Exp Brain Res (1989) 78:465478 Experimental Brain Research �9 Springer-Verlag 1989

Pattern of projections of group I afferents from forearm muscles to motoneurones supplying biceps and triceps muscles in man P. Cavallari* and R. Katz Clinical Neurophysiology, Department of R~6ducation, HSpital de la Salp~tri~re, 47 Bd. de l'HSpital, F-75651 Paris Cedex 13, France

Summary. 1) Two independent methods were used, in man, to assess the modifications of the excitabil- ity of biceps and triceps brachii motoneurone pools following the stimulation of group I afferents com- ing from muscles acting at the wrist: a) the modifi- cations of the excitability of a motoneuronal popu- lation were studied using a reflex technique, b) the modifications of the excitability of an isolated mo- tor unit were estimated using a post-stimulus time histogram (p.s.t.h.) method. 2) The activation of group I afferents contained in the median nerve, originating from wrist flexors and pronators, re- sulted in a strong, short-latency facilitation of the biceps brachii motoneurones. A similar effect was also evoked by stimulation of group I afferents in the radial nerve, distally to the branch supplying the brachio-radialis muscle. The latency of both median and radial-induced facilitations is compati- ble with a monosynaptic linkage. 3) The stimula- tion of group I afferents in the median or the radial nerves produced inhibition of triceps motoneu- rones, with a latency compatible with a disynaptic linkage. 4) The prolonged vibration of the tendon of the flexor carpi radialis (FCR) or of the extensor carpi radialis (ECR) raised the threshold for both the facilitation of biceps and the inhibition of tri- ceps motoneurones. The same pattern of excitatory and inhibitory convergence could also be obtained when the electrical conditioning stimulus to the median or radial nerves was replaced by a tap ap- plied to the tendons of FCR or ECR respectively. Both results suggest that the conditioning fibres were Ia fibres. 5) The pattern of distribution of Ia afferents from muscles acting at the wrist onto motoneurones of muscles acting at the elbow has

* Present address: Istituto di Fisiologia Umana II, Universitfi degli Studi di Milano, I-Milano, Italy

Offprint request to: R. Katz (address see above)

been compared to that described in the cat and monkey. A comparison has also been made be- tween Ia connections of muscles acting at different joints in the upper and lower limb in man. The differences are discussed in relation to the manipu- lating capacity of the hand.

Key words: Ia projections - Monosynaptic reflex - Post-stimulus time histogram - Upper limb - Man

Introduction

The pattern of projections of group I afferents to motoneuronal pools supplying the muscles of the corresponding hind limb has been extensively stud- ied in the cat (Eccles et al. 1957), in the monkey (Hongo et al. 1984) and to a lesser extent in the lower limb in man (Pierrot-Deseilligny et al. 1981). Further experiments concerning the changes in the excitability of these group I reflex pathways during locomotion, voluntary movement or active main- tainance of posture have been carried out subse- quently in man (for references see Pierrot-Deseil- ligny and Mazi6res 1984).

In contrast, only a few studies had been devot- ed to the pattern of group I fibre connections in the cat and the monkey forelimb (Schmidt and Willis 1963; Willis et al. 1966; Clough et al. 1968) prior to the detailed description of Ia connections by Fritz and Illert (1981) in the cat forelimb.

In man, Baldissera et al. (1983) and Day et al. (1984) have shown a very short central latency in- hibition between wrist flexors and extensors. This inhibition, probably evoked by the stimulation of Ia fibres, corresponds in its features to the recipro- cal Ia inhibition described in the cat. Modifications of this reciprocal Ia inhibition during voluntary

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wrist movements (Cavallari et al. 1984) and of the subsequent Ib facilitation after cutaneous stimula- tion have also been studied in wrist muscles (Caval- lari et al. 1985). However, nothing is known in the upper limb about the distribution of group I affer- ent projections onto motoneurone pools of muscles acting at different joints.

This study is devoted to the projections of group I fibres originating from wrist muscles onto motor nuclei supplying elbow muscles: triceps and biceps brachii. Two experimental procedures were used to estimate the effects of the stimulation of group I afferents onto these motoneurones: 1) the excitability of a motoneurone pool was deduced from studying the modifications of the amplitude of a monosynaptic test reflex, 2) the modifications of the probability of discharge of an isolated volun- tary activated motor unit were studied by the post stimulus time histogram method.

Methods

The experiments were carried out on 9 healthy subjects (aged 30~43) who gave informed consent to the procedure. The surface electromyogram (e.m.g.) was recorded by two non po- larizable disk electrodes (0.9 mm diameter). In the reflex experi- ments they were placed over the belly of the long head of the biceps muscle in its more proximal portion, the long head of the triceps muscle 2 cm distally to the deltoid sulcus, the flexor carpi radialis (FCR), the flexor carpi utnaris (FCU) and the extensor carpi ulnaris (ECR). In the p.s.t.h, experiments they were placed over the distal part of the same muscles. The e.m.g. was amplified, filtered and computer-analysed " o n line" and the results stored on disk for further analysis.

Conditioning stimuli

Electrical pulses of 0.5 ms or 1 ms durat ion were delivered per- cutaneously through bipolar electrodes. The median nerve was stimulated just above the elbow, the ulnar nerve in the ulnar groove, the radial nerve a few cm below the elbow, so that the stimulation did not involve the brachio-radialis muscle branch. The electrodes were carefully positioned so that the stimulation resulted in a clear direct motor response (M) of the FCR, the FCU or the ECR muscles, always taking care that the threshold for the M response of the forearm muscles was lower than the one for the hand muscles. It should be emphasized however, that the median, radial and ulnar nerves supply numerous muscles of the forearm, hand and fingers. Even though it was possible, by palpating the tendons, to deter- mine the exact muscle origin of the M or the reflex response, it was impossible to exclude that group I afferents originating from muscles other than the one in which the M or the reflex response was evoked, were not also activated by the condition- ing stimulation. The current delivered by the stimulators was measured by a current probe (Tektronix 6021) and the stimulus intensity was expressed in multiples of the threshold intensity of the direct motor wave ( x MT). In some experiments the conditioning stimulus was delivered to the median or the radial nerve after a continuous vibration (166 Hz during 25 rain), ap- plied on the distal tendon of the FCR or ECR muscle, an artifice that selectively increases the electrical threshold of the

Ia afferents, as described in the cat by Coppin et al. (1970), while the Ia receptor mechanical threshold to muscle stretch remains unimpaired (Fetz et al. 1979). In man, Heckman et al. (1984) have shown that after such prolonged tendon vibration, the electrical stimulation of the posterior tibial nerve is marked- ly less effective in eliciting monosynaptic H reflexes in the soleus muscle. However it is not possible to be sure that the vibration of the distal tendon of the FCR or ECR muscle would not also affect Ia fibres originating from neighbouring muscles.

A low intensity mechanical tap applied to the distal tendon of the FCR or ECR muscles was also used as a conditioning stimulus (see below for more details).

The stimulation of the median, radial or ulnar nerves also activated cutaneous afferents, producing a local pricking sensa- tion under the stimulation electrodes and/or a paresthesia irra- diating along the nerve to the fingers. Similar cutaneous sensa- tions were evoked without stimulating the nerve trunk. The local pricking was reproduced by displacing the electrodes later- ally on the arm, 2-3 cm away from the nerve trajectory, so that the stimulus was applied only to the skin. To reproduce the irradiating paresthesia, large plate electrodes were placed over the nerve projection area, on the skin of the fingers. The time taken by the cutaneous afferent volley to run from the electrodes placed on the fingers to the sites of the electrical conditioning stimuli described above was determined and the part of the conditioning-test interval corresponding to this ex- tra-peripheral conduction time was subtracted. The intensity of the stimulus was expressed in multiples of the perception threshold. On most of the trials the subject was unable to differ- entiate the cutaneous sensation thus obtained from the one evoked by stimulation of the nerve trunk.

Test of the motoneuronal population (tendon tap reflex)

Since the H-reflex wave of the biceps or triceps brachii muscles is not clearly distinguishable from the direct motor response (see also Bratzlavsky et al. 1971), the excitability of their moto- neuronal pool was tested by eliciting monosynaptic reflexes with a tendon tap. The tap was applied to the distal tendon of the muscle by an electromagnetic hammer (Briiel et Kja~r model 4809) which produced a very quick transient stretch (8 mm during 5 ms). The examined arm was loosely fixed with the elbow flexed (90 deg) and the wrist slightly flexed (10 deg) in supine position. The intensity of the percussion was graded using a power amplifier and expressed in multiples of the threshold for eliciting a tendon-jerk reflex ( x TT). Special care was taken to ensure that the hammer struck the tendon at the same position throughout the experiment.

The size of the test reflex, measured as the peak-to-peak amplitude of the muscle action potentials was expressed as a percentage of the maximal motor response (Mmax). Biceps and triceps brachii are innervated by several deeply located nerve branches and when using the maximal intensity delivered by the stimulator to evoke the Mmax response, it is possible that not all the nerve branches were stimulated. This could lead to an underestimation of the amplitude of the Mmax response and therefore to an overestimation of the size of the test re- flexes, expressed as a percentage of Mmax. The reflexes were chosen to be large enough so that inhibition as well as facilita- tion could be clearly seen. In the biceps brachii the size of the unconditioned test reflex varied among the subjects ( N = 7) and the different experiments (N=20) , from 15 to 27% of Mmax; in the triceps brachii it varied between 7 and 30% of Mmax (6 subjects, 23 experiments).

By convention, the timing of the pulse triggering the tap (test stimulus) was referred to the timing of the conditioning electrical shock. Because of the delay introduced by the electro-

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magnetic coupling of the hammer, the simultaneous arrival of the conditioning and test volleys in the spinal cord was obtained when the conditioning stimulus was delivered after the tap trig- ger. In such a case the conditioning-test interval was said to be negative. Series of 20 control and 20 conditioned reflexes were randomly alternated in each sequence. Variance analysis was used for testing the significance of the changes of the test reflex amplitudes.

Test of the excitability of single motor units (p.s.t.h.)

The effect of a conditioning stimulus on a voluntarily activated motor unit can be determined by constructing a time histogram of the occurrence of motor unit spikes following repeated pre- sentation of the stimulus. The post-stimulus time histogram (p.s.t.h.) extracts from the naturally occurring spike train only those changes in firing probability which are time-locked to the stimulus (Stephens et al. 1976). The validity of the method to detect post-synaptic potentials in motoneurones has also been established in animal experiments (Fetz and Gustafsson 1983; Gustafsson and McCrea 1984).

A detailed description of the particular method used in this section has been already published (Fournier et al. 1986) and will be only summarized here. The e.m.g, from single motor units of the biceps and triceps brachii was recorded by conven- tional surface electrodes: while the subject performed a very weak but steady contraction the electrode was moved on the skin (previously rubbed with abrasive paste) until it was possi- ble to isolate one motor unit, either because it was the only one active or because it was significantly larger than the others. After several training sessions this was achieved rather easily using auditory and visual feed-back of the e.m.g, potential. In all the subjects thus examined the contraction strength was below 5% of maximal voluntary power. The motor units stud- ied were therefore all in the low-threshold range. The e.m.g. potentials of single motor units were converted into standard pulses by a discriminator with variable trigger levels and were used to trigger first a computer (Apple II) and then the stimula- tor delivering nerve stimulations. The motor unit potential and the trigger pulse were continuously monitored to detect false triggers due to other active units and to ensure that the motor unit shape and trigger position remained constant within and between sequences. Furthermore, a special test (see Fig. 1 E) was used to ensure that the discriminated pulse did not originate from different motor units.

When the nerve stimulation is delivered at a fixed interval after the previous motor unit discharge, it is possible to choose a delay at which the probability for a new discharge is high (provided that there is a relatively regular firing frequency dur- ing voluntary contraction). This implies that the number of triggers necessary to reveal obvious peaks in the p.s.t.h, can be much lower than if nerve stimulations are given without reference to the motor unit discharge. The conditioning stimula- tion of the nerves was therefore triggered at a fixed delay after the preceding motor unit discharge (Fournier et al. 1986). This delay was chosen so that the conditioning stimulus was trig- gered 10 ms before the next "spontaneous" firing (see Fig. 1 A). The latency of the motor unit potential following the condition- ing stimulus was then computed. The p.s.t.h.'s of the voluntary motor unit discharge were constructed for the period 10-40 ms following the stimulation using 0.2 ms bins (Fig. 1 C). This method also implies that the probability of discharge in the p.s.t.h, does not depend only on the postsynaptic potentials evoked by the stimulation, but also on the motoneurone mem- brane trajectory during the interspike interval (Fig. 1 B). To take account of the latter, a histogram of firing probability was also constructed in a control situation without stimulation

(Fig. 1 D). The control and the different conditioning situations were randomly alternated (same number of triggers) within a sequence. The control histogram represented the background firing probability to which the results following stimulation were compared. Within different time interval windows a ;g2 test was used to determine to what extent the distribution of firing probability after stimulation differed from that obtained in the control situation. Such an analysis was only performed after having checked (using a )~2 test) that in the control situa- tion the firing probability within the window of analysis did not differ from the mean probability of discharge of this unit (10 ms before and 10 ms after the window).

Results

L Effects of the stimulation of group I afferents contained in the median nerve on biceps motoneurones

A. Responses of the motoneurone population

Figure 2A shows the time course of the changes in a biceps brachii tendon reflex when conditioned by stimulation of the median nerve at an intensity of 0.9 x MT. The facilitation of the test reflex started for a conditioning-test interval of - 5 ms, with an abrupt onset and peaked at - 4 ms. At its peak, the test reflex size had increased to 169% of its control value. Later, the facilitation declined to be replaced by an inhibition which ended at + 4 ms. When the inhibition was maximum, the test reflex amplitude reached 75% of the control value. At the peak of facilitation the test reflex amplitude varied among the 7 subjects from 120% to 400% of their control value.

A first attempt at determining which afferent fibres were responsible for the biphasic time course was to study the changes in the test reflex ampli- tude while varying the intensity of the conditioning stimulus. Figure 2B (filled circles) represents the results obtained at a conditioning test interval of - 4 . 5 ms (arrow on Fig. 2A) i.e. at the very onset of the facilitation. The strength of the conditioning stimulus was increased by steps of 0.05 x MT and a progressive increase of the test reflex amplitude started above 0.8 x MT and rose up to 1 x MT.

Similar experiments were repeated after having selectively raised the electrical threshold of Ia fibres contained in the median nerve (see Meth- ods). An example is illustrated on Fig. 2B (open circles) which shows that the threshold of the facili- tation of the biceps test reflex was increased, the effect now appearing at a conditioning stimulus intensity of 1 x MT. For higher intensities the faci- litation of the test reflex increased but always re- mained below that observed in control conditions (Fig. 2 B). 20 minutes after the end of the vibration

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Fig. 1A-E. P.s.t.h. technique. A Photograph of a single oscilloscope sweep showing the spontaneous firing of a single biceps voluntary activated motor unit. Upper trace: e.m.g, signal recorded by surface electrodes; lower trace: the motor unit potential converted into a standard pulse by a discriminator - the zero of the time scale corresponds to the occurrence of the first motor unit potential. B a Photograph of 20 superimposed e.m.g, sweeps during the spontaneous firing of a single voluntary activated biceps motor unit; b standard pulses triggered by the e.m.g, motor unit potentials; e p.s.t.h, of the same biceps motor unit obtained with 550 triggers (including the 20 illustrated in a, b). Ordinate: number of counts expressed as a percentage of the number of triggers. Abscissa: time elapsed since the occurrence of the previous motor unit potential. Note that the spontaneous firing after the previous spike was first interrupted during 60 ms and then progressively increased with increased time intervals, reflecting the post spike motoneurone membrane trajectory and thus indicating that the p.s.t.h, was obtained in a single motor unit. C a 5 superimposed e.m.g, sweeps of a single biceps motor unit following a conditioning median stimulation triggered 90 ms after the previous spike; b as in B; c p.s.t.h, of the same motor unit obtained with 170 triggers. Same coordinates as in B except that the time scale indicates the time elapsed since the conditioning stimulus. D 5 superimposed e.m.g, sweeps of the same motor unit as in C without conditioning stimulation, a, b , c : as in C. The p.s.t.h, was obtained with 150 triggers. E 5 superimposed e.m.g, sweeps of the same motor unit as in C and D, but the conditioning stimulus is triggered 0 ms after the previous spike. As already shown (B) with such a short delay the after hyperpolarization was deep and prevented the motoneu- tone from discharging. Such a result indicates that only one single motor unit e.m.g, potential was recorded. Arrow below time scale in A, B indicates when the conditioning stimulus was applied. Note in B that this delay corresponds to the end of the rapid increase in the spontaneous firing which explains that the control histogram in Fig. D is rather flat.

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Fig. 2A, B. Changes in the amplitude of the biceps brachii ten- don reflex following a conditioning electrical stimulation of the median nerve (0.9 x MT). .A Time course of the effects of the median nerve stimulation: the amplitude of the biceps bra- chii test reflex expressed as a percentage of its unconditioned value (15% Mmax) is plotted against the time interval between conditioning and test stimuli. By convention, the timing of the test stimulation is referred to that of the conditioning one. Neg- ative delays correspond to the cases in which the test shock came first. B Effects of changing the intensity of the median conditioning stimulation. The amplitude of the test reflex (ex- pressed as a percentage of "its unconditioned value) is plotted against the strength of the conditioning stimulus (expressed in multiples of the threshold strength of the M wave: x MT). The explored conditioning test interval (--4.5 ms) is indicated by an arrow on Fig. 1 A. Filled circles represent the variations obtained in control conditions. Open circles represent the varia- tions obtained during a selective increase of the electrical threshold of the conditioning Ia fibres by prolonged vibrations. Fil led arrow indicates the threshold of the facilitation in control conditions; open arrow the one during the increase of the electri- cal threshold of conditioning Ia fibres. Each symbol represents the mean of 20 measurements. The vertical bars 1 standard error of the mean

the threshold of the test reflex facilitation returned to its control value.

Figure 3 B (open circles) shows the time course of the changes in the biceps brachii test reflex when preceded by a low intensity tap applied to the FC R distal tendon (0.5 x TT). The mechanical condi- tioning stimulus, adequate for selectively activating the muscle spindle primary afferents (Lundberg and Winsbury 1960), produced a strong facilitation of the biceps test-reflex delayed by about 5 ms compared to the one evoked by electrical stimula- tion of the median nerve at 0.9 MT (illustrated for comparison with filled symbols). This can be ex- pected if one takes into account that the tap was applied distally at the wrist, the hammer had a delay in the electromagnetic coupling and the tap introduced a mechanical delay. It should also be noted that the tap conditioning stimulus was not effective in evoking the late inhibitory effect. Simi-

lar results were obtained in all 4 subjects in whom the experiment was performed.

Although a facilitation due both to a weak elec- trical stimulation and to a slight tendon tap is very probably mediated by Ia fibres (see also Pierrot- Deseilligny etal. 1981), a possible contribution from cutaneous afferents must be considered since some cutaneous fibres in the median nerve have conduction velocities which overlap those of Ia fibres (Buchtal and Rosenfalk 1966). Experiments were therefore performed with a purely cutaneous conditioning stimulation mimicking the sensation evoked by the median nerve stimulation (see Meth- odsy. A typical result is illustrated in Fig. 3 C: cuta- neous stimulation applied on the arm, 2-3 cm from the nerve trajectory, (dotted circles) or on the fingers and mimicking the projected paresthesia (open triangles) did not modify the amplitude of the test reflex at conditioning-test intervals corre- sponding to the biphasic time course illustrated in Fig. 3 C (filled circles).

B. Responses of individual motor units

The upper histogram in Fig. 4A shows the sponta- neous firing of a biceps motor unit, whereas the lower one shows the firing probability of the same biceps motor unit following a conditioning stimu- lus applied on the median nerve (0.9 x MT).

To better display the differences, the results ob- tained in the control situation (Fig. 4A upper row) were subtracted in each bin from the results ob- tained with a conditioning stimulus (Fig. 4A lower row). The results of this subtraction are shown in Fig. 4 B with a different time scale. Stimulation of the median nerve thus resulted in an early and highly significant (P<0.001) increase in firing probability of the biceps motor unit, which began 13.6 ms after the conditioning stimulus.

Five subjects were examined and 45 motor un- its recorded. Only 25 of them were considered sat- isfactory. For all these units, the stimulation of the median nerve resulted in an early and large increase in firing probability.

The possibility that cutaneous fibres may con- tribute to this increase in firing probability was ruled out using the same complementary experi- ments as those described in section A: no modifi- cation of firing probability was found following pure cutaneous stimulations.

The modifications of the firing probability of a given biceps motor unit induced by the median nerve conditioning stimulation (heteronymous projections) were compared to those following an electrical stimulation of the musculo-cutaneous

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Fig. 3A-C. Chauges in the amplitude of the biceps brachii tendon reflex following various conditioning stimuli. The experimental paradigm is sketched in A. The test stimulation is a mechanical tap applied on the distal biceps brachii tendon. The conditioning stimuli are; 1) an electrical stimulation of the median nerve (0.9 x MT); 2) a mechanical tap applied on the distal tendon of the FCR muscle; 3) cutaneous stimulation applied on the fingers and mimicking the irradiations induced by the electrical median stinmlation. B Time course of the variations of the biceps brachii test reflex amplitude (expressed as a percentage of its unconditioned value) following an electrical median stimulation (filled circles) and a mechanical tap applied on the distal tendon of the FCR muscle (open circles). C Time courses of the variations of the biceps brachii test reflex following an electrical median stimulation (filled circles), a cutaneous stimulation applied on the fingers (open triangles), a cutaneous stimulation applied on the arm near the site of the stimulation of the median nerve (dotted circles). Same abscissa and ordinate as in Fig. 1 A. Each symbol represents the mean of 20 measurements. Verticals bar 1 standard error of the mean

nerve (homonymous projections). In Fig. 4C the conditioning stimulus (0.9 x MT) was applied to the musculo-cutaneous nerve and resulted in an early increase (12.8 ms) of the firing probability of the same biceps motor unit.

Since it has been demonstrated in man that the earliest part of the soleus H-reflex occurs at monosynaptic latency (Magladery et al. 1951), the onset of the early increase in firing probability fol- lowing homonymous stimulation is usually com- pared to onset of the H-reflex (Mao et al. 1984; Malmgren and Pierrot-Deseilligny 1988). As stated in the Methods, in biceps and triceps muscles, the H-reflex wave evoked at rest overlaps the M wave. An H-reflex was therefore elicited during a sus- tained voluntary contraction of the biceps brachii, by a stimulus intensity below motor threshold and revealed by an average technique. Its latency was in accordance with that of the early increase in firing probability observed in p.s.t.h, experiments. The first two bins (i.e. the first 0.4 ms) of the early increase in firing probability following homonym-

ous stimulation at intensity just below motor threshold are very likely due to monosynaptic Ia input, if one admits that monosynaptic Ia connec- tions are to be found in every motoneurone pool. Since the facilitation following musculo-cutaneous and median nerve stimuli were obtained in the same motor unit, the efferent conduction time (from the C5 spinal level to the muscle) was the same in both situations. Hence the difference be- tween the latencies of these two effects (0.8 ms: 13.6-12-8) (Fig. 4B, C) must be attributed to dif- ferences in afferent conduction time and/or in the central latency. Similar short latencies (from 0.4 ms to 2 ms depending upon the distance be- tween the two conditioning electrodes) were found in the 8 experiments in which it was possible to study the effects of both conditioning stimuli on a same biceps motor unit. In 3 subjects the afferent conduction time of each conditioning volley (mus- culo-cutaneous and median nerve) was then esti- mated by calculating the conduction velocity of the fastest Ia fibres and by measuring the distance

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Fig. 4A-C. Time histogram of the discharge of a voluntary activated biceps brachii motor unit in control conditions (A, upper row), and in response to median (A, lower row and B), and musculo-cutaneous (C) nerve stimulation. The histogram obtained without stimulation (A upper row) was subtracted from that obtained after median nerve stimulation and muscu- lo-cutaneous nerve stimulation and the results of these subtrac- tions are shown in B, C respectively. Ordinate, number of counts expressed as a percentage of the number of triggers. Abscissa, time elapsed since the occurence of the conditioning stimulation. Note that the scale of abscissa is much smaller in B, C than in A. Delay between the stimulation and the pre- vious spike 80 ms; number of triggers 300

from the electrode site to the spinal cord (Table 1). To determine the conduction velocity of the fastest Ia fibres, p.s.t.h's of the same single motor unit (biceps or FCR) were constructed after stimulation at two sites of both the musculo-cutaneous nerve and the median nerve. It was thus possible to calcu- late the time taken by the musculo-cutaneous and the median nerve afferent volleys to reach the bi- ceps motoneurone pool. In the 3 subjects, the dif- ferences between the two afferent conduction times fully accounted for the differences in the latencies of the onset of the two increases in firing probabili-

47]

ty observed in p.s.t.h, experiments. This implies that the central delay of the homonymous and he- teronymous facilitation is identical, which strongly suggests that the facilitation of the biceps moto- neurones induced by the stimulation of the median nerve is monosynaptic, at least at its onset.

The magnitude of the peak in firing probability induced by the median nerve stimulation (Fig. 4 B) was greater than the one obtained after homonym- ous stimulation (Fig. 4C).

As stated in the Methods section, the probability of dis- charge in the p.s.t.h, did not depend only on the post-synaptic potentials evoked by the stimulation but also on the motoneu- rone membrane trajectory during the interspike interval. No conclusion can therefore be drawn from the absolute value of the peak magnitude. Nevertheless since the two conditioning stimuli (median nerve and musculo cutaneous nerve stimula- tion) were randomly alternated in a same sequence and their effects studied in the same motor unit, the homonymous and heteronymous peaks were obtained for the same state of the motoneurone membrane trajectory. It was therefore meaningful to compare the magnitude of the homonymous and heteronym- ous peaks.

In all the biceps motor units studied, the results were the same. This is most probably due to the fact that the electrical stimulation applied to the median nerve involved the whole nerve, whereas the stimulation applied to the musculo-cutaneous nerve, which has already branched at the stimulus site, very likely excited only a portion of it (see Methods and Discussion).

As stated in Methods, the site of the median nerve stimulation was situated just above the el- bow. From this point, the median nerve supplies several muscles, namely the pronator teres, the FCR, the flexor digitorum communis (FDC), the pronator quadratus, intrinsic muscles of the hand, raising the question of which muscles originated the afferent fibres responsible for the early facilita- tion of the biceps motoneurone pool. The nerve branches supplying these muscles divide from the nerve trunk at different levels. Therefore a first indication may be gained from stimulation applied at different sites on the nerve course. When the site of stimulation was situated at the wrist, there was no modification of the excitability of the bi- ceps motoneurone pool. When the site of the stim- ulation was moved on the forearm from the wrist to its upper part there was no effect either. At the elbow level small changes in the electrode posi- tion were crucial. When the stimulation resulted in an H-reflex in the FDC (localised by palpation) and not in the FCR, there was also no effect. When the site of stimulation was progressively moved at the elbow level from its proximal part to its distal part, the facilitation of the biceps motoneurone

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Table 1. "Calculated" difference between the two afferent conduction times : for each conditioning volley (musculo-cutaneous and median nerve) the afferent conduction time was calculated as the ratio distance between the electrode site and the spinal cord/conduction velocity of the fastest Ia fibres. "Difference between the latencies of the two effects" : the latency of the first bin of the increase in firing probability induced by the stimulation of the musculo-cutaneous nerve was compared to that induced by the stimula- tion of the median nerve in the same motor unit (Fig. 3)

Subject Bicpes Ia Median Ia "Calculated" difference Difference in the conduction velocity conduction velocity between the two afferent latencies of the onset (m/s) (m/s) conduction times (ms) of the two peaks

in p.s.t.h. (ms)

MIC 59 60 0.7 0.6 SAB 46 61 0.9 0.8 RIG 56 60 2 1.8

pool disappeared in 3 subjects and was reduced in the fourth one. Taking into account that the branch supplying the pronator teres leaves the me- dian nerve more proximally than the one supplying the F C R it seems possible that the stimulation of afferent fibres coming from the pronator teres is necessary to get the early facilitation of the biceps motoneurone pool. An alternative and/or comple- mentary hypothesis is, however, that when the con- ditioning stimulation is located at the distal part of the elbow only part of the nerve branches sup- plying the F C R are stimulated and thus there are not enough FCR afferent fibres to get the effect.

II. Pattern of group I fibre projections from muscles acting at the wrist onto biceps and triceps brachii motoneurones

The experimental protocol described in the preced- ing sections, was also used to study the effects evoked by stimulation of low threshold afferent fibres contained in the radial, median and ulnar nerves onto biceps and triceps motoneurones.

Results will be presented as a comparison be- tween the effects evoked by median, radial and ulnar nerve stimulations onto both biceps and tri- ceps brachii motoneurones. The results of the con- trol experiments (changes in the test reflex ampli- tude while varying the intensity of the conditioning stimulus, increase of the electrical threshold of Ia afferents, tendon tap as a conditioning stimulus, selective stimulation of cutaneous afferents) are mentioned but not illustrated.

A. Responses of biceps and triceps motoneuronal pools to median, radial and ulnar nerve stimula- tion

1. Median nerve conditioning stimulation. Fig- ure 5 A, B show that the same median nerve condi-

200

150

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150

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150

100

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, , ........ ,r

-6=4-2 0 2 4 6 8

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% , ; - ; .... . ,%

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Fig. 5A-D. Time course of the effects of a median (A, B) and radial (C, D) stimulation (0.9 x MT) on the tendon reflex of the biceps brachii muscle (upper row) and of the triceps brachii muscle (lower row). Same ordinate and abscissa as in Fig. 1 A. Control value of the biceps tendon reflex: 17% Mmax. Control value of the triceps tendon reflex: 20% Mmax. Each symbol represents the mean of 40 measurements. Vertical bars 1 stan- dard error of the mean

tioning stimulus produced opposite effects onto a biceps (A) and a triceps (B) tendon reflex: whereas it resulted in the already described early facilitation of the biceps reflex, it gave rise to an early inhibi- tion of the triceps reflex. This inhibition beginning at a conditioning-test interval of - 4 ms, reached its maximum for an interval of + 1 ms (50% of the control value) - declined progressively and was replaced at + 3 ms interval by a slight facilitation. In 8 experiments the sudden decline of the inhibi-

473

tion around 2.5-3 ms suggests that an excitatory process develops at that time, an interpretation supported by the finding that, in 3 subjects, the inhibition was replaced at + 3 ms by a statistically significant facilitation of the test reflex (112% in Fig. 5B). This slight facilitation had a higher threshold than the inhibition. Among the 23 exper- iments, at the peak of inhibition, the test reflex amplitude ranged between 55 and 89% of its con- trol value. In Fig. 5A, B, the earliest modification of the triceps reflex amplitude (inhibition) began at - 4 ms while the earliest one of the biceps test reflex amplitude (facilitation) began at - 6 ms. The time course of the variations of the triceps test reflex was therefore systematically explored be- tween - 8 and - 3 ms in 11 experiments (by steps of 0.5 ms) but no significant effect was found.

The same complementary experiments de- scribed for the biceps motoneurone pool were per- formed to identify the nature of the afferent fibres responsible for the first effect. The threshold of the inhibition of triceps motoneurones was en- hanced using a prolonged vibration applied to the F CR tendon, thus indicating that Ia fibres are very probably responsible for this inhibition. Moreover, a slight mechanical tap (0.5 x TT) applied to the tendon of the FCR muscle produced the triceps inhibitory effect as it provoked the biceps reflex facilitation. In contrast, a cutaneous conditioning stimulus applied on the skin of the palmar side of the hand did not modify the size of triceps re- flexes at the tested intervals.

2. Radial nerve conditioning stimulation. Figure 5 C shows the time course of the changes in the biceps brachii test reflex amplitude when preceded by a stimulation of the radial nerve at an intensity of 0.9 x MT. This time course is similar to the one obtained with a median nerve conditioning stimu- lus (Fig. 5A). The early facilitation was maximal at - 5 ms, when the test reflex amplitude reached 160% of its unconditioned value, then the facilita- tion declined and was followed by an inhibition, with the test reflex amplitude reaching 56% at - 1 ms. The inhibition gradually decreased to end at +3 ms. Similar results were observed in the 15 experiments performed in 5 subjects. At the peak of the early facilitation, the test reflex ampli- tude ranged from 116 to 160% of its unconditioned value. Figure 5D shows that when the effects of the same radial conditioning stimuli were studied on a triceps brachii tendon reflex, it produced a clear inhibition, followed by a small facilitation that suggested the biphasic time course induced by the median volley in the same motoneurones.

The onset of the inhibitory effect started at a con- ditioning test interval of - 5 ms. This early inhibi- tion was maximum at + 1 ms and the test reflex amplitude reached 58 % of its unconditioned value. Here too, it was carefully verified, by 0.5 ms steps, that no facilitation took place in the 4 ms preced- ing this inhibition. In the 13 experiments (5 sub- jects) at the peak of the inhibition, the test reflex amplitude ranged from 66 to 80% of its uncondi- tioned value and in one subject a slight facilitation (117%) followed this inhibition.

The control experiments gave the following re- sults: the first effects (facilitation for the biceps test reflex and inhibition for the triceps test reflex) were also obtained with an ECR tendon tap; their threshold after electrical stimulation was enhanced when the threshold of the radial Ia fibres was en- hanced; cutaneous stimulations were not effective.

3. Ulnar nerve conditioning stimulation. 10 experi- ments on 6 subjects were performed using the bi- ceps tendon reflex as test and 7 experiments on 4 subjects with the triceps tendon reflex, and ulnar stimulation as conditioning stimulus. The results were the same in all experiments. There was no significant effect of the stimulation of the group I fibres contained in the ulnar nerve either on the biceps or the triceps brachii test reflexes.

B. Responses of individual motor units

The p.s.t.h, protocol previously described was used to study the effects of median, radial and ulnar nerve electrical stimulation (intensity 0.9 x MT) onto isolated biceps or triceps motor units during voluntary activation.

The effects of a median and radial nerve condi- tioning stimulation on the firing probability of a biceps and a triceps motor units are illustrated in Fig. 6. In each set, the spontaneous firing (i.e. with- out any stimulation) is represented in the upper row (A, C. E, G), while the lower row shows the firing probability of the same motor unit following a conditioning stimulus applied on the median nerve (Fig. 6B, F), and on the radial nerve (Fig. 6D, H). The intensity of the conditioning stimuli was adjusted to be below motor threshold. In control experiments, the e.m.g, of the muscles involved by the conditioning stimulus were re- corded and averaged during a whole sequence in order to be sure that during this sequence the con- ditioning stimulus had never resulted in any motor or reflex response. It was thus possible to exclude the activation of motor axons which would have resulted in Renshaw cell activation.

474

Median stimulation

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Fig. 6A-H. Time histograms of the discharge of a voluntary activated biceps brachii motor unit (left column) and of a volun- tary activated triceps brachii motor unit (right column). A, C, E, G Spontaneous firing without stimulation. B, F Histograms obtained after a median nerve stimulation. D, H Histograms obtained after a radial nerve stimulation. The intensity of the median stimulation was 0.32 x MT in order not to evoke any M or H response (see text). The intensity of the radial stimula- tion was 0.8 x MT and did not evoke any M or H response. Ordinate: number of counts expressed as a percentage of the number or triggers. Abscissa: latency after conditioning stimu- lation. Number of triggers 300

The stimulation of the median nerve (B) re- sulted in an early (13.6ms) and significant ( P < 0.001) increase in the firing probability of the bi- ceps motor unit (Fig. 5 B versus A) whereas it pro- duced an early (16.6 ms) and significant decrease (P<0.001) in the firing probability of the triceps motor unit (Fig. 5 F versus E). The stimulation of the radial nerve resulted in an early (15.2 ms) and significant increase in the firing probability of the biceps motor unit (Fig. 6C, D) and in an early (19.2 ms) and significant (P < 0.001) decrease in the firing probability of the triceps motor unit (Fig. 6G, H). Effects induced by the stimulation of the radial nerve began later than those induced by the median nerve stimulation since the radial nerve electrodes were placed more distally than the median ones.

The same pattern was displayed in the 10 bi- ceps motor units (from 4 subjects) and 12 triceps motor units (from 4 subjects) in which it was possi- ble to study during the same session the effects of both radial and median nerve stimulations.

To appreciate the central delay of the heteronym- ous facilitation induced in the biceps motoneurone pool by a median nerve conditioning stimulation, the latencies of the onset of the homonymous and heteronymous facilitation induced in a same biceps motor unit were compared using the protocol de- scribed in section I, B. Exactly the same protocol was used to appreciate the central delay of the heteronymous facilitation induced by a radial nerve stimulation. As far as the triceps motoneu- rone pool is concerned, only inhibitory effects were observed. Katz and A. Rossi have found (unpub- lished results) that the inhibition induced in triceps motoneurones by a musculo-cutaneous nerve stim- ulation at intensity below motor threshold is very likely reciprocal Ia inhibition. Therefore the la- tency of the onset of this reciprocal Ia inhibition was compared to that of the onset of the inhibition induced by the median (or the radial) stimulation in a same single triceps motor unit using a similar protocol as that described in section I, B: the onset of the decrease in firing probability induced by a median (or radial) nerve stimulation was com- pared to the onset of the decrease in firing proba- bility induced by reciprocal Ia inhibition. Those comparisons lead to the conclusion that all the fa- cilitatory effects have the same central latency as the homonymous facilitation and all the inhibitory effects have the same central latency as the recipro- cal inhibition.

Additional experiments, such as those de- scribed in the case of the median nerve condition- ing stimulation (section I, B), were performed to identify the muscle origin of the afferent fibres con- tained in the radial nerve responsible for the first effect. The site of the radial nerve stimulation was in all cases too distal to involve brachio-radialis afferent fibres. It was verified however that, ap- plied at this site, even stimulation at maximal in- tensity did not evoke any response in the brachio- radialis muscle. When the radial nerve stimulation gave rise to an M response in the extensor digito- rum communis (EDC) no effect was found, where- as it appeared when the radial nerve stimulation evoked an M response in the ECR.

Discussion

The pattern of distribution of low threshold affer- ents contained in the median, radial and ulnar nerves onto biceps brachii and triceps brachii mo- toneurones were studied by two different experi- mental methods, leading to similar results.

Low threshold afferent fibres originating from flexor and extensor muscles of the wrist were

shown to produce short latency facilitation in bi- ceps motoneurones and short latency inhibition in triceps motoneurones. No effect was observed in biceps and triceps motoneurones after stimulation of the ulnar nerve.

1. Afferent fibres responsible for the effects

a) The effects evoked by median and radial nerve stimulation on both biceps and triceps motoneu- rones have common characteristics: they are ob- tained for a stimulus intensity below motor thresh- old; they are not obtained by low threshold cutane- ous afferents. It may thus be concluded that they are produced by volleys in group I fibres.

b) The electrical conditioning stimuli gave rise to early effects both on biceps and triceps test re- flexes. The threshold of the earliest effects, facilita- tory for the biceps test reflex, inhibitory for the triceps test reflex was enhanced when the threshold of the conditioning Ia fibres was raised after hav- ing applied long lasting vibration on the corre- sponding tendon. These earliest effects were also obtained with a slight conditioning tendon tap, which is supposed to selectively activate muscle spindle primary endings (Lundberg and Wisbury 1960). The slight conditioning mechanical tap, ap- plied on the F C R or the ECR tendon certainly activates spindle primary endings contained in the FCR or the ECR muscles, but it might also acti- vate spindles contained in other muscles of the forearm or spindles contained in the biceps or the triceps brachii muscle since Katz et al. (1977) have shown in the lower limb that a subthreshold (0.95 x TT) mechanical tap applied on the quadri- ceps tendon can activate soleus spindles. To mini- mize the activation of the spindles contained in the proximal arm muscles by the tendon tap ap- plied to the wrist level, the intensity of the condi- tioning tendon tap was low (0.5 TT). Moreover it was verified that this slight tendon tap was no longer effective when it was moved slightly to the ulnar part of the wrist and that the same condition- ing tendon tap induced opposite effects on the bi- ceps and the triceps test reflex. Nevertheless, acti- vation of spindles contained in the proximal mus- cles and above all of those contained in forearm muscles other than those to which the tendon tap was applied (FCR on the flexor side and ECR on the extensor side) cannot be completely ex- cluded. In conclusion, the results obtained with both electrical and mechanical stimulation support the hypothesis that Ia fibres contained in the radial and median nerves are responsible for the short

475

latency excitation and inhibition of biceps and tri- ceps motoneurones. An uncertainty remains about the muscle (FCR or pronator teres among muscles supplied by the median nerve) from which the ef- fective Ia afferents originate.

c) In the biceps motoneurones the early facilitation was followed by a significant inhibition, while in triceps motoneurones, the early inhibition was fol- lowed by a weak facilitation, statistically signifi- cant only in a few cases. These longer latency ef- fects have a higher threshold than the earliest la- tency effects, and were not obtained when the con- ditioning stimulus was a tendon tap. It is thus tempting to suppose that the late effects could be Ib in origin. It might seem surprising that one can distinguish Ia from Ib effects, in view of the fact that in the cat forelimb there is a considerable over- lap between the electrical threshold of Ia and Ib fibres (Rosen and Sj61und 1973). As a matter of fact, in our experiments we have been able to dis- tinguish a different threshold between two effects and not a difference in the threshold of Ia and Ib fibres. The threshold of Ib effects reflects both the threshold of Ib fibres and that of Ib interneu- rones, whereas there are no interneurone in the facilitatory monosynaptic Ia pathway.

Surprisingly, the increase in firing probability following stimulation of heteronymous nerves was always greater than that produced by stimulation of the musculo-cutaneous nerve. This does not nec- essarily mean, however, that the heteronymous connections are more powerful than the homony- mous ones. In fact, the well-known ease in evoking a biceps tendon reflex in man argues in favour of a very efficient homonymous Ia linkage. An al- ternative explanation for the predominance of the heteronymous peak in the p.s.t.h, could be that while the heteronymous Ia afferents contained in median and radial trunks are activated in full, part of the homonymous Ia fibres may escape activa- tion by the conditioning stimulus because the mus- culo-cutaneous nerve is already branched when it runs under the electrodes.

2. Synaptic linkage

The p.s.t.h, experiments allow study of the precise latency of the effect. After calculation of the effer- ent conduction time, the latency of the onset of the heteronymous facilitation was found within the range of the homonymous Ia facilitation.

Even though oligosynaptic facilitatory Ia path- ways such as those described in the cat by Jan- kowska et al. (1981b) may contribute to the later

476

Table 2. Comparison is drawn between the pattern of projections of group I afferents from forearm muscles to motoneurones supplying biceps and triceps brachii muscles in man, monkey and cat. + : presence of excitatory connections; - : presence of inhibitory connections; @: absence of excitatory and inhibitory connections in man; �9 absence of excitatory connections in cat and monkey; ND: no data available

Ia fibres coming from MNs

Man Monkey Cat

Biceps Triceps Biceps Triceps Biceps Triceps

Muscles acting on digits innervated C) (5) by the median nerve (ex : FDC)

Muscles acting on the wrist and innervated + - by the median nerve (ex: FCR, pronator teres)

Muscles acting on digits and innervated G G by the radial nerve (ex : EDC)

ECR (radial nerve) + -

Muscles acting on digits or on the wrist C) Q) innervated by the ulnar nerve

+ ND �9 �9 un-identified fibres

contained ND § from pronators § from FCR in the median nerve

ND ND o o

+ ND + o

ND ND o �9

par t of the he te ronymous facilitation, the early par t is very p robab ly monosynap t i c in origin.

The latency o f the onset o f the transjoint inhibi- t ion was found to be within the range o f the recip- rocal inhibit ion between biceps and triceps brachii. The dura t ion o f the transjoint inhibi t ion found in p.s.t.h, experiments (see Fig. 6F, H) is longer than that o f the reciprocal Ia inhibit ion described with a similar technique by Mao et al. in 1984 (see their Fig. 4) in a tibialis anter ior m o t o r unit. To exclude the possibility that recurrent inhibit ion m ay con- t r ibute to this t ransjoint inhibi t ion some experi- ments were per formed in which it was carefully verified - with an averaging technique that the condi t ioning stimuli did no t evoke any M or H responses in any Of the muscles innervated by the median or radial nerves. Under such condit ions, the transjoint inhibit ion lasted between 4 and 8 ms, whereas the reciprocal Ia inhibit ion described by Mao et al. (1984) between tibialis anter ior and so- leus lasted 5 ms with a 1 x M T condi t ioning stimu- lus intensity and the one between triceps and biceps brachii less than 4 ms (unpublished results). The non reciprocal Ia inhibit ion described by Jankows- ka et al. (1981 a) in the cat may therefore contr ib- ute to the later par t of the transjoint inhibition.

3. Comparison of the distribution of group I fibres in the man, monkey and cat a) Comparison of the distribution of la excitation in the upper limb in man, monkey and cat. Table 2 summarizes our results concerning the h u m an up- per limb, the distr ibution o f monosynap t i c Ia exci- ta t ion in the forel imb o f the mon k ey (N. Fritz,

M. Illert, F. Kolb, R. Lemon, E. Wiedemann and T. Yamaguchi unpubl ished results) and the data obta ined by N. Fritz, M. Illert, S. de la Motte , P. Reech and P. Saggau in the cat (unpublished results). Only monosynap t i c Ia connect ions may be compared since only the latter are available in animals. As far as the biceps m o toneu rone pool is concerned there are no striking differences be- tween species except that in man Ia afferents f rom F C R m ay contr ibute to the facili tation of the bi- ceps m o t o n e u r o n e pool, a connect ion which is al- most absent in cat. In the case o f the triceps moto- neurones, no data are available in the monkey and the differences between cat and man again concern the project ions f rom FCR. While exci ta tory Ia connect ions f rom the F C R were found in the cat, we could not demons t ra te any facil i tatory effect f rom Ia afferents in the median nerve onto triceps motoneurones . In our experiments Ia fibres o f the median nerve where shown to produce short la- tency inhibit ion of triceps motoneurones . Our technique did not allow, however, to discern f rom which muscles this effect originated.

b) Comparison of the distribution of group I afferent between upper and lower limbs in man. The compar- ison between the results obta ined here in the hu- man upper limb and by Pierrot-Deseil l igny et al. ( /981) in the human lower limb revealed two main differences. 1) In the upper limb, Ia fibres originat- ing f rom flexor (and/or pronators) and extensor muscles o f the forearm have similar project ions onto biceps (or triceps) brachii motoneurones . Such projections were not found in the correspond-

477

ing situation in the lower limb. 2) The magnitude of the first facilitatory or inhibitory effects induced by the stimulation of forearm group I fibres onto motoneurone pool supplying muscles acting at el- bow is much greater than that found in the corre- sponding situations in the lower limb, a feature which may reflect a different strength of the affer- ent connections. The alternative explanation i.e. that the excitability of the monosynaptic reflex arc is higher in the upper limb than in the lower limb may be ruled out taking into account that the am- plitude of the monosynaptic reflexes are not greater in the upper limb.

4. Functional significance

The connections found in the lower limb have been interpreted by Pierrot-Deseilligny et al. (1981) in relation with the requirements of bipedal locomo- tion and it is tempting to interpret the results ob- tained in the upper limb in relation with the manip- ulation capacity of the hand. Carrying is obviously a function of the human arm, but to set the hand in a position allowing its use for explorating move- ments or visomotor control tasks as during eating, drawing or other kinds of manual activity is cer- tainly also a human specificity. When the arms are used in such aiming movements, the elbows are more often semiflexed, whatever the wrist posi- tion, and excitation connections between Ia fibres originating from wrist muscles onto biceps moto- neurones probably facilitate this arm posture. It should also be remembered that in spastic patients with upper motoneurone disease the voluntary contraction is often restricted to syncinetic con- tractions, with lifting of the arm and flexion of the elbow, whatever the wrist position. Finally, the discrepancies of group I afferent patterns between human upper and lower limbs suggest that the widespread group I connections in man are not vestigial, but have been subjected to phylogenetic adaptation.

Acknowledgements. The authors wish to express their gratitude to Professors Fausto Baldissera and Emmanuel Pierrot-Deseil- ligny for reading and commenting upon the manuscript. Our thanks are also due to Annie Rigaudie and Mich61e Dodo for excellent technical assistance, and to David MacGregor for scrutinizing the English. This work was supported by grants from the Pierre and Marie Curie University (Paris VI), INSERM (866014), IRME, and ETP (Tw 86/57).

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Received February 20, 1989 / Accepted August 9, 1989