power in the frequencies of tremorabove 30 Hz; a result similar to that reported previously (Elble andKoller 1990; van Emmerik et al. 1993).

Splints for the joints of the index ®nger, wrist and elbow of theright limb were made for each subject using a ¯exible thermoplasticsplinting material (Aquaplast WFR, Aquaplast, Ramsay, N.J.,USA). The ®nger splint weighed 18.7 g, measured 16.2 cm by1.9 cm and was designed to restrict ¯exion and extension of theindex ®nger about the second metacarpophalangeal and the distal,middle and proximal interphalangeal joints. The wrist splintweighed 20.8 g, measured 14.7 cm by 4.2 cm and was designed torestrict ¯exion and extension movement about the distal radio-carpal joint. The elbow joint splint weighed 28.5 g, measured25.7 cm by 8.1 cm and was designed to restrict ¯exion and exten-sion movement about the humero-radial and humero-ulnar joints.All splints were attached tightly about the respective joint usingadjustable Velcro straps. During the application of the splints, carewas taken to ensure that no splint was in direct physical contactwith any other splint, or that they overlapped more than the in-tended joints for which they were designed.

Procedures

Subjects participated in nine testing conditions that were completedwithin a single session. Each condition related to a di�erent level ofjoint splinting. Splints were applied to only the right arm through-out the duration of the testing period. The conditions were: nosplinting of any joint (control condition, CL); loose splinting (LS);index ®nger splinted only (FS); wrist joint splinted only (WS); elbowjoint splinted only (ES); wrist and ®nger joint splinted (WF); elbowand ®nger joint splinted (EF); elbow and wrist joint splinted (EW);and elbow, wrist and ®nger joint splinted (All). Under the loosesplinting (LS) condition, the Velcro straps attaching the splints wereloosened so that they hung o� the subjects' arm and did not restrictjoint motion. This condition was included to examine the e�ect ofthe extra mass of the splints on the tremor for each limb segments.Eight trials were performed for each condition. Each trial lasted fora period of 30 s. The order in which the splinting conditions werepresented was randomized between subjects.

All subjects sat on a stool with no back support that was ad-justed to a comfortable sitting height. Subjects positioned theirarms parallel to the ground with their ®ngers pointing directlyahead. The positions of the upper limbs were as follows: shoulders¯exed 90 degrees in the sagittal plane with the elbow fully extended,forearm pronated and wrist held in the neutral position. The index®nger was extended at the metacarpophalangeal joint with thethumb adducted and ®ngers 3, 4 and 5 fully ¯exed. The task goal,which was made explicit to the subjects, was to minimize motion ofthe tips of the index ®ngers. Figure 1 illustrates the experimentalsetup for the CL condition.

Data analysis

Acceleration data were analyzed in both the time and frequencydomain, as a function of limb segment, level of limb support, andtrials. Data analysis was structured into two sections.

Analysis of individual segment tremor

Two time-domain analysis techniques were applied to the tremordata. Each raw acceleration signal was recti®ed and the absolutemean and standard deviation of tremor amplitude for each segmentwas determined. Second, analysis of the structure or regularity ofthe accelerometer (tremor) signal was conducted using a measure ofapproximate entropy (ApEn) (Pincus 1991). Signals that are ran-dom in nature produce a higher ApEn value (close to two), whilelower values (tending towards zero) are observed for signals thatdisplay high regularity in their time-series pro®le. In the context ofthe current task, it is assumed that a lower ApEn value re¯ectsmore active control being exerted at the joint that controls therespective limb segment. Thus, this analysis provides an ApEnmeasure that determines the regularity or ``complexity'' in thetremor signal of each limb segment. Ninety-®ve percent con®denceintervals (CI) were also calculated for all ApEn values.

Frequency analysis of the tremor signal was performed usingpower spectral analysis on the raw acceleration data. The speci®cdependent measures calculated from this analysis were peak am-plitude and frequency of peak amplitude. Frequency analysis wasapplied over three speci®c bandwidths; 0±7 Hz, 7±17 Hz and 17±30 Hz. These bandwidths were selected in order to isolate the majorfrequency components for postural ®nger and hand tremor (Ran-dall and Stiles 1964; Marsden 1984; Elble and Koller 1990).

Inter- and intra-limb analysis

Examination of the coupling between ipsilateral and contralaterallimb segments in the time-domain analysis was performed usingcross-correlation analysis. This was conducted within a trial andbetween all possible paired limb-segment combinations.

The degree of relationship between any two signals in the fre-quency domain was determined using coherency and phase ana-lyses (Jenkins and Watts 1968). Coherency analysis determines therelationship between two di�erent frequency signals based upon thecross- and auto-spectral properties of the each signal (Shiavi 1991).The peak coherency measure within each bandwidth was used as ameasure of the degree of coupling in the frequency domain betweenthe selected paired signals. An upper 95% con®dence line wascalculated for this analysis. This method was chosen to determinewhich coherence peaks were signi®cantly greater than the back-ground level and has been used previously in tremor studies(McAuley et al. 1997). For the phase analysis, the mean, standarddeviation and 95% CI of the phase angle between two selectedfrequency signals were calculated. Calculations of the phase angledi�erences between segments were performed for the point of peakcoherency within each frequency bandwidth. The same frequencybandwidths used for the power spectral analysis were employed forthe coherency and phase analysis.

Inferential statistical analysis included the use of a three-factor(splinting condition, limb segment, trial), within-subject, repeated-

Fig. 1 Example of the experimental setup for the control, non-splinted (CL) condition

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measures analysis of variance (ANOVA) to determine the signi®-cance of changes in each of the dependent measures.

Results

Tremor in independent degrees of freedom:Time-domain analysis

Amplitude measures

An example of a typical raw (unrecti®ed) accelerometersignal from each limb segment of a single arm during theCL condition is shown in Fig. 2. The mean and standarddeviation of the absolute acceleration (tremor) ampli-tude for each limb segment are plotted in Fig. 3a,b, re-spectively as a function of the level of joint splinting. Ingeneral, the results reveal that the pattern of data for themean and standard deviation of tremor amplitudeshowed clear proximal-distal e�ects [M ) F(7,392) =2699.17; SD ) F(7,392) = 1609.52; P < 0.01], with thetremor being greater in the segments of the left limb.This pattern was basically preserved in both limbs as aresult of splinting the right limb.

The general within-limb e�ects of joint splintingshowed that the mean tremor amplitude and variability

for the distal segments of either limb, namely the handand index ®nger, signi®cantly increased from the controlconditions as a consequence of externally constrainingthe limb [M ) F(8,392) = 6.09; SD ) F(8,392) = 8.45;P < 0.01]. Figure 4 highlights the changes in meantremor amplitude for these distal segments, observed asa result of splinting.

Regularity analysis of acceleration signals

There was a signi®cant di�erence in the pattern of reg-ularity, as determined by changes in ApEn measure, forthe tremor across the di�erent limb segments[F(7,392) = 895.6; P < 0.01]. The lowest ApEn(greatest regularity) was seen within the tremor signalfor the hand, while the greatest structure (highest ApEn)was found for the tremor signal for the forearm andindex ®nger. No di�erence in ApEn was found betweenthe following contralateral limb segments; left arm-rightarm, left forearm-right forearm and left ®nger-right®nger (all P < 0.01).

While the pattern of ApEn was preserved across allconditions, there was a signi®cant decrease in ApEn forthe particular limb segment as a result of splinting[F(8,392) = 5.20; P < 0.01]. Post-hoc analysis showed

Fig. 2 Typical example of araw accelerometer signalfrom each segment of a singlelimb during the CL condition

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thatApEn for theCLandLS conditionswere signi®cantlygreater than that seen during all other conditions. Thedegree of regularity of the acceleration signal in the index®nger was also shown to signi®cantly increase (lowerApEn) under conditions where this segment was splinted(LS, All, EF,WF and FS). Figure 5 illustrates the patternof mean ApEn results (with 95% CI) for each limb seg-ment across the nine di�erent splinting conditions.

In summary, splinting of any joint of the right limbresulted in a lower ApEn for the hand, indicating thatgreater control was exerted about the wrist joint in ane�ort to overcome both the physical constraint of

splinting and the task constraint of minimizing ®ngertremor. The increased control about the wrist joint wasalso manifested in a signi®cant decrease in ApEn for theindex ®nger of both limbs.

Frequency analysis

Power spectral density

The frequency pro®le for the tremor in any limb segmentacross all conditions displayed at least two prominentfrequency peaks, one between 2±4 Hz and another be-tween 8±12 Hz. A third peak (at 18±22 Hz) was ob-served in the frequency pro®le for the index ®nger ofeach hand. This peak has been reported to re¯ect thepassive mechanical properties of the index ®nger (Foxand Randall 1970; Stiles 1980; Elble and Koller 1990;van Emmerik et al. 1993). Since this higher frequencycomponent was only observed in the ®nger, results forthe frequency, coherence and phase analysis will belimited to these e�ectors.

Splinting the right limb altered the frequency pro®leof the tremor signal in each limb segment, the majorchange being a signi®cant increase in the power (am-plitude) of both tremor peaks (2±4 Hz and 8±12 Hz)within the segments of both limbs [0±7 Hz ) F(7,392)= 149.80; 7±17 Hz ) F(7,392) = 294.56; P < 0.01]. Asigni®cant change in the modal frequency of both peakswas also seen as a result of splinting [0±7 Hz ) F(7,392)= 86.69; 7±17 Hz ) F(7,392) = 872.95; P < 0.01].Speci®cally, the lower frequency components (2±4 Hz)shifted up in frequency, while the frequency peaks be-tween 8 and 12 Hz decreased. The frequency changesobserved in both peaks were typically of the order of0.3±0.8 Hz.

Splinting also produced a decrease in the power andfrequency of the 18±22 Hz component of tremor for theright ®nger, particularly under conditions where thedistal segments were splinted (FS, WF). The principalfrequency components of the tremor signal under un-splinted conditions and the typical changes found in thefrequency pro®le as a result of splinting are shown inFig. 6.

Intra- and inter-limb coupling of tremor

Correlation analysis

The results of this analysis show that under conditionswhere no joint was splinted (CL), the same signi®cantintra-limb correlations were observed for both limbs,with no signi®cant inter-limb relationships (r values<0.2). The signi®cant within-limb relationships wereobserved between adjacent proximal (upper arm-fore-arm), and distal (hand-®nger) limb-segment combina-tions (P < 0.05). The highest coupling was seen for themore distal combinations (right hand-right ®nger,

Fig. 3 The mean absolute acceleration level (a) and variability (b)of the tremor signal for each limb segment as a function of arm andsplinting. The splinting conditions were: no splinting of the limb(control ± CL), loose splinting (LS), all joints of the right limb fullysplinted (All), splinting of a single joint of the right limb (®ngeronly, FS; wrist only, WS; elbow only, ES) and those conditionswhere two joints of the right limb was splinted (®nger and wrist,WF; wrist and elbow, EW; elbow and ®nger, EF). (LArm Leftupper arm, LFor left forearm, LHnd left hand, LFin left ®nger,RArm right upper arm, RFor right forearm, RHnd right hand, RFinright ®nger)

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r = 0.87; left hand-left ®nger, r = 0.73). No signi®cantinter-limb relationships or intra-limb relationships be-tween non-adjacent limb segments were observed (allP > 0.05).

Splinting the right limb a�ected the nature of thewithin-limb correlations in both arms, even though nodistinct relationship between limbs was observed as aresult of applying external constraints. Splinting resultedin an increase in the strength and number of signi®cantintra-limb correlations for both limbs (from four to six),with the notable change being a signi®cant increase inthe strength of the forearm-hand relationship. In addi-tion, splinting of the right index ®nger either singularly(FS) or in combination with other joints (All, EF, WF),resulted in signi®cantly increased coupling between theright hand and right ®nger (all P < 0.001).

Across the eight splinting conditions the same patternof relationships between adjacent limb segments was ob-served in both arms. These results show that the proximalleft arm combinations (left arm-left forearm, left forearm-

left hand) were more highly correlated than contralaterallimb-segment combinations for the right limb.

Exceptions to this were the correlations observedbetween the right hand-right ®nger during conditionswhere splinting of the right ®nger was performed (All,FS, EF, WF). During these conditions, the strength ofthis coupling between these e�ectors was greater thanthat observed for any other joint con®guration and forany other condition (r = 0.87±0.98). The signi®cantwithin-limb correlations are illustrated as a function oflimb splinting in Fig. 7.

Correlation values were converted into Z scores forinferential analysis using repeated-measures ANOVA.The results of this analysis demonstrated a signi®cantdi�erence between the di�erent splinting conditions[F(7,392) = 47.14, P < 0.001] and between the di�er-ent limb-segment combinations [F(27,392) = 9.03,P < 0.001]. Post-hoc analysis showed that therelationships between the upper-arm-forearm and hand-index ®nger were signi®cantly greater than all otherlimb-segment groupings. The principal e�ect of the jointsplinting was to increase the strength and number of theintra-limb relationships from the CL conditions (allP < 0.001).

Fig. 4 Di�erences in mean tremor level observed in the distalsegments of either limb as a result of splinting conditions. SeeFig. 3 for a description of the splinting conditions

Fig. 5 Approximate entropy (ApEn) values (with 95% con®denceintervals) for each limb segment as a function of arm and thedi�erent levels of limb splinting. See Fig. 3 for a description of thesplinting conditions

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Coherency analysis

Coupling between limb segments was assessed in thefrequency domain through coherency analysis. UnderCL conditions, peak coherence was highest at lower

frequencies (2±4 Hz) and between adjacent limb seg-ments (upper arm-forearm and hand-®nger). Speci®cal-ly, coherence was greatest for the distal segmentcombinations, namely the right hand-right ®nger (range0.80±0.92) and left hand-left ®nger (range 0.79±0.81)combinations. Coherence between non-adjacent seg-ments was signi®cantly lower [less than 0.35;F(27,1568) = 1291.69; P < 0.01].

The strength of the coupling between these samelimb-segment combinations for the 8- to 12-Hz peaks

Fig. 6 Typical changes seen in power spectral density plots ofacceleration in each limb segment of the right arm in a singlesubject during the control (unsplinted), elbow and wrist splinted(EW), and ®nger splinted only (FS) conditions

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decreased (left hand-left ®nger, 0.51±0.55; right hand-right ®nger, 0.64±0.77), but was still signi®cantly greaterthan that for other segment combinations[F(27,1568) = 446.80; P < 0.01]. Peak coherence be-tween non-adjacent segments decreased markedly at thehigher frequency range (<0.22).

Peak coherence for all inter-limb relationships werenon-signi®cant, being markedly lower (<0.18 across allfrequencies) than that observed within-limb, irrespectiveof the splinting condition (all P < 0.001). The ®nding ofno signi®cant between-limb relationships indicates nostrong coupling of the frequency components of anye�ector unit between the right and left limbs.

Splinting the right limb resulted in a signi®cant in-crease in coherence between adjacent segments of both

limbs [F(8,1568) = 2.56; P < 0.01]. In all cases, themost notable increase in coherence was found betweenthe splinted limb segments for the 2- to 4-Hz-frequencycomponents. The change in coherence was greatest inthe splinted limb, but also increased in the left limb(although the change was smaller). In particular, peakcoherence increased between the forearm and hand from0.35 under CL conditions to 0.67±0.69 during splintingconditions.

Overall, the results of the coherency analysis showedno between-limb e�ect for joint splinting, indicating thatcoupling between contralateral limb segments did notemerge as a result of splinting a single limb. The within-limb e�ects of joint splinting showed a signi®cant in-crease in the limb segment relationships for the splinted(right) limb primarily, with a small (but non-signi®cant)change in peak coherency between adjacent limb-seg-ment combinations in the left (unsplinted) limb. Thegreatest increase in peak coherency as a result ofsplinting was found between the 2±4 Hz peaks for thedistal limb-segment combinations of the right limb(hand-®nger and forearm-hand).

Phase analysis

All phase angle results were calculated for the point ofpeak coherence within each selected bandwidth. Theresults showed that, across all conditions, the strength ofthe within-limb relationships was greatest for the peaksfound between 2±4 Hz, with the smallest angle changebeing observed for the upper arm-forearm and index®nger-hand combination of either limb[F(27,1568) = 357.08; P < 0.01]. The mean and stan-dard deviation of the phase angle increased signi®cantly(�180 degrees) at successively higher frequencies andbetween non-adjacent limb-segment pairs[F(27,1568) = 153.19, P < 0.01].

Under the CL conditions, the smallest phase anglewith least variation was found between the upper arm-forearm (range; �48±52 degrees; CI, 12±15 degrees)and hand-index ®nger (range; �12±14 degrees; CI, 3±6degrees) combinations. The phase angle between thehand and forearm (range; �81±92 degrees; CI, 18±24 degrees) indicated an intra-limb relationship that wascompensatory (out of phase) in nature about the actionof the wrist joint. The phase angle between non-adjacentintra-limb segments showed large ¯uctuations at ahigher phase angle (�141±162 degrees; CI, 22±38degrees).

Splinting resulted in a signi®cant decrease in thephase angle between adjacent limb segments[F(8,1568) = 2.37, P < 0.01]. This e�ect was greatestwithin the splinted (right) arm, being particularly no-ticeable for distal segment combinations, but signi®cantdecreases in phase angle were also observed betweenadjacent segments in the left (non-splinted) limb. Thegreatest within-limb e�ect of joint splinting was foundbetween the upper arm-forearm and forearm-hand

Fig. 7 The signi®cant correlations for each adjacent limb segmentcombination seen as a function of the di�erent levels of jointsplinting. (LArm-LFor Left arm-left forearm combination, LFor-LHnd left forearm-left hand combination, LHnd-LFin left hand-left®nger combination, RArm-RFor right arm-right forearm combina-tion, RFor-RHnd right forearm-right hand combination, RHnd-RFin right hand-right ®nger combination). See Fig. 3 for adescription of the splinting conditions

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combinations in the right (splinted) limb. Splinting thejoints of the right limb resulted in a decreased phaseangle between adjacent limb-segment pairs. In particu-lar, the phase angle relationship for the forearm and®nger of either limbs decreased markedly from around�81±92 degrees under non-splinting conditions to�53±63 degrees (95% CI, 13±17 degrees) following theapplication of the external constraints. Splinting had noe�ect on the between-limb organization, since the meanand SD of the phase angle still remained high(�180 degrees) across all conditions.

Splinting of the right ®nger, whether in combinationwith or without splinting of other joint structures (All,LS, FS, EF and WF) resulted in a marginally decreasedphase angle range (�9±10 degrees; CI, 2±5 degrees)compared to the phase angle when the ®nger-handstructure was not splinted.

Bilateral asymmetry of tremor

A consistent between-limb asymmetry in the tremoroutput was observed under normal (CL) conditions forall subjects. During this condition, tremor amplitudeand variability were greater in the left limb as comparedto the right limb. In addition, the strength of the intra-limb coupling (both in time and frequency) was weakerin the left limb as compared to the right. This limbasymmetry was small but reliable throughout all testingconditions.

The between-limb e�ects of splinting on this apparentasymmetry varied according to the limb segment com-pared. Tremor amplitude and variability in the leftforearm and index ®nger remained higher than thatobserved in the right (splinted) limb during all condi-tions. However, the pattern about the respective wristjoints (between left and right hands) was reversed, withincreased tremor amplitude and variability beingrecorded in the right hand as compared to the left.

Discussion

In this study we investigated the e�ect of selectivesplinting of the joints of the right limb on the bilateralorganization of physiological tremor and the tremorpro®le for individual upper-limb degrees of freedom.The main ®ndings were: (1) there was no inter-limbcoupling of tremor under any condition, although thesame pattern of intra-limb organization was observed ineach limb, (2) splinting of the right limb changed thepattern of the intra-joint couplings within each limb, and(3) splinting of the joints of the right limb resulted in asigni®cant change in the tremor pro®le for both limbs.These ®ndings relate to the conceptual nature of theneural oscillator mechanism(s) that drives posturaltremor and the theoretical issues of the degrees-of-free-dom problem in movement coordination.

Intra- and inter-limb coupling of tremor

The results of this study show that the same pattern ofintra-limb coupling was found in either limb. This pat-tern was characterized by strong coupling between themore proximal (upper arm-forearm) and distal (hand-index ®nger) segment pairs, with the motion of theproximal-limb segment pairing being compensatory(�81±92 degrees or close to out of phase) to the motionof the distal-limb segment pairs. The link between thesetwo segments was the wrist joint, which acted as a formof fulcrum for the coupled motion of these segmentpairs. This within-limb pattern has been described as acompensatory synergy (Arutyunyan et al. 1968, 1969;Morrison and Newell 1996).

Irrespective of the splinting manipulation applied, nosigni®cant correlation (in either time or frequency) wasseen between any of the contralateral limb segments.This ®nding supports those of previous studies that havereported no inter-limb coupling of tremor in distal seg-ments (index ®nger; Marsden et al. 1969a; Newell andSprague 1994), and expands on this by demonstratingthat the postural tremor observed in any segment of theupper limb is unrelated to the tremor seen in any con-tralateral limb segment. Thus, the two limbs showed thesame pattern of intra-limb coupling, but no inter-limbrelationships were found.

Despite the fact that there was no relationship be-tween the left and right limbs, splinting the joints of asingle limb produced a signi®cant change in the degreeof tremor and the pattern of intra-limb coupling in bothlimbs. This result suggests that some form of relation-ship does exist between the limbs that is not apparentfrom traditional correlation analyses.

One potential explanation that has been suggested isthat the intra-limb relationships simply re¯ect theproduct of mechanical coupling between adjacent limbsegments. Under this premise, the tremor seen within asingle limb is merely a product of intra-limb mechanicalcoupling with no inter-limb connection. Thus, splintinga single limb should not a�ect the nature or pattern oftremor in the other limb. The fact that intra-limbchanges were found for both limbs following splintingmeans that it is unlikely that such a change is theproduct of mechanical linkages. Furthermore, it is dif-®cult to conceive of mechanical linkages being primarilyresponsible for this relationship, since some link betweenlimb and torso tremor would probably be evident, a factthat has not been previously supported for this type ofpostural task (Morrison and Newell 1996).

A second potential explanation for this result is thatsome form of neural commonality between the limbsexists in this task. The lack of inter-limb coupling andsimilar intra-limb organization, suggest that some com-monality of the neural drive between limbs exists, but thatthis commonality does not include strict inter-limb rela-tionships in either the time or frequency of the tremor.

These data are consistent with the view that, for thistask, a large proportion of the postural tremor is de-

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rived from some common central oscillatory mecha-nism (Lippold 1970; Llinas 1984; Elble 1996; Britton1997; Llinas and Pare 1997), and that a common (bi-lateral) strategy is employed to minimize these oscilla-tions within a single limb (Arutyunyan et al. 1968,1969; Morrison and Newell 1996). The lack of tremorrelationships between limbs suggests further that theoutput from this central oscillator is subsequently ®l-tered in parallel prior to e�ecting output in each limb(Marsden et al. 1969a, b; Stein and Lee 1981). Thisview that the output from a central oscillator may bedi�erentially organized accounts for the common butuncoupled tremor and organizational output betweenlimbs in this task. This ®nding is consistent with recentneurophysiological ®ndings of the output of the centraloscillatory mechanisms underlying tremor (Colebatchet al. 1990).

Alternatively, the similar changes in the contralateralpattern of tremor could be incidental to modi®cation ofa common strategy employed to control both limbs. Thiscommon strategy could be typi®ed by a similar patternof muscle activation in each limb for this postural task.The act of splinting a single limb would then produce asingular change in the strategy, and hence muscle ac-tivity, in both limbs. Consequently, the bilateral changesin tremor may be considered to be a secondary productof associated changes in muscle activation rather than aprimary result of changes in a strategy to control theoscillations within a limb.

Overall, splinting of the right limb increased thenumber of limb segments that were signi®cantly coupledin both limbs. Thus, the between-limb reorganization wasmanifested by changes in the pattern of coupling betweenipsilateral limb segments, but there is no coupling be-tween the contralateral segments. We would speculatethat limb-segment splinting changes the organization ofthe neural output (strategy) that produces coordinativechanges in the pattern of intra-limb coupling.

Tremor in a single degree of freedom

A central theme of Bernstein's (1967) perspective onmotor control is that the problem of coordination is theharnessing of the redundant degrees of freedom of thehuman motor system. A hypothesis that emanates fromthis perspective is that the increased availability of de-grees of freedom, rather than being a problem for systemcontrol (as proposed in many traditional perspectives),actually a�ords more adaptive coordination solutionsand facilitates performance outcome. This central no-tion of Bernstein has only been examined indirectlythrough evidence of the changing organization inmovement coordination that arises from learning anddevelopment (Newell and McDonald 1994), but thesplinting manipulation used in the current experimentprovides a more direct test of this idea.

Minimization of tremor at the periphery during apostural pointing task is achieved through exploitation

of the biomechanical properties of the limb degrees offreedom. Externally constraining the degrees of freedomto act together produced an increase in tremor ampli-tude and, more noticeably, variability. Thus, constrain-ing the system by reducing the available degrees offreedom did prove to be an optimal solution for mini-mizing tremor. The optimal solution actually existswhen the arm is freer to move.

The ®ndings from this study con®rm that the adap-tive coordination solution to this pointing task, when alljoint degrees of freedom are available for regulation, isthat of a within-limb compensatory synergy that is op-erating predominantly about the wrist joints (Morrisonand Newell 1996). The evidence for a compensatorysynergy is drawn from the CL (no splinting) posturalcondition, but it is also buttressed by the ®nding thatselective splinting of particular combinations of the rightlimb led to enhanced variability in the motion of theindex ®nger in both limbs. In other words, constrainingthe performance of this postural task by reducing theavailability of proximal limb degrees of freedom as apart of the coordination solution increased the nature ofthe tremor at the most distal e�ector (the index ®nger) inboth limbs.

The demonstration of a compensatory limb synergyand its adaptive link to performance outcome is con-sistent with Bernstein's (1967) perspective on the orga-nization of the degrees of freedom in movementcoordination. It is interesting to note that the e�ect ofmanipulation of the degrees of freedom on the perfor-mance outcome in this task was manifested more in thevariability of the most distal e�ector rather than theabsolute mean level of acceleration output. This suggeststhat the stability of the limb organization was di�erentin the control versus splinted conditions.

Asymmetry of contralateral arm tremor

Under normal (control) conditions in the dual limb-pointing task, a bilateral asymmetry in the level ofphysiological tremor was observed between limbs. Thiswas a small but reliable e�ect and was seen in all sub-jects, irrespective of their hand dominance. While evi-dence of between-limb asymmetry has been reportedduring goal-directed movements (Guirad 1987; Jeanne-rod 1988), symmetry of limb oscillations between limbshas generally been assumed to be the norm (Craske andCraske 1986; Arblaster et al. 1990; Lakie et al. 1994).However, results have typically been based on relation-ships between a single e�ector in each limb. Thus, thequestion of symmetry in upper-limb postural tremorbetween multiple segments has not previously beendemonstrated.

The presence of an asymmetry between the limbs inthe unsplinted (CL) condition is surprising given the factthat no di�erences between limbs has been reported(Arblaster et al. 1990; Lakie et al. 1994) and also ap-pears to be contradictory with the notion that handed-

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ness may in¯uence the degree of tremor seen in eachlimb (Gur®nkel et al. 1971). This latter statement isparticularly di�cult to substantiate given that all sub-jects, even those who are left-hand dominant, showed agreater degree of tremor in the left limb. One potentialexplanation for this distinction between limbs mayconcern the previously reported anatomical descriptionof asymmetry that exists within the corticospinal tractitself, which does not appear to be related to handedness(Nathan et al. 1990). In addition, this explanation al-lows for the proposed idea that the neural output to eachlimb arises from a common central oscillator. Thus, eachlimb exhibited similar organizational coordinativeproperties, but this similarity of contralateral organiza-tion is not manifested by similarities in tremor output.

In summary, the ®ndings suggest that the compen-sation to splinting is not merely local to the splinted,joint(s), but is also global across limbs, suggesting somefunctional relationship between limbs that has not beendemonstrated previously.

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