Back
36
Spinal Reflexes
Keir Pearson
James Gordon
DURING NORMAL MOVEMENTS the central nervous system uses information from a vast array of sensory receptors to ensure the generation of the correct pattern of muscle activity.
Sensory information from muscles, joints, and skin, for example, is essential for regulating movement. Without this somatosensory input, gross movements tend to be imprecise, while
tasks requiring fine coordination in the hands, such as fastening buttons, are impossible (see Chapter 33).
Charles Sherrington was among the first to recognize the importance of sensory information in regulating movements. In an influential monograph published in 1906 he proposed that
simple reflexes, stereotyped movements elicited by the activation of receptors in skin or muscle, are the basic units for movement. He further proposed that complex sequences of
movements can be produced by combining simple reflexes. This view has been the guiding principle in motor physiology for much of this century. Only relatively recently has it been
modified by the recognition that many coordinated movements can be produced in the absence of sensory information. For example, in a variety of species locomotor patterns can be
initiated and maintained in the absence of patterned sensory input (Chapter 37). Nevertheless, the notion that reflexes play an important role in the patterning of motor activity is beyond
doubt. The contemporary view is that reflexes are integrated with centrally generated motor commands to produce adaptive movements.
Figure 36-1 Reflex responses are often complex and can change depending on the task.
A. Perturbation of one arm causes an excitatory reflex response in the contralateral elbow extensor muscle when the contralateral limb is used to prevent the body from moving forward,
but the same stimulus produces an inhibitory response in the muscle (reduced EMG) when the contralateral hand holds a filled cup. (Adapted from Marsden et al. 1981.)
B. Loading the thumb during a rhythmic sequence of finger-to-thumb movements produces a reflex response (shaded blue area) in the muscle moving the finger as well as the loaded
thumb muscle. The additional movement of the finger ensures that the pinching movement remains accurate. (Adapted from Cole et al. 1984.)
P.714
In this chapter we consider the principles underlying the organization and function of reflexes, focusing on spinal reflexes. The sensory stimuli for spinal reflexes arise from receptors in
muscles, joints, and skin and the neural circuitry responsible for the motor response is entirely contained within the spinal cord. Reflexes have been viewed traditionally as automatic,
stereotyped movements in response to stimulation of peripheral receptors. This view arose primarily from early studies on reduced animal preparations in which reflexes were examined
under a set of standard conditions. However, as investigators extended their studies to measure reflexes during normal behavior, our concept of reflexes changed substantially. We now
know that under normal conditions reflexes can be modified to adapt to the task. This flexibility allows reflexes to be smoothly incorporated into complex movements initiated by central
commands.
Reflexes Are Highly Adaptable and Control Movements in a Purposeful Manner
A good example of the adaptability of reflexes is seen when the muscles of the wrist of one arm are stretched while a subject is kneeling or standing. The muscles that are stretched
contract, but muscles in other limbs also contract to prevent a loss of balance. Interestingly, the reflex response of the elbow extensor of the opposite arm depends on the task being
performed by that arm. If the arm is used to stabilize the body (by holding the edge of a table), a large excitatory response is evoked in the elbow extensor muscles to resist the forward
sway of the body. If the arm is holding an unsteady object, such as a cup of tea, a reflex inhibition of the elbow extensors prevents movement of the cup (Figure 36-1A).
Another example of adaptability in reflexes is the reflex of finger and thumb flexor muscles in response to
P.715
stretching the thumb muscles. If flexion of the thumb is resisted while a subject is attempting to touch the tip of the finger rhythmically to the tip of the thumb, a short-latency reflex
response is produced in both the finger and thumb flexor muscles. The reflex in the finger flexor muscle produces a larger flexion movement of the finger to compensate for the reduced
flexion of the thumb, thus ensuring the performance of the intended task (Figure 36-1B). If the subject is simply making rhythmic thumb movements, a reflex response is produced only
in the thumb flexor muscle.
A third example of the adaptable nature of reflexes involves a conditioned flexion-withdrawal reflex. Flexion withdrawal can be associated with an auditory tone by classical conditioning
techniques (Chapter 62). Subjects are asked to place an index finger, palmar surface down, on an electrode. A mild electrical shock is then paired with the auditory tone. As one might
expect, after only a very few such pairings the auditory tone alone will elicit the withdrawal reflex. What exactly has been conditioned? Is it the contraction of a fixed group of muscles or
a behavioral act that withdraws the finger from the noxious stimulus? This question can be answered by having the subjects turn their hands over after conditioning is complete, so that
now the dorsal surface of the finger is in contact with the electrode. Most subjects will withdraw their fingers from the electrode when the tone is played, even though this means that the
opposite muscles now contract. Thus, the conditioned reflex in response to the tone is not only a stereotyped set of muscle contractions but also an appropriate behavior.
Three important principles are illustrated by these examples. First, transmission in reflex pathways is set according to the motor task. The state of the reflex pathways for any task is
referred to as functional set. Exactly how functional set is established for most motor tasks is largely unknown (the unraveling of the underlying mechanisms constitutes one of the
challenging and exciting areas of contemporary research on motor systems). Second, sensory input from a localized source generally produces reflex responses in many muscles, some of
which may be distant from the stimulus. These multiple responses are coordinated to achieve an intended goal. Third, supraspinal centers play an important role in modulating and
adapting spinal reflexes, even to the extent of reversing movements when appropriate.
In order to understand the neural basis for reflexes and how they are modified for a particular task, we must first have a thorough knowledge of the organization of reflex pathways in the
spinal cord. The spinal cord is a major site for integrating reflexes with central commands, and many qualitative features of reflexes are maintained after transection of the spinal cord.
Spinal Reflexes Produce Coordinated Patterns of Muscle Contraction
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 the limb is quickly withdrawn from a painful stimulus, usually by simultaneous contraction of all the flexor
muscles in the limb. We know that this is a spinal reflex because it persists after complete transection of the spinal cord, a condition that isolates the spinal circuits from the brain. Flexion
withdrawal is a protective reflex in which a discrete stimulus causes muscles to contract in a coordinated fashion at multiple joints. Through divergent polysynaptic reflex pathways the
sensory signal both excites motor neurons that innervate flexor muscles of the stimulated limb and inhibits motor neurons that innervate extensor muscles of the limb (Figure 36-2A).
Excitation of one group of muscles and inhibition of their antagonists is what Sherrington first called reciprocal innervation. (Antagonist muscles are those that act in the opposite
direction of a given muscle; for example, knee extensors are the antagonists of knee flexors.) Reciprocal innervation is a key principle of motor organization and is discussed later in this
chapter.
Along with flexion of the stimulated limb, 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. Contraction 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
While flexion reflexes are relatively stereotyped in form, both the spatial extent and the force of muscle contraction depend on stimulus intensity (Chapter 33). Touching a stove that is
only slightly hot may produce moderately fast withdrawal only at the wrist and elbow, while touching a stove that is very hot 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.
Thus, reflexes are not simply repetitions of a stereotyped movement pattern; they are modulated by properties of the stimulus.
Figure 36-2 Spinal reflexes involve coordinated contractions of numerous muscles in the limbs.
A. Flexion and crossed-extension reflexes are mediated via polysynaptic pathways in the spinal cord. An excitatory pathway activates motor neurons supplying ipsilateral flexor muscles,
which withdraw the limb from noxious stimuli. At the same time, motor neurons supplying contralateral extensor muscles are excited to provide support during withdrawal of the limb.
Inhibitory interneurons ensure that the motor neurons supplying antagonist muscles are inactive during the reflex response. (Adapted from Schmidt 1983.)
B.1. Stretch reflexes are mediated by monosynaptic pathways. Ia afferent fibers 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 inhibitory interneurons to inhibit the
motor neurons that innervate antagonist muscles. When a muscle is stretched the Ia afferents increase their firing rate. 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. 2. The reflex nature of contractions produced
by muscle stretch is revealed by the large contraction of an extensor muscle when it is stretched compared with the small force increase after cutting the sensory afferents in the dorsal
roots. (Adapted from Liddell and Sherrington 1924.)
P.716
P.717
Because of the similarity of the flexion-withdrawal reflex to stepping, it was once thought that walking might be generated merely as a series of flexion reflexes. We now know that a
major component of the neural control system for walking is a set of intrinsic spinal circuits that do not require sensory stimuli to produce the basic walking pattern (see Chapter 37).
Nevertheless, in mammals the intrinsic spinal circuits that control walking share many of the same interneurons that are involved in flexion reflexes.
The Stretch Reflex Acts to Resist the Lengthening of a Muscle
Perhaps the most important and certainly the most studied spinal reflex is the stretch reflex, a contraction of muscle that occurs when the muscle is lengthened. Stretch reflexes were
originally thought to be an intrinsic property of muscles. However, Sherrington showed at the turn of the century that they could be abolished by cutting either the dorsal or the ventral
roots, thus establishing that they require sensory input from the muscle to the spinal cord and a return path to the muscles. We now know that the receptor that senses the change of
length is the muscle spindle (see Box 36-1) and that the afferent axons from this receptor make direct excitatory connections to motor neurons (Figure 36-2B).
In his investigation of reflexes, Sherrington developed a valuable experimental model for investigating spinal circuitry. He carried out his experiments with 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.
When Sherrington attempted to flex passively the rigidly extended hindlimb of a decerebrate cat, he felt increased contraction of the muscles being stretched (Figure 36-2B). He called
this the stretch reflex. Sherrington also discovered that stretching a muscle caused the antagonist muscles to relax. He concluded that the stretch stimulus caused excitation of certain
motor neurons and inhibition of others (reciprocal innervation).
Decerebrate animals have stereotyped and usually heightened spinal reflexes, making it is easier to examine the factors controlling their expression. They also show a dramatic increase
in extensor muscle tone, sometimes sufficient to support the animal in the standing position. Muscle tone is increased because, in the absence of control by higher brain centers,
descending pathways from the brain stem powerfully facilitate the neuronal circuits involved in the stretch reflexes of extensor muscles.
In normal animals spinal reflexes are weaker and considerably more variable in strength than those in decerebrate animals because there is a balance between facilitation and inhibition.
Descending pathways from the cerebral cortex and other higher centers of the brain continuously modulate the strength of stretch reflexes.
Neuronal Networks in the Spinal Cord Contribute to the Purposeful Integration of Reflex Responses
The Stretch Reflex Involves a Monosynaptic Pathway
The neural circuit responsible for the stretch reflex was one of the first reflex pathways to be examined in detail (see Chapter 4). The physiological basis of this reflex was elucidated by
measuring the latency of the response evoked in ventral roots when the dorsal roots were stimulated electrically. When the large Ia afferent fibers from the primary spindle endings are
selectively activated, the reflex latency through the spinal cord is less than 1 ms. (The classification of sensory fibers from muscle is discussed in Box 36-2.) Since the delay introduced by
a single synapse is between 0.5 and 0.9 ms, it can be inferred that the Ia fibers make direct connections on the alpha motor neurons, creating a monosynaptic pathway (Figure 36-4).
Ia fibers from a muscle excite not only the motor neurons innervating that muscle (homonymous connections) but also those innervating muscles having a similar mechanical action
(heteronymous connections). The pattern of connections of Ia fibers to motor neurons can be shown directly by intracellular recording techniques. Intracellular recording has also shown
that alpha motor neurons innervating antagonistic muscles receive inhibition from Ia fibers via a specific class of inhibitory interneurons, the Ia inhibitory interneurons. This disynaptic
inhibitory pathway is the basis for reciprocal innervation; when a muscle is stretched, the antagonists relax.
Inhibitory Interneurons Coordinate the Muscles Surrounding a Joint
Reciprocal innervation is useful not just in stretch reflexes but also in voluntary movements. Relaxation of the antagonist muscle during movements enhances speed and efficiency
because the muscles that act as prime movers are not working against the contraction of opposing muscles. The Ia inhibitory interneurons
P.718
P.719
P.720
involved in the stretch reflex are also used to coordinate muscle contraction during voluntary movements. The interneurons receive inputs from collateral fibers of axons descending from
neurons in the motor cortex, which make direct excitatory connections to spinal motor neurons (Figure 36-5A). This organizational feature simplifies the control of voluntary movements
since higher centers do not have to send separate commands to the opposing muscles.
Box 36-1 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 the muscle. Their main function is to
signal changes in the length of the muscle within which they reside. Changes in the length of muscles are closely associated with changes in the angles of the joints that the muscles
cross. Thus, muscle spindles can be 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 whose central regions are noncontractile; (2) large-diameter myelinated sensory endings
that originate from the central regions of the intrafusal fibers; and (3) small-diameter myelinated motor endings that innervate the polar contractile regions of the intrafusal fibers
(Figure 36-3A). When the intrafusal fibers are stretched, often referred to as “loading the spindle,” the sensory 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, the activity in the sensory endings of muscle spindles is increased. When a muscle shortens, the spindle is unloaded and the activity
decreases.
The motor innervation of the intrafusal muscle fibers comes from small-diameter motor neurons, called gamma motor neurons to distinguish them from the large-diameter alpha
motor neurons that innervate the extrafusal muscle fibers. Contraction of the intrafusal muscle fibers does not contribute to the force of muscle contraction. Rather, activation of
gamma motor neurons causes shortening of the polar regions of the intrafusal fibers. This in turn stretches the noncontractile central region from both ends, leading to an increase in
firing rate of the sensory endings or to a greater likelihood that stretch of the muscle will cause the sensory ending to fire. Thus, the gamma motor neurons provide a mechanism for
adjusting the sensitivity of the muscle spindles.
The structure and functional behavior of muscle spindles is considerably more complicated than this simple description implies. When a muscle is stretched, there are two phases of
the change in length: 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 2
or 3 bag fibers and a variable number of chain fibers, usually about 5. Furthermore, there are two types of sensory fiber endings: a single primary ending and a variable number of
secondary endings (up to 8). The primary (Ia fiber) ending spirals around the central region of all the intrafusal muscle fibers (Figure 36-3B). The secondary (group II fiber) endings
are located adjacent to the central regions of the static bag and chain fibers. The gamma motor neurons can also be divided into two classes, dynamic and static. Dynamic gamma
motor neurons innervate the dynamic bag fibers, while the static gamma motor neurons innervate the static bag and the chain fibers.
This duality of structure is reflected in a duality of function. The steady-state or tonic discharge of both primary and secondary sensory endings signals the steady-state length of the
muscle. The primary 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, primary endings provide quick information about unexpected changes in length, useful for generating quick corrective reactions.
Increases in activity of dynamic gamma motor neurons increase the dynamic sensitivity of the primary endings but have no influence on the secondary endings. Increases in activity
of static gamma motor neurons increase the tonic level of activity in both primary and secondary endings, decrease the dynamic sensitivity of primary endings, and can prevent the
silencing of primary activity when a muscle is released from stretch (Figure 36-3C). Thus, the central nervous system can independently adjust the dynamic and static sensitivity of
the sensory fibers from muscle spindles.
Figure 36-3
A. The main components of the muscle spindle are intrafusal muscle fibers, afferent sensory fiber endings, and efferent motor fiber endings. The intrafusal fibers are specialized
muscle fibers; their central regions are not contractile. The sensory fiber endings spiral around the central regions of the intrafusal fibers and are responsive to stretch of these
fibers. Gamma motor neurons innervate the contractile polar regions of the intrafusal fibers. Contraction of the intrafusal fibers pulls on the central regions from both ends and
changes the sensitivity of the sensory fiber endings to stretch. (Adapted 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 fiber innervates all three types
of fibers, forming a primary sensory ending. A group II sensory fiber innervates 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 from Boyd 1980.)
C. Selective stimulation of the two types of gamma motor neurons has different effects on the firing of the primary sensory endings in the spindle (the Ia fibers). 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 steadystate 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 from Brown and Matthews 1966.)
Box 36-2 Selective Activation of Sensory Fibers from Muscle
Sensory fibers are classified according to their diameter. Axons with larger diameters conduct action potentials more rapidly. Because each class of receptors gives rise to afferent
fibers with diameters within a restricted range, this method of classification distinguishes to some extent the fibers that arise from the different groups of sensory receptors. The
main groups of sensory fibers from muscle are listed in Table 36-1 (see Chapter 24 for the classification of sensory fibers from skin and joints).
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 central
responses evoked by different classes of sensory fibers can be assessed by grading the strength of the electrical stimulus, and certain classes of receptors can be activated in
isolation (impossible in natural conditions).
The strength of electrical stimuli required to activate a sensory fiber is measured relative to the strength required to activate the largest afferent fibers since the largest fibers have
the lowest threshold for electrical activation. Thus group I fibers are usually activated over the range of one to two times the threshold of the largest afferents (with Ia fibers having,
on average, a slightly lower threshold than Ib fibers). Most group II fibers are activated over the range of 2-5 times the threshold, while the small group III and IV fibers require
stimulus strengths in the range of 10-50 times the threshold for activation.
Table 36-1 Classification of Sensory Fibers from Muscle
Type
Ia
Ib
II
II
III
IV
Receptor
Primary spindle endings
Golgi tendon organs
Secondary spindle endings
Nonspindle endings
Free nerve endings
Free nerve endings
Axon
12-20 µm myelinated
12-20 µm myelinated
6-12 µm myelinated
6-12 µm myelinated
2-6 µm myelinated
0.5-2 µm nonmyelinated
Sensitive to
Muscle length and rate of change of length
Muscle tension
Muscle length (little rate sensitivity)
Deep pressure
Pain, chemical stimuli, and temperature (important for physiological response to exercise)
Pain, chemical stimuli, and temperature
Reciprocal innervation of opposing muscles is not the only useful mode of coordination. Sometimes it is advantageous to contract the prime mover and the antagonist at the same time.
Such co-contraction has the effect of stiffening the joint and is most useful when precision and joint stabilization are critical. An example of this phenomenon is the co-contraction of
flexor and extensor muscles of the elbow immediately before catching a ball. The Ia inhibitory interneurons receive both excitatory and inhibitory signals from all of the major descending
pathways (Figure 36-5A). By changing the balance of excitatory and inhibitory inputs onto these interneurons, supraspinal centers can reduce reciprocal inhibition and enable cocontraction, thus controlling the relative amount of joint stiffness to meet the requirements of the motor act.
The activity of spinal motor neurons is also regulated by another important class of inhibitory interneurons, the Renshaw cells (Figure 36-5B). Renshaw cells are excited by collaterals of
the axons of motor neurons, and they make inhibitory synaptic connections to several
P.721
populations of motor neurons, including the same motor neurons that excite them, and to the Ia inhibitory interneurons. The connections of Renshaw cells to motor neurons form a
negative feedback system that may help stabilize the firing rate of the motor neurons, while the connections to the Ia inhibitory interneurons may regulate the strength of reciprocal
inhibition to antagonistic motor neurons. In addition, Renshaw cells receive significant synaptic input from descending pathways and distribute inhibition to task-related groups of motor
neurons and Ia interneurons. Thus, it is likely that they contribute to establishing the pattern of transmission in divergent group Ia pathways according to the motor task.
Divergence in Reflex Pathways Amplifies Sensory Inputs and Coordinates Muscle Contractions
In all reflex pathways in the spinal cord the afferent neurons form divergent connections with a large number of target neurons through branching of the central component of the axon.
The flexion-withdrawal reflex, for example, involves extensive divergence within the spinal cord. Stimulation of a small number of sensory afferents from a localized area of skin is
sufficient to cause contractions of widely distributed muscles and thus to produce a coordinated motor pattern.
Lorne Mendell and Elwood Henneman used computer enhancement techniques to determine the extent to which action potentials in single Ia afferent fibers are distributed among spinal
motor neurons. Examining the medial gastrocnemius motor neurons of the cat, they found that individual Ia axons make excitatory synapses with all homonymous motor neurons. This
widespread divergence effectively amplifies the effect of the signals in individual Ia fibers, producing a strong excitatory drive to the muscle within which they originate (autogenic
excitation).
Group Ia axons also provide excitatory inputs to many of the motor neurons innervating synergist muscles (up to 60% of the motor neurons for some synergists). These connections,
though widespread, are not quite as strong as the connections to homonymous motor neurons. The strength of these connections varies from muscle to muscle in a complex way
according to the similarity of the mechanical actions of the synergists. We have already noted that, in the control of voluntary movements, descending pathways make use of reciprocal
inhibition of antagonists in the stretch reflex. A similar principle holds for synergist muscles. Thus, stretch reflex pathways provide a principal mechanism by which the contractions of
different muscles can be linked together in voluntary as well as reflex actions.
Figure 36-4 Intracellular recording can be used to infer the number of synapses in a reflex pathway.
A. An intracellular recording electrode is inserted into the cell body of a motor neuron in the spinal cord that innervates an extensor muscle. Afferent axons (Ia fibers) in the nerves of
flexor and extensor muscles are stimulated and the volley of action potentials that results is recorded at the dorsal root.
B.1. When Ia fibers in the nerve to the extensor muscle are stimulated, the latency between the recording of the afferent volley and the excitatory postsynaptic potential in the motor
neuron is 0.7 ms. Since this is approximately equal to the duration of signal transmission across a single synapse, it can be inferred that the excitatory action of the stretch reflex
pathway is monosynaptic. 2. When Ia fibers in the nerve of an antagonist flexor muscle are stimulated, the latency between the recording of the afferent volley and the inhibitory
postsynaptic potential in the motor neuron is 1.6 ms. Since this is approximately twice the duration of signal transmission across a single synapse, it can be inferred that the inhibitory
action of the stretch reflex pathway is disynaptic.
Convergence of Inputs on Interneurons Increases the Flexibility of Reflex Responses
Thus far we have considered reflex pathways as though each was specialized for transmitting information from one type of sensory fiber. However, an enormous amount of sensory
information from many different
P.722
sources converges on interneurons in the spinal cord. The Ib inhibitory interneurons are one of the most intensively studied groups of interneurons that receive extensive convergent
input. These interneurons receive their principal input from Golgi tendon organs, sensory receptors that signal the tension in a muscle (Box 36-3).
Figure 36-5 Inhibitory interneurons play special roles in coordination of reflex actions.
A. The Ia inhibitory interneuron allows higher centers to coordinate opposing muscles at a joint through a single command. This inhibitory interneuron mediates reciprocal innervation in
stretch reflex circuits. In addition, it receives inputs from corticospinal descending axons, so that a descending signal that activates one set of muscles automatically leads to relaxation
of the antagonists. Other descending pathways make excitatory and inhibitory connections to this interneuron. When the balance of input is shifted to greater inhibition of the Ia
inhibitory interneuron, reciprocal inhibition will be decreased and co-contraction of opposing muscles will occur.
B. Renshaw cells produce recurrent inhibition of motor neurons. These spinal interneurons are excited by collaterals from motor neurons and then inhibit those same motor neurons.
This negative feedback system regulates motor neuron excitability and stabilizes firing rates. Renshaw cells also send collaterals to synergist motor neurons (not shown) and Ia
inhibitory interneurons. Thus, descending inputs that modulate the excitability of the Renshaw cell adjust the excitability of all the motor neurons around a joint.
Stimulation of tendon organ afferent fibers produces disynaptic or trisynaptic inhibition of homonymous motor neurons (autogenic inhibition). The action of Ib fibers is complex because
the interneurons mediating these effects also receive input from the Ia fibers from muscle spindles, low-threshold afferent fibers from cutaneous receptors, and afferent fibers from joints,
as well as both excitatory and inhibitory input from various descending pathways (Figure 36-7A). Moreover, Ib fibers form widespread connections with motor neurons innervating
muscles acting at different joints. Therefore, the spinal cord connections of the afferent fibers from tendon organs are thought to be part of spinal reflex networks that regulate whole
limb movements.
Golgi tendon organs were originally thought to have a protective function, preventing damage to muscle, since
P.723
it was assumed that they fired only when high tensions were achieved. But we now know that they also signal minute changes in muscle tension, thus providing the nervous system with
precise information about the state of contraction of the muscle. The convergence of afferent input from tendon organs, cutaneous receptors, and joint receptors onto interneurons that
inhibit motor neurons may allow for precise spinal control of muscle tension in activities such as grasping a delicate object. Combined input from these receptors excites the Ib inhibitory
interneurons
P.724
when the limb contacts the object and so reduces the level of muscle contraction to permit an appropriate soft grasp.
Box 36-3 Golgi Tendon Organs
Golgi tendon organs are sensory receptors located at the junction between muscle fibers and tendon; they are therefore connected in series to a group of skeletal muscle fibers.
These receptors are slender, encapsulated structures about 1 mm long and 0.1 mm in diameter. Each tendon organ is innervated by a single (group Ib) axon that loses its
myelination after it enters the capsule and branches into many fine endings, each of which intertwines among the braided collagen fascicles. Stretching of the tendon organ
straightens the collagen fibers, thus compressing the nerve endings and causing them to fire (Figure 36-6A). Because the free nerve endings intertwine among the collagen fiber
bundles, even very small stretches of the tendon organs can deform the nerve endings.
Whereas muscle spindles are most sensitive to changes in length of a muscle, tendon organs are most sensitive to changes in muscle tension. A particularly potent stimulus for
activating a tendon organ is a contraction of the muscle fibers connected to the collagen fiber bundle containing the receptor. The tendon organs are thus readily activated during
normal movements. This has been demonstrated by recordings from single Ib axons in humans making voluntary finger movements and in cats walking normally.
Studies in more restricted situations have shown that the average level of activity in the population of tendon organs in a muscle gives a fairly good measure of the total force in a
contracting muscle (Figure 36-6B). This close agreement between firing frequency and force is consistent with the view that the tendon organs continuously measure the force in a
contracting muscle.
Figure 36-6A When the Golgi tendon organ is stretched (usually because of contraction of the muscle), the afferent axon is compressed by the collagen fibers (see inset) and its
rate of firing increases. (Adapted from Schmidt 1983; inset adapted from Swett and Schoultz 1975.)
Figure 36-6B The discharge rate of a population of Golgi tendon organs signals the force in a muscle. Linear regression lines show the relationship between discharge rate and
force for Golgi tendon organs of the soleus muscle of the cat. (Adapted from Crago et al 1982.)
Figure 36-7 The reflex action of Ib afferent fibers from Golgi tendon organs is modulated by multiple inputs to Ib inhibitory interneurons and depends on the
behavioral state of an animal.
A. The Ib inhibitory interneurons receive convergent input from tendon organs, muscle spindles (not shown), joint and cutaneous receptors, and descending pathways.
B. When an animal is resting (quiescent), stimulation of Ib afferent fibers from the ankle extensor muscle (plantaris) inhibits ankle extensor motor neurons via Ib inhibitory
interneurons, as shown by the intracellular recording from a motor neuron (top trace). During locomotion the same stimulus excites the motor neurons via polysynaptic excitatory
pathways (bottom trace).
Centrally Generated Motor Commands Can Alter Transmission in Spinal Reflex Pathways
Both the strength and sign of synaptic transmission in spinal reflex pathways can be altered during behavioral acts. An interesting example is the change in sign in the responses evoked
by stimulation of group Ib axons during walking. As we have seen, the Ib afferent fibers from extensor muscles have an inhibitory effect on extensor motor neurons in the absence of
locomotor activity. However, during locomotion the same Ib fibers produce an excitatory effect on extensor motor neurons, and transmission in the disynaptic Ib inhibitory pathway is
depressed (Figure 36-7B). This phenomenon is referred to as state-dependent reflex reversal. Another example is the progressive decline in the strength of the monosynaptic reflex in leg
extensor muscles of humans in going from standing to walking to running. In both these examples descending signals associated with the central motor command for walking modify the
properties of transmission in spinal reflex pathways.
Tonic and Dynamic Mechanisms Regulate the Strength of Spinal Reflexes
Earlier we noted that the force of a reflex can vary even though the sensory stimulus stays constant. This variability in reflex strength depends on the flexibility of synaptic transmission in
reflex pathways. There are three possible sites in the spinal cord for modulating the strength of a spinal reflex: the alpha motor neurons, interneurons in all reflex circuits except those
having monosynaptic pathways with group Ia afferent fibers, and the presynaptic terminals of the afferent fibers (Figure 36-8A).
Descending neurons from higher centers of the nervous system, as well as from other regions of the spinal cord, make synaptic connections at these sites. These neurons can thus
regulate the strength of reflexes by changing the background (tonic) level of activity at any of these sites. For example, an increase in the tonic excitatory input to the alpha motor
neurons moves the membrane potential of these cells closer to threshold so that even the slightest reflex input will more easily activate the motor neurons (Figure 36-8B).
In addition to the modulatory effect of changes in the level of tonic activity, we have seen that reflex strength can be dynamically modulated depending on the task and the behavioral
state. The mechanisms for this dynamic modulation are thought to be similar to those for tonic modulation. However, intracellular recording experiments have suggested that presynaptic
inhibition of the primary (Ia) afferent fibers is particularly important. During locomotor activity the level of presynaptic inhibition is rhythmically modulated; this action presumably
modulates the strength of reflexes during walking.
Gamma Motor Neurons Provide a Mechanism for Adjusting the Sensitivity of Muscle Spindles
Reflexes that are initiated by stimulation of muscle spindles can also be modulated by changing the level of activity
P.725
in the gamma motor neurons, which innervate the intrafusal muscle fibers (see Box 36-1). During large muscle contractions the spindle slackens and therefore is unable to signal further
changes in muscle. One role of the gamma motor neurons is to maintain tension in the muscle spindle during active contraction, thereby ensuring its responsiveness at different lengths.
When alpha motor neurons are selectively stimulated under experimental conditions, the firing of the spindle sensory fiber shows a characteristic pause during the contraction because
the muscle is shortening and therefore unloading (slackening) the spindle. If, however, gamma motor neurons are activated at the same time as alpha motor neurons, the pause
becomes filled in because contraction of the intrafusal fibers keeps the central region of the spindle loaded, or under tension (Figure 36-9). Thus, an essential role of intrafusal fiber
innervation by gamma motor neurons is to prevent the spindle sensory fiber from falling silent when the muscle shortens as a result of active contraction, therefore enabling it to signal
length changes over the full range of muscle lengths.
This mechanism maintains the spindle firing rate within an optimal range for signaling length changes, whatever the actual length of the muscle. In many voluntary movements alpha
motor neurons are normally activated more or less in parallel with gamma motor neurons, a pattern referred to as alpha-gamma coactivation. This results in an automatic maintenance of
sensitivity
In addition to the axons of the gamma motor neurons, collaterals from alpha motor neurons also innervate the intrafusal fibers. These are referred to as skeletofusimotor, or beta,
efferents. A significant, though still unquantified, amount of skeletofusimotor innervation has been found in spindles in both cats and humans. These efferents provide the equivalent of
alpha-gamma coactivation; when skeletofusimotor neurons are activated, unloading of the spindle by contraction of extrafusal fibers is at least partially compensated by loading due to
intrafusal contraction.
Nevertheless, the existence of a skeletofusimotor system, with its forced linkage of extrafusal and intrafusal contraction, serves to highlight the importance of the independent fusimotor
system made up of the gamma motor neurons. Apparently, mammals have evolved a mechanism that allows for uncoupling the control of muscle spindles from the control of their parent
muscles. In principle, this uncoupling would allow greater flexibility in controlling the spindle output for different types of motor tasks.
This conclusion is supported by recordings in primary spindle afferents during a variety of natural movements in cats. The amount and type of activity in gamma motor neurons (static or
dynamic) are preset at a fairly steady level but vary according to the specific task or context. In general, both static and dynamic gamma motor neurons are set at higher levels as the
speed and difficulty of the movement increase. Unpredictable conditions, as when a cat is picked up or handled, lead to marked increases in dynamic gamma activity reflected in
increased spindle responsiveness when muscles are stretched. When an animal is performing a difficult task, such as walking across a narrow beam, high levels of both static and
dynamic gamma activation are present (Figure 36-10).
Figure 36-8 The strength of a spinal reflex can be modulated by changes in transmission in the reflex pathway.
A. A reflex pathway can be modified at three sites: (1) alpha motor neurons, (2) interneurons in polysynaptic pathways, and (3) afferent axon terminals. Transmitter release from the
primary afferent fibers is regulated by presynaptic inhibition (see Chapter 13).
B. An increase in tonic excitatory input maintains depolarization in the neuron (shaded) and enables an otherwise ineffective input to initiate action potentials in the neurons (Vth =
threshold voltage; Vm = membrane potential).
Thus, the nervous system uses the fusimotor system—adjusting the level of activation and the balance between activation of static and dynamic gamma motor neurons—to fine-tune the
spindles so that the ensemble output of the muscle spindles provides information most appropriate for a task. The task conditions under which independent activation of alpha and
gamma motor neurons occurs in humans have not yet been established.
Figure 36-9 Activation of gamma motor neurons during active muscle contraction enables the muscle spindles to continue sensing changes in muscle length. (Adapted
from Hunt and Kuffler 1951.)
A. Sustained tension elicits steady firing in the Ia sensory fiber.
B. A characteristic pause occurs in the ongoing discharge of the Ia fiber when the alpha motor neuron alone is stimulated. The Ia fiber stops firing because the spindle is unloaded by the
resulting contraction.
C. If a gamma motor neuron to the spindle is also stimulated, the spindle is not unloaded during the contraction and the pause in discharge of the Ia fiber is filled in.
P.726
Proprioceptive Reflexes Play an Important Role in the Regulation of Both Voluntary and Automatic Movements
All movements activate receptors in the muscles, joints, and skin. These sensory signals generated by the body's own movements were referred to as proprioceptive by Sherrington, who
proposed that they control important aspects of normal movements. A good example is the Hering-Breuer reflex, which regulates the amplitude of inspiration. Stretch receptors in the
lungs are activated during inspiration, and the Hering-Breuer reflex eventually
P.727
triggers the transition from inspiration to expiration when the lungs are expanded. A similar situation exists in the walking systems of many animals; sensory signals generated near the
end of the stance phase initiate the onset of the swing phase (see Chapter 37 for details).
Figure 36-10 Activity in the fusiform system (dynamic and static gamma motor neurons) is set at different levels for different types of behavior. During activities in
which muscle length changes slowly and predictably only static gamma motor neurons are active. Dynamic gamma motor neurons are activated during behaviors in which muscle length
may change rapidly and unpredictably. (Adapted from Prochazka et al. 1988.)
Proprioceptive signals can also contribute to the generation of motor activity during ongoing movements. This has been demonstrated in recent studies on individuals with sensory
neuropathy of the arms. These patients have abnormal reaching movements and have difficulty in accurately positioning the limb (see Chapter 33) because the lack of proprioception
results in a failure to compensate for the complex inertial properties of the human arm.
The primary function of proprioceptive reflexes in regulating voluntary movements is to adjust the motor output according to the biomechanical state of the body and limbs. This ensures
a coordinated pattern of motor activity during an evolving movement, and it provides a mechanism for compensating for the intrinsic variability of motor output.
Reflexes Involving Limb Muscles Are Mediated Through Spinal and Supraspinal Pathways
Reflexes involving the limbs are mediated by multiple pathways acting in parallel via spinal and supraspinal pathways (Figure 36-11A). Consider the response evoked by a sudden stretch
of a flexor muscle of the thumb. This response has two discrete components. The first, the M1 response, is generated via the monosynaptic connection of muscle spindle afferents to the
spinal motor neurons. The second response, the M2 response, is also a reflex response since its latency is shorter than the voluntary reaction time.
The M2 response has been observed in virtually all limb muscles. In the distal muscles M2 responses are evoked via pathways that include the motor cortex, as shown in studies of
patients with Klippel-Feil syndrome (Figure 36-11B). In this unusual condition neurons descending from the motor cortex bifurcate and make connections to homologous motor neurons
on both sides of the body. One consequence is that when the individual voluntarily moves the fingers of one hand, these movements are mirrored by movements of the fingers of the
other hand. Similarly, when the M2 component is evoked by stretching muscles of one hand, a response with the same latency is evoked in the corresponding muscle of the other hand
even though there is no M1 response in the other hand. Thus, the reflex pathway responsible for the M2 response must have traversed the motor cortex.
Reflex responses mediated via the motor cortex and other supraspinal structures are termed long-loop reflexes. Long-loop reflexes have been investigated in numerous muscles in
humans and other animals. The general
P.728
conclusion is that the cortical route for long-loop reflexes may be of primary importance in regulating contractions in distal muscles, while subcortical reflex pathways may be largely
responsible for the afferent regulation of proximal muscles. This type of organization is related to functional demands. Many tasks involving distal muscles require precise regulation by
voluntary commands. Presumably, the transmission of afferent signals to regions of the cortex most involved in controlling voluntary movements allows the commands to be quickly
adapted to the evolving needs of the task. On the other hand, more automatic motor functions, such as maintaining balance and producing gross bodily movements, can be efficiently
executed largely via subcortical and spinal pathways.
Figure 36-11 Sensory signals produce reflex responses through spinal reflex pathways and long-loop reflex pathways that involve supraspinal regions. (Adapted from
Matthews 1991.)
A. In normal individuals a brief stretch of a thumb muscle produces a short-latency M1 response in the stretched muscle followed by a long-latency M2 response. The M2 response is the
result of transmission of the sensory signal via the motor cortex.
B. In individuals with Klippel-Feil syndrome M2 response is also evoked in the corresponding thumb muscle of the opposite hand because neurons in the motor cortex activate motor
neurons bilaterally. EMG = electromyogram.
Stretch Reflexes Reinforce Central Commands for Movements
Proprioceptive reflexes can modulate motor output during voluntary movements because they function not only as discrete reflexes but also as closed feedback loops (Figure 36-12A). For
example, stretch of a muscle produces an increase in spindle discharge, leading to muscle contraction and a consequent shortening of the muscle. But this muscle shortening leads to a
decrease in spindle discharge, a reduction of muscle contraction, and a lengthening of the muscle. Thus, the stretch reflex loop acts continuously, tending to keep muscle length close to a
desired or reference value. This is referred to as feedback because the output of the system (a change in muscle length) is “fed back” and becomes the input. The stretch reflex is a
negative feedback system because it tends to counteract or reduce deviations from the reference value of the regulated variable.
In 1963 Ragnar Granit proposed that, in voluntary movements, the reference value is set by descending signals that act on both the alpha and gamma motor neurons. The rate of firing
of alpha motor neurons is set to produce the desired shortening of the muscle, while the rate of firing of gamma motor neurons is set to produce an equivalent shortening of the intrafusal
fibers of the muscle spindle. If shortening of the whole muscle is less than what is required by a task, as when a load is
P.729
greater than predicted, spindle afferent fibers increase their firing rate since the contracting intrafusal fibers are stretched (loaded) by the relatively longer length of the whole muscle. If
shortening is more than is necessary, spindle afferents decrease their firing rate since the intrafusal fibers are relatively slackened (unloaded).
Thus, one function of the monosynaptic excitatory pathway may be to provide a compensatory mechanism for unexpected alterations in load encountered by the muscles. Although direct
evidence for this role of proprioceptive reflexes is lacking, there is strong evidence that alpha and gamma motor neurons are coactivated during voluntary movements by human subjects.
In the late 1960s Åke Vallbo and Karl-Erik Hagbarth developed a technique known as microneurography to record from the largest afferents in peripheral nerves. Vallbo later showed that
during slow movements of the fingers the primary spindle afferents (group Ia fibers) from the contracting muscles increase their rate of firing even when the muscle shortens as it
contracts (Figure 36-12B). The only explanation for this finding is that the gamma motor neurons are active in synchrony with alpha motor neurons.
Further, when subjects attempted to make slow movements at a constant velocity, the trajectory of the movements showed small deviations from a constant velocity—at times the
muscle shortened quickly and at others times more slowly. The firing of the Ia sensory fiber mirrored the irregularities in the trajectory. When the velocity of flexion increased transiently,
the rate of firing in the Ia fibers decreased because the muscle was shortening more rapidly and therefore exerted less tension on the intrafusal fibers. When the velocity decreased, Ia
fiber firing increased because the muscle was shortening more slowly and therefore relative tension on the intrafusal fibers increased. This information can be used by the nervous system
to compensate for irregularities in the movement trajectory by exciting the alpha motor neurons.
Thus the stretch reflex may function as a servomechanism, that is, a feedback loop in which the output variable (actual muscle length) automatically follows a changing reference value
(intended muscle length). In theory this mechanism could permit the nervous system to produce a movement of a given distance without having to know in advance the actual load or
weight being moved. In practice, however, the stretch reflex pathways do not exert sufficient influence over motor neurons to overcome large unexpected loads. This is immediately
obvious if we consider what happens when we attempt to lift a heavy suitcase that we thought was empty. We have to pause briefly and make a new movement with much greater
muscle activation.
P.730
Stretch reflex pathways therefore provide a mechanism for compensating for small changes in load and intrinsic irregularities in the muscle contraction. This action is mediated by both
monosynaptic and long-loop pathways, with the relative contribution of each pathway dependent on the muscle and the task.
Figure 36-12 Alpha and gamma motor neurons are coactivated during voluntary movements.
A. Coactivation of alpha and gamma motor neurons by a motor command allows feedback from muscle spindles to reinforce the activation of the alpha motor neurons. Since any
disturbance during the movement alters the length of the muscle and changes the activity in the muscle spindles, altering the spindle input to the alpha motor neuron compensates for
the disturbance.
B. Recordings from the primary sensory fiber of a spindle during slow flexion of a finger show the spindle's discharge increasing. This increase in discharge rate depends on alphagamma coactivation. If the gamma motor neurons were not active the spindle would slacken and its discharge rate would decrease as the muscle shortened. (Adapted from Vallbo 1981.)
Damage to the Central Nervous System Produces Characteristic Alterations in Reflex Responses and Muscle
Tone
Stretch reflexes can be evoked in many muscles throughout the body and are routinely used in clinical examinations of patients with neurological disorders. These are typically elicited by
sharply tapping the tendon of a muscle with a reflex hammer. Hence, they are often referred to as tendon reflexes or tendon jerks, although the receptor that is stimulated, the muscle
spindle, is in the muscle belly, not the tendon. Only the primary sensory fibers in the spindle participate in the tendon reflex since these are selectively activated by the rapid stretch of
the muscle produced by the tendon tap. An electrical analog for the tendon jerk reflex is the Hoffmann reflex (Box 36-4).
Measuring alterations in the strength of the stretch reflex can assist in the diagnosis of certain conditions and in the localization of injury or disease in the central nervous system. Absent
or weak stretch reflexes often indicate a disorder of one or more of the components of the reflex arc: sensory or motor axons, the cell bodies of motor neurons, or the muscle itself.
However, because the excitability of motor neurons is dependent on both excitatory and inhibitory descending influences, either hyperactive or hypoactive stretch reflexes can result from
lesions of the central nervous system.
Interruption of Descending Pathways to the Spinal Cord Frequently Produces Spasticity
Muscle tone, the force with which a muscle resists being lengthened, depends on the intrinsic elasticity, or stiffness, of the muscles. Because muscle has elastic elements in series and
parallel that resist lengthening, it behaves like a spring. In addition to this intrinsic stiffness, however, there is a neural contribution to muscle tone; the stretch reflex feedback loop also
acts to resist lengthening of the muscle. The neural circuits responsible for stretch reflexes provide the higher centers of the nervous system with a mechanism for adjusting muscle tone
under different circumstances.
Disorders of muscle tone are frequently associated with lesions of the motor system, especially those that interfere with descending motor pathways, because the strength of stretch
reflexes is controlled by higher brain centers. These may involve both abnormal increases in tone (hypertonus) and decreases (hypotonus). The most common form of hypertonus is
spasticity, which is characterized by hyperactive tendon jerks and an increase in resistance to rapid muscle stretch. Slowly applied stretch of a muscle in a patient with spasticity may
elicit little resistance. As the speed of the stretch is progressively increased, resistance to the stretch also increases progressively. Thus spasticity is primarily a phasic phenomenon. An
active reflex contraction occurs only during a rapid stretch; when the muscle is held in a lengthened position the reflex contraction subsides. In some patients, however, the hypertonus
also has a tonic component; that is, the reflex contraction continues even after the muscle is no longer being lengthened.
The pathophysiology of spasticity is still unclear. It was long thought that the increased gain of stretch reflexes in spasticity resulted from hyperactivity of the gamma motor neurons.
Recent experiments, however, have cast doubt on this explanation. While gamma overactivity may be present in some cases, changes in the background activity of alpha motor neurons
and interneurons are probably a more important factor.
Whatever the precise mechanism that produces spasticity, the effect is a strong facilitation of transmission in the monosynaptic reflex pathway from Ia sensory fibers to alpha motor
neurons. Indeed, this has been the basis for therapeutic treatment. A common procedure today is to mimic presynaptic inhibition in the terminals of the Ia fibers. This is done by
intrathecally administering the drug baclofen to the spinal cord. This drug is an agonist of the γ-aminobutyric acid (GABA)B receptors; binding of GABA to these receptors decreases the
influx of calcium into the presynaptic terminals and hence reduces the amount of transmitter released.
Transection of the Spinal Cord in Humans Leads to a Period of Spinal Shock Followed by Hyperreflexia
Damage to the spinal cord can cause large changes in the strength of spinal reflexes. Each year about 10,000 individuals in the United States have spinal cord injuries in which the cord is
effectively transected. More than half of these injuries produce permanent disability, including impairment of motor and sensory functions (Box 36-5) and disruption of voluntary control
of bowel and bladder function.
When transection is complete there is usually a period immediately after the accident when all spinal reflexes below the level of the transection are reduced or completely suppressed.
This condition is known as
P.731
spinal shock. During the course of weeks and months spinal reflexes gradually return, often greatly exaggerated compared with normal. For example, a light touch to the skin of one foot
may elicit a strong flexion withdrawal reflex of the leg.
Box 36-4 The Hoffmann Reflex
An important technique, based on early work by P. Hoffmann, was introduced in the 1950s to examine the characteristics of the monosynaptic connections from Ia sensory fibers to
spinal motor neurons in humans. This technique involves electrically stimulating the Ia fibers in a peripheral nerve and recording the reflex response in the homonymous muscle. This
is known as the Hoffmann reflex, or H-reflex (Figure 36-13A).
The H-reflex is readily measured in the soleus muscle (an ankle extensor). The Ia fibers from the soleus and its synergists are excited by an electrode placed above the tibial nerve
behind the knee. The response recorded from the soleus muscle depends on stimulus strength. At low stimulus strengths a pure H-reflex is evoked, since the threshold for activation
of the Ia fibers is lower than the threshold for motor axons. As the stimulus strength is increased, motor axons supplying the soleus are excited and two distinct responses are
recorded. The first results from direct activation of the motor axons, and the second is the H-reflex evoked by stimulation of the Ia fibers (Figure 36-13B). These two components of
the evoked electromyogram are called the M-wave and the H-wave, respectively. The H-wave occurs later because it results from signals that travel to the spinal cord, across a
synapse, and back again to the muscle. The M-wave, in contrast, results from direct stimulation of the muscle.
As the stimulus strength is increased still further, the M-wave continues to become larger and the H-wave progressively declines (Figure 36-13C). The decline in the H-wave
amplitude occurs because action potentials in the motor axons propagate toward the cell body (antidromic conduction) and cancel reflexively evoked action potentials in the same
motor axons. At very high stimulus strengths only the M-wave is evoked.
Figure 36-13
A. The H-reflex is evoked by direct electrical stimulation of afferent sensory fibers from primary spindle endings in mixed nerves. The evoked volley in the sensory fibers
monosynaptically excites alpha motor neurons, which in turn activate the muscle. Muscle activation is detected by recording the electromyogram (EMG) from the muscles. At very
low stimulus strengths a pure H-reflex can be evoked because the axons from the primary spindle endings have a lower threshold for activation than all other axons.
B. As the stimulus strength is increased, motor axons are excited and spindle afferents are activated. The former produces the M-wave that precedes the H-reflex in the EMG.
C. The magnitude of the H-reflex declines at high stimulus strengths because the signals generated reflexively in the motor axon are cancelled by action potentials initiated by the
electrical stimulus in the same motor axons. At very high stimulus strengths only an M-wave is evoked. (Adapted from Schieppati 1987.)
The mechanisms underlying spinal shock and recovery are poorly understood. The initial shock is considered to be due to the sudden withdrawal of tonic facilitatory influence from the
brain. Several different mechanisms may contribute to the recovery: denervation supersensitivity, increased numbers of postsynaptic receptors, and sprouting of afferent terminals.
Interestingly, the period of recovery
P.732
P.733
P.734
P.735
from spinal shock is much shorter in animals than in humans. In nonhuman primates the recovery period is rarely more than a week; in cats and dogs it is only a few hours. The longer
recovery period for humans presumably reflects the greater influence of descending input on spinal reflex circuits. This may in turn reflect the increased complexity of upright bipedal
locomotion. Indeed, as we shall see in the next chapter, in humans with spinal cord injury recovery of automatic locomotor patterns is slight when compared with that of quadrupedal
mammals.
Box 36-5 Sensory and Motor Signs of Spinal Cord Lesions
Lesions of the spinal cord give rise to motor or sensory symptoms that are often related to a particular sensory or motor segmental level of the spinal cord. Identification of the level
of sensory or motor loss is crucial for recognizing focal lesions within the spinal cord or external compressive lesions that interrupt function below the level of the damage. Key
landmarks for locating sensory and motor lesions are listed in Tables 36-2 and 36-3.
Table 36-2 Indicators of Motor Level Lesions
Root
C3-5
C5
C7
C8
L2-4
L5
S1
Major muscles affected
Diaphragm
Deltoid, biceps
Triceps, extensors of wrist and fingers
Interossei, abductor of fifth finger
Quadriceps
Long extensor of great toe, anterior tibial
Plantar flexors, gastrocnemius
Reflex loss
—
Biceps
Triceps
—
Knee jerk
—
Ankle jerk
Motor Signs
When motor roots are injured, or when motor neurons are affected focally, symptoms in the affected muscles include weakness, wasting, fasciculation, and loss of tendon reflexes.
When descending motor tracts are injured, symptoms in the muscles innervated below the level of the lesions include weakness, increased tendon reflexes, and spasticity. For
unilateral lesions of the spinal cord motor signs will almost always be ipsilateral, since the main motor tracts, and especially the corticospinal tract, cross in the brain stem and
descend on the same side of the spinal cord as the motor neurons they innervate.
Sensory Signs
The characteristic pattern of sensory loss is loss of cutaneous sensation below the level of the lesion. For unilateral lesions, however, the pattern may be complex. The pathway
carrying pain and temperature information (the anterolateral system) ascends on the opposite side of the cord, while the pathway responsible for discriminative touch, vibration
sense, and position sense ascends on the same side of the cord. In addition, it is necessary to distinguish between sensory loss resulting from spinal lesions and sensory loss caused
by lesions of peripheral nerves or isolated nerve roots.
When multiple peripheral nerves are affected by disease (polyneuropathy), cutaneous sensation loss occurs in the hands and feet (Figure 36-14A). This predominately distal pattern
is attributed to impaired axonal transport, or dying back (Chapter 16). The parts most affected are those most distant from the sensory neuron cell bodies in the dorsal root ganglia.
When single peripheral nerves or sensory roots are injured, the distribution of sensory loss is more restricted and can be recognized by reference to sensory charts (Figure 36-15).
Complete Transection of the Spinal Cord
Complete transection of the spinal cord leads to loss of all sensation and all voluntary movement below the level of the lesion (Figure 36-14B). Bladder and bowel control are also
lost. If the lesion is above C3, breathing may be affected. It is important to remember that the spinal cord ends at the level of the base of the second lumbar vertebra. Below this
level the spinal canal is occupied by the lower nerve roots. Therefore, injuries to the spinal canal below vertebral level L2 cause sensory loss in the regions of the body innervated by
the lower lumbar and sacral nerve roots as well as weakness and decreased tendon reflexes in certain leg muscles (Figure 36-14C).
Table 36-3 Indicators of Sensory Level Lesions
Root
C4
C8
T4
T10
L1
L3
L5
S1
S3-5
Major sensory areas affected
Clavicle
Fifth finger
Nipples
Umbilicus
Inguinal ligament
Anterior surface of the thigh
Great toe
Lateral aspect of the foot
Perineum
Partial Transection
With partial transection of the spinal cord some ascending or descending tracts may be spared. Partial function is retained but specific motor and sensory signs are evident.
Hemisection of the spinal cord, also called Brown-Séquard syndrome, causes a characteristic and easily recognized pattern (Figure 36-14D). If one side of the cord is transected,
there are ipsilateral weakness and spasticity in certain muscle groups (corticospinal tract), ipsilateral loss of discriminative touch, vibration, and position sense (dorsal column), and
contralateral loss of pain and temperature (anterolateral system). While a precise hemisection is quite rare, this syndrome is fairly common since many traumatic lesions
predominately affect one side of the cord or the other.
Another example of a lesion that causes an incomplete transection is syringomyelia, a condition in which cysts form within the central portion of the spinal cord and progressively
worsen. Because the lesions start centrally, the first fibers to be affected are those carrying pain and temperature fibers, since they decussate in the anterior commissure. This
usually causes bilateral loss of pain and temperature sensation, restricted to the segments involved (Figure 36-14E). Unless and until the cysts significantly enlarge, discriminative
touch and position sense are usually spared.
Figure 36-14 Sensory deficits resulting from damage to the spinal cord or nerve roots (segmental) and deficits resulting from damage to peripheral nerves.
Figure 36-15 Map of cutaneous innervation of the body differ depending on whether one is looking at the areas of skin innervated by nerve roots (center) or
peripheral nerves (right and left). By carefully mapping the area of sensory loss, therefore, one can determine the locus of damage (nerve root or peripheral nerve) and the
specific nerves or roots involved. Note that the area of skin innervated by a single nerve root is often referred to as a dermatome.
An Overall View
Reflexes are coordinated, involuntary motor responses initiated by a stimulus applied to peripheral receptors. Some reflexes initiate movements to avoid potentially hazardous situations,
whereas others automatically adapt motor patterns to maintain, or to achieve, a behavioral goal. The purposeful responses evoked by reflexes depend on mechanisms that set the
strength and pattern of responses according to the task and behavioral state (known as functional set). Currently we know little about the details of these mechanisms, except for the fact
that modification of transmission in spinal reflex pathways by descending signals from the brain is thought to be an important factor.
Many groups of interneurons in the reflex pathways of the spinal cord are also involved in producing complex movements such as walking and transmitting voluntary commands from the
brain. In addition, some components of reflex responses, particularly components of reflexes involving the limbs, are mediated via supraspinal centers (brain stem nuclei, cerebellum, and
motor cortex). The convergence of afferent signals onto spinal and supraspinal interneuronal systems involved in initiating movements provides the basis for the smooth integration of
reflexes into centrally generated motor commands. Establishing details of these integrative events is one of the major challenges of contemporary research on reflex regulation of
movement.
Because descending pathways from the brain continuously modulate transmission in spinal reflex pathways, damage or disease of the central nervous system often results in significant
alterations in the strength of spinal reflexes. The pattern of changes is an important aid to diagnosis of patients with neurological disorders.
Selected Readings
Baldissera F, Hultborn H, Illert M. 1981. Integration in spinal neuronal systems. In: JM Brookhart, VB Mountcastle, VB Brooks, SR Geiger (eds). Handbook of Physiology: The
Nervous System, pp. 509-595. Bethesda, MD: American Physiological Society.
Boyd IA. 1980. The isolated mammalian muscle spindle. Trends Neurosci 3:258–265.
Dietz V. 1992. Human neuronal control of automatic functional movements: interaction between central programs and afferent input. Physiol Rev 72:33–61.
Jankowska E. 1992. Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38:335–378.
Matthews PBC. 1991. The human stretch reflex and the motor cortex. Trends Neurosci 14:87–90.
Prochazka A. 1996. Proprioceptive feedback and movement regulation. In: L Rowell, JT Sheperd (eds). Handbook of Physiology: Regulation and Integration of Multiple Systems, pp.
89-127. New York: American Physiological Society.
References
Appenteng K, Prochazka A. 1984. Tendon organ firing during active muscle lengthening in normal cats. J Physiol (Lond) 353:81–92.
Brown MC, Matthews PBC. 1966. On the subdivision of the efferent fibres to muscle spindles into static and dynamic fusimotor fibres. In: BL Andrew (ed). Control and Innervation of
Skeletal Muscle, pp. 18-31. Dundee, Scotland: University of St. Andrews.
Cole KJ, Gracco VL, Abbs JH. 1984. Autogenetic and nonautogenetic sensorimotor actions in the control of multiarticulate hand movements. Exp Brain Res 56:582–585.
Crago A, Houk JC, Rymer WZ. 1982. Sampling of total muscle force by tendon organs. J Neurophysiol 47:1069–1083.
Gossard JP, Brownstone RM, Barajon I, Hultborn H. 1994. Transmission in a locomotor-related group Ib pathway from hindlimb extensor muscles in the cat. Exp Brain Res
98:213–228.
Granit R. 1970. Basis of Motor Control. London: Academic.
Hagbarth KE, Kunesch EJ, Nordin M, Schmidt R, Wallin EU. 1986. Gamma loop contributing to maximal voluntary contractions in man. J Physiol (Lond) 380:575–591.
Hoffman P. 1922. Untersuchungen über die Eigenreflexe (Sehuenreflexe) menschlicher Muskeln. Berlin: Springer.
Hulliger M. 1984. The mammalian muscle spindle and its central control. Rev Physiol Biochem Pharmacol 101:1–110.
Hunt CC, Kuffler SW. 1951. Stretch receptor discharges during muscle contraction. J Physiol (Lond) 113:298–315.
Liddell EGT, Sherrington C. 1924. Reflexes in response to stretch (myotatic reflexes). Proc R Soc Lond B Biol Sci 96:212–242.
Marsden CD, Merton PA, Morton HB. 1981. Human postural responses. Brain 104:513–534.
Matthews PBC. 1972. Muscle Receptors. London: Edward Arnold.
P.736
Mendell LM, Henneman E. 1971. Terminals of single Ia fibers: location, density, and distribution within a pool of 300 homonymous motoneurons. J Neurophysiol 34:171–187.
Pearson KG, Collins DF. 1993. Reversal of the influence of group Ib afferents from plantaris on activity in model gastrocnemius activity during locomotor activity. J Neurophysiol
70:1009–1017.
Prochazka A, Hulliger M, Trend P, Dürmüller N. 1988. Dynamic and static fusimotor set in various behavioural contexts. In: P Hnik, T Soukup, R Vejsada, J Zelena (eds).
Mechanoreceptors: Development, Structure and Function, pp. 417-430. New York: Plenum.
Schieppati M. 1987. The Hoffman reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol 28:345–376.
Schmidt RF. 1983. Motor systems. In: RF Schmidt and G Thews (eds), MA Biederman-Thorson (transl). Human Physiology, pp. 81-110. Berlin: Springer.
Sherrington CS. 1906. Integrative Actions of the Nervous System. New Haven, CT: Yale Univ. Press.
Swett JE, Schoultz TW. 1975. Mechanical transduction in the Golgi tendon organ: a hypothesis. Arch Italian Biol 113:374–382.
Vallbo ÅB. 1981. Basic patterns of muscle spindle discharge in man. In: A Taylor and A Prochazka (eds). Muscle Receptors and Movement, pp. 263-275. London: Macmillan.
Vallbo ÅB, Hagbarth KE, Torebjörk HE, Wallin BG. 1979. Somatosensory, proprioceptive, and sympathetic activity in human peripheral nerves. Physiol Rev 59:919–957.