Malgorzata Klass

Age-related decline in rate of torque development is accompanied by lower maximal motor unit discharge frequency during fast contractions

The aim of this study was to investigate the association between the rate of torque development and maximal motor unit discharge frequency in young and elderly adults as they performed rapid submaximal contractions with the ankle dorsiflexors. Recordings were obtained of the torque exerted by the dorsiflexors during the isometric contractions and the surface and intramuscular electromyograms (EMGs) from the tibialis anterior. The maximal rate of torque development and integrated EMG (percentage of total EMG burst) at peak rate of torque development during fast contractions were lower in elderly than young adults by 48% (P < 0.05) and 16.5% (P < 0.05), respectively. The young adults, but not the elderly adults, exhibited a positive association (r2 = 0.33; P < 0.01) between the integrated EMG computed up to the peak rate of torque development and the maximal rate of torque development achieved during the fast contractions. These age-related changes during fast voluntary contractions were accompanied by a decline (P < 0.001) in motor unit discharge frequency (19, 28, and 34% for first 3 interspike intervals, respectively) and in the percentage of units (45%; P < 0.05) that exhibited double discharges (doublets) at brief intervals (<5 ms). Because aging decreased the maximal rate of torque development of fast voluntary contractions to a greater extent ( approximately 10%) than that of an electrically evoked twitch, collectively the results indicate that the age-related decline in maximal motor unit discharge frequency likely limit, in addition to the slowing of muscle contractile properties, the performance of fast voluntary contractions.

Voluntary activation during maximal contraction with advancing age: a brief review

It is well established that the loss of muscle mass (i.e. sarcopenia) is the primary factor contributing to the reduction in muscle force with ageing. Based on the observation that force declines at a faster rate than muscle mass, neural alterations are also thought to contribute to muscle weakness by reducing central drive to the agonist muscles and by increasing coactivation of the antagonist muscles. Researchers have attempted to quantify the contribution of impaired voluntary drive to the decline in muscle force using superimposed electrical stimulation during maximal voluntary contractions (MVCs) and by recording surface electromyographic (EMG) activity. Although reduced voluntary activation of agonist muscles and increased coactivation of antagonist muscles during a MVC have been reported with advancing age, such changes are not supported by all studies. These discrepancies may be explained by differences in sensitivity between the methods used to assess voluntary activation, as well as differences between the characteristics of the study population, the muscle group that is tested, and the type of contraction that is performed. The objective of this review is to summarize current knowledge regarding the activation of agonist and antagonist muscles during MVC in elderly and to try to clarify the disparities in literature concerning the influence of a possible deficit in voluntary activation on the maximal force capacity of muscles in elderly adults.

Unraveling the neurophysiology of muscle fatigue

Despite 100years of research since the seminal work of Angelo Mosso (1846-1910), our understanding of the interactions between the nervous system and muscle during the performance of fatiguing contractions remains rather rudimentary. Although the nervous system simply needs to provide an activation signal that will elicit the net muscle torque required for a prescribed action, changes in the number and diversity of synaptic inputs that must be integrated by the spinal motor neurons to accommodate the changes in the force-producing capabilities of the muscle fibers complicate the process of generating the requisite activation signal. This brief review examines two ways in which the activation signal can be compromised during sustained contractions and thereby contribute to the rate at which the muscles fatigue. These examples provide insight on the types of adjustments that occur in the nervous system during fatiguing contractions, but emphasize that much remains to be learned about the physiological processes that contribute to the phenomenon known as muscle fatigue.

Spinal Mechanisms Contribute to Differences in the Time to Failure of Submaximal Fatiguing Contractions Performed With Different Loads

This study compared the mechanisms that limit the time to failure of a sustained submaximal contraction at 20% of maximum when the elbow flexors either supported an inertial load (position task) or exerted an equivalent constant torque against a rigid restraint (force task). The surface electromyogram (EMG), the motor-evoked potential (MEP) in response to transcranial magnetic stimulation (TMS) of the motor cortex, and the Hoffmann reflex (H-reflex) and maximal M-wave (Mmax) elicited by electrical stimulation of the brachial plexus were recorded in biceps brachii during the two tasks. Although the time to failure for the position task was only 44% of that for the force task, the rate of increase of the average EMG (aEMG; % initial MVC) and MEP area (% Mmax) did not differ significantly during the two tasks. At task failure, however, the increases in normalized aEMG and MEP area were significantly (P < 0.05) greater for the force task (36.4 and 219.9%) than for the position task (22.4 and 141.7%). Furthermore, the superimposed mechanical twitch (% initial MVC), evoked by TMS during a brief MVC of the elbow flexors immediately after task failure, was increased similarly in both tasks. Although the normalized H-reflex area (% Mmax) decreased during the two fatiguing contractions, the reduction was more rapid and greater during the position task (59.8%) compared with the force task (34.7%). Taken together, the results suggest that spinal mechanisms were a major determinant of the briefer time to failure for the position task.

Effects of noradrenaline and dopamine on supraspinal fatigue in well-trained men.

PURPOSE Prolonged exhaustive exercise induces a failure of the nervous system to activate the involved muscles maximally (i.e., central fatigue). Part of central fatigue may reflect insufficient output from the motor cortex (i.e., supraspinal fatigue), but the cause is unresolved. To investigate the potential link between supraspinal fatigue and changes in brain concentration of dopamine and noradrenaline in temperate environment, we combined neurophysiological methods and pharmacological manipulation of these two neurotransmitters. METHODS Changes in performance of a cycling exercise (time trial [TT]) were tested after oral administration of placebo (Pla), dopamine, or noradrenaline reuptake inhibitors (methylphenidate and reboxetine [Rebox], respectively) in well-trained male subjects. Changes in voluntary activation, corticospinal excitability, and muscle contractile properties were tested in the knee extensors using transcranial magnetic stimulation and motor nerve electrical stimulation before and after exercise. A psychomotor vigilance task (PVT) was also performed. RESULTS Compared with Pla, methylphenidate did not affect exercise performance (P = 0.19), but more time was needed to complete the TT after administration of Rebox (approximately 9%, P < 0.05). For the latter condition, the reduced performance was accompanied by a central/supraspinal fatigue (5%-6%, P < 0.05) and worsened PVT performance (7%, P < 0.05). For the three conditions, corticospinal excitability was unchanged, and peripheral fatigue was similar. Because the ingestion of Rebox induced a greater decrease in voluntary activation and PVT performance after the TT than Pla, with no modification in corticospinal excitability, the noradrenaline reuptake inhibitor likely affected supraspinal circuits located before the motor cortex. CONCLUSION These results suggest that noradrenaline, but not dopamine reuptake inhibition, contributes to the development of central/supraspinal fatigue after a prolonged cycling exercise performed in temperate conditions.

Discharge properties of motor units during steady isometric contractions performed with the dorsiflexor muscles

The purpose of this study was to record the discharge characteristics of tibialis anterior motor units over a range of target forces and to import these data, along with previously reported observations, into a computational model to compare experimental and simulated measures of torque variability during isometric contractions with the dorsiflexor muscles. The discharge characteristics of 44 motor units were quantified during brief isometric contractions at torques that ranged from recruitment threshold to an average of 22 ± 14.4% maximal voluntary contraction (MVC) torque above recruitment threshold. The minimal [range: 5.8-19.8 pulses per second (pps)] and peak (range: 8.6-37.5 pps) discharge rates of motor units were positively related to the recruitment threshold torque (R(2) ≥ 0.266; P < 0.001). The coefficient of variation for interspike interval at recruitment was positively associated with recruitment threshold torque (R(2) = 0.443; P < 0.001) and either decreased exponentially or remained constant as target torque increased above recruitment threshold torque. The variability in the simulated torque did not differ from the experimental values once the recruitment range was set to ∼85% MVC torque, and the association between motor twitch contraction times and peak twitch torque was defined as a weak linear association (R(2) = 0.096; P < 0.001). These results indicate that the steadiness of isometric contractions performed with the dorsiflexor muscle depended more on the distributions of mechanical properties than discharge properties across the population of motor units in the tibialis anterior.

Noradrenaline Reuptake Inhibition Impairs Cortical Output and Limits Endurance Time.

PURPOSE To assess the neural mechanisms that limit endurance time, we compared a fatiguing task performed under the influence of reboxetine (REB), a noradrenaline reuptake inhibitor, and placebo (PLA). METHODS Nine male subjects (age = 24 ± 2 yr) participated in this study. The fatiguing task involved repeated 3-s submaximal isometric contractions of the knee extensors (∼33% maximal voluntary contraction) with a 2-s rest between each contraction and performed until task failure. Before, during, and after exercise, changes in voluntary activation, corticospinal (motor-evoked potential) and spinal excitability (Hoffman reflex), and muscle contractile properties were tested using electrical and transcranial magnetic stimulations. A psychomotor vigilance task assessed reaction time before and after exercise. RESULTS Compared with PLA, REB reduced the endurance time by 15.6% (P = 0.04). The maximal voluntary contraction torque decreased to a similar extent at task failure in both conditions (P < 0.01), whereas the rate of decline was greater in REB than that in PLA (P = 0.02). The level of voluntary activation tested by transcranial magnetic stimulation and electrical stimulation decreased (P < 0.01) by 10%-15% at the end of the task, but the mean rate of decline was greater in REB (P ≤ 0.03). Although motor-evoked potential did not change during fatigue, Hoffman reflex, and electrically evoked torque decreased similarly in the PLA and REB conditions (P ≤ 0.02). After exercise, reaction time increased by 3.5% (P = 0.02) in REB but did not change in the PLA condition. CONCLUSION These findings suggest that because of the noradrenaline reuptake inhibition, the output from the motor cortex is decreased at a greater rate than that in the PLA condition, contributing thereby to shorten endurance time.

Contractile properties of single motor units in elderly

Ageing is usually associated with decreased motor control, muscle force and slowing of contractile properties. In addition to changes in muscle architecture and tendon compliance (Narici et al. 2002), these alterations are related to adaptations in motor unit (MU) structure and function. Although some studies have already investigated the adaptations in MU recruitment, discharge frequency or contractile properties in aged population, most of them were performed in hand muscles (Roos et al. 1997). Since the age-related changes may vary specifically with the muscle group investigated, it was interesting to examine these adaptations in a lower limb muscle. More precisely, we chose the tibialis anterior (TA) which is involved in locomotion and stabilization of the body, two functions that are often altered in elderly adults.

Age-related decline in rate of torque development during fast contractions is caused by lower neural activation and slower muscle contractile kinetics

Aging is not only associated with a progressive loss of force (Klass et al. 2005), but also with a slower rate of force development during fast contractions (Barry et al. 2005). This slowing may have important repercussions on motor control and equilibrium. Therefore, the aim of this study was to investigate if the reduced rate of torque development can be partly related to a lower neural activation, quantified by motor unit (MU) discharge frequency.

Age-related changes in fatigability during concentric and eccentric contractions

Despite the great number of studies that have examined the mechanisms of fatigue, relatively few works have investigated the effect of ageing on the neuromuscular fatigability (Allman and Stuart 2001, Vandervoort 2002). Furthermore, to our knowledge, no study has investigated the effect of eccentric (ECC) contractions on muscle fatigue and its possible difference with concentric (CON) contractions in elderly adults. Since, it is well known that fatigue is task-dependent (Enoka and Stuart 1992), it was interesting to compare muscle fatigability during CON and ECC contractions in young and elderly adults and to determine the relative contribution of central and peripheral mechanisms to the decline in force.