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 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
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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 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
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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 (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).
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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 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
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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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