Sensory information is integrated at all levels of the nervous system and causes appropriate motor responses that begin in the spinal cord with relatively simple muscle reflexes, extend into the brain stem with more complicated responses, and finally extend to the cerebrum, where the most complicated muscle skills are controlled.
In this chapter, we discuss the control of muscle function by the spinal cord. Without the special neuronal circuits of the cord, even the most complex motor control systems in the brain could not cause any purposeful muscle movement. For example, there is no neuronal circuit anywhere in the brain that causes the specific to-and-fro movements of the legs that are required in walking. Instead, the circuits for these movements are in the cord and the brain simply sends command signals to the spinal cord to set into motion the walking process.
Let us not belittle the role of the brain, however, because the brain gives directions that control the sequential cord activities—to promote turning movements when they are required, to lean the body forward during acceleration, to change the movements from walking to jumping as needed, and to monitor continuously and control equilibrium. All this is done through “analytical” and “command” signals generated in the brain. But it also requires the many neuronal circuits of the spinal cord that are the objects of the commands. These circuits provide all but a small fraction of the direct control of the muscles.
Organization of the Spinal Cord for Motor Functions
The cord gray matter is the integrative area for the cord reflexes. Figure 54-1 shows the typical organization of the cord gray matter in a single cord segment. Sensory signals enter the cord almost entirely through the sensory (posterior) roots. After entering the cord, every sensory signal travels to two separate destinations: (1) One branch of the sensory nerve terminates almost immediately in the gray matter of the cord and elicits local segmental cord reflexes and other local effects. (2) Another branch transmits signals to higher levels of the nervous system—to higher levels in the cord itself, to the brain stem, or even to the cerebral cortex, as described in earlier chapters.
Figure 54-1 Connections of peripheral sensory fibers and corticospinal fibers with the interneurons and anterior motor neurons of the spinal cord.
Each segment of the spinal cord (at the level of each spinal nerve) has several million neurons in its gray matter. Aside from the sensory relay neurons discussed in Chapters 47 and 48, the other neurons are of two types: (1) anterior motor neurons and (2) interneurons.
Anterior Motor Neurons
Located in each segment of the anterior horns of the cord gray matter are several thousand neurons that are 50 to 100 percent larger than most of the others and are called anterior motor neurons (Figure 54-2). They give rise to the nerve fibers that leave the cord by way of the anterior roots and directly innervate the skeletal muscle fibers. The neurons are of two types, alpha motor neurons and gamma motor neurons.
Figure 54-2 Peripheral sensory fibers and anterior motor neurons innervating skeletal muscle.
Alpha Motor Neurons
The alpha motor neurons give rise to large type A alpha (Aα) motor nerve fibers, averaging 14 micrometers in diameter; these fibers branch many times after they enter the muscle and innervate the large skeletal muscle fibers. Stimulation of a single alpha nerve fiber excites anywhere from three to several hundred skeletal muscle fibers, which are collectively called the motor unit. Transmission of nerve impulses into skeletal muscles and their stimulation of the muscle motor units are discussed in Chapters 6 and 7.
Gamma Motor Neurons
Along with the alpha motor neurons, which excite contraction of the skeletal muscle fibers, about one half as many much smaller gamma motor neurons are located in the spinal cord anterior horns. These gamma motor neurons transmit impulses through much smaller type A gamma (Aγ) motor nerve fibers, averaging 5 micrometers in diameter, which go to small, special skeletal muscle fibers called intrafusal fibers, shown in Figures 54-2 and 54-3. These fibers constitute the middle of the muscle spindle, which helps control basic muscle “tone,” as discussed later in this chapter.
Figure 54-3 Muscle spindle, showing its relation to the large extrafusal skeletal muscle fibers. Note also both motor and sensory innervation of the muscle spindle.
Interneurons are present in all areas of the cord gray matter—in the dorsal horns, the anterior horns, and the intermediate areas between them, as shown in Figure 54-1. These cells are about 30 times as numerous as the anterior motor neurons. They are small and highly excitable, often exhibiting spontaneous activity and capable of firing as rapidly as 1500 times per second. They have many interconnections with one another, and many of them also synapse directly with the anterior motor neurons, as shown in Figure 54-1. The interconnections among the interneurons and anterior motor neurons are responsible for most of the integrative functions of the spinal cord that are discussed in the remainder of this chapter.
Essentially all the different types of neuronal circuits described in Chapter 46 are found in the interneuron pool of cells of the spinal cord, including diverging, converging, repetitive-discharge, and other types of circuits. In this chapter, we examine many applications of these different circuits in the performance of specific reflex acts by the spinal cord.
Only a few incoming sensory signals from the spinal nerves or signals from the brain terminate directly on the anterior motor neurons. Instead, almost all these signals are transmitted first through interneurons, where they are appropriately processed. Thus, in Figure 54-1, the corticospinal tract from the brain is shown to terminate almost entirely on spinal interneurons, where the signals from this tract are combined with signals from other spinal tracts or spinal nerves before finally converging on the anterior motor neurons to control muscle function.
Renshaw Cells Transmit Inhibitory Signals to Surrounding Motor Neurons
Also located in the anterior horns of the spinal cord, in close association with the motor neurons, are a large number of small neurons called Renshaw cells. Almost immediately after the anterior motor neuron axon leaves the body of the neuron, collateral branches from the axon pass to adjacent Renshaw cells. These are inhibitory cells that transmit inhibitory signals to the surrounding motor neurons. Thus, stimulation of each motor neuron tends to inhibit adjacent motor neurons, an effect called lateral inhibition. This effect is important for the following major reason: The motor system uses this lateral inhibition to focus, or sharpen, its signals in the same way that the sensory system uses the same principle to allow unabated transmission of the primary signal in the desired direction while suppressing the tendency for signals to spread laterally.
Multisegmental Connections from One Spinal Cord Level to Other Levels—Propriospinal Fibers
More than half of all the nerve fibers that ascend and descend in the spinal cord are propriospinal fibers. These fibers run from one segment of the cord to another. In addition, as the sensory fibers enter the cord from the posterior cord roots, they bifurcate and branch both up and down the spinal cord; some of the branches transmit signals to only a segment or two, while others transmit signals to many segments. These ascending and descending propriospinal fibers of the cord provide pathways for the multisegmental reflexes described later in this chapter, including reflexes that coordinate simultaneous movements in the forelimbs and hindlimbs.
Muscle Sensory Receptors—Muscle Spindles and Golgi Tendon Organs—and Their Roles in Muscle Control
Proper control of muscle function requires not only excitation of the muscle by spinal cord anterior motor neurons but also continuous feedback of sensory information from each muscle to the spinal cord, indicating the functional status of each muscle at each instant. That is, what is the length of the muscle, what is its instantaneous tension, and how rapidly is its length or tension changing? To provide this information, the muscles and their tendons are supplied abundantly with two special types of sensory receptors: (1) muscle spindles (see Figure 54-2), which are distributed throughout the belly of the muscle and send information to the nervous system about muscle length or rate of change of length, and (2) Golgi tendon organs (see Figures 54-2 and 54-8), which are located in the muscle tendons and transmit information about tendon tension or rate of change of tension.
Figure 54-8 Golgi tendon organ.
The signals from these two receptors are either entirely or almost entirely for the purpose of intrinsic muscle control. They operate almost completely at a subconscious level. Even so, they transmit tremendous amounts of information not only to the spinal cord but also to the cerebellum and even to the cerebral cortex, helping each of these portions of the nervous system function to control muscle contraction.
Receptor Function of the Muscle Spindle
Structure and Motor Innervation of the Muscle Spindle
The organization of the muscle spindle is shown in Figure 54-3. Each spindle is 3 to 10 millimeters long. It is built around 3 to 12 tiny intrafusal muscle fibers that are pointed at their ends and attached to the glycocalyx of the surrounding large extrafusal skeletal muscle fibers.
Each intrafusal muscle fiber is a tiny skeletal muscle fiber. However, the central region of each of these fibers—that is, the area midway between its two ends—has few or no actin and myosin filaments. Therefore, this central portion does not contract when the ends do. Instead, it functions as a sensory receptor, as described later. The end portions that do contract are excited by small gamma motor nerve fibers that originate from small type A gamma motor neurons in the anterior horns of the spinal cord, as described earlier. These gamma motor nerve fibers are also called gamma efferent fibers, in contradistinction to the large alpha efferent fibers (type A alpha nerve fibers) that innervate the extrafusal skeletal muscle.
Sensory Innervation of the Muscle Spindle
The receptor portion of the muscle spindle is its central portion. In this area, the intrafusal muscle fibers do not have myosin and actin contractile elements. As shown in Figure 54-3 and in more detail in Figure 54-4, sensory fibers originate in this area. They are stimulated by stretching of this midportion of the spindle. One can readily see that the muscle spindle receptor can be excited in two ways:
1. Lengthening the whole muscle stretches the midportion of the spindle and, therefore, excites the receptor.
2. Even if the length of the entire muscle does not change, contraction of the end portions of the spindle’s intrafusal fibers stretches the midportion of the spindle and therefore excites the receptor.
Figure 54-4 Details of nerve connections from the nuclear bag and nuclear chain muscle spindle fibers.
Modified from Stein RB: Peripheral control of movement. Physiol Rev 54:225, 1974.
Two types of sensory endings are found in this central receptor area of the muscle spindle. They are the primary ending and the secondary ending.
In the center of the receptor area, a large sensory nerve fiber encircles the central portion of each intrafusal fiber, forming the so-called primary ending or annulospiral ending. This nerve fiber is a type Ia fiber averaging 17 micrometers in diameter, and it transmits sensory signals to the spinal cord at a velocity of 70 to 120 m/sec, as rapidly as any type of nerve fiber in the entire body.
Usually one but sometimes two smaller sensory nerve fibers—type II fibers with an average diameter of 8 micrometers—innervate the receptor region on one or both sides of the primary ending, as shown in Figures 54-3 and 54-4. This sensory ending is called the secondary ending; sometimes it encircles the intrafusal fibers in the same way that the type Ia fiber does, but often it spreads like branches on a bush.
Division of the Intrafusal Fibers into Nuclear Bag and Nuclear Chain Fibers—Dynamic and Static Responses of the Muscle Spindle
There are also two types of muscle spindle intrafusal fibers: (1) nuclear bag muscle fibers (one to three in each spindle), in which several muscle fiber nuclei are congregated in expanded “bags” in the central portion of the receptor area, as shown by the top fiber in Figure 54-4, and (2) nuclear chain fibers (three to nine), which are about half as large in diameter and half as long as the nuclear bag fibers and have nuclei aligned in a chain throughout the receptor area, as shown by the bottom fiber in the figure. The primary sensory nerve ending (the 17-micrometer sensory fiber) is excited by both the nuclear bag intrafusal fibers and the nuclear chain fibers. Conversely, the secondary ending (the 8-micrometer sensory fiber) is usually excited only by nuclear chain fibers. These relations are shown in Figure 54-4.
Response of Both the Primary and the Secondary Endings to the Length of the Receptor—“Static” Response
When the receptor portion of the muscle spindle is stretched slowly, the number of impulses transmitted from both the primary and the secondary endings increases almost directly in proportion to the degree of stretching and the endings continue to transmit these impulses for several minutes. This effect is called the static response of the spindle receptor, meaning simply that both the primary and secondary endings continue to transmit their signals for at least several minutes if the muscle spindle itself remains stretched.
Response of the Primary Ending (but Not the Secondary Ending) to Rate of Change of Receptor Length—“Dynamic” Response
When the length of the spindle receptor increases suddenly, the primary ending (but not the secondary ending) is stimulated powerfully. This excess stimulus of the primary ending is called the dynamic response, which means that the primary ending responds extremely actively to a rapid rate of change in spindle length. Even when the length of a spindle receptor increases only a fraction of a micrometer for only a fraction of a second, the primary receptor transmits tremendous numbers of excess impulses to the large 17-micrometer sensory nerve fiber, but only while the length is actually increasing. As soon as the length stops increasing, this extra rate of impulse discharge returns to the level of the much smaller static response that is still present in the signal.
Conversely, when the spindle receptor shortens, exactly opposite sensory signals occur. Thus, the primary ending sends extremely strong, either positive or negative, signals to the spinal cord to apprise it of any change in length of the spindle receptor.
Control of Intensity of the Static and Dynamic Responses by the Gamma Motor Nerves
The gamma motor nerves to the muscle spindle can be divided into two types: gamma-dynamic (gamma-d) and gamma-static (gamma-s). The first of these excites mainly the nuclear bag intrafusal fibers, and the second excites mainly the nuclear chain intrafusal fibers. When the gamma-d fibers excite the nuclear bag fibers, the dynamic response of the muscle spindle becomes tremendously enhanced, whereas the static response is hardly affected. Conversely, stimulation of the gamma-s fibers, which excite the nuclear chain fibers, enhances the static response while having little influence on the dynamic response. Subsequent paragraphs illustrate that these two types of muscle spindle responses are important in different types of muscle control.
Continuous Discharge of the Muscle Spindles Under Normal Conditions
Normally, particularly when there is some degree of gamma nerve excitation, the muscle spindles emit sensory nerve impulses continuously. Stretching the muscle spindles increases the rate of firing, whereas shortening the spindle decreases the rate of firing. Thus, the spindles can send to the spinal cord either positive signals—that is, increased numbers of impulses to indicate stretch of a muscle—or negative signals—below-normal numbers of impulses to indicate that the muscle is unstretched.
Muscle Stretch Reflex
The simplest manifestation of muscle spindle function is the muscle stretch reflex. Whenever a muscle is stretched suddenly, excitation of the spindles causes reflex contraction of the large skeletal muscle fibers of the stretched muscle and also of closely allied synergistic muscles.
Neuronal Circuitry of the Stretch Reflex
Figure 54-5 demonstrates the basic circuit of the muscle spindle stretch reflex, showing a type Ia proprioceptor nerve fiber originating in a muscle spindle and entering a dorsal root of the spinal cord. A branch of this fiber then goes directly to the anterior horn of the cord gray matter and synapses with anterior motor neurons that send motor nerve fibers back to the same muscle from which the muscle spindle fiber originated. Thus, this is a monosynaptic pathway that allows a reflex signal to return with the shortest possible time delay back to the muscle after excitation of the spindle. Most type II fibers from the muscle spindle terminate on multiple interneurons in the cord gray matter, and these transmit delayed signals to the anterior motor neurons or serve other functions.
Figure 54-5 Neuronal circuit of the stretch reflex.
Dynamic Stretch Reflex and Static Stretch Reflexes
The stretch reflex can be divided into two components: the dynamic stretch reflex and the static stretch reflex. The dynamic stretch reflex is elicited by the potent dynamic signal transmitted from the primary sensory endings of the muscle spindles, caused by rapid stretch or unstretch. That is, when a muscle is suddenly stretched or unstretched, a strong signal is transmitted to the spinal cord; this causes an instantaneous strong reflex contraction (or decrease in contraction) of the same muscle from which the signal originated. Thus, the reflex functions to oppose sudden changes in muscle length.
The dynamic stretch reflex is over within a fraction of a second after the muscle has been stretched (or unstretched) to its new length, but then a weaker static stretch reflex continues for a prolonged period thereafter. This reflex is elicited by the continuous static receptor signals transmitted by both primary and secondary endings. The importance of the static stretch reflex is that it causes the degree of muscle contraction to remain reasonably constant, except when the person’s nervous system specifically wills otherwise.
“Damping” Function of the Dynamic and Static Stretch Reflexes
An especially important function of the stretch reflex is its ability to prevent oscillation or jerkiness of body movements. This is a damping, or smoothing, function, as explained in the following paragraph.
Damping Mechanism in Smoothing Muscle Contraction
Signals from the spinal cord are often transmitted to a muscle in an unsmooth form, increasing in intensity for a few milliseconds, then decreasing in intensity, then changing to another intensity level, and so forth. When the muscle spindle apparatus is not functioning satisfactorily, the muscle contraction is jerky during the course of such a signal. This effect is demonstrated in Figure 54-6. In curve A, the muscle spindle reflex of the excited muscle is intact. Note that the contraction is relatively smooth, even though the motor nerve to the muscle is excited at a slow frequency of only eight signals per second. Curve B illustrates the same experiment in an animal whose muscle spindle sensory nerves had been sectioned 3 months earlier. Note the unsmooth muscle contraction. Thus, curve A graphically demonstrates the damping mechanism’s ability to smooth muscle contractions, even though the primary input signals to the muscle motor system may themselves be jerky. This effect can also be called a signal averagingfunction of the muscle spindle reflex.
Figure 54-6 Muscle contraction caused by a spinal cord signal under two conditions: curve A, in a normal muscle, and curve B, in a muscle whose muscle spindles were denervated by section of the posterior roots of the cord 82 days previously. Note the smoothing effect of the muscle spindle reflex in curve A.
Modified from Creed RS et al: Reflex Activity of the Spinal Cord. New York: Oxford University Press, 1932.
Role of the Muscle Spindle in Voluntary Motor Activity
To understand the importance of the gamma efferent system, one should recognize that 31 percent of all the motor nerve fibers to the muscle are the small type A gamma efferent fibers rather than large type A alpha motor fibers. Whenever signals are transmitted from the motor cortex or from any other area of the brain to the alpha motor neurons, in most instances the gamma motor neurons are stimulated simultaneously, an effect called coactivation of the alpha and gamma motor neurons. This causes both the extrafusal skeletal muscle fibers and the muscle spindle intrafusal muscle fibers to contract at the same time.
The purpose of contracting the muscle spindle intrafusal fibers at the same time that the large skeletal muscle fibers contract is twofold: First, it keeps the length of the receptor portion of the muscle spindle from changing during the course of the whole muscle contraction. Therefore, coactivation keeps the muscle spindle reflex from opposing the muscle contraction. Second, it maintains the proper damping function of the muscle spindle, regardless of any change in muscle length. For instance, if the muscle spindle did not contract and relax along with the large muscle fibers, the receptor portion of the spindle would sometimes be flail and sometimes be overstretched, in neither instance operating under optimal conditions for spindle function.
Brain Areas for Control of the Gamma Motor System
The gamma efferent system is excited specifically by signals from the bulboreticular facilitatory region of the brain stem and, secondarily, by impulses transmitted into the bulboreticular area from (1) the cerebellum, (2) the basal ganglia, and (3) the cerebral cortex.
Little is known about the precise mechanisms of control of the gamma efferent system. However, because the bulboreticular facilitatory area is particularly concerned with antigravity contractions, and because the antigravity muscles have an especially high density of muscle spindles, emphasis is given to the importance of the gamma efferent mechanism for damping the movements of the different body parts during walking and running.
Muscle Spindle System Stabilizes Body Position During Tense Action
One of the most important functions of the muscle spindle system is to stabilize body position during tense motor action. To do this, the bulboreticular facilitatory region and its allied areas of the brain stem transmit excitatory signals through the gamma nerve fibers to the intrafusal muscle fibers of the muscle spindles. This shortens the ends of the spindles and stretches the central receptor regions, thus increasing their signal output. However, if the spindles on both sides of each joint are activated at the same time, reflex excitation of the skeletal muscles on both sides of the joint also increases, producing tight, tense muscles opposing each other at the joint. The net effect is that the position of the joint becomes strongly stabilized, and any force that tends to move the joint from its current position is opposed by highly sensitized stretch reflexes operating on both sides of the joint.
Any time a person must perform a muscle function that requires a high degree of delicate and exact positioning, excitation of the appropriate muscle spindles by signals from the bulboreticular facilitatory region of the brain stem stabilizes the positions of the major joints. This aids tremendously in performing the additional detailed voluntary movements (of fingers or other body parts) required for intricate motor procedures.
Clinical Applications of the Stretch Reflex
Almost every time a clinician performs a physical examination on a patient, he or she elicits multiple stretch reflexes. The purpose is to determine how much background excitation, or “tone,” the brain is sending to the spinal cord. This reflex is elicited as follows.
Knee Jerk and Other Muscle Jerks Can Be Used to Assess Sensitivity of Stretch Reflexes
Clinically, a method used to determine the sensitivity of the stretch reflexes is to elicit the knee jerk and other muscle jerks. The knee jerk can be elicited by simply striking the patellar tendon with a reflex hammer; this instantaneously stretches the quadriceps muscle and excites a dynamic stretch reflex that causes the lower leg to “jerk” forward. The upper part of Figure 54-7 shows a myogram from the quadriceps muscle recorded during a knee jerk.
Figure 54-7 Myograms recorded from the quadriceps muscle during elicitation of the knee jerk (above) and from the gastrocnemius muscle during ankle clonus (below).
Similar reflexes can be obtained from almost any muscle of the body either by striking the tendon of the muscle or by striking the belly of the muscle itself. In other words, sudden stretch of muscle spindles is all that is required to elicit a dynamic stretch reflex.
The muscle jerks are used by neurologists to assess the degree of facilitation of spinal cord centers. When large numbers of facilitatory impulses are being transmitted from the upper regions of the central nervous system into the cord, the muscle jerks are greatly exaggerated. Conversely, if the facilitatory impulses are depressed or abrogated, the muscle jerks are considerably weakened or absent. These reflexes are used most frequently in determining the presence or absence of muscle spasticity caused by lesions in the motor areas of the brain or diseases that excite the bulboreticular facilitatory area of the brain stem. Ordinarily, large lesions in the motor areas of the cerebral cortexbut not in the lower motor control areas (especially lesions caused by strokes or brain tumors) cause greatly exaggerated muscle jerks in the muscles on the opposite side of the body.
Clonus—Oscillation of Muscle Jerks
Under some conditions, the muscle jerks can oscillate, a phenomenon called clonus (see lower myogram, Figure 54-7). Oscillation can be explained particularly well in relation to ankle clonus, as follows.
If a person standing on the tip ends of the feet suddenly drops his or her body downward and stretches the gastrocnemius muscles, stretch reflex impulses are transmitted from the muscle spindles into the spinal cord. These impulses reflexively excite the stretched muscle, which lifts the body up again. After a fraction of a second, the reflex contraction of the muscle dies out and the body falls again, thus stretching the spindles a second time. Again, a dynamic stretch reflex lifts the body, but this too dies out after a fraction of a second, and the body falls once more to begin a new cycle. In this way, the stretch reflex of the gastrocnemius muscle continues to oscillate, often for long periods; this is clonus.
Clonus ordinarily occurs only when the stretch reflex is highly sensitized by facilitatory impulses from the brain. For instance, in a decerebrate animal, in which the stretch reflexes are highly facilitated, clonus develops readily. To determine the degree of facilitation of the spinal cord, neurologists test patients for clonus by suddenly stretching a muscle and applying a steady stretching force to it. If clonus occurs, the degree of facilitation is certain to be high.
Golgi Tendon Reflex
Golgi Tendon Organ Helps Control Muscle Tension
The Golgi tendon organ, shown in Figure 54-8, is an encapsulated sensory receptor through which muscle tendon fibers pass. About 10 to 15 muscle fibers are usually connected to each Golgi tendon organ, and the organ is stimulated when this small bundle of muscle fibers is “tensed” by contracting or stretching the muscle. Thus, the major difference in excitation of the Golgi tendon organ versus the muscle spindle is that the spindle detects muscle length and changes in muscle length, whereas the tendon organ detects muscle tension as reflected by the tension in itself.
The tendon organ, like the primary receptor of the muscle spindle, has both a dynamic response and a static response, reacting intensely when the muscle tension suddenly increases (the dynamic response) but settling down within a fraction of a second to a lower level of steady-state firing that is almost directly proportional to the muscle tension (the static response). Thus, Golgi tendon organs provide the nervous system with instantaneous information on the degree of tension in each small segment of each muscle.
Transmission of Impulses from the Tendon Organ into the Central Nervous System
Signals from the tendon organ are transmitted through large, rapidly conducting type Ib nerve fibers that average 16 micrometers in diameter, only slightly smaller than those from the primary endings of the muscle spindle. These fibers, like those from the primary spindle endings, transmit signals both into local areas of the cord and, after synapsing in a dorsal horn of the cord, through long fiber pathways such as the spinocerebellar tracts into the cerebellum and through still other tracts to the cerebral cortex. The local cord signal excites a single inhibitory interneuron that inhibits the anterior motor neuron. This local circuit directly inhibits the individual muscle without affecting adjacent muscles. The relation between signals to the brain and function of the cerebellum and other parts of the brain for muscle control is discussed in Chapter 56.
Inhibitory Nature of the Tendon Reflex and Its Importance
When the Golgi tendon organs of a muscle tendon are stimulated by increased tension in the connecting muscle, signals are transmitted to the spinal cord to cause reflex effects in the respective muscle. This reflex is entirely inhibitory. Thus, this reflex provides a negative feedback mechanism that prevents the development of too much tension on the muscle.
When tension on the muscle and, therefore, on the tendon becomes extreme, the inhibitory effect from the tendon organ can be so great that it leads to a sudden reaction in the spinal cord that causes instantaneous relaxation of the entire muscle. This effect is called the lengthening reaction; it is probably a protective mechanism to prevent tearing of the muscle or avulsion of the tendon from its attachments to the bone. We know, for instance, that direct electrical stimulation of muscles in the laboratory, which cannot be opposed by this negative reflex, can occasionally cause such destructive effects.
Possible Role of the Tendon Reflex to Equalize Contractile Force Among the Muscle Fibers
Another likely function of the Golgi tendon reflex is to equalize contractile forces of the separate muscle fibers. That is, those fibers that exert excess tension become inhibited by the reflex, whereas those that exert too little tension become more excited because of absence of reflex inhibition. This spreads the muscle load over all the fibers and prevents damage in isolated areas of a muscle where small numbers of fibers might be overloaded.
Function of the Muscle Spindles and Golgi Tendon Organs in Conjunction with Motor Control from Higher Levels of the Brain
Although we have emphasized the function of the muscle spindles and Golgi tendon organs in spinal cord control of motor function, these two sensory organs also apprise the higher motor control centers of instantaneous changes taking place in the muscles. For instance, the dorsal spinocerebellar tracts carry instantaneous information from both the muscle spindles and the Golgi tendon organs directly to the cerebellum at conduction velocities approaching 120 m/sec, the most rapid conduction anywhere in the brain or spinal cord. Additional pathways transmit similar information into the reticular regions of the brain stem and, to a lesser extent, all the way to the motor areas of the cerebral cortex. As discussed in Chapters 55 and 56, the information from these receptors is crucial for feedback control of motor signals that originate in all these areas.
Flexor Reflex and the Withdrawal Reflexes
In the spinal or decerebrate animal, almost any type of cutaneous sensory stimulus from a limb is likely to cause the flexor muscles of the limb to contract, thereby withdrawing the limb from the stimulating object. This is called the flexor reflex.
In its classic form, the flexor reflex is elicited most powerfully by stimulation of pain endings, such as by a pinprick, heat, or a wound, for which reason it is also called a nociceptive reflex, or simply a pain reflex. Stimulation of touch receptors can also elicit a weaker and less prolonged flexor reflex.
If some part of the body other than one of the limbs is painfully stimulated, that part will similarly be withdrawn from the stimulus, but the reflex may not be confined to flexor muscles, even though it is basically the same type of reflex. Therefore, the many patterns of these reflexes in the different areas of the body are called withdrawal reflexes.
Neuronal Mechanism of the Flexor Reflex
The left-hand portion of Figure 54-9 shows the neuronal pathways for the flexor reflex. In this instance, a painful stimulus is applied to the hand; as a result, the flexor muscles of the upper arm become excited, thus withdrawing the hand from the painful stimulus.
Figure 54-9 Flexor reflex, crossed extensor reflex, and reciprocal inhibition.
The pathways for eliciting the flexor reflex do not pass directly to the anterior motor neurons but instead pass first into the spinal cord interneuron pool of neurons and only secondarily to the motor neurons. The shortest possible circuit is a three- or four-neuron pathway; however, most of the signals of the reflex traverse many more neurons and involve the following basic types of circuits: (1) diverging circuits to spread the reflex to the necessary muscles for withdrawal; (2) circuits to inhibit the antagonist muscles, called reciprocal inhibition circuits; and (3) circuits to cause afterdischarge lasting many fractions of a second after the stimulus is over.
Figure 54-10 shows a typical myogram from a flexor muscle during a flexor reflex. Within a few milliseconds after a pain nerve begins to be stimulated, the flexor response appears. Then, in the next few seconds, the reflex begins to fatigue, which is characteristic of essentially all complex integrative reflexes of the spinal cord. Finally, after the stimulus is over, the contraction of the muscle returns toward the baseline, but because of afterdischarge, it takes many milliseconds for this to occur. The duration of afterdischarge depends on the intensity of the sensory stimulus that elicited the reflex; a weak tactile stimulus causes almost no afterdischarge, but after a strong pain stimulus, the afterdischarge may last for a second or more.
Figure 54-10 Myogram of the flexor reflex showing rapid onset of the reflex, an interval of fatigue, and, finally, afterdischarge after the input stimulus is over.
The afterdischarge that occurs in the flexor reflex almost certainly results from both types of repetitive discharge circuits discussed in Chapter 46. Electrophysiologic studies indicate that immediate afterdischarge, lasting for about 6 to 8 milliseconds, results from repetitive firing of the excited interneurons themselves. Also, prolonged afterdischarge occurs after strong pain stimuli, almost certainly resulting from recurrent pathways that initiate oscillation in reverberating interneuron circuits. These, in turn, transmit impulses to the anterior motor neurons, sometimes for several seconds after the incoming sensory signal is over.
Thus, the flexor reflex is appropriately organized to withdraw a pained or otherwise irritated part of the body from a stimulus. Further, because of afterdischarge, the reflex can hold the irritated part away from the stimulus for 0.1 to 3 seconds after the irritation is over. During this time, other reflexes and actions of the central nervous system can move the entire body away from the painful stimulus.
Pattern of Withdrawal
The pattern of withdrawal that results when the flexor reflex is elicited depends on which sensory nerve is stimulated. Thus, a pain stimulus on the inward side of the arm elicits not only contraction of the flexor muscles of the arm but also contraction of abductor muscles to pull the arm outward. In other words, the integrative centers of the cord cause those muscles to contract that can most effectively remove the pained part of the body away from the object causing the pain. Although this principle, called the principle of “local sign,” applies to any part of the body, it is especially applicable to the limbs because of their highly developed flexor reflexes.
Crossed Extensor Reflex
About 0.2 to 0.5 second after a stimulus elicits a flexor reflex in one limb, the opposite limb begins to extend. This is called the crossed extensor reflex. Extension of the opposite limb can push the entire body away from the object causing the painful stimulus in the withdrawn limb.
Neuronal Mechanism of the Crossed Extensor Reflex
The right-hand portion of Figure 54-9 shows the neuronal circuit responsible for the crossed extensor reflex, demonstrating that signals from sensory nerves cross to the opposite side of the cord to excite extensor muscles. Because the crossed extensor reflex usually does not begin until 200 to 500 milliseconds after onset of the initial pain stimulus, it is certain that many interneurons are involved in the circuit between the incoming sensory neuron and the motor neurons of the opposite side of the cord responsible for the crossed extension. After the painful stimulus is removed, the crossed extensor reflex has an even longer period of afterdischarge than does the flexor reflex. Again, it is presumed that this prolonged afterdischarge results from reverberating circuits among the interneuronal cells.
Figure 54-11 shows a typical myogram recorded from a muscle involved in a crossed extensor reflex. This demonstrates the relatively long latency before the reflex begins and the long afterdischarge at the end of the stimulus. The prolonged afterdischarge is of benefit in holding the pained area of the body away from the painful object until other nervous reactions cause the entire body to move away.
Figure 54-11 Myogram of a crossed extensor reflex showing slow onset but prolonged afterdischarge.
Reciprocal Inhibition and Reciprocal Innervation
We previously pointed out several times that excitation of one group of muscles is often associated with inhibition of another group. For instance, when a stretch reflex excites one muscle, it often simultaneously inhibits the antagonist muscles. This is the phenomenon of reciprocal inhibition, and the neuronal circuit that causes this reciprocal relation is called reciprocal innervation. Likewise, reciprocal relations often exist between the muscles on the two sides of the body, as exemplified by the flexor and extensor muscle reflexes described earlier.
Figure 54-12 shows a typical example of reciprocal inhibition. In this instance, a moderate but prolonged flexor reflex is elicited from one limb of the body; while this reflex is still being elicited, a stronger flexor reflex is elicited in the limb on the opposite side of the body. This stronger reflex sends reciprocal inhibitory signals to the first limb and depresses its degree of flexion. Finally, removal of the stronger reflex allows the original reflex to reassume its previous intensity.
Figure 54-12 Myogram of a flexor reflex showing reciprocal inhibition caused by an inhibitory stimulus from a stronger flexor reflex on the opposite side of the body.
Reflexes of Posture and Locomotion
Postural and Locomotive Reflexes of the Cord
Positive Supportive Reaction
Pressure on the footpad of a decerebrate animal causes the limb to extend against the pressure applied to the foot. Indeed, this reflex is so strong that if an animal whose spinal cord has been transected for several months—that is, after the reflexes have become exaggerated—is placed on its feet, the reflex often stiffens the limbs sufficiently to support the weight of the body. This reflex is called the positive supportive reaction.
The positive supportive reaction involves a complex circuit in the interneurons similar to the circuits responsible for the flexor and cross extensor reflexes. The locus of the pressure on the pad of the foot determines the direction in which the limb will extend; pressure on one side causes extension in that direction, an effect called the magnet reaction. This helps keep an animal from falling to that side.
Cord “Righting” Reflexes
When a spinal animal is laid on its side, it will make uncoordinated movements trying to raise itself to the standing position. This is called the cord righting reflex. Such a reflex demonstrates that some relatively complex reflexes associated with posture are integrated in the spinal cord. Indeed, an animal with a well-healed transected thoracic cord between the levels for forelimb and hindlimb innervation can right itself from the lying position and even walk using its hindlimbs in addition to its forelimbs. In the case of an opossum with a similar transection of the thoracic cord, the walking movements of the hindlimbs are hardly different from those in a normal opossum—except that the hindlimb walking movements are not synchronized with those of the forelimbs.
Stepping and Walking Movements
Rhythmical Stepping Movements of a Single Limb
Rhythmical stepping movements are frequently observed in the limbs of spinal animals. Indeed, even when the lumbar portion of the spinal cord is separated from the remainder of the cord and a longitudinal section is made down the center of the cord to block neuronal connections between the two sides of the cord and between the two limbs, each hindlimb can still perform individual stepping functions. Forward flexion of the limb is followed a second or so later by backward extension. Then flexion occurs again, and the cycle is repeated over and over.
This oscillation back and forth between flexor and extensor muscles can occur even after the sensory nerves have been cut, and it seems to result mainly from mutually reciprocal inhibition circuits within the matrix of the cord itself, oscillating between the neurons controlling agonist and antagonist muscles.
The sensory signals from the footpads and from the position sensors around the joints play a strong role in controlling foot pressure and frequency of stepping when the foot is allowed to walk along a surface. In fact, the cord mechanism for control of stepping can be even more complex. For instance, if the top of the foot encounters an obstruction during forward thrust, the forward thrust will stop temporarily; then, in rapid sequence, the foot will be lifted higher and proceed forward to be placed over the obstruction. This is the stumble reflex. Thus, the cord is an intelligent walking controller.
Reciprocal Stepping of Opposite Limbs
If the lumbar spinal cord is not split down its center, every time stepping occurs in the forward direction in one limb, the opposite limb ordinarily moves backward. This effect results from reciprocal innervation between the two limbs.
Diagonal Stepping of All Four Limbs—“Mark Time” Reflex
If a well-healed spinal animal (with spinal transection in the neck above the forelimb area of the cord) is held up from the floor and its legs are allowed to dangle, the stretch on the limbs occasionally elicits stepping reflexes that involve all four limbs. In general, stepping occurs diagonally between the forelimbs and hindlimbs. This diagonal response is another manifestation of reciprocal innervation, this time occurring the entire distance up and down the cord between the forelimbs and hindlimbs. Such a walking pattern is called a mark time reflex.
Another type of reflex that occasionally develops in a spinal animal is the galloping reflex, in which both forelimbs move backward in unison while both hindlimbs move forward. This often occurs when almost equal stretch or pressure stimuli are applied to the limbs on both sides of the body at the same time; unequal stimulation elicits the diagonal walking reflex. This is in keeping with the normal patterns of walking and galloping because in walking, only one forelimb and one hindlimb at a time are stimulated, which would predispose the animal to continue walking. Conversely, when the animal strikes the ground during galloping, both forelimbs and both hindlimbs are stimulated about equally; this predisposes the animal to keep galloping and, therefore, continues this pattern of motion.
An especially important cord reflex in some animals is the scratch reflex, which is initiated by itch or tickle sensation. It involves two functions: (1) a position sense that allows the paw to find the exact point of irritation on the surface of the body and (2) a to-and-fro scratching movement.
The position sense of the scratch reflex is a highly developed function. If a flea is crawling as far forward as the shoulder of a spinal animal, the hind paw can still find its position, even though 19 muscles in the limb must be contracted simultaneously in a precise pattern to bring the paw to the position of the crawling flea. To make the reflex even more complicated, when the flea crosses the midline, the first paw stops scratching and the opposite paw begins the to-and-fro motion and eventually finds the flea.
The to-and-fro movement, like the stepping movements of locomotion, involves reciprocal innervation circuits that cause oscillation.
Spinal Cord Reflexes That Cause Muscle Spasm
In human beings, local muscle spasm is often observed. In many, if not most, instances, localized pain is the cause of the local spasm.
Muscle Spasm Resulting from a Broken Bone
One type of clinically important spasm occurs in muscles that surround a broken bone. The spasm results from pain impulses initiated from the broken edges of the bone, which cause the muscles that surround the area to contract tonically. Pain relief obtained by injecting a local anesthetic at the broken edges of the bone relieves the spasm; a deep general anesthetic of the entire body, such as ether anesthesia, also relieves the spasm. One of these two anesthetic procedures is often necessary before the spasm can be overcome sufficiently for the two ends of the bone to be set back into their appropriate positions.
Abdominal Muscle Spasm in Peritonitis
Another type of local spasm caused by cord reflexes is abdominal spasm resulting from irritation of the parietal peritoneum by peritonitis. Here again, relief of the pain caused by the peritonitis allows the spastic muscle to relax. The same type of spasm often occurs during surgical operations; for instance, during abdominal operations, pain impulses from the parietal peritoneum often cause the abdominal muscles to contract extensively, sometimes extruding the intestines through the surgical wound. For this reason, deep anesthesia is usually required for intra-abdominal operations.
Still another type of local spasm is the typical muscle cramp. Electromyographic studies indicate that the cause of at least some muscle cramps is as follows: Any local irritating factor or metabolic abnormality of a muscle, such as severe cold, lack of blood flow, or overexercise, can elicit pain or other sensory signals transmitted from the muscle to the spinal cord, which in turn cause reflex feedback muscle contraction. The contraction is believed to stimulate the same sensory receptors even more, which causes the spinal cord to increase the intensity of contraction. Thus, positive feedback develops, so a small amount of initial irritation causes more and more contraction until a full-blown muscle cramp ensues.
Autonomic Reflexes in the Spinal Cord
Many types of segmental autonomic reflexes are integrated in the spinal cord, most of which are discussed in other chapters. Briefly, these include (1) changes in vascular tone resulting from changes in local skin heat (see Chapter 73); (2) sweating, which results from localized heat on the surface of the body (see Chapter 73); (3) intestinointestinal reflexes that control some motor functions of the gut (see Chapter 62); (4) peritoneointestinal reflexes that inhibit gastrointestinal motility in response to peritoneal irritation (see Chapter 66); and (5) evacuation reflexes for emptying the full bladder (see Chapter 31) or the colon (see Chapter 63). In addition, all the segmental reflexes can at times be elicited simultaneously in the form of the so-called mass reflex, described next.
In a spinal animal or human being, sometimes the spinal cord suddenly becomes excessively active, causing massive discharge in large portions of the cord. The usual stimulus that causes this is a strong pain stimulus to the skin or excessive filling of a viscus, such as overdistention of the bladder or the gut. Regardless of the type of stimulus, the resulting reflex, called the mass reflex, involves large portions or even all of the cord. The effects are (1) a major portion of the body’s skeletal muscles goes into strong flexor spasm; (2) the colon and bladder are likely to evacuate; (3) the arterial pressure often rises to maximal values, sometimes to a systolic pressure well over 200 mm Hg; and (4) large areas of the body break out into profuse sweating.
Because the mass reflex can last for minutes, it presumably results from activation of great numbers of reverberating circuits that excite large areas of the cord at once. This is similar to the mechanism of epileptic seizures, which involve reverberating circuits that occur in the brain instead of in the cord.
Spinal Cord Transection and Spinal Shock
When the spinal cord is suddenly transected in the upper neck, at first, essentially all cord functions, including the cord reflexes, immediately become depressed to the point of total silence, a reaction called spinal shock. The reason for this is that normal activity of the cord neurons depends to a great extent on continual tonic excitation by the discharge of nerve fibers entering the cord from higher centers, particularly discharge transmitted through the reticulospinal tracts, vestibulospinal tracts, and corticospinal tracts.
After a few hours to a few weeks, the spinal neurons gradually regain their excitability. This seems to be a natural characteristic of neurons everywhere in the nervous system—that is, after they lose their source of facilitatory impulses, they increase their own natural degree of excitability to make up at least partially for the loss. In most nonprimates, excitability of the cord centers returns essentially to normal within a few hours to a day or so, but in human beings, the return is often delayed for several weeks and occasionally is never complete; conversely, sometimes recovery is excessive, with resultant hyperexcitability of some or all cord functions.
Some of the spinal functions specifically affected during or after spinal shock are the following:
1. At onset of spinal shock, the arterial blood pressure falls instantly and drastically—sometimes to as low as 40 mm Hg—thus demonstrating that sympathetic nervous system activity becomes blocked almost to extinction. The pressure ordinarily returns to normal within a few days, even in human beings.
2. All skeletal muscle reflexes integrated in the spinal cord are blocked during the initial stages of shock. In lower animals, a few hours to a few days are required for these reflexes to return to normal; in human beings, 2 weeks to several months are sometimes required. In both animals and humans, some reflexes may eventually become hyperexcitable, particularly if a few facilitatory pathways remain intact between the brain and the cord while the remainder of the spinal cord is transected. The first reflexes to return are the stretch reflexes, followed in order by the progressively more complex reflexes: flexor reflexes, postural antigravity reflexes, and remnants of stepping reflexes.
3. The sacral reflexes for control of bladder and colon evacuation are suppressed in human beings for the first few weeks after cord transection, but in most cases they eventually return. These effects are discussed in Chapters 31 and 66.
Alvarez F.J., Fyffe R.E. The continuing case for the Renshaw cell. J Physiol. 2007;584:31.
Buffelli M., Busetto G., Bidoia C., et al. Activity-dependent synaptic competition at mammalian neuromuscular junctions. News Physiol Sci. 2004;19:85.
Dietz V., Sinkjaer T. Spastic movement disorder: impaired reflex function and altered muscle mechanics. Lancet Neurol. 2007;6:725.
Dietz V. Proprioception and locomotor disorders. Nat Rev Neurosci. 2002;3:781.
Duysens J., Clarac F., Cruse H. Load-regulating mechanisms in gait and posture: comparative aspects. Physiol Rev. 2000;80:83.
Frigon A. Reconfiguration of the spinal interneuronal network during locomotion in vertebrates. J Neurophysiol. 2009;101:2201.
Glover J.C. Development of specific connectivity between premotor neurons and motoneurons in the brain stem and spinal cord. Physiol Rev. 2000;80:615.
Goulding M. Circuits controlling vertebrate locomotion: moving in a new direction. Nat Rev Neurosci. 2009;10:507.
Grillner S. The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci. 2003;4:573.
Grillner S. Muscle twitches during sleep shape the precise muscles of the withdrawal reflex. Trends Neurosci. 2004;27:169.
Heckman C.J., Hyngstrom A.S., Johnson M.D. Active properties of motoneurone dendrites: diffuse descending neuromodulation, focused local inhibition. J Physiol. 2008;586:1225.
Ivanenko Y.P., Poppele R.E., Lacquaniti F. Distributed neural networks for controlling human locomotion: lessons from normal and SCI subjects. Brain Res Bull. 2009;78:13.
Kandel E.R., Schwartz J.H., Jessell T.M. Principles of Neural Science, ed 4. New York: McGraw-Hill, 2000.
Kiehn O. Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci. 2006;29:279.
Marchand-Pauvert V., Iglesias C. Properties of human spinal interneurones: normal and dystonic control. J Physiol. 2008;586:1247.
Marder E., Goaillard J.M. Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci. 2006;7:563.
Pearson K.G. Generating the walking gait: role of sensory feedback. Prog Brain Res. 2004;143:123.
Rekling J.C., Funk G.D., Bayliss D.A., et al. Synaptic control of motoneuronal excitability. Physiol Rev. 2000;80:767.
Rossignol S., Barrière G., Alluin O., et al. Re-expression of locomotor function after partial spinal cord injury. Physiology (Bethesda). 2009;24:127.
Rossignol S., Barrière G., Frigon A., et al. Plasticity of locomotor sensorimotor interactions after peripheral and/or spinal lesions. Brain Res Rev. 2008;57:228.