Neuroscience and Biobehavioral Reviews 33 (2009) 271278

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Neuroscience and Biobehavioral Reviews

journal homepage: www.elsevier.com/locate/neubiorev

Review

Proprioceptive sensibility in the elderly:

Degeneration, functional consequences and plastic-adaptive processes
Daniel J. Goble *, James P. Coxon, Nicole Wenderoth, Annouchka Van Impe, Stephan P. Swinnen
Motor Control Laboratory, Research Center for Movement Control and Neuroplasticity, Department of Biomedical Kinesiology, Katholieke Universiteit Leuven Tervuurse Vest 101,
B-3001 Heverlee, Belgium

A R T I C L E I N F O

A B S T R A C T

Article history:
Received 11 June 2008
Received in revised form 19 August 2008
Accepted 20 August 2008

As the percentage of individuals over the age of 60 years continues to rise, determining the extent and
functional signicance of age-related declines in sensorimotor performance is of increasing importance.
This review examines the specic contribution of proprioceptive feedback to sensorimotor performance
in older adults. First, a global perspective of proprioceptive acuity is provided assimilating information
from studies where only one of several aspects of proprioceptive function (e.g. sense of position, motion
or dynamic position) was quantied, and/or a single joint or limb segment tested. Second, the
consequences of proprioceptive decits are established with particular emphasis placed on postural
control. Lastly, the potential for plastic changes in the aging proprioceptive system is highlighted,
including studies which relate physical activity to enhanced proprioceptive abilities in older adults.
Overall, this review provides a foundation for future studies regarding the proprioceptive feedback
abilities of elderly individuals. Such studies may lead to greater advances in the treatment and prevention
of the sensorimotor decits typically associated with the aging process.
2008 Elsevier Ltd. All rights reserved.

Keywords:
Proprioception
Aging
Elderly
Kinesthesis
Joint position sense
Sensorimotor function
Plasticity
Physical activity

Contents
1.
2.

3.
4.

5.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Impaired proprioceptive acuity in the elderly . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.
Position sense . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.
Motion sense . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3.
Dynamic position sense . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The consequences of proprioceptive declines in the elderly . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Degenerative and plastic-adaptive processes in the aging proprioceptive system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.
Neurophysiological mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.
Training induced plastic-adaptive changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction
Proprioception refers to the sense of knowing where ones body
is in space and is classically comprised of both static (i.e. joint
position sense) and dynamic (i.e. kinesthetic movement sense)

* Corresponding author. Fax: +32 16 329197.

E-mail address: Daniel.Goble@faber.kuleuven.be (D.J. Goble).
0149-7634/$ see front matter 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neubiorev.2008.08.012

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components (Gandevia et al., 2002). Following the early observations of Sherrington (1906), muscle spindles have been shown to
provide essential proprioceptive feedback to the central nervous
system, mediating the conscious perception of movement and limb
position (Clark et al., 1985; Gandevia et al., 1992; Goodwin et al.,
1972a; Matthews, 1982; McCloskey, 1978; Proske et al., 2000).
Sources of proprioceptive information, such as cutaneous and joint
mechanoreceptors, are also important for determining the position
of distal body segments and/or signaling extremes in range of

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motion (Collins and Prochazka, 1996; Edin, 2001; Edin and Abbs,
1991; Hulliger et al., 1979). For a recent, detailed review of
peripheral and central aspects related to proprioceptive sense see
Dijkerman and de Haan (2007).
A wealth of literature exists underscoring the importance of
proprioceptive feedback in the control of voluntary movements.
Studies detailing the consequences of large ber sensory neuropathy
have provided a clear demonstration of this showing that, when
visual feedback is unavailable, deafferented individuals have
difculties: (1) calibrating hand position in space (Teasdale et al.,
1993b), (2) sustaining constant muscle force levels/movement
amplitudes (Rothwell et al., 1982), (3) discriminating object weights
(Rothwell et al., 1982), (4) performing targeted movements (Messier
et al., 2003; Sanes et al., 1984), (5) producing coordinated gait
patterns (Lajoie et al., 1996) and (6) controlling the timing of muscle
contractions in order to compensate for the intersegmental
dynamics associated with multi-joint movement (Bard et al.,
1992; Sainburg et al., 1993, 1995). Degradation in movement
performance has also been shown in healthy young individuals
when proprioception is non-invasively perturbed through muscle
tendon vibration (Capaday and Cooke, 1981; Cody et al., 1990; Cordo
et al., 1995b; Roll and Vedel, 1982; Steyvers et al., 2001; Verschueren
and Swinnen, 2001; Verschueren et al., 1999a,b). This method
involves the transcutaneous application of high frequency, low
amplitude vibration to a target muscle in order to increase the neural
ring rate of, primarily, type 1a afferents from muscle spindles
(Bianconi and van der Meulen, 1963; Burke et al., 1976a,b). In this
way, proprioceptive feedback is altered by an inherent rise in the
baseline noise of the sensory signal provided to the central nervous
system (Bock et al., 2007; Pyykko et al., 1990; Roll et al., 1989), as
well as through induced illusions of joint position and motion that
are consistent with lengthening of the vibrated muscle (Goodwin
et al., 1972a,b; Sittig et al., 1985).
Beyond such acute disruptions of proprioception, mounting
evidence now suggests that declines in proprioceptive function
may represent a fundamental aspect of the aging process. Given
the rising proportion of individuals over 60 years of age, these
decits have, therefore, spurred increased interest in the eld of
motor neuroscience regarding the proprioceptive abilities of older
individuals, and the role of proprioceptive feedback in elderly
movement. The present review aims to (1) elucidate the acuity of
proprioceptive sense in older adults, (2) describe the functional
consequences associated with age-related proprioceptive decits
and (3) discuss the neurophysiological factors responsible for
declines in proprioception with age. In addition, several studies
demonstrating the potential for neuroplasticity in older adults are
highlighted, including studies that indicate a role for physical
activity in counteracting the effects of aging on proprioceptive
ability. Overall, this review provides a foundation for future studies
regarding the utilization of proprioceptive feedback by older
individuals. Such investigations will, hopefully, foster new
advances in the treatment/prevention of age-related sensorimotor
decits through use-dependent neuroplastic changes within the
proprioceptive system.
2. Impaired proprioceptive acuity in the elderly
While there have been a multitude of studies attempting to
quantify the acuity, or sharpness, of proprioceptive sense in older
adults, these investigations have typically been limited to either a
single body region and/or a particular type of sensory feedback (i.e.
position, motion or dynamic position sense). In the following
section, these relatively specic ndings are incorporated into a
broader framework demonstrating the extent of declines in
proprioceptive acuity for older individuals.

2.1. Position sense

The ability to sense the static position of a joint, or limb
segment, is by far the most common assessment of proprioceptive
acuity conducted in the elderly. Tests of position sense typically
focus on the accuracy by which an individual can identify and/or
match a target joint angle in the absence of vision, and are
conducted in one of two ways. First, in ipsilateral remembered
matching tasks, a subjects joint is displaced to the target position
and held for several seconds prior to being returned to its starting
angle. Next, the subject is asked to replicate the target position
with the same (ipsilateral) effector based on proprioceptive
memory. In the second type of task, contralateral concurrent
matching, a similar procedure is undertaken involving the
displacement of a joint to a target position. However, in this task,
the joint is not returned to the start angle but, rather, is left at the
target position while matching is performed with the contralateral
limb. One advantage of this latter procedure is that it avoids the
potential confound of decreased memory abilities in the elderly
(Reuter-Lorenz and Sylvester, 2005), by allowing for concurrent
proprioceptive information to be available throughout the task
from the limb remaining at the target position. On the other hand,
contralateral concurrent matching is also subject to limitation of
its own in that this task relies heavily on interhemispheric
communication. In this case, poor performance may not reect a
decit in proprioception per se but, rather, decreased integrity of
the corpus callosum, a known consequence of the aging process
(Ota et al., 2006; Salat et al., 2005).
Table 1 presents a summary of studies involving the assessment
of proprioceptive position sense for a single joint or limb segment
(Adamo et al., 2007; Barrack et al., 1983; Deshpande et al., 2003;
Hurley et al., 1998; Kaplan et al., 1985; Lord et al., 1991b, 1999;
Petrella et al., 1997; Pickard et al., 2003; Stelmach and Sirica, 1986;
Tsang and Hui-Chan, 2003, 2004; Westlake et al., 2007; You, 2005).
In this case, absolute matching errors are reported from studies
involving untrained subjects performing ipsilateral remembered
or contralateral concurrent matching tasks. This commonly
reported measure of proprioceptive acuity has been highly
successful in distinguishing differences between young and old
adults. Indeed, despite a diverse sampling of joints and body
segments and a clear bias in the literature towards studies of the
lower limb, comparisons between young and elderly subjects have,
almost unanimously, indicated a signicant deterioration of
position sense with age.
While the error values provided in Table 1 can be used as a
general guideline of elderly proprioceptive acuity, they should not
necessarily be seen as norms. This is because the magnitude of
absolute errors in position matching tasks has been shown to be
inuenced by a number of task-related factors. For example, in
studies of both young (Goble and Brown, 2008; Goble et al., 2006)
and older (Adamo et al., 2007; Stelmach and Sirica, 1986; Kaplan
et al., 1985) adults, greater errors have been found for the matching
of targets located farther from the starting joint position. In
addition, position matching ability appears to be enhanced under
weight-bearing conditions (Bullock-Saxton et al., 2001; Gilsing
et al., 1995) and when active versus passive matching occurs
(Pickard et al., 2003). For this reason, these task-related factors
have been included in Table 1 as a point of comparison.
In contrast to absolute errors, few reports of other error
measures have been made with respect to position matching tasks
in elderly subjects. Interestingly, where constant errors have been
quantied, no differences have been found between young and
older adults (Ferrell et al., 1992; Meeuwsen et al., 1993). Based on
the known relationship between absolute error, constant error and
variable error (Shultz and Roy, 1973), this observation suggests

D.J. Goble et al. / Neuroscience and Biobehavioral Reviews 33 (2009) 271278

273

Table 1
Summary of results from studies of proprioceptive position sense in the elderly
Joint/limb segment

Study

Elbow

Adamo et al. (2007)

Experimental design

Absolute error

IR/CC

Weight bearing?

Active vs. passive match

Target amp

Old

Young controls

IR

No

Active

CC

No

Active

108
308
608
108
308
608

3.38
4.68
5.58
3.88
5.18
6.68

1.68
3.38
4.08
2.28
4.58
6.08

Arm

Stelmach and Sirica (1986)b

CC

No

Active

025 cm
25.151 cm
51.177 cm

2.1 cm
2.5 cm
4.4 cm

2.1 cm
2.1 cma
2.1 cma

Hip

Pickard et al. (2003)

IR

No

Active (outer)
Active (inner)
Passive

208
208
208

2.28
1.88
2.48

2.28
1.88
2.48

Knee

Barrack et al. (1983)

Kaplan et al. (1985)

IR
CC

No
No

Active
Active

Petrella et al. (1997)

Hurley et al. (1998)
Tsang and Hui-Chan (2003)
Tsang and Hui-Chan (2004)

IR
IR
IR
IR

Yes
No
No
No

Active
Active
Passive
Passive

5258
158
308
708
10608
1908
38
38

4.68
58
58
88
4.68
2.78
4.08
3.98

3.68a
38
38
48
2.08a
1.58a
N/A
1.18a

Ankle

Deshpande et al. (2003)

You (2005)
Westlake et al. (2007)

IR
IR
IR

Yes
Yes
No

Active
Active
Passive

5, 5, 108
1378
10, 12, 158

2.38
2.68
3.28

N/A
1.48a
3.38

Toe

Lord et al. (1991a,b)

Lord et al. (1999)

CC
CC

No
No

Active
Active

Not given
Not given

2.68
1.68

N/A
N/A

Reects signicantly greater acuity in young controls versus elderly subjects (p < .05).
Results reect the constrained movement condition only. Outer = more abducted range of motion, inner = less abducted range of motion (closer to neutral),
IR = ipsilateral remembered and CC = contralateral remembered.
b

that young and old adults have similar biases (i.e. constant errors),
but differ with respect to the consistency of matching performance
(i.e. variable errors). Such enhanced variability during position
matching tasks parallels the results of several studies involving the
assessment of visually guided reaching performance. In this case,
greater variability has been reported for reaction time (Spirduso,
1975; Verhaeghen and Salthouse, 1997; Welford, 1959) and
reaching movement trajectories (Darling et al., 1989; Seidler et al.,
2002), which may indicate a reduced signal to noise ratio in older
individuals.
2.2. Motion sense
The ability to sense joint movement, known as kinesthesia, has
received less attention in the aging literature. Despite this, several
early studies of proprioceptive function demonstrated signicant
differences in motion sense between young and old by quantifying
the threshold for which passive joint movement could be
perceived. Kokmen et al. (1978) examined motion sense in 52
adults over 60 years by measuring the ability to sense progressively larger movements of the metacarpophalangeal and metatarsophalangeal joints in the absence of vision. Compared to young
adults, older subjects were less capable of sensing joint motion,
especially at lower displacement rates. Two subsequent studies
addressing decits in motion sense at the knee joint showed a
similar decline in kinesthesis with age (Barrack et al., 1983;
Skinner et al., 1984). In one of these studies (Barrack et al., 1983),
old adults were able to detect movements of only 5.98 compared to
3.88 in young adults. In the other study (Skinner et al., 1984),
regression analysis revealed that acuity declined, on average, 0.068
per year of adult life.
More recently, a baseline measure of joint motion sense was
derived from a control group of older adults in a study addressing

the role of physical activity type on proprioception (Xu et al., 2004).

Subjects were asked to press a hand switch when they felt exion/
extension of the knee or dorsiexion/plantarexion of the ankle. In
this case, the threshold for detecting passive motion of the knee
was found to differ depending on the direction of joint displacement. Specically, older adults could distinguish signicantly
smaller knee movements in the exion (1.18) versus extension
(1.78) direction. In contrast, motion detection sense at the ankle
did not differ based on direction of joint displacement, with a mean
acuity of 1.28. These results further highlight the need to consider
both the joint of interest, and direction of motion, when assessing
motion sense in the elderly.
A different approach to the assessment of proprioceptively
based motion sense was used by Westlake et al. (2007) in a study
regarding the effects of balance training on proprioception in the
elderly. In addition to the traditional method of joint motion sense
assessment, where subjects pressed a response button when ankle
joint movement is perceived, this study also examined the
discrimination of passive ankle displacements at different speeds.
In particular, the threshold for motion sense was determined as the
smallest difference between pairs of movements that yielded three
correct responses. It was shown that the elderly individuals could
discriminate, on average, between ankle rotation speeds as small
as 1.38/s. This value was signicantly smaller than that found using
the traditional method of threshold motion detection (2.18) and,
therefore, it was concluded that tests of velocity discrimination
might be more sensitive in determining kinesthetic acuity.
2.3. Dynamic position sense
Although the base components of proprioceptive function are
position and motion sense, it is often necessary to coordinate these
types of information during complex sensorimotor tasks. For

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D.J. Goble et al. / Neuroscience and Biobehavioral Reviews 33 (2009) 271278

example, during an activity such as placing a tea cup on a saucer,

proprioceptive monitoring of both the speed and position of the
shoulder, elbow and wrist joints is necessary. This ability to
monitor position during motion has been termed dynamic
position sense and has been assessed thoroughly in healthy
young individuals using a task involving opening the hand when
the elbow joint rotates through a predetermined target position at
a particular velocity (Bevan et al., 1994; Cordo et al., 1994, 1995a,b;
Cordo, 1990).
With respect to older adults, Verschueren et al. (2002) were the
rst to quantify the acuity of dynamic position sense. Male
participants (n = 102) between the ages of 55 and 75 years had
their ankle passively displaced. During displacement, subjects
were asked to monitor the position of the moving joint and to
briskly open their hand when they felt their ankle at a joint angle of
108 plantarexion. The speed at which the joint was rotated was
varied in order to minimize the use of temporal cues. It was shown
that the mean acuity of dynamic ankle position sense was 2.78 for
older adults regardless of the speed at which the ankle joint was
moving. Performance was signicantly less than young controls
(2.28), primarily due to greater variability in the elderly subjects.
This study also included a muscle tendon vibration condition,
where tibialis anterior was vibrated during passive ankle rotation.
Interestingly, this perturbation affected the elderly to a lesser
degree than young subjects, indicating that decits in dynamic
position sense with age are not due solely to degradation in muscle
spindle feedback, but also altered feedback from sources such as
joint or skin receptors.
Using similar methods, Madhavan and Shields (2005) also
assessed the acuity of dynamic position sense at the ankle. In this
study, individuals over the age of 60 years were subjected to a
greater range of ankle movement speeds while electromyographic
measures of dorsi/plantarexor muscle activity were recorded.
The results of this study, in contrast to Verschueren et al. (2002),
showed that the acuity of dynamic position sense was signicantly inuenced by the speed of joint movement. Comparable
absolute errors to Verschueren et al. (2002) were seen during the
slower movement speeds (10408/s), but larger errors (468)
were reported for faster movement s between 50 and 908/s.
Even though the ankle joint was passively displaced in this
experiment by a motorized system, elderly subjects co-contracted
dorsiexors and plantarexors during the task. This result may
reect an attempt by older adults to increase muscle spindle
feedback gain to compensate for degradation in proprioceptive
signaling mechanisms.
3. The consequences of proprioceptive declines in the elderly
In light of the declines in proprioceptive acuity outlined above,
several researchers have sought to determine the extent to which a
relationship exists between decits in proprioceptive function and
sensorimotor performance in the elderly. Postural control is one
area of the literature where this has been of particular interest,
with a large amount of attention being focused on the task of
maintaining balance/stability during upright stance. This task,
which involves keeping the center of gravity over the base of
support (for review see Horak et al., 1989), has likely been of
interest for two reasons. First, proprioception is known to be a
critical source of sensory feedback for the preservation of balance
during upright standing regardless of age (Diener et al., 1984;
Fitzpatrick and McCloskey, 1994; Fitzpatrick et al., 1994). Second,
balance tasks have proven to be sensitive to manipulations of
proprioceptive feedback in elderly individuals. In particular,
increased instability in older adults has been demonstrated in
response to such perturbations as muscle tendon vibration (Hay

et al., 1996; Teasdale and Simoneau, 2001), unexpected movements of the support surface (Manchester et al., 1989; Woollacott
et al., 1986), and platform-based sway referencing (Camicioli et al.,
1997; Cohen et al., 1996; Doumas et al., 2008; Forth et al., 2007;
Speers et al., 2002).
The rst known study to demonstrate a link between
proprioceptive acuity in the elderly and performance on balance
tasks was conducted by Lord et al. (1991b). In this study of 95 older
adults, a signicant relationship was found between toe position
acuity and the magnitude of subject sway. Individuals with poor
proprioception showed larger sway in the anteriorposterior
direction, regardless of whether the task was performed with/
without vision or on a compliant surface with eyes open. This study
also assessed two clinical measures of balance dealing with the
static and dynamic aspects of stability. In the static task, the length
of time subjects could maintain upright stance in foam and no
foam conditions was measured, while the dynamic task involved
walking on the spot with eyes closed for 1 min. Performances on
both these tasks were positively correlated with proprioceptive
acuity. Taken together, these results show that proprioceptive
information is vital for postural control in the elderly.
The relationship between lateral stability during standing and
proprioception has also been examined in the elderly (Lord et al.,
1999). Male and female subjects (n = 156) aged between 63 and 90
years were tested on a modied version of the tandem stance
stability test. This test involved standing with one foot in front of
the other (and slightly to the side) for 30 s with or without visual
feedback. While all subjects could perform the task with vision,
closing the eyes resulted in increased lateral sway and forced many
older adults to take a step in order to prevent falling. These
measures of balance were subsequently found to be positively
correlated with lower limb proprioceptive acuity, as indicated by
toe position matching error. Further, when correlated with the selfreported occurrence of falls over the previous 12 months,
proprioceptive function signicantly predicted the total number
of falls experienced. This nding has particular relevance given the
physical and nancial costs associated with falls in the elderly
(Burt and Fingerhut, 1998; Hirsch et al., 1990; Tinetti et al., 1988)
and is in line with other reports linking proprioception and falls
(Lord et al., 1991a; Sorock and Labiner, 1992).
Unlike the studies of Lord et al. (1991b, 1999), where
proprioceptive function was measured through a somewhat crude
toe position matching test, McChesney and Woollacott (2000)
determined the threshold joint position sense for both the knee
and ankle joints. In this case, the minimum amount of knee exion/
extension and ankle dorsiexion/plantarexion that elderly
subjects could perceive was determined. Participants were
separated into groups with high and low proprioceptive acuity
and center of pressure variability was measured with eyes open
and eyes closed. It was shown that older adults with very poor
proprioception of the knee and ankle joints had signicantly worse
balance than those individuals with very good proprioception.
Interestingly, however, the use of electromyography to determine
muscle responses to unexpected movements of the support surface
did not reveal any group differences. This nding suggests that the
relationship between joint position sense and postural stability
may be specic to the task of maintaining quiet stance, rather than
dynamically recovering from a balance perturbation.
Beyond studies assessing balance/stability, at least one study
has compared proprioceptive acuity with activities of daily living
in the elderly. In this study, Hurley et al. (1998) assessed
proprioceptive acuity and timed measures of functional performance in a sample of young (mean age = 23 years), middle aged,
(mean age = 56 years) and old (mean age = 72 years) individuals.
Proprioceptive acuity of the knee joint was assessed with an

D.J. Goble et al. / Neuroscience and Biobehavioral Reviews 33 (2009) 271278

ipsilateral remembered matching task, while functional performance was dened as the aggregate amount of time required to (1)
walk 15.5 m, (2) get out of a chair and walk 15.5 m, (3) ascend 11
stairs and (4) descend 11 stairs. Although no signicant differences
were found between middle-aged and young subjects on either the
proprioceptive or functional tasks, old subjects were signicantly
worse than both younger age groups in all cases. More importantly,
performance on functional tasks was signicantly correlated with
knee position acuity in the elderly. This may have implications for
clinical settings, where knee position sense tests may be predictive
of overall sensorimotor ability in the elderly.
When assessing the impact of proprioceptive decits in the
elderly on sensorimotor performance, it is also important to
consider biomechanical factors/body anthropometrics. For example, in a study by You (2005) the acuity of ankle joint position sense
for elderly individuals was found to be approximately 2.68. While
this value may seem insignicant, simple body-geometry dictates
otherwise. If one considers the human body as an inverted
pendulum rotating about the ankle during quiet stance with a
center of mass approximately 1 m above the ankles, a 2.68 error at
the ankle can translate into as much as 4.5 cm center of mass
excursion. This amount of displacement will certainly impact
whole body balance and stability. Similarly, in the upper limb,
Adamo et al. (2007) calculated matching errors across all tasks to
be on average 5.78 in magnitude. Given that the adult forearmhand link is approximately 44 cm in length (Chafn and Anderson,
1999), this degree of inaccuracy could lead to as much as a 4.4-cm
endpoint error at the ngertip in situations where vision is not
available.
4. Degenerative and plastic-adaptive processes in the aging
proprioceptive system
While early investigations focused largely on the extent and
functional signicance of age-related declines in proprioceptive
sense, the past decade has seen increased efforts to determine the
mechanisms by which these decits occur and how they might be
prevented through training interventions.
4.1. Neurophysiological mechanisms
Research concerning the neurophysiological basis of agerelated declines in proprioception has involved both central and
peripheral nervous system changes. In the peripheral nervous
system, a myriad of changes occur with age at the level of the
individual proprioceptors (see Shaffer and Harrison, 2007 for
review). Briey, human and animal work involving aged muscle
spindles has shown: (1) increased capsular thickness (Swash
and Fox, 1972), (2) decreased spindle diameter (Kararizou et al.,
2005), (3) decreased sensitivity (Burke et al., 1996; Kim et al.,
2007; Miwa et al., 1995), (4) a fewer total number of intrafusal
bers (Liu et al., 2005; Swash and Fox, 1972) and (5) axonal
swelling/expanded motor endplates (Swash and Fox, 1972) that
may be the result of denervation (Jennekens et al., 1972; Lexell
and Downham, 1992; Liu et al., 2005). In addition, cutaneous
mechanoreceptors such as the Meissner and Pacinian type
corpuscles are altered, showing a decreased number and mean
density of receptors per unit of skin area (Bolton et al., 1966;
Bruce, 1980; Iwasaki et al., 2003). Furthermore, a decline in the
number of joint mechanoreceptors is experienced with age,
especially for Rufni, Pacinian and Golgi-tendon type receptors
(Aydog et al., 2006; Morisawa, 1998). Taken together, these
peripheral changes are a potential source of proprioceptive
decits in the elderly, although no direct correlation with tests
of proprioceptive acuity has been made.

275

Beyond these peripheral alterations, declines in proprioceptive

function are also thought to be a result of changes in the central
nervous system. Indeed, inadequate processing of proprioceptive
feedback has been inferred from various behavioral studies of older
adults. For example, in accordance with studies conducted in
children and young adults (Goble and Brown, 2007; Goble et al.,
2005), Adamo et al. (2007) compared three position matching tasks
of varying processing demands in 12 healthy older adults (mean
age = 75 years). In the rst task, subjects matched elbow
displacement based largely on proprioceptive memory (ipsilateral
remembered matching). Second, subjects performed contralateral
concurrent elbow position matching, which did not require
memory but induced a greater reliance on interhemispheric
transfer. Lastly, a contralateral remembered matching task was
utilized combining the main processing demands of the previous
two tasks. It was found that joint position errors were systematically modulated by the amount of proprioceptive feedback
processing required. When tasks involved only memory or only
interhemispheric transfer of proprioceptive information, no
signicant differences in matching accuracy were seen in elderly
subjects. In contrast, the more difcult contralateral remembered
task resulted in errors that were on average 238 larger than in
either of the two less difcult conditions. As both memory and
interhemispheric transfer were necessary for this task, it was
concluded that increased proprioceptive processing demands
signicantly impacted the assessment of acuity in the elderly.
Decreased attentional resources may also contribute to the
diminished proprioceptive abilities of elderly individuals. Indirect
evidence for this comes from studies demonstrating a decline in
postural stability when older adults are faced with dual-task
situations (Doumas et al., 2008; Stelmach et al., 1990; Teasdale
et al., 1993a; Teasdale and Simoneau, 2001; Westlake and Culham,
2007). For example, Doumas et al. (2008), tested upright stance in
older adults (mean age = 71.0 years) during a concurrent n-back
working memory task. With vision, and a xed support surface,
postural sway increased when attention was divided. However,
participants were still able to perform the cognitive task at an
optimal level. In contrast, when the quality of proprioceptive
feedback was reduced through platform-based sway referencing,
elderly subjects sacriced performance on the working memory
task in favour of maintaining postural stability. This result
demonstrates that older adults perform balance tasks with less
automaticity than younger adults when placed in compromised
proprioceptive feedback conditions. Thus, greater attentional
resources are devoted to the task of maintaining balance, which
may be at the expense of other cognitive processes.
Another indication that cognitive processes inuence proprioceptive abilities of older adults follows from studies assessing
reintegration of proprioceptive feedback (Hay et al., 1996;
Teasdale and Simoneau, 2001). In these studies, the quality of
proprioceptive information provided during quiet stance was
transiently manipulated by vibrating the soleus and tibialis
anterior muscles for a number of seconds. As expected, when
proprioceptive information was degraded by vibration, old
subjects showed increased sway parameters indicating a decrease
in overall stability. Interestingly, when proprioceptive feedback
was restored by removing the vibratory stimulus, older individuals
remained unstable relative to the pre-perturbation level of
performance. This suggests that, even when proprioceptive inputs
to the central nervous system are adequate, older adults may be
limited by a diminished capacity for central integration and
reweighing of proprioceptive information.
While the above behavioral results are suggestive of age-related
central processing decits related to proprioceptive feedback,
there has been little attempt in the literature to determine the

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D.J. Goble et al. / Neuroscience and Biobehavioral Reviews 33 (2009) 271278

neural correlates associated with such deciencies. This is despite

numerous reports demonstrating a general loss of neural substrate
with age (for review see Raz and Rodrigue, 2006), including reports
of decreased grey matter in postcentral gyrus, site of the primary
somatosensory cortex (Good et al., 2001; Quiton et al., 2007). With
respect to this key proprioceptive area, further insight regarding
age-related changes comes from animal research where electrophysiological recordings and optical imaging have been used (Coq
and Xerri, 2000, 2001; Godde et al., 2002; Spengler et al., 1995).
These studies have shown that the amount of primary somatosensory cortex devoted to, especially, the hindlimb of older rats is
signicantly reduced by the aging process. In contrast, in humans,
research investigating handfoot interlimb coordination in an
fMRI environment has revealed an extended network of neural
activation in elderly individuals (particularly more successful
ones), which includes secondary somatosensory area as well as
other potential sensory integration areas located in, for example,
superior temporal and supramarginal gyri (Heuninckx et al., 2005,
2008a,b). This increased brain activation may reect a greater need
for proprioceptive monitoring and/or sensorimotor integration in
older versus younger individuals.
4.2. Training induced plastic-adaptive changes
A question of critical importance is, to what extent are the
proprioceptive abilities of elderly individuals subject to neuroplastic changes? Certainly, in young individuals, there is evidence
to suggest that acute and chronic adaptations can occur at the level
of the muscle proprioceptors in response to greater use (see Hutton
and Atwater, 1992 for review). Such changes can be either basal
metabolic or structural in nature and largely result in enhanced
proprioceptive output gains. Further, an increase in the cortical
representation of sensory hand maps has been reported in young
adults following training on somatosensory tasks such as Braille
reading (Pascual-Leone and Torres, 1993) and following coactivation of adjacent cutaneous receptors over a prolonged (3 h) period
of time (Pleger et al., 2003). While these results are not specic to
elderly individuals per se, it seems likely that similar plastic
changes would occur with training in older adults.
Physical activity is a potent stimulus for sensorimotor
reorganization, a phenomenon which has recently began to be
exploited in several studies assessing the efcacy of training-based
interventions on the preservation and/or improvement of proprioceptive function in the elderly. These studies can be placed into
two categories based on the type of experimental design employed
by the researchers. One common approach has been to use a crosssectional design whereby elderly individuals from different
physical activity groups are compared on some test of proprioceptive function. In an relatively early attempt to apply this
method, Petrella et al. (1997) performed a comparison of knee joint
position sense in active versus sedentary elderly, as determined by
measures of peak oxygen consumption level and maximal heart
rate during exercise. Based on this paradigm, proprioceptive acuity
was shown to be signicantly enhanced in the group of active
elderly individuals.
In contrast to the results of Petrella et al. (1997), however, more
recent studies have shown that improvements in elderly
proprioception may be specic to the type of physical training
undertaken (Tsang and Hui-Chan, 2003, 2004; Xu et al., 2004). One
activity that has shown a strong relationship with proprioceptive
ability is the traditional Chinese exercisetai chi, which involves
slow movements and continuous monitoring of body position. Tai
chi has been related to increased joint position sense (Tsang and
Hui-Chan, 2003, 2004) and an enhanced threshold for detecting
joint motion in the elderly (Xu et al., 2004). Similarly, proprio-

ceptive benets have been reported for joint position sense in older
individuals who practice golf, a sport that requires precise
movement and balance control (Tsang and Hui-Chan, 2004). On
the other hand, individuals engaged in more gross motor tasks (i.e.
swimming and running) that may not be as proprioceptive
feedback-dependent, were not shown to have a decreased
threshold for detecting joint motion (Xu et al., 2004).
Caution should be taken when interpreting the results from
cross-sectional studies, as increased proprioceptive acuity in older
adults who engage in certain sports/activities does not necessarily
prove that the activity enhanced or improved proprioception.
Rather, it might simply be that older adults with better
proprioceptive acuity are more successful at golf, for example,
and therefore are more likely to engage in this activity. An
alternative approach to determine the effects of exercise on
proprioceptive ability in the elderly is that of more longitudinal,
intervention-based studies. To date, there are two known
investigations that have used this design, with both showing
some benet of balance-related exercises on proprioceptive
function. Waddington and Adams (2004) tested the effect of 5
weeks wobble board training on ankle movement discrimination
in 20 community dwelling elderly. Compared to untrained
subjects, individuals who trained proprioception on the wobble
board were able to sense signicantly smaller amounts of ankle
inversion. In the second, more detailed, study, Westlake et al.
(2007) divided elderly subjects into either an active balance
exercise group or a more passive falls education group. The balance
exercise group attended classes three times a week for 8 weeks
that emphasized static and dynamic balance exercises. In contrast,
falls education involved a 1-h lecture on falls prevention once per
week for 8 weeks. Three measures of proprioceptive function were
taken pre- and post-intervention. A signicant increase in
proprioceptive ability for the balance exercise group was found,
but only for the threshold velocity detection measure. These
results, taken together, provide encouragement for future proprioceptive-based training interventions in the elderly. Further,
they underscore the need to explore other, perhaps more
proprioceptive feedback-specic interventions, as well as to assess
long-term maintenance of any improvements through an adequate
follow-up.
5. Conclusion
The purpose of the present review was to summarize the
current state of knowledge regarding age-related proprioception
research. It has been shown that proprioceptive decits in position
and motion sense clearly exist for the elderly and that these agerelated declines impact sensorimotor tasks such as balance.
Degenerative changes in the peripheral nervous system, as well
as decreases in central processing abilities, likely serve as comechanisms for such changes in function. Given the mounting
evidence that proprioceptive acuity can be improved through
training-based interventions, however, a major challenge for the
future will be to more adequately determine the peripheral and
central contributions to age-related proprioceptive decits. This
will likely require the combination of well established behavioral
protocols with more advanced techniques such as neural recording
and brain imaging and may ultimately lead to the development
more effective neurorehabilitation strategies to enhance the
sensorimotor abilities of elderly individuals.
Acknowledgements
Support for this study was provided through grants from the
Research Council of K.U. Leuven, Belgium (OT/07/073) and the

D.J. Goble et al. / Neuroscience and Biobehavioral Reviews 33 (2009) 271278

Flanders Fund for Scientic Research (G.0292.05 & G.0593.08).

Post-doctoral funding from the above sources was also obtained by
D. Goble (GP00408N & F/07/063) and J. Coxon (GP00608N & F/07/
064). Special thanks to M. Doumas for scholarly input into this
project.
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