- Email: [email protected]
Proprioceptive weighting changes in persons with low back pain and elderly persons during upright standing
Neuroscience Letters 366 (2004) 63–66
Proprioceptive weighting changes in persons with low back pain and elderly persons during upright standing Simon Brumagne a,∗ , Paul Cordo b , Sabine Verschueren c a
Department of Rehabilitation Sciences, Faculty of Physical Education and Physiotherapy, K.U. Leuven, Tervuursevest 101, B-3001 Leuven, Belgium b Neurological Sciences Institute, Oregon Health and Science University, West Campus, 505 N.W. 185th Avenue, Beaverton, OR 97006, USA c Department of Kinesiology, Faculty of Physical Education and Physiotherapy, K.U. Leuven, Leuven, Belgium Received 21 January 2004; received in revised form 8 April 2004; accepted 8 May 2004
Abstract The purpose of this study was to examine whether postural instability observed in persons with spinal pain and in elderly persons is due to changes in proprioception and postural control strategy. The upright posture of 20 young and 20 elderly persons, with and without spinal pain, was challenged by vibrating ankle muscles (i.e. tibialis anterior, triceps surae) or paraspinal muscles. Center of pressure displacement was recorded using a force plate. Persons with spinal pain were more sensitive to triceps surae vibration and less sensitive to paraspinal vibration than persons without spinal pain. Elderly persons were more sensitive to tibialis anterior vibration than young healthy persons. These results suggest that spinal pain and aging may lead to changes in postural control by refocusing proprioceptive sensitivity from the trunk to the ankles. © 2004 Elsevier Ireland Ltd. All rights reserved. Keywords: Postural control; Proprioception; Vibration; Low back pain; Aging; Inverted pendulum; Somatosensory integration
Postural stability is achieved, in part, through input from the proprioceptive, visual, and vestibular systems, which the central nervous system (CNS) must weight relative to one another depending on the immediate conditions. An important property of the postural control system is its ability to gate sensory input in accordance with the internal representation of the current posture, so as to avoid undesirable responses triggered by external or internal perturbations [8]. In some circumstances, it might be advantageous for the CNS to be able to reweight sensory input based on location of origin, rather than modality. For example, if the quality of input from a particular body location decreases due to injury, disease, or normal aging, the CNS might increase the weighting of input from other locations that provide information useful for maintaining a stable posture. Without spatial reweighting of sensory input, reliance on impoverished input from a particular body location might lead to loss of balance and falling. Proprioceptive input from the muscles of the legs and trunk plays an important role in maintaining postural stabil-
∗
Corresponding author. Tel.: +32 16 329121; fax: +32 16 329197. E-mail address: [email protected] (S. Brumagne).
ity [1], suggesting that sensory deficits from either location might result in instability. Postural instability has been observed in patients with low back pain [11] as well as in elderly persons [12]. Patients with low back pain have also been attributed reduced lumbosacral proprioception [3], which might be a causative factor in their instability. The study described in this paper investigated whether the weighting of proprioceptive input in the back and ankles changes in persons with low back pain and persons who are elderly. Tendon and muscle vibration was used as an experimental probe to quantify the weighting of proprioceptive input from the areas of the lumbar back and the ankles, at least as far as it influences stability during quiet standing. Vibration is a potent stimulus for muscle spindle Ia afferents [2], and applied to the leg muscles during quiet standing, it can induce postural instability, sometimes to the point of falling (e.g., [5]). Mechanical vibrations were applied, during quiet standing, to the triceps surae, tibialis anterior, or lumbar paraspinal muscles in young and elderly persons with low back pain (LBP) and age-matched healthy persons during quiet standing. Twenty young adults (10 healthy, 10 LBP; mean age = 25 years) and 20 elderly persons (10 healthy, 10 LBP; mean age = 63 years) participated in this study. The patients
0304-3940/$ – see front matter © 2004 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2004.05.013
64
S. Brumagne et al. / Neuroscience Letters 366 (2004) 63–66
were recruited from the Department of Physical Medicine and Rehabilitation, University Hospitals of Leuven. Most of these patients did not have a more specific diagnosis than mechanical LBP. They had an average score of 20/100 on the Oswestry Disability Index, version 2 [6]. A 6-channel force plate (Bertec, OH, USA) recorded the moments of force around the frontal (Mx ) and sagittal (My ) axes and the vertical ground reaction force (Fz ). Force plate data were sampled at 500 Hz using a Micro1401 data acquisition system and Spike2 software (Cambridge Electronic Design, UK) and low pass filtered (fc = 5 Hz). The subjects stood barefoot on the force plate with the feet separated by the width of the hips, the arms hanging loosely at the sides. The subjects were instructed to remain still and relaxed. Each subject was tested under four experimental conditions: (1) control (no vibration); (2) bilateral vibration of the triceps surae tendons; (3) bilateral vibration of the tibialis anterior tendons; and (4) bilateral vibration of the paraspinal muscle bellies. In all four conditions, vision was occluded by means of liquid-crystal goggles (Translucent Technologies, Canada). Trials lasted 60 s. Tendon and muscle vibration (60 pps, ≈0.5 mm) started 15 s after the start of the trial and lasted for 15 s. Displacement of the center of pressure (CoP) was estimated from the force plate data using the equation: CoP = Mx /Fz , and the CoP was averaged over the 15 s periods prior to and during vibration to quantify the directional effect of vibration. In control trials, the root mean square (RMS) value of the CoP was also calculated to quantify the baseline variability in each group of subjects. Postural recovery times were determined as the total time from cessation of vibration until CoP displacement of the subject was again within the limits of two standard deviations of the mean position, that was determined over the 15 s period prior to vibration. During all conditions, minor force variations were measured in the frontal plane. Hence, for clarity, the analysis will only be carried out in the sagittal plane and no data relative to the frontal plane will be given. Differences in CoP measurements between control conditions and vibration conditions, and between patient group and healthy control group, and between the young and elderly persons were based on F-test analysis of variance, using one-way and two-way procedures with repeated measures on one factor (Statistica, OK, USA). The significance level was set at P < 0.05. In the absence of vibration, the RMS CoP displacement in the anterior–posterior direction was quite small (0.5–1.0 cm), but significantly greater in the persons with low back pain compared to the healthy individuals (F(1, 39) = 4.33, P < 0.05) (see Fig. 1). When vibration was applied bilaterally to the triceps surae, all subjects shifted the CoP posteriorly (see Fig. 2), but much larger sways were seen in the persons with low back pain (10.4 ± 4.1 cm) compared to the healthy individuals (5.9 ± 5.2 cm) (F(1, 39) = 8.78, P < 0.01). When vibration was applied to the tibialis anterior muscles, all subjects shifted the CoP anteriorly (see Fig. 2), but the CoP displacement in the elderly (7.2 ± 3.2 cm) was significantly
Fig. 1. Anteroposterior sways for the four conditions and subgroups. Mean RMS values and standard deviations.
larger than that in the young individuals (4.8 ± 2.8 cm) (F(1, 39) = 6.9, P < 0.05). In addition, the CoP displacement in the persons with low back pain (7.0 ± 3.1 cm) was significantly larger than that in the healthy individuals (5.0 ± 3.0 cm) (F(1, 39) = 7.22, P < 0.05). When vibration was applied bilaterally to the paraspinal muscles, the persons with low back pain and the elderly produced little or no displacement of the CoP, whereas the CoP of healthy individuals were displaced anteriorly by an average of 3.5 ± 2.4 cm (F(1, 39) = 4.23, P < 0.05) (see Fig. 2). In individuals with low back pain, both young and elderly, and in the healthy elderly as well, these differences in CoP displacement produced by vibration may reflect a refocusing of proprioceptive control of balance away from proximal and axial proprioception input to that derived from receptors in the ankle muscles. Following the cessation of vibration, the vibration-evoked displacement of the CoP diminished over a period of time, although the length of time depended on the subject group. For example, following the cessation of the triceps surae vibration, the persons with low back pain had significantly longer postural recovery times (16.2 ± 8.6 s) than the healthy individuals (7.9 ± 4.4 s) (F(1, 79) = 15.55, P < 0.001). When age is taken into account, the young healthy persons recovered their postural stability significantly faster
Fig. 2. Anteroposterior sways for the muscle vibration conditions and subgroups. Group mean values and standard deviations.
S. Brumagne et al. / Neuroscience Letters 366 (2004) 63–66
Fig. 3. Anteroposterior sways of a representative healthy person (A) and a person with low back pain (B) during the vibration trials: (1) bilateral triceps surae muscles vibration; (2) lumbar paraspinal muscles vibration; (3) bilateral tibialis anterior muscles vibration. Note the absence of postural recovery after cessation of ankle muscles vibration in the person with low back pain.
after vibration stopped (4.9 ± 1.9 s) than the elderly healthy persons (10.9 ± 4.1 s) (F(1, 39) = 16.93, P < 0.001). Fig. 3 displays the anteroposterior CoP displacement during the muscle vibration conditions of a representative healthy young person (panel A) compared to a representative young person with LBP (panel B). Healthy subjects, both young and elderly, proved sensitive to muscle vibration at the ankles and lumbar trunk. This sensitivity manifested as a change in the average displacement in the CoP away from the center of support, in the forward direction to vibration of tibialis anterior and paraspinal muscles and posterior to vibration of triceps surae muscles. Our observation that elderly healthy persons are as sensitive to muscle vibration as young individuals are not in agreement with previous studies that reported little [13] or no sensitivity to muscle vibration [12] in elderly persons. A possible explanation for this disparity could be that the age of the elderly in these previous studies was much higher (i.e., 82 years) than in our study. An alternative explanation might be that only triceps surae muscles vibration was used in these studies (and not tibialis anterior muscle vibration). Moreover, a recent study on dynamic position sense at the ankle in elderly persons showed that the age-related decline in position sense performance was not due to muscle spindle changes of tibialis anterior muscle [14]. Our results suggest that both LBP and aging alter proprioceptive sensitivity in different parts of the body, at least
65
as far as proprioception influences standing posture. In our comparison of the vibration responses of individuals with and without LBP, sensitivity to vibration of the paraspinal muscles was lower in persons with LBP. In contrast, persons with LBP were more sensitive to vibration of the triceps surae muscles compared to the healthy persons. In our comparison of young and elderly persons, tibialis anterior vibration induced a larger displacement of the CoP in elderly individuals. In addition, after cessation of muscle vibration, healthy persons recover their normal postural orientation after the offset of vibration much faster than persons with LBP, and young individuals much faster than their elderly counterparts. These changes in sensitivity to vibration in the lower back and ankles produced by aging and back pain could have resulted from a decrease in the sensitivity of paraspinal muscle spindles or to changes in the central processing of this afferent information [3]. In healthy persons, it has been shown that the interpretation and use of sensory information can be altered in accordance with the internal representation of the current posture [8]. Similarly, sensorimotor deficits may result from pathology or normal aging, as observed in patients with low back pain [3]. One way to compensate for these proprioceptive deficits is to increase reliance on other sensory systems such as vision, for instance, in the control of posture [9,12]. Alternatively, individuals can shift the focus of attention from loci with deficient sensory input to others with intact input. The hypothesized sensory deficiency might be due to specific proprioceptive deficits from a particular part of the body or to the individual’s unwillingness to move that part of the body, thereby generating proprioceptive information, because movement causes pain or it induces a fear of injury. For example, patients with LBP might stiffen the trunk and pelvis and hyperextend the knees in order to decrease the number of degrees of freedom. Similar observations have been reported in deafferented patients and individuals with Parkinson disease, who seem to stiffen their trunk and pelvis, possibly to compensate for defective information about body position [16]. Fear of falling, for example, in the elderly, decreases the CoP excursion due to increased muscle activity and axial stiffness [4]. In patients with LBP, anteroposterior sway increases during complex conditions or tasks, but not in quiet stance [11]. In elderly individuals, who are generally less flexible in the axial parts of the body, the CoP moves less during quiet stance than in young adults. It can be argued that this kind of postural control strategy, i.e., inverted pendulum model of postural control [17], seems to be sufficient during quiet stance, resulting sometimes in even a smaller CoP displacement compared to healthy persons, but in more complex conditions or tasks, such as unstable support surface which decreases the reliance on the ankle proprioception [8], this postural control strategy seems to be inadequate resulting in postural instability and even falls. The advantage of controlling fewer degrees of freedom is offset by loss of flexible responses to dampen external perturbations. Instead, perturbations are transferred
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S. Brumagne et al. / Neuroscience Letters 366 (2004) 63–66
more equally to all body segments in stiff persons. Postural chain mobility seems to be necessary for postural stability, in particular, in the pelvic and lumbar spine regions [7,10]. Whether the observed reduced proprioceptive sensitivity of the lower back is a result of or a cause of LBP remains an intriguing question to be solved. In either case, the observed change in proprioceptive sensitivity in persons with LBP might be an underlying cause of the high recurrence rate seen in patients with low back pain. Similarly, the altered proprioceptive sensitivity seen in the elderly group could partially explain the higher risk for falling in complex postural activities. Flexibility and efficient central processing might be a key factor in postural stability, as previously shown in expert gymnasts [15], and such flexibility could be important for preventing LBP and falls. In conclusion, elderly individuals and persons with LBP have altered proprioceptive sensitivity. Reweighting of proprioceptive input by increasing the gain at the ankle joints seems to take place in both groups of individuals. The adapted postural control strategy might be effective in simple conditions, but perhaps less so when postural demands increase.
Acknowledgements This work was partially supported by grants PDM/99/121 (Research Council K.U. Leuven) and 1.5.104.03 (Fund for Scientific Research—Flanders).
References [1] B.R. Bloem, J.H. Allum, M.G. Carpenter, F. Honegger, Is lower leg proprioception essential for triggering human automatic postural responses? Exp. Brain Res. 130 (2000) 375–391. [2] M.C. Brown, I. Engberg, P.B.C. Matthews, Relative sensitivity to vibration of muscle receptors of the cat, J. Physiol. 192 (1967) 773– 800.
[3] S. Brumagne, P. Cordo, R. Lysens, S. Swinnen, S. Verschueren, The role of paraspinal muscle spindles in lumbosacral position sense in individuals with and without low back pain, Spine 25 (2000) 989– 994. [4] M.G. Carpenter, J.S. Frank, C.P. Silcher, G.W. Peysar, The influence of postural threat on the control of upright stance, Exp. Brain Res. 138 (2001) 210–218. [5] G. Eklund, General features of vibration-induced effects on balance, Ups. J. Med. Sci. 77 (1972) 112–124. [6] J.C.T. Fairbank, P.B. Pynsent, The Oswestry Disability Index, Spine 25 (2000) 2940–2953. [7] P.W. Hodges, V.S. Gurfinkel, S. Brumagne, T.C. Smith, P.J. Cordo, Coexistence of stability and mobility in postural control: evidence from postural compensation for respiration, Exp. Brain Res. 144 (2002) 293–302. [8] Y.P. Ivanenko, I.A. Solopova, Y.S. Levik, The direction of postural instability affects postural reactions to ankle muscle vibration in humans, Neurosci. Lett. 292 (2000) 103–106. [9] K.E. Jones, J. Wessberg, A. Vallbo, Proprioceptive feedback is reduced during adaptation to a visuomotor transformation: preliminary findings, Neuroreport 12 (2001) 4029–4033. [10] E. Kantor, L. Poupard, S. Le Bozec, S. Bouisset, Does body stability depend on postural chain mobility or stability area? Neurosci. Lett. 308 (2001) 128–132. [11] M.I. Mientjes, J.S. Frank, Balance in chronic low back pain patients compared to healthy people under various conditions in upright standing, Clin. Biomech. 14 (1999) 710–716. [12] I. Pyykkö, P. Jantti, H. Aalto, Postural control in elderly subjects, Age Ageing 19 (1990) 215–221. [13] C. Quoniam, L. Hay, J.P. Roll, F. Harlay, Age effects on reflex and postural responses to propriomuscular inputs generated by tendon vibration, J. Gerontol. A. Biol. Sci. Med. Sci. 50 (1995) 155– 165. [14] S.M.P. Verschueren, S. Brumagne, S.P. Swinnen, P.J. Cordo, The effect of aging on dynamic position sense at the ankle, Behav. Brain Res. 136 (2002) 593–603. [15] N. Vuillerme, N. Teasdale, V. Nougier, The effect of expertise in gymnastics on proprioceptive sensory integration in human subjects, Neurosci. Lett. 311 (2001) 73–76. [16] N. Wijnberg, Posture in Parkinson patients: a proprioceptive problem?, in: J. Duysens, B.C.M. Smits-Engelsman, H. Kingma (Eds.), Control of Posture and Gait, Maastricht, 2001, pp. 758– 761. [17] D.A. Winter, A.E. Patla, F. Prince, M. Ishac, K. Gielo-Perczak, Stiffness control of balance in quiet standing, J. Neurophysiol. 80 (1998) 1211–1221.
Proprioceptive weighting changes in persons with low back pain and elderly persons during upright standing Simon Brumagne a,∗ , Paul Cordo b , Sabine Verschueren c a
Department of Rehabilitation Sciences, Faculty of Physical Education and Physiotherapy, K.U. Leuven, Tervuursevest 101, B-3001 Leuven, Belgium b Neurological Sciences Institute, Oregon Health and Science University, West Campus, 505 N.W. 185th Avenue, Beaverton, OR 97006, USA c Department of Kinesiology, Faculty of Physical Education and Physiotherapy, K.U. Leuven, Leuven, Belgium Received 21 January 2004; received in revised form 8 April 2004; accepted 8 May 2004
Abstract The purpose of this study was to examine whether postural instability observed in persons with spinal pain and in elderly persons is due to changes in proprioception and postural control strategy. The upright posture of 20 young and 20 elderly persons, with and without spinal pain, was challenged by vibrating ankle muscles (i.e. tibialis anterior, triceps surae) or paraspinal muscles. Center of pressure displacement was recorded using a force plate. Persons with spinal pain were more sensitive to triceps surae vibration and less sensitive to paraspinal vibration than persons without spinal pain. Elderly persons were more sensitive to tibialis anterior vibration than young healthy persons. These results suggest that spinal pain and aging may lead to changes in postural control by refocusing proprioceptive sensitivity from the trunk to the ankles. © 2004 Elsevier Ireland Ltd. All rights reserved. Keywords: Postural control; Proprioception; Vibration; Low back pain; Aging; Inverted pendulum; Somatosensory integration
Postural stability is achieved, in part, through input from the proprioceptive, visual, and vestibular systems, which the central nervous system (CNS) must weight relative to one another depending on the immediate conditions. An important property of the postural control system is its ability to gate sensory input in accordance with the internal representation of the current posture, so as to avoid undesirable responses triggered by external or internal perturbations [8]. In some circumstances, it might be advantageous for the CNS to be able to reweight sensory input based on location of origin, rather than modality. For example, if the quality of input from a particular body location decreases due to injury, disease, or normal aging, the CNS might increase the weighting of input from other locations that provide information useful for maintaining a stable posture. Without spatial reweighting of sensory input, reliance on impoverished input from a particular body location might lead to loss of balance and falling. Proprioceptive input from the muscles of the legs and trunk plays an important role in maintaining postural stabil-
∗
Corresponding author. Tel.: +32 16 329121; fax: +32 16 329197. E-mail address: [email protected] (S. Brumagne).
ity [1], suggesting that sensory deficits from either location might result in instability. Postural instability has been observed in patients with low back pain [11] as well as in elderly persons [12]. Patients with low back pain have also been attributed reduced lumbosacral proprioception [3], which might be a causative factor in their instability. The study described in this paper investigated whether the weighting of proprioceptive input in the back and ankles changes in persons with low back pain and persons who are elderly. Tendon and muscle vibration was used as an experimental probe to quantify the weighting of proprioceptive input from the areas of the lumbar back and the ankles, at least as far as it influences stability during quiet standing. Vibration is a potent stimulus for muscle spindle Ia afferents [2], and applied to the leg muscles during quiet standing, it can induce postural instability, sometimes to the point of falling (e.g., [5]). Mechanical vibrations were applied, during quiet standing, to the triceps surae, tibialis anterior, or lumbar paraspinal muscles in young and elderly persons with low back pain (LBP) and age-matched healthy persons during quiet standing. Twenty young adults (10 healthy, 10 LBP; mean age = 25 years) and 20 elderly persons (10 healthy, 10 LBP; mean age = 63 years) participated in this study. The patients
0304-3940/$ – see front matter © 2004 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2004.05.013
64
S. Brumagne et al. / Neuroscience Letters 366 (2004) 63–66
were recruited from the Department of Physical Medicine and Rehabilitation, University Hospitals of Leuven. Most of these patients did not have a more specific diagnosis than mechanical LBP. They had an average score of 20/100 on the Oswestry Disability Index, version 2 [6]. A 6-channel force plate (Bertec, OH, USA) recorded the moments of force around the frontal (Mx ) and sagittal (My ) axes and the vertical ground reaction force (Fz ). Force plate data were sampled at 500 Hz using a Micro1401 data acquisition system and Spike2 software (Cambridge Electronic Design, UK) and low pass filtered (fc = 5 Hz). The subjects stood barefoot on the force plate with the feet separated by the width of the hips, the arms hanging loosely at the sides. The subjects were instructed to remain still and relaxed. Each subject was tested under four experimental conditions: (1) control (no vibration); (2) bilateral vibration of the triceps surae tendons; (3) bilateral vibration of the tibialis anterior tendons; and (4) bilateral vibration of the paraspinal muscle bellies. In all four conditions, vision was occluded by means of liquid-crystal goggles (Translucent Technologies, Canada). Trials lasted 60 s. Tendon and muscle vibration (60 pps, ≈0.5 mm) started 15 s after the start of the trial and lasted for 15 s. Displacement of the center of pressure (CoP) was estimated from the force plate data using the equation: CoP = Mx /Fz , and the CoP was averaged over the 15 s periods prior to and during vibration to quantify the directional effect of vibration. In control trials, the root mean square (RMS) value of the CoP was also calculated to quantify the baseline variability in each group of subjects. Postural recovery times were determined as the total time from cessation of vibration until CoP displacement of the subject was again within the limits of two standard deviations of the mean position, that was determined over the 15 s period prior to vibration. During all conditions, minor force variations were measured in the frontal plane. Hence, for clarity, the analysis will only be carried out in the sagittal plane and no data relative to the frontal plane will be given. Differences in CoP measurements between control conditions and vibration conditions, and between patient group and healthy control group, and between the young and elderly persons were based on F-test analysis of variance, using one-way and two-way procedures with repeated measures on one factor (Statistica, OK, USA). The significance level was set at P < 0.05. In the absence of vibration, the RMS CoP displacement in the anterior–posterior direction was quite small (0.5–1.0 cm), but significantly greater in the persons with low back pain compared to the healthy individuals (F(1, 39) = 4.33, P < 0.05) (see Fig. 1). When vibration was applied bilaterally to the triceps surae, all subjects shifted the CoP posteriorly (see Fig. 2), but much larger sways were seen in the persons with low back pain (10.4 ± 4.1 cm) compared to the healthy individuals (5.9 ± 5.2 cm) (F(1, 39) = 8.78, P < 0.01). When vibration was applied to the tibialis anterior muscles, all subjects shifted the CoP anteriorly (see Fig. 2), but the CoP displacement in the elderly (7.2 ± 3.2 cm) was significantly
Fig. 1. Anteroposterior sways for the four conditions and subgroups. Mean RMS values and standard deviations.
larger than that in the young individuals (4.8 ± 2.8 cm) (F(1, 39) = 6.9, P < 0.05). In addition, the CoP displacement in the persons with low back pain (7.0 ± 3.1 cm) was significantly larger than that in the healthy individuals (5.0 ± 3.0 cm) (F(1, 39) = 7.22, P < 0.05). When vibration was applied bilaterally to the paraspinal muscles, the persons with low back pain and the elderly produced little or no displacement of the CoP, whereas the CoP of healthy individuals were displaced anteriorly by an average of 3.5 ± 2.4 cm (F(1, 39) = 4.23, P < 0.05) (see Fig. 2). In individuals with low back pain, both young and elderly, and in the healthy elderly as well, these differences in CoP displacement produced by vibration may reflect a refocusing of proprioceptive control of balance away from proximal and axial proprioception input to that derived from receptors in the ankle muscles. Following the cessation of vibration, the vibration-evoked displacement of the CoP diminished over a period of time, although the length of time depended on the subject group. For example, following the cessation of the triceps surae vibration, the persons with low back pain had significantly longer postural recovery times (16.2 ± 8.6 s) than the healthy individuals (7.9 ± 4.4 s) (F(1, 79) = 15.55, P < 0.001). When age is taken into account, the young healthy persons recovered their postural stability significantly faster
Fig. 2. Anteroposterior sways for the muscle vibration conditions and subgroups. Group mean values and standard deviations.
S. Brumagne et al. / Neuroscience Letters 366 (2004) 63–66
Fig. 3. Anteroposterior sways of a representative healthy person (A) and a person with low back pain (B) during the vibration trials: (1) bilateral triceps surae muscles vibration; (2) lumbar paraspinal muscles vibration; (3) bilateral tibialis anterior muscles vibration. Note the absence of postural recovery after cessation of ankle muscles vibration in the person with low back pain.
after vibration stopped (4.9 ± 1.9 s) than the elderly healthy persons (10.9 ± 4.1 s) (F(1, 39) = 16.93, P < 0.001). Fig. 3 displays the anteroposterior CoP displacement during the muscle vibration conditions of a representative healthy young person (panel A) compared to a representative young person with LBP (panel B). Healthy subjects, both young and elderly, proved sensitive to muscle vibration at the ankles and lumbar trunk. This sensitivity manifested as a change in the average displacement in the CoP away from the center of support, in the forward direction to vibration of tibialis anterior and paraspinal muscles and posterior to vibration of triceps surae muscles. Our observation that elderly healthy persons are as sensitive to muscle vibration as young individuals are not in agreement with previous studies that reported little [13] or no sensitivity to muscle vibration [12] in elderly persons. A possible explanation for this disparity could be that the age of the elderly in these previous studies was much higher (i.e., 82 years) than in our study. An alternative explanation might be that only triceps surae muscles vibration was used in these studies (and not tibialis anterior muscle vibration). Moreover, a recent study on dynamic position sense at the ankle in elderly persons showed that the age-related decline in position sense performance was not due to muscle spindle changes of tibialis anterior muscle [14]. Our results suggest that both LBP and aging alter proprioceptive sensitivity in different parts of the body, at least
65
as far as proprioception influences standing posture. In our comparison of the vibration responses of individuals with and without LBP, sensitivity to vibration of the paraspinal muscles was lower in persons with LBP. In contrast, persons with LBP were more sensitive to vibration of the triceps surae muscles compared to the healthy persons. In our comparison of young and elderly persons, tibialis anterior vibration induced a larger displacement of the CoP in elderly individuals. In addition, after cessation of muscle vibration, healthy persons recover their normal postural orientation after the offset of vibration much faster than persons with LBP, and young individuals much faster than their elderly counterparts. These changes in sensitivity to vibration in the lower back and ankles produced by aging and back pain could have resulted from a decrease in the sensitivity of paraspinal muscle spindles or to changes in the central processing of this afferent information [3]. In healthy persons, it has been shown that the interpretation and use of sensory information can be altered in accordance with the internal representation of the current posture [8]. Similarly, sensorimotor deficits may result from pathology or normal aging, as observed in patients with low back pain [3]. One way to compensate for these proprioceptive deficits is to increase reliance on other sensory systems such as vision, for instance, in the control of posture [9,12]. Alternatively, individuals can shift the focus of attention from loci with deficient sensory input to others with intact input. The hypothesized sensory deficiency might be due to specific proprioceptive deficits from a particular part of the body or to the individual’s unwillingness to move that part of the body, thereby generating proprioceptive information, because movement causes pain or it induces a fear of injury. For example, patients with LBP might stiffen the trunk and pelvis and hyperextend the knees in order to decrease the number of degrees of freedom. Similar observations have been reported in deafferented patients and individuals with Parkinson disease, who seem to stiffen their trunk and pelvis, possibly to compensate for defective information about body position [16]. Fear of falling, for example, in the elderly, decreases the CoP excursion due to increased muscle activity and axial stiffness [4]. In patients with LBP, anteroposterior sway increases during complex conditions or tasks, but not in quiet stance [11]. In elderly individuals, who are generally less flexible in the axial parts of the body, the CoP moves less during quiet stance than in young adults. It can be argued that this kind of postural control strategy, i.e., inverted pendulum model of postural control [17], seems to be sufficient during quiet stance, resulting sometimes in even a smaller CoP displacement compared to healthy persons, but in more complex conditions or tasks, such as unstable support surface which decreases the reliance on the ankle proprioception [8], this postural control strategy seems to be inadequate resulting in postural instability and even falls. The advantage of controlling fewer degrees of freedom is offset by loss of flexible responses to dampen external perturbations. Instead, perturbations are transferred
66
S. Brumagne et al. / Neuroscience Letters 366 (2004) 63–66
more equally to all body segments in stiff persons. Postural chain mobility seems to be necessary for postural stability, in particular, in the pelvic and lumbar spine regions [7,10]. Whether the observed reduced proprioceptive sensitivity of the lower back is a result of or a cause of LBP remains an intriguing question to be solved. In either case, the observed change in proprioceptive sensitivity in persons with LBP might be an underlying cause of the high recurrence rate seen in patients with low back pain. Similarly, the altered proprioceptive sensitivity seen in the elderly group could partially explain the higher risk for falling in complex postural activities. Flexibility and efficient central processing might be a key factor in postural stability, as previously shown in expert gymnasts [15], and such flexibility could be important for preventing LBP and falls. In conclusion, elderly individuals and persons with LBP have altered proprioceptive sensitivity. Reweighting of proprioceptive input by increasing the gain at the ankle joints seems to take place in both groups of individuals. The adapted postural control strategy might be effective in simple conditions, but perhaps less so when postural demands increase.
Acknowledgements This work was partially supported by grants PDM/99/121 (Research Council K.U. Leuven) and 1.5.104.03 (Fund for Scientific Research—Flanders).
References [1] B.R. Bloem, J.H. Allum, M.G. Carpenter, F. Honegger, Is lower leg proprioception essential for triggering human automatic postural responses? Exp. Brain Res. 130 (2000) 375–391. [2] M.C. Brown, I. Engberg, P.B.C. Matthews, Relative sensitivity to vibration of muscle receptors of the cat, J. Physiol. 192 (1967) 773– 800.
[3] S. Brumagne, P. Cordo, R. Lysens, S. Swinnen, S. Verschueren, The role of paraspinal muscle spindles in lumbosacral position sense in individuals with and without low back pain, Spine 25 (2000) 989– 994. [4] M.G. Carpenter, J.S. Frank, C.P. Silcher, G.W. Peysar, The influence of postural threat on the control of upright stance, Exp. Brain Res. 138 (2001) 210–218. [5] G. Eklund, General features of vibration-induced effects on balance, Ups. J. Med. Sci. 77 (1972) 112–124. [6] J.C.T. Fairbank, P.B. Pynsent, The Oswestry Disability Index, Spine 25 (2000) 2940–2953. [7] P.W. Hodges, V.S. Gurfinkel, S. Brumagne, T.C. Smith, P.J. Cordo, Coexistence of stability and mobility in postural control: evidence from postural compensation for respiration, Exp. Brain Res. 144 (2002) 293–302. [8] Y.P. Ivanenko, I.A. Solopova, Y.S. Levik, The direction of postural instability affects postural reactions to ankle muscle vibration in humans, Neurosci. Lett. 292 (2000) 103–106. [9] K.E. Jones, J. Wessberg, A. Vallbo, Proprioceptive feedback is reduced during adaptation to a visuomotor transformation: preliminary findings, Neuroreport 12 (2001) 4029–4033. [10] E. Kantor, L. Poupard, S. Le Bozec, S. Bouisset, Does body stability depend on postural chain mobility or stability area? Neurosci. Lett. 308 (2001) 128–132. [11] M.I. Mientjes, J.S. Frank, Balance in chronic low back pain patients compared to healthy people under various conditions in upright standing, Clin. Biomech. 14 (1999) 710–716. [12] I. Pyykkö, P. Jantti, H. Aalto, Postural control in elderly subjects, Age Ageing 19 (1990) 215–221. [13] C. Quoniam, L. Hay, J.P. Roll, F. Harlay, Age effects on reflex and postural responses to propriomuscular inputs generated by tendon vibration, J. Gerontol. A. Biol. Sci. Med. Sci. 50 (1995) 155– 165. [14] S.M.P. Verschueren, S. Brumagne, S.P. Swinnen, P.J. Cordo, The effect of aging on dynamic position sense at the ankle, Behav. Brain Res. 136 (2002) 593–603. [15] N. Vuillerme, N. Teasdale, V. Nougier, The effect of expertise in gymnastics on proprioceptive sensory integration in human subjects, Neurosci. Lett. 311 (2001) 73–76. [16] N. Wijnberg, Posture in Parkinson patients: a proprioceptive problem?, in: J. Duysens, B.C.M. Smits-Engelsman, H. Kingma (Eds.), Control of Posture and Gait, Maastricht, 2001, pp. 758– 761. [17] D.A. Winter, A.E. Patla, F. Prince, M. Ishac, K. Gielo-Perczak, Stiffness control of balance in quiet standing, J. Neurophysiol. 80 (1998) 1211–1221.