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Neural Control of Skeletal Muscle: The Role of Muscle Spindles and Golgi Tendon Organs, Study notes of Medicine

The function and significance of muscle spindles and golgi tendon organs in the neural control of skeletal muscle. The authors discuss their anatomical arrangement, sensitivity to muscle length changes and force development, and the role they play in feedback control. The document also touches upon recent research on the effects of vibration on muscle spindles and the importance of studying groups of synergistic muscles.

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Muscle spindles, Golgi tendon organs, and the neural control
of skeletal muscle
JOHN N. HOWELL, Ph.D.
Ohio University
College of Osteopathic Medicine
Athens, Ohio
MARC D. BINDER, Ph.D.
University of Washington
School of Medicine
Seattle, Washington
T.
RICHARD
NICHOIS, Ph.D.
Emory University
Atlanta,
Georgia
GERALD E. LOEB, M.D.
National Institutes
of
Health
Bethe&, Maryland
The purpose ofthis report is to share with
the readershia of
JAOA.
hiahliahts of a
symposium hdd at the
30tc
~nnual
Re-
search Conference of the AOA in March
1986. The invited speakers
in
the sym-
posium were Dr.-Gerald E. Loeb of
the
National Institutes
of
Health, who also
delivered the keynote address, Dr. Man:
D. Binder of the University of Wash-
ington, and Dr.
T.
Richard Nichols of
Emory University. Dr. John N. Howell of
the Ohio University College of Os-
teopathic Medicine, program chairman
for the 1986 conference,
acted
as moder-
ator for the symposium.
In introducing the symposium, Dr.
Howell pointed out that the traditional
importance
of
somatic dysfunction and its
treatment in osteopathic practice has led
to
a natural interest within osteopathic
medicine in the aroblem of control of skel-
etal muscle fun'ction. In 1974, Korr pub-
lished an important article entitled,
"Roprioceptors and somatic dysfunc-
tion."l
In
it he related the clinical find-
ings of osteopathic practitioners to what
was
then knowh about the physiology of
the proprioceptive organs within skeletal
muscle. Specifically, he postulated that
alterations of the gain of the stretch
re
ceptor system might contribute to the
etiology of somatic dyefunction and
to
its
treatment through osteopathic manip-
ulative treatment. Korr's hypothesis has
been widely accepted within osteopathic
medicine because it provided a mecha-
nism that appeared to be consistent with
a
good deal of clinical experience.
However, as Korr pointed out in a recent
article,2 his h*thesis still awaits test-
ing in the laboratory. Since the publica-
tion of Ko~r's hypothesis, additional
information has come
to
light about the
function of muscle proprioceptors. The
goal of the symposium
was
to summarize
this newer information so that it might be
available for integration into thinking
about the pathophysiology and treatment
of somatic dysfunction.
Dr.
Binder led off wi* a summary of
the traditional ideas about how muscle
epindles and Golgi tendon organs func-
tion and then focused on newer informa-
tion about the tendon organs. On
anatomical grounds, it is clear that the
spindles are arranged parallel
to
the
ex-
trafusal muscle fibers and are thus suited
to sensing length changes of the muscle.
The tendon organs, on the other hand, are
located in series with the muscle fibers
and are thus suited to detecting force gen-
erated by the muscle fibers. Spindles have
been known for some time to be sensitive
to very small perturbetions in muscle
length, producing a reflex activation, or
shortening, of the muscle being
stretched. In contrast, tendon organs
were
thought to respond only to high lev-
els of force and to provide protection
again& the development of
too
much force
by inhibiting the homonymous muscle
(i.e., muscle of origin of the reflex).
Recent work has shown this idea about
tendon organ function to be unlikely.3.4
Each tendon organ provides a point of
insertion for 3 to
25
muscle fibers.6 Ex-
perimental stimulation of a single motor
unit, one or more fibers of which insert on
a given tendon organ, will stimulate that
organ, producing a train of spikes in
Ib
afferent neurons to the spinal cord. Stim-
ulation of a motor unit which hasno fibers
inserting on a particular tendon organ
mmetimes silences that tendon or'gan if it
has been previously activated by sus-
tained stretch of the muscle. This pre-
sumably results from unloading of the
tendon organ by virtue of contraction of
adjacent muscle fibers. Each tendon
organ appears to provide insertion for fi-
bers from motor units producing a wide
range of forces. Thus, each organ may
sample muscle activity over the full range
of force development, from the small
motor units that are the first to be re-
cruited to the large units that are re-
cruited only during maximal con-
tractions. This means that the tendon
organ input
to
the cord is not restricted
to
conditions of high force development but
can
be graded over the entire range of
muscle force.
Determination of the effect of Golgi ten-
don activity on neurons within the spinal
cord has been difficult because it has not
been possible
to
selectively stimulate the
tendon organs or their Ib afferent fibers
without at the same time stimulating the
muscle spindles or their Ia sensory fibrs.
Recently it has been shown that applica-
tion of prolonged, high-frequency, low-
amplitude vibration to muscles, which is
an effective stimulus to the muscle spin-
dles: can cause a transient elevation of
the electrical thresholds of the Ia fibers.7
Under these conditions the Ib fibers can
be
eelectively stimulated and their cen-
tral connections studied.8 Available evi-
dence indicates that activation of the Ib
sensory fibers, like the activation of cuta-
neous aiTerents, can cause either excit-
atory or inhibitory postsynaptic poten-
tials to occur in motoneurons.s The site of
integration involving the Ib input as well
as inputs from other areas within the cen-
tral nervous system appears not to be the
motoneurons, but rather interneurons in
laminae
V
and
VI.
Dr. Nichols traced the development of
theories concerning the mechanical as-
pects of the spindle-mediated stretch re-
flex and went on
to
point out that most of
our knowledge has been based on the
~tudy of single muscles. He stressed the
need for extending the analysis of stretch
reflexes to groups of synergistic muscles
acting together upon a joint. A rather ex-
treme view of the role of the stretch reflex
system was proposed in 1953 by Mertonlo
who hypothesized that normal activation
of muscle might always
be
preceded by
gamma activation of the muscle spindles,
and the resultant stimulation of Ia af-
ferent~ would in turn provide the excit-
atory input to the alpha motor neurons
and cause muscle contraction. This the-
ory was referred to as the "follow-up
length servo hypothesis." It stressed the
feedback control of muscle length and the
primacy of gamma activation for muscle
contraction. It is now known, however, for
many movements, including ballistic
types and patterned activities of a re-
petitive nature, simultaneous activation
of both gamma and alpha motor neurons
occurs, generally referred to as coactiva-
tion.11 Because the larger alpha motor
neurons conduct action potentials faster
than the smaller gamma fibers, coactiva-
tion implies that extrafusal muscle fibers
must be activated before intrafusal fibers.
Thus the initial phase of contraction
oc-
curs independently of any feedback con-
tribution from the muscle spindle system.
F'urthermore, it was pointed out that the
Golgi tendon organs might also play an
important role in feedback control, so
that not only muscle length, but some
function of both force and length would
be
controlled.l2
The latter idea
was
extended further by
Houk>3 who suggested that the param-
eter controlled bv stretch reflex might
be
stiffness, definid
as
the ratio of force
,
change
to
length change. Nichols and
Houkl4 demonstrated that the linearity
,
of the spring-like behavior of muscles in
the decerebrate cat preparation
was
lost
when the proprioceptive feedback loop
was i~terrupted, i.e. when the dorsal
continued on
page
6001117
Sept. 1986lJournal of AOAIvol. 86lno. 9
pf3
pf4

Partial preview of the text

Download Neural Control of Skeletal Muscle: The Role of Muscle Spindles and Golgi Tendon Organs and more Study notes Medicine in PDF only on Docsity!

Muscle spindles, Golgi tendon organs, and the neural control

of skeletal muscle

JOHN N. HOWELL, Ph.D. Ohio University College of Osteopathic Medicine Athens, Ohio MARC D. BINDER, Ph.D. University of Washington School of Medicine Seattle, Washington

T. RICHARD NICHOIS, Ph.D.

Emory University Atlanta, Georgia GERALD E. LOEB, M.D. National Institutes of Health Bethe&, Maryland

The purpose ofthis report is to share with the readershia of JAOA. hiahliahts of a

symposium hdd a t the 30tc ~ n n u a lRe-

search Conference of the AOA in March

  1. The invited speakers in the sym-

posium were Dr.-Gerald E. Loeb of the

National Institutes of Health, who also delivered the keynote address, Dr. Man: D. Binder of the University of Wash-

ington, and Dr. T. Richard Nichols of

Emory University. Dr. John N. Howell of the Ohio University College of Os- teopathic Medicine, program chairman

for the 1986 conference, acted as moder-

ator for the symposium. In introducing the symposium, Dr. Howell pointed out that the traditional importance of somatic dysfunction and its treatment in osteopathic practice has led to a natural interest within osteopathic medicine in the aroblem of control of skel- etal muscle fun'ction. In 1974, Korr pub- lished an important article entitled, "Roprioceptors and somatic dysfunc-

tion."l In it he related the clinical find-

ings of osteopathic practitioners to what was then knowh about the physiology of the proprioceptive organs within skeletal muscle. Specifically, he postulated that

alterations of the gain of the stretch r e

ceptor system might contribute to the etiology of somatic dyefunction and to its treatment through osteopathic manip- ulative treatment. Korr's hypothesis has been widely accepted within osteopathic medicine because it provided a mecha- nism that appeared to be consistent with

a good deal of clinical experience.

However, as Korr pointed out in a recent article,2 his h*thesis still awaits test- ing in the laboratory. Since the publica- tion of Ko~r'shypothesis, additional

information has come to light about the

function of muscle proprioceptors. The goal of the symposium was to summarize this newer information so that it might be available for integration into thinking about the pathophysiology and treatment of somatic dysfunction. Dr. Binder led off wi* a summary of the traditional ideas about how muscle epindles and Golgi tendon organs func- tion and then focused on newer informa- tion about t h e tendon organs. On

anatomical grounds, it is clear that the

spindles are arranged parallel to the ex-

trafusal muscle fibers and are thus suited to sensing length changes of the muscle. The tendon organs, on the other hand, are located in series with the muscle fibers and are thus suited to detecting force gen- erated by the muscle fibers. Spindles have been known for some time to be sensitive to very small perturbetions in muscle length, producing a reflex activation, or s h o r t e n i n g , of t h e muscle b e i n g stretched. In contrast, tendon organs were thought to respond only to high lev- els of force and to provide protection

again& the developmentof too much force

by inhibiting the homonymous muscle (i.e., muscle of origin of the reflex). Recent work has shown this idea about tendon organ function to be unlikely.3. Each tendon organ provides a point of insertion for 3 to 25 muscle fibers.6 Ex- perimental stimulation of a single motor unit, one or more fibers of which insert on a given tendon organ, will stimulate that

organ, producing a train of spikes in Ib

afferent neurons to the spinal cord. Stim- ulation of a motor unit which hasno fibers inserting on a particular tendon organ mmetimes silencesthat tendon or'gan if it has been previously activated by sus- tained stretch of the muscle. This pre- sumably results from unloading of the tendon organ by virtue of contraction of adjacent muscle fibers. Each tendon organ appears to provide insertion for fi- bers from motor units producing a wide range of forces. Thus, each organ may sample muscle activity over the full range of force development, from the small motor units that are the first to be re- cruited to the large units that are re- cruited only during maximal con- tractions. This means that the tendon

organ input to the cord is not restricted to

conditions of high force development but

can be graded over the entire range of

muscle force. Determination of the effect of Golgi ten- don activity on neurons within the spinal cord has been difficult because it has not been possible to selectively stimulate the tendon organs or their Ib afferent fibers without at the same time stimulating the muscle spindles or their Ia sensory fibrs. Recently it has been shown that applica- tion of prolonged, high-frequency, low- amplitude vibration to muscles, which is an effective stimulus to the muscle spin- dles: can cause a transient elevation of the electrical thresholds of the Ia fibers. Under these conditions the Ib fibers can

be eelectively stimulated and their cen-

tral connections studied.8 Available evi- dence indicates that activation of the Ib sensory fibers, like the activation of cuta- neous aiTerents, can cause either excit- atory or inhibitory postsynaptic poten- tials to occur in motoneurons.s The site of integration involving the Ib input as well as inputs from other areas within the cen- tral nervous system appears not to be the motoneurons, but rather interneurons in laminae V and VI. Dr. Nichols traced the development of theories concerning the mechanical as- pects of the spindle-mediated stretch re- flex and went on to point out that most of our knowledge has been based on the ~ t u d yof single muscles. He stressed the need for extending the analysis of stretch reflexes to groups of synergistic muscles acting together upon a joint. A rather ex- treme view of the role of the stretch reflex system was proposed in 1953by Mertonlo who hypothesized that normal activation

of muscle might always be preceded by

gamma activation of the muscle spindles, and the resultant stimulation of Ia af- ferent~would in turn provide the excit- atory input to the alpha motor neurons and cause muscle contraction. This the- ory was referred to as the "follow-up length servo hypothesis." It stressed the feedback control of muscle length and the primacy of gamma activation for muscle contraction. It is now known, however, for many movements, including ballistic types and patterned activities of a re- petitive nature, simultaneous activation of both gamma and alpha motor neurons occurs, generally referred to as coactiva- tion.11 Because the larger alpha motor neurons conduct action potentials faster than the smaller gamma fibers, coactiva- tion implies that extrafusal muscle fibers must be activated before intrafusal fibers. Thus the initial phase of contraction oc- curs independently of any feedback con- tribution from the muscle spindle system. F'urthermore, it was pointed out that the Golgi tendon organs might also play an important role in feedback control, so that not only muscle length, but some

function of both force and length would be

controlled.l The latter idea was extended further by Houk>3 who suggested that the param-

eter controlled bv stretch reflex might be

stiffness, definid as the ratio o f force , change^ to^ length change. Nichols and Houkl4 demonstrated that the linearity , of the spring-like behavior of muscles in the decerebrate cat preparation was lost when the proprioceptive feedback loop was i~terrupted,i.e. when the dorsal continued on page 6001117

Sept. 1986lJournalof AOAIvol. 86lno. 9

roots were cut. In the absence of reflex

control, muscles demonstrated highly nonlinear properties which included a

brief failure, or yield, of force generation

when the active muscle was stretched. The linearization and maintenance of the spring-like properties of muscle and t h e enhancement of stiffness by the stretch receptors occurs in both the exten- mrs and flexore ofthe feline ankle, but not

equally so. Reflex action is weaker in the

flexors than in the anti-gravity extensors.

However, this inequality ie not intrinsic

to the musclea; it is a function of the or- ganization of the neural control system.

Certain brain stem lesions can alter rela-

tive reflex strength, and it has now been &own that monosynaptic reflex strength

can be changed through operant con-

ditioning.16 These experimental observa- tions emphasize the degree of control exerted by the descending influences within the central nervous system over

the refiex activity that occurs in the cord.

This comes as no surprise to clinicians

accustomed to taking advantage of the

J e n h i k maneuver to enhance reflex activity in patients.

Dr. Nichols went pn to present the re-

malts of recent studies from his laboratory

that demonstrated interactions between the flexors and extensors at the feline an- kle joint, muscles that function together at a joint and can thus be regarded as a myotatic unit. Although the extensors ex- hibit greater stretch reflex activity than

the flexom, they do not have a correepon-

dingly powerful inhibitory effect on flexor activity. Stretch of the flexors, on the other hand, produces a strong inhibitory effect on the extensors. This may relate to the greater force capability and reflex

gain of the anti-gravity exteneore in the

cat, making it necessary for these mus-

cles to be inhibited in order for their

weaker antagonists to shorten during a tiexion movement. These observations il- lustrate how the action of two muscles actitlg on the same joint is coordinated, allowing them to act together as a unit.

Such interaction undoubtedly occurs not

.only between antagoniats about a single

joint but also between synergists and be-

tween mueeles acting on different joints within the same or even different limb,

ae, for htanca, in the cmmd extensor

Alex. The final speaker ofthe symposium was

Dr. Laeb. He too emphasized the need to

consider the integrative as- of pro-

prioceptor function, reminding us that the stretch receptors are not "wholly owned subsidiaries" of the muscles in which they wide. On the contrary, their signals go many places in the central

nervous system and they are in turn in-

fluenced by signals originating in many loci. One experimental approach to these h u e s is to make measurements in intaet, conscious animals, rather than in the re: duced ~reoaratione(i.e.. aneathetized or

decerebrak that are &ful for the elu-

dication of the receptor mechanisms themsetm. One im~ortantauestionis whether or not the signals &nt to the

lbseamh

spinal cord from the muscle spindles in behaving animals correlate with length

or velocity or any other identifiable vari-

able.

Dr. Loeb described experiments carried

out in his laboratom at NIH on conscious animals carrying surgically implanted muscle length and force transducers, EMG electrodes, electrodes for recording

Ia units from a lumbar dorsal root gang-

lion, an electrode CUEaround the femoral

nerve for recording nerve activity and for irrigation of the nerve ~ l t hlocal anes- thetic from an external syringe, and elec- trodes for stimulating the saphenous nerve and t h e nerve to t h e ham- strings.1618 The results showed that no simple correlation between Ia Aring and length or velocity exists. Spindles gener- ate signals over a variety of lengths whether the muscles are shortening or

lengthening. As has been recognized for

eome time, there must be a fusimotor pro- gram causing contraction of the intra- fueal fibers in order to maintain spindle sensitivity and thus to keep information

coming in to the central nervous system

at all times.

In recent yeam it has been shown that

there are at least two identifiabletypes of

gamma innervation to the intrafusal fi- bers, a gamma dynamic system largely associated with one type of nuclear bag fiber and a gamma static system associ- ated with a different type of nuclear bag fiber and with nuclear chain fibers.19 The nuclear bag fibers under gamma dynamic control appear to be responsible for the sensitivity of the primary afferent end- ings to velocity and acceleration, whereas

the nuclear chain fibers are res6nsible

primarily for the static length sensitivity

of both primary and secondary endings.

Activity in the gamma system, both dy- namic and static, is such that afferent information from the stretch receptors continuesto flow into the central nervous system during patterned activity involv-

ing any combination of muscle shorten-

ing and lengthening. In order for this to occur, the activation patterns of the gamma fibers must be driven indepen- dently of alpha motor neurons.

The freauencv of firing of Ia afferent

from the siindltk duringvoluntary motor behavior tend to be restricted to the range of 50 to 200 pulses per second regardlean of the muscle activity occurring. The- oretical considerations20 suggest that fir- ing rates below this range do not occur because the rate of information transfer from spindleswould become limiting, i.e.,

would be too low to provide useful infor-

mation during continuing motor func-

tion. At frequencies above 200 pulses per

second, the signal to noiee ratio becomes

severely erodd, possibly because of the

existence of multiple traneduction zones within the Ia neuron innervating the in- trafusal fiber. Normally the two trans- duction zones are electrically coupled,

somewhat like the S A and A-V nodes of

the heart, so that the faster zone locks the other zone to its lurce. Under conditions of intense activati&, however, these zones

may become uncoupled so that each zone

generates signals independently,produc- ing irregular interspike intervals and a (^) I noisy signal. Thus, the job of the gamma program appears to keep the spindle ad-

justed so that the firing rate in the sen-

sory Ia fibers is kept within the appropri- ate range for optimal signaling. This / appears to occur in the cat during pre-

programmed motor patterns such as loco-

motion and even paw-shaking, but does not occur in response to single unexpected perturbations.1S

The question remains as to just what is

being sensed and regulated by the spindle system. The possibilities provided by the gamma system suggest that different pa- rameters can be regulated depending on the type of activity occurring in the gamma efferent system. In muscles whose length is being changed passively by the action of gravity or of other mus- cles, the gamma motoneurons may act alone to establish the mixture of static (length) and dynamic (velocity) influ- ences on spindle afferent sensitivity that

is appropriate for the anticipated muscle

length changes. In active muscles, sim- ilar fusimotor control may be viewed as part of the servocontrol loops involving active alpha motoneurons that reaulate length, kiffness, or other features i f mo- tor output, depending on the motor task being performed. These variations are represented schematically in Figure 1. h e r a l interesting p i n t s arose during the discussion that followed the Dresenta- tions summarized above. ~ l t d o u ~ hwe tend to focus on the well-defined pro- prioceptive sense organs in muscle, namely the spindles and the tendon organs, free nerve endings are also found in muscles. Much of their function is not

known but it is conceivable that they too

are important in proprioception, andthey mav be ~articularlvim~ortantin the re- sponse & direct tierabutic manipula- tion of muscle, perhaps acting through interneurons that carry oligosynapticre- flexes and/or establish baseline levels of alpha motoneuron polarization. The idea that altered output of the gamma system plays a role in altering the sensitivity of the myotatic reflex has not yet found s u p port experimentally. For instance, the Jendrasaik maneuver, which is employed clinically in order to enhance the stretch reflex response, is not mediated by altera- tions in gamma output.21 It appears to result from changes in the excitability of the motor neurons themeelves in a way that is not related to activity in the gamma loop. However, this observation does not appear to exclude the possibility, suggested by Korr, that gamma loop changes occur in the kind of pathologic dysfunction that is Been clinically. Given

the importance of the gamma loop output

in maintaining sensory information flow

ftom the spindlesduring muscle activity,

  • any inappropriate changes would cer- "tainly be expected to have serious patho- logic consequences. It is clear that direct

meaeurements are needed to resolve this

question.

1. Kon; lrvin M.: Roprioceptors and somatic dysfunction. JAOA 74638-50, ~ a 75 r

2. Korr, Irvin M.: Somatic dysfunction, 0s- teopathic manipulative treatment, and the nervous system. A few facts, some theories, many questions. JAOA 86:109-14, Feb 86 3. Houk, J., and Henneman, E.: Responses of Golgi tendon organs to active contractions of the soleus muscle of the cat. J Neurophysiol 30:466-a, May 67

  1. Binder, M.D.: Further evidence that the h l g i tendon organ monitors the activity of a discrete set ofmotor units within a muscle. Enp Brain Res 43:186-92, 5. Barker, D.: The morphology of muscle recep- tors. In Handbook of sensory physiology, edited by H. Autrum, et al. Vol. 3, Part 2, Muscle receptors, edited by C.C. Hunt, e t al. Springer- Verlag, New York, 1974, PP 1-
  2. Brown, M.C., Enberg, I., and Matthews, P.B.: The relative wnsitivity to vibration of muscle receptors of t h e cat. J Physiol (London) 192:773-800,Oct 67 7. Jack, J.J., and Roberts, R.C.: The role of mus- cle spindle fierents in stretch and vibration reflexes of the soleus muscle of the decerebrate cat. Brain Res 146:366-72.12 May 78
  3. Jankowska, E.: New observations on neu- ronal organization of reflexes from tendon

organ afferents and their relation to reflexes evoked from muscle spindle afferents. Prog Brain Res 50:29-36, g. Powers, R.K., and Binder, M.D.: Distribution of oligosynaptic group I input to the cat medial gastrocnemius motoneuron pool. J Neu- rophysiol 53:497-517, Feb 85

  1. Merton, P.A.: Speculations on the servo con- trol of movement. In The spinal cord, edited by J.L. Malcolm, and J.A.B. Gray. Little, Brown and Co., Boston, 1953, pp. 183-
  2. Vallbo, A.B.: Discharge patterns in human muscle spindle afferents during isometric vol- untary contractions. Acta Physiol Scand 80:552-66, Det 70
  3. Matthews, P.C.B.: The dependence of ten- sion upon extension in the stretch reflex of the soleus muscle of the decerebrate cat. J Physiol 147:521-46, Oct 59
  4. Houk, J.C.: The phylogeny of muscular con- trol configurations. In Biocybernetics, vol. 4, edited by H. Drischel, and A. Dettmar. Fischer, Jena, 1972, pp. 125-
  5. Nichols, T.R., and Houk, J.C.: Improvement in linearity and regulation of stiffness that re- sults from actions of stretch reflex. J Neu- mphysiol 39:119-42, Jan 76
  6. Wolpaw, J.R., O'Keefe, J.A., and Dowman, R.: Adaptive plasticity in the primate spinal stretch reflex (SSR). A two phase process. Soc

Research

Neumsci Abstr 10:129,

  1. Loeb, G.E., Hoffer, J.A., and Pratt, C.A.: Ac- tivity of spindle afferents from cat anterior thigh muscles. I. Identification and patterns during normal locomotion. J Neurophysiol 64:549-64, Sep 85
  2. Loeb, G.E., and Hoffer,J.A.: Activity of spin- (^)! dle afferents from cat anterior thigh muscles.
  3. Effects of fusimotor blockade. J Neu- rophysiol 54:565-77, Sep 85
  4. Loeb, G.E., Hoffer, J.A., and Marks, W.B.: Activity of spindle afferents from cat anterior thigh muscles. 111. Effects of external stimuli. J Neurophysiol 54:578-91, Sep 85
  5. Matthews, P.C.B.: Muscle spindles. Their message and their fusimotor supply. In Hand- book of physiology. Section I: The nervous sys- tem. Volume 2, Motor control, edited by Eric R. Kandel. American Physiological Society, Beth- esda, Maryland, 1977, pp. 189- 20. Loeb, G.E., andMarks, W.B.: Optimal prin- ciples for sensory transducers. International Symposium on the Muscle Spindle, edited by J.A. Boyd and M.H. Gladen. MacMillan Ltd., London, 1985, pp. 409-
  6. Burke,D., McKeon, B., and Skuse, N.E: The irrelevance of fusimotor activity to the Achilles tendon jerk of relaxed humans. Ann Neurol 10547-50. Dec 81