Postural changes after sustained neck muscle contraction in persons with a lower leg amputation

Postural changes after sustained neck muscle contraction in persons with a lower leg amputation

Available online at www.sciencedirect.com Journal of Electromyography and Kinesiology 19 (2009) e214–e222 www.elsevier.com/locate/jelekin Postural c...

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Available online at www.sciencedirect.com

Journal of Electromyography and Kinesiology 19 (2009) e214–e222 www.elsevier.com/locate/jelekin

Postural changes after sustained neck muscle contraction in persons with a lower leg amputation Cyril Duclos a,b,c,*, Re´gine Roll a, Anne Kavounoudias a, Jean-Philippe Mongeau b,c, Jean-Pierre Roll a, Robert Forget b,c a

Laboratoire de Neurobiologie Humaine, UMR/CNRS 6149, Aix-Marseille Universite´s, Centre St. Charles, Pole 3C, Case B, 3, Place Victor Hugo, 13331 Marseille Cedex 03, France b Centre de Recherche Interdisciplinaire en Re´adaptation, Institut de Re´adaptation de Montre´al, 6300 Ave Darlington, Montre´al, QC, Canada H3S 2J4 c ´ Ecole de Re´adaptation, Faculte´ de Me´decine, Universite´ de Montre´al, C.P. 6128, Succ. Centre-ville, Montre´al, QC, Canada H3C 3J7 Received 11 October 2007; received in revised form 9 April 2008; accepted 9 April 2008

Abstract Lower leg amputation generally induces asymmetrical weight-bearing, even after rehabilitation treatment is completed. This is detrimental to the amputees’ long term quality of life. In particular, increasing strains on joint surfaces that receive additional weight load causes back and leg pain, premature wear and tear and arthritis. This pilot study was designed to determine whether subjects with lower leg amputation experience postural post-effects after muscle contraction, a phenomenon already observed in healthy subjects, and whether this could improve the weight-bearing on their prosthesis. Fifteen subjects with a unilateral lower leg amputation and 17 control subjects volunteered to participate in this study. Centre of pressure (CP) position was recorded during standing posture, under eyes closed and open conditions. Recordings were carried out before the subjects performed a 30-s voluntary isometric lateral neck muscle contraction, and again 1 and 4 min after the contraction. Postural post-effects characterized by CP shift, occurred in the medio-lateral plane in the majority of the amputated (7/15 eyes closed, 9/15 eyes open) and control (9/17 eyes closed, 11/17 eyes open) subjects after the contraction. Half of these subjects had a CP shift towards the side of the contraction and the other half towards the opposite side. In four amputated subjects tested 3 months apart, shift direction remained constant. These postural changes occurred without increase in CP velocity. Thus, a 30-s voluntary isometric contraction can change the standing posture of persons with lower leg amputation. The post-effects might result from the adaptation of the postural frame of reference to the proprioceptive messages associated with the isometric contraction. Ó 2008 Elsevier Ltd. All rights reserved. Keywords: Lower leg amputation; Postural asymmetry; Isometric contraction; Post-effects; Proprioception; Vision

1. Introduction Training for symmetrical weight-bearing is an important issue in the rehabilitation of persons with unilateral lower limb amputation. It is motivated by frequent clinical obser*

Corresponding author. Address: Centre de Recherche Interdisciplinaire en Re´adaptation, Institut de Re´adaptation de Montre´al, 6300 Ave Darlington, Montre´al, QC, Canada H3S 2J4. Tel.: +1 514 340 2111x3151; fax: +1 514 340 2154. E-mail address: [email protected] (C. Duclos). 1050-6411/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2008.04.007

vations of an asymmetrical weight-bearing in addition to laboratory measures confirming that more weight is taken on the non-amputated leg (Fernie and Holliday, 1978; Geurts et al., 1992; Hermodsson et al., 1994; Isakov et al., 1992). Altered force platform centre of pressure (CP) measures have also been demonstrated in persons with lower leg amputation. Increased anterior–posterior and medio-lateral CP oscillations have been shown (Fernie and Holliday, 1978; Geurts et al., 1992; Hermodsson et al., 1994; Isakov et al., 1992) while others reported decreased oscillations (Gauthier-Gagnon et al., 1986; Vittas et al., 1986).

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Beside affecting walking performance, the postural changes, and particularly the increased load on the nonamputated leg, are thought to cause additional blood flow deficits in persons with vascular disease (Gauthier-Gagnon et al., 1986), back and leg pain (Hagberg and Branemark, 2001) and premature wear and tear and arthritis on a long term basis because of the increased ground reaction forces (Nadollek et al., 2002). Thus, asymmetrical weight-bearing could impair functional capacities (Jones et al., 2001), thereby further reducing the quality of life of persons with lower leg amputation. Moreover, the postural asymmetry was shown to be difficult to correct through either classical rehabilitation (Geurts et al., 1992; Isakov et al., 1992), or training using augmented sensory feedback of limb load pressure (Gauthier-Gagnon et al., 1986). A procedure able to alter standing posture by means of a 30-s neck muscle isometric contraction with head straight has recently been described in able-bodied people (Duclos et al., 2004). It is based on the well-known ‘‘Kohnstamm phenomenon” where an involuntary movement occurs after a sustained isometric muscle contraction (Kohnstamm, 1915). The contraction, which was exerted in a sitting position, induced an involuntary, oriented and prolonged body leaning when the subjects stood up and closed their eyes after the end of the contraction. As an example, 11 of the 14 tested subjects were leaning leftward after 30 s of isometric effort towards the left side. Moreover, this ‘‘postural post-effect” persisted and remained oriented in this same direction for an average of 8 min after the end of contraction. Authors suggested that the post-effect is a consequence of a change in postural reference induced by the prolonged and strong proprioceptive message associated with the isometric voluntary contraction. Interestingly, this post-contraction postural effect was quite comparable to that described after muscle vibration (Duclos et al., 2005, 2007; Gilhodes et al., 1992; Wierzbicka et al., 1998). Such a postural change could eventually help amputees to increase weight-bearing on their prosthetic side. In order to test whether a postural post-effect could be induced in persons with an amputation, we assessed the effects of a 30-s neck muscle isometric contraction on these persons’ standing posture in eyes closed and open conditions and we compared them with those of non-amputated control subjects. The hypothesis of this study was that post-effects can alter standing posture in some lower leg amputees to help them place more weight on their prosthesis. Thus, the objectives of this pilot study were: (1) to confirm medio-lateral postural changes in persons with lower limb amputation by studying centre of pressure displacements, (2) to investigate the proportion of these persons that can show oriented postural post-effects following a maneuver as simple as a voluntary isometric neck muscle contraction, and (3) to document the impact of this maneuver on weight-bearing with and without vision in the subjects who experienced post-effects in the two groups. The results encourage future studies to evaluate postural posteffects training as a tool in the rehabilitation process.

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2. Methods 2.1. Subjects Fifteen subjects (42 ± 10 years old) with lower limb amputation (Table 1) were selected according to the following inclusion criteria: less than 60 years old, unilateral amputation due to trauma or cancer, more than 6 months of prosthetic training, and painless weight-bearing on the prosthesis. Subjects were excluded if the amputation was of vascular origin and if the Berg Balance Scale score (see below) was less than 50/56. The levels of amputation were trans-tibial (N = 10), trans-femoral (N = 4) and through knee (N = 1). Six subjects were amputated on the right leg, nine on the left leg. The mean average time since amputation was 5 years 4 months (median: 4 years; range: from 8 months to 21 years) before the study. Seventeen non-amputated healthy individuals of the same age (38 ± 10 years old, p = 0.21) participated as control subjects. This study was approved by the institutional ethics committee and informed consent to the experimental procedure was obtained for all participants. 2.2. Clinical evaluations Each subject’s balance was clinically assessed by means of the Berg Balance Scale (Berg et al., 1992, 1995). A score equal or above 50/56 was required to have subjects with balance skills sufficient for the needs of the postural experimental tasks. Amputated participants experienced most of the difficulties in tandem standing (six did not reach the maximal score) and forward reaching (five did not reach the maximal score). The Berg Balance Scale scores are presented in Table 1. The mean score of the amputees group (55 ± 1, mean ± SD) confirmed the good balance ability level of the amputees group. No exclusion occurred because of this test. The control group obtained a mean of 55.9/56 (one subject did not obtain the maximal score on forward reaching). Subjects with an amputation were also asked to fill in the Prosthetic Profile of Amputees (Grise et al., 1993) for information on their level of activity and use of their prosthesis. All the amputees could put on their prosthesis without aid, walk on all surfaces (two needed supervision), wear their prosthesis more than 8 h a day (median: 14 h; range: 8–16 h) and all but one (femoral amputee, 6 months since the beginning of prosthetic training) were involved in physical activity (i.e. walking, golf, skating, hiking, etc.) more than 4 h per week. 2.3. Equipment The Balance Master (NeuroComÒ International, Clackamas, USA) was used as a force platform to record centre of pressure (CP) displacements during the postural tests. Subjects were free to move, yet they were secured by means of a parachute-like harness that prevented them from falling to the ground but was not used to support their weight. A manual dynamometer (LafayetteÒ Manual Muscle Test System, Lafayette, USA; equipped with a Wheatstone bridge strain gauge load cell) was used to measure the maximal isometric force exerted during lateral head and trunk efforts (see Section 2.5). 2.4. Postural test Subjects were asked to ‘‘stand quietly, and as relaxed as possible”, on the platform in order to oscillate as naturally and freely

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Table 1 Characteristics of the amputated individuals Number

Age (years)

Time since amputation (months)

Amputation level

Side of amputation

Cause of amputation

Berg Balance Scale score (/56)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

42 58 42 26 36 43 58 33 56 44 45 53 35 36 29

144 53 18 38 87 72 24 18 8 252 68 29 10 54 84

TT TF TT TT TT TT TF TT TT TF TF TT TT TK TT

R R R L R L L R L L L R L L L

Traumatic Traumatic Traumatic Traumatic Traumatic Traumatic Traumatic Traumatic Cancer Traumatic Traumatic Traumatic Traumatic Traumatic Traumatic

55 54 55 56 55 56 52 56 56 55 55 55 55 55 55

Notes: TT = trans-tibial; TF = trans-femoral; TK = through-knee; R = right; L = left; Berg Balance Scale max score = 56.

as possible. Their feet were wedged against the inner corners of a T-shaped block, set in the centre of the platform, to maintain a distance of 3 cm between their heels. Subjects were tested under eyes closed and eyes open conditions, in this order. In both cases, they were asked to ‘‘look forwards”, even with the eyes closed under a blindfold. A trial consisted in 1 min recording of the CP displacements (100 Hz sampling rate) in the frontal and anteroposterior planes. Two trials, with a 2-min seated rest period between, were repeated both before, and immediately after standing up, after the lateral neck muscle contraction. Therefore, post-effects could be analyzed in the first and fourth minutes after the end of the contraction and compared with the two pre-contraction trials. An identical procedure was used under both vision conditions. In four amputated subjects demonstrating posteffects, the procedure was repeated 3 months later in order to evaluate the stability of the post-effect (amplitude and direction) over time.

given by the experimenter when the subject was more than 5% away from their target contraction intensity. The subject then stood up and CP displacements were recorded with eyes closed during two trials at the first and fourth minutes after the voluntary contraction. A 2-min seated rest separated the two trials. Then a second 30-s contraction was asked before two postural trials with eyes open, separated by a 2-min seated rest. This procedure was used because strong postural effects were already documented in healthy subjects when standing with eyes closed (Wierzbicka et al., 1998). We first wanted to replicate this result in amputated subjects, and then, investigate the possibility to induce post-effects with eyes open. In addition, we wanted to introduce another condition with eyes open in a sequence that would be similar to a rehabilitation session, where more than one contraction would be used.

2.5. Experimental procedure

To answer our first objective, mean CP position and root mean square (RMS) of the CP velocity were calculated from the CP coordinates during the minute of recording of each pre-contraction trial (Prieto et al., 1996). These values were compared between the two groups. In each group, the effect of vision on these CP characteristics was also tested. The raw data were then normalized for each subject by subtracting the mean CP position value obtained before contraction from each data point before and after contraction. This enabled the effect of the contraction to be shown independently of the pre-contraction position, which was variable across control subjects and even more variable across subjects with an amputation. To answer our second objective, we defined a clinically significant change as a shift of the CP larger than 0.5 cm in one of the two post-contraction trials. This was used to determine the proportion of subjects who experienced a post-effect. This threshold was chosen because it corresponds to a value equal to three standard deviations from the mean position observed in control subjects during standing (see Section 3). The shift of the CP was defined as the absolute value of the difference between the mean CP position in each trial and the mean CP position of the pre-contraction trials in the same vision condition. The proportion of subjects who experienced a post-effect was reported. To answer our third objective (characterize the

The design was chosen to determine if isometric contraction produces a postural post-effect that is liable to alter standing posture of subjects with an amputation. Amputated and control subjects followed the same procedure. Before doing any neck muscle contractions, two trials in standing posture were recorded eyes closed, then two with eyes open to determine pre-intervention CP position and displacement. The maximal isometric force during lateral head tilt was then measured using the manual dynamometer. It was held by the experimenter on the side of the head of the subjects seated on a chair without trunk constraint. To maintain subject concentration, this maximal voluntary contraction (MVC) was performed with eyes closed, as in the Wierzbicka et al. study (1998) showing post-effects after neck muscle vibration. It was asked towards the side of amputation for the amputees and towards the side opposite to leg dominancy for the control subjects. Over 4 s, subjects were verbally encouraged to produce the strongest effort they could. The peak force measured during two to three trials was considered the MVC. For the experimental procedure, the intervention consisted in a 30 s isometric contraction, in this direction, at an intensity of 50% MVC monitored by means of the dynamometer. Oral indications were

2.6. Data analysis

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post-effects), CP shift and CP velocity were compared before and after contraction for the subjects who experienced post-effects. Data are presented according to the side of the amputation or to the subjects’ leg dominancy, defined according to the leg used to kick a ball, in control subjects. Because Levene tests for homogeneity of variance were significant when comparing the two groups, non-parametric statistics were used. Wilcoxon ranked tests were used for repeated measures within each subjects’ group to compare successive trials, and pre- and post-contraction trials in subjects who experienced a post-effect and to compare both vision conditions. The differences between the two groups were assessed using Mann–Whitney Utest to compare corresponding conditions.

3. Results 3.1. Before contraction Before neck muscle contraction, with eyes closed, the amputated subjects exhibited a significant asymmetrical weight-bearing, compared to the control subjects (Mann– Whitney U-test, ZU = 2.89, p = 0.003) (Fig. 1). Their mean CP position was away from the centre of the platform, towards the non-amputated side (1.1 ± 0.3 cm, mean ± SEM) while the CP position of the control subjects was only 0.2 ± 0.1 cm towards their dominant side. The amputees’ CP also oscillated at a higher velocity (ZU = 2.02, p = 0.043) than that of the healthy subjects (Fig. 2A, pre-contraction trial). Under eyes open condition, amputees’ asymmetry decreased to 0.7 ± 0.2 cm away from the centre (Zw = 2.61, p = 0.009). However, they were still bearing more weight on their non-amputated leg, away from the position of the healthy subjects (ZU = 2.12, p = 0.034). The healthy subjects kept the same position as with the eyes closed (0.2 ± 0.1 cm to the right) (Fig. 1B). Opening the eyes also decreased CP velocity in control subjects (Zw = 3.62, p < 0.001) and in subjects with an amputation (Zw = 3.41, p < 0.001), who no longer oscillated faster than non-amputated subjects (RMS velocity: ZU = 1.42, p = 0.157) (Fig. 2B).

Fig. 1. Mean centre of pressure (CP) position (with ±SEM) before contraction in eyes closed (A, upper row) and eyes open (B, lower row) conditions in healthy subjects (grey squares) and amputees (black dots). Negative values are on the non-dominant side for healthy subjects or on the amputated side in amputees, positive values are on the dominant side in healthy subjects or on the non-amputated side in amputees. A clear postural asymmetry is shown in amputees where the CP is shifted towards the non-amputated leg.

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3.2. Effect of contraction Once the subjects stood up after the contraction, the majority (see below) experienced involuntary body leaning that pulled them laterally away from their pre-contraction standing posture. As an example, Fig. 3 shows, for a single amputated subject, the alterations of the CP displacements induced after muscle contraction in the eyes open condition. The two pre-contraction trials reveal the preferential weight-bearing on the non-amputated side. Once the subject stands up at 1 and 4 min after the contraction, the CP is gradually shifted towards the prosthetic side. Because the isometric lateral neck muscle contraction did not produce a post-effect in the antero-posterior plane, i.e. a CP shift larger than the chosen threshold of 0.5 cm (see Section 2), in any of the amputees or control subjects, only the results in the medio-lateral plane are presented. In the amputee group with eyes closed, CP displacements shifted more than 0.5 cm compared to pre-contraction trials (post-effect threshold) in seven subjects (Fig. 2A, on the right). The shift was observed both at 1 min (0.8 ± 0.3 cm) and 4 min (0.7 ± 0.1 cm) after the contraction. Similar postural changes were observed in 9 out of 17 control subjects (CP shift: first minute: 0.9 ± 0.1 cm, fourth minute: 0.4 ± 0.1 cm) (Fig. 2A, on the left; Table 2). This lateral CP shift was directed toward the non-amputated or dominant side in half of the subjects and toward the amputated or nondominant side in the other half in either the amputated or control group of subjects. In the eyes open condition, the isometric contraction shifted the displacements of the CP in nine subjects with an amputation (CP shift: first minute: 1.4 ± 0.2 cm, fourth minute: 0.4 ± 0.1 cm) and 11 healthy subjects (CP shift: first minute: 0.6 ± 0.2 cm, fourth minute: 0.4 ± 0.1 cm) (Fig. 2B; Table 2). A significant decrease (p = 0.01) of the CP shift amplitude between the first and fourth minute post-contraction was observed only in the amputees in the eyes open condition. It is also important to note that the RMS of the CP velocity was similar before and after the contraction in both groups, under both vision conditions, except for a small but significant decrease in the second test 4 min post-contraction in the eyes open condition for the amputees (Zw = 2.67, p = 0.008) (Fig. 2B, on the right). The four amputees tested 3 months later once again showed a strong post-effect. The direction of the CP shifts remained constant, that is, in the same direction as observed in the first session’s trials (i.e. three towards the Table 2 CP shifts after neck muscle contraction (in cm) Eyes closed

Amputated group Control group

Eyes open

1 min

4 min

1 min

4 min

0.8 ± 0.3 0.9 ± 0.1

0.7 ± 0.1 0.4 ± 0.1

1.4 ± 0.2 0.6 ± 0.2

0.4 ± 0.1 0.4 ± 0.1

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Fig. 2. Mean postural post-effects of a neck muscle contraction in healthy subjects (left column) and in amputees (right column) in eyes closed (A) and eyes open (B) quiet standing conditions. Black bars represent centre of pressure (CP) shift magnitude from mean pre-contraction CP position and white squares represent RMS of the CP velocity before (Pre), 1 and 4 min after neck muscle contraction (arrow). Values are expressed as mean ± SEM. CP position is shifted after contraction without higher CP velocity.

Fig. 3. Example of frontal displacement of one amputated subject’s centre of pressure (CP) during eyes open quiet standing test before (pre1, pre2), and 1 and 4 min after the contraction (arrow) of the neck muscles on the amputated side. The CP is on the non-amputated side before the contraction and is shifted on the amputated side during the first minute after contraction.

prosthesis, one towards the non-amputated leg). CP shift magnitude also remained in the same range between the two sessions. In the eyes open condition, the CP shift was 1.7 ± 0.5 cm vs. 1.2 ± 0.9 cm (first minute) and 0.5 ±

0.2 cm vs. 0.6 ± 0.1 cm (fourth minute) in the first vs. second session. In the eyes closed condition, the CP shift was 0.6 ± 0.5 cm vs. 1.6 ± 0.6 cm (first minute) and 0.1 ± 0.1 cm vs. 0.5 ± 0.3 cm (fourth minute).

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4. Discussion 4.1. Asymmetrical weight-bearing and postural deficits in amputees The results obtained in this study confirmed the previous findings that, before the treatment, there is an asymmetrical weight-bearing in subjects with a lower leg amputation compared to that of non-amputated subjects (Arsenault and Valiquette, 1981; Gauthier-Gagnon et al., 1986; Nadollek et al., 2002; Summers et al., 1987). Proprioceptive and cutaneous loss due to leg amputation probably contributes to the asymmetry, since central integration of multiple sensory inputs arising from both body sides is known to be crucial for symmetrical posture (Geurts and Mulder, 1992). Indeed, forced asymmetric pressure distribution under the foot soles, induced either by anesthesia or by vibration, gives rise to an erroneous sensation of body inclination (Andre´-Dehays and Revel, 1988; Roll et al., 2002) or to an actual body leaning to compensate for the virtual disequilibrium (Kavounoudias et al., 1999). Our data also confirm that visual information is useful in subjects with amputation to decrease the velocity of CP oscillations (Fernie and Holliday, 1978; Hermodsson et al., 1994; Isakov et al., 1992; Nadollek et al., 2002). However, even with the use of vision, the mean CP position of the persons with an amputation was still away from the mean position of the control subjects (i.e. asymmetrical weight-bearing). This suggests that the proprioceptive loss was not totally compensated for by visual information even many years after amputation. It has been shown that subjects with an amputation due to diabetes complications rely heavily on visual information at the beginning of the rehabilitation process and that this dependence is still present, but decreased, after prosthetic training while postural balance improves (Geurts et al., 1992; Isakov et al., 1992). Our results suggest that visual information is also important after a traumatic amputation even though the postural abilities have been shown to be better in unilateral traumatic amputees than in unilateral diabetic amputees (Hermodsson et al., 1994). The postural changes observed in the amputees could have an impact on their functional abilities. Faster oscillations of the CP were correlated with an increased risk of falling in the elderly (Fernie et al., 1982) and especially during multitask activity in people with a history of falling (Shumway-Cook et al., 1997). Moreover, the increased load may augment the risk of arthritic joint degeneration of the non-amputated leg and thus the risk to impinge on the daily functional ability and quality of life of the lower leg amputees (Hagberg and Branemark, 2001). Conversely, the faster oscillations could be an adaptation to the loss of the lower leg afferents because of the amputation. The postural oscillations may be used by the central nervous system to collect more information from the remaining sensory receptors liable to partly compensate the sensory loss from the amputated foot (Gatev et al.,

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1999; Loram et al., 2005). This adaptation is all the more important since it appears that the compensation strategy for the loss of sensory inputs in unilateral amputees does not come from an increased sensitivity of the contralateral non-amputated leg (Kavounoudias et al., 2005). This sensory loss may thus require more postural oscillations to obtain enough sensory information necessary for efficient postural control. 4.2. Postural post-effects after muscle contraction The weight-bearing alteration observed in the majority of amputees and control subjects confirms that a 30-s neck muscle contraction can produce oriented post-effects and that they can persist at least 4 min after the end of the contraction (Duclos et al., 2004). This postural deviation, when present, was induced in a specific medio-lateral direction, which is the plane of action of the contracting muscles. Previous results support the notion that the postural post-effect is oriented as a function of the contraction site (Duclos et al., 2004; Kluzik et al., 2005; Wierzbicka et al., 1998) and that this orientation is consistent over time for the same subject, as shown in this study with the four amputees tested 3 months apart, and also across sessions (Kluzik et al., 2005; Sapirstein et al., 1937). Although confirmation with a larger group of amputees is required, this result is important for the eventual use of these post-effects in rehabilitation. An important question remains as to why the posteffect was experienced only by 7 or 9 of the 15 subjects with an amputation in the eyes closed and open conditions, respectively. Based on a visual analysis of the individual data, the level of amputation or the time since amputation did not seem to directly influence the posteffects. No trend appeared among the above-knee amputees to show more or less post-effects than the below-knee amputees, or in recent vs. older amputees. The fact that only 15 amputated subjects participated in the study limited the possibility to statistically test the effect of these factors. Since all subjects performed well (score above 52/56) in the Berg evaluation and had no pain (see exclusion criteria), these factors, including physical inability to shift towards the prosthesis, cannot be held responsible for the absence of post-effects either. However, it is possible that the visual inputs decreased the duration of, or inhibited, the post-effects in the amputees who rely more on vision than healthy subjects, as stated above. This would be supported by the finding that the CP shift amplitudes decreased rapidly after the first minute post-contraction. It must also be reminded that the post-effects were measured after only one or two muscle contractions in a single session. Future studies should evaluate if training with multiple contractions in repeated sessions could induce the postural effects, eventually longer and with larger amplitude, and determine if it is possible to induce in that way post-effect in every subject.

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The impact of post-effects on functional tasks is a relevant question, as well, for their use in rehabilitation. Recently, walking direction of healthy subjects was reoriented according to the preceding rotational effort exerted at the pelvis level during 30 s (Ivanenko et al., 2006). Also, stepping in place (Bove et al., 2002) and walking (Bove et al., 2001) were affected after a prolonged vibration of muscles on the side of the neck in control subjects. However, the orientation of the post-effects in these later studies was much more variable than the one described after contraction in the Ivanenko and colleagues’ study (Ivanenko et al., 2006). It must be noted that, in these last three studies, the contraction or vibration was applied to subjects while standing, as in Kluzik et al. (2005), and contrary to our experimental setup. The importance of applying the proprioceptive stimulation generated by muscle vibration in sitting in order to change the postural reference system has been discussed before (Duclos et al., 2007). Briefly, it was argued that it is better to vibrate while sitting because the perturbations produced by the vibration in standing could interfere with the proprioceptive inputs of the stimulation used to change the postural reference system. 4.3. Sustained proprioceptive afferents may modify the postural reference The hypothesis we hold concerning the mechanisms of the post-effect is that a change of the postural reference (Duclos et al., 2004; Kluzik et al., 2005; Wierzbicka et al., 1998) is caused by the sustained 30-s proprioceptive message that accompanies the isometric voluntary contraction (Vedel and Roll, 1983; Edin and Vallbo, 1990). The postural reference, and a control level, are the two parts of the postural system conceived as a two-level organization (Horak and Macpherson, 1996; Massion, 1998) (or ‘‘conservative” and ‘‘operative” levels, respectively, Gurfinkel et al., 1995). The reference level is a representation of the body configuration fed with and continuously updated on the basis of different sensory inputs such as proprioceptive, foot sole, visual and vestibular afferents. The control level effectively organizes the body posture depending on the configuration set at the reference level. The experimental indexes we used in this study are possibly related to these two levels of organization. It was previously proposed that the reference level could be cued by the position of the CP and the control level by the RMS velocity index (Prieto et al., 1996). That we found a shift of the CP without increase of the RMS velocity values after the contraction supports the hypothesis of an adaptation of the reference, whereas the control of the CP displacements was not affected. In other words, the subjects oscillated around a new mean position with the control level managing the body oscillations in the same way than before the contraction. Finally, that the direction of the post-effects in the medio-lateral plane is not the same between the subjects after the contraction may be due to the preference of a different postural frame of reference, i.e. to different weights

attributed to the proprioceptive and vestibular afferents in the control of the standing posture (Duclos et al., 2007; Kluzik et al., 2005). Subjects who rely mainly on the proprioceptive frame of reference complied with this reference and leaned to the side of the contraction once they stood up. Contrarily, the subjects who rely on a gravity-based reference frame would react against this altered reference, which would lead to asymmetrical inputs that do not fit with the gravity-based reference frame. Thus, they leaned to the opposite of the modified postural reference to counter-balance it. 5. Conclusion A post-effect, induced by a 30-s voluntary isometric contraction of neck muscles in sitting, can involuntarily modify the standing posture of subjects with a lower leg amputation. In a single session, one or two contractions led to an involuntary increase of weight-bearing on the prosthetic side in half the subjects who experienced the post-effect, while the others showed a weight shift in the opposite direction. The reasons for this are still speculative and could involve the use of a different frame of reference. More studies are needed to understand the determinants of these behaviors and the consequences of a regular training program involving the use of the contraction-induced post-effect in a full physical therapy treatment to improve postural symmetry. A better understanding of the impact of the post-effect, particularly during dynamic equilibrium and functional activities, will also be necessary to evaluate if such induced postural changes can benefit individuals with a lower leg amputation or other pathologies leading to asymmetrical weight-bearing. Acknowledgements We are grateful to the employees of the Institut de Re´adaptation de Montre´al, Christian Murie, for his clinical advice, Michel Goyette for his computer programming skills and Daniel Marineau for his technical assistance. This study was supported by Consulat Ge´ne´ral de France au Que´bec and Ministe`re des Relations Internationales du Que´bec and CNRS (France) Grants. References Andre´-Dehays C, Revel M. Roˆle sensoriel de la plante du pied dans la perception du mouvement et le controˆle postural. Med Chir Pied 1988;4:217–23. Arsenault AB, Valiquette C. Etude de la statique posturale des ampute´s du membre infe´rieur: corre´lations the´oriques et pratiques de la mise en charge. Physiother Canada 1981;33:17–23. Berg KO, Wood-Dauphinee SL, Williams JI. The Balance Scale: reliability assessment with elderly residents and patients with an acute stroke. Scand J Rehabil Med 1995;27:27–36. Berg KO, Wood-Dauphinee SL, Williams JI, Maki B. Measuring balance in the elderly: validation of an instrument. Can J Public Health 1992;83:S7–S11.

C. Duclos et al. / Journal of Electromyography and Kinesiology 19 (2009) e214–e222 Bove M, Courtine G, Schieppati M. Neck muscle vibration and spatial orientation during stepping in place in humans. J Neurophysiol 2002;88:2232–41. Bove M, Diverio M, Pozzo T, Schieppati M. Neck muscle vibration disrupts steering of locomotion. J Appl Physiol 2001;91:581–8. Duclos C, Roll R, Kavounoudias A, Roll JP. Long-lasting body leanings following neck muscle isometric contractions. Exp Brain Res 2004;158:58–66. Duclos C, Roll R, Kavounoudias A, Roll JP, Forget R. Change in standing posture of lower limb amputees after muscle vibration: a potential tool for rehabilitation. Gait Posture [Abstracts of the XVIIth conference of posture and gait research] 2005;21(Suppl. 1):S129. Duclos C, Roll R, Kavounoudias A, Roll JP, Forget R. Vibration-induced post-effects: a means to improve postural asymmetry in lower leg amputees? Gait Posture 2007;26:595–602. Edin BB, Vallbo AB. Muscle afferent responses to isometric contractions and relaxations in humans. J Neurophysiol 1990;63:1307–13. Fernie GR, Gryfe CI, Holliday PJ, Llewellyn A. The relationship of postural sway in standing to the incidence of falls in geriatric subjects. Age Ageing 1982;11:11–6. Fernie GR, Holliday PJ. Postural sway in amputees and normal subjects.J Bone Joint Surg 1978;60-A:895–8. Gatev P, Thomas S, Kepple T, Hallett M. Feedforward ankle strategy of balance during quiet stance in adults. J Physiol 1999;514:915–28. Gauthier-Gagnon C, St-Pierre D, Drouin G, Riley E. Augmented feedback in the early training of standing balance of below-knee amputees. Physiother Canada 1986;38:137–42. Geurts AC, Mulder TW. Reorganisation of postural control following lower limb amputation: theoretical considerations and implications for rehabilitation. Physiother Theor Pract 1992;8:145–57. Geurts AC, Mulder TW, Nienhuis B, Rijken RA. Postural reorganization following lower limb amputation. Possible motor and sensory determinants of recovery. Scand J Rehabil Med 1992;24:83–90. Gilhodes JC, Gurfinkel VS, Roll JP. Role of Ia muscle spindle afferents in post-contraction and post-vibration motor effect genesis. Neurosci Lett 1992;135:247–51. Grise MC, Gauthier-Gagnon C, Martineau GG. Prosthetic profile of people with lower extremity amputation: conception and design of follow-up questionnaire. Arch Phys Med Rehabil 1993;74:862–70. Gurfinkel VS, Ivanenko YP, Levik YS, Babakova IA. Kinesthetic reference for human orthograde posture. Neuroscience 1995;68:229–43. Hagberg K, Branemark R. Consequences of non-vascular trans-femoral amputation: a survey of quality of life, prosthetic use and problems. Prosthet Orthot Int 2001;25:186–94. Hermodsson Y, Ekdahl C, Persson BM, Roxendal G. Standing balance in trans-tibial amputees following vascular disease or trauma: a comparative study with healthy subjects. Prosthet Orthot Int 1994;18:150–8. Horak FB, Macpherson JM. Postural orientation and equilibrium. In: Rowell L, Shepherd J, editors. Handbook of physiology. Section 12. Exercise: regulation and integration of multiple systems. New York: Oxford University Press; 1996. p. 255–92. Isakov E, Mizrahi J, Ring H, Susak Z, Hakim N. Standing sway and weight-bearing distribution in people with below-knee amputations. Arch Phys Med Rehabil 1992;73:174–8. Ivanenko YP, Wright WG, Gurfinkel VS, Horak F, Cordo P. Interaction of involuntary post-contraction activity with locomotor movements. Exp Brain Res 2006;169:255–60. Jones ME, Bashford GM, Bliokas VV. Weight-bearing, pain and walking velocity during primary transtibial amputee rehabilitation. Clin Rehabil 2001;15:172–6. Kavounoudias A, Roll R, Roll JP. Specific whole-body shifts induced by frequency-modulated vibrations of human plantar soles. Neurosci Lett 1999;266:181–4. Kavounoudias A, Tremblay C, Gravel D, Iancu A, Forget R. Bilateral changes in somatosensory sensibility after unilateral below-knee amputation. Arch Phys Med Rehabil 2005;86:633–40.

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Cyril Duclos received his state degree in Physical Therapy in 1998, a bachelor degree in Cognitive Sciences in 2000 from Universite´ de Provence, France, a MSc degree in Biomechanics and Physiology in 2002, from Universite´ Paris-XI, France. He also received a cosupervised PhD degree in Neuroscience (Universite´ de Provence, France) and Biomedical Sciences, option rehabilitation (Universite´ de Montre´al, Canada) in 2006. He is a post-doctoral fellow in pathokinesiology laboratory at the Centre for Interdisciplinary Research in Rehabilitation, Montre´al Rehabilitation Institute. His research interests are in the area of sensory-motor control of balance and gait, in relation with rehabilitation. Re´gine Roll, PhD 1980, is a Research Engineer in the Laboratory of Integrative and Adaptive Neurobiology, National Center of Scientific Research (CNRS, UMR 6149) and Aix-Marseille University, France. With a scientific background in Psychology and Neuroscience, she is involved in basic and applied research in the field of perception and control of human movement with special interest in somesthesia in human posture, visuo-motor coordinations, multisensory integration and sensorimotor rehabilitation.

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Anne Kavounoudias is an Assistant Professor of Neuroscience in the Laboratory of Integrative and Adaptive Neurobiology, National Center of Scientific Research (CNRS, UMR 6149) and Aix-Marseille University, France. She received a PhD degree from Aix-Marseille University in 1999 followed by post-doctoral training at the Institut de Re´adaptation de Montre´al (Que´bec, Canada). She conducts basic neuroscience research on multisensory integration to better understand how various sensory modalities contribute jointly to human postural control and body movement perception. Jean-Philippe Mongeau received his BSc in Physiotherapy from the School of Rehabilitation, Faculty of Medicine of the Universite´ de Montre´al in 2005. He participated to this project as a summer research student. He currently works in orthopaedic rehabilitation in a private practice.

Jean-Pierre Roll has been a Professor in the Laboratory of Integrative and Adaptive Neurobiology, National Center of Scientific Research (CNRS, UMR 6149) and Aix-Marseille University, France since 1983. He received his PhD in Sciences in 1981 from the University of Provence. Head of the Human Neurobiology team, he is involved in and supervises research in the field of human motor control and kinaesthesia. His research interest mainly concerns proprioception for posture and movement purposes in healthy and disabled persons.

Robert Forget has a BSc in Physical Therapy from McGill University. After 3 years of clinical practice, he did a MSc and a PhD in Neurological Sciences at Universite´ de Montre´al. He pursued post-doctoral work in human neurophysiology at Hoˆpital de la Salpeˆtrie`re in Paris, France and in Psychophysiology at Tilburg University in The Netherlands. He is a full ´ cole de Re´adaptation” of professor at the ‘‘E the Faculty of Medicine at Universite´ de Montre´al. In April 2000, he founded the Centre de Recherche Interdisciplinaire en Re´adaptation du Montre´al me´tropolitain (CRIR) and has been the scientific director of biomedical research of this Research Center ever since. His scientific interests are in sensory-motor integration during normal and pathological posture and movement in human; somatosensory sensibility and adaptation after lesions of the peripheral and central nervous system; excitability of nervous circuits in relation to muscle force and coordination and sensory input based interventions for neurological rehabilitation.