Modulations in corticomotor excitability during passive upper-limb movement: Is there a cortical...

Brain Research 943 (2002) 263–275www.elsevier.com/ locate/bres

Research report

M odulations in corticomotor excitability during passive upper-limbmovement: Is there a cortical influence?

*Gwyn N. Lewis , Winston D. ByblowHuman Motor Control Laboratory, Department of Sport and Exercise Science, University of Auckland, Auckland, New Zealand

Accepted 10 March 2002

Abstract

Modulations in the excitability of corticomotor pathways to forearm musculature have previously been demonstrated during passivewrist movement [Brain Res. 900 (2001) 282]. Investigations were conducted to determine the level of the neuroaxis at which thesemodulations arise, and to establish the influence of proprioceptive task constraints on pathway excitability. Forearm motor evokedpotentials (MEPs) in response to transcranial magnetic stimulation (TMS) were examined during passive wrist movement while subjectsmaintained a low-level muscle activation, thus stabilising the excitability of the motoneuron pool. Modulations in response amplitudeduring movement were evident in both forearm flexor and extensor muscles. The pattern of modulation generally mirrored that seen inquiescent musculature during movement, with responses potentiated during the phases where the muscle was in a shortened position.Variations in MEP amplitude were not detected while the wrist was constrained statically at various joint angles. This suggests a dynamicinfluence of movement, most likely mediated by spindle receptors, arising at a supraspinal level. We also investigated the influence of akinesthetic tracking task on corticomotor excitability during passive movement of the wrist joint. MEPs were recorded from the targetdriven limb while the contralateral limb was stationary, while the contralateral limb actively tracked the movements of the target limb, andwhile the contralateral limb moved actively in time with a metronome. The results revealed no differences in MEP characteristics in thedriven limb between the three conditions. Placing the movement elicited afferent information in an active movement context does notappear to enhance the modulations in cortical excitability. 2002 Elsevier Science B.V. All rights reserved.

Theme: Motor systems and sensorimotor integration

Topic: Cortex

Keywords: Passive movement; Ia afferent; Motor cortex; Transcranial magnetic stimulation; Sensorimotor integration

1 . Introduction have employed passive movement paradigms. In thesestudies, rhythmic limb movement is imposed on quiescent

Modulations in motor pathway excitability have been musculature, eliminating the influence of descending com-reported during dynamic activities in both the upper [10] mands on motor pathway excitability. Investigations usingand lower limbs [4,7]. Recently, there has been much both spinal (H-reflex; e.g. [3]) and cortical (transcranialdebate as to the possible origin and mechanisms of these magnetic stimulation, TMS; [9,25]) stimulation techniquesmodulations, and their relevance to the performance of have revealed that modulations in the level of excitation offunctional movements. Two different viewpoints that have motor pathways are evident in passive limb movement.been put forward are that the alterations in pathway These studies confirm the influence of movement elicitedexcitability arise from: (a) peripherally mediated influences afference on excitability of associated motor pathways, but[3,14]; or (b) a single, centrally-specified origin [8,24,33]. the level /s of the neuroaxis at which these peripheralTo examine the influence of peripheral sensory com- influences are mediated remains unclear.ponents on motor pathway excitability, many researchers A recent investigation in our laboratory [25] examined

evoked responses in the flexor carpi radialis (FCR) musclein response to TMS during passive wrist movement. It was*Corresponding author. Tel.:164-9-373-7599x3766; fax:164-9-373-found that responses were potentiated during the phases of7043.

E-mail address: [email protected](G.N. Lewis). wrist flexion and relatively inhibited during wrist exten-

0006-8993/02/$ – see front matter 2002 Elsevier Science B.V. All rights reserved.PI I : S0006-8993( 02 )02699-9

mailto:[email protected]

264 G.N. Lewis, W.D. Byblow / Brain Research 943 (2002) 263–275

sion, and that these modulations in response size were al wrist while the ipsilateral wrist actively tracked themore pronounced at higher movement frequencies. This imposed movements. It was hypothesised that the kines-suggested that alterations in pathway excitability were thetic tracking task may result in a potentiation of responsearising from Ia afferent input, however, as the musculature amplitude during passive movement, reflecting the in-was quiescent, it was difficult to discern whether this input fluence of altered sensory gain on the descending motorwas acting at spinal or supraspinal levels, or both. In the pathway.same study, paired magnetic stimulation revealed modula-tions in the extent of intracortical inhibition (ICI) through-out the movement cycle, indicating a possible cortical 2 . Materials and methodsinvolvement. Many previous investigations using TMShave demonstrated alterations in cortical excitability of 2 .1. Subjectshomonymous and antagonistic musculature after condition-ing with peripheral nerve stimulation [2,11,18,39,40], Eighteen (eight female, 10 male) right-handed subjectsproviding a potential neural basis for the suggested effects [28] volunteered for the study (mean age 26.668.8 years,at the level of the cortex. Aimonetti and Nielsen [1] found range 20–55; some subjects participated in more than onethat conditioning with antagonist nerve stimulation in- experiment). All participants were required to have nofluenced the extent of ICI and intracortical facilitation contra-indications to TMS or any known neurological(ICF) in wrist flexor and extensor muscles. They con- impairments. Informed consent was obtained from allcluded that antagonist muscular afferent information may subjects prior to testing and ethical approval for the studyinduce reciprocal facilitation at the cortical level, an idea was obtained from the University of Auckland Humanthat is congruent with our earlier findings [25]. Subjects Ethics Committee in accordance with the declara-

The relative influence of afferent input on motor path- tion of Helsinki.ways may also be influenced by the context of themovement. Staines et al. [36] have demonstrated that the2 .2. Equipmentgain of sensory pathways can be altered when the ascend-ing information is placed within a task relevant context. In Subjects were seated in front of two purpose-builttheir study, somatosensory evoked potentials (SEPs) were manipulanda, the details of which have been describedrecorded over the scalp after peripheral stimulation to the elsewhere [25,37]. Briefly, the subjects sat with theirtibial nerve while the foot was passively moved. SEP shoulders in slight abduction (10–208), elbows at 90–1108amplitudes were found to increase when the subjects were and forearms supported and in a neutral position. Eachasked to actively match the movement trajectory of the hand was inserted and secured in a hand piece that allowedpassive limb by moving the opposite foot. The subjects flexion/extension movements of the wrist joint. An ACwere without vision during the movement period and were servo motor located under the left unit enabled passivetherefore forced to rely on proprioceptive information from movement of a programmable amplitude, frequency andthe ankle to guide the active movements. This finding duration to be generated in the left wrist. The rightraises the possibility that selective facilitation of prop- manipulandum was able to be freely moved by the subject.rioceptive information, by placing it in a relevant context, The shafts of the left- and right-hand pieces were con-may accentuate its influence on sensory and motor regions nected to potentiometers to enable accurate specificationof the cortex. and collection of displacement signals of the two units.

In the current study, we conducted three experiments tofurther examine the modulations in corticomotor excitabili- 2 .3. Stimulation techniquety during passive limb movement. In the first experiment,subjects maintained a consistent level of forearm muscle Motor evoked potentials in the left FCR and ECRactivation while the wrist joint underwent passive move- muscles were elicited by TMS over the right motor cortex.ment. Magnetic stimuli were delivered over the contrala- A Magstim 200 stimulator (Magstim, Whitland, Dyfed)teral motor cortex at different phases of the movement and a figure-of-eight coil (70 mm each) were used tocycle. During muscle activation the level of excitation in deliver magnetic stimuli. The stimulating coil wasthe motoneuron pool is stabilised, therefore any remaining positioned over the subject’s right cortex orientated at anmodulations in response amplitude in these conditions are angle 458 to the midline and tangential to the scalp, suchlikely due to supraspinal mechanisms. In the second that the induced current flow was in an posterior–anteriorexperiment, forearm motor evoked potentials (MEPs) were direction along the motor strip [43]. A head rest placedcollected with the hand stationary at different wrist joint behind the subject’s occipital lobe ensured that headangles while subjects maintained a consistent level of position was maintained during the experimental sessions.background activation. In the final experiment, FCR MEPs The subjects wore a tightly fitting cotton cap withwere compared during passive movement of the contrala- pre-marked grid locations that was securely fastened to theteral wrist and during passive movement of the contralater- head by velcro straps. The centre of the cap (0,0) was

G.N. Lewis, W.D. Byblow / Brain Research 943 (2002) 263–275 265

aligned at the intersection of the inter-aural and inion- while the left wrist joint was stationary and while undergo-nasion lines. To determine the optimal site of stimulation, ing passive movement in both relaxed and activatedthe coil was systematically moved around the grid loca- conditions. Stimuli during passive movement were de-tions, with six stimuli delivered at each, until the site livered in eight equidistant phases of the movementeliciting the averaged MEP of the largest amplitude in the cycle—four during wrist flexion and four during wristleft FCR was located. This site was defined as the ‘hot extension (see Fig. 1). Subjects received high gain visualspot’ and all further stimuli were delivered with the coil feedback of EMG activity in the target FCR and ECRsecured at this location by a series of clamps. In all muscles throughout the experimental session. Test stimulussubjects, a discernable MEP in the ECR muscle was also intensity during relaxed conditions was set as 110% RTh,obtainable at this site. while it was lowered to 100% of individual RTh during

Individual rest threshold (RTh) was determined for each muscle activation.subject by detecting the minimum intensity at which four EMG activity during a maximum voluntary contractionof eight consecutive stimuli yielded a response of at least (MVC) of the FCR and ECR muscles was obtained by50 mV in the FCR muscle. The threshold was determined asking subjects to maximally flex/extend their wrist jointto the nearest 2% of stimulator output. Throughout the over a 5-s period while the hand piece was constrained in aexperimental sessions the position and angle of the neutral posture. Rectified EMG signals were averaged overstimulating coil relative to the subject’s head were checked 500-ms intervals and the peak value determined as MVC.repeatedly. During activated conditions, stimuli were only delivered

when the target muscle was within62% of the required2 .4. Recording technique level of EMG activity.Vision of the left hand was obscured

in all movement conditions and the right hand remainedElectromyographic (EMG) activity of the left FCR and relaxed throughout the testing session.

ECR muscles was recorded using 10 mm Ag/AgCl surface MEPs were first collected while the left wrist joint waselectrodes (Hydrospot, Physiometrix Inc., MA, USA). stationary and in a neutral posture. Eights responses wereElectrodes were placed 2 cm apart on the belly of each collected in each of three conditions: both FCR and ECRmuscle. One-hundred ms of EMG data were collected for muscles relaxed; FCR activation at 6% MVC; ECReach stimulus, plus an additional 20 ms prior to stimulus activation at 6% MVC. Stimuli were then delivered whileonset. EMG signals were amplified (Grass P511) and the left wrist underwent passive movement of 908 am-bandpass filtered (30–1000 Hz). Signals were sampled at plitude at frequencies of 0.05 and 0.2 Hz (average velocity4000 Hz using a MacLab A/D (ADInstruments, Castle of 9 and 368 /s respectively). Eight MEPs were collected inHill, NSW) acquisition system and stored on disc for each of the eight cycle phases during movement in fourfurther analysis. conditions: both FCR and ECR muscles relaxed (0.05, 0.2

Hz); FCR activated at 6% MVC (0.05 Hz); ECR activated2 .5. Protocol at 6% MVC (0.05 Hz). The slower movement frequency

(0.05 Hz) was selected to enable the subjects to maintain a2 .5.1. Experiment 1 consistent background muscle activation level more easily.

Nine subjects participated in the first experiment. Tran- Each individual movement trial was 60 s in duration, withscranial magnetic stimuli were delivered over the hot spot one stimulus delivered in each of the eight cycle phases

Fig. 1. Position of the hand piece (wrist joint) at each of the eight cycle phases. Cycle phase position was the same for both frequencies of movement.


per trial. In order to obtain eight MEPs in each cycle trials, magnetic stimuli were delivered to the left (quies-phase, eight trials were completed for each movement cent) FCR at the eight phases of the movement cycle, in acondition (some subjects required an extra 1–2 trials in the similar manner to that completed during passive movementmuscle activation conditions to collect the required number trials.of responses). The order of conditions was randomised In the timed active movement condition, the left wristthroughout the session. At the conclusion of all passive was again passively moved at 0.6 Hz and 908 amplitude.movement trials eight stimuli were again delivered in the Subjects were instructed to actively move their right wristthree conditions while the left wrist was stationary and in a by flexing and extending it in time with a metronome. Theneutral posture. metronome specified a movement frequency of 0.6 Hz and

instructions were given to subjects to ‘‘flex your wrist on2 .5.2. Experiment 2 the beat’’, so that flexion of the right wrist corresponded to

To investigate the effect that static wrist joint angle may passive extension of the left wrist. This resulted in thehave on pathway excitability, in a further eight subjects we same movement pattern of both hands as in the kinestheticexamined MEP amplitude while the hand was stationary at tracking task. Subjects were asked to make the activefour wrist joint angles (1438, 1188, 2188, 2438). These movements of the right hand at an amplitude that wasangles corresponded to the position of the hand piece at the comfortable for them. Magnetic stimuli were again de-eight cycle phases examined during passive movement in livered to the right cortex in eight phases of the movementExperiment 1 (positions repeated during wrist flexion and cycle.extension). Magnetic stimuli were delivered over the hot Eight kinesthetic tracking trials and eight timed activespot while the subjects maintained a 6% MVC in either the movement trials were completed in a random order,FCR or ECR muscle. Eight stimuli were delivered at each resulting in the collection of eight MEPs in each of thejoint angle during separate activation of two target mus- eight cycle phases for both conditions. Static trials, incles. The order of wrist angles tested was randomised which eight stimuli were delivered while both wrist jointsbetween subjects. Test stimulus intensity was set at were relaxed and constrained in a neutral posture, wereindividual RTh. completed before and after the passive movement con-

ditions.2 .5.3. Experiment 3

In the third experiment (eight subjects), TMS stimuli 2 .6. Data processing and analysiswere delivered over the right motor cortex during passivemovement of left wrist while subjects simultaneously Data were processed and analysed using custom builtperformed active movements with the right hand.Vision of routines housed on a Unix workstation. For each responseboth the left and right hands was obscured during all collected during relaxed conditions the root mean squaremovement conditions. Magnetic stimuli were delivered in (rms) amplitude of EMG activity 10 ms prior to thethe same eight phases of the movement cycle as Experi- stimulus was determined. Responses were removed fromment 1, with eight stimuli delivered in each cycle phase. further analysis if EMG silence was not maintained in thisResponses in the FCR muscle were recorded. Test stimulus period (rms value within mean62 S.D.s of static trials). Allintensity for TMS was set to 110% of RTh. remaining responses in each of the cycle phases and

Magnetic stimuli were first delivered while subjects conditions, and those obtained during voluntary musclecompleted eight 60-s trials of passive left wrist joint activation, were averaged and the maximum peak-to-peakmovement of 908 amplitude at 0.6 Hz (average velocity amplitude and latency of the averaged responses deter-1088 /s). In previous experiments it has been demonstrated mined.that modulations in response amplitude are greater at In the trials involving passive wrist movement (Experi-higher movement rates [25], therefore movement fre- ments 1 and 3), MEP amplitudes and latencies for eachquency was increased for the final experiment. The right individual were normalised to the amplitude and latency ofhand was relaxed and constrained in a neutral position responses obtained in the static trials. This provided anduring this movement. The subjects then completed kines- indication of response modulation in relation to static,thetic tracking and timed active movement tasks. During resting conditions.kinesthetic tracking, the left wrist was passively moved at0.6 Hz and 908 amplitude, the same movement pattern as 2 .6.1. Statistical analysisthat specified previously. Subjects were instructed to Data obtained during relaxed conditions in Experiment 2replicate the movements of the left wrist by actively were analysed using a two-way repeated measuresmoving their right wrist in an anti-phase pattern, so that ANOVA (frequency3phase), while data obtained in acti-flexion of the left wrist corresponded to extension of the vated conditions were analysed using a one-way ANOVAright wrist and vice-versa. It was stressed to the subjects to with the factor of phase.try and make the active movements at the same frequency FCR and ECR MEPs from Experiment 2 were analysedand amplitude as that imposed in the left hand. During the using a one-way repeated measures ANOVA with the


factor of wrist joint angle. In Experiment 3, repeated ence of phasic modulation of MEP amplitude during themeasures ANOVAs (condition3phase) were used to com- movement cycle [9,25]. Across both frequencies, MEPpare MEP amplitude and latency at the eight cycle phases amplitude was potentiated above static values at cyclebetween the three movement conditions (passive move- phases 6–8 (allP,0.005). An interaction between move-ment, kinesthetic tracking, timed active movement). ment frequency and cycle phase was also present (F 57,42

The main effects of phase were investigated usingt-tests 2.8,P50.04). From Fig. 2 it is evident that differences inwhich compared MEP amplitude/ latency to unity (1), the the pattern of response modulation are present between thevalue that would be obtained if static and passive move- two frequencies of movement. At the cycle phases corre-ment MEPs were equivalent. Ana level of 0.05 was used sponding to muscle shortening (5–8), FCR MEP amplitudeas a guide for establishing significant results. A Hunyh– was greater during movement at 0.2 Hz in comparison toFeldt correction factor and a Bonferroni correction factor movement at 0.05 Hz, i.e. there was a greater range ofwere used to adjust the ANOVA andt-test results respec- response amplitude modulation at the higher movementtively. Results are reported as mean6standard deviation. frequency. The phases of peak response amplitude also

shifted from phases 6 and 7 at 0.2 Hz to phases 7, 8 and 1at 0.05 Hz.

3 . Results FCR MEP latency (Table 1) generally mirrored theresults found for MEP amplitude, with the largest am-

3 .1. Experiment 1 plitude responses also demonstrating a shorter latency.Post-hoc analysis of a main effect of phase (F 53.3,7,42

3 .1.1. FCR MEPs in relaxed conditions P50.03) revealed that evoked potentials at cycle phase 7Fig. 2 (top) illustrates FCR MEP amplitude at each had a significantly shorter latency compared to static

cycle phase during movement at 0.05 and 0.2 Hz. A main conditions (P,0.001). MEPs elicited during movement ateffect of phase was present (F 55.1, P50.003), con- 0.2 Hz were also found to have a shorter latency than those7,42

firming previous studies that have demonstrated the pres- obtained during movement at 0.05 Hz (F 57.0,P50.04).1,6

3 .1.2. FCR MEPs in activated conditionsExample MEPs from an individual subject obtained

during movement at 0.05 Hz are shown in Fig. 3. Groupaverages of FCR MEP amplitude during muscle activationare shown in Fig. 4. An effect of phase was also presentfor these data (F 55.5, P,0.001), indicating the pres-7,56

ence of modulations in response amplitude during themovement cycle. The most potentiated periods of themovement cycle at 0.05 Hz in relaxed conditions werephases 7, 8 and 1. These three cycle phases were also themost potentiated in the activated movement condition.T-tests comparing the amplitude of the response at cycle

Table 1FCR MEP latency during passive movement

Cycle phase MEP latency (ms)

0.2 Hz 0.05 Hz (relaxed) 0.05 Hz (activated)

1 18.061.8 17.161.7 17.161.42 17.361.8 18.261.5 17.561.93 18.261.9 19.162.9 18.061.14 18.161.7 18.261.5 18.461.45 17.761.2 17.861.5 17.361.86 17.061.5 17.861.8 16.862.37 15.961.8* 17.061.1* 16.861.58 17.161.4 17.961.5 16.461.1Static (relaxed) 17.761.3Static (activated) 17.061.6

Data indicate the average (6S.D.) MEP latency at each cycle phaseFig. 2. FCR (top) and ECR (bottom) MEP amplitudes during passive during movement in relaxed conditions (0.2, 0.05 Hz) and duringmovement at 0.05 and 0.2 Hz. Values are expressed relative to the MEP movement with FCR activation (0.05 Hz). Static values in relaxed andamplitude obtained in static conditions. *, Phases significantly different activated conditions are also provided. *, Significant difference fromfrom unity (static MEP amplitude). Error bars represent 1 S.E.M. static (relaxed) values.


Fig. 3. Example FCR MEPs from an individual subject during static trials and during passive movement at 0.05 Hz in relaxed (left) and activated (right)conditions. Each trace represents the average of eight responses. Responses in static conditions are shown in grey, followed by cycle phases 1 to 8 (top tobottom). The left and right scale bars refer to MEP amplitude in relaxed and active conditions respectively. Note the similar modulations in MEP amplitudein the two conditions.

phases 7, 8 and 1 during activated conditions to static conditions (Fig. 2). Although MEPs tended to have a(activated) values revealed that response amplitude was greater amplitude during the cycle phases when the ECRalso facilitated above static MEP amplitude at these cycle muscle was shortening (1–4), these modulations in re-phases (P50.02). sponse size were less marked than that seen in the wrist

FCR MEP latency data (Table 1) obtained during 0.05 flexor muscle. No significant effects or interactions withHz movement with muscle activation demonstrated slight cycle phase were detected (allP.0.1).modulations between the cycle phases, however the effect MEP latency (Table 2) also demonstrated slight varia-of phase did not reach significance (F 51.8, P50.1). tions during the movement cycle. An effect of phase was7,56

present (F 55.0, P50.003), however furthert-tests7,35

3 .1.3. ECR MEPs in relaxed conditions failed to detect any significant differences between in-Two subjects were unable to maintain EMG silence in dividual cycle phases and values obtained in static con-

the ECR muscle during all of the movement cycles. The ditions (allP.0.01, correcteda50.006).results of these subjects have not been included in thegroup analysis. 3 .1.4. ECR MEPs in Activated conditions

Modulations in response amplitude were not evident in MEPs in the ECR muscle during movement at 0.05 Hzthe ECR muscle during passive movement in relaxed with muscle activation displayed a reciprocal relationship


and end of the test session. For the FCR muscle, therewere no significant differences detected in MEP amplitudefrom either the relaxed (start 118695 mV; end 93685 mV)or active (start 5446419 mV; end 4506408 mV) statictrials (two-tail, both P.0.3). The amplitude of staticresponses obtained in the ECR muscle were also notsignificantly different before and after passive movementin both relaxed (start 2216126mV; end 2036131mV) andactive (start 5006180 mV; end 4936243 mV) conditions(both P.0.7).

3 .2. Experiment 2

MEP amplitude and latency results for the FCR andECR muscles during activation in static conditions areshown in Fig. 5. There were no significant effects of wristFig. 4. FCR and ECR MEP amplitude during passive movement at 0.05joint angle on MEP amplitude or latency for either muscleHz with 6% MVC muscle activation. Values are expressed relative to the

MEP amplitude obtained in static conditions. Error bars represent 1 (all P.0.2).S.E.M.

3 .3. Experiment 3to those seen in the FCR muscle during equivalent muscleactivation (Fig. 4). A main effect of phase was present for Results of FCR MEP amplitude and latency during thethese data (F 52.9, P50.02). In relaxed conditions, three movement conditions are illustrated in Fig. 6.7,56

MEPs in the ECR muscle obtained in cycle phases 3–5 Displacement signals of the left and right manipulandademonstrated the largest facilitation during movement at were collected during the timed active movement and0.05 Hz. We compared the same cycle phases to static kinesthetic tracking tasks (Fig. 7). It was verified thatvalues in the activated condition. The facilitated response active movements of the right hand were of an equivalentamplitude above static conditions was significant at these amplitude, frequency and phase relation in these two tasks,cycle phases (P,0.001). indicating that the movement patterns of both hands were

The effect of phase for MEP latency data duringactivated conditions did not reach conventional levels ofsignificance (F 52.3, P50.07; Table 2).7,56

3 .1.5. Repeatability of static trialsTo examine the repeatability of responses obtained

during the test session, pairedt-tests were used to compareMEP amplitude from the static trials completed at the start

Table 2ECR MEP latency during passive movement

Cycle phase MEP latency (ms)

0.2 Hz 0.05 Hz (relaxed) 0.05 Hz (activated)

1 16.562.0 17.361.1 16.461.22 17.061.8 17.461.4 16.562.03 17.861.7 17.860.8 17.862.64 17.661.5 17.560.7 16.061.35 16.961.6 17.560.8 17.562.96 17.062.0 17.761.7 17.262.47 16.161.3 16.961.4 16.461.68 16.661.3 16.561.6 16.661.4Static (relaxed) 17.161.4Static (activated) 16.862.5

Data indicate the average (6S.D.) MEP latency at each cycle phaseduring movement in relaxed conditions (0.2, 0.05 Hz) and during Fig. 5. FCR and ECR MEP amplitude (top) and latency (bottom) whilemovement with ECR activation (0.05 Hz). Static values in relaxed and the wrist joint was stationary at the four wrist joint angles. The targetactivated conditions are also provided. *, Significant difference from muscle was activated at 6% MVC during stimulation. Error bars representstatic (relaxed) values. 1 S.E.M.


Fig. 6. FCR MEP amplitude (top) and latency (bottom) during the eight cycle phases in the three movement conditions. MEP parameters are expressedrelative to the values obtained in the static trials. *, Phases significantly different from unity (static MEP values). Error bars represent 1 S.E.M.

comparable in the active movement and kinesthetic track- 3 .3.2. MEP Latencying conditions. A main effect of phase was also evident for MEP

latency data (F 510.0, P,0.001). Further analysis7,56

3 .3.1. MEP Amplitude revealed that normalised MEP latency at phases 5, 6 and 7A significant effect of phase was found for MEP (allP,0.001) was significantly lower than unity, indicat-

amplitude data (F 57.0, P50.001).T-tests revealed that ing a latency shorter than that obtained in static, resting7,56

MEP amplitude at phases 5 (P,0.001), 6 (P,0.001), 7 conditions. Again, the main effect of condition and the(P,0.001) and 8 (P50.004) was significantly facilitated in condition by phase interaction did not reach conventionalcomparison to static conditions. The main effect of con- levels of significance (bothP.0.3).dition and the condition by phase interaction did not reachconventional levels of significance for this task (both 3 .3.3. Repeatability of static trialsP.0.1). Therefore, MEP amplitude in the passive limb To examine the repeatability of responses obtainedFCR did not differ between conditions where the contrala- during the test session, a pairedt-test was again used toteral hand was static, tracking the passive limb, or flexing compare MEP amplitude from the static trials completed atand extending in time with a metronome. the start and end of the test session. The difference in MEP

Fig. 7. Angular displacement data from the driven (top) and active (bottom) hand pieces during a 60-s trial. Displacement data from the active hand duringa kinesthetic tracking trial is indicated by the dark line; data from the active hand during an active movement trial is indicated by the light line Positivedisplacements represent wrist flexion. Note the similarity in active hand displacement between the two conditions.


amplitude between the two sets of trials (start 70642 mV; with heightened pathway excitability [25]. Reciprocalend 70655 mV) was found to be non-significant (two-tail, inhibitory connections between agonist–antagonist muscleP51.0). pairs are well known at the spinal level, making it likely

that antagonist muscle spindle discharge is also contri-buting to changes in motor pathway excitability. The

4 . Discussion marked potentiation of responses evident at high move-ment frequencies suggests a strong facilitatory effect of Ia

4 .1. Modulations in corticomotor excitability in output in comparison to input from static receptors.quiescent musculature Contributions from joint and cutaneous receptors to

alterations in pathway excitability cannot be discounted.The results of the passive movement conditions clearly The unloading of muscle tension when the muscle is

demonstrate modulations in FCR MEP amplitude during shortened may serve to reduce Ib inhibition, increasingthe different phases of the flexion–extension cycle. This motoneuron excitability. However, this effect is likely tosupports earlier findings from our laboratory using similar be small as Ib afferents are less influential during passivelyexperimental paradigms, which have been discussed in induced movement compared to active movements anddetail elsewhere [25]. Previously, we implicated Ia afferent make a minimal contribution to the resting potential ininput from the agonist–antagonist forearm muscle pairs in relaxed conditions [5]. Similarly, although cutaneous andthese alterations in pathway excitability. In accordance joint receptors are sensitive to alterations in joint angle, thewith the findings from our earlier study, modulations in majority respond at the limits of joint motion [6] unless anresponse amplitude in the current investigation were exaggerated stretch of skin is imposed [16]. They aregreater at the higher movement frequency, supporting the therefore unlikely to account for the facilitated responseproposed involvement of receptors sensitive to changes in amplitude during the mid ranges of wrist joint angle seenthe rate of muscle stretch. in the present investigations.

A recent study by Pinniger and colleagues [30] investi- The evoked potentials in the ECR muscle in Experimentgated the magnitude of the soleus and medial gastroc- 1 demonstrated a reciprocal response modulation to thatnemius H-reflex during passive muscle lengthening and seen in the FCR muscle, however the modulations wereshortening. In comparison to static H-reflex amplitude, less marked and failed to reach significance. It is knownthey found that responses in both muscles were signifi- that flexors of the hand and forearm have a greatercantly depressed during muscle lengthening and poten- distribution of direct corticomotoneuronal pathways thantiated during muscle shortening, a comparable finding to the extensors, and that for a unit change in firing intensitythat in our study. They also attributed the modulation to of these cells, a greater change in force is observed for thealterations in the discharge of primary spindle afferents. flexors than extensors [13]. These factors may contribute

An interesting feature of the pattern of response modula- to a reduced sensitivity of corticomotor pathways to thetion evident in our recent studies at different movement ECR muscle to changes in afference induced by wrist jointfrequencies is the apparent phase shift in peak response movement. Similar discrepancies in modulation betweenpotentiation in the wrist flexor muscle [25]. During passive flexor and extensor pathways have been reported in themovement at 1.0 Hz, the periods of the movement cycle tibialis anterior and soleus muscles of the lower limbcorresponding to rapid muscle shortening (phases 6 and 7) during rhythmic walking tasks [34]. The lack of significantdemonstrate the greatest response facilitation, with the findings in the extensor muscle may also be explained inpeak generally occurring at phase 6. By phase 8, where the part by the reduced subject number, as some participantswrist joint is decelerating and approaching maximum struggled to maintain quiescence in this muscle duringflexion, pathway excitability seems to return to static movement, and the determination of stimulus location andvalues or below. At movement frequencies of 0.2–0.6 Hz intensity based on responses recorded in the FCR muscle.responses are still facilitated during muscle shortening, Our results in both Experiments 1 and 3 also demon-however the peak amplitude generally shifts to phase 7 and strated phasic alterations in MEP latency that coincidedresponses remain potentiated at phase 8. At the slow with the modulations in MEP amplitude. At the cycle0.05-Hz movement frequency implemented in the current phases in which MEP amplitude was relatively facilitated,study, motor pathway excitability peaked at phases 7, 8 concurrent reductions in MEP latency were noted. Theand 1, or when the wrist joint was in a flexed posture covarying nature of these two parameters is a commonrather than when it was flexing. These findings may reflect feature of studies utilising TMS [32], and the findings inthe reduced influence of dynamic spindle endings (Ia) at the current study provide further evidence of increasedlow movement frequencies and an enhanced influence of cortico–motoneuronal pathway excitability during thestatic (IIa) receptors. We reported earlier that FCR MEP phases of the movement cycle where the muscle isamplitude was relatively facilitated when constrained shortening. The reductions in MEP latency likely reflect astatically in a flexed posture compared to extended, which shift in the descending volley mediating the evokedsuggests that reduced static spindle output is associated response. Studies examining single motor units have


demonstrated that multiple descending volleys separated comparison to relaxed conditions [22]. Similarly, a studyby 1–2 ms are generated in response to a single magnetic by Wise, Gregory, and Proske [41] revealed that jointstimulus over the motor cortex [17]. These have been movement detection threshold is higher during co-contrac-termed ‘I’ (indirect) waves and are numbered in order of tion of joint effector muscles compared to relaxed con-their appearance. At rest, it is thought that temporal ditions. This damping of receptor response output andsummation of 2–3 descending waves is required to de- modulation may contribute to the reduced modulation ofpolarise the motoneuron sufficiently to threshold [38]. If MEP amplitude during muscle activation conditions in thethe resting potential of the motoneuron is raised, or if the present study. It is also possible that the sensitivity ofsize of the descending volley is increased, the motoneuron secondary endings, which are likely to mediate pathwaymay depolarise upon receipt of the first descending wave, excitability more at the slow movement velocity, is downresulting in a latency shift of 1–2 ms. This may also occur regulated more so than primary endings, which are lessif cortical excitability is raised [19]. influenced by the 0.05 Hz rate. The potential influence of

golgi receptors is also likely to be reduced in the activated4 .2. Modulations in corticomotor excitability during conditions. The maintenance of a consistent level ofmuscle activation activation during movement would serve to stabilise

tension in the muscle, thereby reducing alterations in IbIn the upper limb, a number of levels exist at which output.

peripheral input may influence the excitability of the The pattern of response modulation during activateddescending motor pathway. The monosynaptic corticospi- conditions tended to follow that evident in relaxed mus-nal pathway is subject to direct input at the level of the culature at the equivalent frequency of movement. That is,motoneuron and to influences at the level of the cortex. It responses were elevated above static values at the cyclehas been demonstrated that responses to TMS in the upper phases where the target muscle was in a shortenedlimb also contain input from disynaptic pathways, which position. As MEPs evoked in the two muscles while theinvolve a population of premotoneurons located within the wrist joint was positioned statically at each of the cycleupper cervical region of the spinal cord (for review see phases did not demonstrate any effects of joint angle, theRef. [29]). Notably, these premotoneurons are subject to facilitated responses at these phases during movementexcitatory and inhibitory input from the periphery. likely reflect a dynamic effect of joint movement. The

By stabilising the excitability of the motoneuron pool non-significant results found in the static trials of Experi-with muscle activation, factors influencing the motor ment 2 are in contrast to our earlier study examining thepathway are essentially limited to those acting at a level effects of static joint angle in quiescent musculature [25].prior to the motoneuron. It is possible that alterations in The previous findings indicated a heightened pathwayefferent drive during the movement cycle, occurring in excitability while the muscle was constrained in a shor-response to variations in sensory input, may also influence tened position, whereas MEP amplitude was unaffected bythe size of the response to stimulation. During muscle joint angle in the current study while a consistent level ofshortening, a reduction in Ia output would lower muscle activation was maintained. Macefield and col-motoneuron excitability, thus resulting in a compensatory leagues [27] have demonstrated that, in the lower limb,increase in corticospinal axon recruitment to maintain the spindle receptor output progressively declines during iso-required level of EMG activity. This would, in turn, metric muscle activation. With the ankle in a dorsi-flexedincrease the number of refractory corticospinal axons, position, they found that the firing rate of spindle receptorsreducing the number available for recruitment by stimula- within an activated soleus muscle reduced to approximate-tion. However, with the very low levels of activation ly 50% of initial levels within 1 min of contraction. Onerequired in the current study, it is likely that this factor outcome of this would be a general disfacilitation ofwould make little contribution to changes in the size of the homonymous motoneruons. It is almost certain that aevoked response, and, notably, would also modulate similar disfacilitation would have occurred in the staticresponse amplitude in a manner opposite to that seen trials of the current study, although probably to a lesserduring the movement cycle. That alterations in response extent. As subjects maintained a consistent level of muscleamplitude were still evident at the different cycle phases activity, compared to a constant level of force in theduring muscle activation strongly indicates a supraspinal / Macefield et al. [27] study, it would likely manifest as anpre-motoneuronal influence on pathway excitability. Even increase in force output and efferent drive as subjectsthough modulations were modest in comparison to quies- attempted to maintain the required level of activationcent conditions, it seems likely that alterations in response during the 60-s trial. The relatively low levels of muscleamplitude in the relaxed forearm are likely attributable to output would, however, likely have minimal impact uponboth spinal and supraspinal mechanisms. response amplitude in the present study. It is also possible

Recent investigations have demonstrated that muscle that the thixotropic nature of muscle spindle output mayspindle primary afferents maintain their sensitivity to have influenced response amplitude in the various staticpassive stretch during voluntary muscle activation, al- positions. It is well known that spindle discharge isthough the modulation of output is down regulated in influenced by the length and activation history of the


muscle [31]. Response amplitude at a certain joint angle during the different phases of the movement cycle arewould be affected by whether the target muscle was predominantly determined by the position and movementlengthened or shortened from the previous position of the of the target limb itself and are not influenced significantlywrist joint. However, this is again likely have a minimal by the contralateral limb. From these findings, it wouldeffect on results in the current study as any slack in the appear that alterations in the gating of sensory input thatintrafusal fibres from re-positioning would have been have been noted in previous passive movement studieslargely taken up by the activation of the target muscle [20]. [35,36] do not necessarily influence the modulations ofThis would suggest that the influence of static muscle motor output to the homonymous muscle during passivelength on corticospinal excitability arises at the level of the movement. This is consistent with previous studies demon-motoneuron and has little, if any, supraspinal component. strating an independence of lower limb H-reflex amplitudeIn contrast, the marked modulations in response amplitude during tasks with different kinesthetic requirementsarising during movement appear to involve a supraspinal [15,26].influence. Controversy exists in the literature regarding the modu-

In a previous experiment with movement at 1.0 Hz [25], lation of afferent information during specific tasks requir-we found evidence of reduced ICI in the FCR muscle at ing increased afferent awareness. Some studies have beenthe initial two phases of wrist flexion, suggesting an unable to demonstrate changes in SEP amplitude duringenhanced cortical excitability. This was attributed to the tasks with high sensory demands [21], while it is alsoreduced Ia input during this period, which is likely to be apparent that alterations in SEP amplitude are less pro-highly modulated at this movement frequency. Other nounced in tasks involving the upper limb in comparisonresearchers have demonstrated that deafferentation reduces to the lower limb [23]. Staines et al. [36] noted alterationsICI and enhances cortical representation of muscles located in SEP gating of cutaneous- and proprioceptive-dominatedproximal to the site of blockage [12,42]. Aimonetti and nerves that were specific to the relevance of cutaneous andNielsen [1] also found that they could modulate ICI and proprioceptive information to the task. This specificity ofICF in forearm musculature (FCR, ECR) by conditioning gating may indicate that a required awareness of selectivewith antagonist nerve stimulation. Although antagonist proprioceptive information is insufficient to induce altera-nerve conditioning had no effect on non-conditioned MEP tions in general motor output. The lack of change in MEPamplitude, it facilitated ICF and inhibited ICI induced by amplitude during the tracking task in the current study maypaired pulse stimulation. Conditioning the homonymous also have been due to a relatively low level of tasknerve had no effect on either conditioned or non-con- complexity.ditioned MEP amplitude. The authors suggested that the In conclusion, this study demonstrated modulations inobserved reciprocal excitation may be useful in regulating motor pathway excitability during passive movement of aor maintaining co-contraction during tasks where the wrist pre-activated muscle. This suggests that movement elicitedjoint needs to be stabilised. In the current study we provide afference is influencing the motor pathway at a level priorfurther evidence of afferent input, in this case from to the motoneuron. The hypothesis that kinesthetic trackingmovement, influencing the excitability of motor pathways may further enhance changes in cortical excitability wasat a supraspinal level in a similar manner to that seen in not supported by the results of the study, although thisperipheral nerve conditioning studies. condition might best be further investigated with a more

complex kinesthetic task requirement, or in populations4 .3. Influence of kinesthetic tracking on corticomotor with motor and/or sensory dysfunction.excitability

It was hypothesised that corticomotor excitability would A cknowledgementsincrease when passive movement of the target wrist jointwas accompanied by active movement of the opposite The authors would like to express their gratitude to Jimwrist joint that was directed by proprioceptive information Stinear, Cathy Stinear and Shane Warbrooke for theirfrom the target limb. If the gain of Ia afferent input arising assistance in the laboratory. G.N. Lewis is supported byfrom the induced movement was increased by placing it in the Foundation for Research, Science and Technology.an active movement context, it follows that there may be This study was funded in part by a University of Aucklandsubsequent alterations in MEP amplitude. However, the Staff Research Grant.results of the current study did not support this hypoth-esis—FCR MEP amplitudes during the eight cycle phaseswere found to be equivalent between the passive move-

R eferencesment and kinesthetic tracking conditions. In an activecontrol condition, where movement of the active limb was

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