An Anatomic Demonstration of Afferent Fibers in the IV, V, and Vi Cranial Nerves of the Macaca...
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AN ANATOMIC DEMONSTRATION OF AFFERENT FIBERS I N T H E I V , V, A N D V I CRANIAL NERVES OF THE MACACA MULATTA* JAMES . TAREN, M.D. Ann Arbor, Michigan Since Thomsen,^^ in 1887, noted the pres- ence of peculiar patches of tissue in the roots of cranial nerves III, V I and VII, the presence of afferent proprioceptive fibers in the roots of cranial nerves III, IV and VI has been vigorously disputed. Although these fibers have been inferred on physiologic bases by Sherrington," Cooper^' = and others, and muscle spindles have been demonstrated in the human extraocular muscles by Cooper in 1949,^ complete anatomic demonstration has been lacking. That the cell bodies of the afferent fibers in cranial nerves IV and VI are in the nucleus of the mesencephalic tract of V has been proved in this laboratory by creating a lesion in the mesencephalic tract of V and observing the resulting degeneration in cra- nial nerves IV and VI. METHOD Two adult macaque animals (Macaca mulatta) were utilized in this study. Under ether anesthesia and using sterile techniques, the animal was positioned face-down and a suboccipital craniectomy was performed through a midline incision. The foramen magnum and the posterior arch of the first cervical vertebra were removed to facilitate exposure. The dura was opened in a cruci- ate manner and the vermis split, thus allow- ing exposure of the area through which some cells of the nucleus of the mesen- cephalic root of V and the root could be destroyed. A lesion was then made into this root (and its accompanying cells) to a depth of two to three mm. on the right side (fig. 1) with a right-angled knife. The in- cision was closed in layers and the animals allowed to recover. * From the Neurosurgical Research Laboratory, Section of Neurosurgery, Department of Surgery, University of Michigan Medical School. No abnormalities could be detected by repeated examinations in the postoperative period. The animals were killed at 17 days and the brains were removed and fixed in 10-percent formaldehyde. Serial sections of Marchi preparations of the brainstem were made. RESULTS Microscopic examination of the Marchi serial sections revealed degeneration that could be traced from the mesencephalic root of nerve V into ipsilateral and contralateral cranial nerves IV and ipsilateral V and VI cranial nerves (figs. 2, 3 and 4 ) . The cells of origin for the proprioceptive fibers of the trochlear nerve are believed to be situated within the nucleus of the mesen- cephalic tract of nerve V at the lateral mar- gin of the anterior medullary velum. In the anterior medullary velum each unipolar pro- prioceptive cell gives off one process (den- drite) to the decussating trochlear root, and the other process (the axon) proceeds with the trochlear fibers to the trochlear nucleus. Figure 2 demonstrates the degeneration in the decussation in both trochlear nerves that was traced from the unilateral lesion in the mesencephalic root of nerve V. The possi- bility of injury to the cranial nerves IV or to their nuclei was considered as a possible cause of this degeneration; however, the main trochlear nucleus is cephalad from the site of our lesion and, moreover, there is bilateral degeneration in the trochlear nerves. The cells of origin for the proprioceptive fibers of the trigeminal nerve also lie within the nucleus of the mesencephalic root of nerve V (fig. 3). The peripheral proc- esses (dendrites) of these cells enter with the trigeminal root but bypass the motor trigeminal nucleus on their way to the mesencephalic root of nerve V. As these proprioceptive fibers pass the motor tri- 408
Transcript of An Anatomic Demonstration of Afferent Fibers in the IV, V, and Vi Cranial Nerves of the Macaca...
A N A N A T O M I C D E M O N S T R A T I O N O F A F F E R E N T F I B E R S I N T H E I V ,
V , A N D V I C R A N I A L N E R V E S O F T H E M A C A C A M U L A T T A *
JAMES Α . TAREN, M . D . Ann Arbor, Michigan
Since Thomsen,^^ in 1887, noted the presence of peculiar patches of tissue in the roots of cranial nerves III, V I and V I I , the presence of afferent proprioceptive fibers in the roots of cranial nerves III , I V and V I has been vigorously disputed. Although these fibers have been inferred on physiologic bases by Sherrington," Cooper^' = and others, and muscle spindles have been demonstrated in the human extraocular muscles by Cooper in 1949,^ complete anatomic demonstration has been lacking.
That the cell bodies of the afferent fibers in cranial nerves I V and V I are in the nucleus of the mesencephalic tract of V has been proved in this laboratory by creating a lesion in the mesencephalic tract of V and observing the resulting degeneration in cranial nerves I V and V I .
METHOD
Two adult macaque animals (Macaca mulatta) were utilized in this study. Under ether anesthesia and using sterile techniques, the animal was positioned face-down and a suboccipital craniectomy was performed through a midline incision. The foramen magnum and the posterior arch of the first cervical vertebra were removed to facilitate exposure. The dura was opened in a cruciate manner and the vermis split, thus allowing exposure of the area through which some cells of the nucleus of the mesencephalic root of V and the root could be destroyed. A lesion was then made into this root (and its accompanying cells) to a depth of two to three mm. on the right side (fig. 1) with a right-angled knife. The incision was closed in layers and the animals allowed to recover.
* From the Neurosurgical Research Laboratory, Section of Neurosurgery, Department of Surgery, University of Michigan Medical School.
N o abnormalities could be detected by repeated examinations in the postoperative period. The animals were killed at 17 days and the brains were removed and fixed in 10-percent formaldehyde. Serial sections of Marchi preparations of the brainstem were made.
RESULTS
Microscopic examination of the Marchi serial sections revealed degeneration that could be traced from the mesencephalic root of nerve V into ipsilateral and contralateral cranial nerves I V and ipsilateral V and V I cranial nerves (figs. 2, 3 and 4 ) .
The cells of origin for the proprioceptive fibers of the trochlear nerve are believed to be situated within the nucleus of the mesencephalic tract of nerve V at the lateral margin of the anterior medullary velum. In the anterior medullary velum each unipolar proprioceptive cell gives off one process (dendrite) to the decussating trochlear root, and the other process (the axon) proceeds with the trochlear fibers to the trochlear nucleus. Figure 2 demonstrates the degeneration in the decussation in both trochlear nerves that was traced from the unilateral lesion in the mesencephalic root of nerve V . The possibility of injury to the cranial nerves I V or to their nuclei was considered as a possible cause of this degeneration; however, the main trochlear nucleus is cephalad from the site of our lesion and, moreover, there is bilateral degeneration in the trochlear nerves.
The cells of origin for the proprioceptive fibers of the trigeminal nerve also lie within the nucleus of the mesencephalic root of nerve V (fig. 3 ) . The peripheral processes (dendrites) of these cells enter with the trigeminal root but bypass the motor trigeminal nucleus on their way to the mesencephalic root of nerve V . A s these proprioceptive fibers pass the motor tri-
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A F F E R E N T FIBERS IN T H E C R A N I A L N E R V E S 409
Fig. 1 (Taren). Pliotomicrograpli of a cross section of a Marchi preparation of tlie pons of the Macaca mulatta. Magnification is approximately X9.5. (a) Lesion in the mesencephalic root of nerve V. (b) Intrapontine course of cranial nerve VII. (c) Intrapontine course of cranial nerve VI.
geminal nucleus, they give off short branches
(axons ) .
The lateral rectus muscle is known to
have proprioceptive terminations.' Figure
4A demonstrates degeneration in the ab
ducens nerve ( c ) on one side. This is in
the dendrites of the proprioceptive fibers
which can be seen also at d, bypassing the
abducens nucleus on their way to their cells
of origin in the mesencephalic nucleus of V
Fig. 2 (Taren). Photomicrographs. Cross section of Marchi preparation of the pons of the Macaca mulatta at the level of decussation of cranial nerves IV. ( A ) Magnification is approximately χ9.5. (Β) Magnification is approximately X28.S and is taken from ( A ) , (a) Degeneration in decussation of cranial nerves IV in anterior medullary velum, ( b and c) Degeneration in cranial nerves IV.
410 JAMES Α. T A R E N
Fig. 3 (Taren). Photomicrographs of cross section of Marchi preparation of pons of Macaca mulatta. ( A ) Magnified approximately X9.5. (a) Lesion in mesencephalic root of nerve V. (b) Degeneration in proprioceptive fibers en route to cells of origin in mesencephalic root of nerve V. (c) Motor nucleus of nerve V. (d) Degeneration in cranial nerve V. (B) Magnification approximately X28.S taken from ( A ) .
located in the area of the lesion at a. These
are unipolar cells and the course of the de
generated axons to the abducens nucleus
can be seen in Figure 4B at c.
Degeneration was not found in the oculo
motor nerve as the lesions were made in the
caudal portions of the mesencephalic tract
of nerve V .
DISCUSSION
Horsley/" in 1 9 1 0 , was among the earliest
dissidents inasmuch as he could find no de
generation in the extraocular nerves after
making a lesion in the mesencephalic tract
of V in the Macaca mulatta. Tozer,'"* in 1912,
shared Horsley's views based upon his own
failure to find degeneration in the mesen
cephalic tract of nerve V after section of
cranial nerves III, I V and V I , a not un
expected result. Corbin'' and Irvine and Lud-
vigh* also were unable to support the pres-
Fig 4 (Taren). Photomicrographs of cross section of a Marchi preparation of pons of Macaca mulatta. ( A ) Magnified χ9.5 approximately, (a) Lesion in mesencephalic root of nerve V. (b) Abducens nucleus, (c) Degeneration in cranial nerve VI. (d) Degeneration in proprioceptive fibers enroute to their cells of origin in the mesencephalic root of nerve V. (B) Taken from ( A ) and magnified approximately X28.5. (a) Lesion in mesencephalic root of nerve V. (b) Abducens nucleus, (c) Degeneration of axons of proprioceptive fibers joining abducens nucleus, (d) Degeneration in dendrites of proprioceptive fibers from cranial nerve V I en route to cells of origin in mesencephalic root of V.
A F F E R E N T FIBERS IN T H E C R A N I A L N E R V E S 411
ence of afferent proprioceptive fibers in the extraocular nerves.
In 1894, however, Sherrington^^ had produced evidence that the sensory fibers found in large numbers at the tendon-muscle junction in the eye muscles degenerate after section of cranial nerves III, I V and V I . He devised an interesting experiment to illustrate the important part played by sensory stimuli proceeding from the extrinsic eye muscles in judgment and appreciation of visual sensations.
If a vertical line A — Β (fig. 5) one-foot long is drawn on a wall one yard in front of the eyes, this will produce a linear image on the macula. If, now, another vertical line C—D, which lies to the side higher up than A — Β is viewed, the image of C—D will fall on the macula obliquely across the position of the image originally produced by A — B , because after viewing A — Β the eyes will rotate and turn to view C — D . A l though then the image falls across a different area of the macula, we judge both lines to be vertical. According to Sherrington, our judgment in this case must be influenced
Β Fig. S (Taren). Diagram to illustrate
Sherrington's experiment.
by sensations from the intrinsic eye muscles associated with the movements of the eyes.
Sherrington's theory of visual space perception, while of historic interest, cannot refute the evidence of Ludvigh who showed that a person in a dark room could not accurately estimate the position of a spot of light. It has been noted clinically that the movement of an eye with a paralyzed muscle
Conjugate innervation
Space representation
Perceived
Proprioception impulses
Parometric • ' , ι Cjr^ adjustment —I Muscle h g g
I froprioception Impulses
Not perceived
Fig. 6 (Taren). Diagram taken from Ludvigh to illustrate the role of proprioceptive impulses in parametric feedback.
412 J A M E S Α . T A R E N
may give rise to apparent motion of the visual field.'
While Sherrington believed that the proprioception information from the extraocular muscles was responsible for the ability of the organism to correct for false information supplied by retinal stimulation, Lud-vigh" suggests a different role for the muscle spindle discharges, that which he terms parametric feedback (fig. 6 ) . According to this theory, the afferents from the eye muscles, while supplying no fine positional information relating to the accuracy of achieving an eye movement, do provide information as to the gross difference in position of the eye and differences in tonus and muscle metabolism, all of which must be essential to the eye's ability to shift rapidly and accurately.
Further physiologic confirmation was obtained in 1953 by Cooper^ who recorded responses from the mesencephalic tract of nerve V of goats after stretching of the extraocular muscles and jaw muscles.
SUMMARY
Degeneration in the trochlear, the trigeminal and the abducens nerves has been demonstrated following a lesion in the caudal portion of the nucleus of the mesencephalic tract of V in the Macaca mulatta. Presumably these are afferent fibers with cell bodies in the nucleus of the mesencephalic tract of nerve V . In view of the physiologic evidence cited herein, it is reasonable to suppose that this afferent system is a proprioceptive or feedback mechanism whereby information pertaining to gross position and tonus is furnished to the effector cell bodies in the nuclei of the eye muscle nerves although the pathways into consciousness are not known.
University Hospital.
ACKNOWLEDGMENT
I wish to acknowledge the assistance of Parke, Davis & Company in obtaining certain materials utilized in this study.
REFERENCES
1. Alpem, M . : Physiologic characteristics of extraocular movements. In The Eye. Edited by H. Dausom, New York and London, Academic Press, v. 3, pp. 153-173.
2. Cooper, S., and Daniel, P. M . : Muscle spindles in human extrinsic eye muscles. Brain, 72:1-24 (Mar., pt. 1) 1949.
3. Cooper, S., Daniel, P. M., and Whitteridge, D.: Nerve impulses in the brainstem of the goat: Short latency responses obtained by stretching the extrinsic eye muscles and the jaw muscles. J. Physiol., 120: 471-490, 1953
4. •: Nerve impulses in the brainstem of the goat: Responses with long latencies obtained by stretching the extrinsic eye muscles. J. Physiol., 120:491-513, 1953.
5. : Muscle spindles and other sensory endings in the extrinsic eye muscles: The physiology and anatomy of these receptors and of their connections with the brainstem. Brain, 78:564-583 (pt. 4) 1955.
6. Corbin, K. R.: Observations on the peripheral distribution of fibers arising in the mesencephalic nucleus of the fifth cranial nerve. J. Comp. Neurol., 1940, pp. 173-177.
7. Crosby, E. C , Humphrey, T., and Laver, Ε. W . : Correlative Anatomy of the Nervous Systein. New York, MacMillan, 1962, pp. 238-244.
8. Irvine, S. R., and Ludvigh, E. J.: Is ocular proprioceptive sense concerned in vision? Arch. Ophth., 72:1037-1049 (June) 1936.
9. Ludvigh, E.: Possible role of proprioception in the extraocular muscles. A M A Arch. Ophth., 48:436-441, 1952.
10. May, O., and Horsley, V . : The mesencephalic root of the fifth nerve. Brain, 33 :12-203 (Oct. pt. 2) 1910.
11. Sherrington, C. S.: Physiol. Soc. Proc, June, 1894 12. : Observations on sensual role or proprioceptive nerve supply of extrinsic ocular muscles.
Brain, 41:332-343, 1918. 13. Thomsen, R.: Virchow's Arch., CIX, 1887. 14. Tozer, F. M. : On the presence of ganglion cells in the roots of III, IV, and VI crania! nerves.
Proc. Physiol. Soc. London, July 27, 1912, pp. 15-16.
