CHAPITRE V EFFECTS OF INTENSITY AND LOCUS OF PAINFUL STIMULATION ON POSTURAL STABILITY

(Soumis à Pain)

Philippe Corbeil1, Jean-Sébastien Blouin1 & Normand Teasdale1

1 Division de Kinésiologie, Faculté de médecine, Université Laval, Québec, Canada.

Correspondence should be addressed to

Normand Teasdale

Division de kinésiologie, Université Laval, Cité universitaire, Québec, Canada G1K 7P4

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

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

ACKNOWLEDGMENTS

This study was supported by a grant from NSERC-Canada. PC is supported by a Doctoral scholarship from NSERC-Canada and ÉGIDE-France. JSB is supported by a Doctoral scholarship from CIHR-FCQ.

RÉSUMÉ

Cette étude documente les effets d’une stimulation douloureuse, d’une durée de dix secondes, de faible, de moyenne et de forte intensité sur la stabilité posturale. De plus, une stimulation douloureuse électrique de moyenne intensité a été appliquée sur les mains afin d’étudier les effets de la douleur sur des parties du corps n’étant pas impliquées dans la régulation de l’équilibre en station debout. L’augmentation de l’intensité du stimulus douloureux entraîne une augmentation accrue des oscillations posturales alors qu’une stimulation électrique moyenne appliquée sur la main, n’entraîne aucune altération des caractéristiques globales des mouvements posturaux. Ces résultats suggèrent qu’une stimulation électrique douloureuse altère principalement les mécanismes de contrôle à travers des processus où l’apport de la cognition est restreint. De plus, un seuil lié à l’intensité d’une stimulation douloureuse semble exister, au-delà duquel des mécanismes de contrôle compensatoires ne peuvent plus agir efficacement pour contrer les effets négatifs des nocicepteurs.

ABSTRACT

Stimulation of small diameter afferents can influence motor behavior. Little is known about how a prolonged painful stimulation of these small afferents may affect essential motor behavior such as the maintenance of an erect stance. The present study documents the effects of 10-second weak, moderate and extreme painful stimulations applied to the dorsum of the feet on the postural stability. Also, the moderate painful stimulation was applied to the metacarpal heads to determine if a painful stimulation to a limb not involved in the maintenance of the erect stance affects the postural control mechanisms. Increasing the intensity of the painful stimulation applied to the feet yielded larger postural oscillations whereas stimulation to the hands did not affect the control of posture. This suggests that the painful stimulation mainly affected the postural control mechanisms via reflex circuits rather than via cognitive resources related to the perception of pain.

Keywords: Experimental pain, Postural control, Center of foot pressure, Pain locus, Pain intensity

1. Introduction

The maintenance of an erect stance 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. 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 integrity of both the various sensory inputs (visual, vestibular and proprioceptive afferents) and 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). In addition, it is now well acknowledged that postural control requires cognitive resources (Teasdale and Simoneau, 2001; Yardley and Redfern, 2001; Woollacott and Shumway-Cook, 2002) and that modification in the allocation of the attentional resources alters the control of posture.

Large diameter myelinated afferents provide the primary source of lower limb proprioceptive information (e.g. pressure and position sense receptors) crucial for maintaining an erect stance. Small diameter afferents, however, can also influence motor behaviors. Noxious stimuli (chemical, thermal or mechanical) activate nociceptors which are the peripheral endings of small diameter primary sensory neurons. Sherrington (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). Also, the stimulation of nociceptors influences the excitability of the segmental motor nuclei (gamma and alpha motoneurone pools) (Matre et al., 1998; Rossi et al., 1999a; Capra and Ro, 2000), highlighting the possible role of the high threshold small diameter afferents in the control of movement. Furthermore, Rossi et al. (Rossi and Decchi, 1997) have suggested that steady variations in interneuronal transmission, induced by tonic pain activity, could result in alteration of motor strategies.

After entering the spinal cord, the information generated by noxious stimuli is relayed to the thalamus and subsequently to the parietal and cingular cortices where the perception of the intensity and unpleasantness of the pain arises. Attention has been theorized as the primary mechanism by which nociception accesses awareness and disrupts current activity (Crombez et al., 1998). It has been showed that, compared to a control population, subjects suffering from lower back pain have slower hand reaction times, suggesting that the pain sensation reduces the available cognitive resources (Taimela et al., 1993; Luoto et al., 1998). In addition, Miron et al. (Miron et al., 1989) showed that, when subjects shift their attention away from the pain sensation, they can diminish the intensity of their pain perception.

Despite these evidences showing the effects of small diameter afferents on the motor system as well as the possible interference of the pain perception with the available cognitive resources, the mechanisms underlying the upright standing behavior with painful stimuli has not been well documented. Two important questions still need to be answered: 1. Is there a relationship between the intensity of a painful sensation (weak, moderate or extreme) and the standing behavior? 2. Are postural control mechanisms mainly affected by reflex circuits involving lower limb nociceptors or by cognitive processes mediated by the perception of pain?

2. Methods

2.1 Subjects and apparatus

Ten healthy male subjects participated in the study (age: 28 ± 6 years; height: 175 ± 4 cm, body weight: 80 ± 16 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 the local research ethics committee. 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 1000 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.

2.2 Experimental electrical stimulation

The technique for inducing a painful stimulation was inspired from the work of Arendt-Nielsen et al. (Arendt-Nielsen et al., 2000). The stimulus duration was 10 s. A constant-voltage pulse train of 1-ms pulses was delivered at 10 Hz (ISI = 100ms) via bipolar surface Ag-AgCl electrodes (Meditrace, Canada). Painful stimulations were applied to the dorsum of the first tarso-metatarsal joint of both feet or to the dorsum of the first and second metacarpal heads of both hands. For the painful stimulations applied to the feet, we adopted three levels of intensity depending of the perception of each subject: “weak”, “moderate” and “extreme” pain. Pain was defined as any uncomfortable sensation (particularly prickling) even if the stimulus was tolerable. Weak, moderate and extreme painful intensities were set when subjects’ subjective pain score was equal to “3”, “5” and “7” using a visual analog scale (VAS), respectively. For each trial, subjects rated their perception of pain intensity by drawing a line on the VAS, 10 cm long, at the end of each trial. The scale had a descriptor on each end: at the left end “no pain” and at the right end “worst imaginable pain”. VAS has been validated for experimental pain (Price et al., 1983). For the painful stimulation applied to the hand, we adopted one level of intensity, “moderate” (or 5 on the VAS), also depending on subjective pain perception.

2.3 Postural stability protocol

Subjects were instructed to stand 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. We evaluated the postural stability for the four different painful stimulation conditions: three different intensities (“weak”, “moderate” and “extreme”) of the painful stimulation applied to both feet and one intensity (“moderate”) of the painful stimulation applied to both hands. A series of ten trials was performed for each condition. Each trial lasted 20 seconds and was divided in two intervals: no stimulation for the first 10 s (Control interval) and painful stimulation applied to both feet or hands for the subsequent 10 s (Pain interval). The order of presentation of the conditions was randomized across subjects. Subjects were unaware of the stimulation intensity prior to each trial. 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.

2.4 Data reduction

Global posturographic parameters, e.g. mean CP position, range of the CP trajectory and mean CP velocity, along the A-P and M-L axes were calculated. Under quasi static conditions, the mean CP position represents approximately the center-of-mass location and thereby provides information regarding the standing posture. The range of the CP displacement indicates the average minimum and maximum excursion of the CP within the base of support. 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 (Maki et al., 1990).

In addition, structural posturographic parameters were computed using a sway density plot approach (Baratto et al., 2002). The sway density plot is computed by counting the number of consecutive samples during which the postural oscillations remain inside a 2.5 mm radius (see Fig. 1a). The sway density curve was digitally filtered with a fourth-order Butterworth filter (2.5 Hz low pass cut-off frequency with dual-pass to remove phase shift) in order to perform a better peak extraction of the two structural parameters. The peaks of the sway density curve correspond to time instants in which the CP is relatively stable (e.g. points I to IV in Fig. 1a) and valleys correspond to time instants in which the CP rapidly shifts from one stable value to another. The mean value of all peaks and the mean of all distances between one peak and the successive peak have been extracted from the sway density curve. This analysis was used to document the possible physiological processes underlying the control of an upright stance when a painful stimulation is applied. These parameters have been suggested to reflect the capacity of the postural control system to integrate the sensory information and anticipate physiological internal delays in order to keep the vertical alignment of the whole body (Baratto et al., 2002). It has been shown that the discriminative power of these two sway density parameters, together with the mean CP velocity parameter, was greater than that of other global and structural parameters to distinguish among sensory and pathological conditions in the general framework of postural stabilization (Baratto et al., 2002). The software package used in the present experiment is available at the following website: http://www.laboratorium.dist.unige.it/~recri/.

2.5 Statistical analysis

Within-subject mean of the parameters extracted from the CP oscillations for the one to ten seconds interval (Control interval) and for the 11 to 20 seconds interval (Pain interval) were performed for each painful stimulation intensity or localization. The one-second period prior to both intervals has been removed to avoid the contamination of the computed parameters by a possible startle effect related to the initiation of the trial or to the apparition of the painful stimulation. In a preliminary analysis, we compared the mean value of the parameters computed from the CP displacements during the control interval for all experimental conditions using one-way repeated measured ANOVAs. These analyses revealed that no change was observed between conditions during the Control interval for each parameter (ps > 0.05). Consequently, we averaged the Control interval for all parameters across all painful stimulation intensities or localizations and considered the new mean value of each parameter as the mean of the Control level used in the subsequent statistical analyses. This was done in order to clarify the presentation of the results.

Dependent variables were all submitted to a one-way repeated measures ANOVA (five levels : Control, Weak, Moderate and Extreme intensity stimulation applied to the feet and Moderate intensity stimulation applied to the hands ). When a significant main effect was observed, three post hoc analyses were performed using different pre-planned comparisons to answer appropriately our theoretical questions. To determine if increasing the intensity of the painful stimulation applied to the feet deteriorated gradually the postural control behavior, we performed a linear contrast analysis on the Control (no stimulation), weak, moderate and extreme painful stimulations applied to the feet. Also, we performed a pre-planned comparison to determine if the weak painful intensity applied to the feet affected the control of an upright stance compared to the Control condition. Finally, to document and highlight the possible role of the cognitive perception of pain on the postural control system, pre-planned comparisons were performed between the moderate intensities of the painful stimulation applied to the feet and hands; both conditions yielded a subjective pain rating of five on the VAS. The level of significance was set at p < 0.05.

Figure 1 : Illustration of the center of foot pressure (CP) data for a representative trial of a subject.

(a) Thick traces represent the time intervals from which CP parameters were computed (control: 1 to 10 s; extreme painful stimulation: 11 to 20 s). Medio-lateral (M-L) and antero-posterior (A-P) CP displacements are presented. The vertical force of the ground reaction forces clearly shows that no startle effect was present when the extreme painful stimulation applied to the feet started (at the tenth second, vertical dashed lines). The sway density plot indicates the number of consecutive samples falling inside a 2.5 mm radius. All peaks of the plot are identified to compute the structural parameters: mean amplitude of the peaks and mean distance between two consecutive peaks. Peaks represent instants of the standing behavior where the relative stability is maximal. Two arbitrary consecutive peaks were selected for both the control (points I and II) and extreme painful stimulation (points III and IV) conditions to illustrate the mean distance between consecutive peaks of the sway density curve. (b) For both conditions, A-P trajectory of the CP motion was plotted in function of the M-L trajectory of the CP motion. The CP traces cover a much larger area when the extreme electrical stimulation was applied to the feet of the subject. The four instants, previously shown on the sway density curve of panel a, are indicated by arrows. More specifically, circles of 2.5 mm radius are drawn centered around these instants of relative maximal stability. The direct distance between the centre of circles represents the distance between two consecutive peaks (CP transition from one stable region to another). This measure reflects the capacity of the postural control system to integrate the sensory information and anticipate physiological internal delays in order to keep the vertical alignment of the whole body. (c) Density histograms of the CP dispersion without and with pain. Each column represents the percentage of time the subject spent in that area of the force platform. All data are illustrated for the same trial.

3. Results

Fig. 1 illustrates center of foot pressure (CP) data for a typical trial. The first 10 s represents data without pain stimulation while the last 10 s are for an extreme painful stimulation applied to the feet. Fig. 1a illustrates, for both conditions, the CP antero-posterior (A-P) and medio-lateral (M-L) displacements, the vertical force and the sway density curve. Fig. 1b and c show, for the same trial, CP oscilations (see caption for a description of the four identified circles) and density histograms of the CP dispersion without and with pain. Each column on Fig. 1c represents the percentage of time the subject spent in that area of the force platform. These figures highlight that, compared to the control no-pain condition, the extreme painful stimulation applied to the feet yielded an increased range (also illustrate for each axis on Fig. 1a) and a much greater dispersion of the CP oscillations. Also, Fig. 1a shows that, the introduction of the painful stimulation (vertical dashed line), did not yield a startle effect (CP and Vertical force traces).

All subjects described the electrical stimuli applied to the feet and hands as a distinct prickling sensation. On average, the electrical intensities delivered were 8.1V± 2.9 (mean ± standard deviation), 9.8V± 2.7, 11.2V± 2.7 and 11.5V± 3.6 for the weak, moderate and extreme levels applied to the feet and the moderate level applied to the hands, respectively. For the mean visual analogue scores of the painful stimuli, the ANOVA showed a main effect of Intensity (F3,27 = 29.6, p < 0.001). A decomposition of the main effect showed a gradual linear increase of the pain perception with an increase in the intensity of the electrical stimuli applied to the feet (F1,9 = 189.3, p < 0.001). Furthermore, no difference was observed between the perceived pain from the moderate electrical stimuli applied to the feet and hands (F1,9 = 0.15, p > 0.05). On average, the mean visual analogue scores were 20 ± 6, 50 ± 19, 72 ± 15 mm and 47 ± 17 mm for the weak, moderate and extreme level of intensity applied to the feet and the moderate level of intensity applied to the hands, respectively.

Means, standard deviations and F-values for all dependent variables computed from CP oscillations are presented in Table 1. For the mean position of the CP along both axes, the ANOVAs showed no main effect of Pain (ps > 0.05). Hence, subjects did not modify the mean position of their standing posture when the painful stimuli were applied to the feet or hands. For all other parameters, the ANOVAs showed main effects of Pain (ps < 0.001).

Tableau 1 : Center of foot pressure parameters in relation to the intensity of the painful stimulation.

       

Hands

     

Feet

     

ANOVA results

Parameters

 

Control

 

Moderate

 

Weak

 

Moderate

 

Extreme

 

Pain

Global

                       

Mean Position M-L (mm)

 

-1 (10)

 

-2 (12)

 

-1 (10)

 

-1 (10)

 

-1 (11)

 

1.94

Mean Position A-P (mm)

 

19 (18)

 

19 (16)

 

20 (20)

 

21 (19)

 

22 (24)

 

0.93

Range M-L (mm)

 

8 (3)

 

8 (3)

 

9 (4)

 

10 (4)

 

11 (3)

 

6.70*

Range A-P (mm)

 

9 (2)

 

9 (2)

 

11 (2)

 

12 (4)

 

14 (6)

 

7.27*

Mean Velocity M-L (mm/s)

 

4.1 (1.4)

 

3.6 (1.6)

 

4.2 (1.8)

 

4.8 (2.0)

 

5.9 (2.3)

 

7.44*

Mean Velocity A-P (mm/s)

 

5.2 (0.7)

 

4.7 (0.7)

 

5.1 (0.9)

 

6.0 (1.6)

 

6.8 (1.7)

 

7.83*

Structural

                       

Mean Value of the peaks (s)

 

2.0 (0.6)

 

2.1 (0.6)

 

1.8 (0.5)

 

1.6 (0.5)

 

1.3 (0.6)

 

6.88*

Mean Distance (mm)

 

2.0 (0.6)

 

2.0 (0.5)

 

2.3 (0.7)

 

2.8 (1.1)

 

3.3 (1.0)

 

14.6*

Note: * indicates a significant difference at p<0.001.

Mean (standard deviation in brackets) and ANOVA results of the center of foot pressure parameters

3.1 Effects of the stimulation intensity applied to the feet

For both the range and mean velocity of the CP displacement along the M-L and A-P axes, the ANOVAs showed main effects of Pain (ps < 0.001). For both the M-L and A-P axes, the decomposition of the main effects of Pain revealed a linear increase with the increased intensity of the painful stimulus (range: F1,9 = 20.13, p < 0.01; F1,9 = 8.20, p < 0.05 and mean velocity: F1,9 = 6.99, p < 0.05; F1,9 = 11.80, p < 0.01 for the M-L and A-P axes, respectively). For illustration purposes, the CP mean velocity along both axes for the various painful stimulations and the control condition are presented in Fig. 2. Overall, the global posturographic parameters revealed that, as the intensity of the painful stimulation increased, the subjects showed larger excursions and greater mean velocity of the CP. Concerning structural parameters computed from the sway density curves, the ANOVAs for the mean amplitude of the peaks and the mean distance between one peak and another also revealed main effects of Pain (ps < 0.001). Decomposition of the main effects showed that the mean amplitude of the peaks decreased linearly while the mean distance increased linearly with an increasing pain intensity (F1,9 = 9.48, p < 0.05 and F1,9 = 23.06, p < 0.001, respectively). Hence, as the intensity of the painful stimulation increased, the analyses of the structural posturographic parameters showed that the distance between two stability regions increased and that subjects spent less time in a 2.5 mm radius of CP oscillations.

When compared to the Control condition, the weak intensity of the painful stimulation applied to the feet yielded a small increased range for the A-P axis only (F1,9 = 14.82, p < 0.01). For all other parameters, no difference between the weak intensity of the stimulus applied to the feet and the Control condition was observed (ps > 0.05), suggesting that the weak painful stimulation had a minimal effect on the postural behavior.

Figure 1 : Illustration of the center of foot pressure (CP) data for a representative trial of a subject.

Data for the Control, Weak, Moderate and Extreme intensity stimulation applied to the feet and Moderate intensity stimulation applied to the hands are presented for the M-L and A-P axes. Vertical bars denote the 0.95 confidence intervals.

3.2 Effects of the locus of the painful stimulation

To examine if the postural control mechanisms were mainly affected by reflex circuits involving lower limb nociceptors or by cognitive processes mediated by the perception of pain, comparisons of CP data for the moderate intensity of the painful stimulation applied to the feet and hands were made. For both the M-L and A-P axes, the decomposition of the main effects of Pain revealed a greater range and faster mean velocity of the CP when the painful stimulation was applied to the feet (Range: F1,9 = 10.24, p < 0.05; F1,9 = 15.34, p < 0.01; Mean velocity: F1,9 = 15.03, p < 0.01; F1,9 = 10.24, p < 0.05; for the M-L and A-P axes, respectively). Hence, larger excursions and faster postural oscillations were observed when the painful stimulation arose from their feet than when it originated from their hands (Fig. 2). Similar observations were made for the structural posturographic parameters: the mean peak of the sway density curves was smaller and the mean distance between two stability regions was more important when the moderate painful stimulation was applied to the feet than when it was applied to the hands. (F1,9 = 16.35, p < 0.01 and F1,9 = 11.17, p < 0.01, respectively). Finally, no statistical difference was observed for all postural parameters (Table 1) between the moderate painful stimulation applied to the hands and the Control condition (ps > 0.05).

4. Discussion

The present study examined the control mechanisms of the upright stance of young adults when facing a 10-second painful episode via electrical stimulation applied to their feet or hands. The analysis of the time structure of the CP signal can reveal information about the postural control mechanism because it is proportional to the ankle torque (Sinha and Maki, 1996; Pai and Patton, 1997; Morasso and Schieppati, 1999). This torque is the combination of the descending motor commands as well as the mechanical properties of the muscles acting around the ankle. It serves to maintain vertical the alignment of the multiple body segments and counteract the intrinsic noise in the system (such as respiration and cardiac activities). The global and structural posturographic parameters clearly revealed that, as the intensity of the painful stimulation applied to the feet increased, the postural stability was altered gradually. The global parameters, range and mean velocity of the CP, showed that the postural oscillations were characterized by larger excursions and greater mean velocity as the perception of pain increased. The mean CP velocity is a good indicator of the muscle activity needed to control an upright stance (Maki et al., 1990) and the present results suggest that subjects generated more activity to maintain their orthostatic equilibrium. Concerning the structural parameters, the amplitude of the peaks of the sway density curve which corresponds to time instants in which the ankle torque and the associated motor commands are relatively stable, decreased significantly with an increase of the painful stimulation intensity. Furthermore, the mean distance between one relative stable region to another one, increased significantly with the increase of the perceived pain. This CP transition from one stable region to another reflects the capacity of the postural control system to integrate the sensory information and anticipate physiological internal delays in order to keep the vertical alignment of the whole body (Baratto et al., 2002). Hence, as the painful stimulation applied to the feet increased, subjects spent less time in the stable regions and two consecutive local stability regions were separated by larger distances. It is possible that subjects spent less time in the stable regions because either the level of background sensorimotor noise enhanced with an increase painful stimulation or because subjects needed to increase their general postural oscillations in order to stimulate the various sensory receptors to receive appropriate information about the position of the whole body. The increased distance between one peak and another as the painful stimulation increased suggests that the overall action/detection capabilities of the postural control system were altered as the painful stimulation increased.

The painful stimulation could have altered the postural stability through several physiological mechanisms. It could have modified the ability to generate quick and precise motor commands via segmental reflexes (Schomburg, 1990) changing the excitability of the motor nuclei or via changes in motor cortex excitability (Le Pera et al., 2001). Recently, Weerakkody et al. (Weerakkody et al., 2003) reported that nociceptive inputs from the skin or sore muscles can affect the perception of a produced torque. In their experiment, subjects overestimated the level of torque generated by a limb affected by a pain stimulation. Pain heat stimulus to a remote site had no effect suggesting that the effect was not purely perceptual. On the other hand, Gandevia and Phegan (Gandevia and Phegan, 1999) have suggested that pain can induce a distortion of the body image. For postural stability, the precision of the compensatory ankle torques largely depends upon the incoming sensory information which is known also to be altered by nociceptive stimulations (Rossi and Decchi, 1997; Matre et al., 1998; Rossi et al., 1999b; Capra and Ro, 2000). In the present experiment, the increased loss of stability associated with the increased pain stimulation could have been the result of a reduced accuracy in the integration of the sensory information which ultimately led to a biased estimation of the whole body position in space.

The weak painful stimulation intensity, rated as 3 on the VAS by the subjects, affected minimally the postural stability. This suggests that pain effects appeared when a threshold was attained. The electrical stimulis delivered in the present experiment are likely to have stimulated three main groups of afferent fibers, namely the large-diameter Aβ fibers (low threshold mechanoreceptors) activated at detection-threshold levels of stimulation (Collins, 1960) and small-myelinated Aδ fibers activated at higher intensities and C-fibers at even higher intensities (Laitinen and Eriksson, 1985). The intensities used in the present experiment were higher than the pain threshold for all conditions. The pain threshold is at least two times superior to the detection threshold of an electrical stimulation (Sang et al., 2003). The continuum in fibers recruitment for increased electrical intensities suggests that the weak painful stimulation activated both the Aβ and Aδ fibers while for the moderate and extreme painful stimulations, the proportion of Aδ and C fibers activated gradually increased. Results of the present experiment clearly demonstrate that a weak pain intensity affected minimally the control of posture but that the moderate and extreme pain intensities gradually deteriorated the postural control system. We suggest that the observed deterioration in the control of an erect stance induced by a painful stimulation was mediated via high-threshold small diameter afferents. The present results also suggest that the postural control system was gradually more deteriorated as the proportion of recruited Aδ and C fibers increased.

Clearly, for the same perceived intensity of the pain, moderate painful stimulation applied to the feet deteriorated the postural control mechanisms when compared to the moderate stimulation applied to the hands. This suggests that the sensory perception of the noxious stimulation to the hand, once it had captured attention, did not yield any modification in the upright postural behavior. Hence, in order to deteriorate the control of an upright stance, the locus of the applied painful stimulation is of importance. This strongly suggests that the painful stimulation mainly affected the postural control mechanisms via reflex circuits rather than via the utilization, by the perception of pain, of cognitive resources necessary for the control of an upright stance.

Altogether, results of the present experiment show that the intensity and the locus of pain are crucial parameters to determine whether and to what extent the postural control system will be deteriorated. No association has been made previously between pain sensation and risk of falling. Results presented in this study could certainly lead to the hypothesis that pain is a factor increasing risks of falling, especially for populations at risk of falling (for example, frail elderly).

References

Arendt-Nielsen L, Sonnenborg FA and Andersen OK. Facilitation of the withdrawal reflex by repeated transcutaneous electrical stimulation: an experimental study on central integration in humans. Eur J Appl Physiol 2000;81:165-73.

Baratto L, Morasso PG, Re C and Spada G. A new look at posturographic analysis in the clinical context: sway-density versus other parameterization techniques. Motor Control 2002;6:246-70.

Capra NF and Ro JY. Experimental muscle pain produces central modulation of proprioceptive signals arising from jaw muscle spindles. Pain 2000;86:151-62.

Collins WFJ. Relation of peripheral nerve fiber size and sensation in man. Arch Neurol 1960;3:381-385.

Crombez G, Eccleston C, Baeyens F and Eelen P. Attentional disruption is enhanced by the threat of pain. Behav Res Ther 1998;36:195-204.

Dietz V. Human neuronal control of automatic functional movements: Interaction between central programs and afferent input. Physiol Rev 1992;72:33-69.

Gandevia SC and Phegan CM. Perceptual distortions of the human body image produced by local anaesthesia, pain and cutaneous stimulation. J Physiol 1999;514:609-16.

Laitinen LV and Eriksson AT. Electrical stimulation in the measurement of cutaneous sensibility. Pain 1985;22:139-50.

Le Pera D, Graven-Nielsen T, Valeriani M, Oliviero A, Di Lazzaro V, Tonali PA and Arendt-Nielsen L. Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain. Clin Neurophysiol 2001;112:1633-41.

Lundberg A. Multisensory control of spinal reflex pathways. Prog Brain Res 1979;50:11-28.

Lundberg A, Malmgren K and Schomburg ED. Reflex pathways from group II muscle afferents. 3. Secondary spindle afferents and the FRA: a new hypothesis. Exp Brain Res 1987;65:294-306.

Luoto S, Taimela S, Alaranta H and Hurri H. Psychomotor speed in chronic low-back pain patients and healthy controls: construct validity and clinical significance of the measure. Percept Mot Skills 1998;87:1283-96.

Maki BE, Holliday PJ and Fernie GR. Aging and postural control. A comparison of spontaneous- and induced-sway balance tests. J Am Geriatr Soc 1990;38:1-9.

Massion J. Postural control system. Curr Opin Neurobiol 1994;4:877-887.

Matre DA, Sinkjaer T, Svensson P and Arendt-Nielsen L. Experimental muscle pain increases the human stretch reflex. Pain 1998;75:331-9.

Miron D, Duncan GH and Bushnell MC. Effects of attention on the intensity and unpleasantness of thermal pain. Pain 1989;39:345-52.

Morasso PG and Schieppati M. Can muscle stiffness alone stabilize upright standing? J Neurophysiol 1999;82:1622-6.

Pai Y-C and Patton J. Center of mass velocity-position predictions for balance control. J Biomech 1997;30:347-354.

Price DD, McGrath PA, Rafii A and Buckingham B. The validation of visual analogue scales as ratio scale measures for chronic and experimental pain. Pain 1983;17:45-56.

Rossi A and Decchi B. Changes in Ib heteronymous inhibition to soleus motoneurones during cutaneous and muscle nociceptive stimulation in humans. Brain Res 1997;774:55-61.

Rossi A, Decchi B, Dami S, Della Volpe R and Groccia V. On the effect of chemically activated fine muscle afferents on interneurones mediating group I non-reciprocal inhibition of extensor ankle and knee muscles in humans. Brain Res 1999a;815:106-10.

Rossi A, Decchi B and Ginanneschi F. Presynaptic excitability changes of group Ia fibres to muscle nociceptive stimulation in humans. Brain Res 1999b;818:12-22.

Sang CN, Max MB and Gracely RH. Stability and reliability of detection thresholds for human A-Beta and A-delta sensory afferents determined by cutaneous electrical stimulation. J Pain Symptom Manage 2003;25:64-73.

Schomburg ED. Spinal functions in sensorimotor control of movements. Neurosurg Rev 1990;13:179-85.

Sherrington CS. Flexion-reflex of the limb, crossed extension reflex, and reflex stepping and standing. J Physiol 1910;40:28-121.

Sinha T and Maki BE. Effect of forward lean on postural ankle dynamics. IEEE Trans Rehab Eng 1996;4:348-359.

Taimela S, Osterman K, Alaranta H, Soukka A and Kujala UM. Long psychomotor reaction time in patients with chronic low-back pain: preliminary report. Arch Phys Med Rehabil 1993;74:1161-4.

Teasdale N and Simoneau M. Attentional demands for postural control: the effects of aging and sensory reintegration. Gait Posture 2001;14:203-10.

Weerakkody N, Percival P, Morgan DL, Gregory JE and Proske U. Matching different levels of isometric torque in elbow flexor muscles after eccentric exercise. Exp Brain Res 2003;149:141-50.

Woollacott M and Shumway-Cook A. Attention and the control of posture and gait: a review of an emerging area of research. Gait Posture 2002;16:1-14.

Yardley L and Redfern MS. Psychological factors influencing recovery from balance disorders. J Anxiety Disord 2001;15:107-19.