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Effect of Achilles tendon vibration on postural orientation
Neuroscience Letters 416 (2007) 71–75
Effect of Achilles tendon vibration on postural orientation Hadrien Ceyte a , Corinne Cian a , Raphael Zory c , Pierre-Alain Barraud a , Alain Roux a , Michel Guerraz b,∗ a Centre de Recherches du Service de Sant´ e des Arm´ees, BP 87, 38702 La Tronche Cedex, France Laboratoire de Psychologie et Neurocognition CNRS, UMR 5105, Universit´e de Savoie, 73376 Le Bourget du lac, France c Laboratoire de Physiologie et Physiopathologie de l’Exercice et Handicap (PPEH), Universit´ e de Savoie, 73376 Le Bourget du lac, France b
Received 6 November 2006; received in revised form 12 January 2007; accepted 22 January 2007
Abstract Vibration applied to the Achilles tendon is well known to induce in freely standing subjects a backward body displacement and in restrained subjects an illusory forward body tilt. The purpose of the present experiment was to evaluate the effect of Achilles tendon vibration (90 Hz) on postural orientation in subjects free of equilibrium constraints. Subjects (n = 12) were strapped on a backboard that could be rotated in the antero-posterior direction with the axis of rotation at the level of the ankles. They stood on a rigid horizontal floor with the soles of their feet parallel to the ground. They were initially positioned 7◦ backward or forward or vertical and were required to adjust their body (the backboard) to the vertical orientation via a joystick. Firstly, results showed that in response to Achilles tendon vibration, subjects adjusted their body backward compared to the condition without vibration. This backward body adjustment likely cancel the appearance of an illusory forward body tilt. It was also observed that the vibratory stimulus applied to the Achilles tendon elicited in restrained standing subjects an increased EMG activity in both the gastrocnemius lateralis and the soleus muscles. Secondly, this vibration effect was more pronounced when passive displacement during the adjustment phase was congruent with the simulated elongation of calf muscles. These results indicated that the perception of body orientation is coherent with the postural response classically observed in freely standing subjects although the relationship between these two responses remains to be elucidated. © 2007 Elsevier Ireland Ltd. All rights reserved. Keywords: Body orientation; Vibration; Muscle spindles; Passive movement
The tendon vibration technique has been widely used to investigate the influence of proprioception, particularly muscle spindle endings in spatial perception and motor control. Vibration of sufficient amplitude and frequency applied to a muscle or tendon activates mainly the primary spindle endings connected to the large Ia afferent fibres, for which the firing rate seems to be interpreted by the CNS as an elongation of that muscle [3,21,22]. This erroneous interpretation induces in some circumstances illusory sensation of joint displacement [4,9,11,21] or motor effects such as contraction of the vibrated muscle (tonic vibratory reflex) [11,23] and compensatory postural responses [1,6,8,16,19]. For example, vibration applied to the Achilles tendons of standing subjects induces backward body sway [1,6,13,24]. This response mimics the postural correction that would have occurred if the proprioceptive receptors had been stimulated in a natural way,
∗
Corresponding author. Tel.: +33 4 79 75 81 45; fax: +33 4 79 75 81 48. E-mail address: [email protected] (M. Guerraz).
0304-3940/$ – see front matter © 2007 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2007.01.044
i.e. a stretching of the calf muscles by a forward sway that needs to be corrected. In contrast when those standing subjects were prevented from swaying, the same vibration can induce an illusory tilt in the opposite direction to the backward sway observed in the unrestrained condition [15]. Proprioceptive sensors are involved in the regulation of both equilibrium and orientation (body posture) as they provide the CNS with information about the position of the different body segments relative to each other, and then contribute to update the postural scheme [13]. Therefore, when standing freely, the spatio-temporal characteristics of the vibratory evoked response reflects the functions of both equilibrium and orientation. The classical way of questioning postural orientation in the absence of equilibrium constraints is to ask restrained subjects to report their feeling during the vibratory stimulation. The illusory tilt is evaluated either by asking subjects to verbally report their illusory feeling or by asking them to copy the virtual whole body movements they perceived by moving a joystick [20]. In the present experiment, the effect of a proprioceptive distur-
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H. Ceyte et al. / Neuroscience Letters 416 (2007) 71–75
bance on postural orientation applied to the Achilles tendons was investigated by asking subjects free of equilibrium constraints to adjust the body in a vertical position. Subjects were standing on a rigid floor with the soles of their feet parallel to the ground, and equilibrium constraints were suppressed by strapping them to a servo-controlled motorized backboard that could rotate in the antero-posterior direction with the axis rotating about the ankles. In this context, subjects had to maintain posture against gravity (maintain postural tone) but were not actively engaged in the maintenance of balance (equilibrium). The aim of the present experiment was to investigate the effect of tendon vibration on perceived postural orientation in restrained standing subjects. Twelve-volunteer subjects (6 females and 6 males; mean age 32 years) took part in this experiment. Subjects reported no apparent vestibular or somaesthetic abnormalities. In conformity with the Helsinki Convention, individual written informed consent was obtained. The subjects were restrained on a servo-controlled motorized backboard capable of being rotated in the sagittal plane (pitch dimension) with a 1◦ s−1 maximal velocity, and an initial acceleration and a final deceleration of 0.05◦ s−2 . Moving the backboard at this very slow velocity prevented responses of the semi-circular canals [10]. The pivot on which the platform rotated was approximately at the level of the malleoli. Thus the rotation of the backboard enabled the body of a subject to be tilted backward or forward with the soles of the feet remaining parallel to the ground. The platform position (0.005◦ accuracy) was controlled and recorded using a digital position encoder. All the experiment was computer driven. Once a comfortable upright posture had been adopted by the subject, he/she was secured to the backboard by means of three large straps fixed at the level of the forehead, abdomen and thighs. The system of straps enabled the subject to be stabilized in order to suppress equilibrium constraints. To stimulate the ankle proprioceptive system Achilles tendons were stimulated by an electromechanical physiotherapy vibrator apparatus (Techno-concept VB 115, frequency of 90 Hz and amplitude of 200 m) comprising of two vibrators secured over the Achilles tendons with elastic bands. The subject was placed in a dark room and kept their eyes closed throughout the experimental session. For a given trial, the backboard on which the subjects was strapped tilted and stopped at a preset position, 0◦ (vertical), or 7◦ forward, or backward (see Fig. 1A). After a 20 s delay, subjects were asked to adjust their body to the vertical orientation by means of a joystick input to reposition the backboard. A maximal deflection of the joystick in either a backward or forward direction resulted in a slow movement of the platform by 0.5◦ s−1 in the respective direction with an initial acceleration and final deceleration of 0.25◦ s−2 . No time constraint was imposed during the adjustment phase, but subjects were encouraged to respond without excessive deliberation. Subjects pushed a button on the joystick to signal that they had completed their adjustment. The platform was then rotated to the next preset position. No feedback was given to subjects about their performance during the session.
Fig. 1. (A) Experimental set-up. The subjects were strapped on a backboard that could be rotated in the antero-posterior direction with the axis of rotation at the level of the ankles. (B) Mean setting errors (◦ ) as a function of initial body orientation (7◦ forward, 0◦ vertical, 7◦ backward) with vibration (VIB) and without (NVIB) vibration. Error bars indicate the standard deviations.
Two sessions of 20 min were performed for each subject. Each session comprised 12 trials consisting of two blocks of 3 trials in the no-vibration condition and two blocks of 3 trials in the vibration condition. In each block, the three initial body orientations (7◦ forward, 0◦ vertical, and 7◦ backward) were randomly performed, except that the 0◦ orientation was never presented first. A delay of 1 min was inserted before each block in the upright position. In the vibration condition, the Achilles tendons were vibrated during this 1 min delay without interruption until the end of the block of three trials. The order of presentation of the different blocks was counterbalanced across subjects. The adjustments were expressed as the angle difference (◦ ) between the objective vertical position and the orientation of the backboard. The angle difference was considered to be negative if it deviated backward from the objective vertical orientation or positive if it deviated forward. The individual mean error was calculated for each orientation. We tested in a control experiment the possibility that the vibration evoked in restrained standing subjects a tonic vibratory reflex (TVR). Standing subjects (n = 8; mean age 29 years) were restrained on the backboard (by means of large straps) in a vertical position. EMG activity of the tibialis anterior (TA), the gastrocnemius lateralis (GL) and the soleus (Sol) muscles of the dominant leg was recorded in 6 trials of 40 s (ME 3000 P8, Mega Electronics Ltd., Kuopio, Finland). Silver chloride surface electrodes (Medicotest blue sensor type M-00-S, Olstykke, Denmark) with preamplifiers were placed over the muscle bellies of the TA, GL and Sol in a bipolar configuration with 3.5 cm
H. Ceyte et al. / Neuroscience Letters 416 (2007) 71–75
inter-electrode distance. A reference electrode was attached to a body area remote from the studied muscles. Trials consisted of an initial period of 10 s without vibration (control period) followed by a period of 20 s of vibration (vibration period) and a post-vibratory period of 10 s (post-vibration period). Stimulus artifacts due to movement of the electrodes were excluded from the EMG data using a digital filter (band stop 75–105 Hz). Mean integrated EMG values (IEMG) for each subject in each group were calculated for both the vibration and non-vibration periods. The IEMG corresponding to the activity during voluntary maximal forces recorded for the TA, GL and Sol was considered to be 100% and the level of IEMG activity was calculated as a percentage of that maximal activity. We ensured that when no vibration was applied, no change in IEMG could be detected over a 40 s period. To find out whether vibration affected perception of body orientation, a 2 vibration (with and without) × 3 body initial orientation conditions (7◦ forward, 0◦ vertical, and 7◦ backward). ANOVA with repeated measures on the two factors was applied to the mean errors. A post hoc analysis (Newman–Keuls) was performed when P < .05. Results showed significant main effects of the initial body orientation [F(2,22) = 29.8; P < .05] and vibration conditions [F(1,11) = 29; P < .05] as well as an interaction between these two factors [F(2,22) = 5.88; P < .05]. Fig. 1B shows that without vibration stimulation (control condition), subjects’ estimates were influenced by their initial body orientation. Indeed, the subjective body vertical was close to the true gravitational vertical when subjects were initially vertical (M = −0.01◦ , S.D. = 1.98) but deviated in the direction of the initial orientation. When initially tilted backward or forward, subjects felt upright while being still tilted backward (M = −1.13◦ , S.D. = 2.06) and forward (M = 0.99◦ , S.D. = 1.76), respectively. Compared to the above control condition, vibration of the Achilles tendons induced systematic backward displacements of the subjective vertical body orientation. The mean amplitude of this backward tilt (vibration effect = VIB − NVIB) when the three initial body orientations were combined was −1.84◦ (S.D. = 1.4). As evident from the significant interaction between the two experimental factors (vibration × initial body position), the magnitude of this backward displacement (vibration effect) depended on the initial orientation of the subject. The vibration effect significantly increased from pitching forward to pitching backward and reached −1.21◦ (S.D. = 1.42) when subjects were initially tilted forward, −1.9◦ (S.D. = 1.43) and −2.41◦ (S.D. = 1.27) when subjects were initially vertical and tilted backward, respectively. Pairwise comparison indicated that the vibration effect in the forward orientation differed significantly from backward orientation (P < .05). The difference between the backward and vertical orientations was at the level of significance (P = 0.06) but forward and vertical orientation did not quite reach significance (P = 0.16). To find out whether vibration induces a TVR, mean IEMG values during the three periods of measure (control, vibration, post-vibration periods) were subjected to an ANOVA with repeated measures. A post hoc analysis (Newman–Keuls) was performed when P < .05.
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Fig. 2. Typical raw EMG responses of tibialis anterior (TA), gastrocnemius lateralis (GL) and Soleus (Sol) muscles to vibration (90 Hz).
As can be seen in Fig. 2, a vibratory stimulus applied to the Achilles tendon elicited in restrained standing subjects an increased EMG activity in both the GL [F(2,14) = 4.3, P < .05] and the Sol muscles [F(2,14) = 6.4, P < .05]. This motor response (TVR) observed during vibration decreased when vibration was stopped. Post hoc analysis revealed that the IEMG activity during vibration was significantly different from that measured in the control and post-vibration periods both for the GL (control = 3.4%, vibration = 4.6%, post-vibration = 3.7% of the maximal voluntary force) and the Sol muscles (control = 9.3%, vibration = 12.5%, post-vibration = 9.9%). In contrast, the vibratory stimulus applied to the Achilles tendon did not elicit a significant increased IEMG activity in the TA [F(2,14) = 2.8, P > .05]. Interestingly, seven out of the eight tested subjects reported that vibration induced after a few seconds an illusory forward body tilt and some of them spontaneously reported the feeling of being pushed forward by the backboard. This study was designed to investigate the contribution of muscle proprioception to the perception of body orientation in the absence of equilibrium constraints. Subjects were strapped to a motorized backboard tilting at the level of the ankles, and their task was to adjust their body (the backboard) vertical. Here, the body orientation task primarily concerns the sense of position and not the sense of movement. As reviewed recently by Proske [18], primary endings contribute both to the sense of position and movement, whereas secondary endings contribute to position sense only. In contrast to primary endings, secondary endings (II fibres) have been shown to be either insensitive or only slightly sensitive to tendon vibration. Therefore, the illusory forward tilt (sense of position) evoked by Achilles tendon vibration is likely the consequence of the recruitment of Ia fibers although the involvement of secondary endings cannot be fully excluded. In the condition of Achilles tendon vibration, subjects adjusted their body backward compared to the condition without vibration. This backward positioning is likely the counterpart of the illusory tilt evoked by vibration in upright restrained standing
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subjects as reported in the control experiment and in previous reports [15]. Indeed, vibration of the Achilles tendon simulates a lengthening of the calf muscles [3,21,22] that could be perceived by the subject as a forward tilt. By adjusting themselves backward, subjects cancelled this illusory tilt that would otherwise have occurred. Furthermore, in the EMG control experiment, we observed that Achilles tendon vibration induced in restrained standing subjects a TVR in both the GL and Sol muscles. This evoked motor response is probably an important component of the equilibrium responses in freely standing subjects [14]. In the restrained subjects of the present experiment, this tonic contraction of the calf muscles could create a reaction force of the body against the backboard. The increased pressures against the backboard are similar to what a subject would experience when tilted backward. However, verbal reports in the control EMG experiment and body adjustments in our main experiment disagree with a possible sensation of backward tilt. Indeed, in the control experiment, most subjects reported the illusion of being tilted forward when vibrated. Interestingly, they also had the feeling of being pushed forward by the backboard. The illusory forward body tilt in response to vibration might therefore result from a simulation of a lengthening of the calf muscles and an additional simulation of a push due to reaction forces of the body against the backboard related to the TVR. The backward adjustment observed (∼1.7◦ ) in response to tendon vibration is close to that reported with freely standing subjects in other experiments [1,24] but smaller than illusory tilt reported via a joystick in restrained conditions (∼10◦ in restrained pre-flight condition [22]). Although response amplitudes cannot be directly compared because of methodological reasons, one might have expected larger responses to vibration when equilibrium constraints were suppressed. Indeed, for biomechanical reasons, freely standing subjects have to limit any backward (or forward) body excursion in order not to go beyond the limits of postural equilibrium and fall. Such biomechanical limits were suppressed when strapped to a board as presently. The perception of body orientation is usually considered to be primarily based on vestibular information and secondarily on somesthetic information. However, several authors have challenged this view and showed the limit of otolith contribution in quasi static body orientation [2,7,17]. For instance, when somesthetic cues are altered (by completely immobilizing subjects in a specific device looking like a body cast [2] or in water immersion [17]), perception of upright body orientation becomes particularly inaccurate (body cast M = 6.5◦ of error; water immersion M = 7.3◦ of error). These results suggest that (1) the somesthetic system plays a major role in estimating the postural vertical and (2) the threshold of the otolith organs in detecting upright body orientation is higher than that of the somesthetic system. Therefore, in the range of position manipulated in our experiment (±7◦ ), the otoliths are probably not sensitive enough to provide additional sensory cues of verticality. Although constant contact of the body with the board was maintained by firmly strapping subjects, contact pressure against that board could vary when tilting about the vertical axis. Therefore, in contrast to subjective tasks in which subjects report their illusory body tilt by the use of a joystick [22], when adjusting the
body itself such somesthetic and pressure contact cues could easily be used to estimate body position [25] and therefore reduce the impact of vibration. Another interesting finding of the present experiment is the variable effect of tendon vibration according to the initial position of the subjects. We observed that the effect of tendon vibration observed in the backward initial position was more important than that observed when initially vertical and twice as important as that observed in the forward position. An explanation of such increasing effect of tendon vibration from pitching forward to pitching backward might stem from the basic properties of primary endings. As shown in the pioneer work of Burke et al. [3], during passive movements primary endings exhibited maximal vibration responsiveness during the stretching phase, sometime firing twice per vibration cycle. In contrast, during the shortening phase they usually ceased responding to the vibratory stimulus. When initially tilted backward, body adjustment was achieved by moving the backboard forward with the consequence of stretching calf muscles and placing primary endings in condition of optimal responsiveness. In contrast, when initially tilted forward, backward adjustment had the consequence of shortening calf muscles placing primary endings in condition of reduced responsiveness. Similarly, Cordo et al. [5] recently reported that passive slow and small arm movements could either enhance, stop or even reverse the direction of illusory arm movements when vibration was applied to the triceps brachii. Alternatively, the variable effect of tendon vibration during passive stretch or lengthening might be attributed to enhanced or compromised mechanical transfer of vibration from the tendon to the receptors in the muscle belly. However, such explanation might hold only when passive displacement are quite fast and of large amplitude as with those manipulated in previous experiments on illusory arm displacements [11,12]. In the present experiment, as well as in the experiment of Cordo et al. [5], velocity of passive displacements was small (Cordo et al. [5]: 0.3 ◦ s−1 , present experiment: 0.5 ◦ s−1 ) and the maximal displacement was limited (Cordo et al. [5]: 2.4◦ , present experiment: 7◦ ). Finally, Cordo et al. [5] suggested that such modulation of the vibration effect during slow passive displacements might also be the consequence of additive confluence of vibration evoked Ia input with movement-evoked multi-modal input. In summary, the present results showed that when required to adjust their body vertical in the absence of equilibrium constraints, standing subjects orient their body (backward) in agreement with the simulated elongation of calf muscles induced by vibration. Therefore, the perception of body orientation is coherent with the postural response classically observed in freely standing subjects although the relationship between these two responses remains to be elucidated. Acknowledgements The work was funded by the Centre de Recherches du Service de Sant´e des Arm´ees, BP 87, 38702, La Tronche Cedex, France. We thank Dr. Nicolas Forestier and the Laboratoire de Physiologie et Physiopathologie de l’Exercice et Handicap (PPEH,
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Universit´e de Savoie 73376 Le Bourget du lac, France) to allow us to use their EMG device. References [1] N. Adamcova, F. Hlavacka, Modification of human postural responses to soleus muscle vibration by rotation of visual scene, Gait Posture 25 (2007) 99–105. [2] L. Bringoux, V. Nougier, P.A. Barraud, L. Marin, C. Raphel, Contribution of somesthetic information to the perception of body orientation in the pitch dimension, Q. J. Exp. Psychol. 56 (2003) 909–923. [3] D. Burke, K.E. Hagbarth, L. Lofstedt, B.G. Wallin, The responses of human muscle spindle endings to vibration of non-contracting muscles, J. Physiol. 261 (1976) 673–693. [4] H. Ceyte, C. Cian, V. Nougier, I. Olivier, A. Roux, Effects of neck muscles vibration on the perception of the head and trunk midline position, Exp. Brain Res. 170 (2006) 136–140. [5] P.J. Cordo, V.S. Gurfinkel, S. Brumagne, C. Flores-Vieira, Effect of slow, small movement on the vibration-evoked kinaesthetic illusion, Exp. Brain Res. 167 (2005) 324–334. [6] G. Eklund, General features of vibration-induced effects on balance, Upsala J. Med. Sci. 77 (1972) 112–124. [7] R. Fitzpatrick, D. Burke, S. Gandevia, Task dependant reflex responses and movement illusions evoked by galvanic vestibular stimulation in standing humans, J. Physiol. 478 (1994) 363–372. [8] P.A. Fransson, E.K. Kristinsdottir, A. Hafstrom, M. Magnusson, R. Johansson, Balance control and adaptation during vibratory perturbations in middle-aged and elderly humans, Eur. J. Appl. Physiol. 91 (2004) 595– 603. [9] J.C. Gilhodes, J.P. Roll, M.F. Tardy-Gervet, Perceptual and motor effects of agonist–antagonist muscle vibration in man, Exp. Brain Res. 61 (1986) 395–402. [10] J.M. Goldberg, C. Fernandez, The vestibular system, in: I. Darian-Smith (Ed.), Handbook of Physiology. The Nervous System. Sensory Processes, vol. III, American Physiological Society, Bethesda, 1984, pp. 977– 1022. [11] G.M. Goodwin, M.C. Closkey, P.B. Matthews, The contribution of muscle afferents to kinaesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents, Brain 95 (1972) 705–748.
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[12] T. Kasai, M. Kawanishi, S. Yahagi, Effects of upper limb muscle vibration on human voluntary wrist flexion-extension movements, Percept. Motor Skills 78 (1994) 43–47. [13] A. Kavounoudias, J.C. Gilhodes, R. Roll, J.P. Roll, From balance regulation to body orientation: two goals for muscle proprioceptive information processing? Exp. Brain Res. 124 (1999) 80–88. [14] A. Kavounoudias, R. Roll, J.P. Roll, Foot sole and ankle muscle inputs contribute jointly to human erect posture regulation, J. Physiol. 532 (2001) 869–878. [15] J.R. Lackner, M.S. Levine, Changes in apparent body orientation and sensory localization induced by vibration of postural muscles: vibratory myesthetic illusions, Aviat. Space Environ. Med. 50 (1979) 346–354. [16] H. Lekhel, K. Popov, D. Anastasopoulos, A.M. Bronstein, K. Bhatia, C.D. Marsden, M. Gresty, Postural responses to vibration of neck muscles in patients with idiopathic torticollis, Brain 120 (1997) 583–591. [17] J. Massion, J.C. Fabre, L. Mouchnino, A. Obadia, Body orientation and regulation of the centre of gravity during movement under water, J. Vestib. Res. 5 (1995) 211–221. [18] U. Proske, Kinesthesia: the role of muscle receptors, Muscle Nerve 34 (2006) 545–558. [19] J.P. Roll, R. Roll, From eye to foot. A proprioceptive chain involved in postural control, in: B. Amblard, A. Berthoz, F. Clarac (Eds.), Posture and Gait, Elsevier, Amsterdam, 1988, pp. 155–164. [20] R. Roll, J.C. Gilhodes, J.P. Roll, K. Popov, O. Charade, V. Gurfinkel, Proprioceptive information processing in weightlessness, Exp. Brain Res. 122 (1998) 393–402. [21] J.P. Roll, J.P. Vedel, Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography, Exp. Brain Res. 47 (1982) 177–190. [22] J.P. Roll, J.P. Vedel, E. Ribot, Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study, Exp. Brain Res. 76 (1989) 213–222. [23] P. Romaiguere, J.P. Vedel, J.P. Azulay, S. Pagni, Differential activation of motor units in the wrist extensor muscles during the tonic vibration reflex in man, J. Physiol. 444 (1991) 645–667. [24] B.N. Smetanin, K.E. Popov, G.V. Kozhina, Human postural responses to vibratory stimulation of calf muscles under conditions of visual inversion, Hum. Physiol. 28 (2002) 554–558. [25] M. Trousselard, P.A. Barraud, V. Nougier, C. Raphel, C. Cian, Contribution of tactile and interoceptive cues to the perception of the direction of gravity, Brain Res. Cogn. Brain Res. 20 (2004) 355–362.
Effect of Achilles tendon vibration on postural orientation Hadrien Ceyte a , Corinne Cian a , Raphael Zory c , Pierre-Alain Barraud a , Alain Roux a , Michel Guerraz b,∗ a Centre de Recherches du Service de Sant´ e des Arm´ees, BP 87, 38702 La Tronche Cedex, France Laboratoire de Psychologie et Neurocognition CNRS, UMR 5105, Universit´e de Savoie, 73376 Le Bourget du lac, France c Laboratoire de Physiologie et Physiopathologie de l’Exercice et Handicap (PPEH), Universit´ e de Savoie, 73376 Le Bourget du lac, France b
Received 6 November 2006; received in revised form 12 January 2007; accepted 22 January 2007
Abstract Vibration applied to the Achilles tendon is well known to induce in freely standing subjects a backward body displacement and in restrained subjects an illusory forward body tilt. The purpose of the present experiment was to evaluate the effect of Achilles tendon vibration (90 Hz) on postural orientation in subjects free of equilibrium constraints. Subjects (n = 12) were strapped on a backboard that could be rotated in the antero-posterior direction with the axis of rotation at the level of the ankles. They stood on a rigid horizontal floor with the soles of their feet parallel to the ground. They were initially positioned 7◦ backward or forward or vertical and were required to adjust their body (the backboard) to the vertical orientation via a joystick. Firstly, results showed that in response to Achilles tendon vibration, subjects adjusted their body backward compared to the condition without vibration. This backward body adjustment likely cancel the appearance of an illusory forward body tilt. It was also observed that the vibratory stimulus applied to the Achilles tendon elicited in restrained standing subjects an increased EMG activity in both the gastrocnemius lateralis and the soleus muscles. Secondly, this vibration effect was more pronounced when passive displacement during the adjustment phase was congruent with the simulated elongation of calf muscles. These results indicated that the perception of body orientation is coherent with the postural response classically observed in freely standing subjects although the relationship between these two responses remains to be elucidated. © 2007 Elsevier Ireland Ltd. All rights reserved. Keywords: Body orientation; Vibration; Muscle spindles; Passive movement
The tendon vibration technique has been widely used to investigate the influence of proprioception, particularly muscle spindle endings in spatial perception and motor control. Vibration of sufficient amplitude and frequency applied to a muscle or tendon activates mainly the primary spindle endings connected to the large Ia afferent fibres, for which the firing rate seems to be interpreted by the CNS as an elongation of that muscle [3,21,22]. This erroneous interpretation induces in some circumstances illusory sensation of joint displacement [4,9,11,21] or motor effects such as contraction of the vibrated muscle (tonic vibratory reflex) [11,23] and compensatory postural responses [1,6,8,16,19]. For example, vibration applied to the Achilles tendons of standing subjects induces backward body sway [1,6,13,24]. This response mimics the postural correction that would have occurred if the proprioceptive receptors had been stimulated in a natural way,
∗
Corresponding author. Tel.: +33 4 79 75 81 45; fax: +33 4 79 75 81 48. E-mail address: [email protected] (M. Guerraz).
0304-3940/$ – see front matter © 2007 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2007.01.044
i.e. a stretching of the calf muscles by a forward sway that needs to be corrected. In contrast when those standing subjects were prevented from swaying, the same vibration can induce an illusory tilt in the opposite direction to the backward sway observed in the unrestrained condition [15]. Proprioceptive sensors are involved in the regulation of both equilibrium and orientation (body posture) as they provide the CNS with information about the position of the different body segments relative to each other, and then contribute to update the postural scheme [13]. Therefore, when standing freely, the spatio-temporal characteristics of the vibratory evoked response reflects the functions of both equilibrium and orientation. The classical way of questioning postural orientation in the absence of equilibrium constraints is to ask restrained subjects to report their feeling during the vibratory stimulation. The illusory tilt is evaluated either by asking subjects to verbally report their illusory feeling or by asking them to copy the virtual whole body movements they perceived by moving a joystick [20]. In the present experiment, the effect of a proprioceptive distur-
72
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bance on postural orientation applied to the Achilles tendons was investigated by asking subjects free of equilibrium constraints to adjust the body in a vertical position. Subjects were standing on a rigid floor with the soles of their feet parallel to the ground, and equilibrium constraints were suppressed by strapping them to a servo-controlled motorized backboard that could rotate in the antero-posterior direction with the axis rotating about the ankles. In this context, subjects had to maintain posture against gravity (maintain postural tone) but were not actively engaged in the maintenance of balance (equilibrium). The aim of the present experiment was to investigate the effect of tendon vibration on perceived postural orientation in restrained standing subjects. Twelve-volunteer subjects (6 females and 6 males; mean age 32 years) took part in this experiment. Subjects reported no apparent vestibular or somaesthetic abnormalities. In conformity with the Helsinki Convention, individual written informed consent was obtained. The subjects were restrained on a servo-controlled motorized backboard capable of being rotated in the sagittal plane (pitch dimension) with a 1◦ s−1 maximal velocity, and an initial acceleration and a final deceleration of 0.05◦ s−2 . Moving the backboard at this very slow velocity prevented responses of the semi-circular canals [10]. The pivot on which the platform rotated was approximately at the level of the malleoli. Thus the rotation of the backboard enabled the body of a subject to be tilted backward or forward with the soles of the feet remaining parallel to the ground. The platform position (0.005◦ accuracy) was controlled and recorded using a digital position encoder. All the experiment was computer driven. Once a comfortable upright posture had been adopted by the subject, he/she was secured to the backboard by means of three large straps fixed at the level of the forehead, abdomen and thighs. The system of straps enabled the subject to be stabilized in order to suppress equilibrium constraints. To stimulate the ankle proprioceptive system Achilles tendons were stimulated by an electromechanical physiotherapy vibrator apparatus (Techno-concept VB 115, frequency of 90 Hz and amplitude of 200 m) comprising of two vibrators secured over the Achilles tendons with elastic bands. The subject was placed in a dark room and kept their eyes closed throughout the experimental session. For a given trial, the backboard on which the subjects was strapped tilted and stopped at a preset position, 0◦ (vertical), or 7◦ forward, or backward (see Fig. 1A). After a 20 s delay, subjects were asked to adjust their body to the vertical orientation by means of a joystick input to reposition the backboard. A maximal deflection of the joystick in either a backward or forward direction resulted in a slow movement of the platform by 0.5◦ s−1 in the respective direction with an initial acceleration and final deceleration of 0.25◦ s−2 . No time constraint was imposed during the adjustment phase, but subjects were encouraged to respond without excessive deliberation. Subjects pushed a button on the joystick to signal that they had completed their adjustment. The platform was then rotated to the next preset position. No feedback was given to subjects about their performance during the session.
Fig. 1. (A) Experimental set-up. The subjects were strapped on a backboard that could be rotated in the antero-posterior direction with the axis of rotation at the level of the ankles. (B) Mean setting errors (◦ ) as a function of initial body orientation (7◦ forward, 0◦ vertical, 7◦ backward) with vibration (VIB) and without (NVIB) vibration. Error bars indicate the standard deviations.
Two sessions of 20 min were performed for each subject. Each session comprised 12 trials consisting of two blocks of 3 trials in the no-vibration condition and two blocks of 3 trials in the vibration condition. In each block, the three initial body orientations (7◦ forward, 0◦ vertical, and 7◦ backward) were randomly performed, except that the 0◦ orientation was never presented first. A delay of 1 min was inserted before each block in the upright position. In the vibration condition, the Achilles tendons were vibrated during this 1 min delay without interruption until the end of the block of three trials. The order of presentation of the different blocks was counterbalanced across subjects. The adjustments were expressed as the angle difference (◦ ) between the objective vertical position and the orientation of the backboard. The angle difference was considered to be negative if it deviated backward from the objective vertical orientation or positive if it deviated forward. The individual mean error was calculated for each orientation. We tested in a control experiment the possibility that the vibration evoked in restrained standing subjects a tonic vibratory reflex (TVR). Standing subjects (n = 8; mean age 29 years) were restrained on the backboard (by means of large straps) in a vertical position. EMG activity of the tibialis anterior (TA), the gastrocnemius lateralis (GL) and the soleus (Sol) muscles of the dominant leg was recorded in 6 trials of 40 s (ME 3000 P8, Mega Electronics Ltd., Kuopio, Finland). Silver chloride surface electrodes (Medicotest blue sensor type M-00-S, Olstykke, Denmark) with preamplifiers were placed over the muscle bellies of the TA, GL and Sol in a bipolar configuration with 3.5 cm
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inter-electrode distance. A reference electrode was attached to a body area remote from the studied muscles. Trials consisted of an initial period of 10 s without vibration (control period) followed by a period of 20 s of vibration (vibration period) and a post-vibratory period of 10 s (post-vibration period). Stimulus artifacts due to movement of the electrodes were excluded from the EMG data using a digital filter (band stop 75–105 Hz). Mean integrated EMG values (IEMG) for each subject in each group were calculated for both the vibration and non-vibration periods. The IEMG corresponding to the activity during voluntary maximal forces recorded for the TA, GL and Sol was considered to be 100% and the level of IEMG activity was calculated as a percentage of that maximal activity. We ensured that when no vibration was applied, no change in IEMG could be detected over a 40 s period. To find out whether vibration affected perception of body orientation, a 2 vibration (with and without) × 3 body initial orientation conditions (7◦ forward, 0◦ vertical, and 7◦ backward). ANOVA with repeated measures on the two factors was applied to the mean errors. A post hoc analysis (Newman–Keuls) was performed when P < .05. Results showed significant main effects of the initial body orientation [F(2,22) = 29.8; P < .05] and vibration conditions [F(1,11) = 29; P < .05] as well as an interaction between these two factors [F(2,22) = 5.88; P < .05]. Fig. 1B shows that without vibration stimulation (control condition), subjects’ estimates were influenced by their initial body orientation. Indeed, the subjective body vertical was close to the true gravitational vertical when subjects were initially vertical (M = −0.01◦ , S.D. = 1.98) but deviated in the direction of the initial orientation. When initially tilted backward or forward, subjects felt upright while being still tilted backward (M = −1.13◦ , S.D. = 2.06) and forward (M = 0.99◦ , S.D. = 1.76), respectively. Compared to the above control condition, vibration of the Achilles tendons induced systematic backward displacements of the subjective vertical body orientation. The mean amplitude of this backward tilt (vibration effect = VIB − NVIB) when the three initial body orientations were combined was −1.84◦ (S.D. = 1.4). As evident from the significant interaction between the two experimental factors (vibration × initial body position), the magnitude of this backward displacement (vibration effect) depended on the initial orientation of the subject. The vibration effect significantly increased from pitching forward to pitching backward and reached −1.21◦ (S.D. = 1.42) when subjects were initially tilted forward, −1.9◦ (S.D. = 1.43) and −2.41◦ (S.D. = 1.27) when subjects were initially vertical and tilted backward, respectively. Pairwise comparison indicated that the vibration effect in the forward orientation differed significantly from backward orientation (P < .05). The difference between the backward and vertical orientations was at the level of significance (P = 0.06) but forward and vertical orientation did not quite reach significance (P = 0.16). To find out whether vibration induces a TVR, mean IEMG values during the three periods of measure (control, vibration, post-vibration periods) were subjected to an ANOVA with repeated measures. A post hoc analysis (Newman–Keuls) was performed when P < .05.
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Fig. 2. Typical raw EMG responses of tibialis anterior (TA), gastrocnemius lateralis (GL) and Soleus (Sol) muscles to vibration (90 Hz).
As can be seen in Fig. 2, a vibratory stimulus applied to the Achilles tendon elicited in restrained standing subjects an increased EMG activity in both the GL [F(2,14) = 4.3, P < .05] and the Sol muscles [F(2,14) = 6.4, P < .05]. This motor response (TVR) observed during vibration decreased when vibration was stopped. Post hoc analysis revealed that the IEMG activity during vibration was significantly different from that measured in the control and post-vibration periods both for the GL (control = 3.4%, vibration = 4.6%, post-vibration = 3.7% of the maximal voluntary force) and the Sol muscles (control = 9.3%, vibration = 12.5%, post-vibration = 9.9%). In contrast, the vibratory stimulus applied to the Achilles tendon did not elicit a significant increased IEMG activity in the TA [F(2,14) = 2.8, P > .05]. Interestingly, seven out of the eight tested subjects reported that vibration induced after a few seconds an illusory forward body tilt and some of them spontaneously reported the feeling of being pushed forward by the backboard. This study was designed to investigate the contribution of muscle proprioception to the perception of body orientation in the absence of equilibrium constraints. Subjects were strapped to a motorized backboard tilting at the level of the ankles, and their task was to adjust their body (the backboard) vertical. Here, the body orientation task primarily concerns the sense of position and not the sense of movement. As reviewed recently by Proske [18], primary endings contribute both to the sense of position and movement, whereas secondary endings contribute to position sense only. In contrast to primary endings, secondary endings (II fibres) have been shown to be either insensitive or only slightly sensitive to tendon vibration. Therefore, the illusory forward tilt (sense of position) evoked by Achilles tendon vibration is likely the consequence of the recruitment of Ia fibers although the involvement of secondary endings cannot be fully excluded. In the condition of Achilles tendon vibration, subjects adjusted their body backward compared to the condition without vibration. This backward positioning is likely the counterpart of the illusory tilt evoked by vibration in upright restrained standing
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subjects as reported in the control experiment and in previous reports [15]. Indeed, vibration of the Achilles tendon simulates a lengthening of the calf muscles [3,21,22] that could be perceived by the subject as a forward tilt. By adjusting themselves backward, subjects cancelled this illusory tilt that would otherwise have occurred. Furthermore, in the EMG control experiment, we observed that Achilles tendon vibration induced in restrained standing subjects a TVR in both the GL and Sol muscles. This evoked motor response is probably an important component of the equilibrium responses in freely standing subjects [14]. In the restrained subjects of the present experiment, this tonic contraction of the calf muscles could create a reaction force of the body against the backboard. The increased pressures against the backboard are similar to what a subject would experience when tilted backward. However, verbal reports in the control EMG experiment and body adjustments in our main experiment disagree with a possible sensation of backward tilt. Indeed, in the control experiment, most subjects reported the illusion of being tilted forward when vibrated. Interestingly, they also had the feeling of being pushed forward by the backboard. The illusory forward body tilt in response to vibration might therefore result from a simulation of a lengthening of the calf muscles and an additional simulation of a push due to reaction forces of the body against the backboard related to the TVR. The backward adjustment observed (∼1.7◦ ) in response to tendon vibration is close to that reported with freely standing subjects in other experiments [1,24] but smaller than illusory tilt reported via a joystick in restrained conditions (∼10◦ in restrained pre-flight condition [22]). Although response amplitudes cannot be directly compared because of methodological reasons, one might have expected larger responses to vibration when equilibrium constraints were suppressed. Indeed, for biomechanical reasons, freely standing subjects have to limit any backward (or forward) body excursion in order not to go beyond the limits of postural equilibrium and fall. Such biomechanical limits were suppressed when strapped to a board as presently. The perception of body orientation is usually considered to be primarily based on vestibular information and secondarily on somesthetic information. However, several authors have challenged this view and showed the limit of otolith contribution in quasi static body orientation [2,7,17]. For instance, when somesthetic cues are altered (by completely immobilizing subjects in a specific device looking like a body cast [2] or in water immersion [17]), perception of upright body orientation becomes particularly inaccurate (body cast M = 6.5◦ of error; water immersion M = 7.3◦ of error). These results suggest that (1) the somesthetic system plays a major role in estimating the postural vertical and (2) the threshold of the otolith organs in detecting upright body orientation is higher than that of the somesthetic system. Therefore, in the range of position manipulated in our experiment (±7◦ ), the otoliths are probably not sensitive enough to provide additional sensory cues of verticality. Although constant contact of the body with the board was maintained by firmly strapping subjects, contact pressure against that board could vary when tilting about the vertical axis. Therefore, in contrast to subjective tasks in which subjects report their illusory body tilt by the use of a joystick [22], when adjusting the
body itself such somesthetic and pressure contact cues could easily be used to estimate body position [25] and therefore reduce the impact of vibration. Another interesting finding of the present experiment is the variable effect of tendon vibration according to the initial position of the subjects. We observed that the effect of tendon vibration observed in the backward initial position was more important than that observed when initially vertical and twice as important as that observed in the forward position. An explanation of such increasing effect of tendon vibration from pitching forward to pitching backward might stem from the basic properties of primary endings. As shown in the pioneer work of Burke et al. [3], during passive movements primary endings exhibited maximal vibration responsiveness during the stretching phase, sometime firing twice per vibration cycle. In contrast, during the shortening phase they usually ceased responding to the vibratory stimulus. When initially tilted backward, body adjustment was achieved by moving the backboard forward with the consequence of stretching calf muscles and placing primary endings in condition of optimal responsiveness. In contrast, when initially tilted forward, backward adjustment had the consequence of shortening calf muscles placing primary endings in condition of reduced responsiveness. Similarly, Cordo et al. [5] recently reported that passive slow and small arm movements could either enhance, stop or even reverse the direction of illusory arm movements when vibration was applied to the triceps brachii. Alternatively, the variable effect of tendon vibration during passive stretch or lengthening might be attributed to enhanced or compromised mechanical transfer of vibration from the tendon to the receptors in the muscle belly. However, such explanation might hold only when passive displacement are quite fast and of large amplitude as with those manipulated in previous experiments on illusory arm displacements [11,12]. In the present experiment, as well as in the experiment of Cordo et al. [5], velocity of passive displacements was small (Cordo et al. [5]: 0.3 ◦ s−1 , present experiment: 0.5 ◦ s−1 ) and the maximal displacement was limited (Cordo et al. [5]: 2.4◦ , present experiment: 7◦ ). Finally, Cordo et al. [5] suggested that such modulation of the vibration effect during slow passive displacements might also be the consequence of additive confluence of vibration evoked Ia input with movement-evoked multi-modal input. In summary, the present results showed that when required to adjust their body vertical in the absence of equilibrium constraints, standing subjects orient their body (backward) in agreement with the simulated elongation of calf muscles induced by vibration. Therefore, the perception of body orientation is coherent with the postural response classically observed in freely standing subjects although the relationship between these two responses remains to be elucidated. Acknowledgements The work was funded by the Centre de Recherches du Service de Sant´e des Arm´ees, BP 87, 38702, La Tronche Cedex, France. We thank Dr. Nicolas Forestier and the Laboratoire de Physiologie et Physiopathologie de l’Exercice et Handicap (PPEH,
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