Central Modulation of Motor Unit Activity

Enoka, R.M. (2005). Central modulation of motor unit activity. Medicine and Science in Sports and Exercise, 37, 2111-2112.

The motor unit, which comprises the basic functional unit of the neuromuscular system, consists of a motor neuron in the ventral horn of the spinal cord, its axon and the muscle fibres that the axon innervates. The number of muscle fibres innervated by a single axon ranges from tens to thousands, but typically average a few hundred. The force exerted by a motor unit depends principally on the number of muscle fibres innervated by the motor neuron and the rate at which the motor neuron discharges action potentials.

The group of motor neurons in the spinal cord that innervate a single muscle is referred to as a “motor pool” or a “motor nucleus”. Motor pools typically are composed of a few hundred motor neurons, ranging from about 100 for small muscles to approximately 1000 for large muscles. The motor unit population that forms a motor pool is heterogeneous, because of systematic variations in the properties of both the motor neurons and the muscle fibres. For example, the motor neurons vary widely in their electrical properties and in the relative amplitudes of the inputs that they receive from various sources. Similarly, the contractile properties of the muscle fibres vary with regard to contraction speed, force-generating capacity and resistance to fatigue.

Despite the diversity in the properties of the motor neurons and the muscle fibres, the functional organisation of the motor pool appears to obey some relatively simple rules. Foremost among these rules is the size principle, which states that the order in which motor neurons are activated during a contraction proceeds from smallest to largest. The recruitment order of motor units, therefore, is relatively invariant and is dictated by the physical size of the motor neuron and the intrinsic properties of the motor neuron that are closely related to its size. Although a number of studies have attempted to identify conditions, such as contraction speed and type, in which recruitment order might violate the size principle, no consistent demonstrations show that it does not apply to all types of reflex and voluntary contractions.

A second simplifying feature of motor pool function is that the distribution of the properties among the motor neurons and muscle fibres tend to cluster into a few groups that have been denoted as motor unit and muscle fibre types. Burke et al. (1973), for example, found that with two contractile properties, the profile of an unfused tetanus and resistance to fatigue, it was possible to identify three types of motor units in the hindlimb muscles of cats. The motor units were classified as type S (slow), type FR (fast, fatigue resistant) and type FF (fast, fatigable). Correspondingly, muscle fibres have been characterised based on the histochemical assessment of myosin adenosine triphosphatase (ATPase) content (type I, IIa, IIb) and on the molecular composition of the myosin heavy chain (MHC I, MHC IIa, MHC IIb/IIx). Although such classification schemes are helpful in characterising the range of motor unit properties in a muscle, it is necessary to remember that each of the variables used to distinguish the various types is distributed continuously. For example, the contraction speed of motor units does not cluster into three distinct groups, but exhibits a continuous distribution from fast (20 ms) to slow (100 ms) contraction times for the time to peak twitch force. Thus, the recruitment order of motor units does not precisely proceed in the order of slow twitch before fast twitch.

Over the last decade or so, our understanding of motor pool function has been complicated by the emergence of two new principles: metabotropic control of motor neuron excitability and state-dependent modulation of sensory feedback. Motor neurons receive two types of input, ionotropic and metabotropic. Ionotropic inputs, which are delivered through ligandgated channels, are responsible for much of the synaptic input to motor neurons when a transmitter binds to a receptor. Ionotropic inputs to motor neurons arise from the cortex, the brainstem and from peripheral sensory receptors. These inputs evoke excitatory and inhibitory postsynaptic potentials that depolarise and hyperpolarise, respectively, the membrane potential of the motor neuron. Furthermore, many motor neurons receive common ionotropic input that can concurrently modulate the discharge rates of motor neurons. In contrast, metabotropic input involves the binding of neuro-transmitters to receptors and the subsequent activation of intracellular second messenger pathways. Metabotropic inputs control the excitability (threshold and gain) of motor neurons, which can vary with the state of arousal. When arousal is heightened, for example the excitability of the motor neuron pool is enhanced and less ionotropic input is required to achieve a specific amount of motor output.

In a similar vein, accumulating evidence indicates that the efficacy of peripheral sensory feedback in influencing motor output depends on the task that is being performed by the individual. For example, the amplitude of a reflex response differs during the stance and swing phases of locomotion and can be modulated, depending on whether it destabilises the individual. Furthermore, reflex amplitude can be increased or decreased after training. This type of plasticity is attributable to the prominent role of spinal interneurons in integrating the sensory and motor signals that are transmitted to the motor neurons.

The presentations of Kalmar, Christou and Shinohara (summaries of which follow) in the mini-symposium on the central modulation of motor unit activity described current work that was related to these two new principles on the function of the motor pool. Kalmar reviewed the effects of caffeine on muscle activation and described the consequences for evoked potentials, reflex responses, the discharge of motor units and sensory events. Christou reported on the findings of a study that examined the age-related interaction between a stressor and visual feedback on the performance of a fine motor task. Shinohara summarised the effects of prolonged muscle vibration on motor unit activity and motor performance during voluntary contractions. The functional significance of these reports is that they extend the experimental conditions under which muscle activity is normally studied to include conditions that are often encountered in activities of daily living. These approaches provide new possibilities for examining our traditional concepts, such as the size principle and motor unit types, about the function of the motor pool.

Kalmar, M.J. (2005). The influence of caffeine on voluntary muscle activation. Medicine and Science in Sports and Exercise, 37, 2113-2119.
(Department of Biology, York University, Toronto, Ontario, CANADA)

Abstract: Caffeine is a very common CNS stimulant that has been of interest to physiologists because of its direct effects on skeletal muscle in vitro, as well as ergogenic effects on laboratory tests of human performance. While in vitro studies have clearly demonstrated the effects of the drug on the CNS, the effects of caffeine on the voluntary activation of muscle in humans are less defined. Voluntary as well as involuntary supraspinal input, alpha motor neuron membrane properties and afferent feedback to spinal and supraspinal neurons all modulate voluntary muscle activation and caffeine may therefore alter muscle activation at several sites along the motor pathway. This review explores the effects of caffeine on voluntary muscle activation that have been demonstrated in recent human studies and discusses the central mechanisms that may enhance activation. Evidence of caffeine’s effects on the motor evoked potential, Hoffman reflex, self-sustained firing of the alpha motor neuron and pain and force sensation are presented as well as limitations and considerations of using the drug in human neuromuscular studies.

Christou, A.E. (2005). Visual feedback attenuates force fluctuations induced by a stressor. Medicine and Science in Sports and Exercise, 37, 2126-2133.

Purpose: the fluctuations in force during a steady contraction can be influenced by age, vision and level of physiological arousal. The aim of this study was to determine the effects of a stressor on the force fluctuations and information transmission exhibited by young, middle-aged and older adults when a pinch-grip task was performed with and without visual feedback.

Methods: thirty-six men and women (19-86 yr) participated in a protocol that comprised anticipatory (30 min), stressor (15 min) and recovery periods (25 min). The stressor was a series of noxious electrical stimuli applied to the dorsal surface of the left hand. Subjects sustained a pinch-grip force with the right hand at 2% of the maximal voluntary contraction force. The normalised fluctuations in pinch-grip force (coefficient of variation), information transmission (log2 signal:noise) and the spectra for the force were quantified across the 70-min period.

Results: removal of visual feedback exacerbated the force fluctuations (3.83 ± 3.15 vs. 2.82 ± 1.64%) and reduced the information transmission (5.01 ± 0.86 vs. 5.34 ± 0.71 bits) only during the stressor period. The effect was similar for all age groups. Older adults exhibited greater force fluctuations and lower information transmission compared with young and middle-aged adults, especially during the stressor period. The impairments in fine motor performance during the stressor were associated with an enhancement of the power at 1-2 Hz in the force spectrum (R2 = 0.41-0.52).

Conclusion: removal of visual feedback increased the force fluctuations and decreased information transmission during a stressor period, which suggests that integration of visual feedback can attenuate the stressor-induced enhancement of synaptic input received by the motor neuron pool.

Shinohara, M. (2005). Effects of prolonged vibration on motor unit activity and motor performance. Medicine and Science in Sports and Exercise, 37, 2120-2125.

Abstract: Excitatory input to the α motor neuron pool from Ia afferents is enhanced by brief vibration, yet is depressed when vibration is applied for prolonged periods. The purpose of this article is to synthesize recent findings from several studies on the effects of prolonged vibration on motor unit activity and motor performance during maximal and sub-maximal contractions in humans. Prolonged vibration does not alter voluntary drive during maximal contractions, but it does reduce Ia afferent input to α motor neuron pools and discharge rate of motor units in the vibrated muscles, leading to a reduction in maximal voluntary contraction force. Alterations in the activity of the motor unit pool may be variable across synergistic muscles due to potential neural connections between synergistic muscles. Prolonged vibration reduces the force fluctuations during sub-maximal steady contractions, presumably due to a depression of group Ia feedback from leg muscles. When prolonged vibration evokes a tonic vibration reflex in a hand muscle, the mean discharge rate of motor units during a sub-maximal force-matching contraction increases, leading to an increase in the associated force fluctuations. In summary, prolonged vibration modulates Ia feedback and motor unit activity, which leads to reduced peak force during maximal contractions and altered force fluctuations during sub-maximal contractions.