simple reaction-time situation, and randomly with the right or left foot in the choice

Transcription

1 J. Phy8iol. (1984), 347, pp With 7 text-figures Printed in Great Britain RELATION BETWEEN THE SPECIFIC H REFLEX FACILITATION PRECEDING A VOLUNTARY MOVEMENT AND MOVEMENT PARAMETERS IN MAN BY A. EICHENBERGER AND D. G. RtYEGG From the Institute of Physiology, University of Fribourg, Rue du Musee, CH-1700 Fribourg, Switzerland (Received 30 March 1983) SUMMARY 1. In a reaction-time situation, the monosynaptic spinal reflex (H reflex) is facilitated before the onset of an electromyographic (e.m.g.) response. The aim of the present investigation was to study aspects of this facilitation Human subjects were required to perform isometric plantarflexions of the foot in response to a visual stimulus. The movement was always on the same side in the simple reaction-time situation, and randomly with the right or left foot in the choice reaction-time situation. Stimuli to evoke H reflexes were applied bilaterally ms after the onset of the visual stimulus. Pre-motor time, i.e. the interval between the onset of the visual stimulus and the e.m.g. response, and reaction time, i.e. the interval between the onset of the visual stimulus and the response on the torque recording, were computed. 3. In both reaction-time situations, there was a significant facilitation of the ipsilateral H reflex ms before e.m.g. onset and, in some subjects, a small facilitation of the contralateral H reflex. The specific facilitation, i.e. the difference between the facilitation on the ipsi- and contralateral side relative to the movement, was not significantly different on the right and left side. 4. Pre-motor time was divided into the interval from the light onset until the onset of the specific facilitation, and the interval from the onset of the facilitation until the onset of the voluntary response. Both intervals increased, and the slope and the amplitude of the facilitation decreased with increasing pre-motor time and reaction time. 5. The specificity of the H reflex facilitation in a choice reaction-time situation implies that the interval from light onset until the onset of the facilitation includes stimulus identification and response selection, and the interval from the onset of the facilitation until the e.m.g. response preparation of the motor system for the required movement. 6. The present results suggest that the specific facilitation of the H reflex before a movement is caused by removal of presynaptic inhibition at I a terminals or by activation of interneurones intercalated in polysynaptic components of the H reflex rather than by a subthreshold activation of motoneurones. 18 PHY 347

2 546 A. EICHENBERGER AND D. G. RUEGG INTRODUCTION Information processing in the sensorimotor system in reaction-time (r.t.) situations has been studied by recording evoked potentials with specific positive and negative variations which could be attributed to different steps of sensory and motor processing (Callaway, Tueting & Koslow, 1978). Similarly, the activity of neurones in different areas of the central nervous system has been related to sensory stimuli and voluntary movements (Evarts, 1966; Thach, 1975). In another line ofexperiments, spinal reflexes have been studied during r.t. The monosynaptic spinal reflex (H reflex) is facilitated about 80 ms before the onset of a movement in the same muscle (Gottlieb, Agarwal & Stark, 1970; Coquery & Coulmance, 1971; Pierrot-Deseilligny, Lacert & Cathala, 1971; Michie, Clarke, Sinden & Glue, 1976; Kots, 1977). The origin of this facilitation has remained unclear. An hypothesis put forward by Pierrot- Deseilligny et al. (1971) suggests that the facilitation of the H reflex is due to a removal of presynaptic inhibition acting on I a terminals. However, there are also indications that it reflects a subthreshold input to the motoneurones before e.m.g. activity (Porter & Muir, 1971). The aim of the present investigation was to characterii-ethis facilitation in more detail and to obtain some indications about its origin from these results. The paper reports in particular the specificity and right-left symmetry ofthe H reflex facilitation and its relation to r.t., movement amplitude and duration. A preliminary account of some of the results has already been presented (Eichenberger & Riiegg, 1983). METHODS Subject and material The experiments were performed on one healthy female and three healthy male subjects years old, with the consent and understanding of each of them. They were seated in a comfortable modified car chair with arm and head rests. The angle at the knee was adjusted to 1200, the angle of the foot to 900. Each foot was resting on a plate which was fixed in such a way that the torque produced at the ankle could be measured isometrically with a metal ring on which strain gauges were mounted in a bridge configuration. The electromyographic (e.m.g.) activity of the soleus muscle was recorded with bipolar surface electrodes 3 cm apart, the proximal being 2 cm distal to the insertion of the gastrocnemius muscle on the Achilles tendon. Transcutaneous electrical stimuli to elicit H reflexes were delivered by a modified Simon electrode (Simon, 1962) positioned in the popliteal fossa. This electrode allowed an easy adjustment of the site of stimulation as well as a rigid fixation of the electrode. The whole experimental set-up conformed with the standards described by Desmedt (1973). The visual stimulus to initiate the trials was a light emitting diode of 4 med at 1 m distance. The data from the experiments were recorded on-line with an HP-21MX computer system. The following channels were low-pass filtered (1 khz) and fed into an A/D-converter (sampling rate: 3 khz/channel): (1) light stimulus, (2) stimulus to evoke H reflexes, (3) torque signal from the right foot, (4) torque signal from the left foot, (5) e.m.g. of the right and (6) e.m.g. ofthe left soleus muscle. The data were saved on a hard disk from which they were accessed off-line in order to measure the latency of the movement on the torque and e.m.g. signal, the movement amplitude and movement time. H reflex amplitudes and movement parameters were saved on disk files for later processing whereas the original digitized data were transferred to magnetic tape. Experimental procedure The subjects were tested in two r.t. situations, in both of which they were instructed to carry out a plantarflexion of the foot as quickly as possible. In the simple r.t. situation, the subject always

3 PRE-MO VEMENT H REFLEX FACILITATION 547 flexed the same foot following the onset of the light during the whole session. In the choice r.t. situation, the subject moved the right foot at the onset of a green light and the left foot at the onset of a red light. The green and red lights were turned on in a pseudo-random sequence both with a probability of P = 0-5. The duration of the H reflex stimulus was 1 ms and the intensity (2-5 ma) was adjusted such that, under control conditions, the H reflex was half the amplitude of the maximum reflex which could be elicited. Trials consisted of control H reflexes on both sides which were followed by the light stimulus which conditioned the voluntary movement. The interval between control H reflex and light stimulus varied randomly between 10 and 14 s. The intervals between onset of light and the stimulus to elicit test H reflexes initially covered a range between 40 and 400 ms in steps of 40 ms. In later sessions when the modulation of the H reflex was established, intervals were used which tended to give more data about the H reflex facilitation in the interval ms before movement initiation. The intervals within a session were arranged in a pseudo-random order. A recording session consisted usually of twenty trials in the simple r.t. situation and of forty trials in the choice r.t. situation. Three sessions were recorded in a sequence, two in the simple r.t. situation (right and left side) and one in the choice r.t. situation. The sequence of the three sessions was random in order to control for possible effects of fatigue. Anoly8i8 of data The size of the H reflexes on the e.m.g. recordings was computed on-line during the recording sessions: it was operationally defined as the difference between the maximum and minimum value within a time template extending from 25 to 50 ms after stimulus onset. Pre-motor time (p.m.t.), i.e. the interval between the onset of the light and the onset of the e.mg. response, was measured visually from a display of the rectified e.m.g. record. Since no background activity was present the beginning of the first discharges of motor units was taken as the onset of the response. This method was strictly applied, even when reflex discharges and the accompanying silent period interacted with the voluntary movement. In order to measure r.t., i.e. the interval between the onset of the light and a response on the torque signal, a computer algorithm was developed. If the contraction elicited by the H reflex was superimposed on the voluntary plantarflexion the undisturbed voluntary movement was estimated by an interpolation technique. The time course of the torque signal during the interaction of the H reflex ( ms after the H reflex stimulus) was computed by a fifth-order polynomial which was fitted through fifty original data points (interval 1 ms) on either side of the interval. The points were weighted by a triangular function which was 1 at the point closest to the interval and reached 0 at the most distant point. Occasionally, negative pressure values (0 = the pressure without movement) were interpolated when the movement happened to start during the interval. The pressure was then adjusted to zero till the torque was minimum and a new interpolation was made over the remaining interval. The performance of this technique was inspected visually and the estimated segments corresponded well with the corresponding segments of unperturbed movements. R.t.s were then computed on the rectified torque records using a digital filtering technique which was based on the least-squares fit between a template and the records (Riiegg & Eichenberger, 1983). Movement amplitude, the difference between the torque before the movement and the maximum torque during the movement, and movement time, the interval from the onset of the movement (end of p.m.t.) until the maximum torque was reached, were computed from the torque records. A trial was discarded (1) if both legs moved (since only minor movements on the control side increased the size of the control H reflex size) or (2) if the subject was not attentive and r.t.s were exceedingly long or (3) if the difference between r.t. and p.m.t. happened to be in one of the tail ends (5 % on each side) of the distribution of these differences (the distribution was computed for each subject in each r.t. situation). Test H reflexes which were elicited during r.t. were normalized in relation to the average of the control reflexes. An H reflex size of 100% thus corresponded to a test reflex which was as large as the control reflex. When the time course of the H reflex modulation was plotted, the reference of time was either the onset of the light stimulus, the end of p.m.t. or the end of r.t. A comparison of the different presentations indicated to which reference the modulation was time-locked and enabled us to estimate errors introduced by computing p.m.t. and r.t. These relations were presented with two graphical methods. (1) The time axis was divided into intervals ofequal duration. The average reflex size and the confidence limits (P = 005) were computed within each interval. In contrast to the 18-2

4 548 A. EICHENBERGER AND D. G. R(JEGG s.e. of mean, the confidence limits are independent of the sample size which was different from interval to interval. (2) A smooth curve was fitted through the H reflex values Xi in order to approximate the time course of the H reflex modulation. The curve is given by the values Y(n) (n = 1, 2,...N) and the M data points by Xi(ti) (i = 1, 2,..M) where n and tj represent time in multiples of the sampling interval. The data points Xi were convoluted with a triangular weighing function W: where M T, Xi(ti) W(n-tj) Y(n) = oo z W(n-ti) i-1 W(j) = AIi for Ij A otherwise W(j) = 0. The sampling interval was 1 ms and A was set to 50. In order to study the relation between r.t.s and the size of the H reflex facilitation, r.t.s were arranged according to their duration and then divided into four groups of about equal size (group sizes were not equal since p.m.t.s of equal duration were attributed to the same group and p.m.t.s of equal duration occurred rather often with a time resolution of 5-m*{ RESULTS H reflex facilitation before a movement and its specificity Subjects were instructed to perform plantarflexions of their foot in a simple r.t. situation. The posterior tibial nerve was stimulated at different intervals from the onset of the light stimulus in order to elicit an H reflex. Each trial was preceded by a control H reflex at variable interval. The test H reflexes were normalized in relation to the average control H reflex. The recordings from a typical trial are shown in Fig. 1. Fig. 1 A represents the light stimulus and Fig. 1 B the stimulus to elicit the test H reflex. The interval between onset of the light and H reflex stimulus in this trial was 200 ms. The muscle contraction was recorded by torque (Fig. 1 D and E) and e.m.g. signals (Fig. 1 C and F) which, in this instance, were contaminated by the contraction produced by the H reflex. Special care was taken, and different methods were used, to determine the latencies ofthe voluntary movement on the e.m.g. (p.m.t.) and on the torque signals (r.t.). The pointed line in Fig. 1 D represents the interpolated undisturbed voluntary movement (see Methods) which has been used to measure p.m.t. The relative size of the H reflex referenced to the onset of the light was computed in the simple r.t. situation. The H reflex of the right leg which the subject moved was facilitated (continuous line, Fig. 2A) whereas on the left (control) side no significant changes occurred. The facilitation on the right side was significant at intervals longer than 160 ms, as indicated by the absence of overlaps of the confidence limits. A mean p.m.t. of 256 ms implies that the facilitation of the H reflex started before any movement-related e.m.g. changes. The facilitation in a second subject (Fig. 2B) was about equal (about 50%) to that in the first (Fig. 2A) but, in contrast to the first subject, there was also a facilitation on the control side. This facilitation, which was assumed to be unspecific, was in this subject the largest of

5 PRE-MOVEMENT H REFLEX FACILITATION 549 AJ, / C I P.m.t. N, M a. R.t. M t. D-- E F I'll, 600 Time (ms) Fig. 1. Voluntary plantarflexion of the right foot preceded by a test H reflex. A, light stimulus. B, H reflex stimulus applied bilaterally. C, e.m.g. recording from the right foot. The first synchronous response is the H reflex which is followed by the voluntary movement. Pre-motor time (p.m.t.) is defined as the interval between the onset of the light stimulus and the e.m.g. response. D, isometric record of the torque exerted by the right foot. The early reflex response is superimposed on the voluntary response. The dashed line represents the interpolated segment of the voluntary contraction (see Methods). Reaction time (r.t.) was defined with this interpolated signal. Movement time (m.t.) is the interval between onset and maximal amplitude (m.a.) of the movement. E, isometric recording of the torque of the left foot with the mechanical reflex response. F, H reflex on the left e.m.g. recording. The H reflex on the right side is facilitated in relation to the left-sided reflex. Abscissa: time (ms) after onset of the light stimulus. Ordinate: arbitrary units (A, B), 700 1sV (C, F), 10 Nm (D, E) A Subject A B Subject B I Time (ms) Fig. 2. Specificity of the H reflex facilitation. An unspecific facilitation (dashed line) is absent in subject A (A), while it reached significant values in subject B (B). The specific facilitation (continuous line) was significant in both subjects. Abscissa: time (ms) after onset of light stimulus. Ordinate: size ofthe conditioned H reflex as % ofthe unconditioned H reflex size. Bars indicate confidence limits (P = 0-05).

6 550 A. EICHENBERGER AND D. G. RUEGG all subjects tested. The difference between control and test sides which represents the specific part of the facilitation remained significant, however. All subjects thus had a significant specific facilitation of the H reflex which was confined to the leg that was involved in the movement, and which started before any detectable e.m.g. activation. These results were confirmed with data from the choice r.t. situation (not illustrated). x 200-A Right leg B Left leg 0) 50 cc Time (ms) Fig. 3. Symmetry of the H reflex facilitation in the choice r.t. experiment. The specific facilitation (continuous line) of this subject was statistically significant on the right (A) and left (B) side. Differences were non-significant. Therefore, resut from the right and left side were pooled in the subsequent Figures. Abscissa and ordinate, see Fig. 2. Bars indicate confidence limits (P = 0-05). Symmetry of the H reflex facilitation The H reflex modulations shown in Fig. 2 were from right-handed subjects who performed plantarflexions of the right foot in the simple r.t. situation. The facilitation in both sides was compared in the choice r.t. situation in which the subject had to extend the right and the left ankle in a pseudo-random sequence. In Fig. 3, which was obtained from one subject, the continuous lines represent H reflexes from the side where movements were carried out, and the interrupted lines represent reflexes from the control side obtained during the same session. The specific facilitation was larger on the right (Fig. 3A) than on the left (Fig. 3B) side but it reached a significant level on both sides as indicated by the confidence limits (P = 0 05) at a latency of about 200 ms. The experimental data of the other subjects confirmed the significance of a specific facilitation on both legs in the choice as well as in the simple r.t. situation (not illustrated). The insignificant differences between the facilitation on the right and left side could not be attributed to the right or left handedness of these subjects. The specificity and symmetry of the H reflex facilitation enabled the presentation of further results to be simplified. The difference between H reflex sizes on the test and control sides provided the specific portion of the facilitation which was averaged across the right and left sides and, in addition, across all subjects unless otherwise specified (there were no significant differences of the specific facilitation between subjects). Dependence of the H reflex facilitation on p.m.t. and r.t. The facilitatory phases of the H reflex in Figs. 2 and 3 were obtained from H reflexes which were associated with movements carried out at short as well as long r.t.s. A

7 PRE-MO VEMENT H REFLEX FACILITATION 551 more detailed analysis should disclose if parameters of the facilitation depend on p.m.t. and r.t. The results from the choice r.t. situation were studied since the variability of r.t.s was larger in the choice than that in the simple r.t. situation. On the basis of their duration, the pooled p.m.t.s and r.t.s of all four subjects were arranged into four groups, each of which contained about the same number of members A X _ I -60. ~~~~B ' 80- o Time (ms) Fig. 4. Specific H reflex facilitation in the choice r.t. task for four p.m.t. classes (A-D). Pooled data from four subjects. A, median p.m.t. 240 ms; B, 270 ms; C, 310 ms; D, 380 ms. I. (the latency of the facilitation) increased and the slope and amplitude of the facilitation decreased with increasing p.m.t. Differences between relations A, B, C and D are significant as can be seen by the confidence limits (P = 0-05). Abscissa: time (ms) after light stimulus. Ordinate: size of the specific H reflex facilitation as % of the average control H reflex. The specific facilitation of the H reflex for each class (based on p.m.t.s) was computed by relating the occurrence of the H reflexes to the onset of the light stimulus (Fig. 4). The facilitatory phase which was obvious in all four classes tended to become smaller and less steep with longer p.m.t.s and its latency was delayed at long p.m.t.s. The differences between the classes were significant as indicated by the confidence limits (P = 0 05). In a 'bar' presentation, time resolution is limited to the width of the bars (30 ms) and the phase of the bars affects the quantitative aspects of the relation. Therefore, an additional presentation which is based on a digital smoothing algorithm was added. This improved the time resolution by 1 ms but, on the other hand, no techniques were available to describe the statistical significance of the results presented in this manner. The data presented in Fig. 4 were thus digitally filtered and redrawn in Fig. 5A which reveals more details of the relations. For short p.m.t.s (median 240 ms) the size of the H reflex stayed at control values until about 150 ms after the onset of the light stimulus (origin of the time axis) and for long p.m.t.s (median 380 ms) until

8 552 A. EICHENBERGER AND D. G. RCErG A 'A ms 50_ 250/ B Fig. 5. Specific H reflex facilitation as a function of p.m.t. (A) and r.t. (B). Time reference: onset of light stimulus. Both relations, as Fig. 4, display an increase of I, and a decrease of the slope and amplitude of the facilitation with increasing latencies (p.m.t. and r.t.). X-axis: time after onset of light stimulus. Y-axis: size of the specific H reflex facilitation as % of the average control H reflex. Z-axis: p.m.t. (ms) (A) and r.t. (ms) (B). % A % ~~~~~~ S>1O Oms Fig. 6. Specific H reflex facilitation as a function of p.m.t. (A) and r.t. (B). Time reference: onset of e.m.g. (p.m.t.) in A and onset of torque response (r.t.) in B. Both relations illustrate an increase of 12 (interval between the onset of the facilitation and the e.m.g. response), and a decrease of the slope and the amplitude of the facilitation with increasing p.m.t. and r.t. X, Y and Z-axis as in Fig. 5. about 200 ms. As in Fig. 4, the slope of the facilitation was steeper and reached higher amplitudes for short p.m.t.s than for long ones. These results might be affected by two errors. (1) The population of p.m.t.s was divided into classes which joined each other. Almost equal r.t.s are partly attributed to neighbouring classes which could smear the relation between p.m.t.s and H reflex facilitation. (2) The determination ofp.m.t.s and r.t.s could be contaminated by errors induced by the interference of the H reflexes with the voluntary movement. Errors should, however, be very different for p.m.t.s and r.t.s since the techniques to estimate p.m.t.s and r.t.s were independent of each other. In order to estimate the importance of these errors, the size of the H reflexes has been plotted as being time-locked to the light onset (Fig. 5) as well as to the movement latencies (Fig. 6) and both relations have been calculated on the basis of a p.m.t. and r.t. classification. Some parameters of the curves in the two Figures were estimated

9 PRE-MO VEMENT H REFLEX FACILITATION visually and listed in Table 1. The slope of the facilitatory phase was approximated by the gradient of a straight line, drawn by eye through the rising portion of the facilitation. The onset of the facilitation was defined by the intersection of this straight line and the base line (0%). The interval between the onset of the light stimulus and the facilitation was measured directly from Fig. 5 and it was called I,. TABLE 1. Parameters of the H reflex facilitation as a function of p.m.t. and r.t. Data were aligned by the light onset in A and by the end of p.m.t. (left columns) and r.t. (right columns) in B. P.m.t.s and r.t.s were classified according to their duration. The average movement latency, 11, Is, the slope and the amplitude of the facilitation are listed (on the basis of p.m.t.s: left columns; on the basis of r.t.s: right columns). All values except the average latencies were obtained from Figs. 5 and 6 A Class 1 Class 2 Class 3 Class 4 P.m.t. R.t. P.m.t. R.t. P.m.t. R.t. P.m.t. R.t. Latency (ms) I, (Ms) Slope (% ms-') 1' Amplitude (%) B Class 1 Class 2 Class 3 Class 4 P.m.t. R.t. P.m.t. R.t. P.m.t. R.t. P.M.t. R.t. Latency (ms) I2 (ms) Slope (% ms-1) Amplitude (%) The term I2, which was defined as the interval between the onset of the facilitation and onset of e.m.g. activity, was obtained directly from Fig. 6A. The corresponding interval measured from Fig. 6B was corrected for the difference between median p.m.t.s and r.t.s. In movements which were not perturbed by H reflexes, r.t.s were about 50 ms longer than p.m.t.s when the same techniques as in the present report were used for their determination (Riiegg & Eichenberger, 1983). The median p.m.t.s and r.t.s of the four classes mentioned above (first row of Table 1) differed by less than 50 ms and were even almost equal for class 1. This distortion of the relation between p.m.t.s and r.t.s was due to the interaction by the H reflex stimuli. The durations of I, (second row of Table 1 A) and I (second row of Table 1 B) were similar when they were based on a classification ofp.m.t.s (left columns) or r.t.s (right columns). Important differences in the slope (third row of Table 1) and the amplitude of the facilitation (fourth row of Table 1) were obvious just for class 1. The means of the values based on the classification of p.m.t.s and r.t.s as listed in Table 1 were computed and plotted on Fig. 7. The values of I, and I2 increased steadily with lengthening p.m.t.s (Fig. 7A). The increase of both was about equal at short p.m.t.s and I, tended to increase progressively; I2, however, tended to level out at long p.m.t.s. As already seen from Figs. 5 and 6 and Table 1, the slope and the amplitude of the H reflex were larger at short than at long p.m.t.s (Fig. 7B). By definition, I, and I2 should sum to give p.m.t. Since I, and I2 were measured from different relationships (Fig. 5 and Fig. 6 resp.), the accuracy of the data can be

10 554 A. EICHENBERGER AND D. G. RCEGG estimated by the difference between the median p.m.t.s and the sum of I and I2. The difference was surprisingly low (between -1 and 5 Ms) which points to a good reliability of the results. Relation between the size of the H reflex facilitation and movement time and amplitude Let us suppose that a subject was carrying out two movements at the same latency but with an H reflex facilitation which was larger in the first than in the second movement. The question we wanted to answer was whether the expected amplitude, duration and speed of the two movements would be the same or different. A B CE , l _. _ Time (ms) Time (ms) Fig. 7. The interval I, (El) and the interval I2 (0) as a function of p.m.t. in A. The slope (@) and the amplitude (A) of the facilitation as a function of p.m.t. in B. The data were obtained from Figs. 5 and 6. Abscissa: p.m.t. in ms; ordinate: duration of I, and I2 in ms (A), slope of the facilitation in % ms-1 (left axis in B), and amplitude of the facilitation in % (right axis in B). P.m.t.s were divided into four classes according to duration and, for each class, a mean facilitatory phase was computed as shown in Fig. 6. The deviation of the size of H reflex from this average curve was related to the movement amplitude and duration for each trial and a regression line had been fitted through the points of each relation. In one of the subjects, the regression coefficients of the relation H reflex - movement amplitude and H reflex -movement duration were significant (P < 001 and P < 005). These relations from the data of the simple r.t. situation were confirmed by those of the choice r.t. situation. There was no relationship between the H reflex facilitation and the movement speed. We concluded from these results that this particular subject carried out strong movements without changing speed when the preceding H reflex facilitation was pronounced. The relationships tended to be similar in the second subject, but in the third subject no relationship between H reflex and movement parameters was detected. In the fourth subject the relation between H reflex facilitation and movement amplitude was negative. This finding made it clear that the relation between H reflex size and movement parameters was not the same for all subjects, but that there were individual differences which might be due to different movement strategies. DISCUSSION H reflex facilitation in different experimental conditions Several authors (Gottlieb et al. 1970; Pierrot-Deseilligny et al. 1971; Michie et al. 1976; Kots, 1977) have described that, in a r.t. situation, the monosynaptic reflex in the leg which will move, is facilitated ms before the onset of a voluntary e.m.g. response. A small facilitation of the H reflex can also occur in the contralateral leg or an arm (Pierrot-Deseilligny et al. 1971; Pierrot-Deseilligny & Lacert, 1973).

11 PRE-MO VEMENT H REFLEX FACILITATION We confirmed the existence of a non-specific facilitation in three subjects, although in one athletic subject the H reflex was not facilitated but slightly inhibited on the side contralateral to the movement. Similar to this non-specific facilitation, Luschei, Saslow & Glickstein (1967) recorded small muscle potentials at a latency of 20-S50 ms in a r.t. situation. This short latency activity was interpreted as a startle reaction. The above-mentioned results have been obtained in simple r.t. situations in which the subject could prepare himself for the movement to be carried out before the go-signal. We have extended these findings to a choice r.t. situation and agree qualitatively with Michie, Clark, Sinden & Glue (1975) about the presence of a specific H reflex facilitation in the leg which will be moved. The conclusion can be drawn from this result that the subject must have completed the decision concerning which limb he will move, at the moment of the onset of the facilitation. We were therefore able to divide p.m.t. into two intervals to which specific processes of movement initiation can be attributed. The interval I, from the onset of the light stimulus until the onset of the facilitation includes stimulus identification and response selection (Keele, 1973). We assume that, from 11 onwards, the selected motor programme is running and that, during the interval '2, from the onset of the facilitation until the end of p.m.t., the motor apparatus is pre -set for the execution of the required movement. The facilitation of the H reflex is an expression of this preparation. Since the facilitatory phases in the simple and the choice r.t. situation were similar we have extended the conclusion to include both r.t. situations. A simple r.t. can analogously be divided into a phase I, for information perception and retrieval from memory of the motor response, and a phase '2 during which the motor system is prepared for the movement. Estimation of '1 and '2 The determination of latencies of the e.m.g. and torque recordings was rendered difficult by interference of the H reflex. This problem was avoided by Blair-Thomas & Luschei (1975) who studied conditioned jaw movements in which r.t. is equal on both sides even during the presence of an unilateral H reflex stimulus. P.m.t.s were measured visually on the present records by the first motor unit discharges which were not related to the H reflex. P.m.t.s could have been modified if these discharges occurred shortly after the H reflex during the silent period (Paillard, 1955; Bouaziz, Bouaziz & Hugon, 1975). We did not try to correct for these influences but determined r.t.s in parallel with a technique which was independent of the p.m.t. definition. The computation of r.t.s on the torque signal was, however, complicated by the H reflex contraction. The time course of the voluntary contraction during the interference of the reflex was interpolated. R.t.s were then determined by the best fit between these rectified data and a template which included the contraction onset. Based on the same technique, the correlation between r.t.s and p.m.t.s varied in unperturbed movements between 0-96 and 0-98 (Ruegg & Eichenberger, 1983), and between 0-69 and 0-86 with interfering H reflexes as in the present investigation. Since the correlation was significantly lower in the perturbed than in the unperturbed movements, computations were made on the basis of r.t.s as well as p.m.t.s. The similar results for I,. '2, the amplitude and slope of the facilitation gained with the two techniques indicated that errors in the level of p.m.t. and r.t. determination did not falsify qualitatively the nature of the H reflex facilitation as described in this report. 555 Since one trial provides just one point on the facilitatory phase, it was necessary to pool the results of several trials or even several sessions in order to get its whole time course. This procedure rendered the interpretation of the results more difficult because, (1) p.m.t.s and r.t.s (and therefore also facilitatory phases) were different

12 556 A. EICHENBERGER AND D. G. RUEGG from trial to trial and because, (2) I, I2 and the slope of the facilitation could not be evaluated unequivocally since it was not known if they varied from trial to trial, assuming equal r.t.s. Their value computed from trials with short r.t.s (class 1) presumably corresponds to the true value since they are unlikely to vary at r.t.s close to the minimal r.t. At longer r.t.s, the slope of the facilitation was either less steep and I, and '2 were invariable, or the slope was as steep as for short r.t.s and '1 I2 were variable. Both possibilities would result in the same average facilitation. The first possibility seems more likely and it was taken as the basis for data processing and interpretation. In all these experiments, intersensory facilitation between the light and the H reflex stimulus took place, which led to a shortening of p.m.t., depending on the relative timing of the two stimuli (Riiegg, D. G. & Eichenberger, A., in preparation). Statistical facilitation (Raab, 1962) was proposed by Michie et al. (1976) to account for intersensory facilitation in a simple r.t. task. This implies that the time to detect the light or H reflex stimulus is randomly distributed and that the response is evoked as soon as either stimulus is detected. This mechanism can be excluded as an explanation for the present results since the subject cannot respond to the H reflex stimulus alone in a choice r.t. situation. An interpretation of the results by the alternative preparation enhancement model (Nickerson, 1973) would mean that mainly the later components of r.t. are shortened. We are unable to detect from the present results if I', '2 or both of them were affected by intersensory facilitation. Dependence of I2 on reaction time The question of whether the facilitation of the H reflex is temporally coupled to the onset of the light stimulus or to the onset of the e.m.g. response has never been dealt with in detail. Mitchie et al. (1976) found that the rise of the H reflex was more obviously linked to the e.m.g. onset than to the 'go' signal. In the same sense, Kots (1977) claimed that '2 had a duration of ms independent of r.t. It followed from our detailed investigation that 1, and '2 were increasing with r.t. and that '2 had the tendency to stay constant for long r.t.s. We therefore conclude that the H reflex facilitation is neither time-locked to the onset of the light nor to the onset of the e.m.g. response. Experimental evidence supports the proposition that attention which is correlated with r.t. (Eason, Harter & White, 1969) can be allocated to different information processing stages (Klein, 1976). This view is backed up by our finding that I, (which includes the decision making process) as well as I2 (which represents part of the preparation for the specific movement) are affected by attention. Origin of the H reflex facilitation Various evidence lends support to the hypothesis that the motor cortex or the cerebellum is the source of the facilitation of the H reflex. Neurones in the motor cortex (Evarts, 1966; Luschei, Garthwaite & Armstrong, 1971) and in the cerebellum (Thach, 1975) discharge ms before the e.m.g. onset. The facilitation disappears after lesioning the pyramidal tract of dogs which were conditioned to perform an instrumental avoidance reflex (loffe, 1973). The commonly advanced sites of reflex modulation are the a- and y-motoneurones. and

13 PRE-MO VEMENT H REFLEX FACILITATION However an H reflex can be modulated not only by changes of the afferent input and the excitability of the motoneurones but also by presynaptic inhibition of its afferent terminals or by activation of interneurones intercalated in polysynaptic components of the H reflex (Burke, McKeon & Skuse, 1981). The findings that the tendon reflex is facilitated in parallel to the H reflex before movement initiation (Coquery & Coulmance, 1971; Pierrot-Deseilligny & Lacert, 1973; Michie et al. 1976) and that, during voluntary movements, y-motoneurone activity does not precede a-motoneurone activity (Vallbo, 1971) make it unlikely that y-motoneurone activation is the cause of the H reflex facilitation. If it is assumed that the motor cortex is the origin of the facilitation, the hypothesis that a- motoneurones are activated before movement initiation is supported by anatomical (Porter & Hore, 1969) and electrophysiological (Porter & Muir, 1971; Fetz & Cheney, 1980) findings. On the other hand, Gottlieb et al. (1970) and Pierrot-Deseilligny & Lacert (1973) favoured the hypothesis that removal of presynaptic inhibition results in a facilitation of the H reflex before movement initiation. Experiments in anaesthetized cats have confirmed that stimulation of motor centres can reduce presynaptic inhibition at Ia terminals. Simulation of the motor, cortex -(Lundberg & Vyklicky, 1963) or the red nucleus (Hongo, Jankowska & Lundberg, 1972) inhibits transmission in the pathway mediating depolarization of Ia afferent terminals from Ia afferents. No evidence for or against a modulation of the H reflex by activation of interneurones intercalated in polysynaptic components of the H reflex (Watt, Stauffer, Taylor, Reinking & Stuart, 1976; Burke et al. 1981) is available. The present results point to a mechanism which is independent of motoneurones. If the facilitation reflects the beginning of excitatory input to the a-motoneurones which leads to the movement after summation during I2, one would expect parallel changes in the slope of the facilitation and the slope of the rising phase of the e.m.g. and torque signals. The slope of the voluntary movements was independent of r.t. in all subjects (not illustrated in the Results; supported by Requin, 1980) whereas the slope of the facilitation decreased consistently with increasing r.t. In addition, this hypothesis would require that, at the onset of the voluntary e.m.g. response, the amplitude of the facilitation is the same in all trials. It has been shown, however, that the facilitation decreased in size from short to long p.m.t.s. An alternative explanation of these findings would require an action on two separate motoneuronal pools which seems unlikely, since the size principle is obeyed if I a afferents are stimulated (Henneman, Somjen & Carpenter, 1965) as well as during voluntary movements (Desmedt & Godaux, 1977). The study was supported by the Swiss National Science Foundation (grant no ). We wish to express our gratitude to Dr T. Miles for many helpful comments on the manuscript. The skilful technical assistance of Ms E. Wild, Ms U. Rfiegg and Mr P. Hubscher is gratefully acknowledged. REFERENCES 557 BLAIR-THOMAS, C. & LuSCHEI, E. S. (1975). Increases in reflex excitability of motoneurones before a jaw-bite reaction-time response. J. Neurophysiol. 38, BoUAZIZ, A., BoUAZIZ, M. & HUGON, M. (1975). Modulation of soleus electromyogram during electrical stimulation of medial gastrocnemius nerve in man. Electromyogr. & clin. Neurophy8iol. 15,

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