Muscle produces force and movements that can vary in magnitude, speed, and precision. The variety of force profiles and movements depends on both peripheral factors, such as the anatomy and fiber type composition of muscles, and central factors such as the motor commands. The muscle, no matter how sophisticated in design and composition, acts in response to neural commands to produce the required range of motor outputs.
Anatomically, each muscle is innervated by a group of motoneurons known as the motoneuron pool. The neuroarchitectural and biophysical properties of individual members of a motoneuron pool vary over a wide range (1,2). Some of these properties include the membrane surface area (size) of the cell body including dendrites, conduction velocity of the axon, input resistance, afterhyperpolarization, and terminal arborization that determine the number of muscle fibers innervated by the motoneuron. The values of these properties vary within a motoneuron pool and across motoneuron pools depending on the functions of the innervated muscle (e.g., hand vs postural leg muscles). Each motoneuron innervates a group of muscle fibers forming a motor unit; properties of muscle fibers composing a motor unit are quite similar (Fig. 1). The properties of the motoneurons are complementary to the properties of the innervated muscle fibers; in general, the smaller motoneurons innervate a small number of slow-contracting, fatigue-resistant muscle fibers, whereas larger motoneurons in the pool will innervate a greater number of fast-contracting, easily fatigued muscle fibers (2).
The sources and types of inputs to motoneurons are also numerous. Motoneurons receive inputs from the cortex, brain stem, spinal cord, and directly from the sensory afferents (1,2,7). It is the interaction between the synaptic inputs and the biophysical properties of the motor units that provides an enormous force and movement repertoire to which an individual is accustomed. Although many scientists have examined the question of the activation patterns of motoneurons and control of muscle during the 20th century, only Henneman’s size principle has stood the test of time. According to the size principle, during any muscle contraction, the smaller, slow-contracting and fatigue-resistant motor units are recruited before the larger, fast-contracting fatigable units (7). The statement appears to be simple but it has required in-depth studies on motoneurons, muscle fibers, and afferent and cortical inputs to the spinal cord using a combination of electrophysiological, histological, anatomical, and modeling techniques to understand the arrangement of the neuromuscular system underlying the control of motor units. For detailed treatment of the subject of recruitment, inputs to motoneurons, and properties of motor units, the reader is encouraged to read previous reviews by Binder et al. (1), Burke (2), Calancie and Bawa (3), Enoka and Fuglevand (5), and Henneman and Mendell (7). This review will update the information on recruitment and rate coding of motor units in humans and discuss optimization of force. Because each one of us likes to improve our motor performance, the presence of plasticity in the normal adult motor system and the effects of training are discussed in later parts of the review.
RECRUITMENT IN SIMPLE MUSCLES
We define a simple muscle as one with a single, narrow tendon of origin and insertion such as first dorsal interosseous, and the primary wrist extensors and flexors. Every muscle, no matter how simple, contributes to contractions in many directions. In such muscles, motor units recruited in one direction are also recruited for the other directions, and the order of recruitment of the individual motor units remains the same (8) (Fig. 2). This implies that, for such muscles, force output in different directions is adjusted not by activation of different subgroups of motor units, but simply by different force vectors (3).
Studies on simple muscles and with simple contraction paradigms are important because they allow one to observe results clearly. Different laboratories can repeat the results, and build upon the previous experiments. However, the majority of muscles do not have a simple anatomy.
COMPLEX MUSCLES AND TASK GROUPS
Examples of complex muscles are biceps brachii, deltoid, and extensor digitorum communis (EDC); these muscles have multiple heads and/or tendons of insertion. By not considering the complex architecture of the muscle, a selective recruitment of motor units was initially proposed by several authors when recording from such muscles. Working on biceps brachii, the Dutch group of ter Haar Romeny and Gielen (see Ref. (1)) proposed selective recruitment of motor units during different tasks. What was not realized at that time was that the observed “selective” recruitment did not implicate that one could recruit any motor unit irrespective of the size of the motor unit, thus contradicting the size principle. What it meant, as later realized by the same authors, was that in complex muscles, motor units form subgroups, and the composition of the subgroup depends on the task. Within each subgroup or “task group,” recruitment occurs according to the size principle. In the author’s laboratory, recordings from EDC motor units were made while subjects performed different isometric tasks: extension of the index finger (IF), the middle finger (MF), the ring finger (RF), or the two fingers together (IF + MF or MF + RF), or extension of the wrist with the fingers relaxed. It was observed that for extension of each individual finger a separate subpopulation of EDC motor units was recruited. For extension of two fingers together, the subpopulations of the two fingers merged to form a composite subpopulation. Motor units were recruited in an orderly fashion from small to large within each subpopulation and within each composite subpopulation (Fig. 2, EDC). The existence of subpopulations does not undermine the size principle; in fact, it extends it from a motoneuron pool to a task group (see Riek and Bawa in (1)). From critical assessment of the literature, it would not be too farfetched to claim that the orderly recruitment, from small to large, holds for all types of normal contractions of limb muscles.
RATE CODING AND SPEED OF CONTRACTION
In 1973, Stein and his collaborators at the University of Alberta (see Milner-Brown et al. (1,3)) demonstrated the importance of rate coding in modulation of force output. When one wants to increase force while new, larger units are recruited, the already-recruited units increase their firing rates. The relationship of recruitment and rate modulation differs between the distal muscles and the postural muscles (5,14). In small hand muscles with very small motor units, recruitment of additional motor units is the dominant mechanism at lower forces. Force contribution of each unit is small, and therefore the addition does not cause abrupt changes in force. In muscles in which large motor units are involved, increases in firing rate increase force output before an additional unit is recruited. Rate coding does not seem to occur in postural muscles when contractions have to be maintained for long periods of time (14). Fast rates may fatigue motoneurons, thus preventing maintenance of prolonged postures.
Increases in the magnitude of force are produced by small changes in firing rates of the active units (Fig. 3, A and B). For performance and training, the strength and speed of the onset of contraction are very important. Electromyographic (EMG) recordings from a contracting muscle show a burst of electrical activity at the start of brisk contractions (Fig. 3 C). At the level of single motor units, a motoneuron initially discharges very short one or two interspike intervals at the onset of brisk contractions (Fig. 3 C). This short burst not only increases the rate of rise of force, but also the amount of peak force. The higher the initial firing rate of the motoneuron, the higher the rate of force generation. Furthermore, the initial rate of rise of total muscle force is also increased by a phasic recruitment of higher threshold motor units. These larger motor units fire one or two impulses just to enhance the rate of rise of force and then drop out, leaving the lower threshold units to maintain the required constant force (12) (see more on these short intervals under “Training” sections). Fast contractions do not recruit fast-contracting units preferentially, that is, without also recruiting the slower-contracting units. The size-ordered recruitment appears to be rigid; it simplifies the task of the motor areas of the brain and the spinal cord, yet allows flexibility for subtle changes in force, large changes in force, and production of fast speeds (7,11).
SIZE-ORDERED RECRUITMENT AND SYNAPSE DISTRIBUTION
There are several proposals about the quantitative nature of inputs to a group of motoneurons explaining the size-ordered recruitment pattern. An equal synaptic input to every motoneuron will tend to recruit smaller motoneurons due to their higher input resistance. Similarly, an equal density of synapses favors the size principle as well. The distribution has been investigated in depth for the spindle inputs to the triceps surae motoneuron pool in the cat (7). Heckman and Binder demonstrated larger synaptic currents in smaller motoneurons, and these currents decreased with increasing motoneuron size (see (1)). Recent human work suggests that the motor cortical inputs to the motoneuron pool may be arranged similarly to those of spindle inputs (9). Both inputs recruit motor units in order of their size. The rising phases of the excitatory postsynaptic potentials produced by these two inputs are temporally identical suggesting that the synapses from these two sources are positioned quite similarly on the motoneurons. This should not imply that that the distribution of all other excitatory synaptic inputs is similar (for details, see (1)). Because the corticospinal and the 1a afferent inputs make powerful monosynaptic connections with motoneurons, under physiological conditions these inputs may bias recruitment to occur from small to large, even though synaptic inputs from some of the other pathways may not be arranged as such (6). For example, the electrical stimulation of cutaneous afferents and some descending brainstem pathways has been clearly shown to preferentially excite the large motoneurons and inhibit the small ones (1). Yet behaviorally such reversed recruitment has not been observed. One may argue that electrical stimulation is not physiological. Although it is true, electrical stimulation of primary spindle afferents or the cortex recruits motoneurons from small to large (3). The comparison of such observations suggests that, among members of a motoneuron pool, the effective distribution of inputs from cutaneous sources is quantitatively different compared with those from the spindle afferents and the motor cortex.
TRAINING EFFECTS INPUTS TO MOTONEURONS
Elite athletes, convalescent patients, and even an ordinary person sitting in front of a television set would like to strengthen their muscles and improve their performance. It is a common experience that we can all strengthen our muscles with training (4). Can we improve the central control of the muscle? What is the effect on motor unit recruitment and motor unit firing patterns? Training motor units would require changes in the synaptic inputs to motoneurons (both descending and reflex), changes in motoneurons themselves, and changes in innervated muscle fibers.
Figure 4 is a schematic that illustrates the various neural components one needs to examine for the effects of training in the motor system. Multisite plasticity is essential so that along each communicating channel the pre- and postsynaptic elements change in concert. There is ample evidence from human and animal studies of the effects of various types of training on muscle fiber types (4). Each type of training, namely endurance, sprint, or resistance training, produces appropriate changes in the muscle, but we are not fortunate with the information available on the neural elements. Most of the information on neural adaptation comes from developing, aging, and clinical populations of subjects rather than from studies examining the effects of exercise (or training) on normal adults. The available information from other populations should be extrapolated to normal adult humans with caution, because a developing system is dynamic and can be modified to a great extent with practice. In aging and injured systems, certain inputs are removed, and neurons left behind can sprout to take over the emptied spaces. Such is not the case when training a normal adult system. Let us summarize some of the information available on plasticity of various parts of the motor system.
CHANGES IN SUPRASPINAL CENTERS
Our every day experience tells us that there is evidence of plasticity in the adult motor system. For example, mental imaging of a movement improves both learning and performance. This is a clear example of neural adaptation, but where is the learning and adaptation occurring? Learning and adaptation probably occur at all levels, including the pre-primary motor cortex (pre-M1) areas. The pre-M1 areas, which include the cerebellum and basal ganglia, are more difficult to study because of their complexity and poor accessibility. The primary motor cortex, on the other hand, is more accessible to the experimenters, and therefore experimental data exist. Contrary to what we understand from classical homunculi, M1 does not have a strict somatotopy. Though the leg area is distinct from the arm area, the divisions within one limb of the homunculus are not clearly demarcated for each joint or muscle (10). There is a broad connectional organization that makes the system quite flexible and dynamic. It has been suggested that the balance between inhibition and excitation determines the areas dedicated to certain muscles. From animal and human studies, it appears that this balance between inhibition and excitation changes with practice, and can occur quickly, that is, within hours. In addition to the fast changes in the balance between excitation and inhibition, there may be long-term changes in strength of existing synapses, and formation of new synapses. The motor cortex is also capable of motor learning (10). The physiological mechanisms for plasticity and learning and their time course are not yet well established.
TRAINING AFFECTS MOTONEURONS AND REFLEXES
The muscle fibers of a motor unit change with training; does the motoneuron change as well? In “Rate Coding and Speed of Contraction,” it was mentioned that motoneurons fire very short interspike intervals to start a brisk contraction. In human subjects, training with dynamic contractions has provided evidence of a decrease in such initial interspike intervals, and more synchronous firing of other motor units at the start of a brisk contraction (13). Do these observations mean that there are changes in motoneurons, or is the descending input to the motoneurons more synchronized? There is convincing evidence of changes in motoneuron properties in behaving monkeys (15). Some information is also available on changes in the excitability of motoneuron, its conduction velocity and firing rate, increases in firing of doublets, increases in synchronization of motoneurons, changes in protein synthesis, and axonal transport of these proteins. No change in recruitment order of motoneurons has ever been shown. These studies are tedious, and the changes observed are generally small. Much more carefully obtained data are needed in this area to understand changes in control of muscle.
A few reflex pathways that are suggested to change with training are illustrated in Figure 4. Changes seem to occur in the gain of reflexes and adaptation of muscle afferents. Adaptation in recurrent inhibition and presynaptic inhibition may also play a role during training. This is an area wide open for future, well-designed experiments. Should reflexes become more or less dominant with training? Is the gain of reflexes reduced with training in order for the cortex to have a larger influence, or is the gain increased in order to leave less in the control of higher centers? The answers to such questions are sparse, and when changes are shown, they are not as dramatic as those shown during development and aging. It has been shown that adaptation in the neuromuscular system will optimize only the practiced movement, and not the other movements in which the neuromuscular elements are involved. The reader is encouraged to read the two excellent reviews by Sanes and Donoghue (10) and Wolpaw and Tennissen (15), both of which cover quite distinct areas on the subject of plasticity of the motor system.
CHANGES IN SUPRASPINAL AND SPINAL NEURONS
Different classes of elite athletes and pianists have been tested for motor unit properties, and there is no indication of preferential recruitment of larger fast motor units. This implies that improvement of the motor performance includes changes in various parts of the motor system, yet the size-ordered recruitment is inherent to optimized system (11). If the nervous system activates motor units always in the stereotypical pattern, from small to large, then to train motor units with voluntary activation one has to start always by activating the smallest ones and then progressively activating the larger ones. How can one selectively train the larger units? Physiologically, one would have to activate the muscles maximally to recruit and train the largest units. On the other hand, one could electrically stimulate the motor nerve to activate the largest units selectively depending on strength of stimulation. It must be emphasized that the benefits of weak electrical stimulation of the motor nerve are largely confined to the muscle being stimulated. Strong contractions of large muscles do benefit the cardiorespiratory system as well. Still, the benefits to other body systems are not the same as those brought about by voluntary activation of the motor system. Voluntary activation trains the whole neuromuscular system concordantly, in addition to bringing relevant changes in systems other than the motor system.
Five decades of systematic work on the question of recruitment of motoneurons have produced quite convincing evidence that, under all normal conditions, motor units of limb muscles are recruited in an orderly fashion. Recruitment and rate coding control force and rate of change of force. We know that the motor system is plastic, and therefore it can be trained. However, systematic data are missing on the effects of training on various components of the nervous system involved in motor control. This area is wide open for well-designed studies.
1. Binder M.D., Heckman, C.J. Powers. R.K. The physiological control of motoneuron activity. In: Handbook of Physiology, Exercise: Regulation and Integration of Multiple Systems, edited by Rowell L.B. Shepherd. J.T. New York: Oxford University Press, 1996, p. 3–53.
2. Burke, R.E. Motor units. Anatomy, physiology, and functional organization. In: Handbook of Physiology, Motor Control, Part I, edited by Brooks. V.B. Bethesda, MD: American Physiological Society, 1981, p. 345–422.
3. Calancie, B. Bawa. P. Motor unit recruitment
in humans. In: The Segmental Motor System, edited by Binder E.D. Mendell L.M.. New York: Oxford University Press, 1990, p. 75–95.
4. Edström, L. Grimby. L. Effect of exercise on the motor unit
. Muscle Nerve. 9: 104–126, 1986.
5. Enoka, R.M. Fuglevand. A.J. Motor unit
physiology: some unresolved issues. Muscle Nerve. 24: 4–17, 2001.
6. Haftel V.K., Prather, J. F. Heckman, C. J. Cope. T.C Recruitment
of cat motoneurons
in absence of homonymous afferent feedback. J. Neurophysiol. 86: 616–628, 2001.
7. Henneman, E. Mendell. L.M. Functional organization of motoneuron pool and its inputs. In: Handbook of Physiology, Motor Control, Part I, edited by Brooks. V.B. Bethesda, MD: American Physiological Society, 1981, p. 423–507.
8. Jones, K.E., Bawa, P. McMillan. A.S. Recruitment
of motor units in human
flexor carpi ulnaris. Brain Res. 602: 354–356, 1993.
9. Jones, K.E., Calancie B, B. Hall, A. Bawa. P. Comparison of peripheral 1a and corticomotoneuronal composite EPSPs in human motoneurons
. Electroencephalogr. Clin. Neurophysiol. 101: 431–437, 1996.
10. Sanes, J.N. Donoghue. J.P. Plasticity and primary motor cortex. Annu. Rev. Neurosci. 23: 393–415, 2000.
11. Senn, W.E., Wyler, K. Clamann, H.P. Kleinle, J. Lüscher, H-R Müller. L. Size principle and information theory. Biol. Cybern. 76: 11–22, 1997.
12. Smith, L., Zhong, T. Bawa. P. Nonlinear behaviour of human motoneurons
. Can. J. Physiol. Pharmacol. 73: 113–123, 1995.
13. Van Cutsem, M., Duchateau, J. Hainaut. K. Changes in single motor unit
behaviour contribute to the increase in contraction speed after dynamic training
in humans. J. Physiol. 513: 295–305, 1998.
14. Westguard, R.H. De Luca. C.J. Motor control of low-threshold motor units in the human
trapezius muscle. J. Neurophysiol. 85: 1777–1781, 2001.
15. Walpow, J.R. Tennissen. A.M. Activity-dependent spinal cord plasticity in health and disease. Annu. Rev. Neurosci. 24: 807–843, 2001.