Mechanisms that contribute to differences in motor performance between young and old adults
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
References (95)
Cortical drives to human muscle: the Piper and related rhythms
Prog Neurobiol
(2000)On the use and interpretation of cross-correlation measurements in the mammalian central nervous system
J Neurosci Meth
(1979)- et al.
Discharge pattern of human motor units during dynamic concentric and eccentric contractions
Electromyogr Clin Neurophysiol
(1998) Analysis of firing behaviour of human motoneurones within the ‘subprimary range’
J Physiol Paris
(1999)- et al.
Macro-EMG and motor unit recruitment threshold: differences between the young and the aged
Neurosci Lett
(1994) - et al.
Task-related behavior of motor units in different regions of the human masseter muscle
Arch Oral Biol
(1992) - et al.
The Fourier approach to the identification of functional coupling between neuronal spike trains
Prog Biophys Mol Biol
(1989) - et al.
The effects of motion on force control abilities
Clin Biomech
(2001) - et al.
Motor control and kinetics during low level concentric and eccentric contractions in man
Electromyogr Clin Neurophysiol
(1996) - et al.
The effect of visual feedback on physiological muscle tremor
Electroencephalogr Clin Neurophysiol
(1974)
Firing rate of individual motor units in voluntary contraction of abductor digiti minimi muscle in man
Exp Neurol
Relation between location of a motor unit in the human biceps brachii and its critical firing levels for different tasks
Exp Neurol
The numbers of limb motor neurons in the human lumbosacral cord throughout life
J Neurol Sci
Error, stress and the role of neuromotor noise in space oriented behaviour
Biol Psychol
A mechanism for increased contractile strength of human pennate muscle in response to strength training: changes in muscle architecture
J Physiol
Neuronal mechanisms underlying physiological tremor
J Neurophysiol
The effect of strength training on control of force in older men and women
Aging Clin Exp Res
Strength training can improve steadiness in persons with essential tremor
Muscle Nerve
Effect of task on the degree of synchronization of intrinsic hand muscle motor units in man
J Neurophysiol
Coactivation of the antagonist muscle does not covary with steadiness in old adults
J Appl Physiol
Physiological changes in ageing muscle
J Neurol Neurosurg Psychiat
Force variability and characteristics of force production
A study of the muscle force waveform using a population stochastic model of skeletal muscle
Biol Cybernetics
Age and contraction type influence motor output variability in rapid discrete tasks
J Appl Physiol
Old adults exhibit greater motor output variability than young adults only during rapid discrete isometric contractions
J Gerontol
Modeling variability of force during isometric contractions of the quadriceps femoris
J Motor Behav
Steadiness of lengthening contractions
Grasp force control in older adults
J Motor Behavior
On the relation between motor unit discharge and physiological tremor
Proprioceptive coordination of movement sequences: role of velocity and position information
J Neurophysiol
Experimental simulation of cat electromyogram: evidence for algebraic summation of motor-unit action-potential trains
J Neurophysiol
Common drive in motor units of a synergistic muscle pair
J Neurophysiol
Effects of motor unit losses on strength in older men and women
J Appl Physiol
An electromyographic analysis of compartments in cat lateral gastrocnemius during unrestrained locomotion
J Neurophysiol
Motor unit physiology: some unresolved issues
Muscle Nerve
Effects of aging on motor-unit control properties
J Neurophysiol
Rhythmicity, synchronization and binding in human and primate motor systems
J Physiol
The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man
J Physiol
The information capacity of the human motor system in controlling the amplitude of movement
J Exp Psychol
Models of recruitment and rate coding organization in motor-unit pools
J Neurophysiol
Reduced control of motor output in a human hand muscle of elderly subjects during submaximal contractions
J Neurophysiol
Decrease in human neurones with age
Anat Rec
Older adults use a unique strategy to lift inertial loads with the elbow flexor muscles
J Neurophysiol
Load-independent contributions from motor-unit synchronization to human physiological tremor
J Neurophysiol
Controlling the statistics of action: obstacle avoidance
J Neurophysiol
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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.