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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

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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 substan-

tiate 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

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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

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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.

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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 sti-

mulated 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

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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.

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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 (A-

alpha 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).

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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).

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Descending impulses from the cerebral motor cortex take two separate (though

correlated) pathways. Impulses descending to the gamma motor system, which in-

nervates 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

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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

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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.”

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