Neuromuscular Control

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The mechanical response of muscles also strongly depends on how the muscles are activated. The neuromuscular control of movement is an active area of study where biomechanical research methods have been particularly useful. This section will summarize the important structures and their functions in the activation of muscles to regulate muscle forces and movement.

The Functional Unit of Control: Motor Units

The coordination and regulation of movement is of considerable interest to many scholars. At the structural end of the neuro-muscular control process are the functional units of the control of muscles: motor units. A motor unit is one motor neuron and all the muscle fibers it innervates. A muscle may have from a few to several hundred motor units. The activation of a motor axon results in stimulation of all the fibers of that motor unit and the resulting twitch. All fibers of a motor unit have this synchronized, "all-or-nothing" response. Pioneering work in the neurophysiology of muscle activation was done in the early 20th century by Sherrington, Arian, and Denny-Brown (Burke, 1986).

Application: Force-Time and Range-of-Motion Principle Interaction

Human movements are quite complex, and several biomechanical principles often apply. This is a challenge for the kinesiology professional, who must determine how the task, performer characteristics, and biomechanical principles interact. In the sport of weight lifting, coaches know that the initial pull on the bar in snatch and clean-and-jerk lifts should not be maximal until the bar reaches about knee height. This appears counter to the Force-Time principle, where maximizing initial force over the time of the lift seems to be advantageous. It turns out that there are ranges of motion (postural) and muscle mechanical issues that are more important than a rigid application of the Force-Time principle. The whole-body muscular strength curve for this lift is maximal near knee level, so a fast bar speed at the strongest body position compromises the lift because of the decrease in muscle forces in increasing speed of concentric shortening (Garhammer, 1989; Zatsiorsky, 1995). In other words, there is a Force-Motion advantage of a nearly-maximal start when the bar reaches knee level that tends to outweigh maximal effort at the start of the movement. olympic lifts require a great deal of practice and skill.The combination of speed and force, as well as the motor skills involved in olympic lifting, makes these whole-body movements popular conditioning exercises for high power sports (Garhammer, 1989).

Regulation of Muscle Force

If the muscle fibers of a motor unit twitch in unison, how does a whole muscle generate a smooth increase in tension? The precise regulation of muscle tension results from two processes: recruitment of different motor units and their firing rate.

Recruitment is the activation of different motor units within a muscle. Physiological research has determined three important properties of recruitment of motor units. First, motor units tend to be organized in pools or task groups (Burke, 1986). Second, motor units tend to be recruited in an asynchronous fashion. Different motor units are stimulated at slightly different times, staggering the twitches to help smooth out the rise in tension. There is evidence that some motor unit synchronization develops to increase rate of force development (Semmler, 2002), but too much synchronous recruitment results in pulses of tension/tremor that is associated with disease (Parkinson's) or extreme fatigue (final repetition of an exhaustive set of weight lifting). The recruitment of motor units is likely more complex than these general trends since serial and transverse connections between parallel architecture muscles allows active fibers to modify the tension and length of nearby fibers (Sheard, 2000).

The third organizational principle of recruitment has been called orderly recruitment or the size principle (Denny-Brown & Pennybacker, 1938; Henneman, Somjen, & Carpenter, 1965). It turns out that motor units tend to have specialized innervation and homogeneous fiber types, so motor units take on the characteristics of a particular fiber type. A small motor unit consists of a motor axon with limited myelination and primarily SO muscle fibers, while a large motor unit has a large motor axon (considerable myelination) and primarily FG fibers. The recruitment of a large motor unit by the brain results in the quickest message and build-up in tension, while recruitment of a small motor unit has a slower nerve conduction velocity and a gradual tension build-up (Figure 4.17).

In essence, the size principle says that motor units are recruited progressively from small (slow-twitch) to large (fast-twitch). A gradual increase in muscle force would result from recruitment of SO dominant motor units followed by FOG and FG dominant units, and motor units would be derecruited in reverse order if the force is to gradually decline. This holds true for most movements, but there is the ability to increase firing rate of large motor units within the size principle to move quickly or rapidly build up forces (Bawa, 2002; Burke, 1986). Have you ever picked up a light object (empty suitcase) when you expected a heavy one? If so, you likely activated many pools of large and small motor units immediately and nearly threw the object. Athletes in events requiring high rates of force development (jumping, throwing) will need to train their ability to override the size principle and activate many motor units rapidly. There are also many other factors that complicate the interpretation that the size principle is an invariant in motor control (Enoka, 2002). One example is that recruitment tends to be patterned for specific movements (Desmedt & Godaux, 1977; Sale, 1987), so the hamstring muscles may not be recruited the same in a jump, squat, or knee flexion exercise. Activation of muscles also varies across the kinds of muscle actions (Enoka, 1996; Gandevia, 1999; Gielen, 1999) and can be mediated by fatigue and sensory feedback (Enoka, 2002).

Firing rate or rate coding is the repeated stimulation of a particular motor unit over time. To create the muscle forces for normal movements, the frequency (Hz) that motor units are usually rate coded is between 10 and 30 Hz, while FG motor units have a faster relaxation time and can be rate coded between 30 and 60 Hz (Sale, 1992). The re-

Muscle Unit Synchronization

Interdisciplinary Issue:The Control of Movement

With hundreds of muscles, each with hundreds of motor units that must be repeatedly stimulated, to coordinate in a whole-body movement, can the brain centrally control all those messages? If the brain could send all those messages in a preprogrammed fashion, could it also monitor and evaluate efferent sensory and proprioceptive information and adjust the movement? Early motor learning research and theory focused on the brain's central control of movement or a motor program. More recent research is based on a Bernstein or dynamical systems perspective (Feldman, Levin, Mitnitski, & Archambault, 1998; Schmidt & Wrisberg, 2000), where more general control strategies interact with sensory feedback. Since kinetic variables (torques, forces, EMG) can be measured or calculated using biomechanics, many motor control scholars are interested in looking at these variables to uncover clues as to how movement is coordinated and regulated. Some biomechanists are interested in the control of movement, so here is an ideal area for interdisciplinary research.

peated stimulation of a motor unit increases the twitch force above the level of a single twitch (up to 10 times) because the tension in the fibers begins at a higher level, before the decay or relaxation in tension. Since recruitment tends to be asynchronous and firing rates vary with motor unit size, the twitches of the motor units in a whole muscle combine and fill in variations, resulting in smooth changes in tension. When muscle is artificially stimulated for research or training purposes to elicit maximal force, the frequency used is usually higher than 60 Hz to make sure that motor unit twitches fuse into a tetanus. A tetanus is the summation of individual twitches into a smooth increase in muscle tension.

Both recruitment and firing rate have a dramatic influence on the range of muscle forces that can be created. How recruitment and firing rate interact to increase muscle forces is quite complex, but it appears that recruitment dominates for forces up to 50% of maximum with increasing importance of firing rate (Enoka, 2002). The combined effect of recruitment and firing rate of motor units is reflected in the size, density, and complexity of the eletromyographic (EMG) signal. Special indwelling EMG electrode techniques are used to study the recruitment of individual motor units (Basmajian & DeLuca, 1985).

Recall that in chapter 3 we learned how EMG research has shown that at the whole muscle level muscles are activated to in complex synergies to achieve movement or stabilization tasks. Muscles are activated in short bursts that coordinate with other forces (external and segmental interactions) to create human movement. Figure 4.18 shows the lower extremity muscle activation in several pedal strokes in cycling. Compare the pattern of activation in Figures 4.13 and 4.18. Physical medicine professionals often take advantage of this flexibility of the neuromuscular system by training muscle actions that compensate for

Application: Neuromuscular Training

Unfortunately, athletes are often stereotyped as dumb jocks with gifted physical abilities. How much of movement ability do physical characteristics like muscular strength, speed, and coordination contribute to performance compared to neu-romuscular abilities (a good motor brain)? Think about the ability your favorite athlete would have if he/she had a stroke that affected part of their motor cortex. In training and conditioning there are several areas of research where there is evidence that the effects of training on muscle activation by the central nervous system is underrated. First, it is well known that the majority of the initial gains in strength training (first month) are related to the neural drive rather than hypertrophy (see Sale 1992). Second, it is known that both normal and injured subjects are not usually able to achieve true maximum muscle force in a maximal voluntary contraction. This is called muscle inhibition and is studied using an electrical stimulation method called twitch interpolation technique (Brondino, Suter, Lee, & Herzog, 2002). Another area of neuromuscular research relates to the inability to express bilateral muscular strength (both arms or legs) equal to the sum of the unilateral strength of each extremity.This phenomenon has been called the bilateral deficit but the decrements (3-20%) are not always observed (Jakobi & Cafarelli, 1998). Interest in the biomechanics of the vertical jump has made this movement a good model for examining a potential bilateral deficit (Challis, 1998). How might a professional try to differentiate true differences in muscular strength between sides of the body and a bilateral deficit? If there truly is a bilateral deficit that limits the neuromuscular activation of two extremities, how should you train for bilateral movements (bilaterally, stronger or weaker limb)?

Electromyographic Olympic Snatch
Figure 4.18. Raw EMG of leg muscles in cycling. The position of top dead center (vertical pedal position: T) is indicated by the line. Reprinted from Laplaud et al., Journal of Electromyography and Kinesiology © (2006), with permission from Elsevier.

physical limitations from disease or injury. Motor learning scholars are interested in EMG and the activation of muscles as clues to neuromuscular strategies in learning movements. While there has not been extensive research in this area, it appears that changes in EMG with practice/training depend on the nature of the task (Gabriel & Boucher, 2000). As people learn submaximal movements, the duration of EMG bursts decrease, there are decreases in extraneous and coactivation of muscles, and a reduction in EMG magnitude as the body learns to use other forces (inertial and gravitational) to efficiently create the movement

(Englehorn, 1983; Moore & Marteniuk, 1986; Newell, Kugler, van Emmerick, & McDonald, 1989). Maximal-effort movements are believed to be more reliant on changes in the magnitude and rise time of activation, than the duration of muscle activation (Gottlieb, Corcos, & Agarwal, 1989). In maximal high-speed movements, the magnitude and rate of increase in activation tends to increase (Corcos, Jaric, Agarwal, & Gottlieb, 1993; Darling & Cooke, 1987; Gabriel & Boucher, 2000) with practice. The activation and cooperative actions of muscles to create skilled human movement are very complex phenomena.

Proprioception of Muscle Action and Movement

Considerable information about the body and its environment are used in the regulation of many movements. While persons use all their senses to gather information about the status or effectiveness of their movements, there are musculoskeletal receptors that provide information to the brain to help produce movement. These receptors of information about the motion and force in muscles and joints are called proprioceptors. While we usually do not consciously attend to this information, this information and the various reflexes they initiate are important in the organization of movement. A reflex is an involuntary response initiated by some sensory stimulus. Reflexes are only initiated if the sensory stimulus is above some threshold.

There are many proprioceptive receptors that monitor aspects of movement. Information about joint position is provided by four kinds of receptors. The vestibular system of the inner ear provides information about the head's orientation with respect to gravity. This section will summarize the important MTU proprioceptors that provide information on muscle length (muscle spindles) and force (Golgi tendon organs). Human movement performance relies on an integration of all sensory organs, and training can be quite effective in utilizing or overriding various sensory or reflex responses. A dancer spinning in the transverse plane prevents dizziness (from motion in inner ear fluid) by spotting—ro-tating the neck opposite to the spin to keep the eyes fixed on a point followed by a quick rotation with the spin so as to find that point again. Athletes in "muscular strength" sports not only train their muscle tissue to shift the Force-Velocity Relationship upward, they train their central nervous system to activate more motor units and override the inhibitory effect of Golgi tendon organs.

When muscle is activated, the tension that is developed is sensed by Golgi tendon organs. Golgi tendon organs are located at the musculotendinous junction and have an inhibitory effect on the creation of tension in the muscle. Golgi tendon organs connect to the motor neurons of that muscle and can relax a muscle to protect it from excessive loading. The intensity of this au-togenic inhibition varies, and its functional significance in movement is controversial (Chalmers, 2002). If an active muscle were forcibly stretched by an external force, the Golgi tendon organs would likely relax that muscle to decrease the tension and protect the muscle. Much of high speed and high muscular strength performance is training the central nervous system to override this safety feature of the neuromuscular system. The rare occurrence of a parent lifting part of an automobile off a child is an extreme example of overriding Golgi tendon organ inhibition from the emotion and adrenaline. The action of Golgi tendon organs is also obvious when muscles suddenly stop creating tension. Good examples are the collapse of a person's arm in a close wrist wrestling match (fatigue causes the person to lose the ability to override inhibition) or the buckling of a leg during the great loading of the take-off leg in running jumps.

Muscle spindles are sensory receptors located between muscle fibers that sense the length and speed of lengthening or shortening. Muscle spindles are sensitive to stretch and send excitatory messages to activate the muscle and protect it from stretch-related injury. Muscle spindles are sensitive to slow stretching of muscle, but provide the largest response to rapid stretches. The rapid activation of a quickly stretched muscle (100-200 ms) from muscle spindles is due to a short reflex arc. Muscle spindle activity is responsible for this myo-

Interdisciplinary Issue:

Muscle Inhibition and Disinhibition

The neuromuscular aspects of training and detraining are fertile areas for the cooperation of scholars interested in human movement. Rehabilitation (physical therapists, athletic trainers, etc.) and strength and conditioning professionals, as well as neurophysiologists, and bio-mechanists all might be involved in understanding the inhibition of muscle activation following an injury. They might also collaborate on research questions if the neuromuscular changes in strength development are similar in strength redevelopment following injury and disuse.

tatic reflex or stretch reflex. Use of a small rubber reflex hammer by physicians allows them to check the stretch reflex responses of patients. The large numbers of spindles and their innervation allows them to be sensitive and reset throughout the range of motion. Recall that a stretch reflex is one possible mechanism for the benefit of an SSC. Stretch reflexes may contribute to the eccentric braking action of muscles in follow-throughs. In performing stretching exercises, the rate of stretch should be minimized to prevent activation of muscle spindles.

The other important neuromuscular effect of muscle spindles is inhibition of the antagonist (opposing muscle action) muscle when the muscle of interest is shortening. This phenomenon is call reciprocal inhibition. Relaxation of the opposing muscle of a shortening muscle contributes to efficient movement. In lifting a drink to your mouth the initial shortening of the biceps inhibits triceps activity that would make the biceps work harder than necessary. Reciprocal inhibition is often overridden by the central nervous system when coactiva-tion of muscles on both sides of a joint is needed to push or move in a specific direction. Reciprocal inhibition also plays a role in several stretching techniques designed to utilize neuromuscular responses to facilitate stretching. The contract-relax-ago-nist-contract technique of proprioceptive neuromuscular facilitation (PNF) is designed to use reciprocal inhibition to relax the muscle being stretched by contracting the opposite muscle group (Hutton, 1993; Knudson, 1998). For example, in stretching the hamstrings, the stretcher activates the hip flexors to help relax the hip extensors being stretched. The intricacies of proprio-ceptors in neuromuscular control (Enoka, 2002; Taylor & Prochazka, 1981) are relevant to all movement professionals, but are of special interest to those who deal with disorders of the neuromuscular system (e.g., neurologists, physical therapists).

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