Detailed anatomy of the intracranial portion of the trigeminal nerve. JOSEPH G. I{USHTON~ M.D. Mayo Clinic and Mayo Foundation, Rochester, Minnesota

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1 Detailed anatomy of the intracranial portion of the trigeminal nerve KRISTIN GUDMUNDSSON~ M.D., ALBERT L. RHOTON, JR., M.D., AND JOSEPH G. I{USHTON~ M.D. Mayo Clinic and Mayo Foundation, Rochester, Minnesota Fifty trigeminal nerves were studied at autopsy under various magnifications. Two findings that could explain the preservation of sensation after rhizotomy of the main sensory root are: 1) anastomosis between the motor and sensory root in the majority of nerves, and 2) aberrant sensory rootlets that arose from the pons separately from the main sensory root in one half of the nerves. The motor root is composed of as many as 14 separately originating rootlets that usually join about 1 cm from the pons. At the pontine level, the first division fibers are usually dorsomedial and the third division fibers caudolateral within the main sensory root. However, the third division fibers may vary from being almost directly lateral to directly caudal to the first division fibers. This may explain the variability of sensory loss with partial section in the posterior fossa. KEY WOADS trigeminal nerve trigeminal neuralgia neuroanatomy trigeminal rhizotomy microsurgieal T HE purpose of this study was to examine the relationship between the motor root and each sensory division of the trigeminal nerve after dissecting the nerve free from the surrounding intracranial structure so that all aspects of the nerve could be visualized. Previous attempts to define these anatomical relationships have been on the basis of observation during therapeutic surgical procedures, 2,4,m2 and dissection in cadavers 3,s or at autopsy. 11 Although observations at operation have yielded useful information, they have been disadvantageous in that only a segment of the nerve was exposed, and this isolated segment could be viewed only at an angle limited by the exposure. The cadaver studies reported have not been completely satisfactory because often they have been concerned largely with only one segment of the nerve or have been done in a manner that has not permitted viewing the nerve at all the angles necessary to determine the interrelationship between the motor and the sensory roots. Early in this study it was noted that there may be as many as 15 nerve rootlets with separate origins from the pons in the interval between the trigeminal sensory and motor roots. This study was designed so that the intracranial portion of the nerve could be viewed from all sides, because a decision as to whether each of these rootlets contributes to the motor or the sensory function of the trigeminal nerve could be made only after visualizing all sides of the nerve. Methods Fifty nerves from 25 adults were studied at autopsy. The calvarium was opened, and the cerebral hemisphere was removed after transection of the brain stem at the level of the colliculi. The tentorium was divided 592 J. Neurosurg. / Volume 35 / November, 1971

2 Anatomy of the trigeminal nerve along its attachment to the petrous ridges and the dura over Meckel's cavity, and the ganglion was removed. After transecting each division at its exit from the skull, the brain stem and attached trigeminal nerves were removed and examined at magnifications from 6 to 40 times. Rootlets arising from the pons and eventually joining to form the motor root or the main sensory root were counted. The nerves were examined for anastomosis between the motor and sensory roots, and the location of each anastomosis was recorded. The course of the fibers from each division within the posterior root was determined. Measurements taken were: 1) the length of the sensory root from pons to ganglion, 2) the diameter of the sensory root and motor rootlets, 3) the distance from the sensory root to the largest motor rootlet, and 4) the angle that the sensory root made with the long axis of the body. Results Frequently a lobule of cerebellum projects forward and obscures the course of the posterior root through the middle cerebellar peduncle into the pons. Removal of this lobule reveals that the trigeminal nerve enters the pons about halfway between the lower and upper borders. The length of the sensory root from the pons to the gasserian ganglion varied from 18 to 26 mm, the average being 22 mm. The ganglion was divided into thirds by incisions starting distally between each division and extending posteriorly. This cleavage plane between divisions was then extended back to the pons to identify the location of the fibers from each division within the posterior root. The fibers from the third division remained ventrolateral throughout the interval from the ganglion to the pons, the first division dorsomedial, with second division fibers being in an intermediate position (Figs. 1 and 2). Immediately posterior to the ganglion, many anastomoses were observed between the fibers from each division (Fig. 3). Results of selective rhizotomy of the posterior root in human beings indicate that somatotopic localization with the third division inferolaterally and the ophthalmic division dorsomedially is well maintained posterior to, and in spite of, the prominent retrogasserian anastomosisy,3 FIG. 1. Lateral view of the left trigeminal nerve at its junction with the pons. Each division was identified at the foramen of exit from the skull, and the cleavage plane between the divisions was extended to the pons. In all dissections, the first division fibers ('~q) entered the pons in the dorsomedial portion of the root and in a location adjacent to the motor root (M). The third division (V~) fibers were caudolateral. A cross section of the sensory root between the pons and petrous apex is elliptical. The greatest diameter of the ellipse at the root's emergence from the pons is 3 to 4.5 mm and the least is 1.5 to 3 ram. In most nerves, the angle between the longest diameter of this cross section and the long axis of the body was 40 ~ to 50~ however, the angle can vary from 10 ~ to 80 ~ (Fig. 4). An angle of 80 ~ places the fibers of the third division almost directly lateral to those of the first division, but an angle of 10 ~ places the thirddivision fibers almost directly caudal to those of the first division (Table 1 ). In 26 of the 50 nerves studied, small bundles of sensory fibers arose from the pons outside the main sensory cone (Figs. 5 and 6). These aberrant or accessory sensory fibers were found in 11 nerves on the right and 15 on the left. Of the total of 66 aber- 1. Neurosurg. / Volume 35 / November,

3 K. Gudmundsson, A. L. Rhoton, Jr. and J. G. Rushton Fro. 2. Diagrams of 12 different trigeminal nerves showing the relationship of the trigeminal sensory root, motor rootlets, and aberrant sensory root at site of entry into pons. The central diagrams are for orientation and show the elliptical cross section of the sensory root. Large ovals (A through F) represent the sensory root and are oriented in the same manner as the sensory root in the central diagram. Sites of origin of the motor rootlets are black. Upper: Nerves on the right. Only five motor rootlets are present in B, but 13 are seen in F. Aberrant sensory rootlets are shown by the dark outline with clear center. None is present in D and F. In C and E some aberrant rootlets arose farther from sensory root than some of the motor rootlets. Lower: Nerves on the left. Only three motor rootlets are present in D, but 10 are in B and C. Aberrant sensory rootlets shown by dark outline with clear center. None is present in B and C. In A, D, E, and F some aberrant rootlets arose farther from the sensory root than some of the motor rootlets. Lines through oval representing main sensory root show portions from each division. In all diagrams, the rostromedial portion was from the first division, the caudolateral portion was from the third division, and the second division was in an intermediate position. In all these nerves except A in the left nerve (lower), the second division fibers comprised a greater portion of the medial than of the lateral portion of sensory root. Vascular loops course between the rootlets at the level of entry into the pons shown in all diagrams of both nerves except D in the right nerve (upper). 594 J. Neurosurg. / Volume 35 / November, 1971

4 Anatomy of the trigeminal nerve rant rootlets found, 49 went into the first division, 10 into the second division, and seven into the third division. Aberrant roots arose around the rostral two thirds of the nerve, and these usually entered the root a short distance from the brain stem. Sixty of the 66 rootlets entered the sensory root within 12 mm of the pons. The remaining six entered the distal third of the sensory root. Those arising rostral to the sensory root most frequently entered the first division; those arising more caudally entered the second or third division. No aberrant roots originated around the caudal third of the sensory root. One aberrant root was present in seven nerves, two in six nerves, three in nine nerves, and five to eight in four nerves. The motor root was composed of four to 14 filaments or rootlets each having a separate exit from the pons (Table 2, Figs. 2 and 7). The total number of motor rootlets found in the 50 brains studied was 392, or an average of about eight rootlets in each motor root. The commonest pattern was a motor root composed of seven or eight filaments. The rootlets varied from 0.1 to 1 mm in diameter. The maximal distance from the main sensory root to the largest motor rootlet varied from 0.5 to 4 ram. Fifty-four per cent of the motor rootlets arose directly rostral to the sensory root, 32% lateral to the rostral half of the sensory root, and the re- Fro. 4. The variability of the longest axis of the elliptical cross section of the trigeminal nerve at the pons (broken line) to the longitudinal axis of the body (solid line). The long axis of most nerves makes a 40 ~ to 50 ~ angle with the longitudinal axis of the body (A); however, this can vary from 10 ~ (C) to 80 ~ (B). In B, the third division (V,) is almost directly lateral to the first division (V1), and in C it is almost directly caudal. mainder were medial to the rostral half of the sensory root. Anastomosis between the motor and sensory roots was present in 47 of the 50 nerves studied (Figs. 8, 9 and 10). Eighty-nine anastomoses were counted in the 38 nerves TABLE 1 Angle between the long axis of the cross section of the trigeminal nerve at the pons and long axis of the body Size of Angle (degrees) No. of Nerves Fro. 3. Magnified view of the trigeminal ganglion and root: ganglion is to the left, the posterior trigeminal root to the right. The broken line marks the junction between the root and ganglion. Significant anastomosis (arrows) between the filaments is present immediately posterior to the ganglion ~ Total 50 J. Neurosurg. / Volume 35 / November,

5 K. Gudmundsson, A. L. Rhoton, Jr. and J. G. Rushton Fro. 5. Lateral view of the left trigeminal nerve. Nerve hook is between the large aberrant sensory rootlet and main sensory root. Aberrant rootlet arises from the pons directly lateral to the sensory root and joins the sensory root about 1 cm from the brain stem. Four motor rootlets are seen above the sensory root. having anastomoses from the sensory root proximally to the motor root distally; 66 arose in the proximal third of the nerve, 24 in the middle third, and 14 in the distal third. Ninety-five anastomoses were counted in 38 nerves having anastomoses from the motor root proximally to the sensory root distally; 27 arose in the proximal third of the nerve, 27 in the middle third, and 41 in the distal third. Discussion Horsley and associates ~ suspected that there were sensory fibers in the trigeminal motor root, and Adson 1 implied this by suggesting that the motor root be sectioned if trigeminal neuralgia recurred after complete section of the sensory root. This study suggests two explanations for the accidental preservation of sensation after posterior rhizotomy: 1) sparing the aberrant sensory fibers, and 2) sparing the anastomotic sensory fibers that run with the motor root at the level of the rhizotomy and enter the sensory root distally. Dandy 2 reported the presence of accessory fibers made up of one to 10 or 12 filaments and attributed the preservation of sensation after sensory root section to these fibers. We found a maximum of eight accessory sensory filaments. Since this large number was present in only one of 50 nerves, it seems likely that Dandy might have been counting some motor filaments. Aberrant sensory fibers usually arise closer to the main sensory root than to the motor fibers. However, some aberrant sensory fibers arise further from the main sensory root than the origin of some motor filaments, and, for this reason, it would be easy to confuse aberrant sensory fibers and motor filaments (Fig. 11). Actually, Saunders and Sachs 11 regarded the accessory fibers arising between the motor and sensory roots as mainly motor but did suggest that preservation of touch after total sensory root section at the pons suggested Neurosurg. / Volume 35 / November, 1971

6 Anatomy of the trigeminal nerve FIO. 6. Origin of the aberrant sensory rootlets in relation to the main sensory root. Large, clear oval represents a cross section of the sensory root at the level of entry into the pons. Origin of aberrant rootlets is in solid black. All nerves to the left of the solid line are from the fight side and are oriented the same as the nerves shown in Fig. 2 (upper). Those to the right of the line are from the left side and are oriented as shown in Fig. 2 (lower). Rootlet origin shown with arrow below F goes with sensory root G, and the rootlet origin shown with arrow below M goes with sensory root O. Rostral margin of root is superior and caudal margin is inferior on diagrams. No aberrant sensory root originated caudal to main sensory root. Fig. 7. Lateral view of the left trigeminal nerve at the level of entry into the pons. Seven different motor rootlets (M1-0 which joined to form the motor root have been divided and reflected to show their separate sites of entry into the pons. M1-3 are rostral to the sensory root. M,-7 are lateral. The sensory root and fibers from each division are labeled appropriately. Most motor root fibers arise near the first division (V~), but some arise in a more lateral or caudal location. the existence of an accessory sensory group. Pelletier and associates 1~ demonstrated electrophysiologically that a small number of rootlets entering the ports between the motor TABLE 2 Number of motor rootlets with separate pontine origin (50 trigeminal nerves) No. of Motor Rootlets No. of Trigeminal Nerves I 50 FIG. 8. Anastomosis between the motor and sensory roots of the trigeminal nerve. Proximal portion of the nerve adjacent to the pons is on the right. J. Neurosurg. / Volume 35 / November,

7 K. Gudmundsson, A. L. Rhoton, Jr. and J. G. Rushton Fro. 9. Sensory root below and motor rootlet above showing anastomosis between the motor and sensory compartments. One rootlet (single arrow) actually leaves the sensory root and passes around the lower motor rootlet and back (double arrows) to the sensory root. and sensory roots contained both motor and sensory elements. Aberrant sensory rootlets usually enter the sensory root within 1 cm of the pons, and for this reason they are more likely to be spared if sensory root section is carried out closer to the pons in the posterior fossa than in the middle fossa. Anastomosis is a more likely explanation for the accidental sensory Fro. 10. Right trigeminal nerve showing complex anastomosis between the motor rootlet and sensory root. preservation and recurrence of painful tic after section of the sensory root in the middle cranial fossa because anastomotic rootlets are present throughout the interval from pons to ganglion. Those sensory fibers associated with the motor root from the pons to just proximal to the ganglion where they anastomose with the sensory root would be spared with posterior FIG. 11. LeJt: Lateral view of the right trigeminal nerve near its junction with the pons. Arrow points to the intermediate group of fibers between the motor rootlet and sensory root. Right: Same tfigeminal nerve. Arrow points to intermediate fibers which proved to be a motor rootlet when traced distally. This illustrates the difficulty in telling whether an intermediate group of fibers is motor or sensory unless nerve bundles can be separated and examined individually. 598 J. Neurosurg. / Volume 35 / November, 1971

8 Anatomy of the trigeminal nerve rhizotomy in the middle or posterior fossa. We do not advocate section of the motor root at the time of initial rhizotomy for trigeminal neuralgia but we do suggest consideration of this procedure if a painful tic recurs after complete section of the sensory root. The findings that the third division fibers remain ventrolateral and that the first division fibers remain dorsomedial from the pons to the ganglion are in agreement with data from clinical and laboratory studies. 2,~,6,~~ The demonstration of many anastomoses between sensory root fibers just proximal to the ganglion suggests that topographic localization might not be present posterior to these; however, the results of nerve root section posterior to those prominent anastomoses as done by Dooley and Browder 4 do indicate that topographic localization is well maintained posterior to the anastomosis. Guillaume 6 concluded that divisional localization becomes more prominent as the ganglion is approached. Dandy, 2,12 however, found evidence of functional localization even in the posterior fossa and reported that when the nerve was incompletely sectioned by the suboccipital route, with preservation of the dorsomedial fibers, the most frequent sensory preservation was over the forehead and the least preservation was in the chin. Dandy's z'12 conclusion and our findings agree with electrophysiologic studies 1~ showing that the sensory root contains three spatially distinguishable but greatly overlapping divisions even at the root-entry zone with the ophthalmic division being dorsomedial. This finding is in agreement with the findings of Emmons and Rhoton ~ in their experimental studies of monkeys. The function of the fibers in an intermediate location between the sensory root and the larger of the motor rootlets has been the subject of considerable speculation. Our studies indicate, as did those of Saunders and Sachs, 11 that since most of these fibers join the motor root distally, the majority of them are small motor filaments, but some are sensory fibers and enter the sensory root. Jannetta and Rand 8'9 also noted the presence of accessory or intermediate fibers that leave the main sensory bundle to enter the pons between this and the motor root. In their patients, when this intermediate group of fibers was preserved, light touch was in- tact. Dandy ~,12 also reported the presence of accessory fibers made up of one to 10 or 12 filaments and attributed the preservation of sensation after sensory rhizotomy to these fibers. He stated that they were "quite commonly" but not always present. Dandy ~ stated that the accessory fibers never carried pain. Recent electrophysiologic studies 1~ did not reveal evidence to support the existence of an accessory group or so-called portio intermedius containing a single sensory modality as postulated by Dandy ~,lz and by Jannetta and Rand2 Functional modality in the latter study was found to be distributed at random within each division. Our human autopsy and animal studies ~ indicate that the accessory sensory fibers arising outside the main sensory root are largely from the first division. Those fibers exiting from the pons adjacent to the first and second divisions of the sensory root usually entered the division nearest their origin. Most arose near the first division portion of the sensory root and then joined this portion of the root, a finding in agreement with Dandy's -~ finding that when the accessory fibers are spared, sensation in the first division tends to be spared. The variability in the degree of rotation of the sensory root entering the pons may explain some of the differences in the quantity of sensation retained after partial section of the nerve in the posterior fossa. The most frequent pattern was for the third division fibers to be caudal-lateral to the first division fibers; some nerves, however, were rotated so that third division fibers were almost directly lateral to the first division and others were rotated nearly 70 ~ away from this so that the third division fibers were directly caudal to those of the first division. With the posterior fossa approach to the fifth nerve, the nerve is approached caudally and laterally. The most frequent pattern was 40 ~ to 50 ~ of rotation off the sagittal plane. In such a case, the surgeon cutting through the posterior fossa would have the third division nearest to him. Cutting through the nerve at this point would cause the most pronounced loss of sensation in the third division, and that is what Dandy 2 observed most frequently when he cut through the caudal portion of the nerve. In other cases, however, he found such a great variability in the differ- I. Nem'osurg. / Volume 35 / November,

9 K. Gudmundsson, A. L. Rhoton, Jr. and J. G. Rushton ences in both the quantity and quality of retained sensation "that one's creditability might be tested. ''12 He noted that at times all forms of sensation were totally abolished and that at other times all forms were retained and seemed approximately equal to those on the normal side. Certainly cutting into the nerve partially from a caudal-lateral direction would give a significantly different pattern of sensory loss if the nerve were rotated with the third division being lateral to the first than if the third division were almost directly caudal to the first. It is our opinion that this difference in roots explains the variability in sensory loss after partial section of the trigeminal nerve in the posterior fossa. Conclusions A macroscopic study of the fifth nerve and ganglion in autopsy cases leads us to believe that motor-to-sensory anastomoses explain the preservation of sensation subsequent to rhizotomy of the trigeminal nerve. Aberrant sensory roots were present in only 50% of the nerves studied, and they provided another explanation for sensory preservation with sensory rhizotomy. Aberrant roots contribute mainly to the first division and thus they probably do not convey a specific sensory modality from all three divisions. However, they may be nonspecific fibers separated from the root by transverse pontine fibers. In the posterior fossa, third division fibers may vary from being almost directly lateral to directly caudal to the first division fibers. This may explain the variability of sensory loss with partial section in the posterior fossa. The motor root is composed of as many as 14 separately originating rootlets. References 1. Adson AW: Unpublished data cited by Baker, G.S. Personal communication to authors, Dandy WE: An operation for the cure of tic douloureux: partial section of the sensory root at the pons. Arch Surg (Chicago) 18: , Davis L, Haven HA: Surgical anatomy of the sensory root of the trigeminal nerve. Arch Neurol Psychiat 29:1-18, Dooley DM, Browder EJ: A modification of the Tiffany operation for tic douloureux. J Neurusurg 19: , Emmons WF, Rhoton AL Jr: Functional subdivision of the trigeminal sensory root. Surg Forum 19: , Guillaume J: Cited by White JC, Sweet WH: Pain and the Neurosurgeon, A Forty Year Experience. Springfield, Ill, Charles C Thomas, 1969, p Horsley V, Taylor J, Colman WS: Remarks on the various surgical procedures devised for the relief or cure of trigeminal neuralgia (tic douloureux). Brit Med J 2: , , ; Jannetta PJ, Rand RW: Microanatomy of the trigeminal nerve. Anat Rec 154:362, 1966 (abstract) 9. Jannetta PJ, Rand RW: Transtentorial retrogasserian rhizotomy in trigeminal neuralgia, in Rand RW (ed): Microsurgery. St Louis, C V Mosby Co, 1969, pp Pelletier V, Poulos DA, Lende RA: Localization in the trigeminal root. Presented at the American Association of Neurological Surgeons, Washington, D C, Saunders R, Sachs E: Accessory fibers of the fifth nerve. Presented at the American Association of Neurological Surgeons, Cleveland, Ohio, Troland CE, Otenasek FJ: Selected Writings of Walter E. Dandy. Springfield, Ill, Charles C Thomas, 1957 Received for publication September 21, Address reprint requests to: Albert L. Rhoton, Jr., M.D., Department of Neurologic Surgery, Mayo Clinic, Rochester, Minnesota J. Neurosurg. / Volume 35 / November, 1971