Cutaneous Reflexes Produce Complex Movements That Serve Protective and Postural Functions
A familiar example of a spinal reflex is the flexion- withdrawal reflex, in which a limb is quickly withdrawn from a painful stimulus. Flexion-withdrawal is a protective reflex in which a discrete stimulus causes all the flexor muscles in that limb to contract coordinately. We know that this is a spinal reflex because it persists after complete transection of the spinal cord.
The sensory signal activates divergent polysynaptic reflex pathways. One excites motor neurons that innervate flexor muscles of the stimulated limb, whereas another inhibits motor neurons that innervate the limb's extensor muscles (Figure 35–2A). Excitation of one group of muscles and inhibition of their antagonists—those that act in the opposite direction—is what Sherrington called reciprocal innervation, a key principle of motor organization that is discussed later in this chapter.
Spinal reflexes involve coordinated contractions of numerous muscles in the limbs.
A. Polysynaptic pathways in the spinal cord mediate flexion and crossed-extension reflexes. One excitatory pathway activates motor neurons that innervate ipsilateral flexor muscles, which withdraw the limb from noxious stimuli. Another pathway simultaneously excites motor neurons that innervate contralateral extensor muscles, providing support during withdrawal of the limb. Inhibitory interneurons ensure that the motor neurons supplying antagonist muscles are inactive during the reflex response. (Adapted, with permission, from Schmidt 1983.)
B. Monosynaptic pathways mediate stretch reflexes. Afferent axons from muscle spindles make excitatory connections on two sets of motor neurons: alpha motor neurons that innervate the same (homonymous) muscle from which they arise and motor neurons that innervate synergist muscles. They also act through interneurons to inhibit the motor neurons that innervate antagonist muscles. When a muscle is stretched by a tap with a reflex hammer, the firing rate in the afferent fiber from the spindle increases. This leads to contraction of the same muscle and its synergists and relaxation of the antagonist. The reflex therefore tends to counteract the stretch, enhancing the spring-like properties of the muscles. The records on the right demonstrate the reflex nature of contractions produced by muscle stretch in a decerebrate cat. When an extensor muscle is stretched it normally produces a large force, but it produces a very small force (dashed line) after the sensory afferents in the dorsal roots have been severed. (Adapted, with permission, from Liddell and Sherrington 1924.)
The reflex can produce an opposite effect in the contralateral limb, that is, excitation of extensor motor neurons and inhibition of flexor motor neurons. This crossed-extension reflex serves to enhance postural support during withdrawal of a foot from a painful stimulus. Activation of the extensor muscles in the opposite leg counteracts the increased load caused by lifting the stimulated limb. Thus, flexion-withdrawal is a complete, albeit simple, motor act.
Although flexion reflexes are relatively stereotyped, both the spatial extent and the force of muscle contraction depend on stimulus intensity. Touching a stove that is slightly hot may produce moderately fast withdrawal only at the wrist and elbow, whereas touching a very hot stove invariably leads to a forceful contraction at all joints, leading to a rapid withdrawal of the entire limb. The duration of the reflex usually increases with stimulus intensity, and the contractions produced in a flexion reflex always outlast the stimulus.
Because of the similarity of the flexion-withdrawal reflex to stepping, it was once thought that the flexion reflex is important in producing contractions of flexor muscles during walking. We now know, however, that a major component of the neural control system for walking is a set of intrinsic spinal circuits that do not require sensory stimuli (see Chapter 36). Nevertheless, in mammals the intrinsic spinal circuits that control walking share many of the interneurons that are involved in flexion reflexes.
The Stretch Reflex Resists the Lengthening of a Muscle
Perhaps the most important—certainly the most studied—spinal reflex is the stretch reflex, a lengthening contraction of a muscle. Stretch reflexes were originally thought to be an intrinsic property of muscles. But early in the last century Liddell and Sherrington showed that they could be abolished by cutting either the dorsal or the ventral root, thus establishing that these reflexes require sensory input from muscle to spinal cord and a return path to muscle (Figure 35–2B).
We now know that the receptor that senses the change of length is the muscle spindle (Box 35–1) and that the type Ia axon from this receptor makes direct excitatory connections with motor neurons. (The classification and nomenclature of sensory fibers from muscle are discussed in Box 35–2.) The afferent axon also connects to interneurons that inhibit the motor neurons that innervate antagonist muscles, another instance of reciprocal innervation. This inhibition prevents muscle contractions that might otherwise resist the movements produced by the stretch reflexes.
Box 35–1 Muscle Spindles
Muscle spindles are small encapsulated sensory receptors that have a spindle-like or fusiform shape and are located within the fleshy part of a muscle. Their main function is to signal changes in the length of the muscle within which they reside. Changes in length of muscles are closely associated with changes in the angles of the joints that the muscles cross. Thus muscle spindles are used by the central nervous system to sense relative positions of the body segments.
Each spindle has three main components: (1) a group of specialized intrafusal muscle fibers with central regions that are noncontractile; (2) sensory fibers that terminate in the noncontractile central regions of the intrafusal fibers; and (3) motor axons that terminate in the polar contractile regions of the intrafusal fibers (Figure 35–3A).
When the intrafusal fibers are stretched, often referred to as "loading the spindle," the sensory nerve endings are also stretched and increase their firing rate. Because muscle spindles are arranged in parallel with the extrafusal muscle fibers that make up the main body of the muscle, the intrafusal fibers change in length as the whole muscle changes. Thus, when a muscle is stretched, activity in the sensory endings of muscle spindles increases. When a muscle shortens, the spindle is unloaded and the activity decreases.
The intrafusal muscle fibers are innervated by gamma motor neurons, which have small-diameter myelinated axons, whereas the extrafusal muscle fibers are innervated by alpha motor neurons, with large-diameter myelinated axons. Activation of gamma motor neurons causes shortening of the polar regions of the intrafusal fibers. This in turn stretches the central region from both ends, leading to an increase in firing rate of the sensory endings or to a greater likelihood that the sensory endings will fire in response to stretch of the muscle. Thus the gamma motor neurons adjust the sensitivity of the muscle spindles. Contraction of the intrafusal muscle fibers does not contribute significantly to the force of muscle contraction.
The structure and functional behavior of muscle spindles is considerably more complex than this simple description implies. When a muscle is stretched the change in length has two phases: a dynamic phase, the period during which length is changing, and a static or steady-state phase, when the muscle has stabilized at a new length. Structural specializations within each component of the muscle spindles allow spindle afferents to signal aspects of each phase separately.
There are two types of intrafusal muscle fibers: nuclear bag fibers and nuclear chain fibers. The bag fibers can be divided into two groups, dynamic and static. A typical spindle has two or three bag fibers and a variable number of chain fibers, usually about five. Furthermore, the intrafusal fibers receive two types of sensory endings. A single Ia (large diameter) axon spirals around the central region of all intrafusal muscle fibers and serves as the primary sensory ending (Figure 35–3B). A variable number of type II (medium diameter) axons, located adjacent to the central regions of the static bag and chain fibers, serve as secondary sensory endings.
The gamma motor neurons can also be divided into two classes: Dynamic gamma motor neurons innervate the dynamic bag fibers, whereas the static gamma motor neurons innervate the static bag fibers and the chain fibers.
This duality of structure is reflected in a duality of function. The tonic discharge of both primary and secondary sensory endings signals the steady-state length of the muscle. The primary sensory endings are, in addition, highly sensitive to the velocity of stretch, allowing them to provide information about the speed of movements. Because they are highly sensitive to small changes, the primary endings rapidly provide information about sudden unexpected changes in length, which can be used to generate quick corrective reactions.
Increases in the firing rate of dynamic gamma motor neurons increase the dynamic sensitivity of primary sensory endings but have no influence on secondary sensory endings. Increases in the firing rate of static gamma motor neurons increase the tonic level of activity in both primary and secondary sensory endings, decrease the dynamic sensitivity of primary endings (Figure 35–3C), and can prevent the silencing of primary endings when a muscle is released from stretch. Thus the central nervous system can independently adjust the dynamic and static sensitivity of the different sensory endings in muscle spindles.
The muscle spindle detects changes in muscle length.
A. The main components of the muscle spindle are intrafusal muscle fibers, afferent sensory endings, and efferent motor endings. The intrafusal fibers are specialized muscle fibers with central regions that are not contractile. Gamma motor neurons innervate the contractile polar regions of the intrafusal fibers. Contraction of the polar regions pulls on the central regions of the intrafusal fiber from both ends. The sensory endings spiral around the central regions of the intrafusal fibers and are responsive to stretch of these fibers. (Adapted, with permission, from Hulliger 1984.)
B. The muscle spindle contains three types of intrafusal fibers: dynamic nuclear bag, static nuclear bag, and nuclear chain fibers. A single Ia sensory axon innervates all three types of fibers, forming a primary sensory ending. Type II sensory axons innervate the nuclear chain fibers and static bag fibers, forming a secondary sensory ending. Two types of motor neurons innervate different intrafusal fibers. Dynamic gamma motor neurons innervate only dynamic bag fibers; static gamma motor neurons innervate various combinations of chain and static bag fibers. (Adapted, with permission, from Boyd 1980.)
C. Selective stimulation of the two types of gamma motor neurons has different effects on the firing of the Ia fibers from the spindle. Without gamma stimulation the Ia fiber shows a small dynamic response to muscle stretch and a modest increase in steady-state firing. When a static gamma motor neuron is stimulated, the steady-state response of the Ia fiber increases, but there is a decrease in the dynamic response. When a dynamic gamma motor neuron is stimulated, the dynamic response of the Ia fiber is markedly enhanced, but the steady-state response gradually returns to its original level. (Adapted, with permission, from Brown and Matthews 1966.)
Box 35–2 Classification of Sensory Fibers from Muscle
Sensory fibers are classified according to their diameter. Axons with larger diameters conduct action potentials more rapidly than do fibers of smaller diameters. Because each class of sensory receptors is innervated by fibers with diameters within a restricted range, this method of classification distinguishes to some extent the fibers that arise from the different types of receptor organs. The main groups of sensory fibers from muscle are listed in Table 35–1.
The organization of reflex pathways in the spinal cord has been established primarily by electrically stimulating the sensory fibers and recording evoked responses in different classes of neurons in the spinal cord. This method of activation has three advantages over natural stimulation. The timing of afferent input can be precisely established; the responses evoked in motor neurons and other neurons by different classes of sensory fibers can be assessed by grading the strength of the electrical stimulus; and certain classes of receptors can be selectively activated.
The strength of the electrical stimulus required to activate a sensory fiber is measured relative to the strength required to activate the afferent fibers with the largest diameter because these fibers have the lowest threshold for electrical activation. The threshold of type I fibers is usually one to two times that of the largest afferents (with Ia fibers having, on average, a slightly lower threshold than Ib fibers). For most type II fibers the threshold is 2 to 5 times higher, whereas type III and IV have thresholds in the range of 10 to 50 times that of the largest afferents.
Table 35–1Classification of Sensory Fibers from Muscle ||Download (.pdf) Table 35–1 Classification of Sensory Fibers from Muscle
|Type ||Axon ||Receptor ||Sensitive to |
|Ia ||12–20 μm myelinated ||Primary spindle ending ||Muscle length and rate of change of length |
|Ib ||12–20 μm myelinated ||Golgi tendon organ ||Muscle tension |
|II ||6–12 μm myelinated ||Secondary spindle ending ||Muscle length (little rate sensitivity) |
|II ||6–12 μm myelinated ||Nonspindle endings ||Deep pressure |
|III ||2–6 μm myelinated ||Free nerve endings ||Pain, chemical stimuli, and temperature (important for physiological responses to exercise) |
|IV ||0.5–2 μm nonmyelinated ||Free nerve endings ||Pain, chemical stimuli, and temperature |
Sherrington developed an experimental model for investigating spinal circuitry that is especially valuable in the study of stretch reflexes. He conducted his experiments on cats whose brain stems had been surgically transected at the level of the midbrain, between the superior and inferior colliculi. This is referred to as a decerebrate preparation. The effect of this procedure is to disconnect the rest of the brain from the spinal cord, thus blocking sensations of pain as well as interrupting normal modulation of reflexes by higher brain centers. A decerebrate animal has stereotyped and usually heightened stretch reflexes, making it is easier to examine the factors controlling their expression.
Without control by higher brain centers, descending pathways from the brain stem powerfully facilitate the neuronal circuits involved in the stretch reflexes of extensor muscles. This results in a dramatic increase in extensor muscle tone that sometimes suffices to support the animal in a standing position. In normal animals, owing to the balance between facilitation and inhibition, stretch reflexes are weaker and considerably more variable in strength than those in decerebrate animals.