Passive stretching of a skeletal muscle causes a reflexive contraction of that same muscle and relaxation of the antagonist muscles
Reflexes are among the most basic of neural functions and involve some of the simplest neuronal circuits. A motor reflex is a rapid, stereotyped motor response to a particular sensory stimulus. Although the existence of reflexes had been long appreciated, it was Sir Charles Sherrington N10-2 who, beginning in the 1890s, first defined the anatomical and physiological bases for some simple spinal reflexes. So meticulous were Sherrington's observations of reflexes and their timing that they offered him compelling evidence for the existence of synapses, a term he originated.
Reflexes are essential, if rudimentary, elements of behavior. Because of their relative simplicity, more than a century of research has taught us a lot about their biological basis. However, reflexes are also important for understanding more complex behaviors. Intricate behaviors may sometimes be built up from sequences of simple reflexive responses. In addition, neural circuits that generate reflexes almost always mediate or participate in much more complex behaviors. Here we examine a relatively well understood example of reflex-mediating circuitry.
The CNS commands the body to move about by activating motor neurons, which excite skeletal muscles (Sherrington called motor neurons the final common path). Motor neurons receive synaptic input from many sources within the brain and spinal cord, and the output of large numbers of motor neurons must be closely coordinated to achieve even uncomplicated actions such as walking. However, in some circumstances, motor neurons can be commanded directly by a simple sensory stimulus—muscle stretch—with only the minimum of neural machinery intervening between the sensory cell and motor neuron: one synapse. Understanding of this simplest of reflexes, the stretch reflex or myotatic reflex, first requires knowledge of some anatomy.
Each motor neuron, with its soma in the spinal cord or brainstem, commands a group of skeletal muscle cells; a single motor neuron and the muscle cells that it synapses on are collectively called a motor unit (see pp. 241–242). Each muscle cell belongs to only one motor unit. The size of motor units varies dramatically and depends on muscle function. In small muscles that generate finely controlled movements, such as the extraocular muscles of the eye, motor units tend to be small and may contain just a few muscle fibers. Large muscles that generate strong forces, such as the gastrocnemius muscle of the leg, tend to have large motor units with as many as several thousand muscle fibers. There are two types of motor neurons (see Table 12-1): α motor neurons innervate the main force-generating muscle fibers (the extrafusal fibers), whereas γ motor neurons innervate only the fibers of the muscle spindles. The group of all motor neurons innervating a single muscle is called a motor neuron pool (see pp. 241–242).
When a skeletal muscle is abruptly stretched, a rapid, reflexive contraction of the same muscle often occurs. The contraction increases muscle tension and opposes the stretch. This stretch reflex is particularly strong in physiological extensor muscles—those that resist gravity—and it is sometimes called the myotatic reflex because it is specific for the same muscle that is stretched. The most familiar version is the knee jerk, which is elicited by a light tap on the patellar tendon. The tap deflects the tendon, which then pulls on and briefly stretches the quadriceps femoris muscle. A reflexive contraction of the quadriceps quickly follows (Fig. 16-3). Stretch reflexes are also easily demonstrated in the biceps of the arm and the muscles that close the jaw. Sherrington showed that the stretch reflex depends on the nervous system and requires sensory feedback from the muscle. For example, cutting the dorsal (sensory) roots to the lumbar spinal cord abolishes the stretch reflex in the quadriceps muscle. The basic circuit for the stretch reflex begins with the primary sensory axons from the muscle spindles (see p. 388) in the muscle itself. Increasing the length of the muscle stimulates the spindle afferents, particularly the large group Ia axons from the primary sensory endings. In the spinal cord, these group Ia sensory axons terminate monosynaptically onto the α motor neurons that innervate the same (i.e., the homonymous) muscle from which the group Ia axons originated. Thus, stretching a muscle causes rapid feedback excitation of the same muscle through the minimum possible circuit: one sensory neuron, one central synapse, and one motor neuron (Box 16-1).
FIGURE 16-3 Knee-jerk (myotatic) reflex. Tapping the patellar tendon with a percussion hammer elicits a reflexive knee jerk caused by contraction of the quadriceps muscle: the stretch reflex. Stretching the tendon pulls on the muscle spindle, exciting the primary sensory afferents, which convey their information via group Ia axons. These axons make monosynaptic connections to the α motor neurons that innervate the quadriceps, resulting in the contraction of this muscle. The Ia axons also excite inhibitory interneurons that reciprocally innervate the motor neurons of the antagonist muscle of the quadriceps (the flexor), resulting in relaxation of the semitendinosus muscle. Thus, the reflex relaxation of the antagonistic muscle is polysynaptic.
Motor System Injury
The motor control systems, because of their extended anatomy, are especially susceptible to damage from trauma or disease. The nature of a patient's motor deficits often allows the neurologist to diagnose the site of neural damage with great accuracy. When injury occurs to lower parts of the motor system, such as motor neurons or their axons, deficits may be very localized. If the motor nerve to a muscle is damaged, that muscle may develop paresis (weakness) or complete paralysis (loss of motor function). When motor axons cannot trigger contractions, there can be no reflexes (areflexia). Normal muscles are slightly contracted even at rest—they have some tone. If their motor nerves are transected, muscles become flaccid (atonia) and eventually develop profound atrophy (loss of muscle mass) because of the absence of trophic influences from the nerves.
Motor neurons normally receive strong excitatory influences from the upper parts of the motor system, including regions of the spinal cord, the brainstem, and the cerebral cortex. When upper regions of the motor system are injured by stroke, trauma, or demyelinating disease, for example, the signs and symptoms are distinctly different from those caused by lower damage. Complete transection of the spinal cord leads to profound paralysis below the level of the lesion. This is called paraplegia when only both legs are selectively affected, hemiplegia when one side of the body is affected, and quadriplegia when the legs, trunk, and arms are involved. For a few days after an acute injury, there is also areflexia and reduced muscle tone (hypotonia), a condition called spinal shock. The muscles are limp and cannot be controlled by the brain or by the remaining circuits of the spinal cord. Spinal shock is temporary; after days to months, it is replaced by both an exaggerated muscle tone (hypertonia) and heightened stretch reflexes (hyperreflexia) with related signs—this combination is called spasticity. The biological mechanisms of spasticity are poorly understood, although the hypertonia is the consequence of tonically overactive stretch reflex circuitry, driven by spinal neurons that have become chronically hyperexcitable.
Monosynaptic connections account for much of the rapid component of the stretch reflex, but they are only the beginning of the story. At the same time the stretched muscle is being stimulated to contract, parallel circuits are inhibiting the α motor neurons of its antagonist muscles (i.e., those muscles that move a joint in the opposite direction). Thus, as the knee-jerk reflex causes contraction of the quadriceps muscle, it simultaneously causes relaxation of its antagonists, including the semitendinosus muscle (see Fig. 16-3). To achieve inhibition, branches of the group Ia sensory axons excite specific interneurons that inhibit the α motor neurons of the antagonists. This reciprocal innervation increases the effectiveness of the stretch reflex by minimizing the antagonistic forces of the antagonist muscles.
Force applied to the Golgi tendon organ regulates muscle contractile strength
Skeletal muscle contains another mechanosensory transducer in addition to the stretch receptor: the Golgi tendon organ (see p. 388). Tendon organs are aligned in series with the muscle; they are exquisitely sensitive to the tension within a tendon and thus respond to the force generated by the muscle rather than to muscle length. Tendon organs may respond during passive muscle stretch, but they are stimulated particularly well during active contractions of a muscle. The group Ib sensory axons of the tendon organs excite both excitatory and inhibitory interneurons within the spinal cord (Fig. 16-4). In some cases, this interneuron circuitry inhibits the muscle in which tension has increased and excites the antagonistic muscle; therefore, activity in the tendon organs can yield effects that are almost the opposite of the stretch reflex. Under other circumstances, particularly during rapid movements such as locomotion, sensory input from Golgi tendon organs actually excites the motor neurons activating the same muscle. The reflex effects of Golgi tendon organ activity vary because the interneurons receiving input from Ib axons also receive input from other sensory endings in the muscle and skin, and from axons descending from the brain. In general, reflexes mediated by the Golgi tendon organs serve to control the force within muscles and the stability of particular joints.
FIGURE 16-4 Golgi tendon organ reflex. Contraction of the quadriceps muscle can elicit a reflexive relaxation of this muscle and contraction of the antagonistic semitendinosus muscle. Contraction of the muscle pulls on the tendon; this squeezes and excites the sensory endings of the Golgi tendon organ, which convey their information via group Ib axons. These axons synapse on both inhibitory and excitatory interneurons in the spinal cord. The inhibitory interneurons innervate α motor neurons to the quadriceps, relaxing this muscle. The excitatory interneurons innervate α motor neurons to the antagonistic semitendinosus muscle, contracting it. Thus, both limbs of the reflex are polysynaptic.
Noxious stimuli can evoke complex reflexive movements
Sensations from the skin and connective tissue can also evoke strong spinal reflexes. Imagine walking on a beach and stepping on a sharp piece of shell. Your response is swift and coordinated and does not require thoughtful reflection: you rapidly withdraw the wounded foot by activating the leg flexors and inhibiting the extensors. To keep from falling, you also extend your opposite leg by activating its extensors and inhibiting its flexors (Fig. 16-5). This response is an example of a flexion-withdrawal reflex. The original stimulus for the reflex came from fast pain afferent neurons in the skin, primarily the group Aδ axons.
FIGURE 16-5 Flexion-withdrawal reflex. A painful stimulus to the right foot elicits a reflexive flexion of the right knee and an extension of the left knee. The noxious stimulus activates nociceptor afferents, which convey their information via group Aδ axons. These axons synapse on both inhibitory and excitatory interneurons. The inhibitory interneurons that project to the right side of the spinal cord innervate α motor neurons to the quadriceps and relax this muscle. The excitatory interneurons that project to the right side of the spinal cord innervate α motor neurons to the antagonistic semitendinosus muscle and contract it. The net effect is a coordinated flexion of the right knee. Similarly, the inhibitory interneurons that project to the left side of the spinal cord innervate α motor neurons to the left semitendinosus muscle and relax this muscle. The excitatory interneurons that project to the left side of the spinal cord innervate α motor neurons to the left quadriceps and contract it. The net effect is a coordinated extension of the left knee.
This bilateral flexor reflex response is coordinated by sets of inhibitory and excitatory interneurons within the spinal gray matter. Note that this coordination requires circuitry not only on the side of the cord ipsilateral to the wounded side but also on the contralateral side. That is, while you withdraw the foot that hurts, you must also extend the opposite leg to support your body weight. Flexor reflexes can be activated by most of the various sensory afferents that detect noxious stimuli. Motor output spreads widely up and down the spinal cord, as it must to orchestrate so much of the body's musculature into an effective response. A remarkable feature of flexor reflexes is their specificity. Touching a hot surface, for example, elicits reflexive withdrawal of the hand in the direction opposite the side of the stimulus, and the strength of the reflex is related to the intensity of the stimulus. Unlike simple stretch reflexes, flexor reflexes coordinate the movement of entire limbs and even pairs of limbs. Such coordination requires precise and widespread wiring of the spinal interneurons.
Spinal reflexes are strongly influenced by control centers within the brain
Axons descend from numerous centers within the brainstem and the cerebral cortex and synapse primarily on the spinal interneurons, with some direct input to the motor neurons. This descending control is essential for all conscious (and much unconscious) command of movement, a topic beyond the scope of this chapter. Less obvious is that the descending pathways can alter the strength of reflexes. For example, to heighten an anxious patient's stretch reflexes, a neurologist will sometimes ask the patient to perform the Jendrassik maneuver. The patient clasps his or her hands together and pulls; while the patient is distracted with that task, the examiner tests the stretch reflexes of the leg. Another example of the brain's modulation of a stretch reflex occurs when you catch a falling ball. If a ball were to fall unexpectedly from the sky and hit your outstretched hand, the force applied to your arm would cause a rapid stretch reflex—contraction in the stretched muscles and reciprocal inhibition in the antagonist muscles. The result would be that your hand would slap the ball back up into the air. However, if you anticipate catching the falling ball, for a short period around the time of impact (about ±60 ms), both your stretched muscles and the antagonist muscles contract! This maneuver stiffens your arm just when you need to squeeze that ball to avoid dropping it. Stretch reflexes of the leg also vary dramatically during each step as we walk, thereby facilitating movement of the legs.
Like stretch reflexes, flexor reflexes can also be strongly affected by descending pathways. With mental effort, painful stimuli can be tolerated and withdrawal reflexes suppressed. On the other hand, anticipation of a painful stimulus may heighten the vigor of a withdrawal reflex when the stimulus actually arrives. Most of the brain's influence on spinal circuitry is achieved by control of the many spinal interneurons.
Spinal reflexes are frequently studied in isolation from one another, and textbooks often describe them this way. However, under realistic conditions, many reflex systems operate simultaneously, and motor output from the spinal cord depends on interactions among them as well as on the state of controlling influences descending from the brain. It is now well accepted that reflexes do not simply correct for external perturbations of the body; in addition, they play a key role in the control of all movements.
The neurons involved in reflexes are the same neurons that generate other behaviors. Think again of the flexor response to the sharp shell—the pricked foot is withdrawn while the opposite leg extends. Now imagine that a crab pinches that opposite foot—you respond with the opposite pattern of withdrawal and extension. Repeat this a few times, crabs pinching you left and right, and you have achieved the basic pattern necessary for walking! Indeed, rhythmic locomotor patterns use components of these same spinal reflex circuits, as discussed next.