Paper - The structure of the third, fourth, fifth, sixth, ninth, eleventh and twelfth cranial nerves (1916)
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Koch SL. The structure of the third, fourth, fifth, sixth, ninth, eleventh and twelfth cranial nerves. (1916) J Comp. Neurol. 26: 541-.
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The Structure of the Third, Fourth, Fifth, Sixth, Ninth, Eleventh and Twelfth Cranial Nerves
Sumnkil L. Koch
From the Analomical Laboratory of the Xorthivestern University Medical School
FIVE FIGURES
Introduction
FoUowmg the denioiistration of uiiinyeliiiatccl fibers in the spinal Rentes and in the vagus nerve by means of the pyridinesilver technique (Ranson, '11 and '12; Chase and Ranson '14), Professor Ranson suggested the appUcation of the same method to the study of certain of the cranial nerves, with especial reference to the presence or absence of unmyelinated fibers.
The nerves studied were the oculomotor, trochlear, trigem'nal, and abducens of the dog and of man; and the glossophaiyngeal.. accessory, and hypoglossal nerves of the dog, the cat and the rabbit. The nerves were obtained by Ufting off the skull cap and following them distally from their cerel)ral origin by chipping away the base of the skull about their foramina of exit. The di^sccted specimens were laid on glass slides and prepared by different methods. Some were stained by the p>Tidine-silver method; others were placed in 50 per cent pyridine solution for seven days, washed, and then treated with silver nitrate, water, and pyrogallic acid as in the j^yricUne-silver method; others were stained by the Pa'-Weigert method and the osmic acid method. All were cut and mounted serially.
The oculomotor, trochlear, and aixlucent nerves form a natural group formerly described as pureh' motor and consisting of large and small myelinated axons, but now recognized as containing somatic afferent as well as efferent fibers. The nerves are described as communicating with the ophthalmic division of the trigeminal nerve and with the cavernous plexus of the sympathetic system.
(l;isk(>ll ('S<)) stii(li(Hl the ci'anijil nerves with especial reference to their relation to a ty])ical spinal nerve. The oculomotor, trochlear and abducent nei'A'c^s he described as pure efferent nerves. The oculomotor was composed of large and small myelinated fibers, in the dog 14.4 to 18 micra and 3 to 5 micra in diameter. The smaller fibers passed to the ciliary ganglion, the larger to the extrinsic muscles of the eye. The trochlear nerve consisted of large myehnated fibers, 14.4 to 18 micra in diameter, supplying the external oblique muscle, and small myelinated fibers 3.6 to 5.4 micra in diameter, of unknown function. The abducens consisted of large myelinated fibers 14.4 to 18 micra in diameter, and a few smaller ones, but contained no distinct group of small fibers as did the Ilird and IVth nerves. In the roots of these nerves he saw fibrillar structures which he interpreted as the remains of ganglion cells present at an earlier stage of their development, and representing the afferent portion of the nerves.
Barratt ('98, '99, and '01) described the oculomotor nerve as composed of large and small myelinated fibers, 11 to 15 micra and 3 to 5 micra in diameter, in about the ratio of three to one. He found unmyelinated fibers also, both in the fibrous sheath and in the main trunk; in the latter situation usually at the periphery." He did not find any communication with the cavernous plexus nor with the ophthalmic division of the trigeminal nerve. The trochlear nerve was composed of large and small myelinated fibers 12 to 19 micra and 4 micra in diameter, in the ratio of three to one. There were no unmyelinated fibers present. The abducent nerve he described as composed of large and small myelinated fibers, 11 to 17 and 3 to 6 micra in diameter. A few small twigs composed of small myehnated and unmyehnated fibers joined it 25 mm. from its superficial origin, and left it again 10 mm. distalward.
Carpenter ('06) studied the development of the oculomotor and abducent nerves in the chick. He found that the oculomotor nerve was composed of myelinated axons 3 to 15 micra in diameter. The trunk was composed of comparatively large axons, with a few scattered small axons, and a zone of small axons at the periphery which passed into the ciUary ganglion. He found a ccmmunicating branch extending from the ophthalmic division of the trigem'nal nerve to the ciliary nerve, but none to the undivided oculomotor nerve. He did not speak of a direct communication between the nerves studied and the s>in pathetic system, but referred to Jegorow's suggestion that a distribution of abducent fibers to the eyeball in birds might be accounted for by sympathetic fibers joining the abducens as it passed through the cavernous sinus.
Boughton ('06) found an almost regular increase in the number and size of myehnated fibers in the oculomotor nerve of the white rat and the cat at different ages. In rats of 730 days weighing 414 grams the large fibers averaged 8 1 micni in diameter, the small 4.3 micra. In cats of 2893 grams the large fibers averaged 13.5 micra in diameter, the small 7.2 micra.
Kopsch ('07) described the oculomotor nerve in m;>n as composed of about 15,000 mostly large myeliiuited fibers grou])e(l in a number of sccondaiy bundles. In the roots between the fibers were isolated, branched, s])herical nerve cells. The trochlear nerve he described as ccmposed of about 1200 myelinated fibers, the abducens of about 2600 myeUnated fibers. All three nerves received ccn.niunicating branches from the carotid ])lexus of the sympathetic system, and from the ophthahnic nerve.
The Oculomotor, THOUIILIvVlJ AND AHOUCIIX T XI:RVIvS
Specimens of the oculomotor nerve of the dog and of three human adults were studied in serial sections. Upon dissection at least two fine branches from the sym])athetic system could be seen joining the nerve. ^Microscopically sections showed in each case clear pictures of a typical motor nerve (fig. 1) composed of large and small mj'eUna ed axons. In the human the ratio of large to small axons was about three to one; in the dog it varied between two to one and three to one. In osmic acid preparations the large myelinated fibers of the dog averaged 12 to 16 micra, the small 3 to 6 micra. Close to its peripheral origin the fibei's of the nerve were grouped in one large bundle, with incomplete septa extending toward the center of the nerve. As
The ii(M\(' ;(|)|)i'()uc.lu>{l the cavernous sinus tlio septa became ('()iu|)Iet(>, and divided it into from five to eiglit fasicles of varying .size. Nowhere along the course of the undivided nerve were unmyeUnated fibers seen within its substance. In sections of the intra-ca^'ernous portion of the nerve a few clusters of unin>elinated fibers were seen approaching it, but could not be followed into its substance. The characteristic grouping of small fibers at the periphery of the nerve, noted by Gaskell and Carpenter, could be seen most clearly in osmic acid preparations; but not all of the small fibers were grouped at the periphery, nor did they all leave the nerve to pass to the ciliary ganglion. The cellular structures in the roots of the nerves, mentioned by Gaskell and other observers, were not observed in our preparations, as even in the most proximal sections the roots had already united to form a connnon trunk.
Microscopic sections of the trochlear nerves of the dog closely resembled those of the oculomotor nerve; large and small myelinated fibers, 11 to 15 and 2 to 6 micra- in diameter, in about the ratio of three to one, with a few fibers of intermediate size. No communicating branches from the cavernous plexus or the ophthalmic nerve were seen.
The abducent nerve of the dog near the brain stem consisted of a single group of large and small myelinated fibers. 11 to 15 and 3 to 6 micra in diameter, in about the ratio of three to one. Within the cavernous sinus the ner\-e was joined by a large bundle of sympathetic fibers, the majority of which formed an intimate union with three of the six or seven fasicles which made up the nerve at this ])()int (fig. 2). More distally the main grou]) of sympathetic fibci-s left the ner\(' to ]mrsue an inde])(Mident course.
The striking cliaracteristic of these llnce ii('i\-es is their similarity in structure, botli as to the size of the fibers and the ])ro])ortion of large and small fibers. (Jaskell and Carjienter noted the presence of small fibci-s in tlie oculomotor nerve, and considered the ciliary ganglion ;is their destination, though they did not say that all the small lilxM's entered the ganglion, (laskell further noted tlie similarity in structure between the Ilird and IVth ncrNcs, but said the destination of the small fibers of the latter was as yet unkjiown. Tli(> Xltli nerve he described as ('om])()sed of large myelinated fibers '"with a few smaller ones; with no .sign of any distinct group of small fibers as in the Ilird and I\'th nerves." In our preparations all three nerves showed strikingly similai- cliaracteristics as to \\\v siz(> of the fibers and the ratio of tlie small and large fibers. The \Tth nerve could not be distinguished from the other two by a diminished number of small myelinated fibers, but was characterized by the presence of unmyelinatetl fibers from the sym])athetic system which came into inthnate contact with tlie myelinated fibers and travelled distalward with them as far as the nerve was followed. The only clue to an explanation of this fact is Jegorow's suggestion that a distribution of fibers of the Vlth nerve to the eyeball in the birds might be accounted for by the presence of sympathetic fibers which joined the nerve as it passed through the cavernous sinus. No such communications from the sympathetic system were seen in connection with the Ilird and IVth nerves. Branches of the cavernous plexus, which on gross dissection could be seen to join the Ilird nerve, on microscopic examination were seen to accompany the nerve for a short distance and again separate from it farther distalward, without entering into intimate contact with its fibers. No communication whatever between the IVth nerve and the sympathetic system was seen.
Fig. 2 Section of the abducent nerve of the dog, showing bundles of sympathetic fibers, a, Pyridine-silver. Ocu. 0, Obj. 6.
The unmyelinated fibers seen in connection with the Ilird and Vlth nerves nowhere showed the characteristic arrangement of the unmyehnated fibers seen in the spinal nerves and the vagus. In the Ilird nerve the unmyelinated fibers remained grouped in the nerve sheath and did not enter its substance. More distally they separated from the nerve completely. The unmyelinated fibers which joined the Vlth nerve and entered into intimate association with the myehnated fibers were not uniformly distributed throughout the nerv^e substance, but remained at the periphery, definitely grouped in two or three of the fasicles of the nerve. In no sections did these unmyelinated fibers from the sympathetic system appear evenly and uniformly distributed throughout the nerve substance as do tlie unmyelinated fibers in the spinal nerves and the vagus.
The Trigeminal Nerve
The intracranial portion of the trigeminal nerve of the dog and the cat, and of one human specimen was studied. Pyridinesilver sections showed large and small myelinated fibers, and in addition small munbers of unmyelinated fibers, appearing in hygest numbers in two fasicles of the sensory portion of the nerve. No sj-mpathetic fibers were seen joining the nerve within the cranium. In osmic acid preparations of the Vth nerve of the dog the large myelinated fibers measured 12 to 16 micra in diameter, the small 3 to 6 micra. In the cat the small fibers measured 4 to 7 micra, the large 12 to 16 micra, with occasional fibers 18 micra in diameter.
The Glossopharyngeal, Accessory and Hypoglossal Nerves
The glossopharyngeal nerve is usually described as a mixed nerve, and is recognized, according to Herrick's classification, as containing both general and special v'sceral efferent fibers, and general and special visceral sensory fibers, as well as somatic fibers with sensory function. The accessory and hj^Doglossal nerves are pure motor nerves, the former containing general and special visceral fibers, the latter special somatic fibers.
(Jaskcll (lescrilxMl thv small myeliiuitod fibers in the <;l()ss()pluiryngeiil nerve as 1.8 to 3.G micra in diameter, the large as not exceeding 10.8 micra. He found that large myelinated fibers were present in all the roots of the accessory nerve, but that the small fibers were confined to the bulbar and upper cervical roots. I^arratt described the IXth nerve as composed chiefly of small myelinated fibers 4 micra in diameter. Kopsch described the IXth nerve as consisting of a motor and sensory portion, and receiving sympathetic fibers from the superior cervical ganglion. He described the accessory nerve as arising in two parts, the accessorius vagi, which -joined the vagus as the ramus internus; and the accessorius spinalis, which as the ramus externus received fibers from the jugular ganglion of the vagus. Chase and Ranson found numerous unmyelinated fibers in the roots of the vagus but thought the bulbar rootlets of the accessory nerve contained few if any unmyelinated fibers. Kopsch described the hypoglossal nerve as arising hi 10 to 15 root bundles, and forming anastomoses with the vagus, the upper three cervical nerves, and the superior cervical ganghon of the sympathetic system.
Fig. 3 From a section of the accessory nerve <jf tlie clog, showing a bundle of sympathetic fibers joining the nerve. Pyridiiie-silvor. Ocu. 0, Obj. S.
Pyridine-silver sections of the roots of the glossopharyngeal nerve showed large and small myelinated fibers, and a few unmyelinated fibers. Sympathetic fibers could be followed into the trunk of the IXth nerve between its two gangha. In the trunk of the nerve the small myeUnarted fibers outnumbered the large fibers nine to one. In osmic acid preparations the large fibers measured 9 to 12 micra in diameter, the small 3 to 5 micra. Sections of a pyridiiie-silvcr preparation of the IXth nerve of the cat, just proximal to the superior ganghon, showed few large myelinated fibers 12 to 15 micra in diameter", many small myelinated fibers, 3 to 6 micra, and a few unmyelinated fibers. Sections of the IXth nerve of the rabbit showed a similar picture. No connections with the sympathetic system distal to the petrous ganglion were seen in any preparations.
Fig. Section of the accessory ncivc of the dofi. showing bundles of darkly stained uiiiiivelinated fil.ers. Pyridine-silver. Ocu. 0. Ohj. 8.
The bulbar rootlets of the accessory nerve are composed chiefly of small myelinated fibers 2 to 5 micra in diameter. The spinal portion was composed of large and small myelinated fibers in about the ratio of five to one. The majority of the large fibers were 9 to 12 micra in diameter, with a few larger fibers of 14 to 16 micra; the small fibers 2 to 5 micra. In several preparations at the point of its separation from the vagus, a few unmyelinated fibers could be seen in the ramus externus, arranged in three or four groups. Bundles of sympathetic fibers could be traced for some distance in the sheath of the Xlth nerve, finally entering it (fig. 3) and forming well marked clusters of fibers within its substance (fig. 4). In Pal-Weigert preparations the bluish-black myelin rings were separated in places by small unstained areas, corresponding closely with the location of the unmj'elinated fibers seen in pyridine-silver preparations. No essential differences were seen in the Xlth nerve of the cat and rabbit. The large myelinated fibers of the spinal root of the accessory of the cat were the largest of all the fibers measured, some of them having a diameter of 18 micra.
Fig. 5 From a section of the hypoglossal nerve of the dog, showing bundles of darkly stained unmyelinated fibers joining the nerve. Pyridine-silver. Ocu. 0, Obj. 8.
The hypoglossal nerve of the dog showed a pictm-e closely resembling that of the oculomotor nerve, large and small myelinated fibers in about the ratio of three to one, measuring 11 to 15 micra and 3 to 6 micra in diameter. No unmyelinated fibers were seen within the roots of the nerve, but slender bundles of sympathetic fibers could be followed as they approached the nerve, entered its sheath, and finally joined the nerve substance (fig. 5). The hypoglossal of the cat and rabbit showed similar pictures.
Nowhere did the umnyelinated fibers seen in sections of the Xlth and Xllth aj^jiear evenly distiibuted among the myelinatetl fibers, as in the sj)inal nerves and the vagus; but always grouped in clusters, as hi the \'Ith nerve, and in largest numbers near the periphery.
Summary
- Unmyelinated fibers are present in the Vth, Vltli. IXth, Xlth and Xllth cranial nerves. Those in che Vlth, Xlth and Xllth are probably all derived from the sympathetic system. In these nerves they have an arrangement characteristic of sym]iathetic fibers; they are grouped in clusters, and are most numerous near the periphery of the nerve.
- The oculomotor and trochlear nerves are strikingly similar in composition; they are composed of large and small myelinated fibers, without any accessions or unmyelinated fibers from the sympathetic system.
- The abducens is similar to the Ilird and R'th nerves as regards its myelinated fibers, but in addition receives a large number of unmyelinated fibers from the sympathetic system, some of which outer the nerve sheath and travel distalward with the myelinated fibers.
- The accessory and hypoglossal nerves are composed of large and small myelinated fibers, and are similar in appearance and structure to the Ilird and IVth nerves. Like the Vlth nerve, they receive considerable numbers of unmyelinated fibers from the sympathetic system which can be followed to the termination of the nerves in the muscles which they supply.
Literature Cited
Bakhatt, J. O. W. 1899 Observations on the normal anatomy of the 9th, 10th, nth, and 12th cranial nerves. Arch, of Neur. from the Path. Lab. of the London County Asylums, vol. 1, p. 537.
1899 On the anatomical structure of the 9th, 10th, 11th, and 12th cranial nerves. Brit. Med. Jour. 1899, part II, p. 837. 1901 Observations on the structure of the third, fourth, and sixth cranial nerves. Jour. Anat. and Phys., vol. 35, n. s. 15, p. 214.
BouGHTON, T. H. 1906 The increase in the number and size of the medullated fibers in the oculomotor nerve of the white rat and of the cat at different ages. Jour. Comp. Neur., vol. 16, p. 153.
CARPENTER, F. W. 1906 The development of the oculomotor nerve, the ciliary ganglion and the abducent nerve of the chick. Bull. Mus. Comp. Zool. Harv. Coll., vol. 48, no. 2.
Chase, M. R. and Ranson, S. W. 1914 The structure of the roots, trunk, and branches of the vagus nerve. Jour. Comp. Neur., vol. 24, p. 31.
Gaskell, W. H. 1889 On the relation between the structure, function, distribution and origin of the cranial nerves; together with a theory of the origin of the nervous system of vertebrates. Jour. Phys., London, vol. 10, p. 153.
KopscH, Fr. Rauber's Lehrbuch der Anatomie des Menschens, Abt 5, Leipzig.
Ranson, S. W. 1911 Non-medullated fibers in the spinal nerves. Am. Jour. Anat., vol. 12, p. 67.
1912 The structure of the spinal ganglia and of the spinal nerves. Jour. Comp. Neur., vol. 22, p. 159.
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