CHAPTER 1. The Muscle Spindle and the Central Nervous System
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1 CHAPTER 1 The Muscle Spindle and the Central Nervous System The muscle spindle deserves special attention because of its important role as the prime organ of muscle sense. Although misunderstood (for the most part) and discounted by most research literature as a simple organ of reflex action, its importance becomes obvious when its distribution, structure, innervation and its relationships with the central nervous system are explored. The muscle spindle is found in all skeletal (somatic) muscles. The number of muscle spindles in each muscle varies from one muscle to the next. The concentration of spindle population in a muscle depends upon its function. The more delicate the movement, the higher the muscle spindle count. In the latissimus dorsi muscle, for example, there are approximately 350 muscle spindles or 1.4 muscle spindles per gram of muscle tissue. In the abductor pollicis brevis muscle there are approximately 80 muscle spindles, or 30 muscle spindles per gram of muscle tissue. The latissimus dorsi muscle s primary functions are gross strength and stabilization. It provides the gross shoulder motions of abduction and extension and provides for position stabilization during elbow, wrist and finger machinations. The abductor pollicis brevis performs fine thumb movements. It provides delicate motions of thumb abduction and interrelates with other muscles of the thumb and fingers to provide the complex coordinated movements. Such quantitative relationships between muscle spindle concentration and muscle function suggest the need to examine the muscle spindle construction and function in more depth. The muscle spindle is cylindrical, tapering to thin tails on either end, suggesting a spindle shape. Its covering (or capsule) is made up of connective tissue which encapsulates muscle fibers (intrafusal muscle fibers) varying from three to ten in number. These muscle fibers are separated from the capsule by fluid. The muscle spindle lies within normal muscle fibers (extrafusal muscle fibers) in parallel alignment with them. The intrafusal muscle fibers are made up of two distinct types, nuclear bag and nuclear chain fibers. The nuclear bag fiber is relatively large. It has a broad noncontractile equatorial region made up of a high concentration of nuclear cells. This region is connected to its two ends by striated contractile polar segments that taper down as they extend the full length of the muscle spindle. The nuclear chain fibers are similarly composed, but their noncontractile equatorial regions are thin and made up of a single chain of muscle nuclei. The fibers are considerably shorter than the nuclear bag fibers and depend on inelastic collagen fibers for connection between striated contractile polar segments and the capsular endings. The nuclear chain fibers are more numerous and are believed to surround the nuclear bag fibers. The capsular endings are directly or indirectly inserted on extrafusal muscle tendon by inelastic connective tissue. The muscle spindle is innervated by two afferent (sensory) nerve types that supply the annulospiral and flower spray nerve end organs. The annulospiral nerve end organ (the primary sensory end organ) spirals around the equatorial regions of each of the intrafusal 5
2 fibers. It feeds back information on the length of the muscle spindle and on the speed or velocity of muscle stretch (phasic response). This end organ is supplied by a fairly large sensory neuron (17 microns in diameter) which has a rapid conduction speed compared with the conduction rate of the smaller nerve (eight microns) supplying the flower spray ending. The flower spray nerve end organs are most commonly found on one of the polar segments of each of the nuclear chain intrafusal fibers (a small percentage of nuclear bag polar segments have been reported to be supplied by flower spray end organs). Although considerable conjecture has been made, no hard evidence has been put forth to substantiate flower spray nerve end organ function. They are, however, rather insensitive to rapid changes in fiber length and are therefore thought to be responsible for the perception of tonic response from the nuclear chain fiber. The muscle spindle is also equipped with an efferent (motor) nerve supply in the form of gamma neurons innervating motor end plates (similar to those on extrafusal muscle) and fine axonal elongated end organs called trail endings (gamma nerve fibers account for 30% of the efferent nerve supply). The motor end plates occur only on the nuclear bag fibers (each fiber having several) and the trail endings occur only on the nuclear chain. These endings are supplied by efferent gamma nerve fibers (see Figure 1). Some controversy exists over this contention, and in regard to much of the spindle innervation. For example, it is clear that gamma efferent neurons innervate spindle contractile mechanisms, and this innervation was thought to be exclusive, but there is some evidence that other neuron types may also supply spindle efferent innervation. One study (Adal and Barker, 1965, reported by Brodal) produced enough histological evidence to suggest an efferent beta (or slow-alpha) fiber simultaneous innervation of both extrafusal and intrafusal fibers; this contention was supported by Granit, Henatsch, and Steg (1956, reported by Brodal), who physiologically showed that there are two types of alpha motor neurons supplying extrafusal muscle. One type, the phasic alpha neuron, was shown to be a large fast conducting nerve fiber innervating pale extrafusal fibers utilized for rapid forceful contractions. The other, the tonic alpha motor neuron (sometimes called the slow-beta neuron), is a relatively smaller slow conducting fiber which innervates red extrafusal muscle fibers used to sustain prolonged contractions (in joint stabilization). Some tonic alpha motor neurons have been shown to innervate intrafusal muscle fibers. Presumably, they aid in coordination of the tonic activities of extrafusal and intrafusal muscle, but further research should be conducted to explore this function. Research techniques are still greatly limited and many questions regarding the muscle spindle have yet to be fully answered. It is quite clear that not only is the muscle spindle a sensory mechanism, but also an active mechanism of contraction influenced by the supraspinal structures as well. To understand the muscle spindle and its relationship to the nervous system, we first need to explore its operation. The muscle spindle is stimulated by stretch. First, stretch is perceived by the muscle spindle sensory elements when the entire host muscle is stretched and this stretch is communicated to the muscle spindle via its tendon insertions. Second, it can also be made to perceive stretch by efferent activation of the contractile 6
3 polar segments of its intrafusal muscle fibers. When these segments are made to shorten, the sensory endings perceive this as stretch. Both sensory elements (annulospiral and 7
4 flower spray end organs) send impulses to the spinal cord. Stretch perception results in an increase in the constant nervous impulse rate produced by the sensory nerve endings. The primary receptor (annulospiral sensory end organ) responds to sudden stretching in a fraction of a millisecond, producing a large number of impulses that are translated into information on the speed of receptor length-change. When not being stretched, its steady impulses indicate the actual length of the receptor (the intrafusal fiber). The secondary receptor (flower spray sensory end organ) requires several milliseconds to respond to sudden stretch, and its impulses are interpreted to describe only actual fiber length to the central nervous system. Thus, the muscle spindle serves as a comparator between intrafusal fiber length and extrafusal fiber length. The sensory data supplied by the muscle spindle is important to central nervous system appreciation of muscle length and muscle stretch. The muscle spindle becomes even more important when it is understood how its sensory feedback affects motor activity. Traditionally, the muscle spindle has held a place of honor as the primary organ responsible for the phasic stretch reflex. This reflex is not only useful as a functionally advantageous mechanism, but also as a diagnostic tool. The phasic stretch reflex (PSR) is a fairly simple, monosynaptic mechanism that every voluntary muscle employs. The PSR begins with a sudden stretch of the whole muscle, which is perceived by the annulospiral end organs as the intrafusal fibers are stretched. The annulospiral end organ responds with a sudden increase in the output of sensory impulses that are transmitted via the sensory neurons to the spinal cord. The sensory neuron synapses with the alpha motor nerve to cause the extrafusal muscle to contract (see Figure 2). Coinciding with alpha nerve transmission, the motor nerves of the muscle s antagonist are inhibited to prevent them from causing antagonistic contraction and interfering with the agonist contraction. As the extrafusal fibers become comparatively shorter than the intrafusal fibers, the impulse production of the spindle is discontinued. Stimulation of the alpha motor nerve ceases, and the extrafusal muscle relaxes. This mechanism allows the muscle to automatically oppose any attempt to stretch or lengthen it beyond the tonic length set by the muscle spindle. Simultaneously, as the alpha motor neuron transmits its impulses to the extrafusal muscle, inhibitory impulses are transmitted to the motor neurons of its antagonist to prevent it from contracting and interfering with the stretched muscle s response. The phasic stretch reflex is used diagnostically to assess the degree of facilitation by the central nervous system upon spinal cord centers. If the inhibitory function of some of the central mechanisms are not fully operable (as in a post CVA or other lesion of the central nervous system) the muscle jerks will be exaggerated and may be used to determine the presence of spasticity. If the stretch reflex is missing or weak, it may imply a lesion involving the anterior horn cells. However, relatively few (if any) tendon jerks of the type used diagnostically occur in the life of the muscle, and one can be sure that they were not provided as a convenience for investigators. The phasic stretch reflex serves to help increase the strength of extrafusal muscle contraction if the load on a muscle is suddenly increased. This helps to keep the muscle at the length set by the muscle spindle. 8
5 While the phasic stretch reflex is dependent upon sensory impulses entering the dorsal roots from the muscle spindle, the tonic stretch reflex is dependent upon activation from supraspinal structures. The structures provide continuous stimulation of the gamma motor nerves to the muscle spindle (nuclear chain fibers). If the supraspinal structures influence the intrafusal fibers to contract to a length shorter than the surrounding extrafusal fibers, the sensory elements (flower spray end organs) perceive this pull on its polar attachments as stretch and increase production of sensory impulses above the previous rate. The impulses are conveyed to the spinal cord via the sensory nerve that synapses with the interneuronal pool. The involved interneurons synapse with the appropriate afferent neurons to the supraspinal structures and to alpha motor neurons (see Figure 3). Any increase in this stimulation causes the alpha motor nerves to stimulate the extrafusal muscle to contract. Any decrease in impulse production allows the extrafusal muscle to lengthen. The involved alpha neurons are continually being stimulated to keep the extrafusal fibers at the same length as the intrafusal fibers. The supraspinal structures are able, through this mechanism, to maintain muscle tone required for long-term joint stability. This mechanism plays a large role in maintaining muscle health and strength when the muscle is disused for long periods. It is also responsible for the tension and spasm seen in the psychogenic neuromuscular syndromes (the defense mechanism of somatization). This mechanism is sometimes called the tonic stretch reflex, but really serves as a servo system that affords coordination of agonist and antagonist musculature too. It will continue to maintain the tonic contraction until the 9
6 muscle spindle is readjusted or an extrafusal phasic (voluntary) contraction occurs. This system is responsible for ordinary muscle contractions resulting from tonic muscle spindle activity, programmed in the cerebellum ( learned fine motor skills). The two systems would appear to be incompatible when the phasic control of agonist muscle activity is compared with the tonic control of the antagonist muscle, especially when the effects of the phasic stretch reflex on the antagonist are considered as the agonist is caused to phasically contract. However, a mechanism is provided which allows the extrafusal agonist muscle to phasically contract without interference from the muscle spindles of the antagonist muscle. Should joint notion be desired, the alpha motor system is activated by the cerebral motor cortex. As the impulses descend the corticospinal tract, impulses are also sent to the reticular formation to influence the gamma motor system to inhibit the tonic gamma neurons to the antagonist muscle spindles, allowing the muscle to lengthen as the agonist shortens. Simultaneously, the antagonistic phasic gamma neurons are activated to allow the intrafusal fibers to lengthen only to a given length (as determined by the supraspinal structures) to provide for a phasic stretch reflex when the antagonist has reached the desired length, halting agonist shortening. To prohibit the reflex response from relengthening the agonist, the phasic gamma neurons to the muscle spindles of the agonist set the intrafusal fibers at the desired shortened length to provide a counter phasic stretch reflex. This results in a series of short rebounds or vibrations between the two muscles that eventually allows the joint to come to a fixed and precise position. 10
7 Other sensory organs (including the Pacinian corpuscle) play a role in the task of supplying information to the supraspinal structures on muscle activity. The most important of these is the Golgi tendon organ (GTO). The GTO lies within tendinous muscle tissue. Each GTO is connected in series with small bundles of extrafusal muscle fibers (10 to 15). Its primary function is to detect changes in tension on the tendon from muscle pull or from external force (see Figure 4). When an increase in tension occurs, the GTO responds with a large burst of sensory impulses of short duration. After this over response, it settles down to a steady state of relatively low frequency impulses. The impulses it generates are transmitted by large, rapidly conducting sensory neurons (Aalpha type, slightly smaller than those innervating muscle spindle sensory end organs) to the dorsal columns. Before joining the dorsal cerebellar tract, it synapses with interneurons. The impulses ascending to the cerebellum augment or supplement the afferent impulses from the muscle spindle. The impulses to the alpha motor neurons are inhibitory of alpha motor neuron response to the phasic stretch reflex (see Figure 5). 11
8 The coordination of tonic and phasic elements requires a high degree of coordinated interaction between the supraspinal structures. This coordination depends upon feedback loops existing between these structures. It also depends upon feedback loops between the supraspinal structures and the effector organs (muscles, viscera, etc.) and, to a degree, upon negative feedback from the environment (sight, sound, vibration, etc.) (see Figure 6). In normal human beings, the supraspinal structures primarily depend upon feedback from the muscle spindles to begin the task of motor control ( you need to perceive it to use it ). The effect of the supraspinal structures on efferent motor control impulses are facilitory and/or inhibitory on flexor and/or extensor motor activity. The exploration of these relationships is not deemed pertinent to this discussion, especially in light of the fact that there is a dearth of available information. The afferent impulses from the muscle spindle are conveyed to the cerebellum by the spinocerebellar tracts. Those impulses are passed to the red nucleus and the thalamus. Those impulses to the red nucleus help coordinate data descending from the basal ganglia (caudate nucleus, putamen and globus pallidus), and the cerebral motor cortex via the corticospinal tract to affect the gamma motor system. Those impulses passing to the thalamus are correlated with data from the red nucleus and globus pallidus and are then passed on to the cerebral motor cortex (Figure 7). 12
9 Descending impulses from the cerebral motor cortex take two separate (though correlated) pathways. Impulses descending to the gamma motor system, which innervates the muscle spindles, take a direct route through the basal ganglia. They first enter the caudate nucleus, then the putamen, and finally, the globus pallidus. The data passing through the caudate nucleus and putamen are modified by thalamic impulses as part of the error control mechanism before passing to the globus pallidus. From the globus pallidus, impulses are passed to the thalamus and red nucleus. The impulses that pass to the thalamus complete a major communication loop. The basal ganglia s primary function is to aid in the process of collaboration between the cerebral cortex and the thalamus through this loop. The caudate nucleus and globus pallidus send data to the olive (olivary nuclei) as part of the error control system. Error control data is also sent from the globus pallidus to the subthalamus and substantia nigra. The subthalamus and substantia nigra, in turn, send their error control data to the red nucleus and 13
10 reticular formation, respectively. Those impulses descending from the globus pallidus are correlated with data descending along the corticospinal tract and with ascending data relayed from the cerebellum in the red nucleus, and are then passed on to the reticular formation to be correlated with the error control data from the olive and substantia nigra and with direct impulses from the corticospinal tract, and are then passed through the pons to the reticulospinal tract (to affect both phasic and tonic) gamma motor neurons and finally to the muscle spindle intrafusal fibers. Impulses may also pass from the cerebral motor cortex by way of the corticospinal tract, to directly synapse with the alpha motor neurons that stimulate extrafusal muscle fibers. The alpha and gamma neurons are also affected by other supraspinal structures, including the vestibular nucleus (via the vestibulospinal tract) and the red nucleus (via the rubospinal tract). Little is known about the effects of these structures on the motor activities of man. In animals, a tract from the red nucleus (the rubospinal tract), like the corticospinal tract, is said to affect facilitation of the alpha and tonic gamma neurons that innervate the flexors and inhibit the extensor alpha and tonic gamma neurons. The vestibulospinal tract is said to contrarily affect facilitation of the alpha and gamma neurons, innervating the extensors and inhibiting the flexor neurons. In man, because of the rearrangement of muscle relationships that permit him to stand, the affects on the motor neurons by these tracts would hypothetically be on the flexors of the upper extremities and the extensors of the lower extremities, or on the extensors of the upper extremities and the flexors of the lower extremities. However, evidence that might support the contention that these various tracts affect motor control in man, as they do in animals, is limited. Available evidence would seem to support the contention that the corticospinal tract is the primary facilitator of alpha motor neuron activity and that the reticulospinal tract is the primary facilitator of gamma motor neuron activity in both flexors and extensors of both upper and lower extremities. The other tracts would appear to act upon alpha and gamma neurons as secondary facilitators and inhibitors to help modify muscle activity in specialized functions such as balancing and the optical righting reactions. For our purposes, the vestibulospinal tract would appear to be the most discussion worthy of the accessory tracts because of its direct affect upon balance activities. The vestibular nucleus receives incoming impulses from several sensory sources including the eyes, the vestibular membranous labyrinth (semicircular canals) and the various proprioceptors throughout the body. The vestibular nucleus accepts impulses from these organs and correlates this information with data on motor function from the reticular formation and the cerebellum, and feeds its interpretation of this correlation to the cerebellum (to help modify ongoing motor functions) and to the reticular formation. In the reticular formation these impulses are correlated with both corticospinal and gamma motor system impulses from the supraspinal centers and fed into the vestibulospinal tract. Finally, the efferent fibers from the vestibulospinal tract join the final common pathway of all efferent motor tracts in the ventral horns to synapse with the alpha and gamma motor neurons of extrafusal and intrafusal muscle fibers, respectively. A more in-depth discussion of the vestibular affects on motor activity will not be attempted here. A single example of its value in motor control can be seen in individuals 14
11 suffering from post cerebral vascular accident syndromes who are dominated by third stage developmental reflexes (see Table 1). For example, if such a patient is lying prone and the head is lifted into hyperextension, the myoelectric activity from the upper extremity extensors will immediately increase and/or elbow extension will involuntarily occur, and the myoelectric activity from the flexor muscles of the involved lower extremity will increase and/or the hip and knee will flex. This is due to a reflex affect upon the alpha and gamma motor neurons by proprioceptors in the neck without inhibitory affect from the sensory epithelium of the labyrinth (semicircular canals) as the head position is changed. An illustration of the cosynapsing of spinal tract neurons on alpha and gamma motor neurons with the graphic illustration of primary and error control impulse pathways is offered in Figure 7 as an incomplete representation of the highly complex interrelating pathways that exist between the various supraspinal structures that affect motor activity. Research is not yet complete and Figure 8 is offered to illustrate just how complex the task of fully exploring and understanding central nervous system function really is. Our attempt here is designed to present a look at the forest without getting lost in the trees. 15
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