Individual extraocular muscle function from faradic stimulation of the oculomotor and trochlear nerves of the macaque

Transcription

1 Individual extraocular muscle function from faradic stimulation of the oculomotor and trochlear nerves of the macaque Robert S. Jampel and Charles I. Bloomgarden* T. 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..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 '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 mechanical analysis concerning the actions of certain individual extraocular muscles, 1 ' - and by previous experiments performed in this laboratory 3 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

2 266 ]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.

3 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 ages b. Superior oblique 43 degrees 25 mm. Tendon, 12 mm. 6 mm. 9 mm. 7 mm. 1 mm. Tendon, 0.50 mm. Superior rectus 22 degrees 22 mm. 6.5 mm. 7.5 mm. 11 mm. 1.5 mm. Inferior ohlique 50 degrees 20. mm. 8.5 mm. 12 mm mm. 1 mm. Inferior rectus 20 degrees 18 mm. 8 mm. 8.5 nun, 10 mm. 2 mm. Table II. Actions of the individual eye muscles of the macaque Midline position Adduction about 25 degrees Abduction about 25 degrees * Superior obliqi< Inferior rectus" Inferior ohlique \ Superior rectus Intorsion of the globe Extorsion of the globe Elevation, about 18 Elevation, around an axis whose around an axis whose degrees about 18 pole is located on the pole is located on the degrees horizontal corneal horizontal corneal meridian at the lateral meridian at the medial corneal limbus. Intorsion 25 degrees, desion 22 degrees, de- corneal limbus. Extorpression 16 degrees, pression 16 degrees, abduction 3.5 degrees adduction 3.5 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 around an axis whose pole is located on the horizontal corneal meridian at the medial corneal limbus. Extorsion 22 degrees, depression 16 degrees, adduction 3.5 degrees The globe moves to the Elevation, midline position before about 18 elevating 18 degrees degrees Intorsion of the globe The globe moves to the Elevation, about 18 Elevation around an axis whose midline position while degrees about 18 pole is located on the extorting, etc. degrees horizontal corneal meridian at the lateral corneal limbus. Intorsion 25 degrees, depression 16 degrees, abduction 3.5 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

4 268 Jampel and Bloomgarden InoestiguUooO\ihlh(ilmolng{i June 1963 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 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 depressi obducti. INFERIOR RECTUS depression 16 adduction 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.

5 Volume 2 Number 3 Extraocular muscle function of macaque 269 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 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. 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 \ 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, Fig. 6. The action of the superior rectus muscle. In A the eye is in the midline position, in B in 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.

6 270 Jampel and Bloomgarden Investigative Ophthalmology June 1963 ACTION OF THE SUPERIOR OBLIQUE MUSCLE Fig. 7. The action of the superior oblique muscle. In A the eye is in the midline position, in B in 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 excursion of that muscle produced by oculomotor nerve stimulation. Discussion 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 Fick 7 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-

7 Volume 2 Number 3 Extraocular muscle function of macaque 271 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, Boeder, F.: The cooperation of extraocular muscles, Am. J. Ophth. 51: 469, Jampel, R. S.: Extraocular muscle action from faradic stimulation of the macaque brain, INVEST. OPHTH. 1: 565, Adler, F. H.: Physiology of the eye, clinical application, St. Louis, 1959, The C. V. Mosby Company, p Bender, M. B., and Fulton, J. F.: Functional recovery in ocular muscles of a chimpanzee after section of oculomotor nerve, J. Neurophysiol. 1: 144, Bender, M. B., and Fulton, J. F.: Factors in functional recovery following section of the oculomotor nerve in monkeys, J. Neurol. & Psychiat. 2: 285, Fick, A.: Die Bewegungen des menschlichen Augapfels, Ztschr. f. rat. Med. 4: 101, Volkmann, A. W.: Zur Mechanik der Augenmuskeln, Tr. Leipzig Soc. 21: 28, 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.