Effects of leg muscle tendon vibration on group Ia and group II reflex responses to stance perturbation in humans

doi:10.1113/jphysiol.2003.043331

Effects of leg muscle tendon vibration on group Ia and group II reflex responses to stance perturbation in humans

Marco Bove *, Antonio Nardone † and Marco Schieppati †‡

* Department of Experimental Medicine, Section of Human Physiology, University of Genoa, † Posture and Movement Laboratory, Division of Physical Therapy and Rehabilitation, Scientific Institute of Veruno, Salvatore Maugeri Foundation (IRCCS) and ‡ Human Movement Laboratory (CSAM), Salvatore Maugeri Foundation (IRCCS), Scientific Institute of Pavia and Section of Human Physiology, Department of Experimental Medicine, University of Pavia, Italy

ABSTRACT

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Abstract
Introduction
Methods
Results
Discussion
References

Stretching the soleus (Sol) muscle during sudden toe-up rotations of the supporting platform in a standing subject evokes a short-latency response (SLR) and a medium-latency response (MLR). The aim of the present investigation was to further explore the afferent and spinal pathways mediating the SLR and MLR in lower limb muscles by means of tendon vibration. In seven subjects, toe-up or toe-down rotations were performed under: (1) control, (2) continuous bilateral vibration at 90 Hz of Achilles' tendon or tibialis anterior (TA) tendon, and (3) post-vibration conditions. Sol and TA background EMG activity and reflex responses were bilaterally recorded and analysed. Toe-up rotations induced SLRs and MLRs in Sol at average latencies of 40 and 66 ms, respectively. During vibration, the latency of both responses increased by about 2 ms. The area of the SLR significantly decreased during vibration, regardless of the underlying background activity, and almost returned to control value post-vibration. The area of Sol MLR was less influenced by vibration than SLR, the reduction being negligible with relatively high background activity. However, contrary to SLR, MLR was even more reduced post-vibration. Toe-down rotations induced no SLR in the TA, while a MLR was evoked at about 81 ms. The area of TA MLR decreased slightly during vibration but much more post-vibration. SLRs and MLRs were differently affected by changing the vibration frequency to 30 Hz: vibration had a negligible effect on the SLR, but still produced a significant effect on the MLR. The independence from the background EMG of the inhibitory effect of vibration upon the SLR suggests that vibration removes a constant amount of the Ia afferent input. This can be accounted for by either presynaptic inhibition of group Ia fibres or a 'busy-line' phenomenon. The differential effect of vibration on SLRs and MLRs is compatible with the notions that spindle primaries have a higher sensitivity to vibration than secondaries, and that group II afferent fibres are responsible for the production of the MLR. The decrease of MLRs but not SLRs after vibration is discussed in terms of an interaction between peripheral and central drive on group II interneurones in order to produce sufficient EMG activity to maintain a given postural set.

(Resubmitted 19 March 2003; accepted after revision 23 April 2003; first published online 30 May 2003)
Corresponding author M. Schieppati: Centro Studi Attività Motorie (CSAM), Fondazione Salvatore Maugeri (IRCCS), Via Ferrata 8, 27100 Pavia, Italy. Email: mschieppati{at}fsm.it and marco.schieppati@unipv.it

INTRODUCTION

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Abstract
Introduction
Methods
Results
Discussion
References

When the soleus (Sol) muscle is stretched, as occurs during a sudden toe-up rotation of the supporting platform in quiet standing subjects, two EMG bursts are evoked with different delays.

An early or short-latency response (SLR) occurs at about the latency of the monosynaptic reflex arc, and is mediated by group Ia large afferent fibres from spindle primaries. This is followed by a medium-latency response (MLR), which previous studies indicate is transmitted to the spinal cord by group II afferent fibres from spindle secondary terminations (reviewed in Schieppati & Nardone, 1999). Recording of the MLR and SLR from both proximal (Sol) and distal (flexor digitorum brevis, FDB) muscles showed that the MLR delay with respect to that of the SLR was more pronounced in distal than in the proximal muscles (Schieppati et al. 1995; Nardone et al. 1996). This was explained by differences in the peripheral pathways along which the impulses of the group II fibres travel (Schieppati et al. 1995; Nardone & Schieppati, 1998), rather than travelling by a more circuitous central pathway such as a transcortical long loop as probably occurs in the human upper limb (Noth et al. 1991). Further evidence for the hypothesis that group II fibres are responsible for the late reflex response was conveyed by the observation that the MLR, but not the SLR, also occurs in the homonymous contralateral muscle, in the absence of muscle stretch (Corna et al. 1996). Moreover, cooling of the entire length of the peripheral nerve induced a larger delay in the MLR than in the SLR in both Sol and FDB muscles (Schieppati & Nardone, 1997). Such an effect cannot be produced by any long-loop central pathway, but may be due to the different sensitivity to cooling of fibres of different diameter (Paintal, 1965). The amplitude of the MLR, but not of the SLR, in leg muscles is also susceptible to changes in 'postural set' (Schieppati & Nardone, 1995). In fact, when posture of standing subjects not stabilised by an external support is perturbed, a full-size MLR occurs (Nardone et al. 1990a); on the other hand, when subjects support themselves by holding on to a stable frame, the same foot rotation elicits smaller-size responses, on average less than 20 % of the control value (Nardone et al. 1990b). Interestingly, the same effect is induced by administration of tizanidine (Corna et al. 1995), a noradrenergic $alpha$ 2 agonist agent normally used to alleviate spasticity. Compared to animal data (see Jankowska, 1996), this finding led to the conclusion that monoaminergic brain stem centres selectively modulate the excitability of the interneuronal pathways responsible for the transmission of group II input from spindle secondaries to motoneurones (Schieppati & Nardone, 1999).

The aim of the present investigation was to obtain further evidence for a group II origin of MLRs to stretch in the lower limb muscles and to obtain clues about the central actions of group II fibres in standing humans. To this end, mechanical vibrations were applied to Sol or tibialis anterior (TA) muscles in standing humans. Muscle tendon vibration is an adequate stimulus for the spindle receptor. As reported by Burke et al. (1976), both human primary and secondary spindle endings respond to vibration stimuli. However, the Ia afferent fibres from the muscle spindle primaries are far more sensitive and fire at every vibration cycle over a wide range of frequency rates, whilst secondary endings normally respond with a discharge frequency at a sub-harmonic of the vibration. The working hypothesis of this investigation was that vibration would selectively decrease the amplitude of the SLR through either: (1) an inhibitory presynaptic spinal pathway activated by group Ia afferent fibres (Eccles et al. 1962; Gillies et al. 1969); or (2) a 'busy-line' effect, which would prevent the vibration-locked discharge of the Ia fibres from substantially increasing in response to muscle stretch (Hagbarth et al. 1973), or through both. Conversely, vibration would not affect the amplitude of the MLR, since the input for the MLR is transmitted through group II afferent fibres and relayed to the motor pool through a different spinal circuit with respect to the SLR (Jankowska, 1992; Nardone & Schieppati, 1998). If anything, any decrease in amplitude of the MLR occurring during vibration would be connected with a disfacilitation of group II interneurones caused by a reduction of stretch-induced Ia input during vibration, since animal and human experiments have shown that the interneurones mediating the MLR also receive a converging input from group Ia fibres (Vilis & Cooke, 1976; Burke et al. 1978; Hendrie & Lee, 1978; Lee & Tatton, 1982; Jankowska, 1992; Riddel et al. 1993). The effect of withdrawing vibration was also tested, to verify the possibility of different rates of adaptation of the two reflex circuits to the augmented tonic Ia input.

METHODS

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Abstract
Introduction
Methods
Results
Discussion
References

Subjects and platform perturbations

Seven normal subjects (five males and two females, aged 23-43 years, mean 33.4 years) volunteered for the experiments. Subjects gave informed consent and the study was in conformity with the Declaration of Helsinki. Subjects were asked to stand with eyes open, arms by their side and bare feet spaced 8-10 cm apart, both feet being placed on a movable platform (Lomazzi, Italy). Platform movements consisted of toe-up (upward tilt) or toe-down rotations (downward tilt), which induced stretch and consequent reflex responses in Sol and TA muscles, respectively. The velocity of platform rotations was 50 deg s^-1 for a duration of 60 ms. At the end of the rotation, the platform stopped at +3 or -3 deg from its initial position (Fig. 1 and Fig. 6, top row). Each subject underwent several series of perturbations in each direction. A series consisted of 20-50 trials, including both plantar-flexing and dorsal-flexing platform rotations. The time interval between each trial within a series varied randomly from 8 to 15 s.

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Figure 1. Example of stretch responses of soleus induced by a toe-up platform rotation under control, vibration and post-vibration conditions
A, amplitude of platform displacement was 3 deg, velocity of rotation 50 deg s^-1, equal under all experimental conditions. B, an accelerometer was used to monitor the frequency of the vibration. The post-vibration condition was characterised by a rapid decrease in amplitude and frequency of the vibration. C, in the soleus muscle, short- and medium-latency EMG responses (SLR and MLR) were evoked by a sudden toe-up rotation. D, background EMG activity of the soleus and the antagonist muscle, tibialis anterior (TA), in the three different conditions.

Tendon vibration

Stimulation was carried out by means of two electromechanical vibrators. These consisted of a DC motor with an eccentric on the shaft embedded in a plastic tube 3 cm in diameter and 6 cm long (Dynatronic, France). The cylinder axis of the vibrators was normal to the direction of Achilles' tendons or TA tendons, respectively, in the case of toe-up and toe-down rotations of the supporting platform. Since group II input is bilaterally distributed to the spinal circuits mediating the MLR (Corna et al. 1996), the vibration was delivered bilaterally in order to avoid missing any effect of Ia fibres on interneurones mediating ipsi- and contralateral MLRs. Further, the presence of crossed group II effects would lead to an underestimation of any decrease in amplitude of the MLR of the vibrated muscle, in the case that vibration also affected spindle secondary afferents. Vibrators were tightly fixed to the tendons by large elastic bands. They were driven at a frequency of 90 Hz by a control unit. The vibrators produced a peak-to-peak force of 5 N, as registered by a strain gauge coupled to the vibrator, and exerted an acceleration of ± 10 g normal to the tendon, measured by a one-axis accelerometer (model FA201; FGP Instrumentation, France). During the experiment, the accelerometer was attached to the vibrator on the right leg in order to continuously monitor amplitude, frequency and time course of the vibration applied to the tendons (Fig. 1B and Fig. 6B). In three cases, in order to measure the vibrator displacement in the direction normal to the tendons, two markers were attached to the shaft of the vibrator fixed to the tendon. The horizontal displacement of the vibrator along the sagittal plane was acquired by means of a stereometric device at a sampling frequency of 120 Hz (Vicon 460, Oxford Metrics, UK). The displacement was taken as the peak-to-peak amplitude of the sinusoidal trace thereby produced, measured over all vibration cycles recorded in 1 s. These measures were performed for both Sol and TA tendon positions. The peak-to-peak displacement of the vibrator proved to be between 0.8 and 0.9 mm at 90 Hz vibration frequency. These values are close to those reported in the literature for analogous vibration stimulation in humans (Hendrie & Lee 1978; Cody et al. 1987; Roll et al. 1989). A calculation was made to extrapolate the extent of the longitudinal vibration of the muscle based on this value of horizontal displacement at the vibrator position on the tendon (5 cm cranial to the heel insertion). Assuming a Sol muscle plus tendon length of 25 cm, the above transverse displacement should have produced a longitudinal component of some 10 µm. Local effects, however, could have been fairly large. In three subjects, the experiments were repeated with a vibration frequency of 30 Hz, based on the hypothesis that such a frequency of vibration would exert a selective effect on group II fibres (Roll et al. 1989). At this frequency, the peak-to-peak displacement of the vibrator was about 0.3 mm.

Experimental procedure

In each subject, three series of Sol muscle EMG responses to postural perturbations (toe-up rotation) were collected under three different experimental conditions. In one session, a first series without vibratory stimuli (control) was recorded. Then, in the following series, the vibrators on the Achilles' tendons were switched on and kept on for the entire duration of the series (vibration). Each series of perturbations lasted about 15 min. During this period, a few pauses were intermingled. A third series of trials was performed to observe the possible persistence of vibration-induced effects on the reflex responses immediately after the vibration offset (post-vibration). In another session, the tendon of the TA was bilaterally vibrated and the reflex responses of TA muscles were recorded after toe-down platform rotation, again under the control, vibration, and post-vibration conditions.

To quantify the persistence of the effects on the reflex responses occurring immediately after the vibration offset, the vibrators were shut off and the platform perturbation was triggered after a short, variable delay period. This delay was randomly chosen within the first few hundreds of milliseconds from the vibration offset. The delay from the end of vibration was not calculated from the instant of switch-off, owing to the persistence of rotation of the vibrator eccentric after the power supply was switched off. To define the delay, we calculated the instant at which the peak-to-peak amplitude of the tapering accelerometric signal decreased below 1 S.D. of the signal during vibration. After this instant, the residual vibration was not only very small in amplitude but also decreased in frequency.

EMG recording

EMGs were recorded using surface electrodes. The distance between leads was about 3 cm. Electrodes were positioned over the muscle bellies, 3 cm below the insertion of the gastrocnemii to record the activity of the Sol, and on the upper third of the leg close to the shin for the TA, on both legs. EMG signals were amplified ( times 10 000), band-pass filtered (100 Hz to 3 kHz, -6dB octave^-1), analog-to-digital converted at a sampling frequency of 1 kHz, and fed into a personal computer together with the platform position signal. Subjects were occasionally asked to assume various slightly forward-inclined postures in order to obtain a set of trials characterised by reflex responses pertaining to several values of Sol background EMG activity. As an aid to doing this they could view their rectified and filtered (time constant 100 ms) EMG traces displayed on an oscilloscope. The acquisition period was 500 ms, with the platform rotation starting at 100 ms from the acquisition onset.

EMG processing

Latencies of EMG responses were measured using the onset of platform rotation as the reference point. The onset of responses was taken as the moment at which the EMG signal rose above 2 S.D.s of the mean level of its pre-stimulus background EMG activity, averaged over 100 ms. Responses in the stretched Sol were classified as SLR or MLR when their onset latencies were shorter or longer than 60 ms, respectively. The responses in the stretched TA consisted only of MLRs (see Dietz, 1992) occurring at a latency longer than 60 ms. Measures of the SLR and MLR areas were performed on the average of the rectified and filtered (time constant 1 ms) EMG traces (Fig. 2 and Fig. 7). The areas were measured in a time window of 20 ms (for Sol SLR and MLR) or 30 ms (for TA MLR) from the onset of the responses. The same time windows were then used to measure the areas of the responses in each single trial under control, vibration and post-vibration conditions. In order to compare findings across all subjects, both EMG responses and 100 ms pre-stimulus background activity of each subject were normalised with respect to an EMG activity of equivalent duration recorded during maximal voluntary activity (MVA) of Sol or TA muscles. Reflex responses and Sol background EMG activity areas were defined as a percentage of the MVA, evaluated for the same time duration and related to each subject. In some trials, the responses were characterised by an EMG area greater than the MVA. This may have been due to the fact that during MVA subjects were required to tonically sustain the activation of the Sol muscle for approximately 3 s. The epoch of acquisition of EMG MVA signal began 2 s after MVA onset and lasted 500 ms.

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Figure 2. Averaged soleus short- and medium-latency EMG responses evoked by a toe-up rotation under control, vibration and post-vibration conditions
A, in a quiet standing subject, a sudden toe-up rotation of the supporting platform evoked SLR and MLR in the soleus muscle. Vertical dotted line indicates the onset of platform movement. B, during vibration, with respect to control condition, SLR decreased to a larger extent than MLR. C, SLR recovered immediately after the vibration offset, whilst a further depression of MLR was observed in this condition. Each trace corresponds to the average of 30 rectified and filtered EMG signals from a representative subject.

Statistical analysis

The areas of all EMG responses and background activities and the latencies of the responses were analysed as the mean of all trials from the right and left limb, separately for each subject. The overall averages of the data are presented as means ± S.E.M. A linear regression analysis of the MLR area as a function of SLR area, evaluated trial-by-trial in control and vibration conditions was made. A Student's t test assessed the slope and the intercept of the regression lines fitted through the data points (Armitage, 1971). Except when explicitly stated, an ANOVA was performed, either between the areas of the four EMG activities for toe-up platform rotation (Sol and TA background, Sol SLR and Sol MLR bursts) or between the areas of the three EMG activities for toe-down rotation (Sol and TA background, TA MLR burst) as independent variables, and under control, vibration and post-vibration conditions as repeated measures. For the latency of onset of EMG responses to toe-up rotations, an ANOVA between two responses (Sol SLR and Sol MLR bursts) as independent variables, and control, vibration and post-vibration as repeated measures was performed. For toe-down rotations, an ANOVA of TA MLR latency under control, vibration and post-vibration as repeated measures was performed. When ANOVA gave a significant (P < 0.05) result, the Newman-Keuls post hoc test was employed to assess differences between control, vibration and post-vibration conditions.

RESULTS

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Abstract
Introduction
Methods
Results
Discussion
References

Effect of vibration of Achilles' tendon on SLR and MLR of soleus muscle

Figure 1 shows an example of EMG raw signals recorded from Sol (Fig. 1C) during a toe-up platform rotation (Fig. 1A), along with the background activity of TA (Fig. 1D) under the three experimental conditions (control, vibration and post-vibration). Figure 2 shows a typical rectified and averaged Sol muscle response of one leg under the same conditions. Both figures show that the SLR was strongly decreased with respect to control during vibration of the Achilles' tendon, whilst the MLR was less affected. Shortly after the vibration offset, the SLR almost completely recovered. On the contrary, the MLR did not recover and in many trials it was depressed.

Within each subject, the range of values of Sol background EMG activity, though similar, was not necessarily identical between control, vibration and post-vibration conditions. Therefore, in order to assess the effect of vibration on the areas of the SLR and MLR, in each subject, only those trials showing equal Sol background areas in the three conditions were further analysed. Backgrounds had to be similar across conditions for both Sol and TA, since the activity in the antagonist TA might produce reciprocal inhibition on the Sol SLR and MLR bursts. The percentages of trials not analysed were 8, 5, and 15 % for control, vibration and post-vibration, respectively.

In order to assess the effect of the level of background activity on the areas of SLR and MLR under control, vibration and post-vibration conditions, trials with background Sol EMG activity lower than the median value were separated from those trials with background activity higher than the median value. The median values of the areas of the two populations of SLRs and MLRs thus obtained were calculated and compared (Fig. 3). The ANOVA (2 backgrounds times 2 responses times 3 conditions) showed a significant effect of background level on the areas of both responses (F = 11.67; degrees of freedom (d.f.) = 1, 24; P < 0.005): both responses were larger at higher background EMG. The three conditions affected the responses to a significantly different extent at both background levels (F = 35.75; d.f. = 2, 48; P < 0.001): vibration decreased the SLR but not the MLR, while post-vibration conditions further decreased the MLR at a time when the SLR recovered. A significant interaction was found between responses and conditions (F = 8.17; d.f. = 2, 48; P < 0.001). The SLR values at low and high background EMG appeared to be equally affected by vibration. During vibration, SLRs decreased to about 76 % (post hoc test, P < 0.01) and 74 % (P < 0.001) of control value, with small and large background EMG, respectively. During post-vibration, SLRs recovered to 85 % (P = n.s.) and 84 % (P < 0.05) of their respective control values. When the areas of all SLRs were plotted against their respective Sol background EMG activities, a positive slope was found (control: y = 55.30 + 0.95x; P < 0.001). Vibration did not affect the slope of this relationship (vibration: y = 38.02 + 1.07x; P < 0.001) but induced a significant decrease (ANOVA, P < 0.001) of the intercept of the best-fitting line with respect to the control condition. Unlike SLRs, MLRs were significantly diminished by vibration at low but not at high background EMG. Areas of the MLRs during vibration were about 68 % (P < 0.05) and 94 % (P = n.s.) of the control value, with small and large background, respectively. During post-vibration, MLRs further decreased to 58 % (P < 0.001) and 70 % (P < 0.005) of control values.

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Figure 3. Overall averages of the areas of Sol SLR and MLR under control, vibration and post-vibration conditions as percentages of maximal voluntary EMG activity (MVA), subdivided on the basis of the median values of areas of Sol background activity prior to platform rotation
The effect of vibration and post-vibration on SLR (A) and MLR (B) was evaluated separately for the trials exhibiting Sol background EMG activity lower (open columns) or higher (filled columns) than the median value. The mean areas of the background (bkg) EMGs of Sol and TA are reported in C and D, respectively. Area of the SLR was decreased during vibration and recovered towards control value during post-vibration. This behaviour was common to both background levels. MLR also decreased during vibration, but this was significant only for low background EMG activity. During post-vibration, MLR area further decreased. In this and in the following figures, * = P < 0.05, ** = P < 0.01, *** = P < 0.001.

Since the SLR and MLR actions are probably expressed in the same motoneurone pool (Calancie & Bawa, 1984), it could be that the MLR would be taking place in a motoneurone pool made refractory by the preceding SLR burst (both because of motoneurone afterhyperpolarisation and recurrent inhibition) (Fellows et al. 1993). To verify this point, the area of the MLR was plotted against the area of the SLR, under control and vibration conditions. Figure 4 shows that there was no negative relationship between the areas of MLRs and SLRs under any condition, i.e. small-amplitude MLRs were not necessarily evoked after large SLRs. In particular, under control conditions, no relationship was found between the areas of the two responses (y = 54.41 + 0.08x; P = n.s.). Further, under vibration conditions, the decrease in amplitude of SLRs was accompanied by a significant decrease in MLRs, and vice versa (y = 26.01 + 0.45x; P < 0.001). These phenomena, taken together, are at odds with the conclusion that any decrease in the size of an MLR could be related to a previous SLR burst making the motoneurone pool refractory to a subsequent input.

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Figure 4. Relationship between the areas of Sol MLR and of Sol SLR under control and vibration conditions as percentages of maximal voluntary EMG activity (MVA)
The lack of negative relationship between area of MLR and area of SLR (control condition, A) points against the notion that any decrease in the size of MLR was related to the size of the previous SLR burst. This finding is opposite to what would occur if the motoneurone pool was made refractory to a subsequent input by the SLR burst. B, under vibration conditions, the vibration-induced decrease in size of the SLR is not accompanied by an increase in size of the MLR.

Time course of changes in amplitude of SLR and MLR during the post-vibration period

One aim of the study was to assess the effect of withdrawing vibration on the SLR and MLR, and to verify the possibility of different adaptation rates of the two reflex circuits to the augmented tonic Ia input. The results show that during post-vibration, SLRs and MLRs behaved differently, the former recovering almost completely towards the control value, while the latter further decreasing with respect to the value during vibration. To analyse the time course of the changes in size of the SLR and MLR, we divided the period between termination of vibration and onset of platform movement into intervals lasting 50 ms each. Figure 5 shows that the area of the SLR recovered towards the control value after the 225 ms interval (at this interval its area became significantly larger than that during vibration). On the other hand, the area of the MLR continued to decrease during the whole acquisition epoch, being still depressed at around an interval of 275 ms after the end of vibration.

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Figure 5. Time course of the changes in area of Sol SLR () and MLR () during post-vibration as a function of the time interval between termination of vibration and onset of platform movement
The area of the SLR tended to recover immediately after vibration offset. It was still depressed, though significantly less than during vibration, at 275 ms after the end of vibration. The area of the MLR continued to decrease. Open and filled points represent the means ( ± S.E.M.) of the areas of Sol SLR and MLR, respectively, averaged from each subject within the corresponding 50 ms time intervals between onset of platform movement and termination of vibration. For comparison, the means of the areas of Sol SLR and MLR during control and vibration conditions are shown on the left.

Effect of vibration on tibialis anterior MLR

As has already been described in other investigations (Nardone et al. 1990b; Schieppati & Nardone, 1995), the TA muscle showed a medium-latency burst alone in response to toe-down rotation of the supporting platform (Fig. 6). Figure 7 shows an example of the TA muscle responses averaged from 30 rectified and filtered trials. As shown for the Sol muscle, the MLR was only marginally decreased during vibration of TA tendons (Fig. 7B) with respect to the control condition (Fig. 7A). However, the Fig. 7C shows a strong decrease in MLR amplitude immediately after the vibration offset.

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Figure 6. Example of tibialis anterior (TA) medium-latency response (MLR) evoked by a toe-down platform rotation, under control, vibration and post-vibration conditions
Perturbations consisted of toe-down rotations delivered in the three experimental conditions. Same traces and layout as in Fig. 1.

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Figure 7. Averaged TA MLR evoked by a toe-down rotation under control, vibration and post-vibration conditions
A, in TA muscle an MLR can be evoked by a sudden toe-down rotation. B, during vibration, a slight and non-significant decrease of MLR with respect to control condition was observed. C, MLR was significantly depressed immediately after the vibration offset. Each trace is the average of 30 rectified and filtered EMG signals from a representative normal subject. Vertical dotted lines indicate the onset of platform movement.

In order to avoid the presence of uncontrolled effects produced by the activity of the antagonist Sol muscle, only trials having similar values of Sol background EMG activity were selected for analysis. Within and across subjects, the range of values of the TA background EMG activity, though similar, was not identical between control, vibration and post-vibration conditions. Therefore, in order to assess the effect of vibration on the area of the MLR, in each subject only those trials with equal values of TA background area in the three conditions and less than 5 % of the TA maximal voluntary activity were analysed. Thus, the percentages of trials not analysed because of these restriction criteria were 16, 23 and 25 % for control, vibration and post-vibration conditions, respectively. The mean area of response was then calculated.

Figure 8 shows the overall average of the TA MLR, Sol and TA background EMG activity in control, vibration and post-vibration conditions. ANOVA showed significantly different changes (F = 15.04; d.f. = 2, 18; P = 0.01) in the area of TA MLR, comparing the three conditions. In spite of no change in the areas of background activity of TA and Sol, a significant decrease in the area of the MLR was evident during post-vibration. During vibration, the MLR decreased to only about 88 % of control values. On the other hand, a significant depression effect on MLR, which reduced the response to about 56 % of the control condition, was observed in the post-vibration condition (post hoc test, P < 0.001).

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Figure 8. Overall averages of the areas of TA MLR and TA background activity and Sol background activity under control, vibration and post-vibration conditions as percentages of maximal voluntary EMG activity (MVA)
A, the effect of vibration and post-vibration on the area of TA MLR was evaluated for equal background EMG activity (bkg) of Sol (B) and TA (C). Significant depression of MLR occurred only during the post-vibration condition. This behaviour was similar to that observed in the Sol MLR during a toe-up rotation when the Sol background was greater than its median value.

Effect of vibration on the onset latency of Sol SLR and MLR and TA MLR

No relationship was found between the areas of Sol or TA background activity and the latencies of Sol SLR, Sol MLR or TA MLR across trials and subjects. This was assessed by testing any significance in the slope of the relative regression lines.

Figure 9 (top and middle columns) shows the overall average of onset latencies of Sol SLR and MLR to toe-up rotation in the control, vibration and post-vibration conditions. ANOVA showed a significant effect of the three conditions on the latencies of Sol SLR and MLR to toe-up (F = 15.03; d.f. = 2, 24; P < 0.001). No interaction was found between responses and conditions, pointing to similar changes in the latencies of Sol SLR and MLR under vibration and post-vibration. Vibration induced a significant delay of about 2 ms in Sol SLR and about 3 ms in Sol MLR with respect to control values (post hoc test, P < 0.05 and P = 0.001, respectively). For both responses, this delay disappeared almost completely when the vibrator was shut off.

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Figure 9. Overall averages of the latency of Sol SLR and MLR and TA MLR under control (), vibration () and post-vibration () conditions
The latency of Sol SLR and MLR and TA MLR was increased during vibration. This extra delay tended to vanish in the Sol responses when the vibrator was shut off. On the other hand, TA MLR showed a further delay during post-vibration.

Figure 9 (bottom columns) shows the overall average of onset latencies of TA MLR to toe-down in the three conditions. ANOVA showed that the latency was significantly (F = 7.16; d.f. = 2,12; P < 0.01) affected by the conditions. The latency increased by about 5 and 11 ms during vibration and post-vibration, respectively. The increase in latency was significant post-vibration with respect to control (P < 0.01) and vibration (P < 0.05), but only marginally so (P = 0.15) during vibration with respect to control, due to the rather large variability of the latencies of the TA MLR bursts in the vibration condition.

Effect of changes in vibration frequency

In three subjects, three different vibration frequencies (30, 50 and 70 Hz) were employed in order to identify a possible specific effect of group II spindle fibres, since secondary afferent fibres can respond more to low-frequency than to high-frequency vibration (Roll et al. 1989). These vibrations were applied to both Sol and TA muscles in two different experimental sessions. All in all, there were no major qualitative differences in the effects: only a progressive diminution of the effects with the diminution of vibration frequency was observed. However, one difference deserves a mention. Figure 10 compares the findings obtained for the Sol muscle responses at 30 Hz with those obtained at 90 Hz. It shows that, while the depression of the SLR vanished at 30 Hz vibration frequency, the MLR still appeared to be influenced (P < 0.005).

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Figure 10. Overall averages of the areas of Sol background, Sol SLR, Sol MLR and TA background under control () and 30 Hz () and 90 Hz () vibration conditions, as percentages of maximal voluntary EMG activity (MVA)
In spite of no difference in the area of Sol and TA background activity among the three conditions, a significant depression of SLR could be observed at 90 Hz but not at 30 Hz vibration frequency. MLR appeared to be influenced by both vibration stimuli.

DISCUSSION

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Abstract
Introduction
Methods
Results
Discussion
References

Sol SLR

Long-standing Achilles' tendon vibration induced in all subjects a clear depression of the SLR of Sol muscle to a toe-up rotation of a movable platform upon which subjects stood upright. Such an effect would be the counterpart of the well-known decrease in the amplitude of the Sol tendon tap- and H-reflexes during tendon vibration (Schieppati & Crenna, 1984; for a review, see Pierrot-Deseilligny, 1997). On average, vibration reduced the response amplitude by about 25 % with respect to control. This effect was not related to changes in the activity of the antagonist TA muscle: possible effects of the level of TA background were singled out by analysing only those trials whose average produced a constant background value under control, vibration and post-vibration conditions. The similar effect of vibration at different background EMG levels, and the constant slope of the relationship between area of the SLR and background level across all trials indicate that vibration did not change the $alpha$ -motoneurone gain but, rather, removed a constant amount of the afferent input. Vibration also had an effect on the onset latency of SLR, which was increased by about 2 ms.

These depressive effects, though certainly not negligible and clearly statistically significant, were however of moderate extent. We explain this fact based on the small amplitude of the longitudinal muscle changes produced by the tendon vibration, which was estimated to be around 10 µm. On the other hand, it is notable that this relatively weak vibration was nonetheless able to produce marked postural effects, since, when subjects were requested to close their eyes in preliminary trials devoted to establishing the appropriate position of the vibrators on the tendons, they had a tendency to fall backwards. This is an indirect sign of spindle activation, as indicated by several studies on human posture (Eklund 1972; Gurfinkel et al. 1977).

The vibration-induced effects on SLR persisted, though progressively diminishing, after vibration. The response tended to recover to control condition after the vibration offset, and its amplitude became not significantly different from the value during vibration after the 225 ms interval from the end of vibration. Ribot-Ciscar et al. (1998) have presented results concerning the persistence of a temporary reduction in stretch sensitivity of the primary endings of the resting TA muscle after vibration offset. Such a phenomenon was characterised by a decrease in the firing frequency of the primary endings lasting several seconds. In our standing subjects, this decreased stretch sensitivity of the spindle terminations seemed to play no major role, since the SLR to stretch started recovering immediately after vibration and steadily increased within the range of the analysed post-vibration intervals.

Considered together, the findings obtained under vibration and post-vibration conditions do not allow a determination of the cause of the decrease in SLR amplitude. For example, it is unclear whether such a decrease was due to a reduction in the Ia synaptic input, feeding the $alpha$ -motoneurone pool, determined by a pre-synaptic inhibition of the group Ia afferent fibres, or by a 'busy-line' effect reducing the Ia afferent input to the spinal cord (Hagbarth et al. 1973). It is likely, however, that both contributed to the decreased response. The presence of a significant delay in the onset latency during vibration suggests that the Ia fibres with the highest conduction velocity were rendered 'busy' by the vibration and therefore less responsive to the platform-induced muscle stretch. The delayed latency would then be the consequence of a greater sensitivity of the fastest fibres to the vibratory stimulation. The fact, however, that the recovery of the SLR excitability was not immediate (the amplitude did not reach 100 % of the control response immediately after vibration) cannot allow us to exclude a mechanism of presynaptic inhibition among the factors responsible for the response depression. In fact, the presynaptic inhibition effects can outlast vibration offset and persist beyond the time at which the muscle was stretched by the platform displacement (Eccles et al. 1962; Hultborn et al. 1987; Ashby et al. 1987; Cheng et al. 1995; Morita et al. 1998). Monosynaptic reflexes can also be depressed by the ongoing discharge of muscle spindles in the homonymous muscle, through a mechanism different from the classical presynaptic inhibition (Hultborn et al. 1996; Wood et al. 1996). But the homosynaptic depression, probably caused by a presynaptic effect different from the classical GABAergic presynaptic inhibition and related to the phenomenon of a reduced transmitter release from previously activated fibres, is even longer-lasting than the presynaptic inhibition (Kohn et al. 1997).

Sol MLR

The MLR to stretch of Sol was differently influenced, with respect to SLR, by the continuous vibration and by vibration offset. During vibration, the behaviour of the MLR with respect to the SLR depended on the level of Sol background EMG activity. Vibration induced a significant reduction in the MLR, of about 32 %, only when the background activity was small. When the background activity was large, MLR reduction was only 6 % of the control value.

A generally minor reduction in MLR amplitude was expected, since no 'busy-line' effect would have taken place in the group II fibres, the latter being negligibly affected by vibration at the 90 Hz frequency used in the present investigation (McGrath & Matthews, 1973; Roll et al. 1989). In fact, one might suppose that this frequent longitudinal vibration would have activated mainly, if not almost selectively, the Ia fibres, which are more sensitive to rapid changes in muscle length than group II fibres (Matthews, 1972). The lesser reduction in amplitude of the MLR with vibration resembles the behaviour of late responses to stretch (M2-M3) in the wrist flexor muscles during vibration (Hendrie & Lee, 1978), and is in keeping with a transmission of both leg and wrist late responses through afferent fibres slower than Ia (Thilmann et al. 1991).

This minor effect would be consistent with animal findings showing the near absence of presynaptic inhibition of group II central terminals by group I fibres (Riddel et al. 1995; Jankowska et al. 2002a,b). We would rather interpret the moderate decrease in the MLR amplitude as a consequence of the 'busy-line' effect in the Ia fibres, since these, in addition to monosynaptically exciting the motoneurones, also impinge onto and facilitate the interneurones receiving group II input as shown in cat experiments (Edgley & Jankowska, 1987; Jankowska, 1992; Jankowska et al. 2002a). In this regard, it should be noted that the stretch-induced Ia discharge has ample time to affect group II interneurones, since a tendon-tap-induced volley can last as long as 65 ms (Türker et al. 1997), and the rise time of composite EPSPs is estimated to be around 10 ms in humans (Burke et al. 1984). The inhibitory effect of vibration on the MLR was significant only with low-level background EMG activity. This further suggests that part of the MLR burst is sustained by Ia input. Under this condition, probably associated with a low level of alpha-gamma coactivation and spindle afferent discharge, vibration would remove a sizeable amount of Ia afferent input to effectively reduce motoneurone discharge. Conversely, when the background EMG activity is high, the alpha-gamma coactivation would lead to large group Ia and group II inputs to the interneurones mediating the MLR. These additional inputs may counteract the effects of presynaptic inhibition during vibration. These data also suggest caution in interpreting results obtained from conditioning (by vibration or other types of stimuli) of stretch responses when background EMG activity is not duly taken into account.

In the post-vibration condition, the MLR strongly differed from the SLR. When the vibrator was shut off, a large decrease in Sol MLR was observed. The depression was progressive, at least within the intervals recorded. This effect could reach mean depressions of about 42 % and 30 % of control value, respectively, at low and high Sol background levels. This behaviour was in contrast to the prompt recovery observed in the SLR. Interestingly, this was true regardless of the level of Sol background EMG activity. As an additional note, it might be considered that we cannot exclude that a small proportion of group II afferent fibres was activated by vibration, in spite of the extremely small extent of the vibration-induced muscle lengthening. This is suggested by the small but significant decrease in the MLR when the vibrators were driven at 30 Hz. If indeed group II fibres were partly activated, it might be considered that the presynaptic inhibition of transmission from long-lasting activation of group II afferents potently reduces activation of group II interneurones (see Fig. 11). In fact, presynaptic inhibition from group II to group II afferents terminating on intermediate zone interneurones is very strong (Jankowska et al. 2002a) and could reduce the probability of activation of these interneurones within the post-vibration period analysed here. It could thus at least in part explain the strong post-vibration reduction of the MLR. This presynaptic inhibition from group II to group II afferents terminating on intermediate zone interneurones would be evident only on switching off the vibration. In fact, the vibration-induced Ia (and group II) input can be supposed to facilitate the group II interneurones, thereby counteracting the group II on group II presynaptic inhibition.

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Figure 11. Circuit diagram summarising the possible synaptic connections involved in the SLR and MLR, taking into account the effects observed during control, vibration and post-vibration conditions
For the sake of simplicity, the oligosynaptic connections fed by the group II afferents are represented by one interneurone (II-IN). White, dark grey and light grey arrows show the peripheral afferent drive and supra-spinal central drive, under the control, vibration and post-vibration conditions, respectively. Presyn-I refers to presynaptic inhibition. Note the divergent Ia input to $alpha$ -motoneurones ( $alpha$ MN) and group II interneurones (II-IN). Further explanations are in the text.

TA MLR

An MLR was also evoked in the flexor muscle TA by the toe-down rotation of the platform. Previous investigations have suggested that, also in the case of TA muscle, the MLR is transmitted by group II spindle afferent fibres (see Schieppati & Nardone, 1999). Vibration of the TA tendon had a minor effect on the TA MLR, producing a non-significant decrease of about 12 % with respect to the control value. Conversely, a further and significant decrease, to about 56 % of the control value, was observed post-vibration. These effects were therefore similar to those observed for the MLR of Sol muscle evoked by the toe-up rotation. The same considerations made above, for a possible implication of presynaptic inhibition from group II to group II afferents, can then be made also for the TA MLR.

Effect of vibration on response latencies

The latency of Sol MLR increased to a similar extent to that of the SLR during vibration. This finding would further support the assumption that interneurones mediating the MLR also receive input from Ia fibres, as shown in animal preparations (Edgley & Jankowska, 1987; Riddell et al. 1993). The blockage of the discharge in the latter fibres by the 'busy-line' effect would explain the increased latency of the MLR, since the group II volley would drive the group II interneurones to threshold with a delay connected to the delayed mounting of the preceding Ia facilitation. This blockage is not sufficient, however, to decrease to a major extent the excitability of the group II-receiving interneurones in response to the group II input. The interneurones are in fact driven by group II fibres, which are hardly affected by presynaptic inhibition from Ia afferents (Riddell et al. 1995; Jankowska et al. 2002a,b). As in Sol SLR and MLR, a vibration-induced delay of the onset latency of TA MLR was also observed, which was even larger than that of the Sol responses. The presence of this delay could suggest the existence of similar spinal pathways mediating the MLR of agonist and antagonist muscles such as Sol and TA. In other words, in spite of the poor strength of the monosynaptic reflex in the TA muscle (Nardone et al. 2001), the Ia fibres would nonetheless have access to the group II interneurones. The latency of the TA MLR, however, did not recover towards the control value following vibration: indeed, a further delay was observed, which cannot be readily explained. We can only postulate that the mechanisms responsible for the marked decrease in amplitude of the response during post-vibration, in addition to diminishing the number of spinal interneurones responding to the incoming volley, would also produce an increase in the time required to reach the excitation threshold.

Functional mechanisms

A hypothetical description of the possible spinal pathways and synaptic connections involved in the SLR and MLR is shown in the schematic circuit diagram depicted in Fig. 11. This supports a discussion of the vibration-induced effects and the remarkable post-vibration effects. Group Ia fibres project directly to $alpha$ -motoneurones via monosynaptic pathways. Motoneurones receive projections from group II interneurones which are fed by group II afferents through an oligosynaptic pathway responsible for the MLR. In the figure, white, dark grey and light grey arrows show the peripheral afferent and supra-spinal drives, under control, vibration and post-vibration conditions, respectively. We would argue that the strength of the multiple drives to the Sol motoneurones is different under the three experimental conditions. However, their sum must be the same under the three conditions, if the body has to stand with the same inclination in the sagittal plane - the final output of the postural muscle motoneurones must and did in fact produce the same ankle torque. Failure to respect this condition would induce the body to change its inclination. One can certainly assume that tendon vibration would produce a tonic vibration reflex (as repeatedly shown; see De Gail et al. 1966). However, this extra facilitation (normally responsible for an increment of EMG activity in the vibrated muscle) would be compensated for by a reduction in the central drive to the motoneurones of the postural muscles in standing subjects, so that the output of the final common pathway to these muscles remains the same. This was indeed so under the present conditions, since the background muscle activities were equal under control, vibration and post-vibration conditions when the platform perturbations were delivered. In passing, as a methodological remark, keeping the same level of background muscle activity during control, vibration and post-vibration conditions allows us to draw reliable conclusions from the analysis of reflex response amplitudes, since the importance of keeping the muscle and its spindles in a defined mechanical state when measuring reflexes has been emphasised recently (Gregory et al. 1998). We do not deny that some transient postural disturbance would be initially produced by vibration, as discussed in several reports (Eklund, 1972; Gurfinkel et al. 1977; Lackner & Levine, 1979). However, in our experiments, subjects had ample time to adapt to ongoing vibrations, i.e. to the ongoing increase in the peripheral drive along the Ia fibres. This was simply the consequence of the fact that the vibration was normally delivered for extended periods of time, while the muscle-stretching platform rotations were spaced at various intervals during the vibration.

Figure 11 illustrates that during control conditions, most of the excitatory drive to the motoneurones would come from supraspinal centres, and that this drive is partly direct, and partly mediated via the group II interneurones. During vibration, peripheral drive to the motoneurones would increase, mostly along the Ia fibres, directly, and via the Ia-induced increase in the efficacy of the group II drive relayed by the group II interneurones. In order to maintain the motoneurone output constant, the central nervous system (CNS) has the choice of reducing the central drive funnelled to the spinal cord and directed to either the motoneurones or the group II interneurones, or both. At the end of the vibration, the CNS of the standing subject has to return to its 'default' state, but the time to re-adapt to the abrupt failing of the vibration-induced extra facilitation may be not immediate, due to the induced changes in the postural 'set' (Schieppati & Nardone, 1995). Therefore, any peripheral input would encounter a spinal circuitry still devoid of the appropriate excitatory descending drive.

The SLR reduction during vibration with recovery post-vibration, and the mild reduction of the MLR during vibration, becoming even larger post-vibration, would indicate that the diminution of the central drive during vibration is mainly a diminution of the drive to the group II interneurones. The slow return of the central drive to the default 'set' value, in the absence of the augmented vibration-induced peripheral input, would explain the lasting inhibition of the MLRs (for both Sol and TA). The fact that during and after vibration the central drive to group II interneurones, but not to the monosynaptic reflex, might be decreased comes as no surprise. For several years it has been known that the MLR, even more than the SLR, is subject to a 'set'-dependent descending control. In fact, the amplitude of the MLR, but not the SLR, is reduced by changes in postural 'set' as when subjects stand and hold onto a stable frame during postural perturbations (Nardone et al. 1990a,b). This phenomenon has been shown not to be triggered by the stabilised posture itself but to originate from the descending commands leading to a transition to a new stabilised posture (Schieppati & Nardone, 1995). A similar phenomenon has been shown after administration of tizanidine, a powerful noradrenergic $alpha$ ₂-agonist drug (Corna et al. 1995): the area of the MLR but not the SLR is decreased, and the degree of reduction is similar to that observed when subjects stand and hold onto the stable frame. These findings suggest that noradrenergic pathways, possibly from the locus coeruleus (Noga et al. 1992), strongly modulate the group II interneurones but negligibly modulate the motoneurones (Bras et al. 1989). A differential descending control of the reflex pathways travelled by the group Ia and group II input also appears to occur during locomotion. Under this condition, a continuous vibration of both Achilles' tendons has a negligible effect upon kinematic and EMG characteristics of the gait pattern, pointing to a mechanism of gating of large-fibre spindle input to the spinal cord (Courtine et al. 2001). Conversely, it seems that stretch-reflex effects on the Sol muscles in walking are mediated by group II rather than group I inputs (Dietz et al. 1985; Grey et al. 2001).

To summarise, the present findings confirm the different natures of the peripheral and central pathways responsible for the SLR and MLR to stretch. Moreover, they show that the modulation of the reflex response to stretch of the postural muscles mainly occurs onto spinal circuits mediating the medium-latency burst, i.e. that triggered by the length-sensitive spindle secondary terminations. This descending control seems to take into consideration the fact that the mechanical action of the medium-latency burst exceeds that of the short-latency burst (Allum & Büdingen, 1979). Failure to appropriately control the excitability of the group II reflexes, as in Parkinsonian (Scholz et al. 1987; Schieppati & Nardone, 1991) and hemiparetic patients (Nardone et al. 2001), can indeed be one of the causes of postural instability. We would also speculate that, in order to control equilibrium in standing humans, sensory inflow from length-sensitive receptors overwhelms that from velocity-sensitive receptors.

REFERENCES

Top
Abstract
Introduction
Methods
Results
Discussion
References

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Acknowledgements

This research was supported by the Italian Ministry of Education (MIUR, Progetti di Ricerca di Interesse Nazionale 1999) and by the Italian Ministry of Health (Grant Ricerca Corrente 2001-2002).

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