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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 ity [1], suggesting that sensory deficits from either location
the proprioceptive, visual, and vestibular systems, which might result in instability. Postural instability has been ob-
the central nervous system (CNS) must weight relative to served in patients with low back pain [11] as well as in
one another depending on the immediate conditions. An im- elderly persons [12]. Patients with low back pain have also
portant property of the postural control system is its ability been attributed reduced lumbosacral proprioception [3],
to gate sensory input in accordance with the internal repre- which might be a causative factor in their instability.
sentation of the current posture, so as to avoid undesirable The study described in this paper investigated whether
responses triggered by external or internal perturbations [8]. the weighting of proprioceptive input in the back and an-
In some circumstances, it might be advantageous for the kles changes in persons with low back pain and persons
CNS to be able to reweight sensory input based on location who are elderly. Tendon and muscle vibration was used as
of origin, rather than modality. For example, if the quality an experimental probe to quantify the weighting of propri-
of input from a particular body location decreases due to oceptive input from the areas of the lumbar back and the
injury, disease, or normal aging, the CNS might increase ankles, at least as far as it influences stability during quiet
the weighting of input from other locations that provide in- standing. Vibration is a potent stimulus for muscle spindle
formation useful for maintaining a stable posture. Without Ia afferents [2], and applied to the leg muscles during quiet
spatial reweighting of sensory input, reliance on impover- standing, it can induce postural instability, sometimes to
ished input from a particular body location might lead to the point of falling (e.g., [5]). Mechanical vibrations were
loss of balance and falling. applied, during quiet standing, to the triceps surae, tibialis
Proprioceptive input from the muscles of the legs and anterior, or lumbar paraspinal muscles in young and elderly
trunk plays an important role in maintaining postural stabil- persons with low back pain (LBP) and age-matched healthy
persons during quiet standing.
Twenty young adults (10 healthy, 10 LBP; mean age
∗ Corresponding author. Tel.: +32 16 329121; fax: +32 16 329197. = 25 years) and 20 elderly persons (10 healthy, 10 LBP;
E-mail address: simon.brumagne@flok.kuleuven.ac.be (S. Brumagne). 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 ver-
tical ground reaction force (Fz ). Force plate data were sam-
pled 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 bare-
foot on the force plate with the feet separated by the width of
the hips, the arms hanging loosely at the sides. The subjects
Fig. 1. Anteroposterior sways for the four conditions and subgroups. Mean
were instructed to remain still and relaxed. Each subject was RMS values and standard deviations.
tested under four experimental conditions: (1) control (no
vibration); (2) bilateral vibration of the triceps surae ten-
dons; (3) bilateral vibration of the tibialis anterior tendons; larger than that in the young individuals (4.8 ± 2.8 cm)
and (4) bilateral vibration of the paraspinal muscle bellies. (F(1, 39) = 6.9, P < 0.05). In addition, the CoP displace-
In all four conditions, vision was occluded by means of ment in the persons with low back pain (7.0 ± 3.1 cm)
liquid-crystal goggles (Translucent Technologies, Canada). was significantly larger than that in the healthy individuals
Trials lasted 60 s. Tendon and muscle vibration (60 pps, (5.0 ± 3.0 cm) (F(1, 39) = 7.22, P < 0.05). When vibra-
≈0.5 mm) started 15 s after the start of the trial and lasted tion was applied bilaterally to the paraspinal muscles, the
for 15 s. Displacement of the center of pressure (CoP) was persons with low back pain and the elderly produced little
estimated from the force plate data using the equation: CoP or no displacement of the CoP, whereas the CoP of healthy
= Mx /Fz , and the CoP was averaged over the 15 s periods individuals were displaced anteriorly by an average of 3.5
prior to and during vibration to quantify the directional effect ± 2.4 cm (F(1, 39) = 4.23, P < 0.05) (see Fig. 2). In in-
of vibration. In control trials, the root mean square (RMS) dividuals with low back pain, both young and elderly, and
value of the CoP was also calculated to quantify the baseline in the healthy elderly as well, these differences in CoP dis-
variability in each group of subjects. Postural recovery times placement produced by vibration may reflect a refocusing of
were determined as the total time from cessation of vibra- proprioceptive control of balance away from proximal and
tion until CoP displacement of the subject was again within axial proprioception input to that derived from receptors in
the limits of two standard deviations of the mean position, the ankle muscles.
that was determined over the 15 s period prior to vibration. Following the cessation of vibration, the vibration-evoked
During all conditions, minor force variations were measured displacement of the CoP diminished over a period of
in the frontal plane. Hence, for clarity, the analysis will only time, although the length of time depended on the subject
be carried out in the sagittal plane and no data relative to group. For example, following the cessation of the triceps
the frontal plane will be given. Differences in CoP measure- surae vibration, the persons with low back pain had signif-
ments between control conditions and vibration conditions, icantly longer postural recovery times (16.2 ± 8.6 s) than
and between patient group and healthy control group, and the healthy individuals (7.9 ± 4.4 s) (F(1, 79) = 15.55, P <
between the young and elderly persons were based on F-test 0.001). When age is taken into account, the young healthy
analysis of variance, using one-way and two-way proce- persons recovered their postural stability significantly faster
dures 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 displace-
ment 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 indi-
viduals (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 Fig. 2. Anteroposterior sways for the muscle vibration conditions and
displacement in the elderly (7.2 ± 3.2 cm) was significantly subgroups. Group mean values and standard deviations.
S. Brumagne et al. / Neuroscience Letters 366 (2004) 63–66 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, per-
sons 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 an-
terior vibration induced a larger displacement of the CoP
in elderly individuals. In addition, after cessation of mus-
cle 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 interpre-
tation 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 propriocep-
Fig. 3. Anteroposterior sways of a representative healthy person (A) and tive deficits is to increase reliance on other sensory systems
a person with low back pain (B) during the vibration trials: (1) bilateral such as vision, for instance, in the control of posture [9,12].
triceps surae muscles vibration; (2) lumbar paraspinal muscles vibration;
Alternatively, individuals can shift the focus of attention
(3) bilateral tibialis anterior muscles vibration. Note the absence of postural
recovery after cessation of ankle muscles vibration in the person with from loci with deficient sensory input to others with intact
low back pain. input. The hypothesized sensory deficiency might be due to
specific proprioceptive deficits from a particular part of the
after vibration stopped (4.9 ± 1.9 s) than the elderly healthy body or to the individual’s unwillingness to move that part
persons (10.9 ± 4.1 s) (F(1, 39) = 16.93, P < 0.001). of the body, thereby generating proprioceptive information,
Fig. 3 displays the anteroposterior CoP displacement during because movement causes pain or it induces a fear of injury.
the muscle vibration conditions of a representative healthy For example, patients with LBP might stiffen the trunk
young person (panel A) compared to a representative young and pelvis and hyperextend the knees in order to decrease
person with LBP (panel B). the number of degrees of freedom. Similar observations
Healthy subjects, both young and elderly, proved sen- have been reported in deafferented patients and individuals
sitive to muscle vibration at the ankles and lumbar trunk. with Parkinson disease, who seem to stiffen their trunk and
This sensitivity manifested as a change in the average dis- pelvis, possibly to compensate for defective information
placement in the CoP away from the center of support, in about body position [16]. Fear of falling, for example, in
the forward direction to vibration of tibialis anterior and the elderly, decreases the CoP excursion due to increased
paraspinal muscles and posterior to vibration of triceps surae muscle activity and axial stiffness [4]. In patients with LBP,
muscles. Our observation that elderly healthy persons are as anteroposterior sway increases during complex conditions
sensitive to muscle vibration as young individuals are not in or tasks, but not in quiet stance [11]. In elderly individuals,
agreement with previous studies that reported little [13] or who are generally less flexible in the axial parts of the body,
no sensitivity to muscle vibration [12] in elderly persons. A the CoP moves less during quiet stance than in young adults.
possible explanation for this disparity could be that the age It can be argued that this kind of postural control strategy,
of the elderly in these previous studies was much higher i.e., inverted pendulum model of postural control [17], seems
(i.e., 82 years) than in our study. An alternative explanation to be sufficient during quiet stance, resulting sometimes
might be that only triceps surae muscles vibration was used in even a smaller CoP displacement compared to healthy
in these studies (and not tibialis anterior muscle vibration). persons, but in more complex conditions or tasks, such as
Moreover, a recent study on dynamic position sense at the unstable support surface which decreases the reliance on
ankle in elderly persons showed that the age-related de- the ankle proprioception [8], this postural control strategy
cline in position sense performance was not due to muscle seems to be inadequate resulting in postural instability and
spindle changes of tibialis anterior muscle [14]. even falls. The advantage of controlling fewer degrees of
Our results suggest that both LBP and aging alter pro- freedom is offset by loss of flexible responses to dampen
prioceptive sensitivity in different parts of the body, at least external perturbations. Instead, perturbations are transferred
66 S. Brumagne et al. / Neuroscience Letters 366 (2004) 63–66

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