Different Types Of Motor Units Research Articles

Purinergic Mechanisms of Adaptation of Different Types of Motor Units under Conditions of Allergic Reorganization

Purinergic Mechanisms of Adaptation of Different Types of Motor Units under Conditions of Allergic Reorganization

Metabolic cost underlies task-dependent variations in motor unit recruitment.

Mammalian skeletal muscles are comprised of many motor units, each containing a group of muscle fibres that have common contractile properties: these can be broadly categorized as slow and fast twitch muscle fibres. Motor units are typically recruited in an orderly fashion following the 'size principle', in which slower motor units would be recruited for low intensity contraction; a metabolically cheap and fatigue-resistant strategy. However, this recruitment strategy poses a mechanical paradox for fast, low intensity contractions, in which the recruitment of slower fibres, as predicted by the size principle, would be metabolically more costly than the recruitment of faster fibres that are more efficient at higher contraction speeds. Hence, it would be mechanically and metabolically more effective for recruitment strategies to vary in response to contraction speed so that the intrinsic efficiencies and contraction speeds of the recruited muscle fibres are matched to the mechanical demands of the task. In this study, we evaluated the effectiveness of a novel, mixed cost function within a musculoskeletal simulation, which includes the metabolic cost of contraction, to predict the recruitment of different muscle fibre types across a range of loads and speeds. Our results show that a metabolically informed cost function predicts favoured recruitment of slower muscle fibres for slower and isometric tasks versus recruitment that favours faster muscles fibres for higher velocity contractions. This cost function predicts a change in recruitment patterns consistent with experimental observations, and also predicts a less expensive metabolic cost for these muscle contractions regardless of speed of the movement. Hence, our findings support the premise that varying motor recruitment strategies to match the mechanical demands of a movement task results in a mechanically and metabolically sensible way to deploy the different types of motor unit.

Does a two-element muscle model offer advantages when estimating ankle plantar flexor forces during human cycling?

Traditional Hill-type muscle models, parameterized using high-quality experimental data, are often “too weak” to reproduce the joint torques generated by healthy adults during rapid, high force tasks. This study investigated whether the failure of these models to account for different types of motor units contributes to this apparent weakness; if so, muscle-driven simulations may rely on excessively high muscle excitations to generate a given force. We ran a series of forward simulations that reproduced measured ankle mechanics during cycling at five cadences ranging from 60 to 140 RPM. We generated both “nominal” simulations, in which an abstract ankle model was actuated by a 1-element Hill-type plantar flexor with a single contractile element (CE), and “test” simulations, in which the same model was actuated by a 2-element plantar flexor with two CEs that accounted for the force-generating properties of slower and faster motor units. We varied the total excitation applied to the 2-element plantar flexor between 60 and 105% of the excitation from each nominal simulation, and we varied the amount distributed to each CE between 0 and 100% of the total. Within this test space, we identified the excitation level and distribution, at each cadence, that best reproduced the plantar flexor forces generated in the nominal simulations. Our comparisons revealed that the 2-element model required substantially less total excitation than the 1-element model to generate comparable forces, especially at higher cadences. For instance, at 140 RPM, the required excitation was reduced by 23%. These results suggest that a 2-element model, in which contractile properties are “tuned” to represent slower and faster motor units, can increase the apparent strength and perhaps improve the fidelity of simulations of tasks with varying mechanical demands.

Excitability properties of single human motor axons: are all axons identical?

Under natural motor control, repetitive firing of motoneurons is transmitted by their motor axons to muscle fibers in the “one to one” fashion that allows the analysis of human motoneuron firing via recordings of motor unit (MU) action potentials (see Kernell, 2006; Heckman and Enoka, 2012). However, when axons are diseased or damaged, local increasing axonal excitability may result in disturbing this basic principle and creating an additional focus of excitation in an axon itself, leading to different symptoms, including MU spontaneous discharges. In order to gain an insight into possible pathophysiological mechanisms underlying changes in axonal excitability, many studies were addressed exploring axonal excitability properties in healthy humans and their fundamental characteristics have been obtained (reviewed by Bostock et al., 1998; Burke et al., 2001; Nodera and Kaji, 2006). In particular, axonal activation has been found to be followed by certain excitability recovery cycle as tested commonly after a supramaximal conditioning stimulus (e.g., Kiernan et al., 1996; Bostock et al., 1998; Murray and Jankelowitz, 2011) or after the cessation of maximal voluntary muscle contractions (Vagg et al., 1998; Kuwabara et al., 2001; Rossi et al., 2012). Traditionally, axon excitability properties were explored for whole motoneuronal pool, using a compound muscle action potential (CMAP), without analysing the behavior of single MUs. However, such approach gives no information on the excitability properties of motor axons belonging to different types of MUs. A few reports, beginning with the seminal studies of Bergmans (1970, 1973), addressed the excitability properties of single motor axons, as a rule, low-threshold to electrical stimulation and thus belonging to large MUs, high-threshold to voluntary muscle contraction (Borg, 1980; Bostock and Baker, 1988; Shefner et al., 1996; Hales et al., 2004; Bostock et al., 2005). At the same time there are no data on the excitability properties of axons belonging to small, slow MUs during their natural activation, while these MUs are essential part of motoneuronal pools as they are primarily activated during both voluntary movements and the maintenance of posture, as well as at reflex activation. The question arises of whether or not the excitability properties of these axons are similar to that of MUs with high-threshold to voluntary muscle contraction. Our findings reported below give some possibility to start the discussion of this question.

Distribution of Muscle Fibers in Skeletal Muscles of the African Elephant (Loxodonta africana africana)

The African elephant (Loxodonta africana africana) is the largest land animal on the earth, today. The structure and motion of the elephant are unusual compared with those of other animals. The most significant characteristic regarding the frame of the elephant is the legs, shaped like columns or pillars. The elephant supports its bulk with its straight legs and padded feet. It could be considered that the elephant needs less power to support the body. The elephant walks and swims, but cannot run (Gambaryan 1974; Hutchinson et al. 2006; Ren et al. 2008; Genin et al. 2010). Elephant moves with straighter limbs, and has limited speed and gait. The elephant cannot perform locomotion with an aerial phase. However, elephant has been reported to reach speeds of up to 40 km/h using a fast walk (Hutchinson et al. 2006). The elephant performs fast walking mainly by increasing the stride frequency (Biewener 2003; Hutchinson et al. 2006). The movements are produced by activation of the muscles. To understand movements during the locomotion of animals, studies of muscles are indispensable. In the elephant, the placement, origin, and insertion of skeletal muscles throughout the body have been performed by many researchers (Shindo and Mori 1956a, 1956b, 1956c; Gambaryan 1974; Mariappa 1986). However, to understand the function of skeletal muscles, we must studied the force and action produced by muscle. The skeletal muscles contain different types of muscle fiber (Burke 1981). Muscle fibers can be classified into Types I, IIa, IIb, and IIx by staining with monoclonal antibody for each myosin heavy chain (MHC) isoform and metabolic enzyme activities (Pette and Staron 1993, 1997). Type I is a muscle fiber with a high metabolic cost of maintenance and a small force output, Type IIa is a muscle fiber with a high metabolic cost of maintenance and larger force output, and Type IIb is a muscle fiber with a low metabolic cost for maintenance and the largest force output. Type IIx has intermediate characteristics between Types IIa and IIb. A single motor neuron and the muscle fibers that it innervates comprise a motor unit. The motoneuron properties are exquisitely matched to properties of the motor units supplying the muscles and properties of the muscles themselves (Burke 1981). There are systematic differences in the size, excitability, and corresponding variation of speed, power, and endurance in different types of motor unit. Motor units are classified into S, FR, FI, and FF types (Burke 1981). The muscle fibers in S, FR, FI, and FF types correspond to Types I, IIa, IIx, and IIb, respectively. Henneman (1981) showed the existence of a recruitment order among different types of motor unit on the activation of muscle. The recruitment of motor units is very important for motor performance. Studies on muscle fiber compositions are limited to humans and experimental or domestic animals: rat (Ariano et al. 1973; Hintz et al. 1980), cat (Ariano et al. 1973; Reichmann and Pette 1982), dog (Tonilo et al. 2007), horse (Van den Hoven et al. 1985; Kawai et al. 2009), and human (Johnson et al. 1973; Essen et al. 1975). In our previous study, we showed the muscle fiber composition in skeletal muscles from the body of the cheetah, domestic cat, and beagle dog (Goto et al. 2012). Our results indicate that the distribution of different types of muscle fiber reflects the kinematic characteristics of each animal, and studies of muscle fiber distribution are very important to understand animal locomotion. The most important point for studies of muscle fiber composition is the condition of muscles. We had a chance to sample muscles from the African elephant within 24 hours after death.

A Muscle’s Force Depends on the Recruitment Patterns of Its Fibers

Biomechanical models of whole muscles commonly used in simulations of musculoskeletal function and movement typically assume that the muscle generates force as a scaled-up muscle fiber. However, muscles are comprised of motor units that have different intrinsic properties and that can be activated at different times. This study tested whether a muscle model comprised of motor units that could be independently activated resulted in more accurate predictions of force than traditional Hill-type models. Forces predicted by the models were evaluated by direct comparison with the muscle forces measured in situ from the gastrocnemii in goats. The muscle was stimulated tetanically at a range of frequencies, muscle fiber strains were measured using sonomicrometry, and the activation patterns of the different types of motor unit were calculated from electromyographic recordings. Activation patterns were input into five different muscle models. Four models were traditional Hill-type models with different intrinsic speeds and fiber-type properties. The fifth model incorporated differential groups of fast and slow motor units. For all goats, muscles and stimulation frequencies the differential model resulted in the best predictions of muscle force. The in situ muscle output was shown to depend on the recruitment of different motor units within the muscle.

The contractile properties of the medial gastrocnemius motor units innervated by L4 and L5 spinal nerves in the rat

When a muscle innervation originates from more than one spinal cord segment, the injury of one of the respective ventral roots evokes an overload, and alters the activity and properties of the remaining motor units. However, it is not well documented if the three types of motor units are equally represented within the innervating ventral roots. Single motor units in the rat medial gastrocnemius muscle were studied and their contractile properties as well as distribution of different types of motor units belonging to subpopulations innervated by axons in L4 and L5 ventral roots were analyzed. The composition of the three physiological types of motor units in the two subpopulations was similar. Force parameters were similar for motor units belonging to the two subpopulations. However, the twitch time parameters were slightly longer in L4 in comparison to L5 motor units although the difference was significant only for fast resistant to fatigue motor units. The force–frequency relationships in the two subpopulations of motor units were not different. Concluding, the two subpopulations of motor units in the studied muscle differ in the number of motor units, but contain similar proportions of the three physiological types of these units and their contractile properties are similar. Therefore, the injury of one ventral root evokes various degrees of muscle denervation, but is non-selective in relation to the three types of motor units.

Modelling muscle forces: from scaled fibres to physiological task-groups

Muscles contain a collection of motor units that can have different mechanical properties. It should be expected that the mechanical output from a muscle partly depends on the particular motor units that are activated for a given task. However, muscle models used for biomechanical simulations typically assume that a whole muscle can be represented by a scaled-up muscle fibre. Some models allow the intrinsic properties of the muscle to adapt to the activation levels, but even these may miss important features of the muscle contractions. This paper will discuss how the activity from different types of motor units may be detected during a contraction, and will demonstrate how muscle models that incorporate distinct units result in improved predictions of muscle force.

A muscle architecture model offering control over motor unit fiber density distributions

The aim of this study was to develop a muscle architecture model able to account for the observed distributions of innervation ratios and fiber densities of different types of motor units in a muscle. A model algorithm is proposed and mathematically analyzed in order to obtain an inverse procedure that allows, by modification of input parameters, control over the output distributions of motor unit fiber densities. The model's performance was tested with independent data from a glycogen depletion study of the medial gastrocnemius of the rat. Results show that the model accurately reproduces the observed physiological distributions of innervation ratios and fiber densities and their relationships. The reliability and accuracy of the new muscle architecture model developed here can provide more accurate models for the simulation of different electromyographic signals.

Trophic factor expression in phrenic motor neurons

The function of a motor neuron and the muscle fibers it innervates (i.e., a motor unit) determines neuromotor output. Unlike other skeletal muscles, respiratory muscles (e.g., the diaphragm, DIAm) must function from birth onwards in sustaining ventilation. DIAm motor units are capable of both ventilatory and non-ventilatory behaviors, including expulsive behaviors important for airway clearance. There is significant diversity in motor unit properties across different types of motor units in the DIAm. The mechanisms underlying the development and maintenance of motor unit diversity in respiratory muscles (including the DIAm) are not well understood. Recent studies suggest that trophic factor influences contribute to this diversity. Remarkably little is known about the expression of trophic factors and their receptors in phrenic motor neurons. This review will focus on the contribution of trophic factors to the establishment and maintenance of motor unit diversity in the DIAm, during development and in response to injury or disease.

Electromyographic activity during the reflex pharyngeal swallow in the pig: Doty and Bosma (1956) revisited

The currently accepted description of the pattern of electromyographic (EMG) activity in the pharyngeal swallow is that reported by Doty and Bosma in 1956; however, those authors describe high levels of intramuscle and of interindividual EMG variation. We reinvestigated this pattern, testing two hypotheses concerning EMG variation: 1) that it could be reduced with modern methodology and 2) that it could be explained by selective detection of different types of motor units. In eight decerebrate infant pigs, we elicited radiographically verified pharyngeal swallows and recorded EMG activity from a total of 16 muscles. Synchronization signals from the video-radiographic system allowed the EMG activity associated with each swallow to be aligned directly with epiglottal movement. The movements were highly stereotyped, but the recorded EMG signals were variable at both the intramuscle and interanimal level. During swallowing, some muscles subserved multiple functions and contained different task units; there were also intramuscle differences in EMG latencies. In this situation, statistical methods were essential to characterize the overall patterns of EMG activity. The statistically derived multimuscle pattern approximated to the classical description by Doty and Bosma (Doty RW, Bosma JF. J Neurophysiol 19: 44-60, 1956) with a leading complex of muscle activities. However, the mylohyoid was not active earlier than other muscles, and the geniohyoid muscle was not part of the leading complex. Some muscles, classically considered inactive, were active during the pharyngeal swallow.

Simulation of the motor units control during a fast elbow flexion in the sagittal plane

The fact that muscles are composed of different Motor Units (MUs) is often neglected when investigating motor control by macro models of human musculo-skeletal-joint systems. Each muscle is associated with one control signal. This simplification leads to difficulties when mechanical and electrical manifestations of the muscle activity are juxtaposed. That is why a new approach for muscle modelling was recently proposed (Journal of Biomechanics 2002;35:1123–1135). It is based on MUs twitches and a Hierarchical Genetic Algorithm (HGA) is implemented for choosing the moments of activation of the individual MUs, thus simulating the control of the nervous system. Its basic benefit is obtaining the complete information about the mechanical and activation behaviour of all MUs, respectively muscles, during the whole motion. Its possibilities are demonstrated when simulating fast elbow flexion. Three flexor and two extensor muscles, each consisting of approximately real number of different types of MUs, are modelled. The task is highly indeterminate and the optimization is performed according to a fitness function that is an assessed combination of criteria (minimal deviation from the given joint moment, minimal total muscle force and minimal MUs activation). The influence of the weight of the first criterion (the one that reflects the importance of the movement accuracy on the predicted results), is investigated. Two variants concerning the muscle MUs structure are also compared: each muscle is composed of four distinct types MUs and the MUs twitch parameters are uniformly distributed.

Mechanomyograms recorded during evoked contractions of single motor units in the rat medial gastrocnemius muscle.

Acoustic phenomena accompanying contractions of single motor units (MUs) have previously received little attention. Therefore, in the present study, the mechanomyographic (MMG) signals during evoked contractions of single MUs have been recorded from the medial gastrocnemius muscle of the rat. A piezoelectric transducer immersed in a paraffin-oil pool was used for the measurement of these signals. Muscle fibre action potentials, tension and MMG were recorded in parallel during twitch (the weakest) and fused tetanic (the strongest) MU contractions. It was observed that the onset of the MMG signals was coincident with the beginning of the increase in tension for both the twitch and tetanus. Weaker MMG signals than those accompanying the beginning of the first phase of the fused tetanus were seen during the beginning of the relaxation after tetanic contraction. During contraction and relaxation, MMG signals were characterised by the reverse-direction of the first extreme phase, positive and negative, respectively. No MMG signals were observed when the tension was constant during the fused tetanus. The amplitude of MMG signals was correlated with both the tension increase and the velocity of tension increase during both the twitch and the fused tetanus. The strongest MUs (fast fatiguable) generated MMG signals of the highest amplitude. MMG signals were not detected for some of the weakest slow MUs (with tension increases of < or = 2 mN). These results indicate a strong correlation between the MMG and the change of tension. Therefore, we believe that MMG signals are generated by muscle deformation that occurs during the contraction of MU muscle fibres. We conclude that the number of active muscle fibres, their topography, and their localisation in relation to the muscle surface (which is variable for different types of MUs) influence these MMG phenomena.

Morphological adaptations of neuromuscular junctions depend on fiber type.

The neuromuscular junction (NMJ) forms the communicative link between motoneurons and muscle fibers. The properties of motoneurons and muscle fibers are matched in different types of motor units, which are recruited selectively to accomplish various motor behaviors. Motor units and muscle fibers can be classified based upon structural and functional properties, reflecting the essential match between motoneuron and muscle fiber. Using a three-color immunofluorescence technique combined with confocal microscopy, we examined the three-dimensional structure of pre- and postsynaptic elements of NMJs on different fiber types in the rat diaphragm muscle. On type I and IIa fibers, comprising slow-twitch and fast-twitch fatigue-resistant motor units, the structure of NMJs is far less complex than on type IIx6 and IIb fibers comprising fast-twitch fatigue-intermediate and fast-twitch fatigable motor units. We also found a greater extent of overlap between pre- and postsynaptic elements of NMJs on type I and IIa fibers. This review focuses on these normal phenotypic differences in NMJ properties and on the adaptations that occur under various conditions of altered use.

Motor control and kinetics during low level concentric and eccentric contractions in man

Motor unit (MU) recruitment patterns were studied in 6 female subjects during dynamic contractions at relative workloads corresponding to 10% maximum voluntary contraction. The contractions consisted of a 20° elbow flexion (concentric contraction) and extension (eccentric contraction) and MU action potential trains were recorded from the brachial biceps muscle. The mean angular velocity of the dynamic contractions was 10°/s, during which a total of 119 MUs were identified. Additionally, a few contractions were studied at 20°/s during which 30 MUs were identified, and 9 MUs during the 40°/s contraction. About 60% of the identified MUs were active during the concentric as well as the eccentric phase for each of the velocities. Mean firing rate decreased significantly when the contraction changed from concentric to eccentric, whereas the number and properties of identified active MUs were similar. This emphasizes firing rate modulation as important during low level dynamic contractions rather than selective recruitment of different types of MUs in the concentric versus the eccentric phase. Similar kinetic demands occur frequently in occupational tasks, especially during monotonous work. The present data indicate that only a limited pool of MUs are being recruited during such tasks. Extensive recruitment of these MUs may cause fatigue and start a potentially vicious circle leading to work-related muscle disorders.

Motor control and kinetics during low level concentric and eccentric contractions in man

Motor unit (MU) recruitment patterns were studied in 6 female subjects during dynamic contractions at relative workloads corresponding to 10% maximum voluntary contraction. The contractions consisted of a 20° elbow flexion (concentric contraction) and extension (eccentric contraction) and MU action potential trains were recorded from the brachial biceps muscle. The mean angular velocity of the dynamic contractions was 10°/s, during which a total of 119 MUs were identified. Additionally, a few contractions were studied at 20°/s during which 30 MUs were identified, and 9 MUs during the 40°/s contraction. About 60% of the identified MUs were active during the concentric as well as the eccentric phase for each of the velocities. Mean firing rate decreased significantly when the contraction changed from concentric to eccentric, whereas the number and properties of identified active MUs were similar. This emphasizes firing rate modulation as important during low level dynamic contractions rather than selective recruitment of different types of MUs in the concentric versus the eccentric phase. Similar kinetic demands occur frequently in occupational tasks, especially during monotonous work. The present data indicate that only a limited pool of MUs are being recruited during such tasks. Extensive recruitment of these MUs may cause fatigue and start a potentially vicious circle leading to work-related muscle disorders.

Motor Unit Recruitment and the Gradation of Muscle Force

The capabilities of the different types of motor units are reviewed, and their properties in a variety of muscles are discussed. Because the tension-generating capacities of motor units are so different, the order in which they are recruited will have a strong influence on the way force output of the whole muscle is graded. Activation of motor units in a random order produces a roughly linear force increase with progressive recruitment, whereas recruitment of motor units in order of increasing force produces an approximately exponential force increase as the number of active motor units increases. The latter scheme allows fine control of weak movements and rapid production of powerful movements. Motor units are shown to be well adapted to the tasks they must perform, and a "compromise" motor unit will not fulfill all the tasks demanded of it. Finally, changes in motor unit properties produced by different activity patterns and by muscle reinnervation are reviewed, and the implications for rehabilitation are discussed.

Current issues in arthrogenous inhibition.

Joint disease commonly results in severe weakness of associated muscles. Efforts to restore strength are often unsuccessful, even in the absence of pain. This is because of the underlying inhibition of motoneurones by afferent signals from in and around the affected joint, 'arthrogenous inhibition'. This phenomenon has received scant scientific attention, but several experimental techniques are now available with which it can be studied in man. Animal studies suggest possible neurophysiological mechanisms. Selective atrophy of different muscle fibre types, perhaps implying selective inhibition of different types of motor unit, remains unexplained, however. The severity of arthrogenous inhibition can be temporarily reduced by silencing afferent traffic but none of the techniques is yet generally applicable in practice. An alternative therapeutic approach is to produce involuntary muscle contractions by electrical stimulation. The effectiveness of therapeutic electrical stimulation may depend on the frequency and other characteristics of the stimulus.

Contractile properties of single motor units in two multi-tendoned muscles of the cat distal forelimb.

The contractile properties of motor units (MUs) in two multi-tendoned forelimb muscles were investigated. In anesthetized cats single MUs of the extensor carpi ulnaris (ECU) and extensor digitorum communis (EDC) muscles were selectively activated by stimulation of cervical ventral root filaments. MUs were characterized by various tests including single twitches, series of tetanic contractions providing a tension-frequency relation and a fatigue test. They were classified by the parameters contraction time (CT, time-to-peak within unpotentiated single twitches) and fatigue-index (RB, according to Burke). The ECU muscle is composed of 38% type FR MUs (fast, fatigue-sensitive; CT less than 38 ms; RB less than 0.5), 35% type FR MUs (CT less than 38 ms, RB greater than 0.5) and 27% type S MUs (slow; CT greater than 38 ms, RB greater than 0.5). 46% of the EDC MUs were classified as FF (RB less than or equal to 0.25), 29% as FI (fast, intermediately fatiguable; 0.25 less than RB less than 0.75) and 25% as FR/S (fatigue-resistant, fast or slow; RB greater than or equal to 0.75). The latter group was devised since most MUs appeared as fast and the unequivocal presence of slow MUs could neither be demonstrated nor excluded. Normalized tension-frequency relations of fast ECU and EDC MUs were nearly identical and similar to those reported for fast MUs of other muscles. In contrast to this, the tension-frequency relation of slow ECU MUs has a different shape supporting the use of this function to distinguish fast from slow MUs. The distribution of different types of MUs is discussed with regard to the structure and function of the parent muscles and in relation to hindlimb muscles of comparable architecture. As revealed by comparison to EMG data gained in behaving animals (Fritz et al. 1985; Hoffmann et al. 1986, Botterman et al. 1985), the three muscles of the cat distal forelimb investigated so far seem to be adapted to different tasks: the EDC to rapid movements with a high proportion of type FF MUs, flexor carpi radialis to sustained contractions during the body support with a high proportion of fatigue-resistant MUs; the ECU which changes synergism between both muscles has an intermediate composition.

Does orderly recruitment of motoneurons depend on the existence of different types of motor units?

It has recently been proposed that the recruitment of motoneurons is correlated with their type rather than their size. To test this hypothesis the axonal conduction velocities (CVs) of 92 pairs soleus motoneuron (all of the same histochemical type) were compared with their recruitment order. By means of spike-triggered averaging it has been shown that in 89 out 92 pairs of soleus units the motoneuron with the lower CV was recruited first. The results indicate that orderly recruitment occurs in the absence of different types of motoneurons and is correlated with cell size within a cell type.