From the Institute of Physiology, University of Fribourg, stimulus, they

Journal of Physiology (1988), 397, pp. 371-388 371With 7 text-figuresPrinted in Great Britain

ORIGIN OF THE SPECIFIC H REFLEX FACILITATION PRECEDINGA VOLUNTARY MOVEMENT IN MAN

BY ROGER RIEDO AND DIETER G. RUEGGFrom the Institute of Physiology, University of Fribourg,

CH-1700 Fribourg, Switzerland

(Received 28 January 1987)

SUMMARY

1. In a reaction time situation, the monosynaptic spinal reflex (H reflex) isfacilitated before the onset of an electromyographic (EMG) response. The aim of thepresent investigation was to test if the facilitation can be attributed either to asubliminal depolarization of motoneurones or to an increase of the excitatory effectof the afferent volley reaching the motoneurones.

2. At the onset of an acoustic warning signal, human subjects were required toconcentrate on a reaction time task and, in addition, to initiate a steady isometricplantar flexion of medium intensity in both feet. In response to a following visualstimulus, they carried out a ballistic plantar flexion randomly with the right or leftfoot. At different times after the visual reaction signal, H reflexes were elicitedbilaterally.

3. The facilitation of the H reflex was similar in the presence and absence of asteady activation. In addition, the facilitations were similar in absolute amplitudeand duration when the stimuli evoking the H reflexes were at threshold intensities,or at an intensity which produced control H reflexes of 60% maximum amplitude.

4. In a second series of experiments, no H reflexes were elicited but the strengthof the steady plantar flexion was varied. Premotor time, i.e. the interval between theonset of the visual stimulus and the EMG response, and reaction time, i.e. theinterval between the onset of the visual stimulus and the mechanical response, werecomputed. Neither parameter depended significantly on the intensity of steadyflexion and they were the same with steady flexion as without.

5. The rectified EMG records and the torque records were aligned by the end ofpremotor time. Three-dimensional displays of average activity as a function of timeand steady activation level were computed. No activation before premotor andreaction time was detected which could have been related to the H reflex facilitation.

6. The present results suggest that all motoneurones, in particular those beingactivated during the voluntary contraction, can contribute to the H reflex facilitationbefore movement onset and that the basis of this facilitation is an enhancedexcitatory effect of the afferent volley elicited by the H reflex stimulus. Mechanismsleading to the facilitation could be removal of presynaptic inhibition at I a terminalsor facilitation of interneurones intercalated in polysynaptic components of the reflexpathways.

R. RIEDO AND D. C. RUEGG

INTRODUCTION

Conditioned plantar flexions of the foot can be used in man to examine informationprocessing by the nervous system during reaction time (RT) since modulations of themonosynaptic reflex (H reflex) can be investigated in relation to movementparameters. H reflexes are facilitated specifically about 100 ms before the onset ofthe voluntary EMG response in the same muscle (Coquery & Coulmance, 1971;Pierrot-Deseilligny, Lacert & Cathala, 1971; Kots, 1977). This facilitation is not onlyevident in a simple task but also in a choice RT task in which the subject does notknow before the 'go' signal which limb he will have to move (Eichenberger & Riiegg,1983, 1984). It was concluded from these results that the decision as to which limbhas to be moved was already taken at the onset of the facilitation of the H reflex.Although the pathway by which the H reflex is mediated is simple there are several

spinal mechanisms which could account for the facilitation. (1) A subthresholddepolarization of a-motoneurones before movement onset is indicated by the longfiring latencies of motoneurones to electrical stimulation of the motor cortex (Porter& Muir, 1971). (2) There are supraspinal effects on I a and Ib inhibitory interneuronesbefore movement initiation (Tanaka, 1974, 1976; Fournier, Katz & Pierrot-Deseilligny, 1983). (3) The synapses of Ia afferents with motoneurones are underpresynaptic control (Lundberg & Vyklicky, 1963; Hongo, Jankowska & Lundberg,1972; Rudomin, Jimenez, Solodkin & Duenas, 1983). (4) An activation ofinterneurones intercalated in polysynaptic reflex components (Watt, Stauffer,Taylor, Reinking & Stuart, 1976; Burke, Gandevia & McKeon, 1984) can modulatethe H reflex.

Since all the above-mentioned studies were performed with initially relaxedmuscles these mechanisms can be assigned either to a subliminal depolarization ofa-motoneurones or an increase of the excitatory effect of the afferent volley on themotoneuronal membrane. The first alternative can be tested by comparing theperformance of subjects who superimpose a conditioned voluntary movement on arelaxed or on a steadily active muscle. If the H reflex facilitation in a relaxed muscleoriginates from a subliminal depolarization of motoneurones a decrease ofRT shouldbe observed in an initially active muscle. Motoneurones at firing threshold may startfiring and already active motoneurones may increase firing frequency. If noshortening of RT can be detected, then a slight supplementary activation of themotoneuronal pool of an initially active muscle may be detected with EMGaveraging techniques. The aim of the present investigation was to test the firsthypothesis in detail by studying the following: (1) pre-movement H reflex facilitationwith and without steady background activation, (2) dependence ofRT on the steadyactivation level, (3) presence ofa slight activation of motoneurones before movementonset. A preliminary account of some of the results has already been presented(Riedo & Riiegg, 1984).

METHODSSubjects and materialThe experiments were performed on six male and two female subjects (19-25 years old), with the

consent and understanding of each of them. The experimental set-up was described in detail in anearlier paper (Eichenberger & Riuegg, 1984). The subjects were sitting in a modified car chair, the

372

ORIGIN OF PRE-MOVEMENT H REFLEX FACILITATION

knee joint at an angle of 120 deg, and the ankle at an angle of 90 deg. The feet were resting on plateswhich were suspended on an axis which coincided with the axis of the ankle. The torque of isometricmovements was recorded with strain gauges mounted on the plates. The EMG was recorded on eachleg with two surface electrodes 3 cm apart, the proximal one 5 cm distal to the insertion of thegastrocnemius muscle. H reflexes were elicited with a modified Simon electrode (Simon, 1962)positioned in the popliteal fossa above the tibial nerve. The subject performed a steady plantarflexion of both feet when an acoustic signal (frequency: 1 kHz, duration: 200 ms, intensity: 60 dB)was given. The reaction signal for a ballistic plantar flexion of the right and left foot were two light-emitting diodes of 4 mcd, 5 cm apart, and at 1 m distance.The original experimental data were low-pass filtered (cut-off frequency 1 kHz) and fed into an

A/D converter (sampling frequency 3 kHz) of an HP-21MX computer system. The following signalswere recorded: (1) light and H reflex stimulus, (2) torque signal of the right foot, (3) torque signalof the left foot, (4) EMG of the right side, and (5) EMG of the left side.

Experimental procedureIn all experimental sessions, the subjects performed plantar flexions of a foot in a choice RT

situation. The subject flexed the right foot as fast as possible at the onset of the right diode, theleft foot at the onset of the left diode.

In the first series of experiments, a trial was initiated by an H reflex stimulus delivered to bothlegs. The stimulus duration was 1 ms and the strengths we used were threshold of a control reflexand 60% of its maximal value (4-8 mA). (The intensities were not changed from trial to trial butfrom session to session since the equipment did not allow quick switching from one intensity to theother.) Seven seconds after these control H reflexes, the warning signal was given at which thesubjects prepared themselves for the RT task and, depending on the previously given instructions,did or did not initiate a steady plantar flexion of medium size (randomized sequence). The go signalwas switched on 1 s after the warning signal. Test stimuli to evoke H reflexes were applied to bothlegs at different times after the onset of the go signal. The intervals between light onset and teststimuli covered in 40 ms steps a range between 40 and about 320 ms depending on the RTs theparticular subject was producing. They were arranged in a pseudorandom sequence and some trialswith no test H reflexes were intermingled. Two sessions were performed in a sequence withrandomly chosen stimulation intensities.

In the second experimental series, the subjects were instructed to initiate steady plantar flexionsof both feet at the onset of the acoustic warning signal. Four different levels of strength weredistinguished: (1) no, (2) small, (3) medium, and (4) strong activation. In a first session, the subjectswere instructed about the desired absolute strength of steady movements at each level. In thefollowing sessions, no feed-back about the torque was given except when torques deviatedconsistently from the levels specified at the beginning. The variability of the torques produced ateach level was large so that a continuous distribution of strengths was obtained from no activationat level 1 until the maximum activation at level 4. The largest torques recorded corresponded toabout 10 % of the maximal force the subject could maintain. One second after the wariing signal,the light stimulus which initiated the RT task was turned on. The recordings obtained from sucha trial are shown in Fig. 1. The torque levels each subject had to maintain occurred equallyfrequently and they were arranged pseudorandomly within a session. In both series, each sessionconsisted of about fifty trials. The intervals between trials were about 10 s.

Analysi8 of dataThe size of control and test H reflexes was computed on-line by the computer as the difference

between the maximum and minimum value of the EMG within a time window extending fromabout 25 to 50 ms after stimulus onset depending on the reflex latency of the subject. The valueswere displayed to the experimenter which facilitated the control of the stability of stimulationparameters. Computed amplitudes were contaminated by errors during steady contractions sinceH reflexes were superimposed on the steady EMG activity. By computing amplitudes with piecesofEMG recordings of steady motor discharge but without H reflexes, we verified that the error wasin the order of 1% of the maximum control H reflex. Such an amplitude was far below thephysiological variability of the reflexes and was thus neglected.Torque and EMG signals were recorded for 1 s starting 200 ms before the go stimulus. The steady

activation was calculated as the difference between the mean torque level during the initial

373

374 R. RIEDO AND D. G. RUEGG

200 ms and the level with no muscle activation, which was recorded at the beginning and end ofeach session. Since the size ofEMG recordings was affected by electrode contact, skin resistance andother factors, recordings from different sessions were standardized. The method chosen utilized thelinear relation between the size of the rectified EMG and torque of isometric movements (Lippold,1952; Milner-Brown & Stein, 1975). The slope of the regression line of representative sessions wasabout 10-6 V/N m which was taken for standardizing purposes. A calibration factor with whichEMG records were multiplied was computed for each session. It gave the best fit between the givenregression line and the points defined by torque and standardized EMG values during the steadycontraction.

200ms 5 N mm400,pV RT/

A

Torque ___________

B ~~~~~left8

D

Warning Reactionsignal signal

Fig. 1. Plantar flexion of the right foot in an RT situation. The subject was instructed toperform a steady contraction in both legs at the onset of the warning signal. A, torquerecording from the right side. Reaction time (RT) is defined as the interval between onsetof the light stimulus and the onset of the mechanical response. B, torque recording fromthe left side. C, EMG recording from the right soleus muscle. Premotor time (PMT) isdefined as the interval between onset of the light stimulus and the onset of the EMGresponse. D, EMG recording of the left soleus muscle. Abscissa: time (200 ms). Ordinate:5 N m (A and B), 400,uV (C and D).

The latency of the voluntary response was estimated by the premotor time (PMT), i.e. theinterval between the onset of the light and the EMG response, and by the reaction time (RT), i.e.the interval between onset of the light and the mechanical response. Two independent techniqueswere used to compute the two parameters since their dependence on the steady activation level wasa crucial part of the experimental results. PMT was measured visually with a cursor on a graphicsterminal on which the rectified EMG signal was displayed without the concomitant torquerecording. The estimation was unequivocal at zero steady activation level but proved more difficultthe higher the background EMG. The RT was determined by a computer algorithm with no humaninteraction (Riiegg & Eichenberger, 1983; Eichenberger & Riiegg, 1984). The distribution of thedifferences between RT and PMT were computed for each subject. Trials within the tail ends of thedistribution (5% on each side) were excluded from further processing. A regression line wascomputed through the remaining points. The correlation coefficient varied between 0-89 and 0 93for the second series of experiments. The relation is given for one of the subjects in Fig. 2.The maximum control H reflex which could be elicited by an optimal electrical stimulus was

determined for each session. Test H reflexes were normalized in relation to this value and expressed


as a percentage. This normalization allowed us to pool data from different sessions andsubjects.The torque records from the second series of experiments during which no H reflexes were elicited

covered all steady torque levels. The data of all trials were pooled in order to obtain a three-dimensional display of the time course of torque changes as a function of the steady activation. The

500

450-

400

-, 350

H 300 *..

250 -

200

150

10ico XIII " I,, 1 I,I, I, I

100 150 200 250 300 350 400 450 500PMT (ms)

Fig. 2. Relation between RT and PMT in one subject. If the difference between RT andPMT happened to be in one of the tail ends (5% on each side) of the distribution of thesedifferences, the corresponding trial was discarded. Slope of the regression line: 1-02;intercept: 54 ms; regression coefficient: 0-93.

sections within a time window extending from T1 (200 ms before RT) till T2 (40 ms after RT) werealigned by PMT. Average torque levels Xi(m) were computed over the interval m-At/2 tom+At/2 for each of the trials i (i = 1, 2, 3, ... N) where m represents time (m = Tl, T1+ At,T1 + 2At, ... T2). Each trial was performed at a steady activation Zi. The values Xi(m, Zi) (i=1, 2, 3, ... N) define a relation between the background torque level and the average torque at timem. A smooth curve to describe this relation was estimated with a modified version of the techniquepublished in Eichenberger & Riiegg (1984). A point Y(m, n), where n represents the backgroundtorque level in multiples of the torque interval z, was computed by convolution of the data pointsXi(m, Zi) with a Gaussian weighting function W.

E Xi(m,Zi)W(n-Zi)Y(m, n) = n

E W(n-Zi)i=l

where W(j) = exp-(r/jAZ)2.

The following numerical values have been chosen: At = 20 ms, AZ = 0 5 N m, and T = 1 N m.Contour lines were computed with the two-dimensional array Y(m, n) of samples of the surface(Snyder, 1978) and they were then plotted in a three-dimensional co-ordinate system with the axestime, steady torque level and torque. Analogue computations were carried out with the rectifiedEMG signals. The trials were aligned by PMT. The chosen values of At, AZ and r were the same aswith the torque signals.

375

376 R. RIEDO AND D. G. RUEG/G

RESULTS

H reflex facilitation before voluntary movements which are superimposed on a steadyactivation of the involved muscle

In previous experiments on H reflex facilitation, the soleus muscle was relaxed andno EMG activity was evident before the subjects initiated the conditioned movement(Eichenberger & Riiegg, 1983, 1984). If we assume that, under these conditions, allmotor units were below firing level (Burke, 1986), the hypothesis can be put forward

300 - A - B'

250 - -

20050 -

C100

0

E

E~ 0xEo 300 C D

250

CL

200

150

-200 -150 -100 -50 0 -200 -150 -100 -50 0Time (ms)

Fig. 3. H reflex facilitation in one subject. It was obtained with electrical stimuli whichevoked control reflexes of 60% of their maximum value (A and B) and with electricalstimuli which were threshold for control reflexes (C and D). The subjects were relaxedbefore movement onset (A and C) or maintained a steady flexion force (B and D). Barsindicate confidence limits (P = 0 05). Abscissa: time before movement onset (end of RT)in milliseconds. Ordinate: size of the H reflex in percentage of the maximum control reflexwhich could be elicited.

that the H reflex facilitation reflected a subthreshold depolarization of motoneuronesand that the movement was initiated when the first unit reached firing threshold. Inorder to test this hypothesis, we examined in a first step whether a pre-movementH reflex facilitation was also evident if the visually conditioned contraction wassuperimposed on a steady flexion force. These experiments were performed withelectrical stimuli which evoked control H reflexes of about 60% of their maximalvalue (value recommended as standard, Hugon, 1973) and with stimuli which werejust threshold for control reflexes.The subjects carried out trials in which they concentrated on the RT task at the

onset of the warning signal, and trials in which they performed, in addition, a plantar


flexion of medium intensity. Since they did not have any feed-back of the steadytorque level its variability was large. After the warning signal a light turned on at theonset of which they performed as fast as possible a plantar flexion either on the rightor left side depending on whether the right or left light was turned on. The recordingsof a typical trial are shown in Fig. 1. Each trial provided a test reflex to establishthe pre-novement H reflex facilitation.The facilitatory phase obtained without prior steady activation and with control

H reflexes of about 60 % of their maximum value (Fig. 3 A) confirmed previousresults (Eichenberger & Riiegg, 1984). It started about 100 ms before movementonset and reached about twice the size of the maximum control H reflex by whichreflexes were normalized. Values larger than 100% can reasonably be expected sincethe maximum H reflex corresponds in an average subject to about half the size of themaximum M response (Hugon, 1973). The facilitatory phase was alike when thesubject performed a background plantar flexion of 3-9 N m (Fig. 3B). The relationsproved to be similar if these reflexes were plotted in relation to the onset of the EMGresponse (end of PMT) or the mechanical response (end of RT, Fig. 3). Although thisresemblance is not documented here, we felt the double computation to be necessarybecause EMG and torque signals were contaminated by the reflex responses whichrendered the determination of PMT and RT difficult (see Methods).The same experiments were repeated with electrical stimuli at threshold intensity

for control H reflexes. Without background contraction, test reflexes earlier than100 ms before movement onset were as expected close to 0 and the facilitation whichstarted 100 ms before movement onset was similar to that with strong electricalstimuli and reached values of about 150 % close to movement onset (Fig. 3 C). Thefacilitary phase did not undergo a modification in duration but it was reduced inamplitude if the subject maintained a steady contraction during the warning period(Fig. 3D). The diminution was present in all subjects and was about 50% averagedacross subjects. To a lesser extent (10% averaged across subjects) it was also foundwith strong electrical stimulation (cf. Fig. 3A and B). This result was surprising sincean increase, rather than a reduction, had been expected from previous results ofGottlieb & Agarwal (1971). However, the amplitudes of the H reflexes during thewarning period before the onset of the facilitation (Fig. 3) were in line with thesefindings. The reflexes were similar in size whether the muscles were relaxed orsteadily contracted. They were only slightly larger with threshold stimuli. Thediscrepancy between our results and those of Gottlieb & Agarwal (1971) induced usto study whether differences of the motor task modulate the relation between H re-flexes and background activity (R. Krauer & D. G. Riiegg, in preparation). H reflexeswere elicited in the same subjects during force tracking as did Gottlieb & Agarwal(1971) and during the warning period of an RT task as described above. The relationbetween H reflex and motor activity was essentially identical in both situations.Inter-individual differences proved to be much larger than task-related influences. Inmost subjects, there was a slight inhibition (about 10%) with increasing motoractivity, in one subject, there was a slight facilitation and in another subject therewas a strong inhibition. We were thus not able to reproduce the results of Gottlieb& Agarwal (1971).

These findings and additional results with other stimulation strengths (not shown

377

R. RIEDO AND D. G. RUEGG

here) indicated that the duration and absolute amplitude of the facilitary phasebefore movement onset was relatively insensitive to the pre-existing level of motordischarge except when saturation of H reflexes occurred with high stimulationintensities. If we take for granted that an orderly recruitment of motor units wasrespected for the H reflex it can be concluded that small as well as large motor unitswere facilitated.

Dependence of reaction time and premotor time on background activation levelThe conception for the following experiments rests mainly on the conclusions from

the above experiments. A similar facilitation was recorded with weak and strongelectrical stimulation. According to the size principle, different motor units give riseto the facilitary phase in the different conditions. Therefore, it was concluded thatall motor units are facilitated before movement initiation. Furthermore, we have torely upon the evidence which will be presented in the Discussion that motor units ofa muscle are recruited in the same order whether they are activated (1) during themaintenance of a steady flexion force, (2) during the performance of a ballisticmovement, or (3) by electrical stimulation of muscle afferents.

If subjects, as described above, maintain a background motor discharge in theinvolved muscle before the conditioned movement some motoneurones are at acritical firing level. If a postsynaptic facilitation is assumed these motoneuronesshould start discharging during the facilitation (which was subliminal with relaxedmuscles) and the motoneurones already active should increase their firing frequency.This motoneuronal activation should be recorded on the EMG and, consequently, thepremotor time (PMT), i.e. the interval between the onset of the visual stimulus andthe EMG response, and reaction time (RT), i.e. the interval between the onset of thevisual stimulus and the mechanical response, might shorten.The subjects were verbally instructed to maintain flexions of four different levels

(from none to strong) at the onset of a warning signal. Since they did not have visualfeed-back on their performance and since the contractions were isometric, thevariability at each level was large and the distribution of steady torques becamecontinuous. A visually conditioned ballistic contraction was superimposed on thebackground contraction. Latencies on the right and left side were alike and they wereaveraged across sides. Figure 4 A and B shows graphically the relation betweensteady torque and PMT and the relation between steady torque and RT. Bothparameters varied slightly with the torque level but none of the modulations wassignificant (limits: confidence intervals for P = 005). Since the relations were similarin all subjects and the variance of latencies within one subject was large comparedto the inter-individual variance, data from all subjects were pooled (Fig. 4C and D),although mean latencies achieved by the individual subjects were different (up to54 ms). At weak steady flexions, PMT and RT tended to increase, at flexions ofintermediate strength to decrease again to values obtained with a relaxed muscle,and, at strong flexions, they tended to increase again. All these variations were muchsmaller than the duration of the H reflex facilitation and, furthermore, RTs or PMTsshorter than with a relaxed muscle were not found at any activation level. Hence,these results point to an origin of the H reflex facilitation which is not based on adirect subthreshold motoneuronal depolarization with initially relaxed muscles.

378

50145

40E 35EF 30

2520

151c


01 A -010

100 rTa T L

io

)o

I I . . I . I . I I I I . I I . I I I

0 2 4 6 8

Torque (N m)

10 -2

D

.I - . .. .I . .. . .I

0 2 4 6 8 10Torque (N m)

Fig. 4. PMT and RT as a function of the steady activation. A, PMTs from one subject.B, RTs from same subject. C, pooled PMTs from four subjects. D, pooled RTs from foursubjects. Bars indicate confidence limits (P = 005). The confidence limits are not muchsmaller in C and D than in A and B since there were inter-individual differences of meanlatencies. Abscissa: steady activity in N m. Ordinate: PMT in milliseconds (A and B), RTin milliseconds (C and D).

&L

Ut

w-

20

10

0

0 "N-200

Fig. 5. EMG activity as a function of time and steady activation. Data from one subject.Time zero corresponds to the onset of the EMG burst (end of PMT) which gives rise to theballistic contraction. The amplitude of the burst is independent of the steady activation.X-axis: time in milliseconds (reference: end of PMT); Y-axis: EMG activity of the soleusmuscle in microvolts; Z-axis; steady contraction in N m.

379

+1+-

C

l-

cr

500450400350300250200150100

-2

380 R. RIEDO AND D. G. RUEGG

EMG and torque levels before premotor time and reaction timeAlthough PMT and RT did not decrease if the visually conditioned movement was

superimposed on a steady activation of the involved muscle, the primary cause of theH reflex facilitation could have been a direct activation of motoneurones if this was

0

>1-

Fig. 6. EMG activity as a function of time and steady activation. Time zero correspondsto the onset of the EMG burst (end of PMT). Mean steady EMG has been subtracted whichmade it possible to amplify the EMG 50 times more than in Fig. 5. There is no indicationof an enhanced EMG activity before movement onset in parallel with the pre-movementH reflex facilitation. X-, Y- and Z-axes, see Fig. 5.

too weak to be detected by PMT or RT determination, which was based onrecordings of individual trials. Small modulations on individual EMG recordingswere difficult to identify due to the discontinuous nature of EMG recordings.The rectified EMG recordings of all trials were aligned by the corresponding PMT

and time was divided in intervals of 20 ms. For each interval, the average EMGactivity was computed in each trial and the relation between average EMG activityand steady torque level (which was different for each trial) was approximated by asmooth curve. The set of curves obtained from one subject is plotted three-dimensionally in Fig. 5. The linear relation between torque and EMG during thesteady contraction (from 200 to 0 ms before PMT) confirms earlier observations byLippold (1952) of the linearity between EMG and torque. The conditionedsuperimposed movement was ballistic and of similar size at all torque levels. In orderto investigate small modulations of the EMG before PMT, the steady activationduring each trial was estimated by the mean EMG activity during the 200 ms beforelight onset and it was subtracted from the corresponding rectified EMG record. Thethree-dimensional relation between EMG, time and steady torque was computedagain on the basis of these data. Contour lines were determined which enable an easyvisual detection of EMG increases. Since steady EMG levels were subtracted theEMG could be plotted with higher resolution without overflow (Fig. 6). The noise


level before EMG onset (PMT) increased with the steady torque level since motorunit potentials also increased in amplitude with force (Milner-Brown & Stein, 1975).Although the scale on the y-axis was expanded by a factor of 50 from Fig. 5 to Fig. 6there was no indication that EMG activity was enhanced before PMT in parallel to

2-

z

0

0~~~~~~~~~~~~~~

el? 0

V -150 -0Fig. 7. Foot torque as a function of time and steady activation. Time zero corresponds tothe onset of the EMG burst (end of PMT). Mean steady torque has been subtracted. Asin Fig. 5, there is no indication of torque increase before movement onset which mightexplain the origin of the pre-movement H reflex facilitation. Y-axis: torque in N m;X- and Z-axes, see Fig. 5.

the H reflex facilitation (Eichenberger & Riiegg, 1984; see also next section). In orderto confirm these results, the same computations were carried out with the torquerecordings aligned by PMT. Similarly, there was no increase in torque before PMTat all steady torque levels (Fig. 7). The results from all subjects agreed on this point.Both the absence of a shortening of PMT and RT and the absence of even smallincreases of EMG activity and of torque before PMT support the hypothesis that afacilitation or disinhibition within the reflex pathway leads to the H reflexfacilitation before movement initiation.

DISCUSSION

Regulation of the H reflex gainWe assume that the H reflex facilitation resulted from changes in intrinsic spinal

mechanisms which are limited in number by the simplicity of the spinal reflex underinvestigation. All the mechanisms were attributed to two alternatives. The objectiveof the present investigation was to decide between the two.The first alternative includes all mechanisms which, before movement onset and

with initially flaccid muscles, move the motoneurones closer to critical firing level.H reflexes elicited during this period are then facilitated since their size depends on theactivity of the motoneurones (Hagbarth, 1962; Mayer & Mawdsley, 1965; Paillard,

381


1955), the sensibility being largest at small activity levels (Gottlieb & Agarwal,1971). Electrical stimulation experiments on anaesthetized monkeys favour this firstalternative (Porter & Muir, 1971). Latencies of EMG responses could be as long as65 ms if the motor cortex was stimulated with patterns which resemble the naturalfiring behaviour of a representative pyramidal tract unit during a voluntarymovement. This activity impinges on the motoneurones within a few milliseconds infew of the fast-conducting corticospinal fibres (Porter & Hore, 1969; Fetz & Cheney,1980). Therefore subthreshold summation occurs during the main portion of thelatency. This corresponds to the time when H reflexes would be facilitated. Besidesa direct activation by corticomotoneuronal connections, an indirect excitatory effectis possible via Ia interneurones (Tanaka, 1974, 1976), lb interneurones (Fournieret al. 1983) which are activated before movement initiation, and muscle spindleafferents the discharge of which can be altered by fusimotor activation duringmovement (Vallbo, 1971; Hagbarth, Wallin & Lofstedt, 1975).The second alternative contains mechanisms that modulate the excitatory effect

of a Ia volley on the motoneuronal pool. The site of action could be removal ofpresynaptic inhibition at Ia terminals. Stimulation of the bulbar reticular formation(Lundberg & Vyklicky, 1966; Rudomin et al. 1983), the red nucleus (Hongo et al.1972; Rudomin et al. 1983), the dorsolateral funiculus (Rudomin et al. 1983) and themotor cortex (Lundberg & Vyklicky, 1963) reduce presynaptic inhibition evoked byI a stimulation. A further possible mechanism is based on the recent finding that theH reflex is not only monosynaptic but also contains polysynaptic components (Burkeet al. 1984), an activation of which would enhance the reflex amplitude. This secondalternative conforms with the finding that H reflexes are depressed by presynapticinhibition of autogenic spindle afferents immediately after muscle relaxation(Schieppati & Crenna, 1984, 1985).

Activation of the soleus muscle during steady, ballistic and reflex contractionsIn order to draw conclusions from the experimental results, it is of importance to

know if the soleus muscle was activated during steady, ballistic, and reflexcontractions or if, as in cats, it was not active during some ballistic movements(Smith, Betts, Edgerton & Zernickle, 1980). It can safely be expected that the soleusmuscle is active in the H reflex. The question arises whether the EMG activity whichwas recorded during steady and ballistic contractions was from the soleus muscle orfrom the gastrocnemius muscle by crosstalk. In some additional experiments duringwhich the activity of both muscles was recorded, the amplitude of the EMG of thegastrocnemius proved to be smaller than that of the soleus muscle in all testedsubjects. This result was expected since the knee joint was at an angle of about90 deg which was small enough to relax the gastrocnemius muscle. Further supportthat the soleus muscle was activated during steady and ballistic contractions wasprovided by the position of the recording electrodes. The soleus electrodes were about5 cm away from the heads of the gastrocnemius muscle. Taking into account that theskin was about 1 cm thick and the amplitude of the EMG decreases between the firstand second power of the distance between source and electrodes (Milner-Brown &Stein, 1975), a participation of the soleus muscle in steady and ballistic contractionscan reasonably be expected. The important conclusion, on which the interpretation

382


of the results is based, is that the soleus muscle was activated during steady, ballistic,as well as during reflex plantar flexions of the foot.

Motor unit recruitment during different types of contractionThe size principle ofHenneman postulates a relationship between the motoneurone

size, the axon conduction velocity and size of the associated motor unit and statesthat motor units are recruited in order of increasing size (Henneman, Somjen &Carpenter, 1965 a, b; Henneman, 1974). It can reasonably be expected that the sizeprinciple based on recording from ventral root filaments during various reflexes inthe decerebrate cat (Henneman et al. 1965 a) can be extended to H reflexes which areelicited mainly by activation of the muscle's own afferents.The technique of spike-triggered averaging of the force output of the whole muscle

in order to characterize motor units (Stein, French, Mannard & Yemm, 1972)initiated studies of the size principle in man. During voluntary slow rampmovements, there is a good correlation (correlation coefficient 08-0-9) betweentwitch force and the force at which motor units are recruited during voluntary rampmovements (Milner-Brown, Stein & Yemm, 1973). In ballistic movements, the forcelevel at which the motor units are recruited drops but the order of recruitment staysthe same as in slow movements (Desmedt & Godaux, 1977 a, b). The size principle ofHenneman is thus valid for reflex, slow and ballistic contractions. Further supportis provided by Ashworth, Grimby & Kugelberg (1967) who recorded simultanouslyfrom several motor units of the anterior tibial muscle during voluntary and reflexcontractions in man. The recruitment order was the same in 70% of the recordings;recruitment inversion occurred only when the difference of threshold between theunits was small.A further point to clarify is whether the normal recruitment order was respected

when H reflexes were facilitated shortly before movement onset. A partial reversalcan be found in animal preparations or pathological situations: in anaesthetized catsby electrical stimulation of the red nucleus (Burke, Jankowska & ten Bruggencate,1970), in decerebrate cats by electrical and natural stimulation of the sural nerve(Kanda, Burke & Walmsley, 1977) and stimulation of dorsal root filaments(Clamann, Ngai, Kukulka & Goldberg, 1983) and in man by ischaemic or lidocaineblockade of proprioceptive afferent activity (Grimby & Hannerz, 1976) and byelectrical stimulation of digital nerves during ramp contractions (Garnett &Stephens, 1981). There is no evidence for a reversal of the recruitment order inphysiological conditions. Therefore, a normal recruitment order during thefacilitation is assumed. On this basis we have tested which motor units weresubjected to facilitatory effects: either all, including those which were recruitedduring the visually conditioned contraction, or mainly motor units which wererecruited by large test H reflexes as used for all earlier studies (Pierrot-Deseillignyet al. 1971; Eichenberger & Riiegg, 1984). We have demonstrated an H reflexfacilitation with electrical stimuli which were threshold for control reflexes and whichwere 60% of the maximum control H reflex. This suggests that the motor units withthe lowest threshold also received a facilitatory input which is an important aspectsince, during plantar flexions which were at the most 10 % of the maximum muscleforce, these low-threshold motor units were activated.

383


An unexpected result was that the facilitation of the H reflex did not increase withthe background activity as it did in previous studies (Gottlieb & Agarwal, 1971). As Hreflexes before the onset of the facilitation also did not show the awaited relation westudied the influence of the behavioural context on H reflexes during maintained con-tractions (R. Krauer & D. G. Riuegg, in preparation). We were not able to reproducethe results of Gottlieb & Agarwal (1971). A difference in performance of the subjectsmight explain the discrepancy between the relations which was most pronounced atsmall contraction levels. If the subjects tested by Gottlieb & Agarwal (1971) co-contracted soleus and tibialis muscles at small contraction levels in order to stabilizethe foot, H reflexes might have been reduced in size by reciprocal inhibition.

In conclusion, the further discussion of the present experimental results can bebased on the assumption that motor units in the soleus muscle are recruitedaccording to the size principle during reflex, ballistic and steady contractions andthat the same motor units which were activated during the ballistic contraction werefacilitated beforehand.

Spinal mechanisms giving rise to the H reflex facilitationRelying on the considerations outlined above, a direct facilitation of motor units

before movement initiation can be detected on the EMG if there is a pre-existing levelof motor discharge. Motoneurones already active may modulate their activity andmotoneurones close to critical firing level may start to discharge. In an initially silentmuscle, however, all motor units are below firing level (Burke, 1986) and excitabilitychanges are too small to raise any motor units above firing threshold. Theobservation that PMT and RT of the visually conditioned movement which wassuperimposed on a steady activation were not shortened provides an indication thatthe H reflex facilitation did not originate from a direct activation of motoneurones.The small non-significant changes in latency, which were much shorter than theduration of the H reflex facilitation, can be attributed to other factors. The subjectstended to produce more and more steady contractions of similar size (about 7 N m)when they were instructed to perform weak, medium and strong contractions. Theyhad to be admonished from time to time to perform really weak and really strongcontractions. This indicates that it was easiest for them to perform contractions ofmedium size and that weak and strong plantar flexions require more concentration.This might account for the small increase in latency at weak and strongcontractions.Our results do not agree with those of Sanders (1980) who observed a shortening

of RT by some 50 ms if the muscle was tonically activated before the reaction signal.We explain the different results by the different instructions given to the subjects.Sanders (1980) instructed the subjects to contract the muscles optimally to achieveshort RTs. We instructed them, however, to contract the muscle at different degreesand to react as fast as possible at all levels. In a similar paradigm as ours, anincreased EMG before movement was not concomitant with shorter RTs (Haagh &Brunia, 1985).The uniformity of latencies does not exclude a direct motoneuronal activation

leading to the H reflex facilitation since it might have been too small to be detectedon individual EMG or torque recordings. However, this possibility could be excluded

384


by the finding that averaging of the EMG and torque recordings in reference to PMTdid not reveal any pre-movement activation occurring in parallel with the H reflexfacilitation.The findings support the concept that a removal of presynaptic inhibition at Ia

terminals or an activation of polysynaptic components of the reflex pathway lead tothe H reflex facilitation. Further support is provided by findings of Eichenberger &Riiegg (1984): (1) The amplitude of the H reflex facilitation decreases with RT. If onehypothesizes that the facilitation is a subthreshold excitation of motoneurones itsamplitude is expected to be always the same at movement onset. (2) The slope of thefacilitation is positively correlated with RT, but the following movement isindependent of it. Assuming the same hypothesis, we expect parallel changes of theslope of the facilitation and of the slope of the movement. Concordant with theseresults are findings by Schieppati & Crenna (1985) about voluntary muscle releasefrom a constant level of flexion force. During and after the release, the H reflex wasdepressed compared to control values at rest. Recurrent and postsynaptic inhibitionsdid not play a major role but presynaptic inhibition as mechanism for the reflexreduction was supported.

Supraspinal origin of the H reflex facilitationThe activation pattern of neurones during RT tasks has been studied in several

supraspinal structures. Neurones in the motor cortex start discharging 50-150 msbefore movement initiation in monkeys which performed conditioned arm move-ments (Evarts, 1966, 1974; Lamarre, Spidalieri & Lund, 1981) or jaw movements(Luschei, Garthwaite & Armstrong, 1971). Similar latencies were also observed in thecerebellum (Tach, 1975), but divergent temporal correlations of unit activity in thered nucleus and motor cortex have been reported. Otero (1976) required monkeys tolift their arm, position the hand and push a button. Since cortical activity precededred nucleus unit activity in this task, Otero (1976) concluded that movements areinitiated by the motor cortex and not the red nucleus. Other authors requiringsimpler movements found in RT tasks (Ghez & Kubota, 1977) and spontaneouslyinitiated arm movements (Cheney, 1980; Kohlerman, Gibson & Houk, 1982) unitdischarges which preceded movements by 50-150 ms suggesting a role for the rednucleus in movement initiation. A cortical origin is favoured by the finding that theH reflex facilitation disappears after lesion of the pyramidal tract of dogs which wereconditioned to perform an instrumental avoidance reflex (loffe, 1973).

Additional information about the supraspinal origin of the H reflex facilitation isavailable from experiments with anaesthetized cats in which presynaptic inhibitionis reduced by electrical stimulation of supraspinal structures. Stimulation of themotor cortex (Lundberg & Vyklicky, 1963), the pyramidal tract (Hongo et al. 1972;Rudomin et al. 1983) and the bulbar reticular formation (Lundberg & Vyklicky,1966; Rudomin et al. 1983) inhibits transmission in the pathway mediatingdepolarization of I a terminals from I a afferents.

The study was supported by the Swiss National Science Foundation (grant No. 3 026.84). Wewish to express our gratitude to Dr B. Hyland for reading the manuscript and to Dr R. Krauer forparticipating in some of the experiments. The skilful technical assistance of Ms S. Rossier and MrP. Hiibscher is gratefully acknowledged.

385

13 PHY 397


REFERENCES

ASHWORTH, B., GRIMBY, L. & KUGELBERG, E. (1967). Comparison of voluntary and reflexactivation of motor units. Journal of Neurology, Neurosurgery and Psychiatry 30, 91-98.

BURKE, D. (1986). The contribution of spindle afferents to altered states of muscle tone.Proceedings of the International Union of Physiological Sciences 16, 253.

BURKE, D., GANDEVIA, S. C. & McKEoN, B. (1984). Monosynaptic and oligosynaptic contributionsto human ankle jerk and H-reflex. Journal of Neurophysiology 52, 435-448.

BURKE, R. E., JANKOWSKA, E. & TEN BRUGGENCATE, G. (1970). A comparison of peripheral andrubrospinal synaptic input to slow and fast twitch motor units of triceps surae. Journal ofPhysiology 207, 709-732.

CHENEY, P. D. (1980). Response of rubromotoneuronal cells identified by spike triggered averagingof EMG activity in awake monkeys. Neuroscience Letters 17, 137-142.

CLAMANN, H. P., NGAI, A. C., KUKULKA, C. G. & GOLDBERG, S. J. (1983). Motor pool organizationin monosynaptic reflexes: responses in three different muscles. Journal of Neurophysiology 50,725-742.

COQUERY, J. M. & COULMANCE, M. (1971). Variations d'amplitude des reflexes monosynaptiquesavant un mouvement volontaire. Physiology and Behavior 6, 65-69.

DESMEDT, J. E. & GODAUX, E. (1977 a). Fast motor units are not preferentially activated in rapidvoluntary contractions in man. Nature 267, 717-719.

DESMEDT, J. E. & GODAUX, E. (1977b). Ballistic contractions in man: characteristic recruitmentpattern of single motor units of the tibialis anterior muscle. Journal of Physiology 264,673-693.

EICHENBERGER, A. & RtEGG, D. G. (1983). Facilitation of the H reflex in a simple and choicereaction time situation. Experimental Brain Research Supplement 7, 130-134.

EICHENBERGER, A. & RtEGG, D. G. (1984). Relation between the specific H reflex facilitationpreceding a voluntary movement and movement parameters in man. Journal of Physiology 347,545-559.

EVARTS, E. V. (1966). Pyramidal tract activity associated with a conditioned hand movement inthe monkey. Journal of Neurophysiology 29, 1011-1027.

EVARTS, E. V. (1974). Precentral and postcentral cortical activity in association with visuallytriggered movement. Journal of Neurophysiology 37, 373-381.

FETZ, E. E. & CHENEY, P. D. (1980). Postspike facilitation of forelimb muscle activity by primatecortico-motoneuronal cells. Journal of Neurophysiology 44, 751-772.

FOURNIER, E., KATZ, E. & PIERROT-DESEILLIGNY, E. (1983). Descending control of reflexpathways in the production of voluntary isolated movements in man. Brain Research 288,375-377.

GARNETT, R. & STEPHENS, J. A. (1981). Changes in the recruitment threshold of motor unitsproduced by cutaneous stimulation in man. Journal of Physiology 311, 463-473.

GHEZ, C. & KUBOTA, K. (1977). Activity of red nucleus neurons associated with a skilled forelimbmovement in the cat. Brain Research 129, 383-388.

GOTTLIEB, G. L. & AGARWAL, G. C. (1971). Effects of initial conditions on the Hoffmann reflex.Journal of Neurology, Neurosurgery and Psychiatry 34, 226-230.

GRIMBY, L. & HANNERZ, J. (1976). Disturbances in voluntary recruitment order of low and highfrequency motor units on blockades of proprioceptive afferent activity. Acta physiologiascandinavica 96, 207-216.

HAAGH, S. A. V. M. & BRUNIA, C. H. M. (1985). Anticipatory response-relevant muscle activity,CNV amplitude and simple reaction time. Electroencephalography and Clinical Neurophysiology61, 30-39.

HAGBARTH, K.-E. (1962). Post-tetanic potentiation of myotatic reflexes in man. Journal ofNeurology, Neurosurgery and Psychiatry 25, 1-10.

HAGBARTH, K.-E., WALLIN, G. & L6FSTEDT, L. (1975). Muscle spindle activity in man duringvoluntary fast alternating movements. Journal of Neurology, Neurosurgery and Psychiatry 38,625635.

HENNEMAN, E. (1974). Principles governing distribution of sensory input to motor neurons. In TheNeurosciences: 3rd Study Program, ed. SCHMITT, F. 0. & WORDEN, F. G., pp. 281-291. CambridgeMA: MIT Press.

386


HENNEMAN, E., SOMJEN, G. & CARPENTER, D. 0. (1965a). Functional significance of cell size inspinal motoneurons. Journal of Neurophysiology 28, 560-580.

HENNEMAN, E., SOMJEN, G. & CARPENTER, D. 0. (1965b). Excitability and inhibition ofmotoneurons of different sizes. Journal of Neurophysiology 28, 599-620.

HONGO, T., JANKOWSKA, E. & LUNDBERG, A. (1972). The rubrospinal tract. III. Effects on primaryafferent terminals. Experimental Brain Research 15, 39-53.

HUGON, M. (1973). Methodology of the Hoffmann Reflex in Man. New Developments inElectromyography and Clinical Neurophysiology, ed. DESMEDT, J. E., vol. 3, pp. 277-293. Basel:Karger.

IOFFE, M. E. (1973). Supraspinal influences on spinal mechanisms activated prior to learnedmovement. Acta neurobiologiae experimentalis 33, 729-741.

KANDA, K., BURKE, R. E. & WALMSLEY, B. (1977). Differential control of fast and slow twitchmotor units in the decerebrate cat. Experimental Brain Research 29, 57-74.

KOHLERMAN, N. J., GIBSON, A. R. & HOUK, J. C. (1982). Velocity signals related to handmovements recorded from red nucleus neurons in monkeys. Science 217, 857-860.

KOTS, Y. M. (1977). The Organization of Voluntary Movement. Neurophysiological mechanisms. NewYork and London: Plenum Press.

LAMARRE, Y., SPIDALIERI, G. & LUND, J. P. (1981). Patterns of muscular and motor corticalactivity during a simple arm movement in the monkey. Canadian Journal of Physiology andPharmacology 59, 748-756.

LIPPOLD, 0. C. J. (1952). The relation between integrated action potentials in a human muscle andits isometric tension. Journal of Physiology 117, 492-499.

LUNDBERG, A. & VYKLICKY', L. (1963). Inhibitory interaction between spinal reflexes to primaryafferents. Experientia 19, 247-248.

LUNDBERG, A. & VYKLICKY', L. (1966). Inhibition of transmission to primary afferents by electricalstimulation of the brain stem. Archives italiennes de biologie 104, 86-97.

LUSCHEI, E. S., GARTHWAITE, C. R. & ARMSTRONG, M. E. (1971). Relationship of firing patterns ofunits in face area of monkey precentral cortex to conditioned jaw movements. Journal ofNeurophysiology 34, 552-561.

MAYER, R. F. & MAWDSLEY, C. (1965). Studies in man and cat of the significance of the H wave.

Journal of Neurology, Neurosurgery and Psychiatry 28, 201-211.MILNER-BROWN, H. S. & STEIN, R. B. (1975). The relation between the surface electromyogramand muscular force. Journal of Physiology 246, 549-569.

MILNER-BROWN, H. S., STEIN, R. B. & YEMM, R. (1973). The orderly recruitment of human motorunits during voluntary isometric contractions. Journal of Physiology 230, 359-370.

OTERO, J. B. (1976). Comparison between red nucleus and precentral neurons during learnedmovements in the monkey. Brain Research 101, 37-46.

PAILLARD, J. (1955). Rapports entre les durees de la periode de silence et du myogramme dans letriceps sural chez l'Homme. Journal de physiologie 47, 259-262.

PIERROT-DESEILLIGNY, E., LACERT, P. & CATHALA, H. P. (1971). Amplitude et variabilite desreflexes monosynaptiques avant un mouvement volontaire. Physiology and Behavior 7, 495-508.

PORTER, R. & HORE, J. (1969). Time course of minimal motoneuronal excitatory postsynapticpotentials in lumbar motoneurons of the monkey. Journal of Neurophysiology 32, 443-451.

PORTER, R. & MUIR, R. B. (1971). The meaning for motoneurones of the temporal pattern ofnatural activity in pyramidal tract neurones of conscious monkeys. Brain Research 34,127-142.

RIEDO, R. & RtUEGG, D. G. (1984). Origin of the H-reflex facilitation before movement initiationin reaction time tasks. Experientia 40, 598.

RUDOMIN, P., JIMENEZ, I., SOLODKIN, M. & DUENAS, S. (1983). Sites of action of segmental anddescending control of transmission on pathways mediating PAD of Ia- and Ib-afferent fibers incat spinal cord. Journal of Neurophysiology 50, 743-769.

RUEGG, D. G. & EICHENBERGER, A. (1983). Detection of reaction time by an adaptative filter basedon the least squares fit. Electroencephalography and Clinical Neurophysiology 56, 256-258.

SANDERS, A. (1980). Some effects of instructed muscle tension on choice reaction time andmovement time. In Attention and Performance, vol. ViII, ed. NICKERSON, R. S., pp. 59-74.Hillsdale, NJ: Erlbaum.

13-2

387


SCHIEPPATI, M. & CRENNA, P. (1984). From activity to rest: gating of excitatory autogenicafferences from the relaxing muscle in man. Experimental Brain Research 56, 448-457.

SCHIEPPATI, M. & CRENNA, P. (1985). Excitability of reciprocal and recurrent inhibitory pathwaysafter voluntary muscle relaxation in man. Experimental Brain Research 59, 249-256.

SIMON, J. N. (1962). Dispositif de contention des electrodes de stimulation pour l'etude du reflexede Hoffmann chez l'Homme. Electroencephalography and Clinical Neurophysiology, suppl. 22,174-176.

SMITH, J. L., BETTS, B., EDGERTON, V. R. & ZERNICKLE, R. F. (1980). Rapid ankle extensionduring paw shakes. Journal of Neurophysiology 43, 612-619.

SNYDER, W. V. (1978). Contour plotting. ACM Transactions Mathematical Software 4, 290-294.STEIN, R. B., FRENCH, A. S., MANNARD, A. & YEMM, R. (1972). New methods for analysing motor

function in man and animals. Brain Research 40, 187-192.TANAKA, R. (1974). Reciprocal Ia inhibition during voluntary movements in man. Experimental

Brain Research 21, 529-540.TANAKA, R. (1976). Reciprocal Ia inhibition and voluntary movements in man. Progress in Brain

Research 44, 291-302.THACH, W. T. (1975). Timing of activity in cerebellar dentate nucleus and cerebral motor cortex

during prompt volitional movement. Brain Research 88, 233-241.VALLBO, A. B. (1971). Muscle spindle response at the onset of isometric voluntary contractions inman. Time difference between fusimotor and skeletomotor effects. Journal of Physiology 318,405-431.

WATT, D. G. D., STAUFFER, E. K., TAYLOR, A., REINKING, R. M. & STUART, D. G. (1976). Analysisof muscle receptor connections by spike-triggered averaging. I. Spindle primary and tendonorgan afferents. Journal of Neurophysiology 39, 1375-1392.

388

Documents

From the Institute of Physiology, University of Fribourg, stimulus, they