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Localization of muscle spindles in the human Extensor indicis muscle for biopsy purposes.

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Localization of Muscle Spindles in the Human
Extensor lndicis Muscle for Biopsy Purposes
PAUL E. VAN GORP AND WILLIAM R. KENNEDY
Department of Neurology, University o f Minnesota, Minneapolis,
Minnesota 55455
ABSTRACT
The number and spatial relations of muscle spindles in the
extensor indicis have been determined. Approximately forty spindles lie adjacent
to the motor end plate zone dispersed rather equally through this area of the
muscle with a modest increase in density among the distally originating fibers.
A study of the entire innervation pattern of this muscle has also been completed.
These findings have greatly facilitated the isolation of spindles for electron
microscopic study and attempts to perform in vivo recording from the sensory
nerves of muscle spindles in this laboratory. It is now possible, with the aid of
suitable magnification and stimulating and recording devices, to more rapidly
find muscle spindles relative to the gross innervation and the easily located motor
end plate zone.
For some time, individuals in this neuromuscular laboratory have been attempting
to record electrical potentials initiated from
the afferent nerves of human muscle spindles during diagnostic muscle biopsy. If
a consistently successful method of doing
this were achieved, it would be possible to
confirm the presence of a spindle in a strip
of muscle to be removed for subsequent
examination with the light and electron
microscope for diagnostic purposes, In addition, recording could be continued in
vitro, and such studies would provide significant physiological data regarding the
generation of afferent electrical impulses
and their role in the control of movement
and posture in this type of sensory receptor.
The main problem encountered has been
the inability to rapidly locate a spindle.
The first attempt to resolve this problem
involved mapping the dispersement of muscle spindles within the first dorsal interosseous muscle in search of areas of
greater spindle concentration (Sahinen and
Kennedy, '72). It was later decided that the
extensor indicis ( E L ) was more appropriate for our purpose. The E.I. was chosen
because it is innervated by the relatively
protected radial nerve, and it is an extrinsic hand muscle involved in delicate digital
movements, a feature which has been
found indicative of high spindle density
ANAT. REC., 179: 447-452.
(Cooper and Daniel, '63; Wittmeier and
Kennedy; Sahinen and Kennedy, '72).
Since the index finger is also extended by
the common extensor, extensor digitorum
conzmunis, the patient would suffer little
functional loss from the biopsy. Also, the
E.I. is located in an unobtrusive, yet accessible area, there being no major cutaneous nerves or vessels near the incision site.
In view of such advantages, the number
and distribution of spindles within it have
been studied.
MATERIALS AND METHODS
Four muscles to be examined for total
content and distribution of muscle spindles were taken at autopsy from newborn
infants who were without known neuromuscular disease. Infant material was
used, in light of evidence that the muscle
of neonates is already well established in
regard to location, number and innervation
of spindles (Cuajunco, '27), because it required much less time to examine than
adult muscle, and it was readily available.
During the removal of the E.I. for
study, it was noticed that the branch of
the posterior interosseous nerve innervating the muscle was quite variable in position. It was therefore decided to include
Received Aug. 14, '73. Accepted Feb. 11, '74.
447
448
PAUL E. VAN GORP AND WILLIAM R. KENNEDY
determination of the relative occurrence
rates of each type of innervation into the
study. With this intention, the position of
the two dominant nerve branches, and approximate contributions of each, were
sketched in 22 individuals at the time of
muscle biopsy or at autopsy.
After removal, the infant muscle was
fixed in an ethanol-chloral hydrate solution, then stained en. bloc according to a
silver impregnation technique devised by
de Castro (de Castro, '25) and since modified by Barker and Ip (Barker and Ip, '63).
Small pieces of stained muscle were teased
from the main bulk and squashed between
glass slides for examination. The spindle
innervation showed remarkably well using
this method, Recognition of its characteristic pattern allowed easy identification and
made possible a count of the total number
of muscle spindles in each of four muscles
quantitatively examined.
It was realized from previous recording
attempts that during biopsy a constant
means of orientation within the muscle is
essential, so that an area of muscle known
to be spindle dense can rapidly be found
in different individuals. Because the motor
end plate zone is constant in location,
easily located with an electrical stimulator, and known to be closely associated
with spindles (Kennedy, '70), the innervation pattern to the motor end plate zone
was studied in an attempt to define positional interrelationships between it and the
muscle spindles. This was accomplished
by searching additional infant muscles for
spindles in an attempt to approximate their
distribution within the muscle, relative to
the motor innervation and motor end
plates. These latter relationships were
more accurately visualized by cutting frozen sections of several muscles, then demonstrating the location of acetyl cholinesterase activity which occurs at motor end
plates of both extrafusal and intrafusal
muscle using a slight modification of well
established techniques (Coers, '53; Koelle
and Friedenwal, '59). The end plates and
spindles were then viewed in their relative
positions through a dissecting microscope.
OBSERVATIONS
The E.I. originates on the ulnar bone
and inserts in a unipennate fashion upon
a long tendon which crosses the dorsum
of the hand and attaches to the dorsal
expansion of the index finger. An incidental finding in 2 of 20 infant limbs dissected, was its insertion onto more than
one digit by means of one or more thin
accessory tendons. The E.I. is the most
distal muscle innervated by the posterior
interosseous branch of the radial nerve. In
all muscles investigated, the nerve approached the muscle by one or both of two
major patterns. The most common innervation pattern, sole means in 9 of 29 cases,
was one in which a branch of the posterior
interosseous nerve approached the muscle
directly, passing over the superficial surface of extensor pollicis longus to enter the
dorsal surface of E.I. in its most proximal portion, Less often, sole means in 6
of 29 cases, the nerve to E.I. accompanied a sensory division of the posterior
interosseous nerve toward the carpal joints.
Under these circumstances, the nerve
passed beneath the belly of extensor pollicis longus, turning sharply ulnanvard to
penetrate the most distally originating fibers of this muscle and thereby entering
the deep surface of E.I. in a more distal
site. In 14 cases both innervation patterns
were present in a single muscle (fig. 1).
In all cases, after entering the muscle
the nerves distribute motor end plates
throughout the muscle at a point midwaybetween bony origin and tendinous insertion of each muscle fiber. With the stain
for acetyl cholinesterase activity these
were seen as dark specks of precipitate
forming a band across the muscle (fig. 2).
With both the silver stain and with the
stain for acetyl cholinesterase activity the
muscle spindles were found lying parallel
to the extrafusal fibers near the motor end
plates (fig. 3). Some exceptional spindles
were found to lie nearer the origin of extrafusal muscle fibers and may be easily
confused with tendon organs if the tissue
is not well stained. In the four infant muscles examined quantitatively, 35, 37, 41,
and 45 spindles (average 40) were identified. Most of these were found to lie in
the area of concentrated spindle density,
among the motor end plates, which extends
completely across the entire muscle, increasing slightly in concentration near the
distal most end of the muscle.
LOCALIZATION OF HUMAN MUSCLE SPINDLES
ACKNOWLEDGMENTS
Special thanks to Mr. Irvin Wittmeier
for the many hours spent skillfully preparing tissue, to Mr. Frederic Sahinen for his
help in collecting it, and to Miss Koschig
and the staff of Room 88 Jackson Hall for
their help in procuring some of the material used herein.
LITERATURE ClTED
Barker, D., and M. C. Ip 1963 A silver method
for demonstrating the innervation of mammalian muscle i n teased preparations. J.
Physiol. (Lond.), 169: 73-74.
Coers, C. 1953 La detection histochimique de
la cholinesterase au niveau de l a jonction
neuro-musculaire. Rev. Belge. Path., 22: 306315.
Cooper, S., and P. M. Daniel 1963 Muscle spindles in man: their morphology in the lumbri-
449
cals and the deep muscles of the neck. Brain,
86: 563-586.
Cuajunco, F. 1927 Embryology of the neuromuscular spindles. Contra. Embryol. Carneg.
Inst., 19: 45-71.
De Castro, F. 1925 Technique pour la coloration
du system nerveux quand il est pourvu de ses
etuis ossuex. Trav. Lab. Invest. Biol. (uni.
Madr.), 23: 427446.
Kennedy, W. R. 1970 Innervation of normal human muscle spindles. Neurology (Minneap. ),
20: 463-475.
Koelle, G. B., and J. S. Friedenwal 1959 A histochemical method for localizing cholinesterase
activity. Proc. Soc. Exp. Biol., New York, 70:
617-622.
Sahinen, Frederic M., and W. R. Kennedy 1972
Distribution of muscle spindles in the human
first Dorsal Interosseous. Anat. Rec., 173: 151155.
Wittmeier, I., and W. R. Kennedy Unpublished
observation.
PLATE 1
EXPLANATION OF FIGURES
450
1
Gross innervation of E.I. in situ in the right forearm. The posterior
interosseus nerve is shown entering the E.I. by both its proximal and
its distal approaches. The distal nerve is accompanied by vessels in
this photograph. E.P.L., Extensor pollicis Zongus; E.I., Extensor indicis;
p, proximal approach; d, distal approach.
2
The motor end plate zone in a 100 micron thick section of a n infant
E.I. muscle. The muscle stained to demonstrate acetylcholinesterase.
I, the distal tendinous insertion of the muscle. 0, the origin removed
from the ulna.
3
Relationship of four muscle spindles to the motor end plate zone i n
a 100 micron thick section of a n infant E.I. stained for acetylcholinesterase. The spindles, one of which is indicated by the arrow,
show up as chains of precipitate where the gamma motor end plates
are located.
LOCALIZATION OF HUMAN MUSCLE SPINDLES
Paul E. Van Gorp and William R. Kennedy
PLATE 1
45 1
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biopsy, muscle, purpose, localization, indicis, spindle, human, extensor
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