ReviewProprioceptive sensibility in the elderly: Degeneration, functional consequences and plastic-adaptive processes
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) 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 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 fiber sensory neuropathy have provided a clear demonstration of this showing that, when visual feedback is unavailable, “deafferented” individuals have difficulties: (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, Sainburg et al., 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, Verschueren et al., 1999b). This method involves the transcutaneous application of high frequency, low amplitude vibration to a target muscle in order to increase the neural firing rate of, primarily, type 1a afferents from muscle spindles (Bianconi and van der Meulen, 1963, Burke et al., 1976a, Burke et al., 1976b). 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, Pyykkö 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, Goodwin et al., 1972b, 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 deficits have, therefore, spurred increased interest in the field 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 deficits 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 deficits through use-dependent neuroplastic changes within the proprioceptive system.
Section snippets
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 specific findings are incorporated into a broader framework demonstrating the extent of declines in proprioceptive acuity for older individuals.
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 deficits 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
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, 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.
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 deficits in position and motion sense clearly exist for the elderly and that these age-related 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 co-mechanisms for such changes in function. Given the
Acknowledgements
Support for this study was provided through grants from the Research Council of K.U. Leuven, Belgium (OT/07/073) and the Flanders Fund for Scientific 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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