- Email: [email protected]
Acute postural modulation of the soleus H-reflex after Achilles tendon vibration
Neuroscience Letters 523 (2012) 154–157
Contents lists available at SciVerse ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Acute postural modulation of the soleus H-reflex after Achilles tendon vibration Thomas Lapole, Francis Canon, Chantal Pérot ∗ Université de Technologie, Compiègne CNRS UMR 7338, Biomécanique et Bioingénierie, F-60205 Compiègne Cedex, France
h i g h l i g h t s Soleus H-reflex was reported to be decreased when standing compared to sitting position. After prolonged Achilles tendon vibration, this postural modulation was increased. Those results are discussed in terms of changes in presynaptic inhibition.
a r t i c l e
i n f o
Article history: Received 19 April 2012 Received in revised form 9 June 2012 Accepted 25 June 2012 Keywords: Achilles tendon Vibration Soleus Hoffmann reflex Postural modulation Presynaptic inhibition
a b s t r a c t Alteration of Soleus (SOL) H-reflex has been reported after prolonged vibratory exposure and it was hypothesized that presynaptic inhibition, known to depress the H-reflex during vibration, largely contributed to the H-reflex changes. To confirm this hypothesis, the purpose of the present study was to quantify the SOL H-reflex changes between sitting and standing positions (postural modulation) with or without the after-effects of 1 h of Achilles tendon vibration. Indeed, postural modulation of the SOL H-reflex has been reported to inform on the level of presynaptic inhibition exerted on Ia afferents. SOL H-reflex and M waves were measured in healthy voluntary subjects in both sitting and standing positions before and after 1 h of Achilles vibration (frequency: 50 Hz) applied in sitting position (vibration group, n = 11) or before and after 1 h of sitting position only (control group, n = 6). SOL Hmax /Mmax ratios were calculated. Furthermore, in order to quantify presynaptic inhibition induced by prolonged vibration, an index of SOL H-reflex postural modulation was calculated as the standing Hmax /Mmax ratio relative to the sitting one. After 1 h of Achilles tendon vibration, a significant decrease in the SOL Hmax /Mmax ratio was observed both in sitting and standing positions (p < 0.05). However, the decrease was more pronounced in the standing position, leading to a significant decrease of the index of SOL H-reflex postural modulation. Those results suggest that presynaptic inhibition could have largely contributed to the H-reflex decrease observed after one bout of vibration. © 2012 Elsevier Ireland Ltd. All rights reserved.
1. Introduction To propose the benefits of vibrations to subjects who cannot stand on a vibrating platform, we previously proposed a program based on chronic prolonged Achilles tendon vibrations [27]. Maximal isometric torque in plantar-flexion was enhanced after 14 days of 1 h daily vibration and this increase in torque was correlated to an increase in triceps surae activation capacities [27]. These increases could result from changes in volitional drive from the supra-spinal motor structures inducing a higher activation of ␣ motoneurons. Furthermore, changes in spinal excitability could also be expected since tendon vibration induces tonic vibration reflexes through activation of muscle spindle primary endings [7,12]. Indeed, the soleus (SOL) Hoffmann reflex (H-reflex), classical index of changes
∗ Corresponding author. Tel.: +33 3 44 23 43 92; fax: +33 3 44 20 48 13. E-mail address: [email protected] (C. Pérot). 0304-3940/$ – see front matter © 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neulet.2012.06.067
in reflex excitability [36], was increased after chronic Achilles tendon vibration [26]. The amplitude of the H-reflex depends on the motoneuron excitability [33] and on the synaptic efficiency of the Ia-␣ pathways, itself depending on the level of presynaptic inhibition exerted on Ia afferents [29]. Hagbarth and Eklund [15] were the first to report a strong depression in SOL H-reflex during a 100 Hz vibration exposure. Several authors latter demonstrated the same result [28,31]. Furthermore, when vibration is prolonged, it has been reported for the SOL an acute H-reflex depression that was almost recovered in 20 min [35]. This attenuation of Ia afferent efficiency was considered to result from several mechanisms such as the presynaptic inhibition of muscle spindles primary endings [3], an increased firing threshold of those Ia afferents [17], and the transmitter depletion at Ia-␣ synapses [10]. In our previous studies, it was hypothesized that chronic effects of prolonged Achilles tendon vibration were rather located on the presynaptic inhibition of Ia afferents [26].
T. Lapole et al. / Neuroscience Letters 523 (2012) 154–157
The modulation of the H-reflex amplitude is also known to be task-dependant [8]. Indeed, it was reported that presynaptic inhibition of Ia afferents plays a major role in the depression of SOL H-reflex in man while standing or walking [13,21]. Thus, the changes in H-reflex amplitude from prone to standing [25] or from sitting to standing [16] were accredited to presynaptic inhibitory mechanisms and proposed as an index allowing to quantify the weight of presynaptic inhibition. Since vibration was suggested to enhance the level of presynaptic inhibition, the induced effects should be posture-dependant, i.e., the decrease in H-reflex from sitting to standing should be higher after the vibratory exposure. The aim of the present study was therefore to confirm this hypothesis by investigating the acute effects of Achilles tendon vibration on the postural modulation of the SOL H-reflex. 2. Methods 2.1. Subjects 17 healthy and active voluntary subjects (age: 27.3 ± 3.5 years, mass: 70.5 ± 11.4 kg, height: 175.2 ± 8.8 cm) engaged in the study. They were assigned to the vibration group (n = 11) or the control group (n = 6). Written informed consent was provided by the subjects and they were fully advised of the procedures, and free to stop the experiment at any time. The experimental procedures were approved by the local Ethics committee of the University of Compiègne, France. 2.2. EMG recording
155
The position of the stimulating electrode was first adjusted so as to obtain at low intensity the maximal amplitude for the H-reflex, with no (or minimal) motor direct response (M-wave). This point was marked on the skin in order to ensure the same electrode placement between the different testing positions and conditions. At least 15 responses were recorded at the stimulus intensity giving the maximal H-reflex amplitude. Then, 5 responses were recorded at the intensity giving the maximal M-wave. Induced responses were stored and later averaged to give the maximal H-reflex Hmax and the maximal M-wave Mmax respectively. Interstimuli intervals were randomly used and were always more than 3 s to limit postactivation refractory period [36]. Experimental procedures were performed in both sitting and standing positions. Those measurements were performed a first time at the beginning of the testing session (PRE-Vib). Immediately after, subjects were submitted to an 1 h period of Achilles tendon vibration: as previously performed [27], the tendon vibrator (Techno-Concept, VB 115) was strapped on the Achilles tendon of the right ankle and vibration (amplitude: 1 mm; frequency: 50 Hz) was applied during 1 h in a seated position, the subjects being at rest. Just after the end of the vibration period, the same measurements as previously described were performed in order to determine the effects of vibrations on postural modulation of the SOL H-reflexes (POST-Vib). As the time of vibration employed in this study imposed to keep a sitting position during 1 h, we investigated whether this maintain of sitting position could affect H-reflexes. Thus, the control performed the same procedures before (PRE-Con) and after (POSTCon) prolonged seating for 1 h without vibration. 2.5. Data analysis
Electrical stimulations were applied using a constant current stimulator (DS7A, Digitimer Ltd., UK). This device delivered single electrical pulses (1 ms), with adjustable intensity, to the posterior tibial nerve. The cathode (a stainless steel ball, 1 cm diameter) was placed in the popliteal fossa and the anode (a 4 cm × 5 cm plate covered with electrolyte gel) was located on the distal part of the thigh, proximal to the patella. The recording responses were triggered by electrical pulses delivered by the stimulator.
Data were analyzed on a custom made software running under MATLAB (The Mathworks Inc., USA). For each position and condition, the 10 highest Hmax and the 5 Mmax responses were averaged and rectified. Mean peak-to-peak amplitudes of those responses were defined. Hmax responses were normalized to their respective Mmax (Hmax /Mmax ) for test-to-test comparisons. For the PRE and POST conditions, in order to quantify an index of the postural modulation of SOL H-reflex, Hmax /Mmax ratios in standing position were expressed relative to the sitting ones. To compare and interpret changes in H-reflex responses between the standing and sitting positions, and before and after the vibration exposure (or prolonged seating without vibration), it was necessary to ensure that the effective stimulus strength remained relatively constant between the different recording sessions. Only small changes in the distance between the electrode and the nerve would cause changes in the effective stimulus strength and then in the resultant M-wave and H-reflex [4]. Therefore, the mean peak-to-peak amplitudes of the M-waves associated with maximal H-reflexes were also quantified (MHmax ). In some studies, it is suggested to investigate the H-reflex at a constant stimulus strength giving generally 15–20% of the maximal M-wave [1,6,9]. However, since prolonged vibration was reported to raise the electrical threshold of muscle spindles Ia afferents [18], we rather investigated the maximal H-reflex and monitored the corresponding M-wave.
2.4. Experimental protocol
2.6. Statistics
A few days before the test session, subjects were familiarized with the equipment and the testing procedures. Subjects were tested under two randomly ordered conditions: (1) sitting and (2) standing. In sitting condition, subjects sat in a chair with knee flexed to 120◦ and the ankle to 90◦ , neutral reference position suggested for reflex studies [19]. In standing condition, the knee angle was 180◦ and the ankle angle 90◦ .
The effects of vibrations on SOL Hmax /Mmax ratios, MHmax and Mmax amplitudes were analyzed by means of ANOVA for repeated measures, considering the position (2 levels: sitting and standing) and the time (2 levels: pretest and post-test). When ANOVA was significant, post hoc Bonferroni t-tests were used to evaluate the significance of effects (prepost and between positions). Student paired t-tests were used to compare the index of postural
To detect SOL surface electromyograms (EMG), bipolar Ag/AgCl surface electrodes (83060TXIBC15, Dorvit Medical, 10 mm in diameter, spaced 22 mm center-to-center) were placed 2 cm below the insertion of the gastrocnemii on the Achilles tendon. The ground electrode (a 4 cm × 5 cm silver plate) was placed over the tibia. To reduce the electrode impedance below 5 k, the skin area over the electrodes application site was rubbed with an abrasive skin cleaning paste and cleaned with alcohol. EMG signal was sent to an isolated differential amplifier and band-pass-filtered (10 Hz to 1 kHz) before they were sent to the analog/digital board (with a sampling frequency of 10 kHz) and stored for further signal processing. 2.3. Stimulating apparatus
156
T. Lapole et al. / Neuroscience Letters 523 (2012) 154–157
4. Discussion
Fig. 1. SOL Hmax /Mmax amplitude ratios (means ± SEM) in the sitting and standing positions in PRE and POST conditions. * Significant effects of the vibratory stimulation (p < .05). # Significant effects of the postural modulation (p < .05).
Fig. 2. Index of SOL H-reflex postural modulation (the standing H/M ratio expressed relative to the sitting one) (means ± SEM) in PRE and POST conditions for the control (Con) and vibrated (Vib) groups. * Significant differences (p < .05).
modulation of SOL H-reflex between the PRE and POST conditions. The same statistic analysis was performed for the control group. Data are reported as mean ± standard error to the mean (SEM). Differences were considered significant when p was less than 0.05 (p < .05). 3. Results Fig. 1 illustrates the SOL Hmax /Mmax ratios for both control and vibrated groups. For the control group, there was a significant position effect (p = .04), but no time effect (p = .84). The ANOVA performed within the vibrated group revealed a significant position effect (p = .005), a significant time effect (p < .001), and also a significant interaction effect (p = .002). Thus, the index of SOL H-reflex postural modulation, i.e. the standing H/M ratio expressed relative to the sitting one, was significantly decreased only for the vibrated group (Fig. 2). Table 1 reports the mean amplitude of SOL Mmax and MHmax for both control and vibrated groups. There were no significant differences in any of these parameters among the different levels of time or condition.
In the present study, we investigated the postural modulation of SOL H-reflex to assess and quantify the changes in presynaptic inhibition after prolonged Achilles tendon vibration, although other methods have been developed in man [20,23,30]. Indeed, presynaptic inhibitory mechanisms are classically induced on a test reflex by a conditioning volley, resulting in a reflex depression, the amount of which is dependent on presynaptic inhibition [30]. However, such methods were inappropriate here since they involve a relatively long experimental protocol, time incompatible with the 20 min complete recovery of H-reflexes after prolonged Achilles tendon vibration [35]. Thus, to analyze the early after-effects of tendon vibration, we preferred to investigate presynaptic inhibition with a short protocol (10 min maximum) involving postural modulation of SOL H-reflex, as did other authors [16,22,24]. For instance, the postural modulation of SOL H-reflex was reported to be age-dependant with higher decrease in H-reflex from prone to standing in young than in old subjects [2,24,34]. In our protocol, subjects were submitted to 1 h of vibrations while maintaining sitting position [27]. Since our results could have been influenced by the prolonged maintain of sitting position, we also tested a control group. It allowed us to ensure that maintaining the sitting position during 1 h did not modified the studied parameters. Thus, any change observed in the vibrated group could be explained only by the vibratory stimulation. Another methodological point refers to the effective stimulus strength between the different testing sessions: since it is known that vibration can alter the Ia afferents electrical threshold [18], we choose to monitor the amplitude of the M-wave associated with maximal H-reflexes. Our results showed that despite a small inter- and intra-subject variability, the effective stimulus strength remained relatively constant throughout the whole testing session. Accordingly to several authors, we reported on young subjects a postural modulation of the SOL H-reflex from sitting to standing [16,21,22]. Furthermore, the main finding of the present study was that the prolonged Achilles tendon vibration exposure led to a more pronounced H-reflex depression when standing than when sitting, as highlighted by the strong decrease in the index of SOL H-reflex postural modulation. In this study, prolonged vibration successfully induced a significant decrease in H-reflex amplitude in sitting as well as in standing position, as previously reported [35]. This attenuation of the Ia afferent activity efficiency has been considered the result of several mechanisms such as (1) the presynaptic inhibition of muscle spindles primary endings [3], (2) an increased firing threshold of those Ia afferents [17], and (3) the transmitter depletion at Ia-␣ synapses [10]. Since the level of presynaptic inhibition of Ia afferents is known to be greater in the standing position than in the sitting one [21], we hypothesized that the vibration-induced H-reflex depression would be posture-dependant. In both postures, the H-reflex was depressed after prolonged Achilles tendon vibration. However, the greater depression in the standing position confirms that the vibration-induced H-reflex depression may be largely
Table 1 SOL Mmax and MHmax amplitude. PRE
POST
Sitting Control group Vibrated group
SOL Mmax (mV) SOL MHmax (mV%) SOL Mmax (mV) SOL MHmax (mV%)
1.5 0.15 1.8 0.3
± ± ± ±
Standing 0.1 0.04 0.2 0.04
1.6 0.12 2 0.3
± ± ± ±
0.1 0.01 0.2 0.04
Sitting 1.3 0.13 1.7 0.36
± ± ± ±
Standing 0.1 0.05 0.2 0.07
Values are means ± SEM; SOL Mmax : maximal M wave amplitude; SOL MHmax : amplitude of the M-wave associated with the maximal H-reflex.
1.4 0.11 1.9 0.39
± ± ± ±
0.2 0.03 0.2 0.06
T. Lapole et al. / Neuroscience Letters 523 (2012) 154–157
mediated by presynaptic inhibition mechanisms, originated from Ia afferents, being over-activated during the vibratory exposure [7,32]. Despite it was not investigated in the present study, changes in ankle muscles background EMG activity could be ruled out to be involved in the reduced H-reflex in standing position [5]. Hence, after-effects of prolonged vibration exposure may essentially result from similar mechanisms as during the vibration paradox: inhibitory interneurons under supra-spinal control would inhibit Ia afferents, leading to H-reflex depression [11,14]. While acute SOL H-reflex depression is reported here, we previously reported an increase in H-reflex amplitude after 14 days of 1 h daily vibrations [26]. Present findings suggest that prolonged vibratory stimuli induced a strong presynaptic inhibition phenomenon on soleus spindle primary endings. In chronic conditions, it is conceivable that in view to limit this high, unusual and repetitive level of autogenic presynaptic inhibition, some adaptive mechanisms, supra-spinal in origin, take place to decrease presynaptic inhibitory mechanisms. It would explain the increase in SOL H-reflex after 14 days of 1 h daily Achilles vibration [26]. Acknowledgment This study was supported by grants of the Center National d’Etudes Spatiales (CNES, FRANCE). References [1] P. Aagaard, E.B. Simonsen, J.L. Andersen, P. Magnusson, P. Dyhre-Poulsen, Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses, Journal of Applied Physiology 92 (2002) 2309–2318. [2] R.M. Angulo-Kinzler, R.G. Mynark, D.M. Koceja, Soleus H-reflex gain in elderly and young adults: modulation due to body position, Journals of Gerontology Series A: Biological Sciences and Medical Sciences 53 (1998) M120–M125. [3] L.G. Bongiovanni, K.E. Hagbarth, L. Stjernberg, Prolonged muscle vibration reducing motor output in maximal voluntary contractions in man, Journal of Physiology 423 (1990) 15–26. [4] G.I. Boorman, J.A. Hoffer, K. Kallesoe, D. Viberg, C. Mah, A measure of peripheral nerve stimulation efficacy applicable to H-reflex studies, Canadian Journal of Neurological Sciences 23 (1996) 264–270. [5] M. Bove, A. Nardone, M. Schieppati, Effects of leg muscle tendon vibration on group Ia and group II reflex responses to stance perturbation in humans, Journal of Physiology 550 (2003) 617–630. [6] M. Bove, C. Trompetto, G. Abbruzzese, M. Schieppati, The posture-related interaction between Ia-afferent and descending input on the spinal reflex excitability in humans, Neuroscience Letters 397 (2006) 301–306. [7] D. Burke, K.E. Hagbarth, L. Lofstedt, B.G. Wallin, The responses of human muscle spindle endings to vibration of non-contracting muscles, Journal of Physiology 261 (1976) 673–693. [8] C. Capaday, R.B. Stein, Difference in the amplitude of the human soleus H reflex during walking and running, Journal of Physiology 392 (1987) 513–522. [9] G.R. Chalmers, K.M. Knutzen, Soleus H-reflex gain in healthy elderly and young adults when lying, standing, and balancing, Journals of Gerontology Series A: Biological Sciences and Medical Sciences 57 (2002) B321–B329. [10] D.R. Curtis, J.C. Eccles, Synaptic action during and after repetitive stimulation, Journal of Physiology 150 (1960) 374–398. [11] P.J. Delwaide, Human monosynaptic reflexes and presynaptic inhibition: an interpretation of spastic hyperreflexia, in: J.E. Desmedt (Ed.), New Developments in Electromyography and Clinical Neurophysiology, Karger, Basel, 1973, pp. 508–522. [12] G. Eklund, K.E. Hagbarth, Normal variability of tonic vibration reflexes in man, Experimental Neurology 16 (1966) 80–92.
157
[13] M. Faist, V. Dietz, E. Pierrot-Deseilligny, Modulation, probably presynaptic in origin, of monosynaptic Ia excitation during human gait, Experimental Brain Research 109 (1996) 441–449. [14] J.D. Gillies, J.W. Lance, P.D. Neilson, C.A. Tassinari, Presynaptic inhibition of the monosynaptic reflex by vibration, Journal of Physiology 205 (1969) 329–339. [15] K.E. Hagbarth, G. Eklund, Tonic vibration reflexes (TVR) in spasticity, Brain Research 2 (1966) 201–203. [16] R. Hayashi, K. Tako, T. Tokuda, N. Yanagisawa, Comparison of amplitude of human soleus H-reflex during sitting and standing, Neuroscience Research 13 (1992) 227–233. [17] L.F. Hayward, R.P. Nielsen, C.J. Heckman, R.S. Hutton, Tendon vibration-induced inhibition of human and cat triceps surae group I reflexes: evidence of selective Ib afferent fiber activation, Experimental Neurology 94 (1986) 333–347. [18] C.J. Heckman, S.M. Condon, R.S. Hutton, R.M. Enoka, Can Ib axons be selectively activated by electrical stimuli in human subjects? Experimental Neurology 86 (1984) 576–582. [19] M. Hugon, Methodology of the Hoffmann reflex in man, in: J.E. Desmedt (Ed.), Progress in Clinical Neurophysiology, New Developments in Electromyography and Clinical Neurophysiology, vol. 3, Karger, Switzerland, 1973, pp. 227–293. [20] H. Hultborn, S. Meunier, C. Morin, E. Pierrot-Deseilligny, Assessing changes in presynaptic inhibition of I a fibres: a study in man and the cat, Journal of Physiology 389 (1987) 729–756. [21] R. Katz, S. Meunier, E. Pierrot-Deseilligny, Changes in presynaptic inhibition of Ia fibres in man while standing, Brain 111 (Pt 2) (1988) 417–437. [22] N. Kawashima, H. Sekiguchi, T. Miyoshi, K. Nakazawa, M. Akai, Inhibition of the human soleus Hoffman reflex during standing without descending commands, Neuroscience Letters 345 (2003) 41–44. [23] M. Klass, S. Baudry, J. Duchateau, Modulation of reflex responses in activated ankle dorsiflexors differs in healthy young and elderly subjects, European Journal of Applied Physiology 111 (2011) 1909–1916. [24] D.M. Koceja, C.A. Markus, M.H. Trimble, Postural modulation of the soleus H reflex in young and old subjects, Electroencephalography and Clinical Neurophysiology 97 (1995) 387–393. [25] D.M. Koceja, M.H. Trimble, D.R. Earles, Inhibition of the soleus H-reflex in standing man, Brain Research 629 (1993) 155–158. [26] T. Lapole, C. Perot, Hoffmann reflex is increased after 14 days of daily repeated Achilles tendon vibration for the soleus but not for the gastrocnemii muscles, Applied Physiology, Nutrition, and Metabolism 37 (2012) 14–20. [27] T. Lapole, C. Pérot, Effects of repeated Achilles tendon vibration on triceps surae force production, Journal of Electromyography and Kinesiology 20 (2010) 648–654. [28] B.J. Martin, J.P. Roll, G.M. Gauthier, Inhibitory effects of combined agonist and antagonist muscle vibration on H-reflex in man, Aviation Space and Environmental Medicine 57 (1986) 681–687. [29] J.E. Misiaszek, The H-reflex as a tool in neurophysiology: its limitations and uses in understanding nervous system function, Muscle and Nerve 28 (2003) 144–160. [30] E. Pierrot-Deseilligny, D. Mazevet, The monosynaptic reflex: a tool to investigate motor control in humans. Interest and limits, Neurophysiologie Clinique 30 (2000) 67–80. [31] J.P. Roll, B. Martin, G.M. Gauthier, F. Mussa Ivaldi, Effects of whole-body vibration on spinal reflexes in man, Aviation Space and Environmental Medicine 51 (1980) 1227–1233. [32] J.P. Roll, J.P. Vedel, E. Ribot, Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study, Experimental Brain Research 76 (1989) 213–222. [33] M. Schieppati, The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man, Progress in Neurobiology 28 (1987) 345–376. [34] M. Tsuruike, D.M. Koceja, K. Yabe, N. Shima, Age comparison of H-reflex modulation with the Jendrassik maneuver and postural complexity, Clinical Neurophysiology 114 (2003) 945–953. [35] J. Ushiyama, K. Masani, M. Kouzaki, H. Kanehisa, T. Fukunaga, Difference in aftereffects following prolonged Achilles tendon vibration on muscle activity during maximal voluntary contraction among plantar flexor synergists, Journal of Applied Physiology 98 (2005) 1427–1433. [36] E.P. Zehr, Considerations for use of the Hoffmann reflex in exercise studies, European Journal of Applied Physiology 86 (2002) 455–468.
Contents lists available at SciVerse ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Acute postural modulation of the soleus H-reflex after Achilles tendon vibration Thomas Lapole, Francis Canon, Chantal Pérot ∗ Université de Technologie, Compiègne CNRS UMR 7338, Biomécanique et Bioingénierie, F-60205 Compiègne Cedex, France
h i g h l i g h t s Soleus H-reflex was reported to be decreased when standing compared to sitting position. After prolonged Achilles tendon vibration, this postural modulation was increased. Those results are discussed in terms of changes in presynaptic inhibition.
a r t i c l e
i n f o
Article history: Received 19 April 2012 Received in revised form 9 June 2012 Accepted 25 June 2012 Keywords: Achilles tendon Vibration Soleus Hoffmann reflex Postural modulation Presynaptic inhibition
a b s t r a c t Alteration of Soleus (SOL) H-reflex has been reported after prolonged vibratory exposure and it was hypothesized that presynaptic inhibition, known to depress the H-reflex during vibration, largely contributed to the H-reflex changes. To confirm this hypothesis, the purpose of the present study was to quantify the SOL H-reflex changes between sitting and standing positions (postural modulation) with or without the after-effects of 1 h of Achilles tendon vibration. Indeed, postural modulation of the SOL H-reflex has been reported to inform on the level of presynaptic inhibition exerted on Ia afferents. SOL H-reflex and M waves were measured in healthy voluntary subjects in both sitting and standing positions before and after 1 h of Achilles vibration (frequency: 50 Hz) applied in sitting position (vibration group, n = 11) or before and after 1 h of sitting position only (control group, n = 6). SOL Hmax /Mmax ratios were calculated. Furthermore, in order to quantify presynaptic inhibition induced by prolonged vibration, an index of SOL H-reflex postural modulation was calculated as the standing Hmax /Mmax ratio relative to the sitting one. After 1 h of Achilles tendon vibration, a significant decrease in the SOL Hmax /Mmax ratio was observed both in sitting and standing positions (p < 0.05). However, the decrease was more pronounced in the standing position, leading to a significant decrease of the index of SOL H-reflex postural modulation. Those results suggest that presynaptic inhibition could have largely contributed to the H-reflex decrease observed after one bout of vibration. © 2012 Elsevier Ireland Ltd. All rights reserved.
1. Introduction To propose the benefits of vibrations to subjects who cannot stand on a vibrating platform, we previously proposed a program based on chronic prolonged Achilles tendon vibrations [27]. Maximal isometric torque in plantar-flexion was enhanced after 14 days of 1 h daily vibration and this increase in torque was correlated to an increase in triceps surae activation capacities [27]. These increases could result from changes in volitional drive from the supra-spinal motor structures inducing a higher activation of ␣ motoneurons. Furthermore, changes in spinal excitability could also be expected since tendon vibration induces tonic vibration reflexes through activation of muscle spindle primary endings [7,12]. Indeed, the soleus (SOL) Hoffmann reflex (H-reflex), classical index of changes
∗ Corresponding author. Tel.: +33 3 44 23 43 92; fax: +33 3 44 20 48 13. E-mail address: [email protected] (C. Pérot). 0304-3940/$ – see front matter © 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neulet.2012.06.067
in reflex excitability [36], was increased after chronic Achilles tendon vibration [26]. The amplitude of the H-reflex depends on the motoneuron excitability [33] and on the synaptic efficiency of the Ia-␣ pathways, itself depending on the level of presynaptic inhibition exerted on Ia afferents [29]. Hagbarth and Eklund [15] were the first to report a strong depression in SOL H-reflex during a 100 Hz vibration exposure. Several authors latter demonstrated the same result [28,31]. Furthermore, when vibration is prolonged, it has been reported for the SOL an acute H-reflex depression that was almost recovered in 20 min [35]. This attenuation of Ia afferent efficiency was considered to result from several mechanisms such as the presynaptic inhibition of muscle spindles primary endings [3], an increased firing threshold of those Ia afferents [17], and the transmitter depletion at Ia-␣ synapses [10]. In our previous studies, it was hypothesized that chronic effects of prolonged Achilles tendon vibration were rather located on the presynaptic inhibition of Ia afferents [26].
T. Lapole et al. / Neuroscience Letters 523 (2012) 154–157
The modulation of the H-reflex amplitude is also known to be task-dependant [8]. Indeed, it was reported that presynaptic inhibition of Ia afferents plays a major role in the depression of SOL H-reflex in man while standing or walking [13,21]. Thus, the changes in H-reflex amplitude from prone to standing [25] or from sitting to standing [16] were accredited to presynaptic inhibitory mechanisms and proposed as an index allowing to quantify the weight of presynaptic inhibition. Since vibration was suggested to enhance the level of presynaptic inhibition, the induced effects should be posture-dependant, i.e., the decrease in H-reflex from sitting to standing should be higher after the vibratory exposure. The aim of the present study was therefore to confirm this hypothesis by investigating the acute effects of Achilles tendon vibration on the postural modulation of the SOL H-reflex. 2. Methods 2.1. Subjects 17 healthy and active voluntary subjects (age: 27.3 ± 3.5 years, mass: 70.5 ± 11.4 kg, height: 175.2 ± 8.8 cm) engaged in the study. They were assigned to the vibration group (n = 11) or the control group (n = 6). Written informed consent was provided by the subjects and they were fully advised of the procedures, and free to stop the experiment at any time. The experimental procedures were approved by the local Ethics committee of the University of Compiègne, France. 2.2. EMG recording
155
The position of the stimulating electrode was first adjusted so as to obtain at low intensity the maximal amplitude for the H-reflex, with no (or minimal) motor direct response (M-wave). This point was marked on the skin in order to ensure the same electrode placement between the different testing positions and conditions. At least 15 responses were recorded at the stimulus intensity giving the maximal H-reflex amplitude. Then, 5 responses were recorded at the intensity giving the maximal M-wave. Induced responses were stored and later averaged to give the maximal H-reflex Hmax and the maximal M-wave Mmax respectively. Interstimuli intervals were randomly used and were always more than 3 s to limit postactivation refractory period [36]. Experimental procedures were performed in both sitting and standing positions. Those measurements were performed a first time at the beginning of the testing session (PRE-Vib). Immediately after, subjects were submitted to an 1 h period of Achilles tendon vibration: as previously performed [27], the tendon vibrator (Techno-Concept, VB 115) was strapped on the Achilles tendon of the right ankle and vibration (amplitude: 1 mm; frequency: 50 Hz) was applied during 1 h in a seated position, the subjects being at rest. Just after the end of the vibration period, the same measurements as previously described were performed in order to determine the effects of vibrations on postural modulation of the SOL H-reflexes (POST-Vib). As the time of vibration employed in this study imposed to keep a sitting position during 1 h, we investigated whether this maintain of sitting position could affect H-reflexes. Thus, the control performed the same procedures before (PRE-Con) and after (POSTCon) prolonged seating for 1 h without vibration. 2.5. Data analysis
Electrical stimulations were applied using a constant current stimulator (DS7A, Digitimer Ltd., UK). This device delivered single electrical pulses (1 ms), with adjustable intensity, to the posterior tibial nerve. The cathode (a stainless steel ball, 1 cm diameter) was placed in the popliteal fossa and the anode (a 4 cm × 5 cm plate covered with electrolyte gel) was located on the distal part of the thigh, proximal to the patella. The recording responses were triggered by electrical pulses delivered by the stimulator.
Data were analyzed on a custom made software running under MATLAB (The Mathworks Inc., USA). For each position and condition, the 10 highest Hmax and the 5 Mmax responses were averaged and rectified. Mean peak-to-peak amplitudes of those responses were defined. Hmax responses were normalized to their respective Mmax (Hmax /Mmax ) for test-to-test comparisons. For the PRE and POST conditions, in order to quantify an index of the postural modulation of SOL H-reflex, Hmax /Mmax ratios in standing position were expressed relative to the sitting ones. To compare and interpret changes in H-reflex responses between the standing and sitting positions, and before and after the vibration exposure (or prolonged seating without vibration), it was necessary to ensure that the effective stimulus strength remained relatively constant between the different recording sessions. Only small changes in the distance between the electrode and the nerve would cause changes in the effective stimulus strength and then in the resultant M-wave and H-reflex [4]. Therefore, the mean peak-to-peak amplitudes of the M-waves associated with maximal H-reflexes were also quantified (MHmax ). In some studies, it is suggested to investigate the H-reflex at a constant stimulus strength giving generally 15–20% of the maximal M-wave [1,6,9]. However, since prolonged vibration was reported to raise the electrical threshold of muscle spindles Ia afferents [18], we rather investigated the maximal H-reflex and monitored the corresponding M-wave.
2.4. Experimental protocol
2.6. Statistics
A few days before the test session, subjects were familiarized with the equipment and the testing procedures. Subjects were tested under two randomly ordered conditions: (1) sitting and (2) standing. In sitting condition, subjects sat in a chair with knee flexed to 120◦ and the ankle to 90◦ , neutral reference position suggested for reflex studies [19]. In standing condition, the knee angle was 180◦ and the ankle angle 90◦ .
The effects of vibrations on SOL Hmax /Mmax ratios, MHmax and Mmax amplitudes were analyzed by means of ANOVA for repeated measures, considering the position (2 levels: sitting and standing) and the time (2 levels: pretest and post-test). When ANOVA was significant, post hoc Bonferroni t-tests were used to evaluate the significance of effects (prepost and between positions). Student paired t-tests were used to compare the index of postural
To detect SOL surface electromyograms (EMG), bipolar Ag/AgCl surface electrodes (83060TXIBC15, Dorvit Medical, 10 mm in diameter, spaced 22 mm center-to-center) were placed 2 cm below the insertion of the gastrocnemii on the Achilles tendon. The ground electrode (a 4 cm × 5 cm silver plate) was placed over the tibia. To reduce the electrode impedance below 5 k, the skin area over the electrodes application site was rubbed with an abrasive skin cleaning paste and cleaned with alcohol. EMG signal was sent to an isolated differential amplifier and band-pass-filtered (10 Hz to 1 kHz) before they were sent to the analog/digital board (with a sampling frequency of 10 kHz) and stored for further signal processing. 2.3. Stimulating apparatus
156
T. Lapole et al. / Neuroscience Letters 523 (2012) 154–157
4. Discussion
Fig. 1. SOL Hmax /Mmax amplitude ratios (means ± SEM) in the sitting and standing positions in PRE and POST conditions. * Significant effects of the vibratory stimulation (p < .05). # Significant effects of the postural modulation (p < .05).
Fig. 2. Index of SOL H-reflex postural modulation (the standing H/M ratio expressed relative to the sitting one) (means ± SEM) in PRE and POST conditions for the control (Con) and vibrated (Vib) groups. * Significant differences (p < .05).
modulation of SOL H-reflex between the PRE and POST conditions. The same statistic analysis was performed for the control group. Data are reported as mean ± standard error to the mean (SEM). Differences were considered significant when p was less than 0.05 (p < .05). 3. Results Fig. 1 illustrates the SOL Hmax /Mmax ratios for both control and vibrated groups. For the control group, there was a significant position effect (p = .04), but no time effect (p = .84). The ANOVA performed within the vibrated group revealed a significant position effect (p = .005), a significant time effect (p < .001), and also a significant interaction effect (p = .002). Thus, the index of SOL H-reflex postural modulation, i.e. the standing H/M ratio expressed relative to the sitting one, was significantly decreased only for the vibrated group (Fig. 2). Table 1 reports the mean amplitude of SOL Mmax and MHmax for both control and vibrated groups. There were no significant differences in any of these parameters among the different levels of time or condition.
In the present study, we investigated the postural modulation of SOL H-reflex to assess and quantify the changes in presynaptic inhibition after prolonged Achilles tendon vibration, although other methods have been developed in man [20,23,30]. Indeed, presynaptic inhibitory mechanisms are classically induced on a test reflex by a conditioning volley, resulting in a reflex depression, the amount of which is dependent on presynaptic inhibition [30]. However, such methods were inappropriate here since they involve a relatively long experimental protocol, time incompatible with the 20 min complete recovery of H-reflexes after prolonged Achilles tendon vibration [35]. Thus, to analyze the early after-effects of tendon vibration, we preferred to investigate presynaptic inhibition with a short protocol (10 min maximum) involving postural modulation of SOL H-reflex, as did other authors [16,22,24]. For instance, the postural modulation of SOL H-reflex was reported to be age-dependant with higher decrease in H-reflex from prone to standing in young than in old subjects [2,24,34]. In our protocol, subjects were submitted to 1 h of vibrations while maintaining sitting position [27]. Since our results could have been influenced by the prolonged maintain of sitting position, we also tested a control group. It allowed us to ensure that maintaining the sitting position during 1 h did not modified the studied parameters. Thus, any change observed in the vibrated group could be explained only by the vibratory stimulation. Another methodological point refers to the effective stimulus strength between the different testing sessions: since it is known that vibration can alter the Ia afferents electrical threshold [18], we choose to monitor the amplitude of the M-wave associated with maximal H-reflexes. Our results showed that despite a small inter- and intra-subject variability, the effective stimulus strength remained relatively constant throughout the whole testing session. Accordingly to several authors, we reported on young subjects a postural modulation of the SOL H-reflex from sitting to standing [16,21,22]. Furthermore, the main finding of the present study was that the prolonged Achilles tendon vibration exposure led to a more pronounced H-reflex depression when standing than when sitting, as highlighted by the strong decrease in the index of SOL H-reflex postural modulation. In this study, prolonged vibration successfully induced a significant decrease in H-reflex amplitude in sitting as well as in standing position, as previously reported [35]. This attenuation of the Ia afferent activity efficiency has been considered the result of several mechanisms such as (1) the presynaptic inhibition of muscle spindles primary endings [3], (2) an increased firing threshold of those Ia afferents [17], and (3) the transmitter depletion at Ia-␣ synapses [10]. Since the level of presynaptic inhibition of Ia afferents is known to be greater in the standing position than in the sitting one [21], we hypothesized that the vibration-induced H-reflex depression would be posture-dependant. In both postures, the H-reflex was depressed after prolonged Achilles tendon vibration. However, the greater depression in the standing position confirms that the vibration-induced H-reflex depression may be largely
Table 1 SOL Mmax and MHmax amplitude. PRE
POST
Sitting Control group Vibrated group
SOL Mmax (mV) SOL MHmax (mV%) SOL Mmax (mV) SOL MHmax (mV%)
1.5 0.15 1.8 0.3
± ± ± ±
Standing 0.1 0.04 0.2 0.04
1.6 0.12 2 0.3
± ± ± ±
0.1 0.01 0.2 0.04
Sitting 1.3 0.13 1.7 0.36
± ± ± ±
Standing 0.1 0.05 0.2 0.07
Values are means ± SEM; SOL Mmax : maximal M wave amplitude; SOL MHmax : amplitude of the M-wave associated with the maximal H-reflex.
1.4 0.11 1.9 0.39
± ± ± ±
0.2 0.03 0.2 0.06
T. Lapole et al. / Neuroscience Letters 523 (2012) 154–157
mediated by presynaptic inhibition mechanisms, originated from Ia afferents, being over-activated during the vibratory exposure [7,32]. Despite it was not investigated in the present study, changes in ankle muscles background EMG activity could be ruled out to be involved in the reduced H-reflex in standing position [5]. Hence, after-effects of prolonged vibration exposure may essentially result from similar mechanisms as during the vibration paradox: inhibitory interneurons under supra-spinal control would inhibit Ia afferents, leading to H-reflex depression [11,14]. While acute SOL H-reflex depression is reported here, we previously reported an increase in H-reflex amplitude after 14 days of 1 h daily vibrations [26]. Present findings suggest that prolonged vibratory stimuli induced a strong presynaptic inhibition phenomenon on soleus spindle primary endings. In chronic conditions, it is conceivable that in view to limit this high, unusual and repetitive level of autogenic presynaptic inhibition, some adaptive mechanisms, supra-spinal in origin, take place to decrease presynaptic inhibitory mechanisms. It would explain the increase in SOL H-reflex after 14 days of 1 h daily Achilles vibration [26]. Acknowledgment This study was supported by grants of the Center National d’Etudes Spatiales (CNES, FRANCE). References [1] P. Aagaard, E.B. Simonsen, J.L. Andersen, P. Magnusson, P. Dyhre-Poulsen, Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses, Journal of Applied Physiology 92 (2002) 2309–2318. [2] R.M. Angulo-Kinzler, R.G. Mynark, D.M. Koceja, Soleus H-reflex gain in elderly and young adults: modulation due to body position, Journals of Gerontology Series A: Biological Sciences and Medical Sciences 53 (1998) M120–M125. [3] L.G. Bongiovanni, K.E. Hagbarth, L. Stjernberg, Prolonged muscle vibration reducing motor output in maximal voluntary contractions in man, Journal of Physiology 423 (1990) 15–26. [4] G.I. Boorman, J.A. Hoffer, K. Kallesoe, D. Viberg, C. Mah, A measure of peripheral nerve stimulation efficacy applicable to H-reflex studies, Canadian Journal of Neurological Sciences 23 (1996) 264–270. [5] M. Bove, A. Nardone, M. Schieppati, Effects of leg muscle tendon vibration on group Ia and group II reflex responses to stance perturbation in humans, Journal of Physiology 550 (2003) 617–630. [6] M. Bove, C. Trompetto, G. Abbruzzese, M. Schieppati, The posture-related interaction between Ia-afferent and descending input on the spinal reflex excitability in humans, Neuroscience Letters 397 (2006) 301–306. [7] D. Burke, K.E. Hagbarth, L. Lofstedt, B.G. Wallin, The responses of human muscle spindle endings to vibration of non-contracting muscles, Journal of Physiology 261 (1976) 673–693. [8] C. Capaday, R.B. Stein, Difference in the amplitude of the human soleus H reflex during walking and running, Journal of Physiology 392 (1987) 513–522. [9] G.R. Chalmers, K.M. Knutzen, Soleus H-reflex gain in healthy elderly and young adults when lying, standing, and balancing, Journals of Gerontology Series A: Biological Sciences and Medical Sciences 57 (2002) B321–B329. [10] D.R. Curtis, J.C. Eccles, Synaptic action during and after repetitive stimulation, Journal of Physiology 150 (1960) 374–398. [11] P.J. Delwaide, Human monosynaptic reflexes and presynaptic inhibition: an interpretation of spastic hyperreflexia, in: J.E. Desmedt (Ed.), New Developments in Electromyography and Clinical Neurophysiology, Karger, Basel, 1973, pp. 508–522. [12] G. Eklund, K.E. Hagbarth, Normal variability of tonic vibration reflexes in man, Experimental Neurology 16 (1966) 80–92.
157
[13] M. Faist, V. Dietz, E. Pierrot-Deseilligny, Modulation, probably presynaptic in origin, of monosynaptic Ia excitation during human gait, Experimental Brain Research 109 (1996) 441–449. [14] J.D. Gillies, J.W. Lance, P.D. Neilson, C.A. Tassinari, Presynaptic inhibition of the monosynaptic reflex by vibration, Journal of Physiology 205 (1969) 329–339. [15] K.E. Hagbarth, G. Eklund, Tonic vibration reflexes (TVR) in spasticity, Brain Research 2 (1966) 201–203. [16] R. Hayashi, K. Tako, T. Tokuda, N. Yanagisawa, Comparison of amplitude of human soleus H-reflex during sitting and standing, Neuroscience Research 13 (1992) 227–233. [17] L.F. Hayward, R.P. Nielsen, C.J. Heckman, R.S. Hutton, Tendon vibration-induced inhibition of human and cat triceps surae group I reflexes: evidence of selective Ib afferent fiber activation, Experimental Neurology 94 (1986) 333–347. [18] C.J. Heckman, S.M. Condon, R.S. Hutton, R.M. Enoka, Can Ib axons be selectively activated by electrical stimuli in human subjects? Experimental Neurology 86 (1984) 576–582. [19] M. Hugon, Methodology of the Hoffmann reflex in man, in: J.E. Desmedt (Ed.), Progress in Clinical Neurophysiology, New Developments in Electromyography and Clinical Neurophysiology, vol. 3, Karger, Switzerland, 1973, pp. 227–293. [20] H. Hultborn, S. Meunier, C. Morin, E. Pierrot-Deseilligny, Assessing changes in presynaptic inhibition of I a fibres: a study in man and the cat, Journal of Physiology 389 (1987) 729–756. [21] R. Katz, S. Meunier, E. Pierrot-Deseilligny, Changes in presynaptic inhibition of Ia fibres in man while standing, Brain 111 (Pt 2) (1988) 417–437. [22] N. Kawashima, H. Sekiguchi, T. Miyoshi, K. Nakazawa, M. Akai, Inhibition of the human soleus Hoffman reflex during standing without descending commands, Neuroscience Letters 345 (2003) 41–44. [23] M. Klass, S. Baudry, J. Duchateau, Modulation of reflex responses in activated ankle dorsiflexors differs in healthy young and elderly subjects, European Journal of Applied Physiology 111 (2011) 1909–1916. [24] D.M. Koceja, C.A. Markus, M.H. Trimble, Postural modulation of the soleus H reflex in young and old subjects, Electroencephalography and Clinical Neurophysiology 97 (1995) 387–393. [25] D.M. Koceja, M.H. Trimble, D.R. Earles, Inhibition of the soleus H-reflex in standing man, Brain Research 629 (1993) 155–158. [26] T. Lapole, C. Perot, Hoffmann reflex is increased after 14 days of daily repeated Achilles tendon vibration for the soleus but not for the gastrocnemii muscles, Applied Physiology, Nutrition, and Metabolism 37 (2012) 14–20. [27] T. Lapole, C. Pérot, Effects of repeated Achilles tendon vibration on triceps surae force production, Journal of Electromyography and Kinesiology 20 (2010) 648–654. [28] B.J. Martin, J.P. Roll, G.M. Gauthier, Inhibitory effects of combined agonist and antagonist muscle vibration on H-reflex in man, Aviation Space and Environmental Medicine 57 (1986) 681–687. [29] J.E. Misiaszek, The H-reflex as a tool in neurophysiology: its limitations and uses in understanding nervous system function, Muscle and Nerve 28 (2003) 144–160. [30] E. Pierrot-Deseilligny, D. Mazevet, The monosynaptic reflex: a tool to investigate motor control in humans. Interest and limits, Neurophysiologie Clinique 30 (2000) 67–80. [31] J.P. Roll, B. Martin, G.M. Gauthier, F. Mussa Ivaldi, Effects of whole-body vibration on spinal reflexes in man, Aviation Space and Environmental Medicine 51 (1980) 1227–1233. [32] J.P. Roll, J.P. Vedel, E. Ribot, Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study, Experimental Brain Research 76 (1989) 213–222. [33] M. Schieppati, The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man, Progress in Neurobiology 28 (1987) 345–376. [34] M. Tsuruike, D.M. Koceja, K. Yabe, N. Shima, Age comparison of H-reflex modulation with the Jendrassik maneuver and postural complexity, Clinical Neurophysiology 114 (2003) 945–953. [35] J. Ushiyama, K. Masani, M. Kouzaki, H. Kanehisa, T. Fukunaga, Difference in aftereffects following prolonged Achilles tendon vibration on muscle activity during maximal voluntary contraction among plantar flexor synergists, Journal of Applied Physiology 98 (2005) 1427–1433. [36] E.P. Zehr, Considerations for use of the Hoffmann reflex in exercise studies, European Journal of Applied Physiology 86 (2002) 455–468.