Mechanisms that contribute to differences in motor performance between young and old adults

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Abstract

This paper examines the physiological mechanisms responsible for differences in the amplitude of force fluctuations between young and old adults. Because muscle force is a consequence of motor unit activity, the potential mechanisms include both motor unit properties and the behavior of motor unit populations. The force fluctuations, however, depend not only on the age of the individual but also on the muscle group performing the task, the type and intensity of the muscle contraction, and the physical activity status of the individual. Computer simulations and experimental findings performed on tasks that involved single agonist and antagonist muscles suggest that differences in force fluctuations are not attributable to motor unit twitch force, motor unit number, or nonuniform activation of the agonist muscle, but that they are influenced by the variability and common modulation of motor unit discharge in both the agonist and antagonist muscles. Because the amplitude of the force fluctuations does not vary linearly with muscle activation, these results suggest that multiple mechanisms contribute to the differences in force fluctuations between young and old adults, although the boundary conditions for each mechanism remain to be determined.

Introduction

When an individual performs a steady contraction with hand, arm, or leg muscles, the force exerted by the limb is not constant but rather it fluctuates about an average value [15], [54], [62], [69], [73], [85]. The variability of the force about the mean, which can be quantified in absolute terms as the standard deviation or in relative terms as the coefficient of variation, often varies with the average force exerted by the involved muscles. Based on protocols that have largely involved low-to-moderate forces during isometric and anisometric (concentric and eccentric) contractions, a number of studies have found that there can be differences between young and old adults in the amplitude of the force fluctuations. This paper describes some of the differences in force fluctuations that have been observed between young and old adults and examines the physiological mechanisms responsible for these differences.

The presence of force fluctuations during a voluntary contraction influences the capacity of an individual to achieve a desired force and to produce an intended limb trajectory. For example, the minimum force exerted by the thumb and index finger when performing the pinch grip must be greater than the friction force required to prevent slipping [17], [43]. Furthermore, the rapid performance of a simple aiming movement requires a large activation signal, which increases the variability of the trajectory and reduces the accuracy of the final position [28], [34], [42], [87]. These effects are compounded in repeat performances of a task in that the fluctuations in muscle force during a voluntary contraction cause the exerted force and the movement kinematics to vary from trial to trial [9], [11], [12], [15], [19], [35]. The activation signals sent from the nervous system to muscles, therefore, must accommodate the force fluctuations for the successful completion of goal-directed movements.

Section snippets

Force fluctuations during submaximal contractions

The fluctuations in muscle force during a voluntary contraction have been quantified as the standard deviation of force during isometric contractions and as the standard deviation of acceleration during anisometric contractions in hand, arm, and leg muscles. Although the amplitude of the fluctuations has been found to differ between young and old adults, this is not a consistent finding. The factors that influence this relation include the muscle group performing the task, the type of muscle

Mechanisms that influence force fluctuations

The unitary functional element of the neuromuscular system is the motor unit. The net force exerted by a muscle when many motor units are activated results in a force of varying amplitude, the fluctuations of which depend on the contractile and discharge characteristics of the most recently recruited motor units [2], [10], [25] and are, according to the Size Principle, the largest motor units that have been activated for the task. Based on this rationale, it is evident that fluctuations in the

Summary

Despite the functional significance of fluctuations in the motor output for the accuracy of goal-directed movements and its deterioration with advancing age, there is not yet a physiological explanation of the mechanisms that are responsible for this phenomenon. The task of identifying the mechanisms is complicated by the dependence of the force fluctuations on the muscle group performing the task, the type and intensity of the muscle contraction, and the physical activity status of the

Acknowledgements

Supported by National Institute on Aging awards AG09000 and AG13929 to RME and AG05878 to BLT, a Minority Supplement Award to KWK, and an NSF Graduate Research Fellowship to AMT.

Roger M. Enoka completed undergraduate training in physical education at the University of Otago in New Zealand prior to obtaining an MS degree in biomechanics and a PhD degree in kinesiology from the University of Washington in Seattle. He has held faculty positions in the Department of Exercise and Sport Sciences and the Department of Physiology at the University of Arizona and in the Department of Biomedical Engineering at the Cleveland Clinic Foundation. He is currently a professor in the

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    Roger M. Enoka completed undergraduate training in physical education at the University of Otago in New Zealand prior to obtaining an MS degree in biomechanics and a PhD degree in kinesiology from the University of Washington in Seattle. He has held faculty positions in the Department of Exercise and Sport Sciences and the Department of Physiology at the University of Arizona and in the Department of Biomedical Engineering at the Cleveland Clinic Foundation. He is currently a professor in the Department of Kinesiology and Applied Physiology at the University of Colorado in Boulder. His research focuses on the neuromuscular mechanisms that mediate acute adjustments and chronic adaptations in response to physical activity.

    Evangelos A. Christou received a BS degree in Exercise Science at Truman State University in Missouri in 1994 and was certified as an athletic trainer in the same year. He subsequently completed MS (1997) and PhD (2000) degrees in kinesiology at the University of Illinois at Urbana-Champaign. He is currently a postdoctoral fellow in the Department of Kinesiology and Applied Physiology at the University of Colorado in Boulder. His research interests include understanding the neuromuscular mechanism responsible for motor output variability in young and old humans and determining the functional significance of this variability.

    Sandra K. Hunter obtained her Bachelor of Education (Physical Education and Health) at the University of Sydney in Australia (1985). She graduated with a Graduate Diploma in Human Movement Science from the University of Wollongong, Australia (1992) and a PhD degree in Exercise and Sport Science from the University of Sydney, Australia (1998). She is currently a postdoctoral fellow in the Department of Kinesiology and Applied Physiology at the University of Colorado in Boulder. Her research interests include the adaptations in the neural control of muscle with fatigue and aging, as well as understanding the mechanisms responsible for the sex and task differences in muscle fatigue of young and old adults.

    Kurt W. Kornatz received his BS in Commerce from DePaul University in 1991 and was awarded an MS in Kinesiology from the University of Texas at El Paso in 1996. He is currently a doctoral candidate in the Department of Kinesiology and Applied Physiology at the University of Colorado-Boulder. His current research interests relate to healthy aging of the neuromuscular system.

    John G. Semmler obtained an undergraduate degree in exercise science (1991), an honors degree in physiology (1992), and a PhD degree (1996) in neurophysiology from the University of Adelaide in Australia. He received post-doctoral training in clinical neurology from the Department of Medicine at the University of Adelaide and more recently in Kinesiology and Applied Physiology at the University of Colorado in Boulder, U.S.A. His research interests focus on the neural control of movement in humans, with particular emphasis on the control properties of single motor units and the motor cortex control of movement in normal and dysfunctional nervous systems.

    Anna (Mickey) Taylor completed a BS degree in Exercise Science at the University of California at Davis in 1999. She is currently a PhD student in the Department of Kinesiology and Applied Physiology and the Center for Neuroscience at the University of Colorado in Boulder. Mickey is fascinated by the way in which patterns of synaptic input to a motor neuron pool result in muscle activity.

    Brian L. Tracy received BS (1988) and MS (1991) degrees in Exercise and Sport Science at Colorado State University before completing his PhD degree (1997) in Exercise Physiology at the University of Maryland, College Park. Subsequently, he was a post doctoral fellow in the Neural Control of Movement Laboratory in the Department of Kinesiology and Applied Physiology at the University of Colorado, Boulder, and is currently an Assistant Research Professor in the same Department. His research interests focus on the control of muscle contractions in aging, sarcopenia, and frailty, and the effects of strength-training interventions in older adults.

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