CHAPITRE IV POSTURAL STABILITY IS ALTERED BY THE STIMULATION OF Aδ AND C NOCICEPTORS BUT NOT BY Aδ AND C WARM RECEPTORS

(Soumis à Journal of Physiology London)

Jean-Sébastien Blouin1, Philippe Corbeil1-2 & Normand Teasdale1

1 Université Laval, Division de kinésiologie, Faculté de Médecine, Québec, Canada.

2 Université Joseph-Fourier, UFR-APS, Grenoble, France.

Key Words: Postural control, Aδ and C warm receptors, Aδ and C nociceptors

Correspondence to:

Normand Teasdale

Division de kinésiologie, PEPS Local 00233, Université Laval, Québec, Canada G1K7P4

Fax: 418-656-2441, Phone: 418-656-2147

Email: normand.teasdale@kin.msp.ulaval.ca

RÉSUMÉ

Le but de cette étude est de déterminer si les afférences de petit diamètre des thermorécepteurs de la peau peuvent influencer les processus de contrôle impliqués dans le maintien de l’équilibre en station debout. Deux stimulations cutanées (expérience 1 : une stimulation à 40°C; expérience 2 : une stimulation à 45°C) sont livrées à l’aide de grilles thermiques fixées sur les mollets des sujets afin de stimuler les thermorécepteurs et les nocicepteurs (reliés à la sensation de douleur). La stimulation à 40°C provoque une légère sensation de chaleur et la stimulation à 45°C engendre une perception de douleur. Ces stimulations montrent respectivement des résultats moyens de 0 et de 46 mm sur l’échelle visuelle analogue de perception de la douleur. Pour chaque expérience, dix sujets ont effectué huit essais par condition (vision, non vision et non vision vibration avec et sans stimulation cutanée) et chaque essai avait une durée de 30 secondes. La stimulation des thermorécepteurs (40°C) n’a pas altéré les caractéristiques des déplacements du centre de pression observées en situation sans stimulation. Avec la douleur (45°C), une augmentation des oscillations posturales (augmentation de l’étendue, de la variabilité et de la vitesse moyenne des déplacements du centre de pression) est observée. En douleur, l’augmentation observée pour la vitesse moyenne du centre de pression est encore plus prononcée lorsque les sujets devaient se maintenir en station debout les yeux fermés et les yeux fermés avec une co-vibration des tendons de la cheville. Ce résultat appuie l’hypothèse qu’il existe une convergence des informations provenant des nocicepteurs et des fibres afférentes Ia au niveau de la moelle épinière. Ces résultats suggèrent que le système de contrôle postural est affecté par la stimulation des nocicepteurs à travers les processus sensori-moteurs plutôt que les processus liés à la cognition.

SUMMARY

It is now recognized that large diameter myelinated afferents provide the primary source of lower limb proprioceptive information for maintaining an upright standing position. Small diameter afferents transmitting noxious stimuli, however, can also influence motor behaviors. Two cutaneous heat stimulations (experiment 1: non-noxious 40°C; experiment 2: noxious 45°C) were applied bilaterally on the calves of the subject with two thermal grills to stimulate Aδ and C warm receptors and nociceptors in order to examine their effects on postural stability. The non-noxious stimulation induced a gentle sensation of warmth and the noxious stimulation induced a perception of heat pain (visual analogue scores of 0 and 46 mm, respectively). For both experiments, ten healthy young adults were tested with and without heat stimulations of the lower limbs while standing upright on a force platform with eyes open, eyes closed and eyes closed with tendon co-vibration of tibialis anterior and triceps surae muscles. The center of pressure displacements were analyzed to examine how both stimulations affected the regulation of quiet standing and if the effects were exacerbated when vision was removed or ankle proprioception perturbed. The stimulation of the warm receptors did not induce any postural deterioration. With pain, subjects showed an increased standard deviation, range and mean velocity of postural oscillations. The effects of heat pain were exacerbated when subjects had their eyes closed and ankle tendons vibrated (increased mean velocity of the center of pressure). The observed deteriorating effects of the combined stimulation of nociceptors and Ia afferents could result from the convergence of these afferents at the spinal level. The present results suggest that the postural control system was deteriorated by the stimulation of nociceptors via sensorimotor rather than cognitive processes.

INTRODUCTION

The control of an upright standing posture is an essential motor behavior; it offers the stable platform for several goal-directed movements that we perform with the upper limbs. External and internal forces acting on the erect body create destabilizing events yielding postural oscillations (Hunter & Kearney, 1981). The postural control system regulates these body oscillations by maintaining the vertical alignment of the body segments. The effectiveness of the postural control system depends on the availability and reliability of the visual, vestibular and proprioceptive afferent inputs and the motor outputs (Massion, 1994). When any of these components is altered, body sway generally increases and postural muscle activities increase concurrently in order to maintain postural equilibrium (Dietz, 1992). For example, withdrawal of visual information (Brandt et al. , 1986), co-vibrating the ankle tendons (falsifying or masking the muscle spindle inputs from muscles lengthening) (Eklund, 1972; Hayashi et al. , 1988; Hay et al. , 1996) or providing inaccurate ankle sensory information by sway-referencing the support surface (Manchester et al. , 1989; Horak & Diener, 1994) all yield increases in body oscillations.

Large diameter myelinated afferents provide the primary source of lower limb proprioceptive information (e.g. pressure and position sense receptors) for maintaining an erect stance. Small diameter afferents also can influence motor behaviors. Noxious stimuli (chemical, thermal or mechanical) activate nociceptors which are the peripheral endings of small diameter primary sensory neurons. Sherrington (1910) first proposed that the withdrawal of a limb from a noxious stimulus is controlled by the flexor reflex afferent system. The flexor reflex afferent system is characterized by descending commands from supraspinal centers and by convergence of small and large diameter afferent inputs to interneuron pathways (Lundberg, 1979; Lundberg et al. , 1987). The excitability of the segmental gamma and alpha motoneurone pools is influenced by the stimulation of nociceptors (Matre et al. , 1998; Rossi et al. , 1999a; Capra & Ro, 2000), highlighting the possible role of the high threshold small diameter afferents in the control of movement.

Some authors suggested that chronic pain activity induces steady variations in interneuronal transmission that could alter motor strategies (Rossi & Decchi, 1997). For instance, prolonged exposure to nociceptive stimulations from the skin or sore muscles affect the perception of a produced torque (Weerakkody et al. , 2003). In their experiment, Weerakkody et al. (2003) reported that subjects overestimated the level of torque generated by a limb affected by a pain stimulation. Also, pain can induce a distortion of the body image, leading to a biased estimation of the body position in space (Gandevia & Phegan, 1999). Despite these evidences showing the effects of painful stimulations on the sensorimotor system, their effects on the postural control system have not been well documented. A better knowledge of how nociceptive mechanisms affect the control of posture could help for developing new and adapted therapeutic approaches for patients presenting acute and chronic pain.

In the present study, two distinct experiments were performed: first, a 30-s cutaneous heat stimulation (40°C) was used to stimulate small diameter afferents yielding a gentle warmth sensation; second, a 30-s cutaneous heat stimulation (45°C) was used to stimulate small diameter afferents yielding a pain sensation described as a distinct burning and prickling experience. These two experiments were performed to determine if a gentle stimulation of the cutaneous thermal receptors can deteriorate the control of an upright stance or if the stimulation has to be directed specifically towards the nociceptive thermal receptors. The center of pressure displacements were analysed to examine how both cutaneous stimulations affected the regulation of quiet standing. Subjects were tested with and without vision and when ankle proprioception (only without vision) was perturbed using the co-vibration technique (Hayashi et al. , 1988; Pyykko et al. , 1990). This was done in order to reveal if warmth or painful sensations can alter the multisensory integration underlying the postural control system. It was expected that only the noxious stimulus would increase the postural oscillations and that this effect would be exacerbated by the withdrawal of vision and the co-vibration of the ankle tendons.

METHODS

Experiment 1

Subjects and apparatus

Ten healthy male subjects participated in the study (age: 24.5 ± 2.7 years; height: 178 ± 7 cm, body weight: 81.1 ± 8.5 kg). The subjects were recruited at Laval University and had no evidence of gait, postural or musculo-skeletal abnormalities. Informed consent was obtained from each subject according to university protocols. Postural stability was evaluated with the help of a force platform (AMTI OR6-5-1 model). Force and moment components were amplified (Ectron 563H) prior to be sampled at 200 Hz (12 bit A/D conversion). Data were digitally filtered with a fourth-order Butterworth filter (7 Hz low pass cut-off frequency with dual-pass to remove phase shift). The antero-posterior (A-P) and medio-lateral (M-L) coordinates of the CP were derived from filtered data. The tendon vibration technique was used to alter the proprioceptive information of the ankle muscles. Four vibrators were fixed with rubber bands to the subject’s ankles on the tendons of both soleus and tibialis anterior muscles. When applied bilaterally to both antagonistic ankle muscles, the vibration gives instant rise to a background noise and deprives subjects from relevant proprioceptive messages generated by body oscillations (Pyykko et al. , 1990; Teasdale & Simoneau, 2001). The vibrators (n=4) consisted of a plastic cylinder (10 cm long, 3 cm diameter) containing a DC motor. The vibratory stimulation was induced by the DC motor rotating an unbalanced small mass at 80 Hz; it produced a mechanical oscillation of 3 mm amplitude.

Postural stability protocol

We evaluated postural sway for six different conditions. Standing eyes open, eyes closed and eyes closed with co-vibration were performed with and without bilateral non-noxious heat stimulation of the lower limbs. Subjects were instructed to stand upright as still as possible using a standardized stance on the force platform: they had their feet 10 cm apart, centered on the force platform. They stood barefoot on the force platform with their arms comfortably lying on each side and were instructed to fixate a point located 4 meters in front of them. Each trial lasted 30 seconds. A series of four trials was performed for each control condition (without heat stimulation): eyes open, eyes closed and eyes closed with co-vibration. The order of presentation of conditions was randomized across subjects. Three randomly presented series of four trials also were performed with the heat stimulation. Half of the subjects started with the control no-heat stimulation conditions and the other half started with the heat stimulation conditions. Rest periods of 20 seconds were provided between each trial; five-minute periods were provided between conditions. Subjects were told they could interrupt the experimental session at any time if they felt the need.

Heat stimulation protocol

The technique for inducing the non-noxious heat stimulation was inspired from the work of Craig and colleagues (Craig & Bushnell, 1994; Craig et al. , 1996). Heat stimulation was induced bilaterally on the calves of the subject with two 15 by 14.5 cm thermal grills (Fig. 1). Each thermal grill consisted of 10 parallel copper bars (10mm diameter) spaced by 0.5 cm. The bars were connected to each other with plastic tubing. Both thermal grills were fixed on the calves of the subjects with Velcro bands. Non-noxious heat stimuli were produced by the conduction of hot water circulating through the copper bars. Temperature of the grills was maintained at 40.0ºC (± 0.3ºC) and induced a perception of gentle warmth. The temperature was monitored with a thermal probe sensor (Cole-Parmer thermometer, 08402-00, USA). Immediately after the fixation of the thermal grills, subjects were tested for postural stability. Subjects had the thermal grills fixated to their calves approximately 20 s before the beginning of a bloc of heat stimulation trials. Completion of a bloc of four postural trials (with the thermal stimulus) took less than four minutes. For control conditions (no thermal stimulus), the thermal grills were fixed on the calves without hot water.

Non nociceptive receptors, both Aδ and C warm receptors, that are responsible for the gentle sensation of warmth were presumably stimulated by the non-noxious heat stimuli (40 ± 0.3°C) (Plaghki et al., 1998).

Figure 1 : Apparatus.

Thermal grills applied over the calves of a subject standing on the force platform. The vibrators fixed on the subject’s ankle tendons are not illustrated.

Pain intensity assessment

A visual analogue scale (VAS) of 10 cm was used to rate the sensory intensity to noxious heat stimulation. The scale had two descriptors on each end: at the left end ‘no pain’ and at the right end ‘worst imaginable pain’. Pain was defined as any uncomfortable sensation (particularly burning and prickling) even if the stimulus was tolerable. Subjects rated their perception of pain intensity by drawing a line on the visual analogue scale at the beginning and at the end of each trial. Pain for a given trial was defined as the mean visual analogue score of the beginning and the end of that trial. Visual analogue scales have been validated for experimental pain (Price et al. , 1983).

Data reduction

Range and standard deviation of the CP trajectory and mean CP velocity along the A-P and M-L axes were calculated. The range of the CP displacement indicates the average minimum and maximum excursion of the CP within the base of support. The calculation of the standard deviation of the signal provides a measure of amplitude variability of the CP around the mean position. The mean CP velocity represents the total distance covered by the CP (total sway path) divided by the duration of the sampled period and constitutes a good index of the amount of activity required to maintain stability.

Statistical analysis

Dependent variables were all submitted to a 2-way ANOVA (2 Heat x 3 Sensory conditions) with repeated measures on both factors. Post hoc analyses were performed with pre-planned comparisons. The level of significance was set at p < 0.05.

Experiment 2

Subjects and apparatus

Ten healthy male subjects participated in the study (age: 25.7 ± 2.7 years; height: 177 ± 8 cm, body weight: 75.9 ± 10.2 kg). The subjects were recruited at Laval University and had no evidence of gait, postural or musculo-skeletal abnormalities. Informed consent was obtained from each subject according to university protocols. The apparatus was the same as in the first experiment.

Postural stability protocol

Postural sway was evaluated for six different conditions: standing eyes open, eyes closed and eyes closed with co-vibration were performed with and without bilateral pain stimulation of the lower limbs. Each trial lasted 30 seconds. A series of eight trials was performed for each control condition (without heat stimulation): eyes open, eyes closed and eyes closed with co-vibration. The order of presentation of conditions was randomized across subjects. Three randomly presented series of eight trials also were performed with the pain stimulation. Half of the subjects started with the control no-pain stimulation conditions and the other half started with the pain stimulation conditions. Rest periods of 20 seconds were provided between each trial; five-minute periods were provided between conditions. For the pain stimulation conditions, an additional five-minute rest period was provided after the fourth trial. During this period, the pain stimulus was removed. Hence, the painful conditions were performed in two blocs of four trials (total of eight trials).

Pain stimulation protocol

The painful stimulation was delivered with the grill described in experiment 1. Temperature of the grills was maintained at 45.1ºC (± 0.3ºC) with running hot water and the temperature was evaluated with a Cole-Parmer thermometer (08402-00, USA). This thermal stimulation induced a perception of heat pain. Subjects had the thermal grills fixated to their calves approximately 20 s before the beginning of a bloc of heat stimulation trials. Completion of a bloc of four postural trials (with the thermal stimulus) took less than four minutes. For the control conditions (no thermal stimulus), the thermal grills were fixed on the calves without hot water.

Two main groups of receptors, namely the Aδ mechano-thermal receptors and the C mechano-heat nociceptors were presumably stimulated by the pain stimulus delivered in the present experiment (45.1 ± 0.3ºC). The Aδ mechano-thermal receptors respond to noxious heating and are characterized by a threshold ranging from 37 to 47°C (Dubner et al. , 1977). The C mechano-heat nociceptors have thermal threshold ranging from 38 to 49°C with mean values around 44°C (Beitel & Dubner, 1976).

Pain intensity assessment

As for experiment 1, a VAS was used to evaluate the perception of pain induced by the thermal stimulus.

Data reduction

Range and standard deviation of the CP trajectory and mean CP velocity along the A-P and M-L axes were calculated similarly to experiment 1.

Statistical analysis

Dependent variables were all submitted to a 2-way ANOVA (2 Pain x 3 Sensory conditions) with repeated measures on both factors. If a main effect of Sensory conditions or a Pain X Sensory interaction was found, post hoc analyses were performed with pre-planned comparisons. The level of significance was set at p < 0.05.

RESULTS

Experiment 1: The effects of Aδ and C warm receptors on the control of posture

Perceived pain intensity

For the non-noxious heat stimulation, no subject reported any pain (VAS = 0). All subjects described the non-noxious heat stimulation as a gentle sensation of warmth.

Postural analyses

Table 1 presents the mean and standard deviation for all computed variables for the control and non-noxious heat stimulation conditions. The F-values for the ANOVAs also are presented. For all dependent variables, the ANOVAs revealed main effects of the Sensory conditions (ps < 0.01) but no main effect of the non-noxious Heat stimulation and no interaction (ps > 0.05). Withdrawal of vision increased the range and mean velocity of the CP oscillations along both axes (ps < 0.05). Co-vibrating the ankle tendon without vision yielded greater CP standard deviation, range and mean velocity along both axes compared to the no vision condition (ps < 0.05).

Experiment 2: The effects of Aδ and C nociceptors on the control of posture

Perceived pain intensity

The visual analogue scores of heat pain were not different for all experimental pain conditions (p > 0.05). The mean visual analogue score was 46 mm (SD = 17), 46 (SD = 20) and 45 (SD = 19) for the vision, no vision and no vision co-vibration conditions, respectively. All subjects described the heat stimuli as a distinct burning, prickling sensation. All subjects reported no pain for the control conditions.

Postural analyses

Table 2 presents the mean and standard deviation for all computed variables. The F-values for the ANOVAs also are presented. A preliminary comparison of the data for the initial vs subsequent trials with pain revealed that the effects of the painful stimulation were present on the first trial with the painful stimulation. For all dependent variables, there was no sign of habituation. To illustrate this absence of habituation, Fig. 2 presents CP oscillations, for one subject, for all trials without vision with and without a noxious stimulation. Clearly, the effect of the noxious stimulation is observed across all trials and there is no trend towards an increased or a decreased of the range of the CP oscillations when the pain stimulation is applied.

The range of the CP oscillations increased for the Pain conditions for both the A-P and M-L axes (ps < 0.05). The ANOVAs also showed a main effect of Sensory conditions (ps < 0.01) : for both axes, the range of the CP was greater for the no vision compared to the vision condition and also greater for the no vision co-vibration compared to the no vision condition (ps < 0.05). No interaction of Pain by Sensory conditions was observed (ps > 0.05).

For the standard deviation of the CP, the ANOVAs showed an increased CP standard deviation for the Pain conditions for both axes (ps < 0.05). For both axes, the ANOVAs showed a main effect of Sensory conditions (ps < 0.01). The standard deviation of the CP was greater for the no vision compared to the vision condition and also greater for the no vision co-vibration compared to the no vision condition (ps < 0.05). No interaction of Pain by Sensory conditions was observed (ps > 0.05).

Tableau 1 : Mean results of the CP parameters of experiment 1.

Parameters

Vision

No Vision

No Vision co-Vibration

F-Values

No Heat

Heat

No Heat

Heat

No Heat

Heat

Heat

Sensory

Interaction

Mean Velocity A-P (mm/s)

4.7 (0.9)

5.5 (1.5)

7.5 (2.0)

8.1 (1.6)

13.1 (4.8)

13.3 (4.3)

4.35

28.60 ‡

0.18

Mean Velocity M-L (mm/s)

2.4 (0.8)

2.7 (0.9)

3.3 (1.6)

3.2 (1.2)

6.6 (3.6)

6.8 (3.4)

1.74

20.31 ‡

1.19

Range A-P (mm)

14.5 (4.5)

14.4 (3.6)

18.5 (6.3)

18.4 (5.1)

27.6 (10.9)

27.3 (7.7)

0.04

18.69 ‡

0.00

Range M-L (mm)

7.2 (3.2)

8.2 (4.0)

9.2 (4.7)

9.1 (4.9)

13.2 (6.2)

13.2 (5.2)

0.79

21.17 ‡

0.89

Standard Deviation A-P (mm)

3.3 (1.2)

3.1 (0.9)

3.6 (1.2)

3.6 (1.1)

4.8 (1.7)

5.0 (1.4)

0.03

10.30 †

1.23

Standard Deviation M-L (mm)

1.5 (0.7)

1.7 (1.0)

1.8 (0.9)

1.7 (1.0)

2.3 (1.0)

2.4 (1.0)

1.19

14.63 ‡

0.83

Note: *, † and ‡ indicate a significant difference at p<0.05, p<0.01 and p<0.001, respectively.

Mean (standard deviation) and ANOVA results of the center of foot pressure parameters for the various sensory conditions with and without a nonnoxious heat stimulation.

Tableau 2 : Mean results of the CP parameters of experiment 2.

Parameters

Vision

No Vision

No Vision co-Vibration

F-Values

No Pain

Pain

No Pain

Pain

No Pain

Pain

Pain

Sensory

Interaction

Mean Velocity A-P (mm/s)

5.7 (1.0)

6.9 (2.0)

8.1 (1.7)

9.5 (2.6)

15.5 (5.0)

20.0 (5.5)

58.84 ‡

56.34 ‡

5.61 *

Mean Velocity M-L (mm/s)

4.0 (1.2)

4.9 (1.9)

4.6 (2.3)

5.8 (2.6)

10.4 (5.5)

11.0 (5.3)

10.10 *

23.21 ‡

0.43

Range A-P (mm)

16.4 (5.5)

19.8 (6.0)

19.7 (4.6)

24.9 (7.3)

30.6 (11.5)

37.7 (12.3)

13.96 †

33.64 ‡

2.08

Range M-L (mm)

11.3 (3.9)

13.4 (5.4)

12.7 (5.6)

16.3 (7.3)

21.4 (10.3)

21.8 (10.1)

16.50 †

18.95 ‡

2.19

Standard Deviation A-P (mm)

3.5 (1.3)

4.0 (1.1)

3.9 (1.1)

4.6 (1.4)

5.8 (2.3)

6.7 (2.4)

7.01 *

19.62 ‡

0.66

Standard Deviation M-L (mm)

2.2 (0.8)

2.6 (1.0)

2.5 (1.1)

3.1 (1.3)

3.9 (1.8)

3.9 (1.8)

15.23 †

18.33 ‡

2.66

Note: *, † and ‡ indicate a significant difference at p<0.05, p<0.01 and p<0.001, respectively.

Mean (standard deviation) and ANOVA results of the center of foot pressure parameters for the various sensory conditions with and without cutaneous pain.

Figure 2 : Illustration of the CP displacements for all no vision trials.

The CP oscillations are shown for a representative subject. Upper CP traces illustrate Pain trials (lower CP traces: no Pain trials). Vertical and horizontal directions represent the A-P and M-L displacements of the CP, respectively. No sign of habituation was observed across all trials for both conditions.

Fig. 3 presents the mean CP velocity along the A-P and M-L axes. For the A-P axis, the ANOVA revealed an interaction of Pain by Sensory conditions (p < 0.05) and main effects of Pain (p < 0.001) and Sensory conditions (p < 0.001). Post-hoc decomposition of the interaction showed that the linear increase of the CP mean velocity from vision to no vision and no vision co-vibration was greater for the Pain conditions than for the control no-pain conditions (planned comparison, p < 0.05). This result supports our initial hypothesis that the effects of pain on the control of posture would be exacerbated by a decrease in the sensory information available. For the M-L axis, the ANOVA showed an increased mean CP velocity for the Pain conditions (p < 0.05) and a main effect of Sensory conditions (p < 0.001), but no interaction (p > 0.05). The mean CP velocity along the M-L axis increased for the no vision co-vibration condition compared to the vision and no vision conditions (ps < 0.05).

Overall, the pain stimulation of the lower limbs yielded increased range, standard deviation and mean velocity of the postural oscillations along both axes.

Figure 3 : Effects of Aδ and C nociceptors on the control of posture.

Left panel: Mean CP velocity for the pain and no pain conditions under all sensory conditions for the A-P axis. Right panel: Mean CP velocity for the pain and no pain conditions under all sensory conditions for the M-L axis. Vertical bars denote the 0.95 confidence intervals.

DISCUSSION

The present study examined the postural stability of young adults in the presence of non-noxious and noxious heat stimulations under various sensory conditions. Both with and without the heat stimulations, the CP data observed for the different sensory conditions were consistent with previous findings (Brandt et al. , 1986; Hayashi et al. , 1988; Hay et al. , 1996). More specifically, withdrawal of visual information and co-vibrating ankle tendons both yielded large increases in body oscillations.

Effects of Aδ and C warm receptors

Results of experiment 1 showed that the stimulation of warm receptors did not yield a pain sensation and did not affect the control of posture. There are recent neurophysiological evidences showing that the stimulation of warm receptors has only mild effects on spinal interneurons. For example, Plaghki et al. (1998) reported that, compared to noxious stimuli, non-noxious radiant heat stimuli yielded a moderate facilitation of the withdrawal flexor reflex (15-20% compared to 150-200% for the noxious stimuli). Moreover, Schomburg (1990), in a literature review, has reported that thermal stimulation below the nociceptive threshold failed to elicit synaptic effects in α-motoneurons or facilitatory effects onto reflex pathways from group Ib or II muscle afferents or mechanoreceptive cutaneous afferents. In the present experiment, the small effects presumably induced by the non-noxious heat stimulation at the segmental level were not sufficient to deteriorate the maintenance and control of the upright stance.

Effects of Aδ and C nociceptors

The aim of experiment 2 was to document how a noxious heat stimulation inducing a perception of pain would alter the regulation of postural stability in normal quiet standing. In the present experiment, despite the presence of a pain sensation, subjects maintained an erect posture without the presence of any withdrawal movements. The overall effect of the noxious stimulation clearly stresses its negative impact on the postural control system. It appears that the action/detection properties of the postural control system necessary to regulate quiet standing were affected by stimulation of thermal receptors from the skin. The present results are at odd with recent findings showing that the regulation of the upright stance was not affected by pain reduction in patients with knee osteoarthritis (Hassan et al. , 2002). Hassan et al. (2002) have argued that their measure of postural stability might have been insensitive to pain reduction. The effect of pain reduction also could have been attenuated by the decrease of the knee proprioception induced by injection of the anaesthetic substance. In the present experiment, young healthy individuals were tested for postural stability with and without noxious heat stimulation inducing a perception of pain. Thus, any confounding effect of pain with a subjacent pathology is a priori excluded.

Results observed for the CP fluctuations along the M-L direction suggest that pain stimulation clearly modified the upright standing behaviors. The increased variability of the CP amplitude (around the mean position of the CP during the trial), the increased range of the postural oscillations and the increased mean CP velocity all suggest a less stable and more variable behavior with than without pain stimulation. Maki et al. (1994) proposed that an increased postural oscillations along the M-L direction could stress the risk of falling since the M-L postural indicators are good predictors of postural instability. For the A-P direction, subjects also exhibited more and faster postural oscillations, greater CP variability and range with than without pain stimulation of the lower limbs. These effects could be associated with the control of the postural oscillations required to compensate the motor and/or sensory changes induced by the stimulation of Aδ mechano-thermal and C mechano-heat receptors (nociceptive thermoreceptors).

There are several possible interpretations to explain the CP changes observed with the pain stimulation. One possibility resides in the changes occurring at the spinal level induced by nociceptive afferents (e.g. reflex inhibition of the motoneuron pools, presynaptic excitability changes of Ia fibers or increased sensitivity of the muscle spindles) (Rossi & Decchi, 1997; Matre et al. , 1998; Rossi et al. , 1999b; Capra & Ro, 2000). A second possibility could be related to changes in the excitability of the motor cortex (Le Pera et al. , 2001) or in the sensory integration processes (Gandevia & Phegan, 1999). The increased loss of stability associated with the increased pain stimulation could have been the result of an altered central motor command to the periphery or a reduced accuracy in the integration of the sensory information which ultimately led to a biased estimation of the whole body position in space. For balance control, the precision of the compensatory ankle torques to maintain the vertical alignment of the body largely depends upon the incoming sensory information. Both of these possibilities could alter force production or sensory detection capabilities yielding greater and faster displacements of the CP. The present results, however, do not allow to extrapolate on the exact locus of the observed effects of the noxious pain stimulation.

Vibration stimuli can reduce the effects of a painful stimulation (Kakigi & Shibasaki, 1992). This presumably occurs through inhibition of small diameter afferents in the dorsal horn of the spinal cord by large myelinated fibers (Melzack & Wall, 1965). In the present experiment, the tendon co-vibration did not modify the perception of the painful stimulation. This absence of pain relief was certainly related to the short duration of the applied co-vibration (Lundeberg et al. , 1984). Also, it could be that the frequency of the vibration was below that necessary to alleviate pain (Pantaleo et al. , 1986). The ankle tendon co-vibration technique accentuated the deteriorating effects of the painful stimulation on the mean velocity of the CP (A-P axis). This could suggest that the high threshold cutaneous afferents have a significant non linear negative impact on the postural control system when proprioceptive information is masked or falsified. Schomburg (1990) has argued that the convergence of small and large diameter afferents (stimulated respectively by the pain stimulation and the tendon co-vibration technique in our experiment) occurs at the spinal level of the sensorimotor system. This convergence of polymodal sensory information could produce the observed deteriorating effects of the combined nociceptive and Ia afferents on the motor system. An increase in the amplitude of the nociceptive leg flexion reflex by the application of tendon vibration has been observed previously by Guieu & Serratrice (1992).

Overall, the effects of the painful stimulation were not exacerbated when vision was withdrawn. This suggests that the visual information could not compensate for the deteriorating effects of the pain stimulation on the postural control system. This observation provides support to the suggestion that the effects of cutaneous pain alter mainly the sensorimotor systems at the peripheral level rather than through higher and more cognitive processes. It is possible, however, that the contribution of vision to reduce painful stimulation would be different at higher perceived pain intensities. Also, our pain stimulation was continuous throughout the 30-s trial; the effect of a short duration painful event on postural control remains to be determined.

The results presented in this study show that a painful sensation alters the control of an upright stance presumably via sensorimotor processes. Furthermore, a non-noxious stimulation of the small diameter afferents is not sufficient to alter the control of posture. To our knowledge no association has been made between pain sensation and the deterioration of the postural control mechanisms. Results presented in this study could certainly lead to the hypothesis that subjects suffering from lower limb pain present alterations of the postural control mechanisms; especially populations already at risk of falling (for example, frail elderly) or populations suffering from concomitant lower limb pain and sensory deficits (for example, diabetic polyneuropathy).

Acknowledgments

This study was supported in part by the NSERC-Canada, Égide-France and CIHR-FCQ funds. Special thanks to Gilles Bouchard and Marcel Kaszap for technical and programming expertise.

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