Central Modifications of Reflex Parameters May Underlie the Fastest Arm Movements

Serge V. Adamovich, Mindy F. Levin, and Anatol G. Feldman

Institute for Information Transmission Problems, Academy of Sciences, Moscow, Russia; Centre de Recherche, Institut de Réadaptation de Montréal, Montreal, H3S 2J4; and Ecole de Réadaptation, Université de Montréal, Montreal, Quebec, Canada

    ABSTRACT
Abstract
Introduction
Methods
Results
Discussion
References

Adamovich, Serge V., Mindy F. Levin, and Anatol G. Feldman. Central modifications of reflex parameters may underlie the fastest arm movements. J. Neurophysiol. 77: 1460-1469, 1997. Descending and reflex pathways usually converge on common interneurons and motoneurons. This implies that active movements may result from changes in reflex parameters produced by control signals conveyed by descending systems. Specifically, according to the lambda -model, a fast change in limb position is produced by a rapid change in the threshold of the stretch reflex. Consequently, external perturbations may be ineffective in eliciting additional reflex modifications of electromyographic (EMG) patterns unless the perturbations are relatively strong. In this way, the model accounts for the relatively weak effects of perturbations on the initial agonist EMG burst (Ag1) usually observed in fast movements. On the other hand, the same model permits robust reflex modifications of the timing and shape of the Ag1 in response to strong perturbations even in the fastest movements. To test the model, we verified the suggestion that the onset time of the Ag1, even in the fastest movements, depends on proprioceptive feedback in a manner consistent with a stretch reflex. In control trials, subjects (n = 6) made fast unopposed elbow flexion movements of ~60° (peak velocity 500-700°/s) in response to an auditory signal. In random test trials, a brief (50 ms) torque of 8-15 Nm either assisting or opposing the movement was applied 50 ms after this signal. Subjects had no visual feedback and were instructed not to correct arm deflections in case of perturbations. In all subjects, the onset time of the Ag1 depended on the direction of perturbation: it was 25-60 ms less in opposing compared with assisting load conditions. Assisting torques caused, at a short latency of 37 ms, an additional antagonist EMG burst preceding the Ag1. The direction-dependent effects of the perturbation persisted when cutaneous feedback was suppressed. It was concluded that the direction-dependent changes in the onset time and duration of the Ag1 as well as the antagonist activation preceding the Ag1 resulted from stretch reflex activity elicited by the perturbations rather than from a change in the control strategy or cutaneous reflexes. The results support the hypothesis on the hierarchical scheme of sensorimotor integration in which EMG patterns and movement emerge from the modification of the thresholds and other parameters of proprioceptive reflexes by control systems.

    INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References

Many studies address the question of how proprioceptive feedback, or specifically the stretch reflex (SR), is integrated with central commands in the generation of electromyographic (EMG) activity. The SR is associated with an increase or a decrease in EMG activity in response to muscle lengthening or shortening, respectively. The term "tonic SR" refers to length-dependent changes in EMG activity at zero velocity, whereas the term "phasic SR" is used when velocity is a dominant factor in the generation of such activity (e.g., in the knee jerk). The SR usually functions in a part of the physiological range of the joint angle or muscle length: EMG activity arises if the actual muscle length exceeds a threshold length (Feldman 1966; Matthews 1959). The threshold length depends on the influences of different descending systems projecting to alpha - and/or gamma -motoneurons (MNs) (Capaday 1995; Feldman and Orlovsky 1972; Nichols and Steeves 1986).

Proprioceptive feedback is functionally significant in the maintenance of the tonic firing of MNs during postural tasks as well as in the production of slow- and moderate-speed movements (e.g., Bennett 1993; Feldman 1966, 1986; Gerilovsky et al. 1990; Smeets et al. 1995; Stein and Kearny 1995). What remains controversial is the role of this feedback in the production of the fastest movements. The results of perturbation and deafferentation studies are usually considered supportive of the view that the well-described triburst EMG pattern during fast movements (Wacholder 1928) is basically produced by a central generator (CG), although there are divergent views on the ability of proprioceptive reflexes to modify the EMG output of the CG (Brown and Cooke 1986; Forget and Lamarre 1987; Gielen et al. 1984; Gottlieb 1994; Hallett and Marsden 1979; Lestienne 1979; Simmons and Richardson 1993; Smeets et al. 1995; Wadman et al. 1979; Wallace 1981).

An alternative scheme of sensorimotor integration, the lambda -model, is not based on the premise of the preformation of EMG bursts by a CG. It adheres to the view that descending and reflex pathways usually converge on common interneurons and MNs (Jankowska 1992). This convergence, as well as the phenomenon of "reflex gating" (e.g., Drew and Rossignol 1987; Feldman and Orlovsky 1975), implies that active movements may result from changes in reflex parameters such as the threshold and gain by control signals conveyed by descending systems. Specifically, in the lambda -model, it is suggested that fast changes in the limb position are produced by a rapid monotonic change in the reflex threshold. The control systems thus take advantage of, rather than suppress, proprioceptive reflexes even in the production of the fastest movements. We will consider this point in more detail with the use of the condition of muscle activation and the control pattern suggested in the model (Eqs. 1-3 below).

According to the model, EMG activity of a muscle is initiated when the difference between the actual (x) and threshold (lambda *) length of this muscle becomes nonnegative so that
<IT>x</IT>− λ* ≥ 0 (1)
The onset of activation is defined by the equality sign in Eq. 1. In other words, it is observed when the actual and threshold lengths match each other and then diverge in the direction defined by the inequality sign in Eq. 1. Neurophysiologically, the matching occurs at the level of the MN membrane, when the postsynaptic potential resulting from appropriate central and afferent inputs exceeds the threshold potential of the MN (Feldman 1986).

The threshold length is defined as
λ* = λ − μ d<IT>x</IT>/d<IT>t</IT>+ ρ (2)
The component lambda  may be changed by central commands independently of the current kinematic or force output of the system. The time-dimensional parameter µ characterizes the dependency of the threshold on velocity dx/dt (which is positive for muscle lengthening). Threshold lambda * also depends on the reflex influences on this muscle from proprioceptive afferents of other muscles spanning the same or other joints. The intermuscular interaction is measured, in an integral way, by the parameter rho , but it may be decomposed into components rho ij representing the changes in the threshold of the muscle i due to proprioceptive influences from muscle j. Thus intermuscular interaction is described by matrix par-bars rho ijpar-bars . Different physiological systems may likely influence the matrix of intermuscular interaction, in particular Renshaw cells (recurrent inhibition), gamma -MNs, and descending central inputs to interneurons mediating the influence of muscle spindle, tendon organ, and cutaneous afferents to alpha -MNs.

One component of the control pattern leading to the initiation of the initial agonist EMG burst (Ag1) and to changes in a joint angle is a monotonic, ramp-shaped decrease in the agonist threshold (lambda )
λ = λ<SUB>0</SUB>− <IT>s t</IT> (3)
where lambda 0 is the initial value and s is the speed of changes of the threshold by control systems.

Experimentally, the onset of the ramp may be associated with the early gradual increase in the excitability of agonist MNs starting 30-60 ms before the onset of Ag1 (Kots 1975). Thus, time t in Eq. 3 is measured from the onset of the elevation of the MN membrane potential. Indeed, change in the agonist threshold is only a component of the control pattern underlying single-joint movement (see Feldman and Levin 1995). However, this study focuses on the Ag1 initiation, in which central changes in the agonist threshold play a major role.

As estimated in experimental and simulation studies (Abdusamatov et al. 1988; Feldman et al. 1995; St-Onge et al. 1996), the speed of central changes in the SR threshold underlying the fastest elbow movements is high (~600°/s). This angular speed, sand , and the linear speed denoted by s in Eq. 3, are interrelated, to a first approximation, via the moment arm, h, of muscle action (s = h sand ). It follows from Eqs. 1-3 that stretching the muscle, i.e., increasing the variables x and dx/dt by external forces (perturbations) or decreasing threshold lambda  by central commands, are equivalent methods of muscle activation. In the absence of perturbations, the central changes in the threshold are, indeed, a major factor in the initiation of Ag1. Moreover, because of the high rate of central changes in the threshold in fast movements, additional modifications of the threshold associated with external perturbations may have little effect on the EMG patterns, especially Ag1, unless the perturbations elicit changes in the actual joint angle at a comparable speed.

This effect is illustrated schematically in Fig. 1. The centrally mediated ramp decrease in the threshold length (lambda *, thick solid line) underlying a fast elbow flexion starts att = 0. The slope of the ramp is ~32.5 cm/s, corresponding to the angular rate of 600°/s (for the agonist moment arm, h, ~3 cm). In nonperturbed movement, the actual muscle length (x, thick solid line) remains constant before the onset of the Ag1. According to Eq. 1, the Ag1 arises at the point where the two thick solid lines intersect (filled circle). The left vertical line shows the onset of perturbation occurring ~50 ms before the onset of Ag1 in nonperturbed movement. The perturbation influences the MNs after some delay (d) in the transmission of afferent signals to MNs. The changes in the muscle length elicited by the perturbation will also affect the activation threshold (see Eq. 2) and thus the ramp will be modified as shown by thin solid and dashed lambda * curves for movements perturbed by an opposing and an assisting load, respectively. Open circles show the onset of Ag1 in these movements. For the opposing load, the Ag1 starts at tau  = 35 ms, i.e., 15 ms earlier than the Ag1 onset in nonperturbed movement or 30 ms earlier than in movements perturbed by an assisting load. Specific estimations of perturbation effects (APPENDIX) show that these changes in the Ag1 latency can be obtained by applying rather strong load pulses (7.7-9.6 Nm), which have not been used in studies published previously (e.g., Brown and Cooke 1986).


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FIG. 1. According to the lambda -model, the onset time of the initial agonist burst (Ag1), even in the fastest movements, may be changed in a manner consistent with the stretch reflex (SR) elicited by external perturbations. The Ag1 in fast nonperturbed movements arises when the dynamic SR threshold (lambda *, thick solid line) intersects the actual muscle length (x, thick solid line) at the point shown by the filled circle. Fast flexion movement is produced by a centrally mediated ramp decrease in the threshold at a high rate (~600°/s) starting at t = 0. Thick solid curves: nonperturbed movement. Thin solid and dashed curves: movements perturbed by an opposing and an assisting load, respectively. Perturbations start at the time shown by the left vertical line. They begin to influence motoneurons after some reflex delay, d. Open circles: onset of the agonist burst in these movements. In the opposed movement, the agonist electromyogram (EMG) starts at tau  = 35 ms, i.e., ~15 ms earlier than in nonperturbed movements.

The lambda -model may thus account for the relatively weak effects of perturbations on EMG bursts usually observed in fast movements. On the other hand, the same model permits robust reflex modifications of the timing and shape of EMG patterns in response to strong perturbations even in the fastest movements. In particular, the onset time of Ag1 in such movements may be modified by proprioceptive feedback in a manner consistent with the SR.

We tested the prediction of the lambda -model that the onset of Ag1 may be accelerated or decelerated depending on the direction of the load stimulus applied before the initiation of fast elbow flexion movement.

    METHODS
Abstract
Introduction
Methods
Results
Discussion
References

Apparatus and procedures

Healthy subjects (n = 6, aged 25-55 yr) participated in the study after giving informed consent according to the procedure approved by the Ethics Committee of the Institut de Réadaptation de Montréal. Subjects sat in a chair with a solid trunk support. The shoulder was in ~70° flexion and 80° abduction. The forearm of the subject was placed inside a rigid cast that was fixed firmly to the horizontal manipulandum (moment of inertia 0.03 kg/m2) having a vertical handle grasped by the subject. The axis of the elbow joint was aligned vertically with the axis of rotation of the manipulandum and a torque motor so that movements were performed in a horizontal plane. Flexion and extension torques were measured with strain gauges glued to the motor shaft. Position and velocity were measured with a high-precision hybrid electromagnetic resolver aligned with the shaft of the torque motor. EMG activity of an elbow flexor (biceps brachii) and an extensor (the lateral head of triceps brachii) was recorded with active bipolar surface electrodes (1-mm silver chloride strips, 1 cm long and 1 cm apart) with a band-pass filter of 45-550 Hz. The electrodes were highly selective and minimized cross talk. The latter was evidenced by the lack of synchronous spikes in different electrodes, the voluntary activation of separate muscles in isolation, and the presence of a silent period in the EMG activity of one group of muscles associated with a burst of activity in the antagonist muscles. All signals were recorded from 0.2 s before to 1 s after the trigger signal with a sampling rate of 1 kHz for EMG, kinematic, and torque data.

The initial position of the elbow corresponded to ~140° (full extension is 180°) and was achieved by lining up a vertical cursor within a 1° start window on the computer screen in front of the subject. The experiments were controlled by the computer. During training (~20 trials), after an auditory go signal, subjects made discrete elbow flexion movements (50-70°) as rapidly as possible to a 6° target window with the eyes open (peak velocity ranged from 500 to 700°/s and peak elbow torque from 10 to 15 Nm). The time between trials varied randomly from 5 to 15 s. In the subsequent experimental sessions (36 trials), the cursor disappeared when it left the start window, thus eliminating visual feedback. With random occurrence, one third of the movements were not loaded, one third were loaded by a torque pulse applied to the manipulandum that opposed the ongoing movement, and one third were loaded by a torque pulse assisting the ongoing movement. The 8- to 15-Nm torque pulse was applied 50 ms after the go signal and lasted 50 ms. Theoretically, according to estimations based on the lambda -model, this torque magnitude was sufficient to shift the onset time of the Ag1 by about ±15 ms depending on the pulse direction (see APPENDIX).

Load perturbations produced a change in pressure on the surface of the arm. To test whether this additional cutaneous stimulus could influence the observed effects, the experimental protocol was repeated in one subject after complete ischemic block of the cutaneous mechanoreceptors of the hand and the distal part of the forearm. This was achieved by placing a pressure cuff around the forearm distal to the elbow joint. The pressure was maintained at 180-200 mmHg and the experiment was conducted between the 18th and 25th min after the ischemia began.

Data analysis

EMG signals were rectified and low-pass filtered with a 40 Hz cutoff frequency. Onset, amplitude, and duration of EMG signals, as well as movement amplitude, peak velocity, and time to peak velocity were determined with the use of an interactive graphic display. Movement latencies were measured from the auditory go signal to the time at which the Ag1 EMG burst surpassed 2 SD of the baseline activity. Time to peak velocity values were also measured from the auditory go signal. EMG burst amplitude was measured as the peak value of the rectified EMG signal. Values were averaged and submitted to analysis of variance (ANOVA) whose only factor was load condition (assisting load, opposing load, control). Student-Newman-Keuls tests were used for post hoc pairs comparison analysis. The probability level for statistical significance was set to P < 0.05.

The kinematic and EMG traces from each experimental block were aligned according to the trigger signal and then averaged. Traces from control trials (without perturbation), trials with assisting loads, and trials with opposing loads were averaged separately for further comparison.

    RESULTS
Abstract
Introduction
Methods
Results
Discussion
References

Kinematics

Figure 2 shows typical effects of brief torques applied before the onset of fast flexion movements in one subject. Assisting and opposing perturbations resulted in substantial initial deflections of the arm toward or away from the final position (2nd plot, thick and thin lines, respectively). In all subjects, the direction of perturbation significantly affected the magnitude of the peak velocity of movement [ANOVA, F(2,10) = 15.13, P = 0.01], and the time to peak velocity [ANOVA, F(2,10) = 17.26, P = 0.001]. The mean peak velocity and time to peak velocity were 599.5 ± 25.8°/s (mean ± SD) and 348 ± 17 ms (measured from the signal to move) for control nonopposed movements. Opposing load perturbations significantly increased (by 95.3°/s, P < 0.05), whereas assisting loads had no effect on the peak velocity. The time to peak velocity was equally shorter (P < 0.05) for both types of load perturbations (by ~66 ms for assisting loads and 52 ms for opposing loads), compared with control, which may have been a consequence of the overall decrease in movement latency in perturbed movements (see below).


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FIG. 2. Averaged (n = 10) kinematic and EMG patterns in 1 subject (S4 in Fig. 3) making control, unopposed movements and movements perturbed by a brief opposing or assisting load (dotted, thin, and thick traces, respectively). Vertical dashed lines: onset and offset of the current in the torque motor eliciting the perturbations. Arrow: onset of the sound signal (BEEP) to move. The traces near this arrow show the profile of the perturbational torque. Note the substantial changes in kinematic patterns; a decrease in the onset time of the initial EMG bursts in the agonist muscle (Biceps Brachii) for perturbed load conditions; the difference in the onset time of these bursts in assisting and opposing load conditions; an overall decrease in the agonist EMG onset in perturbed compared with nonperturbed movements; an increase in the duration of the 1st agonist burst in opposing compared with assisting load conditions; additional EMG bursts in the antagonist muscle (Triceps Brachii) preceding the Ag1 for assisting load conditions; and changes in the onset time of the regular antagonist burst depending on the direction of perturbation.

Onset time and duration of Ag1 burst

The latency of Ag1 in perturbed movements was less than in control nonperturbed movements, and this effect was greater for opposing than assisting load perturbations (Fig. 2, 3rd plot, compare thin and thick traces with dotted traces). For the data shown in Fig. 2, the mean latency of Ag1 was ~40 ms less in opposing than in assisting load conditions (112 and 152 ms, respectively, or 62 and 102 ms after the onset of the load perturbation).

For all subjects (Fig. 3, top; see also Fig. 2), the onset time of Ag1 was dependent on the direction of the perturbation [ANOVA, F(2,10) = 23.23, P = 0.0002]. This effect was significant for all post hoc pairs comparisons. In particular, the onset time of Ag1 was significantly greater in assisting than in opposing load conditions. The mean group latencies of Ag1 with respect to the signal to move were 111 ± 12 ms for the opposing load; 148 ± 16 ms for the assisting load; and 201 ± 17 ms for the control, nonperturbed movements. Thus, compared with control movements, the mean decrease in onset was 90 and 53 ms when opposing and assisting perturbations, respectively, were applied.


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FIG. 3. Onset time (mean ± SD) of the Ag1 and regular antagonist bursts measured from the signal to move (top and middle) and time to peak velocity (bottom) for different load conditions in 6 subjects. Horizontal dashed: onset and offset of the current in the torque motor eliciting perturbational stimuli. BB, biceps brachii; TB, triceps brachii.

The one exception was subject 2, who had the shortest latencies of control movements compared with all the other subjects (Fig. 3). In this subject, only direction-dependent changes and no overall decreases in the onset time of the Ag1 were observed in perturbed movements (Figs. 3 and 4).


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FIG. 4. Kinematic and EMG effects of perturbations in subject 2. Unlike Fig. 2, in this example only direction-dependent changes and no overall decrease in the onset time of the Ag1 was observed. Conventions as inFig. 2.

For different subjects, the difference in the onset time of the Ag1 for opposing and assisting load conditions was in the range of 25-60 ms (mean ~37 ms). The mean time between the onset of the opposing load perturbation and Ag1 in five subjects was less than, and in one subject just slightly greater than, the minimal latency of possible triggered reactions to perturbations (70 ms) (see Crago et al. 1976; Newell and Houk 1983).

The assisting load elicited an additional EMG burst in the stretched antagonist muscle preceding the Ag1 (Figs. 2 and 4, bottom plots, thick traces). The onset of this additional burst also preceded the Ag1 in control nonperturbed movements. In the example shown in Fig. 2, the additional EMG burst in triceps brachii was initiated 36 ms after the onset of perturbation. This additional antagonist burst was observed in all subjects and in each trial with an assisting load and had a mean latency of ~37 ms after the onset of perturbation. The mean amplitude of this burst for the group was 0.4 of that of the regular antagonist burst.

The antagonist burst following the Ag1 is called "regular" to distinguish it from the additional antagonist burst arising in assisting load conditions. The introduction of either type of load perturbation not only decreased the latencies of Ag1 but also those of the regular antagonist burst (Figs. 2 and 3). In contrast, the effects of the two directions of perturbations on the onset time of this antagonist burst were different in different subjects. For data shown in Fig. 2, bottom plot, the onset time was significantly less in assisting than in opposing load conditions (197 and 226 ms, respectively, after the onset of perturbation). This effect was observed in four out of six subjects (Fig. 3, middle).

The duration of the Ag1 also depended on the direction of the perturbation, being greater in opposed movements. The effect of the load condition on the duration of the Ag1 burst (Fig. 5) was significant [e.g., F(2,10) = 23.54, P = 0.0002]. Post hoc tests revealed that, compared with control, although the prolongation of the duration of Ag1 in opposing load conditions was significant (by ~37 ms, P < 0.001), the decrease in the duration in assisting load conditions was not (by ~13 ms, P > 0.06). Perturbations had no effect on the duration of the regular antagonist EMG burst (P > 0.4). In addition, although the mean amplitudes of Ag1 and the antagonist burst were higher in opposing compared with assisting load conditions, the difference was not significant.


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FIG. 5. Mean duration of the Ag1 and following antagonist EMG bursts for different load conditions in all 6 subjects.

Block of cutaneous afferent feedback from the hand and forearm

Load perturbations produced a substantial pressure on the surface of the arm. To evaluate the effects of cutaneous input on the parameters of agonist and antagonist bursts, we repeated the experiments after complete ischemic block of the cutaneous mechanoreceptors of the hand and the distal part of the forearm. The experiment was performed on subject 2, whose pattern of changes in the onset time of Ag1 to different load directions was typical for the group (Fig. 3). Cutaneous afferent nerve block had no significant effect on the timing of either the kinematic or EMG pattern (Fig. 6). The only noticeable effect was a decrease in the rate of rise of Ag1 in both assisting and opposing load conditions.


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FIG. 6. Kinematic and EMG patterns in perturbed movements before and after a decrease of cutaneous afferent feedback by 21-25 min ischemia of the forearm and hand in subject 2. Solid and dashed traces: movements before and during the cutaneous block, respectively. Thin and thick traces: opposing and assisting load conditions, respectively.

    DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References

SR effects

The main finding of this study is that, in all subjects, strong perturbations resulted in direction-dependent changes in the onset time of the Ag1. The onset time was 25-60 ms less in opposing compared with assisting load conditions. In all but one subject, this effect was combined with an overall decrease in the onset time of the Ag1 and the subsequent antagonist EMG burst in response to both types of perturbation. The duration of the Ag1 was also dependent on the direction of perturbation, being greater in opposed movements. In addition, assisting torques caused the appearance of a short-latency (37 ms) additional antagonist EMG burst preceding the Ag1. The direction-dependent effects of the perturbation persisted when cutaneous feedback from the hand and forearm was suppressed in one subject.

In most subjects the direction-dependent changes in the onset time of the Ag1 were observed at a latency (25-60 ms) less than the minimal latency of triggered reactions (70 ms) and much less than the mean latency of triggered or voluntary reactions to perturbations (>140 ms) (see Newell and Houk 1983). Thus it is unlikely that the direction-dependent changes in the onset time of the Ag1 were elicited by an alteration of the central commands, although such an alteration might be responsible for later effects of perturbations in some subjects (see below). The results of the experiment in which cutaneous afferent feedback from the hand and forearm was suppressed suggest that cutaneous reflexes may not be the main factor determining the direction-dependent effects of perturbations. It is most likely that an SR mediated by muscle afferents was responsible for the changes in the onset time and, as a consequence, the duration of the Ag1.

In a study comparable with ours (Newell and Houk 1983), subjects reestablished an initial wrist position in response to a load or an unload stimulus. Corrective reactions to a load stimulus were triggered ~30 ms earlier on average than were reactions to an unload stimulus. The authors considered an SR as a possible mechanism underlying the directional effects of perturbations, which is similar to the explanation we propose in our study. Newell and Houk could not exclude the possibility that cutaneous reflexes were responsible for the directional effects in their study. In addition, subjects in that study were instructed to trigger compensatory responses to perturbations. Thus the directional effects in the study by Newell and Houk might have been associated with a decision-making process related to the formation of triggered reactions depending on sensory information on the load and unload stimulus. Long reaction times for triggered reactions (see above) would have been sufficient for such a process. The assumption that the initiation of triggered reactions depends on the load direction is indirectly supported by the observation (Crago et al. 1976; see also Fig. 3 in Feldman and Levin 1995) that it is more difficult not to intervene to a load stimulus than to an unload stimulus. In contrast, subjects in our study were instructed not to make corrections in response to perturbations, and the direction-dependent changes in the Ag1 onset in our study were typically observed before the time when triggered reactions could be initiated. Thus our data are more conclusive in support of a major role of the SR reflex in the direction-dependent effects of perturbations.

In other experiments similar to ours by Brown and Cooke (1986), perturbations introduced before movement onset elicited a decrease in the latency of the Ag1. However, in the study by Brown and Cooke, changes in the direction of perturbations had only insignificant effects on Ag1 latency, leading those researchers to conclude that the role of the SR in the initiation of the Ag1 was minimal. The difference between the findings by Brown and Cooke and ours may be explained in terms of the lambda -model. According to the model, the efficiency of perturbations at the initial phase of fast movements is diminished not because of a central suppression of the SR pathway, but, as described in the INTRODUCTION, because the pathways are already largely recruited by the central commands to produce movement. Thus effects of perturbations may only become apparent when perturbations surpass a certain force threshold. Mild perturbations, such as those used in the study of Brown and Cooke (3-5 Nm), would have only small effects on the SR response that could be hidden by comparatively large variations in movement latency typical even for nonperturbed movements. The hypothesis that the SR is functionally significant even at the initial phase of fast movement could only be verified with the use of perturbations of appropriate magnitudes (8-15 Nm, see APPENDIX).

The appearance of an additional antagonist burst in the case of assisting perturbations has previously been observed in fast elbow movements (Abdusamatov et al. 1988) and in slower movements perturbed after the movement onset (Bennett 1993). In the present study, this burst occurred at a short latency (~37 ms) after perturbation and likely represents a reflex response to stretching of the antagonist muscle by the load. This observation is consistent with the lambda -model, which suggests that the timing of any EMG burst is reflex dependent.

Overall decrease in movement latency and other findings

According to the lambda -model (Feldman 1986; see also Bernstein 1967) there are two basic ways of using proprioceptive signals at different levels of motor regulation. At the level of MNs these signals do not modify the current control pattern but continuously influence the timing and magnitude of EMG activity. The changes in movement latency dependent on the direction of the load stimulus observed in the present study refer to the proprioceptive effects at this level.

In contrast, at the level of the formation of central commands, proprioceptive signals may be used noncontinuously to initiate the control pattern or to make discrete corrections during or after the end of the movement according to changing external conditions. The decrease in the movement latency regardless of the direction of the load stimulus found in the present study and previously reported by Brown and Cooke (1986) likely refers to the effects associated with this level.

In the present study the direction-dependent and the overall decreases in movement latency were combined in most subjects. Nevertheless, in one subject (Fig. 3) only direction-dependent changes and no overall decrease in the movement latency were observed, suggesting that the two levels of motor regulation may not only be differentiated in terms of reactions to proprioceptive signals but also may function independently. The assumption on the independence of the two levels is indirectly supported by the observation that, in the monkey, temporary cooling of the cerebellar nuclei resulted in an increase in movement latency without changes in movement kinematics (Brooks 1986).

To explain the later effects of perturbations, such as changes in the onset time of the regular antagonist burst following the Ag1, two factors should be considered. First, our brief perturbations may have elicited not only immediate but also remote reflex effects on the subsequent movement. Second, the control pattern may have been modified in response to the perturbation. The difference in the onset times of the regular antagonist burst across subjects suggests different individual control strategies in dealing with perturbations. We assumed that some subjects maintained the same control pattern regardless of perturbations. In others, the strong perturbations could have triggered changes in the control pattern. It appears difficult if not impossible to verify these assumptions without a dynamic model integrating the mechanical, contractile, central, and reflex mechanisms of the system. This goal can likely be achieved with the use of a nonlinear dynamic formulation of the lambda -model (St-Onge et al. 1997).

Choice between alternative schemes of sensorimotor integration

In the lambda -model, the control process is associated with modifications of SR thresholds and other reflex parameters. In other words, the relationship between the control and reflex systems in this model is hierarchical and the individual effects of each system cannot be identified as separate components of EMG signals. For example, modifications of EMG patterns elicited by perturbations are not purely reflex in nature because they also depend on the current setting of control variables. Similarly, EMG modifications elicited by changes in control variables are not purely central because these variables influence EMG activity not directly but via changing reflex parameters.

In contrast, according to an alternative hypothesis, the triphasic EMG pattern in fast movements is basically produced by a CG, with the reservation that proprioceptive reflexes may modulate this pattern to some extent (see INTRODUCTION). In some studies, the role of proprioceptive reflexes in the generation of EMG bursts in fast movements is considered minimal, i.e., these bursts are "mostly centrally driven" (Gottlieb 1994). This suggestion is difficult to reconcile with electrophysiological observations of a substantial increase in the agonist H reflex before the onset of the Ag1 (Kots 1975). These observations imply that inputs from primary afferents to homonymous MNs become more efficient rather than suppressed or unchanged in fast movements. A decrease in presynaptic inhibition is likely responsible for the increase in the efficiency of afferent inputs (Hultborn et al. 1987).

The observation that the onset time of the Ag1 and its shape during the first 100 ms are insensitive to perturbations (Wadman et al. 1979) was considered a strong argument in favor of the CG hypothesis. Our finding that the onset time of the Ag1, even in the fastest movements, actually depends on proprioceptive feedback in a manner consistent with an SR challenges this argument. In general, taken together, studies of the effects of perturbations suggest that no parameter characterising the timing and shape of EMG bursts in fast movements is independent of proprioceptive reflexes. For example, perturbations made after the movement onset may also influence the duration of Ag1 (Angel 1974; Gielen et al. 1984; Levin et al. 1992; Smeets et al. 1990; Wallace 1981). On the other hand, unexpected increases or decreases in inertial load after the beginning of fast movement elicit short-latency SR modifications in the Ag1 and antagonist bursts (Smeets et al. 1995; cf. Latash 1994).

The observation of a triburst pattern in fast movements of deafferented subjects has also been considered as strong support for the CG hypothesis. The tacit assumption underlying deafferentation experiments is that central and reflex systems act in parallel such that their effects may be dissociated in EMG activity by interruption of the proprioceptive input. The interpretation of deafferentation experiments may be equivocal taking into account, for example, the immediate and long-term consequences of deafferentation such as sprouting and synaptic plasticity (Goldberger and Murray 1974; Hellgren and Kellerth 1989; Kaas 1991). In any case, the results of deafferentation experiments are not in conflict with the hierarchical scheme of sensorimotor integration suggested by the lambda -model. Indeed, deafferentation effectively destroys this hierarchy, making it impossible to offer conclusions about sensorimotor integration in the intact system. Deafferentation experiments may thus not be critical in choosing between different hypotheses on sensorimotor integration in intact systems.

In intact subjects making fast isometric torque exertions or when fast isotonic movements are arrested, triburst patterns may also occur (e.g., Ghez and Gordon 1987; Latash 1993). This too is traditionally considered to be supportive of the view that EMG patterns during fast movements are centrally generated. The lambda -model actually explains the generation of EMG patterns in isometric conditions (Levin and Feldman 1995). Furthermore, when an isotonic movement of a distance greater than a critical level (~50°) is arrested, the triburst pattern is reduced to a single burst involving only agonist muscles. This specific suggestion of the lambda -model was verified in a recent study in which the fastest 60° elbow flexion movements were opposed by a stiff springlike load (Feldman et al. 1995). In these experiments, the final, steady-state levels of elbow position, EMG activity, and torque were reached after ~100 ms after the movement onset instead of 200-300 ms as was the case in unopposed movements. After instructions not to intervene in the load perturbation, subjects did not correct substantial positional errors (up to 45°). Drastic changes in the EMG patterns were observed: the Ag1 was prolonged for as long as the load was presented, whereas the antagonist burst was completely suppressed. It seems unlikely that this transformation resulted from corrections of the central commands, because changes in EMG patterns began at a latency of <60 ms, too early for voluntary or triggered reactions. We concluded that the transformation of the kinematic and EMG patterns resulted from mechanical and reflex reactions to perturbations rather than from changes in the control pattern underlying the movement.

These conclusions are supported by computer simulations showing that the same monotonic control pattern in the lambda -model resulted in a triburst or single-burst EMG pattern in free and arrested movements, respectively (St-Onge et al. 1997). Thus these experimental and simulation results counter the view on the existence of a CG for EMG bursts in fast movements or isometric conditions and are rather consistent with the hierarchical scheme of the relationship between control and reflex systems suggested by the lambda -model.

Indeed, the hypothesis on the specification of EMG patterns predominantly by a CG is not the only alternative to the lambda -model. The best known is the pulse-step model based on the idea that posture and movement may be controlled independently by two central commands. One command ("pulse") initiates movement, whereas the other ("step") holds the system in the final position. The model was initially formulated for eye movements (Robinson 1973) but was later used to describe arm movements as well (Freund and Budingen 1978; Ghez and Gordon 1987). In the existing formulations, it remains unclear how the problem of integration of sensory and control signals is solved in the model. Accepting a hierarchical scheme of integration suggested by the lambda -model may be the first step in reconciling the two models (Weeks et al. 1996). However, the pulse-step control signals in the lambda -model would be inconsistent with our experimental data. Imagine if we replaced the gradual change in the SR threshold shown in Fig. 1 with a step change suggested by the pulse-step model. This would make the onset time of Ag1 practically insensitive to perturbations, because all three intersection points (open and closed circles) defining the onset would lie on a vertical line. This implies that gradual commands are physiologically more plausible than nongradual pulse and step commands. The pulse-step model thus requires some modifications that, we believe, would eventually make this model identical to the lambda -model.

    ACKNOWLEDGEMENTS

  We thank Dr. Francis Lestienne for helpful comments on the manuscript.

  This work was supported by the National Sciences and Engineering Research Council and the Medical Research Council.

    APPENDIX

Influences of load perturbations on the onset of Ag1

The minimal magnitude (P) of an opposing pulse that may elicit a decrease in the onset time of the Ag1 by 15 ms can be estimated on the basis of Eqs. 1-3 complemented by the equation of motion of the forearm
<IT>I</IT>ε = <IT>P − M</IT> (A1)
I is the moment of inertia of the forearm with the manipulandum, epsilon  is the angular velocity (epsilon  > 0 if the forearm is accelerated in the direction of extension); and P and M are the load and muscle torques, respectively. Before the perturbation, all torques and acceleration are zero. Muscles resist perturbations, and therefore, ignoring this resistance, one can get the value
ε<SUB>m</SUB><IT>= P</IT>/<IT>I</IT> (A2)
which overestimates actual acceleration epsilon
ε<SUB>m</SUB>> ε (A3)
The magnitude of the pulse was constant in the present study and therefore epsilon m is the same during the pulse duration (50 ms). According to physical laws a constant acceleration, epsilon m, would result in a linear increase in velocity and a parabolic change in the length of Ag1
d<IT>x</IT>/d<IT>t = h</IT>ε<SUB>m</SUB>τ,
<IT>x = x</IT><SUB>0</SUB><IT>+ hε</IT><SUB>m</SUB>τ<SUP>2</SUP>/2 (A4)
where tau  is the time from the pulse onset and h is the moment arm (Fig. 1). The onset t0 of the Ag1 without perturbations is found with the use of the middle intersection point in Fig. 1. At this point, the actual and the threshold lengths match each other. In case of perturbation in the direction of elbow extension, the matching is observed at the left intersection point in Fig. 1. This may be used to find an analytical expression for epsilon m and P. As described in the INTRODUCTION, the actual and threshold muscle lengths are compared at the level of MNs (Feldman 1986). Information on the actual length and velocity is conveyed by muscle spindle afferents to MNs with a delay d (about half of the total delay in the reflex loop). As a consequence, if tau  is the duration of muscle stretch leading to Ag1 activation, the values of the muscle length and velocity associated with the Ag1 onset are defined by the time tau  - d (instead of tau ) in Eq. A4. These values of muscle length and velocity should be used in Eq. 2 for lambda * and then in the condition of muscle activation (x - lambda * = 0). After simple algebraic transformations, this yields
ε<SUB>m</SUB>= 2[<IT>s</IT><SUP>∧</SUP>φ + (ρ<SUB>+</SUB>− ρ<SUB>0</SUB>)/<IT>h</IT>]/[(τ − <IT>d</IT>)(τ − <IT>d</IT>+ 2μ)] (A5)
Below are the numerical values and definitions of the parameters used in the computation of P according to Eqs. A2 and A5.

I = 0.08 - 0.1 kg/m2 (the range of the moment of inertia of the arm with the cast and manipulandum for different subjects).

sand  = 10 rad/s (the angular rate of changes in lambda , estimated experimentally, Abdusamatov et al. 1988).

phi  = 0.015 s (the required decrease in the onset time of the Ag1).

rho + = rho 0 = 0 (the components of the SR threshold associated with the reflex intermuscular interaction with and without perturbations, respectively).

h = 0.03 m (the moment arm of Ag1).

tau  = 0.035 s (the time between the onset of the load stimulus and Ag1 burst).

d = 0.01 s (about half of the total reflex delay).

µ = 0.05 s (the coefficient characterizing the dependency of the threshold on velocity; this value was identified in simulations of fast elbow movements, St-Onge et al. 1997).

On the basis of these values, we found that the minimal opposing torque P eliciting a decrease in the Ag1 onset by phi  = 15 ms should be in the range of 7.7-9.6 Nm. On the basis of this estimation, we used opposing and assisting load pulses of 8-15 Nm for different subjects.

Equation A5 shows that the acceleration required for a given change (phi ) in the Ag1 onset increases with the speed (sand ) of the central command and decreases with the duration of perturbation (tau ). The delay (d) reduces the efficiency of muscle stretch.

The use of zero values of rho + and rho 0 in the estimation of pulse torque P can be justified. Before the onset of the Ag1, strong facilitation of Ag1 MNs is combined with an inhibition of antagonist MNs. Therefore the reflex influences of antagonist muscle afferents on agonist MNs measured by rho 0 in the absence of perturbations were likely low. An opposing load stretching agonist muscles could further suppress the reflex influences from the antagonist to agonist muscles. In contrast, an assisting load eliciting an antagonist burst before the Ag1 (Figs. 2 and 4) could reinforce the reflex influence from the antagonist muscle afferents to agonist MNs and thus additionally increase the Ag1 onset time in response to an assisting load.

    FOOTNOTES

  Address for reprint requests: A. G. Feldman, Centre de Recherche, Institut de Réadaptation de Montréal, 6300 av. Darlington, Montreal, Quebec H3S 2J4, Canada.

  Received 21 May 1996; accepted in final form 26 November 1996.

    REFERENCES
Abstract
Introduction
Methods
Results
Discussion
References

0022-3077/97 $5.00 Copyright ©1997 The American Physiological Society