34: The Motor Unit and Muscle Action

• The Motor Unit Is the Elementary Unit of Motor Control

  • A Motor Unit Consists of a Motor Neuron and Multiple Muscle Fibers

  • The Properties of Motor Units Vary

  • Physical Activity Can Alter Motor Unit Properties

  • Muscle Force Is Controlled by the Recruitment and Discharge Rate of Motor Units

  • The Input–Output Properties of Motor Neurons Are Modified by Input from the Brain Stem

• Muscle Force Depends on the Structure of Muscle

  • The Sarcomere Contains the Contractile Proteins

  • Noncontractile Elements Provide Essential Structural Support

  • Contractile Force Depends on Muscle Fiber Activation, Length, and Velocity

  • Muscle Torque Depends on Musculoskeletal Geometry

• Different Movements Require Different Activation Strategies

  • Contraction Velocity Can Vary in Magnitude and Direction

  • Movements Involve the Coordination of Many Muscles

  • Muscle Work Depends on the Pattern of Activation

• An Overall View

Any action—ascending a flight of stairs, typing on a keyboard, even holding a pose—requires coordinating the movement of body parts. This is accomplished by the interaction of the nervous system with muscle. The role of the nervous system is to activate just those muscles that will exert the force needed to move in a particular way. This is not a simple task: Not only must the nervous system decide which muscles to activate and how much to activate them in order to move one part of the body, but it must also control muscle forces on other body parts and maintain posture.

This chapter examines how the nervous system controls muscle force and how the force exerted by a limb depends on muscle structure. We also describe how muscle activation differs with different types of movement.

A Motor Unit Consists of a Motor Neuron and Multiple Muscle Fibers

The nervous system controls muscle force with signals sent from motor neurons in the spinal cord to the muscle fibers. A motor neuron and the muscle fibers it innervates are known as a motor unit, the basic functional unit by which the nervous system controls movement, a concept proposed by Charles Sherrington in 1925.

A typical muscle is controlled by a few hundred motor neurons whose cell bodies are clustered in a motor nucleus in the spinal cord or brain stem (Figure 34–1). The axon of each motor neuron exits the spinal cord through the ventral root or through a cranial nerve in the brain stem and runs in a peripheral nerve to the muscle. When the axon reaches the muscle, it branches and innervates from a few to several thousand muscle fibers.

Once synaptic input depolarizes the membrane potential of a motor neuron above threshold, the neuron generates an action potential that is propagated along the axon to its terminal in the muscle. The action potential releases neurotransmitter at the neuromuscular synapse, and this causes an action potential in the sarcolemma of the muscle fibers. A muscle fiber has electrical properties similar to those of a large-diameter, unmyelinated axon, and thus action potentials propagate along the sarcolemma, although more slowly owing to the fiber's higher capacitance. Because the action potentials in all the muscle fibers of a motor unit occur at approximately the same time, they contribute to extracellular currents that sum to generate a field potential near the active muscle fibers.

Most muscle contractions involve the activation of many motor units, whose currents sum to produce signals detected by electromyography. In many instances the electromyogram (EMG) signal is large and can be easily recorded with electrodes placed on the skin over the muscle. The timing and amplitude of EMG activity, therefore, reflect the activation of muscle fibers by the motor neurons. EMG signals are useful for studying the neural control of movement and for diagnosing pathology (see Chapter 14).

In most mature vertebrate muscles each fiber is innervated by a single motor neuron. The number of muscle fibers innervated by one motor neuron, the innervation number, varies with the muscle type and function. In human skeletal muscles it ranges from average values of 5 for an eye muscle to 1,800 for a leg muscle (Table 34–1). Because the innervation number denotes the number of muscle fibers within a motor unit, differences in innervation number indicate differences in the average increment in force that occurs each time a motor unit in the same muscle is activated. Thus the innervation number also indicates the fineness of control of the muscle; the smaller the innervation number, the finer the control achieved by varying the number of activated motor units.

Not all motor units in a muscle have the same innervation number. Indeed, the differences can be substantial. For example, motor units of the first dorsal interosseous muscle of the hand have innervation numbers ranging from approximately 21 to 1,770. Consequently, the strongest motor unit in the hand's first dorsal interosseous muscle can exert about the same force as the average motor unit in the leg's medial gastrocnemius muscle.

The muscle fibers of a single motor unit are distributed throughout the muscle and intermingle with fibers innervated by other motor neurons. The muscle fibers of a single motor unit can occupy from 8% to as much as 75% of the volume in a limb muscle, with 2 to 5 muscle fibers per 100 belonging to the same motor unit. Therefore the muscle fibers in a given volume of muscle belong to 20 to 50 different motor units. This distribution changes with age and with some neuromuscular disorders. For example, muscle fibers lose their innervation after the death of a motor neuron and can be reinnervated by collateral sprouts from neighboring axons.

In some muscles the fibers of motor units are confined to discrete compartments that correspond to the regions of the muscle supplied by the primary branches of the muscle nerve. Selective activation of different compartments that exert forces in different directions provides a biomechanical advantage. Branches of the median and ulnar nerves in the forearm, for example, innervate distinct compartments in three multitendon extrinsic hand muscles that enable the fingers to be moved relatively independently. A muscle can therefore consist of several functionally distinct regions.

The Properties of Motor Units Vary

The force exerted by a muscle depends not only on the number of motor units that are activated during a contraction but also on three properties of those motor units: contraction speed, maximal force, and fatigability. These properties are assessed by examining the force exerted by individual motor units in response to variations in the number and rate of evoked action potentials.

The response to a single action potential is known as a twitch contraction. The time it takes the twitch to reach its peak force, the contraction time, is one measure of the contraction speed of the muscle fibers that comprise a motor unit. Slow-twitch motor units have long contraction times; fast-twitch units have shorter contraction times. A rapid series of action potentials elicits superimposed twitches known as a tetanic contraction or tetanus.

The force exerted during a tetanic contraction depends on the extent to which the twitches overlap and summate: The force varies with the contraction time of the motor unit and the rate at which the action potentials are evoked. At lower rates of stimulation the ripples in the tetanus denote the peaks of individual twitches (Figure 34–2A). The peak force achieved during a tetanus varies as a sigmoidal function of action potential rate, with the shape of the curve depending on the contraction time of the motor unit (Figure 34–2B). Maximal force is reached at different action potential rates for fast-twitch and slow-twitch motor units and is often greater in fast-twitch units.

The functional properties of motor units vary across the population and between muscles. At one end of the distribution motor units have long twitch contraction times and produce small forces, but are difficult to fatigue. These motor units are the first activated during a voluntary contraction. In contrast, the last motor units activated have short contraction times, produce large forces, and are easy to fatigue. As observed by Jacques Duchateau and colleagues, most human motor units produce low forces and have intermediate contraction times (Figure 34–3).

Because these contractile properties of a motor unit depend on the characteristics of its muscle fibers, we can distinguish different types of muscle fibers. This distinction stems from structural specializations and differences in the metabolic properties of muscle fibers. All muscle fibers belonging to a motor unit have similar biochemical and histochemical properties.

One commonly used scheme distinguishes muscle fibers by their reactivity to histochemical assays for the enzyme myosin adenosine triphosphatase (ATPase), which is used as an index of contractile speed. Based on histochemical stains for myosin ATPase, it is possible to identify type I and type II muscle fibers. Slow contracting motor units contain type I muscle fibers, and fast contracting units include type II fibers. The type II fibers can be further classified into the least fatigable (type IIa) and most fatigable (type IIb, IIx, or IId). Another commonly used scheme distinguishes muscle fibers on the basis of genetically defined isoforms of the myosin heavy chain. Those in slow contracting motor units express myosin heavy chain-I, those in fast contracting and least fatigable units express myosin heavy chain-IIa, and fibers in fast contracting and most fatigable units express myosin heavy chain-IIb or -IIx. There is a high degree of correspondence between the two classification schemes for muscle fibers.

Physical Activity Can Alter Motor Unit Properties

Alterations in habitual levels of physical activity can influence the three contractile properties of motor units (contraction speed, maximal force, and fatigability). A decrease in muscle activity, such as occurs with aging, bed rest, limb immobilization, or space flight, reduces the maximal capabilities of all three properties. The effects of increased physical activity depend on the intensity and duration of the activity. Brief sets of high-intensity contractions performed a few times each week can increase contraction speed and motor unit force, whereas prolonged periods of low-intensity contractions can reduce motor unit fatigability. Physical activity regimens that involve such differences are often described as strength training and endurance training, respectively.

Changes in the contractile properties of motor units involve adaptations in the structural specializations and biochemical properties of muscle fibers. The improvement in contraction speed caused by strength training, for example, is associated with an increase in the maximal shortening velocity of a muscle fiber caused by the enhanced capabilities of the myosin molecules in the fiber. Similarly, the increase in maximal force is associated with the enlarged size and increased intrinsic force capacity of the muscle fibers produced by an increase in the number and density of the contractile proteins.

In contrast, alterations in the fatigability of a muscle fiber can be caused by many different adaptations, such as changes in capillary density, the number of mitochondria, excitation-contraction coupling, and the metabolic capabilities of the muscle fibers. Endurance exercise can promote the biogenesis of mitochondria and enhance the oxidative capacity of a muscle fiber, thereby reducing its fatigability. Although the adaptive capabilities of muscle fibers decline with age, the muscles remain responsive to exercise even at 90 years of age.

Despite the efficacy of strength and endurance training in altering the contractile properties of muscle fibers, these training regimens have little effect on the composition of a muscle's fibers. Although several weeks of exercise can change the proportion of type IIa and IIx fibers, there is no change in the proportion of type I fibers. All fiber types adapt in response to exercise, although to varying extents depending on the type of exercise. For example, strength training of leg muscles for 2 to 3 months can increase the cross-sectional area of type I fibers by 0% to 20% and of type II fibers by 20% to 60%, increase the proportion of type IIa fibers by approximately 10%, and decrease the proportion of type IIx fibers by a similar amount. Furthermore, endurance training may increase the enzyme activities of oxidative metabolic pathways without noticeable changes in the proportions of fiber types, but the relative proportions of type IIa and IIx fibers do change as a function of the duration of each exercise session. Conversely, several weeks of bed rest or limb immobilization do not change the proportions of fiber types in a muscle, but they do decrease the size and intrinsic force capacity of muscle fibers.

Although physical activity has little influence on the proportion of type I fibers in a muscle, more substantial interventions can have an effect. Space flight, for example, exposes muscles to a sustained decrease in gravity, reducing the proportion of type I fibers in leg muscles. A few weeks of continuous electrical stimulation at a low frequency causes a marked increase in the proportion of type I fibers and a substantial decrease in fiber size. Similarly, surgically changing the nerve that innervates a muscle alters the pattern of activation; eventually the muscle exhibits properties similar to those of the muscle that was originally innervated by the transplanted nerve. Connecting a nerve that originally innervated a rapidly contracting leg muscle to a slowly contracting leg muscle, for example, will cause the slower muscle to become more like a faster muscle.

Muscle Force Is Controlled by the Recruitment and Discharge Rate of Motor Units

The force exerted by a muscle during a contraction depends on the number of motor units that are activated and the rate at which each of the active motor neurons discharges action potentials. Force is increased during a muscle contraction by the activation of additional motor units, which are recruited progressively from the weakest to the strongest (Figure 34–4). A motor unit's recruitment threshold is the force during the contraction at which the motor unit is activated. Muscle force decreases gradually by terminating the activity of motor units in the reverse order from strongest to weakest.

The order in which motor units are recruited is highly correlated with several indices of motor unit size, including the size of the motor neuron cell bodies, the diameter and conduction velocity of the axons, and the amount of force that the muscle fibers can exert. Because the recruitment threshold of a motor unit depends on the membrane resistance of the motor neuron, which is inversely related to its surface area, a given synaptic current will produce larger changes in the membrane potential of small-diameter motor neurons. Consequently, increases in the net excitatory input to a motor nucleus cause the levels of depolarization to reach threshold in an ascending order of motor neuron size: The smallest motor neuron is recruited first and the largest motor neuron last (Figure 34–5). This effect is known as the size principle of motor neuron recruitment, a principle enunciated by Elwood Henneman in 1957.

The size principle has two important consequences for the control of movement by the nervous system. First, the sequence of motor-neuron recruitment is determined by spinal mechanisms and not by higher regions of the nervous system. This means that the brain cannot selectively activate specific motor units. Second, motor units are activated in order of increasing fatigability, so the least fatigable motor units available produce the initial force required for a specific task.

As suggested by Edgar Adrian in the 1920s, the muscle force at which the last motor unit in a motor nucleus is recruited varies between muscles. In some hand muscles all the motor units have been recruited when the force reaches approximately 60% of maximum during a slow muscle contraction. In the biceps brachii, deltoid, and tibialis anterior muscles, recruitment continues up to approximately 85% of the maximal force. However, because the recruitment threshold of motor units decreases with contraction speed, during a rapid contraction most motor units in a muscle are recruited with a load of approximately 33% of maximum. Beyond the upper limit of motor unit recruitment, muscle force can still be increased by varying the rate of action potentials in the motor neurons. Below the upper limit of recruitment, the rate of firing can also be varied in addition to increasing the number of active motor units (Figure 34–6). In fact, beneath the upper recruitment limit variation in discharge rate can have the greater influence on muscle force.

The Input–Output Properties of Motor Neurons Are Modified by Input from the Brain Stem

The discharge rate of motor neurons depends on the magnitude of the depolarization generated by excitatory inputs and the intrinsic membrane properties of the motor neurons in the spinal cord. These properties can be profoundly modified by input from monoaminergic neurons in the brain stem. In the absence of this input, the dendrites of motor neurons passively transmit synaptic current to the cell body, resulting in a modest depolarization that immediately ceases when the input stops. Under these conditions the relation between input current and discharge rate is linear over a wide range.

The input–output relation becomes nonlinear, however, when the monoamines serotonin and norepinephrine activate L-type Ca²⁺ channels on the dendrites of the motor neurons. The resulting inward Ca²⁺ currents can enhance synaptic currents by five- to tenfold (Figure 34–7). In an active motor neuron this enhanced current can sustain an elevated discharge rate after a brief depolarizing input, a behavior known as self-sustained firing. A subsequent brief inhibitory input at a low velocity returns the discharge rate to its original value.

Because the properties of motor neurons are strongly influenced by monoamines, the excitability of the pool of motor neurons innervating a single muscle is under control of the brain stem. Moderate monoaminergic input to the motor neurons of slow contracting motor units promotes self-sustained firing. This is probably the source of the sustained force exerted by slower motor units to maintain posture. During sleep, when monoaminergic drive is withdrawn, excitability decreases, thus helping to ensure a relaxed motor state. Monoaminergic input from the brain stem can adjust the gain of the motor unit pool to suit the demands of different tasks. This flexibility does not compromise the size principle of orderly recruitment because the threshold for activation of the persistent inward currents is lowest in the motor neurons of slower motor units, which are the first recruited even in the absence of monoamines.

Muscle force depends not only on the amount of motor unit activity but also on the arrangement of the fibers in the muscle. Because movement involves the controlled variation of muscle force, the nervous system must take into account the structure of muscle to achieve specific movements.

The Sarcomere Contains the Contractile Proteins

Individual muscles contain thousands of fibers that vary from 1 to 500 mm in length and from 10 to 60 μm in diameter. The variation in fiber dimensions reflects differences in the quantity of contractile protein. Despite this quantitative variation, the organization of contractile proteins is similar in all muscle fibers. The proteins are arranged in repeating sets of thick and thin filaments, each set known as a sarcomere (Figure 34–8). The physiological length of a sarcomere, which is bounded by Z disks, ranges from 1.5 μm to 3.5 μm. Sarcomeres are arranged in series to form a myofibril, and the myofibrils are aligned in parallel to form a muscle fiber.

The force that each sarcomere can generate arises from the interaction of the contractile thick and thin filaments. The thick filament consists of a few hundred myosin molecules arranged in a structured sequence. Each myosin molecule comprises paired coiled-coil domains that terminate in two globular heads. The myosin molecules in the two halves of a thick filament point in opposite directions and are progressively displaced so that the heads, which extend away from the filament, protrude from the entire thick filament (Figure 34–8C). To maximize the interaction between the globular heads and the thin filaments, six thin filaments surround each thick filament.

The primary components of the thin filament are two helical strands of fibrous F-actin, each of which contains approximately 200 actin monomers. Superimposed on F-actin are tropomyosin and troponin, proteins that control the interaction between actin and myosin. Tropomyosin consists of two coiled strands that lie in the groove of the F-actin helix; troponin is a small molecular complex that is attached to tropomyosin at regular intervals (Figure 34–8C).

The thin filaments are anchored to the Z disk at each end of the sarcomere, whereas the thick filaments occupy the middle of the sarcomere (Figure 34–8B). This organization accounts for the alternating light and dark bands of striated muscle (Figure 34–8A). The light band contains only thin filaments, whereas the dark band contains both thick and thin filaments. When a muscle is activated, the width of the light band decreases, but the width of the dark band does not change, suggesting that the thick and thin filaments slide relative to one another during a contraction. This led to the sliding filament hypothesis of muscle contraction proposed by A. F. Huxley and H. E. Huxley in the 1950s.

The sliding of the thick and thin filaments is triggered by the release of Ca²⁺ within the sarcoplasm of a muscle fiber in response to an action potential at the fiber's membrane, the sarcolemma. Varying the amount of Ca²⁺ in the sarcoplasm controls the interaction between the thick and thin filaments. Under resting conditions the Ca²⁺ concentration in the sarcoplasm is kept low by active pumping of Ca²⁺ into the sarcoplasmic reticulum, a network of longitudinal tubules and chambers of smooth endoplasmic reticulum (Figure 34–8A). Calcium is stored in the terminal cisternae, which are located next to intracellular extensions of the sarcolemma known as transverse tubules. The transverse tubules, terminal cisternae, and sarcoplasmic reticulum constitute an activation system that transforms an action potential into the sliding of the filaments.

As an action potential propagates along the sarcolemma it invades the transverse tubules and causes the rapid release of Ca²⁺ from the terminal cisternae into the sarcoplasm. Once in the sarcoplasm Ca²⁺ diffuses among the filaments and binds reversibly to troponin, which results in the displacement of the troponin- tropomyosin complex and activates the sliding of the thick and thin filaments. Because a single action potential is insufficient to release enough Ca²⁺ to bind all available troponin sites in skeletal muscle, the strength of a contraction increases with the action potential rate.

The sliding of the filaments depends on mechanical work performed by the globular heads of myosin, work that uses chemical energy contained in adenosine triphosphate (ATP). The actions of the myosin heads are regulated by the cross bridge cycle, a sequence of detachment, activation, and attachment (Figure 34–9). In each cycle a globular head undergoes a displacement of 5 to 10 nm. Contractile activity continues as long as Ca²⁺ and ATP are present in the cytoplasm in sufficient amounts.

Noncontractile Elements Provide Essential Structural Support

Structural elements of the muscle fiber maintain the alignment of the contractile proteins within the fiber and facilitate the transmission of force from the sarcomeres to the skeleton. A network of proteins (nebulin, titin) maintains the orientation of the thick and thin filaments within the sarcomere, whereas other proteins (desmin, skelemins) constrain the lateral alignment of the myofibrils (Figure 34–8B). These proteins contribute to the elasticity of muscle and maintain the appropriate alignment of cellular structures when the muscle is loaded.

Although some of the force generated by the cross bridges is transmitted along the sarcomeres in series, some travels laterally from the thin filaments to an extracellular matrix that surrounds each muscle fiber, through a group of transmembrane and membrane-associated proteins called a costamere (Figure 34–8B). The lateral transmission of force follows two pathways through the costamere, one through a dystrophin-glycoprotein complex and the other through vinculin and members of the integrin family. Mutations of genes that encode components of the dystrophin-glycoprotein complex cause muscular dystrophies in humans.

Contractile Force Depends on Muscle Fiber Activation, Length, and Velocity

The force that a muscle fiber can exert depends on the number of cross bridges formed and the force produced by each cross bridge. These two factors are influenced by the Ca²⁺ concentration in the sarcoplasm, the amount of overlap between the thick and thin filaments, and the velocity with which the thick and thin filaments slide past one another. The influx of Ca²⁺ that activates formation of the cross bridges is transitory because continuous pump activity quickly returns Ca²⁺ to the sarcoplasmic reticulum. The release and reuptake of Ca²⁺ in response to a single action potential occurs so quickly that only some of the potential cross bridges are formed. This explains why the peak force of a twitch is less than the maximal force of the muscle fiber (see Figure 34–2A). Maximal force can be achieved only with a series of action potentials that sustains the Ca²⁺ concentration in the sarcoplasm, thus maximizing cross bridge formation.

Although Ca²⁺ activates formation of the cross bridges, cross bridges can be formed only when the thick and thin filaments overlap. This overlap varies as the filaments slide relative to one another (Figure 34–10A). At an intermediate sarcomere length (L_o) the amount of overlap between actin and myosin is optimal, and the relative force is maximal. Increases in sarcomere length reduce the overlap between actin and myosin and the force that can be developed. Decreases in sarcomere length cause the thin filaments to overlap, reducing the number of binding sites available to the myosin heads. Although many muscles operate over a narrow range of sarcomere lengths (approximately 94 ± 13% L_o, mean ± SD), among muscles there is considerable diversity in sarcomere lengths during movement.

Because structures that connect the contractile proteins to the skeleton also influence the force that a muscle can exert, muscle force increases with length over its operating range. This property enables muscle to function like a spring and to resist changes in length. Muscle stiffness, which corresponds to the slope of the relation between muscle force and muscle length (N/m), depends on the structure of the muscle. A stiffer muscle, like a stronger spring, is more resistant to changes in length.

Once activated, cross bridges perform work and cause the thick and thin filaments to slide relative to one another. Because of the elasticity of intermediate-length filaments and the extracellular matrix, sarcomeres can shorten even when the length of the muscle fiber is held fixed. The direction and rate of change in sarcomere length depend on the amount of force relative to the magnitude of the load against which the sarcomere acts. Sarcomere length decreases when the force exceeds the load (shortening contraction) but increases when the force is less than the load (lengthening contraction) . The maximal force that a muscle fiber can exert decreases as shortening velocity increases but increases as lengthening velocity increases (Figure 34–10B).

The maximal rate at which a muscle fiber can shorten is limited by the peak rate at which cross bridges can form. The variation in fiber force as contraction velocity changes is largely caused by differences in the average force exerted by each cross bridge. For example, the decrease in force during a shortening contraction is attributable to a reduction in cross bridge displacement during each power stroke and the failure of some myosin heads to find attachment sites. Conversely, the increase in force during a lengthening contraction reflects the stretching of incompletely activated sarcomeres and the more rapid reattachment of cross bridges after they have been pulled apart.

The rate of cross bridge cycling not only depends on contraction velocity, but also on the preceding activity of the muscle. For example, after a brief isometric contraction the rate increases. When a muscle is stretched while in this state, such as would occur during a postural disturbance, muscle stiffness is enhanced, and the muscle is more effective at resisting the change in length. This property is known as short-range stiffness. Conversely, the cross bridge cycling rate decreases after shortening contractions, and the muscle does not exhibit short-range stiffness.

Muscle Torque Depends on Musculoskeletal Geometry

The anatomy of a muscle has a pronounced effect on its force capacity, range of motion, and shortening velocity. The anatomical features that influence function include the arrangement of the sarcomeres in each muscle fiber, the organization of the muscle fibers within the muscle, and the location of the muscle on the skeleton. These features vary widely among muscles (Figure 34–11).

At the level of the single muscle fiber the number of sarcomeres in series and in parallel can vary. The number of sarcomeres in series determines the length of the myofibril and thus the length of the muscle fiber. Because one sarcomere can shorten by a certain length with a given maximal velocity, both the range of motion and the maximal shortening velocity of a muscle fiber are proportional to the number of sarcomeres in series. The force that a myofibril can exert is equal to the average sarcomere force and is not influenced by the number of sarcomeres in series. The force capacity of a fiber, however, depends on the number of sarcomeres in parallel and hence on the diameter or cross-sectional area of the fiber.

At the level of the muscle, the functional attributes of the fibers are modified by the orientation of the fascicles to the line of pull of the muscle and the length of the fiber relative to the muscle length. In most muscles the fascicles are not parallel to the line of pull but fan out in feather-like (pennate) arrangements (Figure 34–11). The relative orientation, or pennation angle of the fascicles, ranges from 0 degrees (biceps brachii, sartorius) to approximately 30 degrees (soleus). Because more fibers can fit into a given volume as the pennation angle increases, muscles with large pennation angles typically have more myofibrils in parallel and hence large cross-sectional areas. Given the linear relation between cross-sectional area and maximal force (~0.25 N·mm^–2), these muscles are capable of a greater maximal force. However, the fibers in pennate muscles are generally short and have a lesser maximal shortening velocity than those in nonpennate muscles.

The functional consequences of this anatomical arrangement can be seen by comparing the contractile properties of two muscles with different numbers of fibers and fiber lengths. If the two muscles have identical fiber lengths, but one has twice as many fibers, the range of motion of the two muscles will be similar because it is a function of fiber length, but the maximal force capacity will vary in proportion to the number of muscle fibers. If the two muscles have identical numbers of fibers but the fibers in one muscle are twice as long, the muscle with the longer fibers will have a greater range of motion and a greater maximal shortening velocity, even though the two muscles have a similar force capacity. Because of this effect, the muscle with longer fibers is able to exert more force and produce more power (the product of force and velocity) at a given absolute shortening velocity (Figure 34–12).

Muscle fiber lengths and cross-sectional areas vary substantially throughout the human body, which suggests that the contractile properties of individual muscles also differ markedly. In the leg, for example, fiber length ranges from 20 mm (soleus) to 460 mm (sartorius), and cross-sectional area ranges from 200 mm² (sartorius) to 5,800 mm² (soleus). Functionally coupled muscles tend to have complementary combinations of these properties. For example, muscles characterized by large pennation angles, large cross-sectional areas, and short fibers (quadriceps femoris) are often functionally coupled with those that have smaller cross-sectional areas and longer fibers (hamstrings).

Movement is the muscle-controlled rotation of adjacent body segments, which means that the capacity of a muscle to contribute to a movement also depends on its location relative to the joint that it spans. The rotary force exerted by a muscle about a joint is referred to as muscle torque and is calculated as the product of the muscle force and the moment arm, the shortest perpendicular distance from the line of pull of the muscle to the joint's center (Figure 34–13).

The moment arm usually changes as a joint rotates through its range of motion; the amount of change depends on where the muscle is attached to the skeleton relative to the joint. If the force exerted by a muscle remains relatively constant throughout the joint's range of motion, muscle torque varies in direct proportion to the change in the moment arm. For many muscles the moment arm is maximal in the middle of the range of motion, which usually corresponds to the position of maximal muscle force and hence greatest muscle torque.

The human body has approximately 600 muscles, each with a distinct torque profile about one or more joints. To perform a desired movement the nervous system must activate an appropriate combination of muscles with adequate intensity and timing of activity. The activation must be appropriate for the contractile properties and musculoskeletal geometry of many muscles, as well as the mechanical interactions between body segments. As a result of these demands, activation strategies differ with the details of the movement.

Contraction Velocity Can Vary in Magnitude and Direction

Movement speed depends on the contraction velocity of a muscle. The only ways to vary contraction velocity are to alter either the number of motor units recruited or the rates at which they discharge action potentials. The velocity of a contraction can vary in both magnitude and direction (see Figure 34–10B). To control the velocity of a contraction the nervous system must scale the magnitude of the net muscle torque relative to the load torque, which includes both the weight of the body segment and any load applied externally to the body.

When muscle torque exceeds load torque, the muscle shortens as it performs a shortening contraction. When muscle torque is less than load torque, the muscle lengthens as it performs a lengthening contraction. For the example shown in Figure 34–13, the load is lifted with a shortening contraction of the flexor and lowered with a lengthening contraction. Both types of contractions are common in daily activities.

Shortening and lengthening contractions are not simply the result of adjusting motor unit activity so that the net muscle torque is greater or less than the load torque. When the task involves lifting a load with a prescribed trajectory, activation of the motor units must be aligned so that the summed rise times match the desired trajectory during the shortening contraction, whereas the lengthening contraction requires that the summed decay times be matched. The nervous system accomplishes this by varying the descending input and sensory feedback during the two contractions. Because of these differences, some people, such as older adults and persons performing rehabilitation exercises after an orthopedic procedure, have greater difficulty performing lengthening contractions.

The amount of motor-unit activity relative to the load also influences the contraction velocity. This effect depends on both the number of motor units recruited and the maximal rates at which the motor units can discharge action potentials. For example, the maximal rate of increase in muscle torque during a submaximal contraction increases after several weeks of physical training and is associated with a marked increase in the initial discharge rates of the activated motor units. Physical training increases the rate at which motor units can discharge trains of action potentials, an effect that can be mimicked by the rapid injection of current into a motor neuron. Changes in the maximal shortening velocity of a muscle after a change in the habitual level of physical activity are the result, at least partly, of factors that influence the ability of motor units to discharge action potentials at high rates.

Movements Involve the Coordination of Many Muscles

To achieve a prescribed trajectory the nervous system must activate not only the muscles that produce the desired displacement but also muscles that prevent unintended actions. For example, the elbow flexor muscles are used to rapidly rotate the forearm about the elbow joint. But unless the muscles that cross the wrist are also activated to stabilize the wrist joint, rotation of the forearm would cause the hand to flail about the wrist joint.

In the simplest case muscles span a single joint and cause the attached body segments to accelerate about a single axis of rotation (Figure 34–14A). Because muscles can exert only a pulling force, motion about a single axis of rotation requires at least two muscles or groups of muscles. Thus, the flexion-extension motion about the knee joint involves the hamstring muscles to exert force in the direction of flexion and the quadriceps to exert force in the direction of extension.

However, many muscles attach to the skeleton slightly off center and can cause movement about more than one axis of rotation. If one of the actions is not required, the nervous system must activate other muscles to control the unwanted movement. For example, activation of the radial flexor muscle of the wrist can cause the wrist to flex and abduct. If the intended action is only wrist flexion, then the abduction action must be opposed by another muscle, such as the ulnar flexor muscle, which causes wrist flexion and adduction. Depending on the geometry of the articulating surfaces and the attachment sites of the muscles, the multiple muscles that span a joint are capable of producing movements about one to three axes of rotation. Furthermore, some structures can be displaced linearly (eg, the scapula on the trunk), adding to the degrees of freedom about a joint.

This organization enhances the flexibility of the skeletal motor system, for the same movement can be achieved by activating different combinations of muscles. However, this additional flexibility comes with a cost in the corresponding variation in the unwanted actions that must be controlled. A solution used by the nervous system is to organize relations among selected muscles to produce specific actions. A particular balance of muscle activations that changes over time is known as a muscle synergy, and movement is produced through the coordinated activation of these synergies. For example, electromyographic recordings suggest that a range of human movements, such as grasping objects with the hand, reaching and pointing in different directions, and walking and running at several speeds, are controlled by approximately five muscle synergies.

The number of muscles that participate in a movement also varies with the speed of the movement. For example, slow lifting of the load shown in Figure 34–13 requires only that the muscle torque slightly exceed the load torque, and thus only the flexor muscle is activated. This strategy is used when lifting a handheld weight with the elbow flexor muscles. In contrast, to perform this movement rapidly with an abrupt termination, both the flexor and extensor muscles must be activated. First the flexor muscle is activated to accelerate the limb in the direction of flexion, followed by activation of the extensor muscle to accelerate the limb in the direction of extension, and finally a burst of activity by the flexor muscle to reduce the angular momentum of the limb and the handheld weight in the direction of flexion so that it arrives at the desired joint angle (Figure 34–14B). The amount of extensor activity increases with the speed of the movement.

Increases in movement speed introduce another factor that the nervous system must control: unwanted accelerations in other body segments. Because body segments are interconnected, motion in one segment can induce motion in another. At the beginning of the swing phase in running, for example, the hip flexor muscles are activated and accelerate the thigh in a forward direction (Figure 34–15A). The motion of the thigh causes the lower leg to rotate backward about the knee joint. To control the backward displacement of the lower leg, the quadriceps muscles are activated to accelerate the lower leg in the forward direction. As the lower leg rotates backward, the quadriceps muscles perform a lengthening contraction that becomes a shortening contraction to rotate the lower leg forward in the middle of the swing phase.

Muscles that span more than one joint can be used to control the motion-dependent interactions between body segments. At the end of the swing phase in running, activation of the hamstring muscles causes both the thigh and lower leg to accelerate backward (Figure 34–15B). If a hip extensor muscle was used to accelerate the thigh backward instead of the hamstring muscles, the lower leg would accelerate forward, requiring activation of a knee flexor muscle to control the unwanted motion so that the foot could be placed on the ground. Use of the two-joint hamstring muscles is a more economical strategy, but one that can subject the hamstrings to high stresses during fast movements, such as sprinting. The control of such motion-dependent interactions often involves lengthening contractions, which maximize muscle stiffness and the ability of muscle to resist changes in length.

For most movements the nervous system must establish rigid connections between some body segments for two reasons. First, as expressed in Newton's law of action and reaction, a reaction force must provide a foundation for the acceleration of a body segment. For example, in a reaching movement performed by a person standing upright, the ground must provide a reaction force against the feet. The muscle actions that produce the arm movement exert forces that are transmitted through the body to the feet and are opposed by the ground. Different substrates provide different amounts of reaction force, so ice or sand substantially alter movement capabilities.

Second, uncertain conditions are usually accommodated by stiffening the joints through concurrent activation of the muscles that produce force in opposite directions. Coactivation of opposing muscles occurs often when a support surface is unsteady, when the body might experience an unexpected perturbation, or when lifting a heavy load. Because coactivation increases the energetic cost of performing a task, one characteristic of skilled performance is the ability to accomplish a task with minimal activation of muscles that span associated joints.

Muscle Work Depends on the Pattern of Activation

Limb muscles in healthy young adults are active 10% to 20% of the time during waking hours. For much of this time the muscles perform constant-length (isometric) contractions to maintain a variety of static body postures. In contrast, muscle length has to change during a movement so that the muscle can perform work to displace body segments. A muscle performs positive work and produces power during a shortening contraction, whereas it performs negative work and absorbs power during a lengthening contraction. The capacity of muscle to do positive work establishes performance capabilities, such as the maximal height that can be jumped.

The nervous system enhances the work capacity of muscle by commanding a brief period of negative work before positive work. This activation sequence, the stretch-shorten cycle, occurs in many movements. When a person jumps in place on two feet, for example, the support phase involves an initial stretch and subsequent shortening of the ankle extensor and knee extensor muscles (Figure 34–16A). The forces in the Achilles and patellar tendons increase during the stretch and reach a maximum at the onset of the shortening phase. As a result, the muscles can perform more positive work and produce more power during the shortening contraction (Figure 34–16B).

Although negative work involves an increase in the length of the muscle, the length of the fascicles in the muscle often remains relatively constant, which indicates that the connective-tissue structures are stretched prior to the shortening contraction. Thus the capacity of the muscle to perform more positive work comes from strain energy that can be stored in the tendon during the stretch phase and released during the subsequent shortening phase. The ability of a muscle to benefit from this strategy depends on its morphological characteristics and is greatest in muscles with long tendons.

Movement involves the coordinated interaction of the nervous system and muscle. The basic functional unit of motor control is the motor unit, which consists of a motor neuron and the muscle fibers that it innervates. The force exerted by a muscle depends in part on the number and properties of the motor units that are activated. These properties include contraction speed, maximal force, and fatigability, all of which can be altered by physical activity. The rate of firing in each active motor neuron is also a factor in muscle force. Motor units tend to be activated in a stereotypical order that is highly correlated with motor-neuron size.

Muscle force depends not only on the characteristics of motor-unit activity, but also on the arrangement of the muscle fibers. The sarcomere is the smallest element of muscle to include a complete set of contractile proteins. A transient connection between the contractile proteins myosin and actin, known as the cross bridge cycle, enables muscle to exert a force. The organization of the sarcomeres within a muscle varies substantially and has a major effect on the contractile properties of the muscle.

For a given arrangement of sarcomeres, the force a muscle can exert depends on the activation of the cross bridges by Ca²⁺, the amount of overlap between the thick and thin filaments, and the velocity of the moving filaments. The functional capability of a muscle depends on the torque that it can exert, which is influenced both by its contractile properties and by the location of its attachments on the skeleton relative to the joint that it spans.

To perform a movement the nervous system activates multiple muscles and controls the torque exerted about the involved joints. The nervous system can vary the magnitude and direction of a movement by altering the amount of motor unit activity, and hence muscle torque, relative to the load acting on the body. Increases in movement speed, however, enhance motion-dependent interactions between body segments, producing unwanted accelerations that must be controlled by the nervous system. Furthermore, the nervous system must coordinate the activity of multiple muscles to provide a mechanical link between moving body segments and the required support from the surroundings. The patterns of muscle activity vary substantially between movements and often include strategies that augment the work capacity of muscles.