(60 ms). Short-latency reflexes were not seen. fusimotor drive during ...

Journal of Physiology (1988), 401, pp. 77-95 77With 6 text-figure8Printed in Great Britain

ROLE OF THE HUMAN FUSIMOTOR SYSTEM IN A MOTORADAPTATION TASK

BY NAJEM A. AL-FALAHE AND AKE B. VALLBOFrom the Department of Physiology, University of Umea, S-901 87 Umea, Sweden

(Received 23 June 1987)

SUMMARY

1. Single-unit activity was recorded with the microneurographic technique fromthe radial nerve of attending human subjects. During active finger movements,impulses in spindle afferents from the extensor digitorum muscle were analysed alongwith joint movements, size of imposed load and EMG activity of the receptor-bearingmuscle.

2. In a simple motor adaptation task the subjects were requested to performramp-and-hold movements of prescribed amplit-ades and velocities at a singlemetacarpo-phalangeal joint. A test run consisted of a series of movement cycles whenthe flexor muscle was continuously loaded with a constant torque, immediatelyfollowed by cycles when this load was abruptly decreased during the flexionmovement, producing a fast stretch of the receptor-bearing muscle. The subjects'task was to strive for movements of constant velocity and particularly to minimizethe effect of the disturbance. In order to allow prediction on the basis of immediatelypreceding cycles, the disturbance was always injected at the same angular positionin a number of successive cycles.

3. Motor adaptation was manifested as a successive decrease of the perturbationamplitude, usually associated with the development of a continuous and growingEMG activity in the parent muscle and a growing reflex response of long latency(60 ms). Short-latency reflexes were not seen.

4. The main mechanism accounting for the improved performance was a co-contraction of the agonist-antagonist muscle pair during voluntary movements,producing an increased muscular stiffness. The reflex did not contribute to the motoradaptation because it was not fast enough to curtail the perturbation.

5. The development and the growth of the reflex were not due to a growingfusimotor drive during adaptation, because spindle discharge actually decreasedwhen the reflex increased. The size of spindle response was related to the amplitudeof perturbation rather than to the amplitude of the reflex. These findings suggestthat reflex modifications were due to central excitability changes which paralleledthe muscle contraction.

6. Spindle firing rate during active movements was generally higher in disturbedcycles compared to undisturbed cycles, indicating a higher fusimotor drive. Sincemuscle contraction was present mainly in the former, this finding may simplyrepresent a case of fusimotor activation along with skeletomotor activation. Noindication of an independence between the two was found.

N. A. AL-FALAHE AND A. B. VALLBO

7. The findings lend no support for the view that the size of the stretch reflex ina behavioural task is adjusted by selective changes of the fusimotor drive.

INTRODUCTION

Since it was first shown that the simple monosynaptic reflex is but a fraction of themuscle's response to stretch, the separate components as seen in the EMG have beenanalysed extensively (Hammond, 1955, 1956; Hammond, Merton & Sutton, 1956;Desmedt, 1978). It has often been found that the MI response is uniform in size(Hammond, 1956; Hagbarth, 1967; Crago, Houk & Hasan, 1976; Evarts & Granit,1976; Gottlieb & Agarwal, 1979) whereas long-latency responses are modifiable byprior instruction to human subjects (Newson Davis & Sears, 1970; Evarts & Tanji,1974; Evarts & Granit, 1976; Marsden, Merton & Morton, 1976; Gottlieb & Agarwal,1979, 1980).

Modifications of reflex settings are probably one of the means that human subjectsas well as behaving animals may use to adapt their motor output to changingdemands and altered external conditions (Nashner, 1976; Ito, 1984). The presentstudy is concerned with the mechanisms of adaptation to a simple disturbance, i.e.a change of the external load which was repeatedly injected at predictable instantsduring a series of cyclic movements. The purpose was to explore which means humansubjects make use of when trying to perform a smooth movement in spite of adisturbance, i.e. if the motor programme is modified on the basis of prediction, or ifthe stretch reflex is adjusted. Reflex adjustments, in turn, might be accounted foreither by an altered fusimotor drive sensitizing the primary afferents or to centralexcitability changes.

It was found that the behavioural improvement was associated with a simplemodification of the motor programme and the appearance of a long-latency reflexwhich increased in successive cycles as subjects strove to compensate for thedisturbance. Recordings from spindle afferents demonstrated that the adaptation ofthe reflex was not due to an increased fusimotor drive but rather to central reflexadjustments. Moreover, stretch reflexes did not improve motor performance butbehavioural improvement was accounted for by a co-contraction of the agonist andantagonist muscles acting at the joint.

METHODS

Data were collected in five experiments conducted with five healthy subjects, four male and onefemale, 25-33 years old. All subjects were medical students or occupied in medical professions. Theexperiments were performed according to the Declaration of Helsinki, and the subjects had allgiven their informed consent.

Nerve recording. The activity of seven single afferent units was recorded from the left radial nerve6-8 cm above the elbow using the microneurographic method of Vallbo & Hagbarth (1968; fordetails see Vallbo, 1972). Nerve fascicles innervating the finger extensor muscles were exploredwhile the relaxed fingers were continuously flexed and extended by one of the operators. Thecharacteristic sound of multiunit responses from stretch receptors indicated a promising electrodeposition. Minute adjustments of the electrode were then made until a single afferent was clearlydiscriminable. Its responsiveness to passive and active movements of individual fingers was testedin order to identify the receptor-bearing portion of the muscle. The particular finger which evokedthe best movement response was identified as the optimal finger, and it was concluded that it was

78

HUMAN FUSIMOTOR SYSTEM 79

operated by the muscle portion carrying the sense organ. The receptor location as projected on thesurface was assessed by local pressure.

Unit cla&3ifiwation. When a single afferent originating from a deep stretch receptor wasencountered a series of tests were pursued to assess whether it was a muscle spindle or a Golgitendon organ. The classification of the seven units studied largely relied upon four tests. Data arecollected in Table 1.

TABLE 1. Identification dataTwitch Relaxation Dynamic ramp Active movement,

Unit test burst response stretch response1 + + ++ +2 + - / +3 + + / +4 + + + +5 + + + +6 + + ++ +7 + - _

The plus signs signify: in column 2, unloading response to electrically induced muscle twitch; incolumn 3, an impulse burst when the subject relaxed after an isometric contraction; in column 4,a dynamic response during imposed ramp movements; and in column 5, a stretch response duringactive sinusoidal movements as described in the text. Minus signs indicate lack of these featuresand slashes indicate that it could not be assessed whether the feature was present or not.

(1) Twitch tests were performed with electrical stimulation at the motor point of the receptor-bearing muscle portion using a bipolar cushion electrode (Disa, 13K62). With this percutaneousmethod a maximal twitch contraction was achieved without major discomfort for the subject (Edin& Vallbo, 1987). All seven units in this study exhibited a pause during the rising phase of theelectrically induced contraction and four of them an increased discharge on the falling phase. Thetwitch test was done under isometric conditions with four of the seven units. With the other threeafferents, the twitch test was done during active lengthening movements in order to produce abackground discharge, because these units were silent when the muscle was at constant length.

(2) An abrupt relaxation of an isometric voluntary contraction of the parent muscle portionproduced an accelerated discharge in five out of seven units. This was taken as strong support forthe unit being a spindle afferent rather than a Golgi tendon organ whose discharge, if anything,would decelerate when the active tension was falling. Moreover, a response of this kind probablysuggests a primary rather than a secondary spindle afferent. The contraction torque was 0-1 N mwhich corresponded to 12-21 % of the maximal voluntary torque.

(3) A high dynamic sensitivity to stretch of passive muscle indicates a muscle spindle primaryafferent rather than a secondary ending or a Golgi tendon organ (Matthews, 1972). During passiveramp-and-hold movements the dynamic response, including deceleration response, was estimatedfrom instantaneous rate plots. A standard amplitude of 20 deg was used with two velocities ofstretch, 20 and 50 deg/s, and an acceleration of 5000 deg/s2. Two units exhibited a high sensitivity,defined as a dynamic index larger than the difference in sustained discharge at the two hold phases,and one of them had a clear deceleration response at the end of the stretch phase (Matthews, 1972;Cheney & Preston, 1976a, b). Two other units had some dynamic response, and one had none atall. For the last two units the dynamic index could not be properly defined because they did notfire continuously at the stretched position. Muscle relaxation during ramp tests was checked in theEMG and the torque records.

(4) Subjects were asked to perform slow sinusoidal movements with a cycle duration of about5 s and an amplitude of about 25 deg while the parent muscle was opposed by a small load. Sixunits produced a discharge suggesting a stretch response with a considerable dynamic sensitivityduring the active movements, e.g. the rate was higher during lengthening than during shorteningand it was often higher with long muscle than with short muscle. In contrast, a positive relationshipto the amplitude of the EMG was lacking. These observations support, by exclusion, the conclusionthat the units were spindle afferents since it has been shown that tendon organs fire in relation tothe level of motoneuronal discharge in normal movements (Prochazka & Wand, 1980).

80 N. A. AL-FALAHE AND A. B. VALLBO

The outcome of the test battery suggested that at least four or five units were primaries.EMG recording. Before nerve recording was initiated, four silver disc electrodes (SLE, B1-9) were

attached to the skin over the finger extensor muscles at selected positions. Optimal locations werecarefully tested to give adequate recording of the separate portions of the muscles. In theindividual experiment, EMG recordings were made with the pair of electrodes which gave theoptimal signal from the receptor-bearing muscle portion.

Actuator. The subject was comfortably seated in a dentist chair with his left arm semi-extendedwhile the forearm was resting in an adjustable vacuum cast. The hand was strapped to amechanical support which kept the wrist joint in a fixed position whereas the test finger wasconnected to a servo-controlled actuator. A splint kept the inter-phalangeal joint extended whileactive and passive movements were performed at the metacarpo-phalangeal joint. A hinged bar oflow mass joined the finger splint with a rigid arm extending from the actuator axle.The actuator featured a number of different feed-back modes and conditional trigger facilities.

The most essential operational modes employed in the present study were position holding,imposed movements with accurately defined angular amplitudes, velocities, and accelerations, andthe generation of constant torque loads as well as instantaneous changes of load size. Moreover,conditional triggering and conditional shifts between feed-back modes and instantaneous settingsof feed-back parameters were utilized. The actuator was controlled by a microcomputer which wasprogrammed for the individual tests. The computer also controlled a system providing instructionsto the subject using an alpha-numeric display, a set of light diodes, and speakers. During theexperiment proper, the separate test programmes were initiated from the microcomputerkeyboard.Motor adaptation te8t. In the main test run the subject was instructed to perform a series of ramp-

and-hold movements with one single finger on the basis of a criterion movement presentedimmediately before. The movements, which alternated between flexion and extension, wereperformed around the resting position of the finger. Desired amplitudes and velocities were 30 degand 25 deg/s. Two flexible nylon rods were arranged to give light-touch clues at the desired end-positions.

In the instructions to the subjects, it was particularly emphasized that he/she should make aneffort to keep the velocity constant and uniform regardless of any load changes that might occur.In a number of successive movement cycles, a disturbance was injected and the subject's task wasto minimize its effect. The basic load condition was a constant torque load opposing flexion whereasthe disturbance was a sudden reduction of this load to one-third of its basic value during flexion,thus rapidly stretching the receptor-bearing muscle. The disturbance was injected, withoutwarning to the subject, at an identical angular position in a number of successive movementcycles.The baseline load was between 0-06 and 0-15 N m in different runs, corresponding approximately

to 5-10% of maximum voluntary torque of the relevant finger's flexor muscles. After thedisturbance, the original torque was gently restored in a series of twenty small steps during thephase of self-generated extension movement. However, in some cycles the subject failed to producethe desired slow movement and a more abrupt torque restoration occurred.The subjects were exposed to the test procedure in a short session before the nerve recording was

initiated. Thus, they were aware that a disturbance would appear in a number of successive cyclesand at an identical angular position.

Data collection and analy8i8. A Philips analog tape-recorder (Analog 714) was used to recordnerve impulses, EMG activity, angular position at the metacarpo-phalangeal joint, angularvelocity and torque. The signals were displayed off-line on paper with a Gould (ES 1000)electrostatic recorder and selected portions were sampled by a laboratory computer (Nord 500).Nerve impulse rates, amplitudes of movement, and angular velocities of the perturbations were

measured by eye from the displayed record. The raw EMG signal was rectified and low-pass filtered(220 Hz) off-line and sampled at 500 Hz. Its mean amplitude was computed for an interval of250 ms immediately before the disturbance and for the reflex interval, i.e. between 50 and 90 msafter the disturbance.

In order to allow pooling of data from different experiments, variables were normalized. Theamplitude and velocity of perturbation were normalized to the amplitude and velocity of the firstperturbation in the test sequence. Means of EMG during the pre-disturbance sampling period andthe reflex period, as defined above, were normalized to the maximal pre-disturbance EMG of the

HUMAN FUSIMOTOR SYSTEM

whole test run. The number of nerve impulses and impulse rates were normalized to their highestvalue in the test sequence.

StatistC8. Conventional parametric and non-parametric statistical methods were used in theanalysis (Snedecor & Cochran, 1967; Colton, 1974; Daniel, 1978). Pearson's product momentcorrelation coefficient is indicated by r and Spearman rank correlation coefficient by rs. Wilcoxonrefers to Wilcoxon's matched-paired signed-rank test.Sample 8ize. Seven spindle afferents were studied, the majority of which were probably primaries.

With two afferents, the test run was executed twice. Thus, altogether data from nine runs werecollected. Mostly, the individual run included ten successive movement cycles with disturbances,whereas two runs were limited to eight and six such cycles. Thus, the analysis of reflex adaptationwas based on altogether eighty-four cycles of active movements with perturbations. As theexperimental protocol was quite demanding, a large number of additional experiments were donewhich did not yield a stable unit during the whole test period.

120 deg

I(long muscle)

Joint angle 160 deg(short muscle)200

Angular _W_ 0 deg/s

-200

Torque

load _______10 s I_ _ _ -015Fig. 1. Extracts of experimental run. Records show from above, metacarpo-phalangealjoint angle of the test finger, angular velocity, and torque load applied to the finger.Flexion, which implies lengthening of the receptor-bearing muscle, is indicated upwards.The cycle to the left is a passive criterion movement whereas the other six cycles areactively reproduced by the subject. The load which opposed flexion was constant in thefirst three active cycles whereas it was abruptly reduced during the flexion movement inthe following three cycles, thus rapidly stretching the receptor-bearing muscle. The actualtest protocol included twenty-two cycles as described in the text.

RESULTS

Neural activity in single spindle afferents from the finger extensor muscles wasrecorded during a test run which was designed to study a simple form of motoradaptation. The subject's task was to minimize the effect of a sudden load changewhilst performing a series of flexion and extension movements with one single finger.Figure 1 shows extracts from the test run.

Initially, the finger was moved passively by the actuator through three cycleswhich were strictly ramp shaped with short hold phases at the end-positions (Fig. 1,left). The subject was not allowed to see the criterion movements whereas he wasinstructed carefully to observe kinaesthetically their amplitude, time course, andparticularly their velocity.

Immediately following the criterion movements, the subject was requested to

81

82 N. A. AL-FALAHE AND A. B. VALLBO

perform actively similar movements on the basis of his kinaesthetic memory. In theinstructions it was particularly emphasized that he should try to keep the velocityconstant and identical to that of the criterion movement. A tactile clue was providedwith regard to amplitude.

901-

X ' 80

4 E'1 2 3 4 5 6 7 8 9 10

0.a}

0 >. Serial order of cycle

B120

100**-. * *

100 -. .

80

60*~~~~~~~~ *

40

20 40 60 80 100Amplitude of pre-disturbance EMG (%)

Fig. 2. A, adaptation of motor performance with successive movement cycles. Ordinategives the normalized amplitude of perturbation associated with a step change of torquewhereas abscissa gives the serial order of movement cycle. Pooled data from all nine testruns. Filled circles and vertical lines represent means and standard deviations. B,relationship between amplitude of perturbation and amplitude of pre-disturbance musclecontraction measured as the mean integrated EMG for the interval of 250 ms immediatelybefore the disturbance (r =-0-33, P < 0-001).

In the first six cycles of actively reproduced movements, a constant torque loadassisted the receptor-bearing muscle. Hence, contraction of this muscle was notrequired for an adequate performance and, in fact, it often remained passive. Theflexor muscles, on the other hand, were continuously working against the imposedtorque load.As shown in Fig. 1, the reproduced movements did not exactly match the criterion

movements. Particularly, the angular velocity was more irregular and clear holdphases were often lacking. However, the average angular velocity was in the same


range both during flexion and extension movements. Thus, the subject wasreasonably successful in fulfilling his task, i.e. to perform ramp movements of similarvelocity as the criterion movements.

After the first six cycles of actively reproduced movements, a series of ten cyclesfollowed which all carried an identical disturbance, viz. in the middle of the flexionphase, when the receptor-bearing muscle was lengthening, a sudden reduction of thetorque was introduced. This disturbance resulted in a perturbation of the finger, i.e.a fast flexion causing a rapid stretch of the receptor-bearing muscle. After the lastdisturbed cycle, three undisturbed cycles followed (not illustrated in Fig. 1).

Motor adaptationAs the subject knew that a series of successive cycles would carry identical

disturbances, he had the chance to prepare and adjust his motor output successivelyfrom one cycle to the next in order to approach an optimal performance, i.e. a smoothmovement of uniform velocity. In Fig. 1, the decrease of amplitude and peak velocityof perturbation illustrates the progressive improvement of performance.

All the subjects exhibited adaptation of this nature although it was not very largeand not always monotonous in the whole test sequence. Figure 2A displays thepooled data from all test runs. The filled circles represent means of normalizedamplitudes of perturbation whereas the vertical bars give the standard deviations.The diagram shows that there was a decrease of perturbation amplitude from thefirst to the sixth cycle, indicating a successive motor adaptation, whereas asystematic change was not present in the later part of the sequence.The trough of the curve was at 84% indicating that the maximal compensation

averaged a decrease of about 15% relative to the perturbation of the first cycle. Incontrol experiments it was shown that prolongation of the sequence did not providefurther improvement. Corresponding curves from individual test runs showed aconsiderable scatter but they all exhibited a decrease of perturbation with cycleorder, although often not a monotonous decrease.

Absolute amplitudes and velocitiesThe present data are mostly reported in normalized form as described in Methods,

but it seems of interest to point out that the perturbations were fairly large as maybe seen in Fig. 1. In the whole material the amplitude of the perturbation was14 1+4-2 deg and peak angular velocity was 294+68 deg/s (means and S.D.).

Restoration of the loadSometimes an unfavourable effect was present when the bias torque was reapplied.

If the subject failed to produce a return movement of low velocity, the higher loadwas restored quite abruptly as in the first cycle of Fig. 1 (see Methods). This effectmight complicate the subject's motor adjustments, although it was probably ofminor significance for the main results since it occurred only in a few cycles.

Modification of the voluntary skeletomotor activityIn the undisturbed cycles the parent muscle was usually silent whereas a

successively increasing activity often appeared in the second and the following

83


disturbed cycles. Figure 3 shows the first three disturbed cycles from a sample run,demonstrating that the adaptation of motor performance was associated with agrowing pre-disturbance contraction of the parent muscle as well as a growing reflexas seen in the EMG record.

4.li,1111 I,#4..1 0-2 mV120 deg

(long muscle)

160 deg(short muscle)200

0 deg/s

-100

Afferentol_ L-T 17JFrLoad 0-15 N m

7 -_ 0-05

1 s

Fig. 3. Adaptation of responses to disturbance. Sample records showing time windowsfrom the phase of active lengthening of the first three disturbed cycles of a series. Thedisturbance was a sudden decrease of a load assisting the receptor-bearing muscle whichwas then stretched. The traces show, from the top, EMG recorded from the finger extensormuscle with surface electrodes, metacarpo-phalangeal joint angle of the test finger withflexion movements indicated upwards, angular velocity, impulse discharge in a spindleafferent from the extensor muscle, and torque load. Same run as in Fig. 1.

The pre-disturbance EMG did not increase regularly all through the ten cycles butusually varied in a more complex manner. However, a successive increase was oftenpresent during the first few cycles. When data from all tests were quantified it wasfound that the amplitude of perturbation was inversely related to the amount ofEMG activity recorded from the receptor-bearing muscle immediately before theperturbation, although there was a considerable scatter (Fig. 2B).

It can be inferred that the activity in the parent muscle was an expression of a

balanced co-contraction of flexors and extensors with the effect that the stiffness ofthe joint increased. As will be considered below, this was probably the mainmechanism which accounted for the improved performance.

Reflex response

The adaptation of motor performance was associated with the development of a

reflex response in the receptor-bearing muscle which was stretched by theperturbation. In the sample run of Fig. 3, a reflex is lacking altogether in the firstcycle, it is present in the second cycle, and a still larger reflex appears in the third.Similar responses were seen with seven experimental runs, i.e. the reflex usually

EMG L

I~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~

Jointangle

Angularvelocity

84


increased in size with serial order of cycle. In the remaining two runs, reflexes werelacking altogether in the EMG record.

Figure 3 also illustrates that the EMG reflex was larger the smaller the perturbationin the three test cycles. This was generally true as revealed by a linear regressionanalysis ofpooled data from all nine test runs (r = -0-65, P < 0-001). The finding thatthe EMG reflex increased when the perturbation decreased clearly demonstrates thatthe variation of the reflex amplitude was not simply due to a variation in stimulus,i.e. the amplitude and velocity ofperturbation, but neural mechanisms accounted forthe growth of the reflex.

EMG him10.2EMG~~ ~~~~~~~~V05J 0o-2 mV

Afferent

t - ~~~~~~~200deg/s

Angularvelocity 0

J 135 deg (long muscle)

angle 145 deg (short muscle)

Load I0 06 Nm

150ms1Fig. 4. Sample record of events associated with a perturbation presented on an expanded

time scale. The records show the same signals as Fig. 3.

Latency of reflex responseThe fact that the reflex increased when the subject managed to decrease the

perturbation suggests that a modulation of reflex mechanisms was an element in thestrategy of motor adaptation. However, it is clear that this was not an effectivemeans because the reflex was not fast enough, as illustrated by a representativeexample (Fig. 4), showing that the perturbation was largely completed when thereflex appeared. Hence it can be concluded that the reflex did not account for thereduction of perturbation, particularly since another 20 ms is required before themechanical effects come through. The mean latency of the EMG response in the totalsample was 57-5 ms (S.D. = 5-1 ms). No sign of earlier reflexes was found in theoriginal, nor in the rectified and averaged, EMG records.

Modification of the stretch reflexOn the assumption that the EMG response represents a stretch reflex elicited by

spindle afferents, it may be concluded that two different kinds of mechanisms are

85


A

I

S

3

I

S

20 40 60 80Relative number of impulses (%)

8

0 0..0 0 0 ..a B

* 00 0 0

0 0 *s-f ** 0

-0 S*- * * *

0 0

0 *

40 60 80 100 120

Amplitude of perturbation(% of first cycle amplitude)

Fig. 5. A, relationship between spindle afferent response to perturbation and size of reflex.Amplitude of reflex response measured as mean rectified EMG in the period 50-90 ms isplotted against the number of impulses in single spindle afferents. Pooled data from allruns normalized as described in Methods (rs = -0-54 P < 0-001). B, relationship betweennumber of impulses in afferent response and amplitude of perturbation. Pooled data fromall runs normalized as described in Methods (rs =-0-64, P < 0-001). Lines are based on

linear regression analysis.

most likely to account for its modification. Either the excitability of neural elementsin the reflex centre was modified or the fusimotor activity was changed with theeffect that larger responses in spindle afferents were induced by the smallerperturbations. Recordings of spindle afferents during the motor adaptation task werepursued in order to clarify which of these two mechanisms accounted for the reflexmodulation.

86

400 -

s

° 300-a'cn

x10

(o 200-w

0

. 100

E

0

00~~~~~~~~

l

100

100 -

80 -

60-

40

0.at

.0E

-4-

CU'

(UU'

20-. . .

* 0


Muscle spindle response to perturbationSpindle response to perturbation consisted of a few impulses, maximally four, at a

high rate during the fast stretch phase (85 + 37 impulses/s, mean + S.D.) (Figs 3and 4). The records of Fig. 3 are also representative in showing that the impulsedischarge did not increase with the size of the EMG reflex, but rather decreased, asalso demonstrated in the plot of Fig. 5A. Although the relationship between reflexamplitude and number of impulses is not all that striking, the slope of the regressionline is negative and statistically significant. This particular finding directly indicatesthat the increase of the EMG reflex associated with motor adaptation was notaccounted for by a modulation of the fusimotor drive to provide larger spindledischarge in response to smaller perturbations. Hence, it must be assumed that analtered excitability of neural elements other than the extensor spindles was the keyfactor modulating the stretch response as seen in the EMG.The spindle response consisted of a single burst of impulses whereas grouping of

the discharge was not seen (Hagbarth, Hiigglund, Wallin & Young, 1981). Thus, the'resonance hypothesis' is not a valid explanation for the long-latency reflex in thepresent experiments but a long loop seems more likely (Eklund, Hagbarth, Hiigglund& Wallin, 1982).

In contrast, a positive relationship was present between spindle response andperturbation amplitude as shown in Fig. 5B implying that spindle discharge actuallydecreased as the subject's adaptation improved. It can therefore be concluded thatany increase in fusimotor drive that might have occurred in the process of motoradaptation did not overrule the effect of stretch reduction in reducing the spindleresponse to stretch.

Impulse rate of stretch responseIt might be argued that the number of impulses is not the only relevant parameter of the afferent

discharge but the impulse rate might be significant as well. To explore this aspect the relationshipbetween amplitude of EMG reflex and impulse rate of spindle response to perturbation wasanalysed. The findings did not support the assumption that reflex size was directly dependent onimpulse rate.

Reflex size related to pre-disturbance EMOA fairly close relationship existed between the amount of pre-disturbance EMG and the size of

EMG reflex response to the disturbance (r = 044, P < 0001) consistent with the interpretationthat the size of the reflex was related to excitability of the motoneurone pool immediatelybeforehand.

Fusimotor adjustmentIt was shown in preceding sections that the successive increase of the stretch reflex

which occurred in the process of motor adaptation was not the result of an increasedfusimotor drive, making the spindle endings more sensitive to the perturbations. Onthe other hand, this conclusion does not exclude that some modification of thefusimotor drive did occur. However, a measurement of spindle sensitivity toperturbations was complicated by their varying amplitude and velocity.On the other hand, a mere inspection of the records revealed that spindle rates

were often higher in disturbed cycles than in undisturbed cycles and the ratesincreased as the compensation improved (Fig. 3). In the whole sample, the mean

87


impulse rate was about 30% higher in the disturbed cycle (741 impulses/s) than inthe undisturbed cycles (5 4 impulses/s) when measured during a time period of 1 simmediately preceding the disturbance and the difference was statistically significant(P < 0-02, Wilcoxon).An illustration of the effect of anticipation was obtained when the first few cycles

without disturbance after the perturbed sequence were compared (Fig. 6). In the first

A

EMG 0T2 mV

10T deg (long muscle)

JointII12angle1

160 deg (short muscle)

Afferent

Load _ ,r-.---- 015 Nm0*05

2 s

120 deg (long muscle)B

Jointangle lt160 deg (short muscle)

Angular ~50 deg/svelocity _550Impulse . . 20 impulses/srateLoad 0 N

Fig. 6. Effect of anticipation. A shows the last cycle of ten carrying a disturbance as wellas the following two undisturbed cycles whereas B shows the two undisturbed cycles ofA on an expanded time scale. The larger discharge from the spindle primary afferent aswell as the larger EMG activity when the subject was expecting a disturbance areobvious.

one, subjects were still expecting a disturbance. On the other hand, they knew fromprevious experience that the second and the following cycles would be clean, becausedisturbances were always injected in a single series of successive cycles. A comparisonbetween the first and the second cycle after the perturbations indicated that theafferent discharge was usually larger in the first one, as illustrated in the samplerecord of Fig. 6A and B. The finding suggests a larger fusimotor drive when thesubject was expecting a disturbance.

It should be emphasized that, in addition to the increase in spindle afferentdischarge, the extrafusal contraction was usually higher in the first cycle after theperturbations than in the second one, as also illustrated in Fig. 6A.

88


DISCUSSION

Subjects' taskThe present study is concerned with a simple form of motor adaptation in human

subjects. Young adult volunteers were asked to perform cyclic finger movements ofprescribed velocity and amplitude and to compensate for an abrupt change of torquewhich tended to upset the movement. Because the disturbance was injected in aseries of successive cycles and was always presented at identical joint position,the subject was free to engage predictive mechanisms and successively adapt hismotor activity on the basis of previous experience. Since visual control was deniedaltogether, the subject had to rely on information from proprioceptive and cutaneousreceptors exclusively.The experimental paradigm of the present study was different from that in many

other investigations of the stretch reflex (Desmedt, 1978). The task was designed tomake the subject strive for a motor performance which would be assisted by a faststretch reflex in the receptor-bearing muscle. Moreover, the subject was allowed topredict the disturbance and successively improve on the basis of previous experience.It has been shown that adaptation of the stretch reflex is dependent on the subject'santicipation as well as the usefulness of the reflex to approach the desired motorperformance (Nashner, 1976). In contrast, many earlier studies employ a paradigmwhere the stretch reflex is not of help in improving the performance but is merely aresponse to a repeated disturbance which the subject knows he cannot neutralize(Desmedt, 1978). It was hoped that the present approach would be more apt todisclose adaptive mechanisms. Moreover, the present task directly conforms to theinfluential servo-assistance hypothesis, i.e. that an important function of the stretchreflex is to decrease the effect of external forces which tend to upset a movement fromthe desired path (Matthews, 1964).The stretch reflex has previously been studied mostly in a prime mover or a main

force generator of an isometric task whereas the present study is focused on a musclewhich was passively stretched by the prime movers. This design feature was dictatedby an interest to explore reflex mechanisms in the antagonist of the prime moverwhich might be of considerable significance in compensating for external forcesthrough spindle effects on its own motoneurones as well as on I a inhibitoryinterneurones to the prime mover (Eccles & Lundberg, 1958; Hultborn, 1972).

Motor adaptationAll subjects demonstrated adaptive control behaviour (Gibson, 1963; Ito, 1984)

which was evident from the successive decrease of perturbation amplitude in a seriesof cycles. However, the improvement was not very pronounced, about 15% in thepooled data, suggesting that powerful mechanisms are lacking for this kind of loadcompensation in the system studied, i.e. flexor and extensor muscles of humanfingers.

It is interesting that different effects with regard to reflex adaptation compared tothe present ones may be obtained when a different paradigm is used. Rothwell, Day,Berardelli & Marsden (1986) have recently shown that the long-latency stretch reflex(45-50 ms) in human finger muscles, in fact, habituates, i.e. decreases in size when

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the perturbation is repeated. The subject was instructed not to intervene while hewas maintaining a constant level of isometric activation. In this task the reflexseemed to have no behavioural significance. In our study, on the other hand, theinstruction was to decrease the perturbation and here it was found that the reflexincreased with repetition. However, it should be emphasized that the change of reflexsize was not identically defined in the two studies and a detailed comparison istherefore not reasonable. In Rothwell et al.'s (1986) investigation, the pre-disturbanceEMG was kept constant between tests and the size of the reflex was measuredrelative to this activity. In our study, on the other hand, the pre-disturbance EMGwas allowed to vary between tests and the reflex was measured in relation to thehighest pre-disturbance EMG of the complete test sequence.

Mechanisms of adaptationIn Ito's (1984) theory of the cerebellum as a learning device, it is suggested that

cortico-nuclear microcomplex units constitute sidepaths superimposed on individualmotor mechanisms. It is assumed that optimal motor performance is graduallyapproached, by sidepaths modifying two different kinds of systems, i.e. reflexmechanisms and central control systems. In the present task, adaptation wasassociated with adjustments of a stretch reflex response as well as modifications ofskeletomotor activity during active movements. Although the reflex response of thereceptor-bearing muscle was not effective in improving the motor performance in thisparticular test when a very abrupt perturbation was injected, it still seems of interestto analyse the mechanisms which accounted for the reflex adjustments.

Reflex responseThe receptor-bearing muscle which was rapidly stretched by the disturbance

exhibited a gradually increasing reflex response. It was clearly a long-latencyresponse whose nature is still under debate (Marsden, Merton & Morton, 1972 a, b,1976, 1977; Lee & Tatton, 1975; Tatton, Forner, Gerstein, Chambers & Liu, 1975;Desmedt, 1978; Matthews, 1984 a, b). However, our conclusions are largelyindependent of whether the response has a spinal or supraspinal origin (Phillips,1969; Desmedt, 1978; Evarts & Fromm, 1981; Hagbarth et al. 1981; Wiesendanger& Miles, 1982) or whether it is a true reflex or a triggered reaction (Crago et al.1976).

It deserves emphasis that a short-latency reflex was lacking altogether. Theexperimental situation was designed to put the subject in a position where such areflex might be helpful to solve the motor control problem he was facing. Moreover,he was given ample opportunity to take any measures needed to produce such areflex. Thus, the findings suggest that a fast servo-assistance action (Matthews, 1964)which might compensate for load changes with regard to speed of movement islacking in these muscles, at least in this task.The long-latency reflex was too late to improve motor performance in the present

test. It remains to be clarified whether this reflex may produce an effectivecompensation for less-abrupt disturbances during continuous movements.

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Mechanisms of reflex adjustmentThe analysis of spindle response in relation to size ofEMG stretch reflex provided

a definite rejection of the hypothesis that fusimotor adjustments of extensor spindlesaccounted for reflex adaptation. Although the material of spindle recordings is notvery large, the conclusion still seems justified since the findings were totally uniformon this point.

In contrast, the findings are consistent with modifications of central reflexexcitability being responsible rather than muscle spindle sensitivity. This conclusionis largely consistent with previous studies on man, demonstrating that reflexresponses to stretch are adjusted by mechanisms independent of the fusimotorsystem in isometric contractions and during position holding as well as in theJendrassic manoeuvre and in the preparatory phase before a voluntary movement isinitiated (Hagbarth, Wallin, Burke & Lofstedt, 1975; Burke, Hagbarth, Lofstedt &Wallin, 1976; Burke, Hagbarth & Lofstedt, 1978; Burke, McKeon, Skuse &Westerman, 1980).A large number of neural mechanisms might be involved in central reflex settings

(Baldissera, Hultborn & Illert, 1981) but the present findings do not allow veryspecific conclusions in these respects. It seems very likely, however, that a simplemechanism, i.e. a raising of motoneurone excitability, was a prominent elementbecause the size of the reflex was related to the amount of muscular activity presentin the muscle immediately before the stretch. Conceptually, the indication of aroughly parallel change of reflex size and motoneurone excitability suggests that ashift of off-set was the main effect. However, whether a gain shift occurred as wellwas not analysed.

Receptor systemsA basic assumption in the present investigation, as in most other studies concerned

with responses of human muscles to sudden stretch, is that the crucial afferent inputoriginates from muscle spindles. However, recent investigations indicate thatcutaneous afferents in the human hand may give rise to reflexes of similar latency(Johansson & Westling, 1984, 1987; Darton, Lippold, Shahani & Shahani, 1985). Onthe other hand, cutaneous anaesthesia does not regularly decrease or abolish thereflex (Loo & McCloskey, 1985) indicating that proprioceptors, and probably musclespindles, play a significant role in the long-latency reflexes of finger muscles,although complex interactions between separate afferent systems may occur(Marsden et al. 1977).The proportions of spindle primaries and secondaries were not totally clear in the

present sample although a fair proportion were certainly primaries. On this basis, itcan be ruled out that reflex modulations were due to an increase of the dynamicfusimotor activity because our spindle primaries did not exhibit an increased afferentfiring when the reflex increased. On the other hand, if secondary afferents accountedfor the long-latency reflex (Matthews, 1984a, b), a remote possibility remains that wehave missed an increased response from spindle secondaries by static fusimotoractivity assuming that we recorded from primaries exclusively.

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Modifications offusimotor driveAlthough it was demonstrated that fusimotor mechanisms did not account for the

reflex adjustments, spindle recordings clearly demonstrated that the fusimotoractivity did, in fact, increase when disturbances were introduced. Thus it seems thathuman subjects may produce a larger fusimotor output during voluntary movementswhen they are expecting a disturbance which they try to compensate, than in similarmovements without an expected disturbance.

Consistent with many other studies on human subjects, the higher fusimotor driveappeared when the muscle was actively contracting (Vallbo, Hagbarth, Torebjork &Wallin, 1979). However, this does not exclude that it may play a specific role, e.g.providing more-detailed information about the movement when the subject wasanticipating a disturbance.A positive relationship was found between muscle spindle discharge and amplitude

of perturbation implying that the sense organs provided direct information about thesize of the disturbance. Thus, the spindle fulfilled, in a broad sense, the requirementof an error detector.

In the classical model of motor adaptation, the vestibulo-ocular reflex, two sets ofsense organs are involved. The vestibular organs elicit the reflex in a feed-forwardsystem whereas the retina records the adequacy of the reflex. Thus, the visualinformation provides a kind of knowledge of result (Salmoni, Schmidt & Walter,1984) which constitutes the basis of reflex modification. Similar roles of sensoryinformation might be postulated also in other systems (Ito, 1984), i.e. one group ofreceptors might produce the reflex effect whereas another group might provideknowledge of result. However, it is also conceivable that the same group of senseorgans has the two roles. Our findings, which are concerned with a much simpler andmore short-lasting form of motor adaptation, are consistent with the muscle spindleshaving a dual function. They may account for the stretch reflex and, in addition,describe the actual performance and thus provide an error signal which mightconstitute the basis of motor programme adaptation.

Skeletomotor adjustmentsThe actual improvement of performance in the present test was probably due to

a co-contraction of agonist and antagonist which produced an increased stiffnessaround the test joint resulting in smaller perturbations. We explored the hypothesisthat subjects, in addition, used more parsimonious strategies than long-lasting co-contractions. However, there was no indication of more-refined compensatorymechanisms, e.g. a slowing of the movement or an increased co-contractionimmediately before the disturbance. Whether longer periods of training or morespecific instructions would engage more-refined mechanisms remains to be explored.

Interdependence of adaptation mechanismsThe findings indicate that the simple form of motor adaptation studied in the

present investigation was associated with modifications of at least three mechanisms,viz. the motor programme which resulted in a co-contraction of the agonist-antagonist muscle pair, the central reflex state, and the fusimotor activity. Thus

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the adaptation involved adjustments of central control systems as well as reflexmechanisms (Ito, 1984) although the former alone accounted for the improvement ofmotor performance in this particular case. The modification of the reflex state maybe a simple effect of an increased motoneurone excitability and the increasedfusimotor drive may reflect the ubiquitous finding in man that the fusimotor systemis brought into action when the muscle contracts whereas there was no indication ofan independent control of the three mechanisms.

This work was supported by the Swedish Medical Research Council (Grant 3548), the MedicalFaculty of Umea (Fonden for Medicinsk Forskning), and Gunvor and Josef Aners Stiftelse. Thetechnical support by Mr Lars Biickstrom is gratefully acknowledged.

REFERENCES

BALDISSERA, F., HULTBORN, H. & ILLERT, M. (1981). Integration in spinal neuronal systems. InHandbook of Physiology, section I, The Nervous System, vol. II, part 2, pp. 509-595. Bethesda,MD, U.S.A.: American Physiological Society.

BURKE, D., HAGBARTH, K.-E. & LOFSTEDT, L. (1978). Muscle spindle responses in man to changesin load during accurate position maintenance. Journal of Physiology 276, 159-164.

BURKE, D., HAGBARTH, K.-E., LOFSTEDT, L. & WALLIN, G. (1976). The responses of human musclespindle endings to vibration during isometric contractions. Journal of Physiology 261, 695-711.

BURKE, D., MCKEON, B., SKUSE, N. F. & WESTERMAN, R. A. (1980). Anticipation and fusimotoractivity in preparation for voluntary contraction. Journal of Physiology 306, 337-348.

CHENEY, P. D. & PRESTON, J. B. (1976a). Classification and response characteristics of musclespindle afferents in the primate. Journal of Neurophysiology 39, 1-8.

CHENEY, P. D. & PRESTON, J. B. (1976b). Effects of fusimotor stimulation on dynamic and positionsensitivities of spindle afferents in the primate. Journal of Neurophysiology 39, 20-30.

COLTON, T. (1974). Statistics in Medicine. Boston: Little, Brown.CRAGO, P. E., HOUK, J. C. & HASAN, Z. (1976). Regulatory actions of human stretch reflex. Journal

of Neurophysiology 39, 925-935.DANIEL, W. W. (1978). Applied Nonparametric Statistics. Boston: Houghton Mifflin.DARTON, K., LIPPOLD, 0. C. J., SHAHANI, M. & SHAHANI, U. (1985). Long-latency spinal reflexes

in humans. Journal of Neurophysiology 53, 1604-1618.DESMEDT, J. E. (ed.) (1978). Cerebral motor control in man: long loop mechanisms. Progress in

Clinical Neurophysiology, vol. 4. Basel: Karger.EcCLES, R. M. & LUNDBERG, A. (1958). Integrative pattern of Ia synaptic actions on motoneurones

of hip and knee muscles. Journal of Physiology 144, 271-298.EDIN, B. B. & VALLBO, A. B. (1987). Twitch contraction for identification of human muscle

afferents. Acta physiologica scandinavica 131, 129-138.EKLUND, G., HAGBARTH, K.-E., HXGGLUND, J. V. & WALLIN, E. U. (1982). The 'late' reflex

responses to muscle stretch: The 'resonance hypothesis' versus the 'long loop hypothesis'.Journal of Physiology 326, 79-90.

EVARTS, E. V. & FROMM, C. (1981). Transcortical reflexes and servo control of movement.Canadian Journal of Physiology and Pharmacology 59, 757-775.

EVARTS, E. V. & GRANIT, R. (1976). Relation of reflexes and intended movements. In Progress inBrain Research 44, 1-14.

EVARTS, E. V, & TANJI, J. (1974). Gating of motor cortex reflexes by prior instruction. BrainResearch 71, 479-494.

GIBSON, J. E. (1963). Non-linear Automatic Control. New York: McGraw Hill.GOTTLIEB, G. L. & AGARWAL, G. C. (1979). Response to sudden torques about ankle in man:

myotatic reflex. Journal of Neurophysiology 42, 91-106.GOTTLIEB, G. L. & AGARWAL, G. C. (1980). Response to sudden torques about ankle in man II.

Postmyotatic reactions. Journal of Neurophysiology 43, 86-101.

93

9N. A. AL-FALAHE AND A. B. VALLBO

HAGBARTH, K.-E. (1967). Electromyographic studies of stretch reflex in man. Electroencepha-lography and Clinical Neurophysiology 25, suppi., 74-79.

HAGBARTH, K.-E., HXGGLUND, J. V., WALLIN, E. U. & YOUNG, R. R. (1981). Grouped spindle andelectromyographic responses to abrupt wrist extension movements in man. Journal ofPhysiology312, 81-96.

HAGBARTH, K.-E., WALLIN, G., BURKE, D. & LOFSTEDT, L. (1975). Effects of the Jendrassikmanoeuvre on muscle spindle activity in man. Journal ofNeurology, Neurosurgery and Psychiatry38, 1143-1153.

HAMMOND, P. H. (1955). Involuntary activity in biceps following the sudden application ofvelocity to the abducted forearm. Journal of Physiology 127, 23-25P.

HAMMOND, P. H. (1956). The influence of prior instruction to the subject on an apparentlyinvoluntary neuromuscular response. Journal of Physiology 132, 17-18P.

HAMMOND, P. H., MERTON, P. A. & SUTTON, G. G. (1956). Nervous gradation of muscularcontraction. British Medical Bulletin 12, 214-220.

HULTBORN, H. (1972). Convergence on interneurones in the reciprocal Ia inhibitory pathway tomotoneurones. Acta physiologica scandinavica 85, suppl. 375, 1-42.

ITO, M. (1984). The Cerebellum and Neural Control. New York: Raven Press.JOHANSSON, R. S. & WESTLING, G. (1984). Roles of glabrous skin receptors and sensorimotormemory in automatic control of precision grip when lifting rougher or more slippery objects.Experimental Brain Research 56, 550-564.

JOHANSSON, R. S. & WESTLING, G. (1987). Signals in tactile afferents from the fingers elicitingadaptive motor responses during precision grip. Experimenta Brain Research 66, 141-154.

LEE, R. G. & TATTON, W. G. (1975). Motor responses to sudden limb displacements in primateswith specific CNS lesions and in human patients with motor system disorders. Canadian Journalof Neurological Science 2, 285-293.

Loo, C. K. C. & MCCLOSKEY, D. I. (1985). Effects of prior instruction and anaesthesia on long-latency responses to stretch in the long flexor of the human thumb. Journal of Physiology 365,285-296.

MARSDEN, C. D., MERTON, P. A. & MORTON, H. B. (1972a). Servo action in human voluntarymovement. Nature 238, 140-143.

MARSDEN, C. D., MERTON, P. A. & MORTON, H. B. (1972b). Latency measurements compatiblewith a cortical pathway for the stretch reflex in man. Journal of Physiology 230, 58-59P.

MARSDEN, C. D., MERTON, P. A. & MORTON, H. B. (1976). Servo action in the human thumb.Journal of Physiology 257, 1-44.

MARSDEN, C. D., MERTON, P. A. & MORTON, H. B. (1977). The sensory mechanism of servo actionin human muscle. Journal of Physiology 265, 521-535.

MA1TTHEWS, P. B. C. (1964). Muscle spindles and their motor control. Physiological Reviews 44,219-288.

MATTHEWS, P. B. C. (1972). Mammalian Muscle Receptors and their Central Action8. London:Arnold.

MATTHEWS, P. B. C. (1984a). Evidence from the use of vibration that the human long-latencystretch reflex depends upon spindle secondary afferents. Journal of Physiology 348, 383-416.

MATTHEWS, P. B. C. (1984b). The contrasting stretch reflex responses of the long and short flexormuscles of the human thumb. Journal of Physiology 348, 545-558.

NASHNER, L. M. (1976). Adapting reflexes controlling the human posture. Experimental BrainResearch 26, 59-72.

NEWSON DAVIS, J. & SEARS, T. A. (1970). The proprioceptive reflex control of the intercostalmuscles and their voluntary activation. Journal of Physiology 209, 711-738.

PHILLIPS, C. G. (1969). Motor apparatus of the baboon's hand. Proceedings of the Royal Society B173, 141-174.

PROCHAZKA, A. & WAND, P. (1980). Tendon organ discharge during voluntary movements in cats.Journal of Physiology 303, 385-390.

ROTHWELL, J. C., DAY, B. L., BERARDELLI, A. & MARSDEN, C. D. (1986). Habituation andconditioning of the human long latency stretch reflex. Experimental Brain Research 63,197-204.

SALMONI, A. W., SCHMIDT, R. A. & WALTER, C. B. (1984). Knowledge of results and motorlearning: A review and critical reappraisal. Psychological Bulletin 95, 355-386.

94

HUMAN FUSIMOTOR SYSTEM 95

SNEDECOR, G. W. & COCHRAN, W. G. (1967). Statistical Methods, 6th edn. Ames, IA, U.S.A.: IowaState University Press.

TATTON, W. G., FORNER, S. D., GERSTEIN, G. L., CHAMBERS, W. W. & Liu, C. N. (1975). The effectof postcentral cortical lesions on motor responses to sudden upper limb displacements inmonkeys. Brain Research 96, 108-113.

VALLBO, A. B. (1972). Single unit recording from human peripheral nerves: muscle receptordischarge in resting muscles and during voluntary contractions. In Neurophysiology Studied inMan, ed. SOMJEN, G. G., pp. 283-297. Amsterdam: Excerpta Medica.

VALLBO, A. B. & HAGBARTH, K.-E. (1968). Activity from skin mechanoreceptors recordedpercutaneously in awake human subjects. Experimentl Neurology 21, 270-289.

VALLBO, A. B., HAGBARTH, K.-E., TOREBJORK, H. E. & WALLIN, B. G. (1979). Somatosensory,proprioceptive and sympathetic activity in human peripheral nerves. Physiological Reviews 59,919-957.

WIESENDANGER, M. & MILES, T. S. (1982). Ascending pathway of low threshold muscle afferentsto the cerebral cortex and its possible role in motor control. Physiological Reviews 62,1234-1270.

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