Neuroscience and Biobehavioral Reviews 33 (2009) 271–278Contents lists available at ScienceDirect 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 significance of age-related declines in sensorimotor performance is of increasing importance. This review examines the specific 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 quantified, and/or a single joint or limb segment tested. Second, the consequences of proprioceptive deficits 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 deficits typically associated with the aging process. ß 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 one’s 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:
[email protected] (D.J. Goble). 0149-7634/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.neubiorev.2008.08.012 271 272 272 273 273 274 275 275 276 276 276 277 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 1976a.. 2007.. of proprioceptive sense in older adults.. Gilsing et al. and are conducted in one of two ways.. Meeuwsen et al. these investigations have typically been limited to either a single body region and/or a particular type of sensory feedback (i. 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. 1996. contralateral concurrent matching is also subject to limitation of its own in that this task relies heavily on interhemispheric communication. In the second type of task. Kaplan et al. indicated a significant deterioration of position sense with age. (2) sustaining constant muscle force levels/movement amplitudes (Rothwell et al. In this case. 2007.. decreased integrity of the corpus callosum. In this way. On the other hand. Edin and Abbs. 2001. 1990. 1982). by allowing for concurrent proprioceptive information to be available throughout the task from the limb remaining at the target position.. this review provides a foundation for future studies regarding the utilization of proprioceptive feedback by older individuals. 2003). 1986. 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. 2005).. Verschueren et al. Given the rising proportion of individuals over 60 years of age. Tsang and Hui-Chan. the subject is asked to replicate the target position with the same (ipsilateral) effector based on proprioceptive memory. ‘‘deafferented’’ individuals have difficulties: (1) calibrating hand position in space (Teasdale et al. several studies demonstrating the potential for neuroplasticity in older adults are highlighted. 1982). where constant errors have been quantified.. Edin. this observation suggests . when visual feedback is unavailable. Stelmach and Sirica. comparisons between young and elderly subjects have. Such investigations will. Impaired proprioceptive acuity in the elderly While there have been a multitude of studies attempting to quantify the acuity. low amplitude vibration to a target muscle in order to increase the neural firing rate of. therefore. 1984). Pyykko¨ et al. 1981. 2001.. 2. 1972a. in this task.b. 1963. Roll et al. few reports of other error measures have been made with respect to position matching tasks in elderly subjects. However. 1991b. Overall.. 2005). Interestingly. You. / Neuroscience and Biobehavioral Reviews 33 (2009) 271–278 motion (Collins and Prochazka. Barrack et al. (2) describe the functional consequences associated with age-related proprioceptive deficits and (3) discuss the neurophysiological factors responsible for declines in proprioception with age. In contrast to absolute errors. 2007.. 1995).... foster new advances in the treatment/prevention of age-related sensorimotor deficits through use-dependent neuroplastic changes within the proprioceptive system. rather. 1992. 1973). Hurley et al. 1995b. hopefully.. a subject’s joint is displaced to the target position and held for several seconds prior to being returned to its starting angle. Table 1 presents a summary of studies involving the assessment of proprioceptive position sense for a single joint or limb segment (Adamo et al. Next. 1985).1. spurred increased interest in the field of motor neuroscience regarding the proprioceptive abilities of older individuals. primarily.e.. 2001. 1993b). While the error values provided in Table 1 can be used as a general guideline of elderly proprioceptive acuity.. no differences have been found between young and older adults (Ferrell et al. 2003. motion or dynamic position sense). 1989). position matching ability appears to be enhanced under weight-bearing conditions (Bullock-Saxton et al.. in ipsilateral remembered matching tasks. In addition. 1983. 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. Studies detailing the consequences of large fiber sensory neuropathy have provided a clear demonstration of this showing that. In addition. 1998. For a recent.. Salat et al.. 2. This is because the magnitude of absolute errors in position matching tasks has been shown to be influenced by a number of task-related factors. Verschueren and Swinnen.. Sanes et al. Lord et al.. For example. 2001. 1979). including studies that indicate a role for physical activity in counteracting the effects of aging on proprioceptive ability. contralateral concurrent matching. Cordo et al. rather. Cody et al. Beyond such acute disruptions of proprioception. 2005).. Goble et al. is left at the target position while matching is performed with the contralateral limb. poor performance may not reflect a deficit in proprioception per se but. these task-related factors have been included in Table 1 as a point of comparison. For this reason. 1990. Sittig et al.. Sainburg et al.. 2003. 1993).. Steyvers et al. these deficits have. Indeed.. 1982. (5) producing coordinated gait patterns (Lajoie et al. mounting evidence now suggests that declines in proprioceptive function may represent a fundamental aspect of the aging process. constant error and variable error (Shultz and Roy. First. 2007. or limb segment. 1999a. these relatively specific findings are incorporated into a broader framework demonstrating the extent of declines in proprioceptive acuity for older individuals. the joint is not returned to the start angle but. 2003. The present review aims to (1) elucidate the acuity of proprioceptive sense in older adults. (4) performing targeted movements (Messier et al. 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. A wealth of literature exists underscoring the importance of proprioceptive feedback in the control of voluntary movements. a similar procedure is undertaken involving the displacement of a joint to a target position. In this case. 1991.b). type 1a afferents from muscle spindles (Bianconi and van der Meulen.. 1985. and the role of proprioceptive feedback in elderly movement. a known consequence of the aging process (Ota et al. Position sense The ability to sense the static position of a joint.. despite a diverse sampling of joints and body segments and a clear bias in the literature towards studies of the lower limb.. 1993. 2006. Westlake et al. 1999. One advantage of this latter procedure is that it avoids the potential confound of decreased memory abilities in the elderly (Reuter-Lorenz and Sylvester. Stelmach and Sirica. 1985) adults. 1992. 2006) and older (Adamo et al. 1997.b). Hulliger et al.. greater errors have been found for the matching of targets located farther from the starting joint position. almost unanimously. This commonly reported measure of proprioceptive acuity has been highly successful in distinguishing differences between young and old adults. (3) discriminating object weights (Rothwell et al. 1986. Deshpande et al. 2003.J. Kaplan et al. Based on the known relationship between absolute error.. detailed review of peripheral and central aspects related to proprioceptive sense see Dijkerman and de Haan (2007). position. as well as through induced illusions of joint position and motion that are consistent with lengthening of the vibrated muscle (Goodwin et al.. This method involves the transcutaneous application of high frequency. Burke et al.. they should not necessarily be seen as ‘‘norms’’. or ‘‘sharpness’’. 1995) and when active versus passive matching occurs (Pickard et al.272 D. 2008. absolute matching errors are reported from studies involving untrained subjects performing ipsilateral remembered or contralateral concurrent matching tasks... In the following section.. Petrella et al. in studies of both young (Goble and Brown. Goble et al. 2004. Pickard et al. Roll and Vedel.. is by far the most common assessment of proprioceptive acuity conducted in the elderly. 4 cm 2.e. These results further highlight the need to consider both the joint of interest. especially at lower displacement rates.98 3.58a N/A 1.. (2007) in a study regarding the effects of balance training on proprioception in the elderly. (1983) Kaplan et al. Kokmen et al.08 2. 1959) and reaching movement trajectories (Darling et al. 1984). 108 1–378 10. Verhaeghen and Salthouse. when assessing motion sense in the elderly.68 N/A N/A a Reflects significantly greater acuity in young controls versus elderly subjects (p < . 2002).88 2.38/s. 1983. inner = less abducted range of motion (closer to neutral).38 4. Welford. Skinner et al. it is often necessary to coordinate these types of information during complex sensorimotor tasks. (2003) IR No Active (outer) Active (inner) Passive 208 208 208 2. on average.. 1984).98 compared to 3.D. / Neuroscience and Biobehavioral Reviews 33 (2009) 271–278 273 Table 1 Summary of results from studies of proprioceptive position sense in the elderly Joint/limb segment Study Elbow Adamo et al. greater variability has been reported for reaction time (Spirduso. In the other study (Skinner et al.38 Toe Lord et al. old adults were able to detect movements of only 5. several early studies of proprioceptive function demonstrated significant differences in motion sense between young and old by quantifying the threshold for which passive joint movement could be perceived.48 Knee Barrack et al.78 4.5 cm 4. Subjects were asked to press a hand switch when they felt flexion/ extension of the knee or dorsiflexion/plantarflexion of the ankle. For . In contrast.88 in young adults. Such enhanced variability during position matching tasks parallels the results of several studies involving the assessment of visually guided reaching performance.68 1.38 4. In particular.e.78) direction. 1983). older adults could distinguish significantly smaller knee movements in the flexion (1.2. 1989. 5.68 2. In addition to the traditional method of joint motion sense assessment. Two subsequent studies addressing deficits in motion sense at the knee joint showed a similar decline in kinesthesis with age (Barrack et al.38 2. known as kinesthesia. (1999) CC CC No No Active Active Not given Not given 2. on average.08 3.18a Ankle Deshpande et al.. constant errors).28 1. Compared to young adults. regression analysis revealed that acuity declined. (1997) Hurley et al.28.068 per year of adult life. which may indicate a reduced signal to noise ratio in older individuals. 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.28 N/A 1. Outer = more abducted range of motion.28 1. 2. therefore. In one of these studies (Barrack et al.05). where subjects pressed a response button when ankle joint movement is perceived.68 1. Results reflect the constrained movement condition only. In this case. variable errors). it was concluded that tests of velocity discrimination might be more sensitive in determining kinesthetic acuity. Dynamic position sense Although the base components of proprioceptive function are position and motion sense.08 Arm Stelmach and Sirica (1986)b CC No Active 0–25 cm 25. and direction of motion. More recently. older subjects were less capable of sensing joint motion.48 2.J. 1975.18 6. with a mean acuity of 1.58 3. between ankle rotation speeds as small as 1. Motion sense The ability to sense joint movement.1–77 cm 2. (1991a.. motion detection sense at the ankle did not differ based on direction of joint displacement.08a 1. (2007) Experimental design Absolute error IR/CC Weight bearing? Active vs. Despite this. In this case.1 cma 2. Goble et al. but differ with respect to the consistency of matching performance (i. Seidler et al.3. 2004). (2007) IR IR IR Yes Yes No Active Active Passive 5. the threshold for detecting passive motion of the knee was found to differ depending on the direction of joint displacement.. 12.88 5. 158 2. A different approach to the assessment of proprioceptively based motion sense was used by Westlake et al.68 3.b) Lord et al.1 cm 2.88 2. has received less attention in the aging literature. (1998) Tsang and Hui-Chan (2003) Tsang and Hui-Chan (2004) IR IR IR IR Yes No No No Active Active Passive Passive 5–258 158 308 708 10–608 1–908 38 38 4.68a 38 38 48 2.58 6. 1997. (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. the threshold for motion sense was determined as the smallest difference between pairs of movements that yielded three correct responses.68 5. (2003) You (2005) Westlake et al.18) and.68 3.1 cm 2. this study also examined the discrimination of passive ankle displacements at different speeds.48a 3. 2..18) versus extension (1. 0.1–51 cm 51.. b that young and old adults have similar biases (i. Specifically.68 58 58 88 4.28 4. This value was significantly smaller than that found using the traditional method of threshold motion detection (2. (1985) IR CC No No Active Active Petrella et al.1 cma Hip Pickard et al. It was shown that the elderly individuals could discriminate. IR = ipsilateral remembered and CC = contralateral remembered. passive match Target amp Old Young controls IR No Active CC No Active 108 308 608 108 308 608 3. but larger errors (4–68) were reported for faster movement s between 50 and 908/s. 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. Proprioceptive acuity of the knee joint was assessed with an . several researchers have sought to determine the extent to which a relationship exists between deficits in proprioceptive function and sensorimotor performance in the elderly.274 D. This study also included a muscle tendon vibration condition. 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 plantarflexion.. 1999).. Cordo et al. has likely been of interest for two reasons. where proprioceptive function was measured through a somewhat crude toe position matching test. Male participants (n = 102) between the ages of 55 and 75 years had their ankle passively displaced. but also altered feedback from sources such as joint or skin receptors. during an activity such as placing a tea cup on a saucer. Hurley et al. (1991b).. Performances on both these tasks were positively correlated with proprioceptive acuity. 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. which involves keeping the center of gravity over the base of support (for review see Horak et al. The speed at which the joint was rotated was varied in order to minimize the use of temporal cues.b. Male and female subjects (n = 156) aged between 63 and 90 years were tested on a modified version of the tandem stance stability test. 1988) and is in line with other reports linking proprioception and falls (Lord et al. With respect to older adults. 1986).78 for older adults regardless of the speed at which the ankle joint was moving. In this study. proprioceptive monitoring of both the speed and position of the shoulder. In this study. balance tasks have proven to be sensitive to manipulations of proprioceptive feedback in elderly individuals. 1992). Fitzpatrick et al. (2002) were the first to quantify the acuity of dynamic position sense. 1997.J. 1990. at least one study has compared proprioceptive acuity with activities of daily living in the elderly. During displacement. indicating that deficits in dynamic position sense with age are not due solely to degradation in muscle spindle feedback. 1998. 1984. 1989.. 1989). Beyond studies assessing balance/stability. 1996. 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. showed that the acuity of dynamic position sense was significantly influenced by the speed of joint movement. Using similar methods. Tinetti et al. 1991a. While all subjects could perform the task with vision. The results of this study.. unexpected movements of the support surface (Manchester et al.28). It was shown that older adults with very poor proprioception of the knee and ankle joints had significantly worse balance than those individuals with very good proprioception. Goble et al. In this case. 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. (1991b. where tibialis anterior was vibrated during passive ankle rotation. 1994. 1996. Cohen et al. closing the eyes resulted in increased lateral sway and forced many older adults to take a step in order to prevent falling. the use of electromyography to determine muscle responses to unexpected movements of the support surface did not reveal any group differences. This finding suggests that the relationship between joint position sense and postural stability may be specific to the task of maintaining quiet stance. Forth et al.. proprioceptive function significantly predicted the total number of falls experienced.. The first known study to demonstrate a link between proprioceptive acuity in the elderly and performance on balance tasks was conducted by Lord et al. In the static task. and platform-based sway referencing (Camicioli et al. (mean age = 56 years) and old (mean age = 72 years) individuals. / Neuroscience and Biobehavioral Reviews 33 (2009) 271–278 example.. Even though the ankle joint was ‘‘passively’’ displaced in this experiment by a motorized system.. Verschueren et al. Interestingly. 1995a. individuals over the age of 60 years were subjected to a greater range of ankle movement speeds while electromyographic measures of dorsi/plantarflexor muscle activity were recorded. In particular. Participants were separated into groups with high and low proprioceptive acuity and center of pressure variability was measured with eyes open and eyes closed. this perturbation affected the elderly to a lesser degree than young subjects. 1994. Fitzpatrick and McCloskey. Performance was significantly less than young controls (2. This result may reflect an attempt by older adults to increase muscle spindle feedback gain to compensate for degradation in proprioceptive signaling mechanisms. elderly subjects co-contracted dorsiflexors and plantarflexors during the task. The consequences of proprioceptive declines in the elderly In light of the declines in proprioceptive acuity outlined above. 2002). with a large amount of attention being focused on the task of maintaining balance/stability during upright stance. 1994. This study also assessed two clinical measures of balance dealing with the static and dynamic aspects of stability.. the minimum amount of knee flexion/ extension and ankle dorsiflexion/plantarflexion that elderly subjects could perceive was determined. Further. (1998) assessed proprioceptive acuity and timed measures of functional performance in a sample of young (mean age = 23 years).. This task. primarily due to greater variability in the elderly subjects. increased instability in older adults has been demonstrated in response to such perturbations as muscle tendon vibration (Hay et al. elbow and wrist joints is necessary. 2008.. middle aged. 2007.. (2002). in contrast to Verschueren et al. Interestingly. Cordo. (2002) were seen during the slower movement speeds (10–408/s). regardless of whether the task was performed with/ without vision or on a compliant surface with eyes open. Taken together. 1990). as indicated by toe position matching error. the length of time subjects could maintain upright stance in ‘‘foam’’ and ‘‘no foam’’ conditions was measured. when correlated with the selfreported occurrence of falls over the previous 12 months. however.. Teasdale and Simoneau. These measures of balance were subsequently found to be positively correlated with lower limb proprioceptive acuity. In this study of 95 older adults. 1994). McChesney and Woollacott (2000) determined the threshold joint position sense for both the knee and ankle joints. Woollacott et al.. rather than dynamically recovering from a balance perturbation. Second. 3. Speers et al. Unlike the studies of Lord et al. while the dynamic task involved walking on the spot with eyes closed for 1 min. Hirsch et al. This finding has particular relevance given the physical and financial costs associated with falls in the elderly (Burt and Fingerhut. 2001). 1999). Doumas et al. Individuals with poor proprioception showed larger sway in the anterior–posterior direction. Madhavan and Shields (2005) also assessed the acuity of dynamic position sense at the ankle. Comparable absolute errors to Verschueren et al.. Postural control is one area of the literature where this has been of particular interest. Sorock and Labiner. First.. It was shown that the mean acuity of dynamic ankle position sense was 2. a significant relationship was found between toe position acuity and the magnitude of subject sway. Degenerative and plastic-adaptive processes in the aging proprioceptive system While early investigations focused largely on the extent and functional significance of age-related declines in proprioceptive sense. Goble et al. 2005). Decreased attentional resources may also contribute to the diminished proprioceptive abilities of elderly individuals. 2007. For example. Lastly. a 2. (3) decreased sensitivity (Burke et al. it was concluded that increased proprioceptive processing demands significantly impacted the assessment of acuity in the elderly. For example. a contralateral remembered matching task was utilized combining the main processing demands of the previous two tasks. Similarly. (2007) compared three position matching tasks of varying processing demands in 12 healthy older adults (mean age = 75 years). 1972) that may be the result of denervation (Jennekens et al. Doumas et al. older adults may be limited by a diminished capacity for central integration and reweighing of proprioceptive information. Furthermore. (2) get out of a chair and walk 15. Liu et al. Indeed.. old subjects showed increased sway parameters indicating a decrease in overall stability. When assessing the impact of proprioceptive deficits in the elderly on sensorimotor performance. Goble et al. in the upper limb. 4. in a study by You (2005) the acuity of ankle joint position sense for elderly individuals was found to be approximately 2. there has been little attempt in the literature to determine the . Miwa et al. especially for Ruffini. 2007. Briefly.. while functional performance was defined as the aggregate amount of time required to (1) walk 15. the more difficult contralateral remembered task resulted in errors that were on average 2–38 larger than in either of the two less difficult conditions. showing a decreased number and mean density of receptors per unit of skin area (Bolton et al. (2008). 275 Beyond these peripheral alterations. 1966. no significant differences in matching accuracy were seen in elderly subjects.68 error at the ankle can translate into as much as 4. old subjects were significantly worse than both younger age groups in all cases. Thus. 1996. Second. While the above behavioral results are suggestive of age-related central processing deficits related to proprioceptive feedback. Another indication that cognitive processes influence proprioceptive abilities of older adults follows from studies assessing reintegration of proprioceptive feedback (Hay et al.. Teasdale and Simoneau. 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. 1992. Stelmach et al. a myriad of changes occur with age at the level of the individual proprioceptors (see Shaffer and Harrison. 1972). human and animal work involving aged muscle spindles has shown: (1) increased capsular thickness (Swash and Fox. and a fixed support surface. even when proprioceptive inputs to the central nervous system are adequate. 1998). subjects matched elbow displacement based largely on proprioceptive memory (ipsilateral remembered matching). 1999). However. cutaneous mechanoreceptors such as the Meissner and Pacinian type corpuscles are altered. This result demonstrates that older adults perform balance tasks with less automaticity than younger adults when placed in compromised proprioceptive feedback conditions. Teasdale et al.. Neurophysiological mechanisms Research concerning the neurophysiological basis of agerelated declines in proprioception has involved both central and peripheral nervous system changes. where knee position sense tests may be predictive of overall sensorimotor ability in the elderly. This suggests that. As both memory and interhemispheric transfer were necessary for this task. Teasdale and Simoneau. 2007 for review). 2001.78 in magnitude..4-cm endpoint error at the fingertip in situations where vision is not available. This may have implications for clinical settings. older individuals remained unstable relative to the pre-perturbation level of performance. In addition. In these studies. elderly subjects sacrificed performance on the working memory task in favour of maintaining postural stability.0 years) during a concurrent ‘‘n-back’’ working memory task. 2007).. 1993a. 1996. simple body-geometry dictates otherwise.1. Interestingly. when proprioceptive feedback was restored by removing the vibratory stimulus.68. With vision. 1972) and (5) axonal swelling/expanded motor endplates (Swash and Fox. subjects performed contralateral concurrent elbow position matching. More importantly. 1972.J. Lexell and Downham. it is also important to consider biomechanical factors/body anthropometrics. In contrast. Morisawa. (2007) calculated matching errors across all tasks to be on average 5. Swash and Fox. Taken together. inadequate processing of proprioceptive feedback has been inferred from various behavioral studies of older adults. 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. these peripheral changes are a potential source of proprioceptive deficits in the elderly. When tasks involved only memory or only interhemispheric transfer of proprioceptive information. Pacinian and Golgi-tendon type receptors (Aydog˘ et al. 2005)... 2005. 2001). As expected. 1990. 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. In the peripheral nervous system.5 cm center of mass excursion. in accordance with studies conducted in children and young adults (Goble and Brown. performance on functional tasks was significantly correlated with knee position acuity in the elderly.5 m. which did not require memory but induced a greater reliance on interhemispheric transfer. declines in proprioceptive function are also thought to be a result of changes in the central nervous system.5 m. Adamo et al. tested upright stance in older adults (mean age = 71. when the quality of proprioceptive feedback was reduced through platform-based sway referencing. 1980. 4. 2003). 1995). (4) a fewer total number of intrafusal fibers (Liu et al. postural sway increased when attention was divided. Iwasaki et al.. the past decade has seen increased efforts to determine the mechanisms by which these deficits occur and how they might be prevented through training interventions. Although no significant differences were found between middle-aged and young subjects on either the proprioceptive or functional tasks. Kim et al.D.. 2008. Given that the adult forearmhand link is approximately 44 cm in length (Chaffin and Anderson. Westlake and Culham. For example. participants were still able to perform the cognitive task at an optimal level. While this value may seem insignificant. which may be at the expense of other cognitive processes.. (2) decreased spindle diameter (Kararizou et al.. In contrast. when proprioceptive information was degraded by vibration. 2005). greater attentional resources are devoted to the task of maintaining balance. Adamo et al. although no direct correlation with tests of proprioceptive acuity has been made. Bruce. / Neuroscience and Biobehavioral Reviews 33 (2009) 271–278 ipsilateral remembered matching task.. This amount of displacement will certainly impact whole body balance and stability. In the first task. (3) ascend 11 stairs and (4) descend 11 stairs. this degree of inaccuracy could lead to as much as a 4... It was found that joint position errors were systematically modulated by the amount of proprioceptive feedback processing required. a decline in the number of joint mechanoreceptors is experienced with age. 2006. 1993) and following coactivation of adjacent cutaneous receptors over a prolonged (3 h) period of time (Pleger et al.U. but only for the threshold velocity detection measure. study. 2003. This is despite numerous reports demonstrating a general loss of neural substrate with age (for review see Raz and Rodrigue. One activity that has shown a strong relationship with proprioceptive ability is the traditional Chinese exercise—tai chi. To date. 2003. taken together. 2001. These results. intervention-based studies.. more detailed. Conclusion The purpose of the present review was to summarize the current state of knowledge regarding age-related proprioception research. Acknowledgements Support for this study was provided through grants from the Research Council of K. to what extent are the proprioceptive abilities of elderly individuals subject to neuroplastic changes? Certainly. 2004). 2004. 2000. Training induced plastic-adaptive changes A question of critical importance is. a sport that requires precise movement and balance control (Tsang and Hui-Chan. 2007). as determined by measures of peak oxygen consumption level and maximal heart rate during exercise. An alternative approach to determine the effects of exercise on proprioceptive ability in the elderly is that of more longitudinal. 2004).2.. These studies can be placed into two categories based on the type of experimental design employed by the researchers. likely serve as comechanisms for such changes in function. A significant increase in proprioceptive ability for the balance exercise group was found. It has been shown that proprioceptive deficits in position and motion sense clearly exist for the elderly and that these agerelated declines impact sensorimotor tasks such as balance. it might simply be that older adults with better proprioceptive acuity are more successful at golf.. In contrast. in young individuals. as well as to assess long-term maintenance of any improvements through an adequate follow-up. which includes secondary somatosensory area as well as other potential sensory integration areas located in. however. (1997) performed a comparison of knee joint position sense in active versus sedentary elderly. 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. Three measures of proprioceptive function were taken pre. Similarly. as increased proprioceptive acuity in older adults who engage in certain sports/activities does not necessarily prove that the activity enhanced or improved proprioception. perhaps more proprioceptive feedback-specific interventions.e. superior temporal and supramarginal gyri (Heuninckx et al. a major challenge for the future will be to more adequately determine the peripheral and central contributions to age-related proprioceptive deficits. individuals engaged in more gross motor tasks (i. 2005. In contrast. falls education involved a 1-h lecture on falls prevention once per week for 8 weeks. Compared to untrained subjects.. (2007) divided elderly subjects into either an active balance exercise group or a more passive falls education group. Given the mounting evidence that proprioceptive acuity can be improved through training-based interventions. These studies have shown that the amount of primary somatosensory cortex devoted to. 2004). Waddington and Adams (2004) tested the effect of 5 weeks wobble board training on ankle movement discrimination in 20 community dwelling elderly. Such changes can be either basal metabolic or structural in nature and largely result in enhanced proprioceptive output gains. Degenerative changes in the peripheral nervous system. especially. proprioceptive acuity was shown to be significantly enhanced in the group of active elderly individuals. Further. While these results are not specific to elderly individuals per se. (1997). however. Spengler et al. with both showing some benefit of balance-related exercises on proprioceptive function. there are two known investigations that have used this design. for example. Petrella et al. 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. they underscore the need to explore other. 2003). proprio- ceptive benefits have been reported for joint position sense in older individuals who practice golf. Tai chi has been related to increased joint position sense (Tsang and Hui-Chan. it seems likely that similar plastic changes would occur with training in older adults. Physical activity is a potent stimulus for sensorimotor reorganization. / Neuroscience and Biobehavioral Reviews 33 (2009) 271–278 neural correlates associated with such deficiencies. the hindlimb of older rats is significantly reduced by the aging process. site of the primary somatosensory cortex (Good et al. as well as decreases in central processing abilities... Quiton et al. In an relatively early attempt to apply this method. Further. Xu et al. Rather.b). 2004). Caution should be taken when interpreting the results from cross-sectional studies. In the second. 2008a.. 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. individuals who trained proprioception on the wobble board were able to sense significantly smaller amounts of ankle inversion. Leuven.. Goble et al. On the other hand. This increased brain activation may reflect a greater need for proprioceptive monitoring and/or sensorimotor integration in older versus younger individuals. which involves slow movements and continuous monitoring of body position. In contrast to the results of Petrella et al. 5.and post-intervention. including reports of decreased grey matter in postcentral gyrus. 1995). for example. 2001. 2006). research investigating hand–foot interlimb coordination in an fMRI environment has revealed an extended network of neural activation in elderly individuals (particularly more successful ones). 2002. Belgium (OT/07/073) and the . a phenomenon which has recently began to be exploited in several studies assessing the efficacy of training-based interventions on the preservation and/or improvement of proprioceptive function in the elderly. 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. 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. With respect to this key proprioceptive area. 1992 for review)..276 D. provide encouragement for future proprioceptive-based training interventions in the elderly. 2004) and an enhanced threshold for detecting joint motion in the elderly (Xu et al. The balance exercise group attended classes three times a week for 8 weeks that emphasized static and dynamic balance exercises. more recent studies have shown that improvements in elderly proprioception may be specific to the type of physical training undertaken (Tsang and Hui-Chan. Godde et al. further insight regarding age-related changes comes from animal research where electrophysiological recordings and optical imaging have been used (Coq and Xerri. 4. and therefore are more likely to engage in this activity. in humans.J. Westlake et al. Based on this paradigm. Ezure. 30. J.C. 168. Brain Res.D. Phys. 976–981. Wenderoth. Carlton. Cody. Lamarre. Quadriceps function. Goble (GP00408N & F/07/063) and J. Kaplan.... Ashburner. J.. B. Brain Res... E. Proprioceptive coordination of movement sequences: role of velocity and position information. Kerr. Goodwin.. Stable human standing with lowerlimb muscle afferents providing the only sensory input.. Newham.. 109–115. P. L.. O. Korkusuz.. 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