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Facilitation of late reflexes in humans during the preparatory period of voluntary movement
176
Brain Research, 153 (1978) 176~-182 ((', Elsevier/North-HollandBiomedical Press
Facilitation of late reflexes in humans during the preparatory period of voluntary movement
KEITH C. HAYES and ALEX M. CLARKE Department of Kinesiology, University o]' Waterloo, Ontario, N2L 3Gl (Canada) arm Department of Psychology, University of Wollongong, New South Wales (Australia)
(Accepted March 30th, 1978)
Several recent studies have attempted to identify the roles of the spinal and supraspinal components of the human stretch reflex4,6-8,15--17, and the means by which the components are modulated 7,15,29. The postural demands at the time of perturbation (refs. 3, 4, 9, 15, 30), the environmental context e°, learning 4,15 and preparatory 'set '7.30 are all known to modify the amplitude of the normal muscular responses. The influence of prior instruction to the subject, where a preparatory 'set' with high probability of response appropriateness is established, has been shown to profoundly modify the amplitude of both the M I (spinal) and M2 (transcortical) responses7,1°, 11. Under these conditions, the intentional response of the subject to the perturbation may also merge with the late M3 reflex (involving the cerebellum), making the two responses indistinguishable 3°. Tanji and Evarts 28 recently demonstrated that neurons in monkey's sensorimotor cortex exhibit directionally specific changes of activity, according to 'set', during the preparatory period prior to overt muscular activity. These changes were observed after the appearance of a green or red light, indicating the instructional 'set' to either push or pull, but prior to the kinesthetic stimulus that signalled the moment to respond. In the present study H-reflexes and 'late reflexes"13, possibly corresponding to the M3 response, were recorded from human soleus muscles during the preparatory period of a voluntary response to a visual stimulus. The aim of the study was to identify any modulation of the supraspinal response occurring (a) during the foreperiod of a reaction time task, i.e. between the warning signal (WS) and reaction signal (RS), and (b) during the early stages of response execution, i.e. between RS and the voluntary response. It was reasoned that, following the WS, the subjects may'pre-set' the sensitivity, or gain, of the spinal and supraspinal reflexes prior to the overt response and possibly even before the RS. Ten healthy adults were tested while resting supine, with their head looking directly forward 12, and their right foot in contact with a force-transducing heel-plate. The RS was a small light emitting diode (3.5 mcd luminous intensity) that remained illuminated for 250 msec, and which was located 45 cm from the subject. A high pitched (2.5 kHz) warning tone (WS), of 100 msec duration, served to inform the subjects of
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Fig. I. H-reflex amplitudes and late reflex latencies during the foreperiod of a visual reaction time task. The vertical bars correspond to the standard error of the mean of the H-reflex amplitude and the numbers accompanying the late reflex latency values show the number of observations made. WS, warning signal; RS, reaction signal; ES, eliciting (H-reflex) stimulus.
an imminent RS and the foreperiod (WS-RS) was maintained constant at 1 sec in order to maximize expectancy of the response. H-reflexes were elicited at predetermined time intervals throughout both the WS-RS and RS-voluntary response periods. A Grass model $48 nerve stimulator, connected in series with a stimulus isolation unit (SIU5) and a constant current unit (CCU 1), generated the 1.5 msec square-wave pulses which were delivered to the posterior tibial nerve in the region of the popliteal fossa. A 5 m m diameter stimulating electrode was secured in a position capable of evoking a minimal H-reflex without a concomitant direct muscle response, and the dispersive electrode was a moist pad positioned over the patella. Two bipolar surface electrodes (silver, silver chloride), located over the dorsal midline of soleus, led off the evoked muscle action potentials to a preamplifier (Biocom model 2122 differential amplifier; response 3 dB down at 0.05 Hz and 10 kHz) prior to display and storage on a dual trace Hewlett Packard 1201A oscilloscope. Eliciting stimuli (ES) were administered at 12 intervals between WS and the voluntary response. When expressed in relation to the onset of the RS, these intervals (t) corresponded to --800, --600, --400, --200, --150, --100, --50, 0, + 50, + 100, + 150 and + 2 0 0 msec, respectively. In addition, there were 4 comparison conditions: (i) WS and RS but no ES; (ii) WS followed by an ES 1100 msec later (that is, 100 msec after the time at which the RS would usually have occurred); (iii) an ES alone; (iv) an ES alone while the subject maintained a mild isometric plantar flexion. These 16 different conditions were presented in random order in 5 blocks so that each subject
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Fig. 2. H-reflexes and late reflexes recorded during the foreperiod of a visual reaction time task (a-e) and during control conditions if-i). Upper traces show the electromyogram and lower traces the onset of the reaction light (a-f) or the isometric force record (h-i). The time base in all records is 100 msec. The WS-RS interval (see text) is indicated in records a-e. In records g and i the eliciting (H-reflex) stimulus (ES) was delivered while the subject maintained a mild isometric contraction. The late reflex appears as a discrete burst of action potentials 150-250 msec after the H-reflex, and occurs more frequently as the WS-RS interval is reduced. had a total of 80 trials in one experimental session. The trials were separated by variable intervals of at least 15 sec. H-reflex peak-to-peak amplitudes, during the foreperiod, are shown in Fig. J. The mean amplitude o f the H-reflexes elicited without either WS or RS (4.42 mV) was used as the control and corresponded to 25-30 ~ of the maximum H-reflex. The profile o f changes in the H-reflex amplitude, was similar to previous reports 5, 1s,19,21,22. A n early and short lasting period o f facilitation immediately followed the WS2Z,z3; therea6ter there was a reduction in amplitude of the m o n c s y n a p t i c response t h r o u g h o u t the foreperiod, with all values, except at t = - - 1 5 0 msec, slightly less than the control. This reduction in amplitude of the H-reflex has previously been attributed to presynaptic inhibition o f the Ia terminals, which constitutes an important part of the preparatory processes involved in the organization of a voluntary response ~2. After the RS there was an increase in amplitude o f the H-reflex, commencing at t = q-100 msec and continuing to increase until appearance of the voluntary response. H-reflex amplitudes at t = -q-100, + 150 and + 2 0 0 msec were all significantly greater
179 (P < 0.05) than the control value. It has previously been suggested that this increase in the amplitude of the monosynaptic response may be partly attributable to disinhibition of the presynaptic inhibition of la afferent terminals 19. A marked augmentation of the H-reflex was also evident when the ES was delivered while the subject maintained a mild isometric contraction of soleus but did not voluntarily respond to any RS. This effect, which is well documented9,13, most probably results from the subliminal facilitation of fringe motoneurons by the corticofugal input to the motoneuron pool. A large population of subliminal fringe motoneurons are still accessible to the la discharge evoked by the ES during a mild contraction. The 'silent period' which followed the H-reflex, in this condition, is also a well-established phenomenon 1. The mean amplitude for this condition (5.26 mV) was significantly greater (P < 0.05) than the ES-alone condition. The most important results of this study were that discrete bursts of asynchronous muscle activity were observed during the foreperiod in 8 of the subjects. In each case the discharges followed the H-reflex and appeared before the voluntary response. These bursts of activity are shown in Fig. 2. Their frequency of occurrence increased from 24 ~o to 36 ~,, as the RS-ES interval reduced from t -- --800 msec to t = - - 5 0 msec. A substantial increase in occurrence, from 22 ~ to 30 ~ ,was evident between t -- --400 msec and t ~ - - 2 0 0 msec. The latency of these late reflexes also reduced from 282.6 msec at t = --800 msec to 178.3 msec at t - - - 5 0 msec and at t = 0 were indistinguishable from the voluntary response (see Fig. 1). Occasionally, periodic discharges followed the late reflex (see Fig. 2a). In the condition where subjects maintained a mild isometric contraction in soleus, but were not required to voluntarily respond to a RS, the late reflex activity appeared consistently, in 8 of the subjects, with an overall frequency of occurrence of 62 ~ and a mean latency of 150.9 msec (S.D. -- 25.1 msec). This was similar to earlier reported values 13,e4, and is consistent with the view that modulation of late reflex amplitude, as well as the amplitude of the monosynaptic response, occurs according to the postural drive existing at the time of perturbationl,4,1a, 29. When the WS-ES interval of 1100 msec was examined, with no RS, the latency of the late reflex was 188.9 msec, and its frequency of occurrence was 40 ~ . Together these data indicate the high degree of expectancy associated with the preparatory 'set' in this condition. They also suggest a dissociation between the presetting of supraspinal reflex sensitivity and the voluntary response, as no voluntary response was forthcoming. The H-reflex amplitude in this condition was unaltered. Voluntary responses with a latency of 197.8 msec were recorded when the W S - R S interval was 1000 msec and no ES was delivered. When the ES was delivered during the foreperiod, the voluntary responses were significantly longer (P < 0.05), ranging between 243.2 msec at t -- --800 msec and 210.4 msec at t = - - 5 0 msec. The voluntary responses were also longer than the control (P < 0.05) when the ES was delivered after the RS, values of 212.9 msec at t -- + 5 0 msec, 246.6 msec at t ~ q-100 msec, 267.9 msec at t -I- 150 msec, and 259.9 msec at t -- ~-200 msec being recorded. The origins of the excitatory synaptic inputs that lead to the late reflex are of considerable interest. When the late reflex activity appears following an H-reflex super-
180 imposed upon a background isometric contraction there are 3 major sources of facilitation: (a) long loop reflexes evoked by the primary afferent discharge associated with the electrical stimulus 13; (b) primary afferent discharge from muscle spindles during the H-reflex twitch relaxation 2,25, and (c) rebound facilitation of motoneurons following the inhibitory postsynaptic potentials that produce the silent period 13. The posturat drive is apparently required to increase the sensitivity of the spinal and supraspinat reflexes, for without the contraction the late reflex is rarely seen in normal subjects 2~. The results of the present study show that the late reflexes may be elicited in normal subjects, without any postural drive, when the preparatory 'se( to respond serves to modulate the reflex sensitivity. Moreover, since the presumed presynaptic inhibition of Ia terminals maintained the H-reflex amplitude constant in the 600 msec prior to RS, the increased frequency of occurrence and shorter latencies of the late reflexes in this period would appear to be attributable to a progressively increased gain in the supraspinal pathway. The long latency of the late reflex provides some indication of the pathways involved. It is unlikely that a fast conducting transcortical pathway is used as the latency of the M2 response in the flexor hallucis longus muscle occurs between 75 and 90 msec following stimulation of the posterior tibial nerve 15. Responses with latencies between 85 and 1l0 msec appear in soleus when subjects are welt-practised at responding with a plantar flexion to an H-reflex stimulus (unpublished observations). It is more probable that the slower conducting M3 pathway, involving the cerebellum, mediates the response. The latency and time course of the late reflexes closely match the period of "intercurrent facilitation'2v evoked in soleus by a subthreshold conditioning stimulus ~a. Intercurrent facilitation in the H-reflex recovery curve has previously been ascribed to a supraspinal reflex 2v, thought to relay through the cerebellum 2v, but also involving lhe motor cortex 14. The longer latency of the late reflexes elicited during the foreperiod, when compared with the postural drive condition, may be the result of presynaptic blocking of the muscle spindle primary afferent discharge contribution. Also, the occasional appearance of periodic discharges following the late reflex is consonant with the interpretation of a preparatory elevation of gain of the supraspinal reflex. These oscillations are characteristic of an underdamped servosystem. In summary, evidence has been presented of an increased sensitivity of"the M3 or 'late reflex'13 in human subjects during the foreperiod of a visual reaction time task. The increased gain of the response, associated with a well-established preparatory 'set', may be related to the changes in cortical cell activity in monkeys reported by Tanji and Evarts 2s. The altered sensitivity of the reflexes appeared to be associated with the 'set' to respond, as opposed to the volitional response per se, as it was evident even when no RS or voluntary responses were present. The anticipatory presetting of reflex excitability, prior to the visual stimulus, may considered to be an important element in the internal representation of an impending movement 2°. This research was supported by grants from the National Research Council of Canada and from the University of Waterloo Research Council.
181 1 Agarwal, G. C., and Gottlieb, G. L., The muscle silent period and reciprocal inhibition in man, J. Neurol. Neurosurg. Psychiat., 35 (1972) 72-76. 2 Burg, D., Szumski, A. J., Struppler, A. and Velho, F., Afferent and efferent activation of human muscle receptors involved in reflex and voluntary contraction, Exp. Neurol., 41 (19733 754 768. 3 Clarke, A. M., Relationships between the electromyogram and the isometric reflex response under pre-strain conditions in normal human subjects, Nature (Lond.), 214 (1967) 1012 1013. 4 Conrad, B. and Aschoff, J., Effects of voluntary isometric and isotonic activity on late transcortical reflex component in normal subjects and hemiparetic patients, Electroenceph. elin. Neurophysiol., 42(1977) 107 116. 5 Coquery, J. M. et Coulmance, M., Variations d'amplitude des reflexes avant un mouvement vo luntaire, Physiol. Behav., 6 (19713 65-69. 6 Crago, P. E., Houk, J. C. and Hasan, Z., Regulatory actions of the human stretch reflex, J. Neurophysiol., 39 (19763 925-935. 7 Evarts, E. V. and Granit, R., Relations of reflexes and intended movements. In S. Homma (Ed.), Understanding the Stretch Reflex, Progr. Brain Res., Vol. 44, Elsevier, Amsterdam, 1976, pp. 1- 14. 8 Evarts, E. V. and Tanji, J., Reflex and intended responses in motor cortex pyramidal tract neurons of monkeys, J. Neurophysiol., 39 (1976) 1069-1080. 9 Gottlieb, G. L. and Agarwal, G. C., The effects of initial conditions of the Hoffmann Reflex, J. Neurol. Neurosurg. Psychiat., 34 (1970) 226 230. 10 Habgarth, K.-E., EMG studies of stretch reflex in man. In L. Widen (Ed.), Recent Advances in Clinical Neurophysiology, Electroenceph. clin. Neurophysiol., Suppl. 25, Elsevier, Amsterdam, 1967, pp. 74 79. 11 Hammond, P. H., The influence of prior instruction to the subject on an apparently involuntary neuromuscular response, J. Physiol. (Lond.), 132 (1956) 17P 18P. 12 Hayes, K. C. and Sullivan, J., Tonic neck reflex influence on tendon and Hoffmann reflexes in man, Eleetromyograph. olin. Neurophysiol., 16 (1976) 251-261. 13 Hayes, K. C. and Mcllwain, J. S., Late EMG responses in soleus following stimulation of the posterior tibial nerve. In Biomechanies, Vol. 6, University Park Press, Baltimore, 1977, in press. 14 Lachat, J. M., Rihegg, D. G. and Wiesendanger, M., Transcortical facilitation of the H-(monosynaptic)-reflex in monkeys, Experientia (Basel), 33 (1977) 781 (abstract). 15 Marsden, C. D. Merton, P. A. and Morton, H. B., Stretch reflex and servo action in a variety of muscles, J. Physiol. (Lond.), 259 (19763 531--560. 16 Melvill Jones, G. and Watt, D. G. D., Observations on the control of stepping and hopping movements in man, J. Physiol. (Lond.), 219 (1971) 709-727. 17 Milner-Brown, H. S., Stein, R. B. and Lee, R. G., Synchronization of human motor units : possible roles of exercise and supraspinal reflexes, Electroenceph. clin. Neurophysiol., 38 (19753 245 254. [ 8 Michie, P. T., Clarke, A. M., Sinden, J. D. and Glue, L. C. T., Reaction time and spinal excitability in a simple reaction time task, Physiol. Behav., 16 (1976) 311 315. 19 Michie, P. T., Clarke, A. M., Sinden, J. D. and Glue, L. C. T., Facilitation of Hoffmann reflexes prior to voluntary movement in a choice reaction time task, Appl. Neurophysiol., 38 (1976) 191-196. 20 Nashner, L. M., Adapting reflexes controlling the human posture, Exp. Brain Res., 26 (1976) 59 72. 21 Pailiard, J., Functional organization of afferent innervation of muscle studied in man by monosynaptic testing, Amer. J. phys. Med., 38 (1959) 239-247. 22 Requin, J., Some data on neurophysiological processes involved in the preparatory motor activity to reaction time performance. In Aeta Po'chologica, Vol. 30, Attention and PerJbrmance, 11, NorthHolland, Amsterdam, 1969, pp. 358-367. 23 Semjen, A., Bonnet, M. and Requin, J., Relation between the time-course of Hoffmann-reflexes and the foreperiod duration in a reaction time task, Physiol. Behav., 10 (1973) 1041-1050. 24 Stein, R. B. and Bawa, P., Reflex responses of human soleus muscle to small perturbations, J. Neurophysiol., 39 (1976) 1105 1116. 25 Szumski, A. J., Burg, D., Struppler, A. and Velho, F., Activity of muscle spindles during muscle twitch and clonus in normal and spastic human subjects, Electroeneeph. elin. Neurophysiol., 37 (1974) 589-597. 26 TS.botikov~t, H., Supraspinal influences on H-reflexes. in J. E. Desmedt (Ed.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 3, Karger, Basel, 1973, pp. 328-335. 27 TS.botfkovS_, H. and Sax, D., Conditioning of H-reflex by preceding sub-threshold H-reflex stimulus, Brain, 92 (1969) 203 212.
182 28 Tanji, J. and Evarts, E. V., Anticipatory activity of motor cortex neurons in relation to direction of an intended movement, J. Neurophysiol., 39 (1976) 1062-1068. 29 Tatton, W. G. and Lee, R. G., Evidence for abnormal long-loop reflexes in rigid Parkinsonian patients, Brain Research, 100 (1975) 671-676. 30 Thomas, J. S., Brown, J. and Lucier, G. E., Influence of task set on muscular responses to arm perturbations in normal subjects and Parkinson patients, Exp. Neurol., 55 (1977) 618-:628.
Brain Research, 153 (1978) 176~-182 ((', Elsevier/North-HollandBiomedical Press
Facilitation of late reflexes in humans during the preparatory period of voluntary movement
KEITH C. HAYES and ALEX M. CLARKE Department of Kinesiology, University o]' Waterloo, Ontario, N2L 3Gl (Canada) arm Department of Psychology, University of Wollongong, New South Wales (Australia)
(Accepted March 30th, 1978)
Several recent studies have attempted to identify the roles of the spinal and supraspinal components of the human stretch reflex4,6-8,15--17, and the means by which the components are modulated 7,15,29. The postural demands at the time of perturbation (refs. 3, 4, 9, 15, 30), the environmental context e°, learning 4,15 and preparatory 'set '7.30 are all known to modify the amplitude of the normal muscular responses. The influence of prior instruction to the subject, where a preparatory 'set' with high probability of response appropriateness is established, has been shown to profoundly modify the amplitude of both the M I (spinal) and M2 (transcortical) responses7,1°, 11. Under these conditions, the intentional response of the subject to the perturbation may also merge with the late M3 reflex (involving the cerebellum), making the two responses indistinguishable 3°. Tanji and Evarts 28 recently demonstrated that neurons in monkey's sensorimotor cortex exhibit directionally specific changes of activity, according to 'set', during the preparatory period prior to overt muscular activity. These changes were observed after the appearance of a green or red light, indicating the instructional 'set' to either push or pull, but prior to the kinesthetic stimulus that signalled the moment to respond. In the present study H-reflexes and 'late reflexes"13, possibly corresponding to the M3 response, were recorded from human soleus muscles during the preparatory period of a voluntary response to a visual stimulus. The aim of the study was to identify any modulation of the supraspinal response occurring (a) during the foreperiod of a reaction time task, i.e. between the warning signal (WS) and reaction signal (RS), and (b) during the early stages of response execution, i.e. between RS and the voluntary response. It was reasoned that, following the WS, the subjects may'pre-set' the sensitivity, or gain, of the spinal and supraspinal reflexes prior to the overt response and possibly even before the RS. Ten healthy adults were tested while resting supine, with their head looking directly forward 12, and their right foot in contact with a force-transducing heel-plate. The RS was a small light emitting diode (3.5 mcd luminous intensity) that remained illuminated for 250 msec, and which was located 45 cm from the subject. A high pitched (2.5 kHz) warning tone (WS), of 100 msec duration, served to inform the subjects of
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.
.
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Fig. I. H-reflex amplitudes and late reflex latencies during the foreperiod of a visual reaction time task. The vertical bars correspond to the standard error of the mean of the H-reflex amplitude and the numbers accompanying the late reflex latency values show the number of observations made. WS, warning signal; RS, reaction signal; ES, eliciting (H-reflex) stimulus.
an imminent RS and the foreperiod (WS-RS) was maintained constant at 1 sec in order to maximize expectancy of the response. H-reflexes were elicited at predetermined time intervals throughout both the WS-RS and RS-voluntary response periods. A Grass model $48 nerve stimulator, connected in series with a stimulus isolation unit (SIU5) and a constant current unit (CCU 1), generated the 1.5 msec square-wave pulses which were delivered to the posterior tibial nerve in the region of the popliteal fossa. A 5 m m diameter stimulating electrode was secured in a position capable of evoking a minimal H-reflex without a concomitant direct muscle response, and the dispersive electrode was a moist pad positioned over the patella. Two bipolar surface electrodes (silver, silver chloride), located over the dorsal midline of soleus, led off the evoked muscle action potentials to a preamplifier (Biocom model 2122 differential amplifier; response 3 dB down at 0.05 Hz and 10 kHz) prior to display and storage on a dual trace Hewlett Packard 1201A oscilloscope. Eliciting stimuli (ES) were administered at 12 intervals between WS and the voluntary response. When expressed in relation to the onset of the RS, these intervals (t) corresponded to --800, --600, --400, --200, --150, --100, --50, 0, + 50, + 100, + 150 and + 2 0 0 msec, respectively. In addition, there were 4 comparison conditions: (i) WS and RS but no ES; (ii) WS followed by an ES 1100 msec later (that is, 100 msec after the time at which the RS would usually have occurred); (iii) an ES alone; (iv) an ES alone while the subject maintained a mild isometric plantar flexion. These 16 different conditions were presented in random order in 5 blocks so that each subject
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Fig. 2. H-reflexes and late reflexes recorded during the foreperiod of a visual reaction time task (a-e) and during control conditions if-i). Upper traces show the electromyogram and lower traces the onset of the reaction light (a-f) or the isometric force record (h-i). The time base in all records is 100 msec. The WS-RS interval (see text) is indicated in records a-e. In records g and i the eliciting (H-reflex) stimulus (ES) was delivered while the subject maintained a mild isometric contraction. The late reflex appears as a discrete burst of action potentials 150-250 msec after the H-reflex, and occurs more frequently as the WS-RS interval is reduced. had a total of 80 trials in one experimental session. The trials were separated by variable intervals of at least 15 sec. H-reflex peak-to-peak amplitudes, during the foreperiod, are shown in Fig. J. The mean amplitude o f the H-reflexes elicited without either WS or RS (4.42 mV) was used as the control and corresponded to 25-30 ~ of the maximum H-reflex. The profile o f changes in the H-reflex amplitude, was similar to previous reports 5, 1s,19,21,22. A n early and short lasting period o f facilitation immediately followed the WS2Z,z3; therea6ter there was a reduction in amplitude of the m o n c s y n a p t i c response t h r o u g h o u t the foreperiod, with all values, except at t = - - 1 5 0 msec, slightly less than the control. This reduction in amplitude of the H-reflex has previously been attributed to presynaptic inhibition o f the Ia terminals, which constitutes an important part of the preparatory processes involved in the organization of a voluntary response ~2. After the RS there was an increase in amplitude o f the H-reflex, commencing at t = q-100 msec and continuing to increase until appearance of the voluntary response. H-reflex amplitudes at t = -q-100, + 150 and + 2 0 0 msec were all significantly greater
179 (P < 0.05) than the control value. It has previously been suggested that this increase in the amplitude of the monosynaptic response may be partly attributable to disinhibition of the presynaptic inhibition of la afferent terminals 19. A marked augmentation of the H-reflex was also evident when the ES was delivered while the subject maintained a mild isometric contraction of soleus but did not voluntarily respond to any RS. This effect, which is well documented9,13, most probably results from the subliminal facilitation of fringe motoneurons by the corticofugal input to the motoneuron pool. A large population of subliminal fringe motoneurons are still accessible to the la discharge evoked by the ES during a mild contraction. The 'silent period' which followed the H-reflex, in this condition, is also a well-established phenomenon 1. The mean amplitude for this condition (5.26 mV) was significantly greater (P < 0.05) than the ES-alone condition. The most important results of this study were that discrete bursts of asynchronous muscle activity were observed during the foreperiod in 8 of the subjects. In each case the discharges followed the H-reflex and appeared before the voluntary response. These bursts of activity are shown in Fig. 2. Their frequency of occurrence increased from 24 ~o to 36 ~,, as the RS-ES interval reduced from t -- --800 msec to t = - - 5 0 msec. A substantial increase in occurrence, from 22 ~ to 30 ~ ,was evident between t -- --400 msec and t ~ - - 2 0 0 msec. The latency of these late reflexes also reduced from 282.6 msec at t = --800 msec to 178.3 msec at t - - - 5 0 msec and at t = 0 were indistinguishable from the voluntary response (see Fig. 1). Occasionally, periodic discharges followed the late reflex (see Fig. 2a). In the condition where subjects maintained a mild isometric contraction in soleus, but were not required to voluntarily respond to a RS, the late reflex activity appeared consistently, in 8 of the subjects, with an overall frequency of occurrence of 62 ~ and a mean latency of 150.9 msec (S.D. -- 25.1 msec). This was similar to earlier reported values 13,e4, and is consistent with the view that modulation of late reflex amplitude, as well as the amplitude of the monosynaptic response, occurs according to the postural drive existing at the time of perturbationl,4,1a, 29. When the WS-ES interval of 1100 msec was examined, with no RS, the latency of the late reflex was 188.9 msec, and its frequency of occurrence was 40 ~ . Together these data indicate the high degree of expectancy associated with the preparatory 'set' in this condition. They also suggest a dissociation between the presetting of supraspinal reflex sensitivity and the voluntary response, as no voluntary response was forthcoming. The H-reflex amplitude in this condition was unaltered. Voluntary responses with a latency of 197.8 msec were recorded when the W S - R S interval was 1000 msec and no ES was delivered. When the ES was delivered during the foreperiod, the voluntary responses were significantly longer (P < 0.05), ranging between 243.2 msec at t -- --800 msec and 210.4 msec at t = - - 5 0 msec. The voluntary responses were also longer than the control (P < 0.05) when the ES was delivered after the RS, values of 212.9 msec at t -- + 5 0 msec, 246.6 msec at t ~ q-100 msec, 267.9 msec at t -I- 150 msec, and 259.9 msec at t -- ~-200 msec being recorded. The origins of the excitatory synaptic inputs that lead to the late reflex are of considerable interest. When the late reflex activity appears following an H-reflex super-
180 imposed upon a background isometric contraction there are 3 major sources of facilitation: (a) long loop reflexes evoked by the primary afferent discharge associated with the electrical stimulus 13; (b) primary afferent discharge from muscle spindles during the H-reflex twitch relaxation 2,25, and (c) rebound facilitation of motoneurons following the inhibitory postsynaptic potentials that produce the silent period 13. The posturat drive is apparently required to increase the sensitivity of the spinal and supraspinat reflexes, for without the contraction the late reflex is rarely seen in normal subjects 2~. The results of the present study show that the late reflexes may be elicited in normal subjects, without any postural drive, when the preparatory 'se( to respond serves to modulate the reflex sensitivity. Moreover, since the presumed presynaptic inhibition of Ia terminals maintained the H-reflex amplitude constant in the 600 msec prior to RS, the increased frequency of occurrence and shorter latencies of the late reflexes in this period would appear to be attributable to a progressively increased gain in the supraspinal pathway. The long latency of the late reflex provides some indication of the pathways involved. It is unlikely that a fast conducting transcortical pathway is used as the latency of the M2 response in the flexor hallucis longus muscle occurs between 75 and 90 msec following stimulation of the posterior tibial nerve 15. Responses with latencies between 85 and 1l0 msec appear in soleus when subjects are welt-practised at responding with a plantar flexion to an H-reflex stimulus (unpublished observations). It is more probable that the slower conducting M3 pathway, involving the cerebellum, mediates the response. The latency and time course of the late reflexes closely match the period of "intercurrent facilitation'2v evoked in soleus by a subthreshold conditioning stimulus ~a. Intercurrent facilitation in the H-reflex recovery curve has previously been ascribed to a supraspinal reflex 2v, thought to relay through the cerebellum 2v, but also involving lhe motor cortex 14. The longer latency of the late reflexes elicited during the foreperiod, when compared with the postural drive condition, may be the result of presynaptic blocking of the muscle spindle primary afferent discharge contribution. Also, the occasional appearance of periodic discharges following the late reflex is consonant with the interpretation of a preparatory elevation of gain of the supraspinal reflex. These oscillations are characteristic of an underdamped servosystem. In summary, evidence has been presented of an increased sensitivity of"the M3 or 'late reflex'13 in human subjects during the foreperiod of a visual reaction time task. The increased gain of the response, associated with a well-established preparatory 'set', may be related to the changes in cortical cell activity in monkeys reported by Tanji and Evarts 2s. The altered sensitivity of the reflexes appeared to be associated with the 'set' to respond, as opposed to the volitional response per se, as it was evident even when no RS or voluntary responses were present. The anticipatory presetting of reflex excitability, prior to the visual stimulus, may considered to be an important element in the internal representation of an impending movement 2°. This research was supported by grants from the National Research Council of Canada and from the University of Waterloo Research Council.
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