CHAPITRE VI EFFECTS OF PAIN ON THE COGNITIVE PROCESSES INVOLVED IN THE REGULATION OF BALANCE

(Soumis à Cognitive Brain Research)

Philippe Corbeil1, Jean-Sébastien Blouin1 & Normand Teasdale1

1 Faculté de médecine, Université Laval, Québec G1K 7P4, Canada.

Correspondence should be addressed to N.T. (normand.teasdale@kin.msp.ulaval.ca)

RÉSUMÉ

Il est reconnu que le contrôle de l’équilibre et la perception de la douleur nécessitent des ressources cognitives. Le but de cette étude sur la douleur consistait à identifier l’apport des ressources cognitives dans le contrôle de l’équilibre et la perception de la douleur. Le paradigme de la double tâche a été utilisé afin d’évaluer: (1) les effets d’une tâche de calcul mental (tâche prioritaire) sur le contrôle de l’équilibre (tâche secondaire) avec et sans une stimulation électrique douloureuse, et (2) les ressources attentionnelles requises pour maintenir l’équilibre orthostatique (tâche prioritaire) avec et sans une stimulation électrique douloureuse à l’aide d’une tâche de temps de réaction (tâche secondaire). Dans un premier temps, la réalisation de la tâche cognitive n’est pas affecté par la présence d’une stimulation douloureuse. Toutefois, l’exécution de la tâche mentale a entraîné une augmentation de la vitesse moyenne des oscillations posturales avec et sans la présence d’une stimulation douloureuse. En douleur, la variabilité des oscillations posturales n’est pas affectée par la réalisation de la double tâche. Ces résultats suggèrent que les processus cognitifs reliés à la perception de la douleur et ceux impliqués dans le contrôle de la posture sont indépendants. Dans un deuxième temps, aucun changement est observé au niveau des oscillations posturales lorsque les sujets effectuaient la tâche secondaire. Par contre, l’effet douleur est toujours présent. Le coût de l’attention (mesuré par le temps de réaction) est cependant plus élevé lorsque le maintien de l’équilibre se fait en station debout et avec une stimulation douleureuse. Ainsi, les processus de traitement de l’information sont plus lents lorsqu’il y a un stimulus douloureux. Lorsque la tâche posturale nécessitera une supervision plus cognitive des mécanismes de contrôle, la douleur pourrait venir ralentir la mise en action des réponses posturales et ainsi augmenter le risque de produire une réponse inadaptée.

Abstract

It is well recognized that both the control of posture and the perception of pain require cognitive resources but little is known if they share common neural mechanisms. The aim of the present study was two-fold: (1) to assess the effects of the mental task (counting backwards by multiples of three) on the control of upright standing with and without painful stimulation; (2) to quantify the cognitive resources required to maintain an upright stance with and without painful stimulation by assessing the performance of a hand motor reaction time (RT) task. Firstly, the performance of the mental task was similar with and without a painful stimulation. Moreover, the results clearly showed that pain altered the postural stability (increased mean velocity and variability of the center or pressure displacements) but there was no exacerbating effects when subjects performed both tasks with a painful stimulation. These results suggest that noxious stimuli altered mainly the postural stability via low sensorimotor processes. Secondly, larger postural oscillations were observed for all pain trials compared to the trials without pain, but the postural stability was unaffected by the cognitive task. Subjects have slower motor reaction times when they perceived pain, suggesting that the pain perception reduces the available cognitive resources, provoking a general slowing of the speed at which the information is processed. This could likely yield a slowness of the corrective postural responses and increase the risk of selecting inappropriate motor responses when a more demanding postural task is performed than standing upright quietly.

Keywords: Experimental pain, Postural control, Reaction times, Spoken mental task, Cognitive resources, Perception of pain, Center of foot pressure

1. Introduction

Several experiments provided clear evidence for the contribution of central cognitive processes for the on-line regulation of an upright posture [18,19,21,24]. A central hypothesis has been proposed : the small adjustments necessary to maintain an upright posture require some cognitive processing [18]. In dual-task studies involving the control of posture, the performance of a primary task (e.g. cognitive or postural task) is performed in isolation and its performance is compared to when the primary task is performed with a concurrent secondary task. Changes above the baseline level of performance of the secondary task is considered as a dual-task effect, i.e. reflecting changes in the resources necessary to perform the primary task. There are two main outcomes in these dual-task studies. First, there is the possible effect of controlling the upright stance on the performance of the secondary cognitive task. A “posture first” has been suggested that could explain deterioration in the cognitive task performance during dual-task studies [15,18]. This paradigm allows to quantify the cognitive resources required to perform the primary (posture) task. The second main outcome of interest is to document the effects of cognitive tasks on the postural control mechanisms. Here, the primary task is the cognitive task. This second experimental design allows to determine the beneficial or deteriorating effects of a cognitive task on the control of posture. It has been suggested that direction of attention towards a cognitive tasks (or an external focus of attention) is likely to let the control of posture rely on more automatic (reflexive and/or self-organizing) control processes [10,22].

Noxious stimuli activate nociceptors which are the peripheral endings of small diameter primary sensory neurons. After entering the spinal cord, the information generated by the 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 [6], a process likely to require cognitive resources. Indeed, 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 [8,17]. Moreover, shifting the direction of attention away from the painful stimuli alters the ability to discriminate noxious heat stimuli [4] and reduces the perceived intensity and unpleasantness of painful stimuli [11]. Finally, Spence et al. [16] suggested that the more attentional resources that are required by a distractor (distraction technique), the more effectively subjects should reduce reports of pain. These findings suggests that the processing of painful stimuli requires cognitive resources and that its processing can be modulated by selective attention to a particular sensory modality.

Some authors suggested that tonic pain activity could alter motor strategies [14]. For example, Weerakkody et al. [20] reported that subjects overestimated the level of torque generated by a limb affected by a nociceptive stimulation from the skin or sore muscles. Also, pain can induce a distortion of the body image, leading to a biased estimation of the body position in space [7]. The effects of cutaneous pain on the control of posture have been recently studied. It appears that a noxious stimulation of the small diameter afferents is needed to deteriorate the control of posture [2]. Furthermore, a painful stimulation applied on the hand did not deteriorate the postural control system suggesting that the noxious stimulus needed to be applied on a limb involved in the maintenance of an upright stance to deteriorate its control [5]. Although the second study suggests that nociception alters posture through sensorimotor processes, it remains to be determined if pain modifies the cognitive resources needed for the control of posture and also if selective attention directed away from the painful stimulus can diminished the deteriorating effects of pain on the postural control system.

The present study is designed to document the effects of pain on the cognitive processes involve in the regulation of balance by mean of a dual-task paradigms. Painful stimulations were applied bilaterally to the dorsum of the first tarso-metatarsal joint of both feet. More specifically, the aim of the present study was two-fold: (1) to assess the effects of the mental task (counting backwards by multiples of three) on the control of upright standing with and without painful stimulation; (2) to quantify the cognitive resources required to maintain an upright stance with and without painful stimulation by assessing the performance of a hand motor reaction time (RT) task.

2. Materials and methods

2.1. Subjects and apparatus

Eleven healthy male subjects participated in the study (age: 31.5 ± 7.6 years; height: 174.0 ± 6.6 cm, body weight: 76.3 ± 6.9 kg). The subjects were recruited at Laval University and had no evidence of gait, postural or musculo-skeletal abnormalities. All subjects gave informed consent 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 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 Postural stability protocol

Participants were tested individually in a single 75 minute-session. Subjects were instructed to stand as still as possible using a standardized stance on the force platform. For each participant, outline footmarks were traced in the center of the force platform such that the inner edges of their feet were 10 cm apart. 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. In some trials, subjects were asked to sit on a chair immediately behind the force platform and to place their feet on the outline footmarks. These trials were performed in order to assess the cognitive resources needed for a seated posture. For all experimental trials, subjects hold in their right hand a force sensor (UniForceTM system sensors; force range : 220 N). Each trial lasted 40.96 s.

2.3. Experimental electrical stimulation

Subjects were tested under two conditions of pain: without and with an experimental electrical stimulation. The technique for inducing a painful stimulation was inspired from the work of Arendt-Nielsen et al.[1]. A constant-voltage pulse train of 1-ms pulses was delivered at 10 Hz (ISI = 100ms) via bipolar surface Ag-AgCl electrodes (Meditrace, Canada) lasting the entire duration of the trial. Painful stimulations were applied to the dorsum of the first tarso-metatarsal joint of both feet. Pain was defined as any uncomfortable sensation (particularly prickling) even if the stimulus was tolerable. For each pain trial, subjects rated their perception of pain intensity by drawing a line on the visual analog scale (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 [12]. The painful intensity was set when subjects’ subjective pain score was equal to “6” using VAS.

2.4. Cognitive tasks

The additional cognitive task conditions were mental task, motor reaction time task (motor RT task) and no concurrent additional task. The mental task condition was counting backward in steps of three as accurately as possible for the duration of the trial, starting with a randomly selected number ranging between 250 and 750. Subjects were encouraged to maintain the rhythm of their counting as steady as possible. No feedback on performance was given during the testing. Subjects were first instructed how to perform the counting backward task and were corrected until it was mastered. The number of given responses and the number of errors were calculated. For this specific task, subjects were asked to consider the mental tasks as the primary task.

Subjects also performed a motor RT secondary task. They were instructed to press the force sensor as quickly as possible to an unpredictable auditory stimulus. The stimulus was a 1 KHz tone presented for 0.2 s. For each trial, five or six randomly presented auditory stimulus separated by at least 3.2 s could be presented. For both the control (no pain) and pain conditions, the total number (n=16) and the timing of the stimuli given were similar. Subjects were instructed to consider the postural task (i.e. sitting and upright standing) as the primary tasks. The motor RT task was the secondary task and any changes in RT would reflect changes in the cognitive resources necessary to perform the postural task. RT was defined as the temporal interval between the presentation of the auditory stimulus and the onset of the digital waveform of the signal recorded from the force sensor (detected from a voltage rise).

2.5. Design

To summarize the study, participants were required to stand on the force platform on three separate blocks during the session. Trials were blocked by cognitive task conditions (mental, motor RT and no concurrent tasks), and the order of these conditions was randomized between the subjects. There were two pain conditions (with and without the painful stimulus). Three trials were performed for each pain and cognitive conditions, for a total of 36 trials. In addition, for the mental task and the motor RT task, baseline trials (n=3) for the two conditions of pain were undertaken while participants were seated. The order of presentation of the trials within a block (with and without pain, sitting and standing) was randomized across subjects. Rest periods of 20 seconds were provided between each trial; five-minute periods were provided between blocks. Subjects were told they could interrupt the experimental session at any time if they felt the need.

2.6. Data reduction

Standard deviation of the CP trajectory and mean CP velocity along the A-P and M-L axes were calculated. The calculation of the standard deviation of the signal provides a measure of amplitude variability of the CP around a 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 [9,19].

2.7. Statistical analysis

In the first analysis, the effects of the Mental task (counting backwards in multiples of three) on the control of upright standing with and without painful stimulations were assessed. To do so, we compared the mean value of the parameters related to the performance of the mental task (e.g. number of given responses and number of errors) using two-way ANOVA with repeated measured on both factors (Pain vs Posture). In addition, the mean subjective pain rating on the VAS was compared using a one-way ANOVA (three levels: quiet standing with and without mental task and sitting with mental task). Also, we compared the mean value of the parameters computed from the CP displacements for all experimental conditions using two-way ANOVAs with repeated measures on both factors (Mental task vs Pain). In the second analysis, the effects of a balance task with and without painful stimulations on the performance of a motor RT task were documented. We compared the mean value of the RTs using two-way ANOVA repeated measured on both factors (Pain vs Posture). In addition, the mean subjective pain rating on the VAS was compared using a one-way ANOVA (three levels: quiet standing with and without motor RT task and sitting with motor RT task). Dependent variables related to the CP displacements were all submitted to a two-way repeated measures ANOVA (two factors: Dual-task and Pain). Post hoc analyses were performed using a Tukey test. The level of significance was set at p < 0.05.

3. Results

All subjects described the experimental electrical stimuli as a distinct prickling sensation. On average, the electrical intensity applied to the feet was 11.6V± 2.5 (mean ± standard deviation).

3.1. Mental task

3.1.1. Pain perception

For the mean visual analogue scores rated by the subjects, the ANOVA revealed a main effect of the Mental task (F(1,10) = 7.75, p < 0.01). Subjects rated higher the perceived pain on the VAS when standing without cognitive task than when performing the mental task standing or sitting (Tukey comparison of means: p< 0.001 and p < 0.05, respectively). No difference was observed for the perceived pain between standing and sitting while performing the mental task. On average, the mean visual analogue scores were 67 mm ± 15, 56 mm ± 22 and 58 mm ± 23 for quiet standing, dual-task while standing and dual-task while sitting. Hence, counting backward by three yielded a decrease of the perception of pain experienced by the subjects.

3.1.2. Mental task performance

Means, standard deviations and F-values for the number of given responses and number of errors during the mental task are presented in Table 1. For both parameters, the ANOVAs showed no main effect of Pain (ps > 0.05) and no interaction (ps > 0.05). The ANOVAs revealed a main effect of Posture (p < 0.05) only for the number of errors during the mental task. Subjects produced less error in the mental task when performing it in a sitting position. Overall, subjects maintained the same level of performance during the mental task with and without pain.

Tableau 1 : Performance of the spoken mental task.

   

Sitting

 

Quiet Standing

 

F-Values

   

No Pain

Pain

 

No Pain

Pain

 

Pain

Position

Interaction

# of responses

 

24.9 (5.6)

25.2 (5.4)

 

24.6 (5.2)

24.5 (5.4)

 

0.16

3.00

0.80

# of errors

 

0.9 (1.0)

0.7 (0.8)

 

1.1 (1.0)

0.9 (1.1)

 

0.58

4.98*

0.03

Note: * indicates a significant difference at p<0.05.

Mean (standard deviation in brackets) and ANOVA results on the backward counting task as a function of sitting and standing position with and without pain.

3.1.3. Effects of the mental task on postural control

Results of the CP parameters as a function of a Mental task (counting backward by three and quiet standing) and Pain conditions are illustrated in Fig. 1. Concerning the standard deviation of the CP oscillations along the M-L axis, the ANOVA revealed a significant Mental task by Pain interaction (F(1,10) = 12.8 , p < 0.01) and a main effect of Pain (F(1,10) = 8.64 , p < 0.01) but no main effect of the Mental task (p > 0.05). Decomposition of the interaction revealed that the standard deviation of the CP oscillations increased with the presence of Pain only when subjects were standing upright with no concurrent task. Hence, when subjects performed the Mental task, the standard deviation of the CP displacements were similar with and without Pain. For the A-P axis, the ANOVA showed that the standard deviation of the CP increased with the presence of Pain (F(1,10) = 15.3, p < 0.01) but showed no main effect of the Mental task and no interaction (ps > 0.05).

For the mean velocity of the CP displacement along the M-L axis, the ANOVA showed a main effect of Mental task (F(1,10) = 12.4, p < 0.01), a main effect of Pain (F(1,10) = 13.9, p < 0.01) and a significant interaction between both factors (F(1,10) = 5.70, p < 0.05). Decomposition of the interaction revealed that, for both Mental task conditions, the mean CP velocity along the M-L axis was greater with than without the painful stimulation. For the mean velocity of the CP displacement along the A-P axis, the ANOVA showed main effects of Pain (F(1,10) = 18.8, p < 0.01), but no main effect of the Mental task and no interaction were observed (p > 0.05). Subjects oscillated more when a painful stimulation was applied on their feet.

Figure 1 : Effects of spoken mental task on the control of posture with and without a painful stimulation.

Upper panels: Standard deviation of the CP displacements along the A-P (left panel) and M-L (right panel) axes for the pain and no pain conditions with and without the spoken mental task. Lower panels: Mean CP velocity for the pain and no pain conditions with and without the spoken mental task. Vertical bars denote the 0.95 confidence intervals.

3.2. Motor RT task

3.2.1. Pain perception

No effect of the motor RT conditions on the visual analogue scores was observed (p > 0.05). On average, the mean visual analogue scores were 67 mm ± 15, 62 mm ± 17 and 61 mm ± 22 for quiet standing, dual-task while standing and dual-task while sitting, respectively.

3.2.2. RTs

Fig. 2 illustrates means (± confidence intervals) of the motor RTs measured while subjects were sitting or standing with and without cutaneous pain. The ANOVA showed a main effect of Pain (F(1,10) = 6.00, p < 0.05) and a main effect of Posture (F(1,10) = 20.77, p < 0.01). The ANOVA revealed no interaction (p > 0.05). Subjects produced slower motor RTs when standing and with the presence of a painful stimulation.

Figure 2 : Means of the motor reaction times measured while subjects were sitting or standing with and without cutaneous pain.

Vertical bars denote the 0.95 confidence intervals.

3.2.3. Effects of the motor RT task on postural control

Means, standard deviations and ANOVA results of the CP parameters as a function of dual-task (motor RT and quiet standing) and pain factors are presented in Table 2. For the mean velocity and standard deviation of the CP displacement along both the M-L and A-P axes, the ANOVAs showed main effects of Pain (ps < 0.05), no main effects of Dual-task (ps > 0.05) and no interaction (ps > 0.05). On average, subjects exhibited faster mean velocity and greater variability of their postural oscillations when the experimental pain was applied compared to a control no pain condition.

Tableau 2 : Mean results of the CP parameters observed during all quiet standing trials.

   

Control

 

RT-Task

 

F-Values

   

No Pain

Pain

 

No Pain

Pain

 

Dual-task

Pain

Interaction

Standard Deviation M-L (mm)

 

1.9 (0.4)

3.2 (1.5)

 

2.3 (0.7)

3.1 (1.1)

 

0.27

9.79*

2.0

Standard Deviation A-P (mm)

 

3.8 (1.6)

5.6 (1.2)

 

4.3 (1.3)

5.9 (1.8)

 

1.25

11.7**

0.20

Mean Velocity M-L (mm/s)

 

2.7 (0.8)

5.4 (2.5)

 

3.1 (0.9)

5.5 (2.2)

 

1.27

18.7**

0.29

Mean Velocity A-P (mm/s)

 

5.1 (1.2)

7.4 (2.2)

 

5.0 (0.8)

7.0 (1.8)

 

0.27

16.7**

0.66

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

Mean (standard deviation in brackets) and ANOVA results of the center of foot pressure parameters as a function of standing on the platform with and without dual-task (RT-task) and with and without pain.

4. Discussion

It is well recognized that both the control of posture and the perception of pain require cognitive resources. A question of interest concerns if these actions share common neural mechanisms. The dual-task paradigm is an useful tool to study the interaction between control mechanisms that both require attentional resources. In the first part of this study, the cognitive task (counting backward by multiple of three) was considered as the primary task to assess the effects on the control of an upright posture with and without painful stimulation. The results clearly showed that pain altered the postural stability but there was no exacerbating effects when subjects performed both tasks with a painful stimulation. More specifically, for the pain trials, the variability of the postural oscillations along both axes remained statistically unchanged adding or not the mental task. Also, the mean velocity of the CP increased when the subjects performed the mental task, but this increase was less important with than without the painful stimulation, especially along the M-L axis. One explanation that could explain such results is that noxious stimuli altered mainly the postural stability via low sensorimotor processes. This observation is also supported by recent findings [2,5]. In both experiments, authors showed increased postural sways with the presence of a noxious heat stimuli [2], or a noxious electrical stimulation of moderate and extreme intensities [5].

The muscular control of posture is closely linked to muscular control of respiration [3,13,25] and it is possible that muscular and respiratory activity involved in speech directly perturbs posture [23]. Indeed, Yardley and colleagues [23] showed that the increase in postural sway that occurs in normal subjects when performing a spoken mental arithmetic task (counting backwards in multiples of seven) is due to the perturbing effects of articulation, rather than competing demands for attention. The instability could be the result of central interference; the mechanisms involved in the control of the postural and spoken mental tasks may share common neural mechanisms. The present results showed that the negative impact of a spoken task on the postural sways was less important with than without a painful stimulation. It is possible that when the subjects allocated, as a priority, attention to another task, the presence of a noxious stimuli could have reduced further the central influences on the mechanisms involved in the maintenance of an upright posture. On the other hand, the number of given responses and number of errors during the mental task were similar with and without a painful stimulation. These results suggest that pain related effects did not affect the performance of the spoken mental task.

It is clear that the lower painful perception reported by the subjects when performing the postural and spoken mental tasks than when performing the postural task alone, can not explain the observed deterioration of the postural stability with pain. These results support similar observation made by Corbeil et al. [5] who suggested that sensory perception of a noxious stimulation, once it captured attention, did not yield any modification in the upright postural behavior. In their experiment, they showed that, for the same perceived intensity of the pain, stimulation applied to the feet deteriorated the postural control mechanisms when compared to the stimulation applied to the hands.

In the second part of the study, we quantify the cognitive resources required to maintain an upright posture with and without a painful stimulation by assessing the performance of a RT task. Once again, larger postural oscillations were observed for all pain trials compared to the trials without a painful stimulation. However, the postural stability was unaffected by the cognitive task. For all the pain trials, compared to the trials without a painful stimulation, subjects have slower motor RTs, suggesting that the pain sensation reduces the available cognitive resources. Several authors reported similar results when comparing subjects suffering from lower back pain with a control population [8,17]. Pain sensation may provoke a general slowing of the speed at which the information can be processed or a reduction of the attentional capacities. Moreover, the attentional cost increased (as shown by the increased RT) when the postural task became increasingly difficult (standing versus sitting position). In addition of pain effects, attentional deficits (e.g. aging) and/or a more eccentric position of the center of mass (where a corrective response subsequently needs to be selected, programmed and executed) could likely yield a slowness of the corrective postural responses and increase the risk of selecting inappropriate motor responses.

The present experiment provides clear evidence that central mechanisms are used in the regulation of an upright stance as well as in the perception of pain. These central mechanisms necessary to regulate these actions are likely to be independent. However both requires attentionnal resources that might yield balance problems under more highly risky situation.

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.

References

[1] L. Arendt-Nielsen, F.A. Sonnenborg, O.K. Andersen, Facilitation of the withdrawal reflex by repeated transcutaneous electrical stimulation: an experimental study on central integration in humans, Eur. J. Appl. Physiol. 81 (2000) 165-173.

[2] J.S. Blouin, P. Corbeil, N. Teasdale, Postural stability is altered by the stimulation of Ad and C nociceptors but not by Ad and C warm receptors, Submitted to J. Physiol. (2003).

[3] S. Bouisset, J.L. Duchene, Is body balance more perturbed by respiration in seating than in standing posture?, Neuroreport 5 (1994) 957-960.

[4] M.C. Bushnell, G.H. Duncan, R. Dubner, R.L. Jones, W. Maixner, Attentional influences on noxious and innocuous cutaneous heat detection in humans and monkeys, J. Neurosci. 5 (1985) 1103-1110.

[5] P. Corbeil, J.S. Blouin, N. Teasdale, Effects of intensity and locus of painful stimulation on postural stability, Submitted to Pain (2003).

[6] G. Crombez, C. Eccleston, F. Baeyens, P. Eelen, Attentional disruption is enhanced by the threat of pain, Behav. Res. Ther. 36 (1998) 195-204.

[7] S.C. Gandevia, C.M. Phegan, Perceptual distortions of the human body image produced by local anaesthesia, pain and cutaneous stimulation, J. Physiol. 514 (1999) 609-616.

[8] S. Luoto, S. Taimela, H. Alaranta, H. Hurri, Psychomotor speed in chronic low-back pain patients and healthy controls: construct validity and clinical significance of the measure, Percept. Mot. Skills 87 (1998) 1283-1296.

[9] B.E. Maki, P.J. Holliday, G.R. Fernie, Aging and postural control. A comparison of spontaneous- and induced-sway balance tests, J. Am. Geriatr. Soc. 38 (1990) 1-9.

[10] N.H. McNevin, G. Wulf, Attentional focus on supra-postural tasks affects postural control, Hum. Mov. Sci. 21 (2002) 187-202.

[11] D. Miron, G.H. Duncan, M.C. Bushnell, Effects of attention on the intensity and unpleasantness of thermal pain, Pain 39 (1989) 345-352.

[12] D.D. Price, P.A. McGrath, A. Rafii, B. Buckingham, The validation of visual analogue scales as ratio scale measures for chronic and experimental pain, Pain 17 (1983) 45-56.

[13] K.P. Rimmer, G.T. Ford, W.A. Whitelaw, Interaction between postural and respiratory control of human intercostal muscles, J. Appl. Physiol. 79 (1995) 1556-1561.

[14] A. Rossi, B. Decchi, Changes in Ib heteronymous inhibition to soleus motoneurones during cutaneous and muscle nociceptive stimulation in humans, Brain. Res. 774 (1997) 55-61.

[15] A. Shumway-Cook, M. Woollacott, K.A. Kerns, M. Baldwin, The effects of two types of cognitive tasks on postural stability in older adults with and without a history of falls, J. Gerontol. 52A (1997) M232-M240.

[16] C. Spence, D.E. Bentley, N. Phillips, F.P. McGlone, A.K. Jones, Selective attention to pain: a psychophysical investigation, Exp. Brain Res. 145 (2002) 395-402.

[17] S. Taimela, K. Osterman, H. Alaranta, A. Soukka, U.M. Kujala, Long psychomotor reaction time in patients with chronic low-back pain: preliminary report, Arch. Phys. Med. Rehabil. 74 (1993) 1161-1164.

[18] N. Teasdale, C. Bard, J. Larue, M. Fleury, On the cognitive penetrability of posture control, Exp. Aging Res. 19 (1993) 1-13.

[19] N. Teasdale, M. Simoneau, Attentional demands for postural control: the effects of aging and sensory reintegration, Gait Posture 14 (2001) 203-210.

[20] N. Weerakkody, P. Percival, D.L. Morgan, J.E. Gregory, U. Proske, Matching different levels of isometric torque in elbow flexor muscles after eccentric exercise, Exp. Brain Res. 149 (2003) 141-150.

[21] M. Woollacott, A. Shumway-Cook, Attention and the control of posture and gait: a review of an emerging area of research, Gait Posture 16 (2002) 1-14.

[22] G. Wulf, N. McNevin, C.H. Shea, The automaticity of complex motor skill learning as a function of attentional focus, Q. J. Exp. Psychol. A 54 (2001) 1143-1154.

[23] L. Yardley, M. Gardner, A. Leadbetter, N. Lavie, Effect of articulatory and mental tasks on postural control, Neuroreport 10 (1999) 215-219.

[24] L. Yardley, M.S. Redfern, Psychological factors influencing recovery from balance disorders, J. Anxiety Disord. 15 (2001) 107-119.

[25] B.J. Yates, A.D. Miller, Physiological evidence that the vestibular system participates in autonomic and respiratory control, J. Vestib. Res. 8 (1998) 17-25.