Download Individual Extraocular Muscle Function From Faradic

Individual extraocular muscle function from
faradic stimulation of the oculomotor and
trochlear nerves of the macaque
Robert S. Jampel and Charles I. Bloomgarden*
The functions of the individual extraocular muscles of the monkey (Macaco mulatto) were
determined by faradic stimulation of the intracranial segments of the oculomotor and
trochlear nerves. The individual muscles innervated by the oculomotor nerve were isolated,
by sectioning the tendons and check ligaments of those muscles not under study. The superior
oblique muscle produced intorsion of the globe of about 25 degrees around an axis pole
located on the horizontal corneal meridian at the lateral corneal limbus. The intorsion was
associated with a depression of the pupillary axis of about 16 degrees and an abduction of
about 3.5 degrees. The components of the movement ivere not significantly influenced by the
position of the globe in the horizontal plane. The inferior rectus muscle produced two different
eye movements, depending on the stimulus parameters. With higher voltages it mooed, the
globe straight down in the midllne, adducted, and abducted, positions. With lower voltages it
produced extorsion of the globe of about 22 degrees around an axis pole located, on the
horizontal corneal meridian at the medial, corneal limbus. The extorsion of the globe was
associated with a depression of the pupillary axis of about 16 degrees and. an adduction of
about 3.5 degrees. The components of this movement were not influenced by the position of
the globe in the horizontal plane in the midline position and. in adduction. In abduction the
globe mooed toward the midline position while it underwent extorsion. The inferior oblique
and superior rectus muscles elevated the globe in all positions in the liorizontal plane, except
that, in adduction, contraction of the inferior oblique caused the eye to move to the midline
position while it elevated. The medial rectus muscle adducted, the globe to a constant end
position from any site in the horizontal and vertical planes. These findings are at variance
with traditional teachings since they indicate that the actions of the individual extraocular
muscles do not take place around the postulated axis of Fick. The axes of rotation of the individual extraocular muscles appear to vary with the position of the globe.
T.
mechanical analysis concerning the actions
of certain individual extraocular muscles,1' and by previous experiments performed in
this laboratory3 that appeared to contradict
a basic assumption upon which that method
is based. That is, that eye movements produced by individual extraocular muscles
can be deduced by assuming that the
movement is the result of forces acting to
rotate a sphere around fixed axes originating from a fixed center.4
Bender and Fulton"' ° in their investigations of the pseudo—von Graefe phenomenon had occasion to stimulate the oculomotor and trochlear nerves in primates. It
.his research was motivated by the different results obtained from traditional
From the Institute of Ophthalmology, Columbia
University, 635 W. 165th St., New York 32,
N. Y.
This experimental work was supported by the
National Institute of Neurological Diseases and
Blindness of the National Institute of Health,
U. S. Public Health Service, Research Grant
No. B-2211.
'Public Health Service Postdoctoral Fellow,
National Institute of Health, Institute of
Neurological Diseases and Blindness, Grant No.
BF 13,185. Present address: 450 Clarkson Ave.,
Brooklyn 3, N. Y.
265
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266
]ampel and Bloomgarden
occurred to one of us (R. S. J.) to employ
this approach for the study of the mode of
function of the extraocular muscles. Hence,
intracranial faradic stimulation of the
oculomotor and trochlear nerves of the
monkey was carried out. Individual muscles
were isolated in oculomotor nerve stimulation by sectioning the tendons and intermuscular septa of those muscles not under
study. This paper will report on the actions
of individual extraocular muscles obtained
by this technique, and provide experimental
evidence that the above assumption is not
correct. A later paper will report the results of simultaneous stimulation of both
nerves and the actions of various muscle
combinations.
Ineestiuatioe Oiihthalmoloey
June 1963
performed. The parameters of stimulation were
0.05 to 0.5 v., pulse duration 1 msec, and a frequency of 100 to 200 c.p.s.
The homolateral eye was prepared by placing
limbal ligatures at the 3 and 9 o'clock positions
at the limbus. The extraocular muscles were then
identified by careful dissection, and in some cases
silk sutures were placed under their insertions.
The function of individual extraocular muscles was
studied by cutting tendons of extraocular muscle
and check ligaments in various combinations from
the globe and moving the eye passively into different positions in the orbit as described below.
Small pieces of silver foil were placed on the
horizontal corneal meridian at 3 and 9 o'clock
positions at the corneal limbus to facilitate observation and motion picture analysis of the eye
movements.
Materials and methods
Observations were rruide on 10 young monkeys
(Macnca mulntta). This animal is capable of
surviving multiple neurosurgical procedures and
lias a visual system similar to that of man. Of particular interest is the similarity of the extraocular
muscles, especially the angles between the muscle
planes" of vertical muscles and the pupillary
axist (Figs. 1 and 2, Table I). The macaque
also has a range of eye movements of at least 25
degrees in all directions, which is slightly more
than half that of man.
A temporal eranioromy was performed on the
animal in a sitting position under ether anesthesia
as previously described.'1 The oculomotor and
trochlear nerves were isolated by means of a subtemporal approach. A large opening was made
in the skull over the temporal lobe, the dura was
incised and laid back, and the temporal lobe gently
retracted upward. The oculomotor and trochlear
nerves were seen over the edge of the tentorium
cerebelli in the middle cranial fossa. Monopolar
electrodes were employed. These were made of
sharp triple zero insect pins insulated to the tip.
After some practice they could be inserted into
the parenchyma of the nerves. The indifferent
electrode was a platinum bar placed in the rectum.
Two AEL stimulators (model No. 104A) were
employed for faradic stimulation, one connected
to each nerve. Individual and simultaneous stimulation of these nerves (to be reported later) was
•The muscle plane is defined ns thnt plane which pusses
through the midpoint of the origin, the midpoint of the
insertion, and the center of rotation of the eye.
(The pupillary axis is a line normal to the cornea which
passes through the center of the entrance pupil.
Fig. 1. The angle between the muscle plane of
the superior rectus and the pupillary axis in the
macaque (see Table I). The muscle plane (MP)
of the superior rectus and the pupillary axis (PA)
are identified with insect pins in a dissection of
the orbit.
Fig. 2. The angle between the muscle plane of the
superior oblique and the pupillary axis in the
macaque (see Table I). The muscle plane (MP)
of the superior oblique and the pupillary axis
(PA) are identified with insect pins in a dissection of the orbit.
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Extraocular muscle function of macaque
267
Table I. Extraocular muscles of Macaca mulatia (Anatomic data 0 )
Angle of muscle with
pupillary axis
Length of muscle
Width of insertion
Distance of insertion
from limbus
Arc of contact with globe
Thickness of muscle belly
Superior oblique
43 degrees
Superior rectus
22 degrees
25 mm.
Tendon, 12 mm.
6 mm.
9 mm.
7 mm.
1 mm.
Tendon, 0.50 mm.
Inferior ohlique
50 degrees
Inferior rectus
20 degrees
22 mm.
20. mm.
18 mm.
6.5 mm.
7.5 mm.
8.5 mm.
12 mm.
8 mm.
8.5 nun,
11 mm.
1.5 mm.
17.5 mm.
1 mm.
10 mm.
2 mm.
ages b.
Table II. Actions of the individual eye muscles of the macaque
Midline
position
Inferior ohlique
Superior obliqi<
Inferior rectus"
Intorsion of the globe
Elevation, about 18
Extorsion of the globe
around an axis whose
degrees
around an axis whose
pole is located on the
pole is located on the
horizontal corneal
horizontal corneal
meridian at the lateral meridian at the medial
corneal limbus. Extorcorneal limbus. Intorsion 22 degrees, desion 25 degrees, depression 16 degrees,
pression 16 degrees,
adduction 3.5 degrees
abduction 3.5 degrees
\ Superior rectus
Elevation,
about 18
degrees
Adduction
about 25
degrees
Intorsion of the globe
around an axis whose
pole is located on the
horizontal corneal
meridian at the lateral
corneal limbus. Intorsion 25 degrees depression 16 degrees,
abduction 3.5 degrees
Extorsion of the globe
The globe moves to the Elevation,
around an axis whose
midline position before about 18
pole is located on the
elevating 18 degrees
degrees
horizontal corneal
meridian at the medial
corneal limbus. Extorsion 22 degrees, depression 16 degrees,
adduction 3.5 degrees
Abduction
about 25
degrees *
Intorsion of the globe
around an axis whose
pole is located on the
horizontal corneal
meridian at the lateral
corneal limbus. Intorsion 25 degrees, depression 16 degrees,
abduction 3.5 degrees
The globe moves to the Elevation, about 18
midline position while
degrees
extorting, etc.
Elevation
about 18
degrees
rmiy ;ilsu act only as
Experimental results
The significant findings are illustrated
in Figs. 3 through 7 and are summarized
in Table II,
Oculomotor nerve stimulation. The usual
response was adduction of the eye, lid
elevation, and pupillary constriction.1' "•• *'
The actions of the other muscles innervated
by the oculomotor nerve were usually
masked by this response, but by shifting
the electrode to different parts of the
nerve and varying the stimulus parameters,
other responses were obtainable.3 Since it
was found that there was a slight elevation
of the globe associated with contraction
of the levator muscle when all the extraocular muscles were severed (probably because of the surface tension between the
lid and the globe), the observations below
were made with and without the lid held
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InoestiguUooO\ihlh(ilmolng{i
June 1963
268 Jampel and Bloomgarden
ACTION OF THE INFERIOR RECTUS MUSCLE
Fig. 3. Tile action of the inferior rectus muscle.
In A the eye is in the primary position, in B in
adduction, and in C in abduction. The solid line
shows the position of the limbus before stimulation. The small-dash line shows an intermediate
position and the interrupted line the end position
of the limbus produced by stimulation. The inferior rectus muscle rotates the globe eccentrically
outward (extorsion) around an axis pole located
in the horizontal conical meridian at the medial
corneal limbus. In C, from the position of abduction, the eye moves to the midline while it undergoes the movement. D is an enlarged tracing of
the movement made from motion picture frames.
The X's show the position of small pieces of
silver foil placed on the cornea to facilitate analysis. E is a schematic drawing of the movement in
the midline and adducted positions. F depicts the
movement of the eye from the abducted position
while it undergoes extension. I, lateral; LP, lid
position produced by stimulation due to the action of the levator muscle; i», medial; PP', movement of the pupillary axis; R, the axis of rotation
of the globe.
away from the globe with muscle hooks.
No difference was noted.
Medial rectus muscle. The action of this
muscle was studied by stimulation of the
intracranial segment of the oculomotor
nerve under the following conditions: (1)
With the other extraocular muscles and
check ligaments intact. The response was
the same as described under oculomotor
nerve stimulation. (2) With all the other
extraocular muscles cut. The eye adducted
to a constant end position in the horizontal
plane as in (1), regardless of the starting
position. Cutting the lateral rectus tendon
did not affect the movement, i.e., the eye
did not overshoot. (3) With the inferior
or superior rectus muscle cut. With the
superior rectus cut the eye moved down
and in, and with the inferior rectus cut,
up and in.
Inferior rectus muscle (Figs. 3 and 4).
The action of this muscle was studied by
cutting the superior rectus, medial rectus,
and inferior oblique muscles, and then
stimulating the oculomotor nerve. Two different eye movements were observed. With
higher voltages (about 0.5 v.), it moved
the globe straight down in the midline,
adducted, and abducted positions. With
lower voltages (about 0.1 v.), it produced
an extorsion of the globe around an axis
MOVEMENT OF THE PUPILLARY AXIS
SUPERIOR OBLIQUE
INFERIOR RECTUS
depressi
depression
obducti.
adduction
16°
3 5'
Fig. 4. The movement of the pupillary axis produced by contraction of the superior oblique
muscle and of the inferior rectus muscle (schematic). The components of the movements are
shown. They are not influenced by the position
of the eye in the horizontal plane. The calculations are approximate. PP', torsion of the globe
around an axis located on the horizontal meridian at the lateral limbus (superior oblique) or
medial limbus (inferior rectus); PB, abduction;
PD, adduction; BP', depression; DP', depression.
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Volume 2
Number 3
ACTION OF THE INFERIOR OBLIQUE MUSCLE
Fig. 5. The action of the inferior oblique muscle.
In A the eye is in the midline position, in B in
adduction, and in C in abduction. The solid line
shows the position of the limbus prior to stimulation. The small-dash line shows an intermediate
position and the interrupted line the end position
produced by stimulation. The inferior oblique
elevated the eye in the primary and abducted
positions. From the adducted position the eye
moves to the midline position before it elevates.
E is a schematic drawing of the elevation of the
eye from the midline position. F illustrates the
movement of the eye from adduction. G is an enlarged tracing of the movement made from motion picture frames. The X's show the position of
small pieces of silver foil placed on the cornea
to facilitate analysis. I, lateral; LP, lid positions;
vi, medial; PP', movement of pupillary axis.
\
pole located on the horizontal corneal
meridian at the medial corneal limbus
(Figs. 3 and 4). It contained three components, extorsion, depression, and adduction (Fig. 5). These components were not
influenced by moving the globe passively
into different positions in the horizontal
plane. In abduction the muscle moved the
eye to the midline position while it produced extorsion about an axis pole located
at the medial limbus.
Inferior oblique muscle (Fig. 5). The
function of this muscle was studied by
cutting the superior rectus, medial rectus,
Extraocular muscle function of macaque
269
and the inferior rectus muscles from the
globe and stimulating the oculomotor nerve.
It produced elevation in the midline position and in abduction. In abduction the
eye moved to the midline position while it
elevated.
Superior rectus (Fig- 6). The function of
this muscle was studied by cutting the
medial rectus, inferior rectus, and inferior
oblique muscles and then stimulating the
oculomotor nerve. It produced elevation
in all positions in the horizontal plane.
Trochlear nerve stimulation. This resulted in innervation of the superior oblique muscle.
Superior oblique muscle (Figs. 4 and 7).
The function of this muscle was studied by
stimulation of the trochlear nerve with the
other extraocular muscles intact and with
them severed from the globe. No difference
ACTION OF THE SUPERIOR RECTUS MUSCLE
Fig. 6. The action of the superior rectus muscle.
In A the eye is in the midline position, in B in
adduction, and in C in abduction. The solid line
shows the position of the limbus prior to stimulation and the interrupted line the position of the
eye produced by stimulation. The superior rectus
elevates the eye in the midline, abducted, and
adducted positions. D is an enlarged tracing of
the movement made from motion picture frames.
The X's show the positions of small pieces of
silver foil placed on the cornea to facilitate analysis. E is a schematic drawing of the movement.
I, lateral; LP, lid positions; PP', movement of the
pupillary axis.
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Investigative Ophthalmology
June 1963
270 Jampel and Bloomgarden
ACTION OF THE SUPERIOR OBLIQUE MUSCLE
sion of that muscle produced by oculomotor
nerve stimulation.
Discussion
Fig. 7. The action of the superior oblique muscle.
In A the eye is in the midline position, in B in
adduction, and in C in abduction. The solid line
shows the position of the limbus prior to stimulation. The small-dash line shows an intermediate
position and the interrupted line the end position
produced by stimulation. The superior oblique
rotates the globe eccentrically inward (intorsion)
around an axis pole located in the horizontal
corneal meridian at the lateral corneal limbus. D
is an enlarged tracing of the movement made from
motion picture frames. The X's show the positions
of small pieces of silver foil placed on the cornea
to facilitate analysis. £ is a schematic drawing of
the movement. I, lateral; m, medial; PP', movement of the pupillary axis; R, the axis of rotation
of the globe.
was noted in its function under these two
conditions. The muscle produced an intorsion of the globe around an axis pole
located on the horizontal corneal meridian
at the lateral corneal limbus. It contained
three components, intorsion, depression,
and abduction (Fig. 4). These components
were not significantly changed by passively moving the eye into different positions in the horizontal plane.
Check ligaments and muscle fascia.
Sectioning the check ligaments and intramuscular fascial attachments had no apparent effect on the amplitude of the
oculoratory excursions of the muscles
studied. For example, cutting the check
ligaments and fascial attachments of the
medial rectus had no effect on the excur-
The gross anatomy of the extraocular
muscles of the macaque is comparable to
that of man (Figs. 1 and 2, Table I). The
origins and insertions of the extraocular
muscles and the angles that their muscle
planes make with the pupillary axis follow
the same morphologic plan. Thus, if the
system of mechanical analysis originating
with Fick7 and Volkmann,s and employed
by many others 1 ' 2 - 9 to analyze the function of the ocular muscles in man, was
utilized in the macaque, similar results
should be expected. Also, it might be concluded that the function of the individual
vertical muscles of the macaque, as in man,
depended on the position of the eye in the
horizontal plane.
The system of mechanical analysis employed to date assumed that the two vertical recti rotate the eye around a horizontal
axis and the two oblique muscles around
an anteroposterior axis, both of which pass
through a fixed center of rotation of the
eye. Although it is well known that the concept of fixed center of rotation is artificial,10
it is believed that calculations based on
this assumption are accurate enough for
practical purposes. This experimental work
does not confirm this assumption. In the
macaque, the superior oblique and the
inferior rectus (when it acts to produce
extorsion) rotate the globe around axes
whose poles are located at the lateral and
medial limbus. These axes do not correspond to the anteroposterior axis of Fick.7
Also, it was shown experimentally that the
position of the eye in the horizontal plane
has little or no influence on the vector components of these movements. The inferior
oblique and superior rectus muscles proved
to be elevators of the globe in every position in the horizontal plane (except adduction for the inferior oblique). This suggests
that the position of the axes of rotation
varies with the position of the globe.
With the eye in abduction, it was ob-
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Volume 2
Number 3
served that the inferior rectus caused the
eye to move to the midline position while
it underwent extorsion, depression, and
adduction, and with the eye in adduction
the inferior oblique caused the eye to move
to the midline position while it elevated.
This suggests that under these conditions
the inferior rectus (when it acts to produce
extorsion) is relatively ineffective in abduction and the inferior oblique in adduction.
We are grateful to Dr. Irene Lowenfeld and
Miss Judith Feigin for technical assistance.
REFERENCES
1. Krevvson, W. E., Ill: The action of the extraocular muscles, Tr. Am. Ophth. Soc. 48:
443, 1950.
2. Boeder, F.: The cooperation of extraocular
muscles, Am. J. Ophth. 51: 469, 1961.
Extraocular muscle function of macaque
271
3. Jampel, R. S.: Extraocular muscle action
from faradic stimulation of the macaque
brain, INVEST. OPHTH. 1: 565, 1962.
4. Adler, F. H.: Physiology of the eye, clinical
application, St. Louis, 1959, The C. V. Mosby
Company, p. 319.
5. Bender, M. B., and Fulton, J. F.: Functional
recovery in ocular muscles of a chimpanzee
after section of oculomotor nerve, J. Neurophysiol. 1: 144, 1938.
6. Bender, M. B., and Fulton, J. F.: Factors in
functional recovery following section of the
oculomotor nerve in monkeys, J. Neurol. &
Psychiat. 2: 285, 1939.
7. Fick, A.: Die Bewegungen des menschlichen
Augapfels, Ztschr. f. rat. Med. 4: 101, 1854.
8. Volkmann, A. W.: Zur Mechanik der Augenmuskeln, Tr. Leipzig Soc. 21: 28, 1869.
9. Maddox, E. E.: Tests and studies of the
ocular muscles, Philadelphia, 1907, Keystone
Publishing Co.
10. Park, R. S., and Park, G. E.: The center of
ocular rotation in the horizontal plane, Am.
J. Physiol. 104: 545, 1933.
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