Clinical and electrophysiological studies on sensory conduction mediated by the accessory rootlets of the human trigeminal nerve ADOLFO LEY, M.D., LuIs MONTSERRAT, M.D., FERNANDO BACCI, M.D., AND ADOLFO LEY, JR., M.D. Neurosurgery and Electrophysiology Services, Ciudad Sanitaria de la Seguridad Social, Universidad Autbnoma, Barcelona, Spain
u,' The authors present records of potentials evoked in the roots of the trigeminal nerve by stimulation of its cutaneous branches. Records were made during nine operations for tic douloureux in which the main sensory root of the trigeminal nerve was totally sectionedunder the microscope by the transcerebellar route. In every case, the accessory (aberrant) and motor roots were easily identified and spared. Records before and after total main sensory root divisionshowed persistence of evoked potentials in the aberrant and motor fibers. Partial preservation of sensation and blink reflex in these cases reinforced the impression that there is somatic sensory conduction through true aberrant sensory fibers running between the motor and main sensory roots. KEY W o R D s 9 t r i g e m i n a l nerve 9 sensory and motor roots 9 a c c e s s o r y fibers 9 evoked potentials 9 blink reflex 9 microsurgicai technique 9 trigeminal neuralgia
T the meeting of the Scandinavian Society of Neurological Surgeons held at Oslo in September, 1964, the senior author emphasized the importance of the findings reported by Dandy2 nearly 50 years ago concerning the existence of accessory or "aberrant" sensory fibers that leave the pons near or attached to the motor root and join the main sensory bundle at some distance from its pontine origin. Since then, Jannetta and Rand, 7 Saunders and Sachs, 18 Provost and Hardy, le Pertuiset, et al., 15 and the authors, 11'~2have been able to confirm the existence of such nerve rootlets
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by using the surgical microscope both at operation (Fig. 1) and in cadaver dissections. Gudmundsson, et al., 6 found two types of afferent accessory fibers; they identified Dandy's intermediate or "aberrant" bundles in 26 of the 50 nerves studied, and other "anastomotic" fibers from the motor to the main sensory root in 38. The sensory function attributed to these fibers is still controversial. Emmons and Rhoton, 5 studying experimental degeneration in the trigeminal system of monkeys, found that the section of fibers adjacent to the motor root produced degeneration in the 513
A. Ley, L. Montserrat, F. Bacci and A. Ley, Jr.
F~. 1. Photographs taken through surgical microscope during two suboccipital operations for trigeminal neuralgia. A -- acoustic nerve. Upper Left: The dorsal edge of the left main sensory root (arrow) is being retracted caudally with a hook to show anastomotic nerve bundles passing from the motor (M) to the sensory root. Upper Right." Retraction of the stumps (arrows) of the main sensory root exposing the small accessory rootlets and anastomotic bundles that cross from the motor to the distal stump of the severed sensory root. Lower Left: Here, in a second patient, a relatively large vein crosses between the motor (M) and accessory nerve bundles, just rostral to the right main sensory root (arrow). Lower Right: Hook passing around the sheath of the main sensory root (S) which appears distinctly separated from the rostrally placed motor nerve (M) and accessory rootlets (arrows).
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Sensory conduction by accessory nerve rootlets areas corresponding to the first and third division, that is, the ventral and dorsal portions of the main sensory and spinal nucleus. However, Pelletier's ls'14 clinical and anatomical studies in man and electrophysiological studies in apes suggested that even the smallest bundles of the motor root carried both motor and sensory impulses, the latter activated by jaw opening or stretch applied directly to the appropriate muscle group. Furthermore, all accessory fibers tested had similar functions, and none exhibited other types of sensory activity. The following study was undertaken to determine whether the sparing of sensation found after section of the main sensory root close to the pons in man could be attributed, as Dandy ~ thought, to sensory transmission along intermediate, anastomotic, and motor rootlets of impulses originating in the cutaneous area of the trigeminal nerve. Materials and Methods
Selection of Patients From a series of 33 consecutive cases of tic douloureux, we chose at random nine patients, seven women and two men, 29 to 62 years old; each had been admitted for total division of the main sensory root by the posterior approach. Surgical Procedure The following anesthesia protocol was followed: as premedication, haloperidol, atropine, and dextromoramide tartrate (Palfium); for induction, diazepam (Valium) and sodium pentothal; for relaxation, pancuronium bromide (Pavulon); for maintenance, halothane and 100% oxygen, administered with an Engstrom respirator.* Patients were placed in the sitting position. A plate measuring 1 x 0.5 cm was placed on the skin of the forehead over the supraorbital branch of the corresponding fifth nerve to be used as a cathode stimulator; a similar anode plate was placed 3 cm above it. In Cases 4 and 7, a second pair of electrodes was placed over the infraorbital branch of the maxillary division, and in Case 8, a third pair over the mental branch of the third division. In Case 9 we attempted to stimulate the three divisions using three pairs *Engstrom respirator made by L.K.B. Medical AB, Box 11075, S-161, Bromma, Sweden. J. Neurosurg. / Volume 42 / May, 1975
of hypodermically inserted stainless steel needles, 0.5 mm in diameter and 20 mm long, instead of plates. As active recording electrodes we used mostly shallow s~ainless steel hooks with rounded heads about 0.2 mm in diameter, electrically isolated by a coating that extends up to 2 to 2.5 mm from the tip. The indifferent electrode was a 1-cm long stainless steel needle inserted in the dura mater. The stimuli used were rectangular pulses of 0.2 msec duration; these were set at supramaximal intensity to obtain stimulation of all the sensory fibers of the corresponding peripheral branch of the trigeminal nerve, and thus prevenL fluctuations in the evoked potentials recorded from the nerve roots at their entrance into the pons. The stimulator was attached to a DISA electromyograph, model 14A-21, and the display was photographed by a Polaroid camera, model 14B-25.# In Cases 8 and 9, the signals were recorded using the DISA FM recorder, model 14F-60.~: The data were processed in a Digital PDP-8 analyzer and the potentials of 20 sweeps quantitated in an Intertechnique DIDAC4,000 machine.w In all cases, after surgical exposure of the fifth nerve in the cerebellopontine angle, we stimulated the supraorbital branch; in two (Cases 4 and 7) the infraorbital nerve was also stimulated, and all three divisions were stimulated in two (Cases 8 and 9). In the last two cases, infraorbital stimulation was ineffective probably because of the drapes placed by the anesthetist around the nose and mouth of the patients. ! n all but one case, the evoked potentials were first recorded from the main sensory root, and after its surgical transection, from the remaining intermediate and motor rootlets. Exceptions were Case 1, in which the root was severed by the electrode before we could start stimulation, and Case 9, in which evoked potentials were also recorded from the tiny intermediate and motor rootlets before the main root was divided. tDISA electromyograph and DISA FM recorder made by DISA Elemtronik A/S, DK2730 Herlev, Denmark. Polaroid camera made by Polaroid Corporation, Cambridge, Massachusetts. SDigital PDP-8 analyzer made by Digital Equipment Corporation, 146 Main Street, Maynard, Massachusetts 01754. w DIDAC-4,000 machine made by Intertechnique, 78370 Plaisir. France. 515
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Fl6. 2. Cases 1-7. Recordings of potentials evoked at operation by cutaneous stimulation of the supraorbital nerve (S). Potentials were recorded from the main sensory root before and from the intermediate and motor bundles after, sensory root division. In Cases 4 and 7 the infraorbital branch was also stimulated (S~). In Case 1, recording was done only after section of the main sensory root; the refractory periods (RI and R2) recorded after double stimulation indicated that the potentials obtained originated in the fifth nerve. 516
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FIG. 3. Case 8. Recordings of potentials evoked by stimulation of the supraorbital nerve (S). In A, the signal from the main sensory root has been averaged and widened by two.
FI6. 4. Case 9. Recordings of potentials evoked in various nerve fibers by stimulation of the supraorbital nerve (S). A and B are recordings from main sensory root, C from the intermediate bundles, D from the motor root, first half before and last half after root section, E from the cerebellum, F from a brain stem vein, G from acoustic nerve, H from accessory bundles, I from distal, and J from proximal stumps of the divided main sensory root. All potentials were averaged from 20 sweeps. Calibration is 1 msec/division, except for A which was 5 msec/division. The potential recorded from the distal stump (I) couldhave been generated by the damaged fibers and that from the proximal stump (J) by a shunted pickup from the accessory bundle and/or motor rootlet.
Results In all but Case 1, a monophasic negative potential was recorded from the trigeminal root after stimulation of the supraorbital branch, and in Cases 4 and 7, also after stimulation of the infraorbital nerve (Figs. 2, 3, and 4). In Cases 8 and 9, stimulation of the second division produced no response.
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Table 1 shows that the amplitude of the potentials ranged from 30 to 350 #V; the latency was relatively constant (1.6 to 2.4 msec). In nine patients, after complete division of the major part of the nerve, we stimulated and recorded the nerve potentials with electrodes placed over or around the accessory 517
A. Ley, L. Montserrat, F. Bacci and A. Ley, Jr. TABLE 1
the active electrode plates had come off the skin of the chin. In Case 8, an electrode was also placed in the ipsila[eral orbicular muscle of the eye. Prerhizotomy Postrhizotomy During the operation, the dorsal root was Nerve Case Division Amp. CT Amp CT stimulated to elicit the blink reflex. With low No. Involved (~V) (msec) ( ~ V ) (msec) voltage, no response could be recorded from the muscle; increased intensity of the stimulus 1 I --25 1.8 2 I 60 1.7 20 1.9 produced a violent massive contraction of all 3 I 30 2.4 25 2.6 the contralateral muscles, and no further 4 I 35 2.0 30 2.0 attempts to stimulate were made. II 50 2.0 --In all cases we studied the blink reflex 5 I 100 1.6 50 1.6 before and after rhizotomy? 7 Unilateral elec6 I 30 1.9 30 1.9 7 I 350 2.0 110 2.0 trical stimulation of the supraorbital nerve II 200 1.6 200 1.6 evoked an early ipsilateral reflex ( R d of m. 8 I 80 1.7 75 1.8 orbicularis oculi and a late reflex (R2) on both 9 I 100 2.0 100 2.0 sides. Before trigeminal root section, these III 70 2.2 65 2.3 two normal responses were clearly dem* Amp. = amplitude; CT = conduction time. onstrated in all but Case 3, in which R1 was missing while R~ was normal, with a 35 msec TABLE 2 latency (Table 2). After rhizotomy, they persisted with similar latencies in all but four Blink reflex before and after rhizotomy* cases: in Case 1, there was a residual facial Prerhizotomy Postrhizotomy Case paresis, and in Cases 5, 8, and 9 there was loss No. R1 R~, R1 R~ of both R~ and R~. In Case 5, the resulting anesthesia was very marked in all three 1 ll 35 --divisions. Nevertheless, we must point out 2 13 35 14 42 3 -35 -44 that the blink reflex persisted in Cases 1 and 3 4 11 45 II 50 in which there was also nearly complete 5 12 30 --anesthesia after the operation. 6 I1 32 11 38 7 11 28 11 28 Discussion 8 8 28 --9 12 32 --Although we were familiar with the so* R 1 = early reflex; R2 = late reflex. Unit of measurecalled " t r i g e m i n a l dorsal root reflex" ment is msec. ( T D R R ) studied in experimental animals by King and Meagher 9 and King and Barnett 8 and m o t o r rootlets. The latency and and later by others, 1 the only reference we characteristics of the potential did not vary, could find to electrophysiological investigabut the amplitude was clearly diminished in tion of sensory conduction in the roots of the Cases 2, 5, and 7, and remained practically trigeminal nerve in man was a short response unchanged in Cases 3, 4, 6, 8, and 9. by Crue to a question put to him in the discusIn Cases 4 and 7, the infraorbital branch sion of a paper? was also stimulated; in Case 4, the potential We are quite aware of the potential inacof 50 uV and latency of 2 msec before division curacies of our method, but emphasize that disappeared after the main root was cut. our main purpose was to relieve our patients However, in Case 7 we obtained identical from the pain of tic douloureux without addresults before and after the nerve division ing unnecessary risks to the standard (200 uV and 1.6 msec). In Case 9, in which operative procedure. Nevertheless, we feel needles were used for stimulation, evoked that the electrophysiological data collected in potentials arose only from stimulation of the this study contribute to an understanding of supraorbital and mandibular divisions; no sensory conduction in the human trigeminal response could be obtained from the infraor- nerve. bital nerve. In Case 8, stimulation of the secWe consider that the evoked potentials obond division was also ineffective, but in this tained from the main sensory root in response case at the end of the operation we found that to stimulation of the cutaneous branches of Evoked potentials in main sensory root before and after accessory and motor roots rhizotomy*
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Sensory conduction by accessory nerve rootlets the nerve are authentic and comparable to the direct or primary response of the TDRR. Their latency corresponds to a conduction speed of 50 m/sec, slightly lower than some authors' estimates, based on the polysynaptic blink reflex?T M On the other hand, we were unable to demonstrate in man the delayed or antidromic potentials of the TDRR found in different animals, even though in Cases 8 and 9 the responses were tape recorded and later processed (Fig. 4). This may have been related to the shallow hook electrodes employed or, conceivably, to the anesthesia. 3a~ We believe that the electrical records obtained from the accessory and motor bundles after complete division of the main sensory root in Cases 2, 3, 4, 6, and 7 also represented evoked potentials conducted by sensory nerve fibers lying within these nerve structures. The loss of the negative spike with preservation of only positive or approaching potential, clearly seen in Cases 5, 8, and 9 (Figs. 2, 3, and 4), probably results from the damage caused by repeated application of electrodes. We think that the response recorded from the proximal stump of the divided main sensory root in Case 9 (Fig 4 J) represented a pickup of shunted potentials generated in the spared accessory and motor rootlets entering the pons only a few millimeters away (Fig. 1 upper right).
TABLE 3
Sensory loss after microsurgical division of main sensory root of trigeminal nerve by posterior approach
Type and Distribution of Anesthesia total in 3 divisions partial in 3 divisions fractional (in 1 or 2 divisions) no sensoryloss total
No. of Cases
%
6* 15 10 1 32
18.8 46.8 31.3 3.1
* Two had had previous partial anesthesia from Frazier's operation and three from preoperative studies with electrodes. root." We believe these are the fiber bundles we spared while operating with the microscope through the posterior approach. A few clinical aspects of this study seem important. In 80% of the 32 patients who survived an operation in which we totally divided the dorsal root of the fifth nerve close to the pontine conus under the microscope, a variable amount and extent of sensation was spared over the trigeminal area (Table 3), almost twice as much trigeminal sensation was preserved as in our previously reported series of 29 patients operated on without the microscope. 11 However, the distribution of sparing was similar in both; the areas retaining most sensation were the forehead and the peripheral boundaries of the third division as reported by Pertuiset, et al. ~5 To assess the average loss of sensibility after transection, we plotted the sensory perception of pin-prick and light touch, graded from 4 to 0, into a conventional graph of 244 squares showing the cutaneous distribution of the trigeminal nerve. This study was restricted to the 19 cases in which there had been no previous phenolization of the Gasserian ganglia, root section by the transtemporal route, nor peroperative manipulation with electrodes. In the nine cases in which electrodes were used, the proportion showing complete anesthesia (33%) had been more than twice as great as that found in the remaining 23 cases (Table 3) probably because of trauma to the nerve bundles. The results of the 19 cases were processed in a Digital laboratory 8/e computer* and the resulting averages presented
The ability to produce blink reflex following section of the main sensory root in most cases (Table 2) affords additional evidence of the existence of sensory fibers in the accessory and motor branches. If we were to assume that afferent conduction in the trigeminal system is restricted to proprioceptive impulses from muscles of mastication, as asserted by Pelletier, et al.? 4 it would be difficult to explain why the supraorbital electrode could stimulate these muscles; this would lead to the alternative hypothesis that proprioceptive fibers arise from spindles of facial muscles that as far as we know have not yet been demonstrated in man. However, in their latest paper, Pelletier, et al.? s refer to " . . . occasional splinters of fibers from the sensory root which were seen entering the pons separately at the root entry zone," and later they seem to agree with the *Digital laboratory 8/3 computer made by finding by Gudmundsson, et al., 6 of " . . . Digital Equipment Corporation, 146 Main Street, bundles that were clearly part of the sensory Maynard, Massachusetts 01754. J. Neurosurg. / Volume 42 / May, 1975
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F. B a c c i a n d A. L e y , J r .
Fro. 5. Graphic representation of the computerized average loss of sensibility in 19 patients after operation. Grading of sensation is from 4 (normal) to 0 (anesthesia). See also cover illustration. graphically in Fig. 5. (See cover illustration, also.) The mean values for each of the accepted cutaneous areas of distribution of the three main branches of the trigeminal nerve were 2.4 for the ophthalmic, 1.6 for the maxillary, and 1.8 for the mandibular branch. We should like to emphasize that with the posterior approach the surgeon can always be certain of the boundaries of the main sensory root, thus making an unintentional partial section very unlikely? ,x9 This would even be true in the presence of vascular or other abnormalities, because the component fiber bundles are bounded by a well-defined common pia-arachnoidal covering (Fig. 1 lower right). A second clinical deduction is that there seems to be a definite correlation between the pattern of sensory sparing and the relatively somatotopic arrangement of the motor and accessory rootlets around the main sensory division? ,6 This seems to confirm the findings of Emmons and Rhoton, who in their degeneration experiments in apes found that after section of the rostral fibers adjacent to 520
the motor root, the degeneration was more intense in those regions shown by selective rhizotomy to come from the ophthalmic division. And after section of the caudal fibers adjacent to the brain stem, degeneration was more extensive in those regions that came from the mandibular division. Unfortunately, we were not aware of this study until recently, and so did not make precise references on that matter in the operation records. However, it was obvious that, in accordance with the findings of Gudmundsson, et al., 6 in most of our cases the accessory and anastomotic rootlets were found near the rostral portion of the main root, the region where the fibers from the first division are located. This may also explain why the blink reflexes were usually preserved. Finally, it is important to realize that the term "selective rhizotomy of the trigeminal nerve" merely means section of some particular root. It does not mean that any particular type of sensibility has been spared because, contrary to what was assumed by early investigators, modern research has J. Neurosurg. / Volume 42 / May, 1975
Sensory conduction by accessory nerve rootlets repeatedly demonstrated that within the trigeminal nerve roots there is no specific location for each sensory modality2 ,e Nevertheless, as in most areas of the body, sharp pin-prick and light touch are the first and most seriously impaired senses following nerve injuries of any sort. All of these findings prove how appropriate was Dandy's choice of the term "aberrant" to designate these rootlets.
10.
Acknowledgments
12.
We should like to thank our anesthetist Antonio Castells, M.D.; Maria C. Lizuain, Ph.D., for her invaluable assistance in processing and computerizing the electrophysiological data and the sensory findings; and Rafael Papi, M.D., Chief of the Service of Electrophysiology, for all the facilities and assistance given to us.
References 1. Alvarez-Carregal E, Crue BL Jr, Todd EM: Further observations of trigeminal antidromic potentials. Possible physiological function of sensory antidromic potentials. J Neurosurg 20:277-288, 1963 2. Dandy WE: An operation for the cure of tic douloureux: partial section of the sensory root at the pons. Arch Surg 18:687-734, 1929 3. Darian-Smith I: The neural coding of "tactile" stimulus parameters in different trigeminal nuclei, in Hassler R, Walker AE (eds): Trigeminal Neuralgia. Stuttgart, Georg Thieme Verlag, 1970 4. Davis L, Haven HA: Surgical anatomy of the sensory root of the trigeminal nerve. Arch Neurol Psychiatry 29:1-18, 1933 5. Emmons WF, Rhoton AL Jr: Subdivision of the trigeminal sensory root. Experimental study in the monkey. J Neurosurg 35:585-591, 1971 6. Gudmundsson K, Rhoton AL Jr, Rushton JG: Detailed anatomy of intracranial portion of the trigeminal nerve. J Neurosurg 35: 592-600, 1971 7. Jannetta P J, Rand RW: Transtentorial retrogasserian rhizotomy in trigeminal neuralgia by microneurosurgical technique. Bull Los Angeles Neural Sac 31:93-99, 1966 8. King RB, Barnett JC: Studies of trigeminal nerve potentials: overreaction to tactile facial
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9.
11.
13. 14.
15.
16. 17. 18.
19. 20.
stimulation in acute laboratory preparations. J Neurosurg 14:617-627, 1957 King RB, Meagher JN: Studies of trigeminal nerve potentials. J Neurasurg 12:393-402, 1955 King RB, Meagher JN, Barnett JC: Studies of trigeminal nerve potentials in normal compared to abnormal experimental preparations. J Neurasarg 13:176-183, 1956 Ley A, Guitart JM: Clinical observations on sensory effects of trigeminal dorsal root section. J Neural Neurosurg Psychiatry 34:260-264, 1971 Ley A, Guitart JM, Bacci F: Microsurgical procedure for the selective neurotomy of the Vth nerve root by the suboccipital approach, in Purkyn~ JE (ed): Abstracts Fourth European Congress of Neurosurgery. Prague, Avicenum Czechoslovak Medical Press, 1971, abstract No. 155 Pelletier VA, Poulos DA, Lende RA: Functional localization in the trigeminal root. J Neurasurg 40:504-513, 1974 Pelletier V, Poulos DA, Lende RA: Localization in the trigeminal root. Presented at the Annual Meeting of American Association of Neurological Surgeons, Washington DC, 1970 Pertuiset B, Philippon J, Fohanno D, et al: Traitement microchirurgical de la nevralgie faciale essentielle par neurotomie r6trogass6rienne s61ective transtentorielle. Rev Neural (Paris) 126:97-106, 1972 Provost J, Hardy J: Microchirurgie du trijumeau: anatomie fonctionelle. Neurachirurgie 16:459-470, 1970 Rushworth G: Observations on blink reflexes. J Neurol Neurosarg Psychiatry 25:93-109, 1962 Saunders RL, Sachs E Jr: Relation of the accessory rootlets of the trigeminal nerve to its motor root. A microsurgical autopsy study. J Neurosurg 33:317-324, 1970 Stookey B, Ransohoff J: Trigeminai Neuralgia, Its History and Treatment. Springfield, I11, Charles C Thomas, 1959 Struppler A, Dobbelstein H: Elektromyographische Untersuchung des Glabellareflexes bei verschiedenen neurologischen StSrungen. Nervenartz 34:347-352, 1963
Address reprint requests to: Adolfo Ley, M.D., Services of Neurosurgery and Electrophysiology, Ciudad Sanitaria de la Seguridad Social, Universidad Aut6noma, Barcelona, Spain.
521
u,' The authors present records of potentials evoked in the roots of the trigeminal nerve by stimulation of its cutaneous branches. Records were made during nine operations for tic douloureux in which the main sensory root of the trigeminal nerve was totally sectionedunder the microscope by the transcerebellar route. In every case, the accessory (aberrant) and motor roots were easily identified and spared. Records before and after total main sensory root divisionshowed persistence of evoked potentials in the aberrant and motor fibers. Partial preservation of sensation and blink reflex in these cases reinforced the impression that there is somatic sensory conduction through true aberrant sensory fibers running between the motor and main sensory roots. KEY W o R D s 9 t r i g e m i n a l nerve 9 sensory and motor roots 9 a c c e s s o r y fibers 9 evoked potentials 9 blink reflex 9 microsurgicai technique 9 trigeminal neuralgia
T the meeting of the Scandinavian Society of Neurological Surgeons held at Oslo in September, 1964, the senior author emphasized the importance of the findings reported by Dandy2 nearly 50 years ago concerning the existence of accessory or "aberrant" sensory fibers that leave the pons near or attached to the motor root and join the main sensory bundle at some distance from its pontine origin. Since then, Jannetta and Rand, 7 Saunders and Sachs, 18 Provost and Hardy, le Pertuiset, et al., 15 and the authors, 11'~2have been able to confirm the existence of such nerve rootlets
A
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by using the surgical microscope both at operation (Fig. 1) and in cadaver dissections. Gudmundsson, et al., 6 found two types of afferent accessory fibers; they identified Dandy's intermediate or "aberrant" bundles in 26 of the 50 nerves studied, and other "anastomotic" fibers from the motor to the main sensory root in 38. The sensory function attributed to these fibers is still controversial. Emmons and Rhoton, 5 studying experimental degeneration in the trigeminal system of monkeys, found that the section of fibers adjacent to the motor root produced degeneration in the 513
A. Ley, L. Montserrat, F. Bacci and A. Ley, Jr.
F~. 1. Photographs taken through surgical microscope during two suboccipital operations for trigeminal neuralgia. A -- acoustic nerve. Upper Left: The dorsal edge of the left main sensory root (arrow) is being retracted caudally with a hook to show anastomotic nerve bundles passing from the motor (M) to the sensory root. Upper Right." Retraction of the stumps (arrows) of the main sensory root exposing the small accessory rootlets and anastomotic bundles that cross from the motor to the distal stump of the severed sensory root. Lower Left: Here, in a second patient, a relatively large vein crosses between the motor (M) and accessory nerve bundles, just rostral to the right main sensory root (arrow). Lower Right: Hook passing around the sheath of the main sensory root (S) which appears distinctly separated from the rostrally placed motor nerve (M) and accessory rootlets (arrows).
514
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Sensory conduction by accessory nerve rootlets areas corresponding to the first and third division, that is, the ventral and dorsal portions of the main sensory and spinal nucleus. However, Pelletier's ls'14 clinical and anatomical studies in man and electrophysiological studies in apes suggested that even the smallest bundles of the motor root carried both motor and sensory impulses, the latter activated by jaw opening or stretch applied directly to the appropriate muscle group. Furthermore, all accessory fibers tested had similar functions, and none exhibited other types of sensory activity. The following study was undertaken to determine whether the sparing of sensation found after section of the main sensory root close to the pons in man could be attributed, as Dandy ~ thought, to sensory transmission along intermediate, anastomotic, and motor rootlets of impulses originating in the cutaneous area of the trigeminal nerve. Materials and Methods
Selection of Patients From a series of 33 consecutive cases of tic douloureux, we chose at random nine patients, seven women and two men, 29 to 62 years old; each had been admitted for total division of the main sensory root by the posterior approach. Surgical Procedure The following anesthesia protocol was followed: as premedication, haloperidol, atropine, and dextromoramide tartrate (Palfium); for induction, diazepam (Valium) and sodium pentothal; for relaxation, pancuronium bromide (Pavulon); for maintenance, halothane and 100% oxygen, administered with an Engstrom respirator.* Patients were placed in the sitting position. A plate measuring 1 x 0.5 cm was placed on the skin of the forehead over the supraorbital branch of the corresponding fifth nerve to be used as a cathode stimulator; a similar anode plate was placed 3 cm above it. In Cases 4 and 7, a second pair of electrodes was placed over the infraorbital branch of the maxillary division, and in Case 8, a third pair over the mental branch of the third division. In Case 9 we attempted to stimulate the three divisions using three pairs *Engstrom respirator made by L.K.B. Medical AB, Box 11075, S-161, Bromma, Sweden. J. Neurosurg. / Volume 42 / May, 1975
of hypodermically inserted stainless steel needles, 0.5 mm in diameter and 20 mm long, instead of plates. As active recording electrodes we used mostly shallow s~ainless steel hooks with rounded heads about 0.2 mm in diameter, electrically isolated by a coating that extends up to 2 to 2.5 mm from the tip. The indifferent electrode was a 1-cm long stainless steel needle inserted in the dura mater. The stimuli used were rectangular pulses of 0.2 msec duration; these were set at supramaximal intensity to obtain stimulation of all the sensory fibers of the corresponding peripheral branch of the trigeminal nerve, and thus prevenL fluctuations in the evoked potentials recorded from the nerve roots at their entrance into the pons. The stimulator was attached to a DISA electromyograph, model 14A-21, and the display was photographed by a Polaroid camera, model 14B-25.# In Cases 8 and 9, the signals were recorded using the DISA FM recorder, model 14F-60.~: The data were processed in a Digital PDP-8 analyzer and the potentials of 20 sweeps quantitated in an Intertechnique DIDAC4,000 machine.w In all cases, after surgical exposure of the fifth nerve in the cerebellopontine angle, we stimulated the supraorbital branch; in two (Cases 4 and 7) the infraorbital nerve was also stimulated, and all three divisions were stimulated in two (Cases 8 and 9). In the last two cases, infraorbital stimulation was ineffective probably because of the drapes placed by the anesthetist around the nose and mouth of the patients. ! n all but one case, the evoked potentials were first recorded from the main sensory root, and after its surgical transection, from the remaining intermediate and motor rootlets. Exceptions were Case 1, in which the root was severed by the electrode before we could start stimulation, and Case 9, in which evoked potentials were also recorded from the tiny intermediate and motor rootlets before the main root was divided. tDISA electromyograph and DISA FM recorder made by DISA Elemtronik A/S, DK2730 Herlev, Denmark. Polaroid camera made by Polaroid Corporation, Cambridge, Massachusetts. SDigital PDP-8 analyzer made by Digital Equipment Corporation, 146 Main Street, Maynard, Massachusetts 01754. w DIDAC-4,000 machine made by Intertechnique, 78370 Plaisir. France. 515
A. Ley, L. Montserrat, F. Bacci and A. Ley, Jr.
Fl6. 2. Cases 1-7. Recordings of potentials evoked at operation by cutaneous stimulation of the supraorbital nerve (S). Potentials were recorded from the main sensory root before and from the intermediate and motor bundles after, sensory root division. In Cases 4 and 7 the infraorbital branch was also stimulated (S~). In Case 1, recording was done only after section of the main sensory root; the refractory periods (RI and R2) recorded after double stimulation indicated that the potentials obtained originated in the fifth nerve. 516
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Sensory conduction by accessory nerve rootlets
FIG. 3. Case 8. Recordings of potentials evoked by stimulation of the supraorbital nerve (S). In A, the signal from the main sensory root has been averaged and widened by two.
FI6. 4. Case 9. Recordings of potentials evoked in various nerve fibers by stimulation of the supraorbital nerve (S). A and B are recordings from main sensory root, C from the intermediate bundles, D from the motor root, first half before and last half after root section, E from the cerebellum, F from a brain stem vein, G from acoustic nerve, H from accessory bundles, I from distal, and J from proximal stumps of the divided main sensory root. All potentials were averaged from 20 sweeps. Calibration is 1 msec/division, except for A which was 5 msec/division. The potential recorded from the distal stump (I) couldhave been generated by the damaged fibers and that from the proximal stump (J) by a shunted pickup from the accessory bundle and/or motor rootlet.
Results In all but Case 1, a monophasic negative potential was recorded from the trigeminal root after stimulation of the supraorbital branch, and in Cases 4 and 7, also after stimulation of the infraorbital nerve (Figs. 2, 3, and 4). In Cases 8 and 9, stimulation of the second division produced no response.
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Table 1 shows that the amplitude of the potentials ranged from 30 to 350 #V; the latency was relatively constant (1.6 to 2.4 msec). In nine patients, after complete division of the major part of the nerve, we stimulated and recorded the nerve potentials with electrodes placed over or around the accessory 517
A. Ley, L. Montserrat, F. Bacci and A. Ley, Jr. TABLE 1
the active electrode plates had come off the skin of the chin. In Case 8, an electrode was also placed in the ipsila[eral orbicular muscle of the eye. Prerhizotomy Postrhizotomy During the operation, the dorsal root was Nerve Case Division Amp. CT Amp CT stimulated to elicit the blink reflex. With low No. Involved (~V) (msec) ( ~ V ) (msec) voltage, no response could be recorded from the muscle; increased intensity of the stimulus 1 I --25 1.8 2 I 60 1.7 20 1.9 produced a violent massive contraction of all 3 I 30 2.4 25 2.6 the contralateral muscles, and no further 4 I 35 2.0 30 2.0 attempts to stimulate were made. II 50 2.0 --In all cases we studied the blink reflex 5 I 100 1.6 50 1.6 before and after rhizotomy? 7 Unilateral elec6 I 30 1.9 30 1.9 7 I 350 2.0 110 2.0 trical stimulation of the supraorbital nerve II 200 1.6 200 1.6 evoked an early ipsilateral reflex ( R d of m. 8 I 80 1.7 75 1.8 orbicularis oculi and a late reflex (R2) on both 9 I 100 2.0 100 2.0 sides. Before trigeminal root section, these III 70 2.2 65 2.3 two normal responses were clearly dem* Amp. = amplitude; CT = conduction time. onstrated in all but Case 3, in which R1 was missing while R~ was normal, with a 35 msec TABLE 2 latency (Table 2). After rhizotomy, they persisted with similar latencies in all but four Blink reflex before and after rhizotomy* cases: in Case 1, there was a residual facial Prerhizotomy Postrhizotomy Case paresis, and in Cases 5, 8, and 9 there was loss No. R1 R~, R1 R~ of both R~ and R~. In Case 5, the resulting anesthesia was very marked in all three 1 ll 35 --divisions. Nevertheless, we must point out 2 13 35 14 42 3 -35 -44 that the blink reflex persisted in Cases 1 and 3 4 11 45 II 50 in which there was also nearly complete 5 12 30 --anesthesia after the operation. 6 I1 32 11 38 7 11 28 11 28 Discussion 8 8 28 --9 12 32 --Although we were familiar with the so* R 1 = early reflex; R2 = late reflex. Unit of measurecalled " t r i g e m i n a l dorsal root reflex" ment is msec. ( T D R R ) studied in experimental animals by King and Meagher 9 and King and Barnett 8 and m o t o r rootlets. The latency and and later by others, 1 the only reference we characteristics of the potential did not vary, could find to electrophysiological investigabut the amplitude was clearly diminished in tion of sensory conduction in the roots of the Cases 2, 5, and 7, and remained practically trigeminal nerve in man was a short response unchanged in Cases 3, 4, 6, 8, and 9. by Crue to a question put to him in the discusIn Cases 4 and 7, the infraorbital branch sion of a paper? was also stimulated; in Case 4, the potential We are quite aware of the potential inacof 50 uV and latency of 2 msec before division curacies of our method, but emphasize that disappeared after the main root was cut. our main purpose was to relieve our patients However, in Case 7 we obtained identical from the pain of tic douloureux without addresults before and after the nerve division ing unnecessary risks to the standard (200 uV and 1.6 msec). In Case 9, in which operative procedure. Nevertheless, we feel needles were used for stimulation, evoked that the electrophysiological data collected in potentials arose only from stimulation of the this study contribute to an understanding of supraorbital and mandibular divisions; no sensory conduction in the human trigeminal response could be obtained from the infraor- nerve. bital nerve. In Case 8, stimulation of the secWe consider that the evoked potentials obond division was also ineffective, but in this tained from the main sensory root in response case at the end of the operation we found that to stimulation of the cutaneous branches of Evoked potentials in main sensory root before and after accessory and motor roots rhizotomy*
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Sensory conduction by accessory nerve rootlets the nerve are authentic and comparable to the direct or primary response of the TDRR. Their latency corresponds to a conduction speed of 50 m/sec, slightly lower than some authors' estimates, based on the polysynaptic blink reflex?T M On the other hand, we were unable to demonstrate in man the delayed or antidromic potentials of the TDRR found in different animals, even though in Cases 8 and 9 the responses were tape recorded and later processed (Fig. 4). This may have been related to the shallow hook electrodes employed or, conceivably, to the anesthesia. 3a~ We believe that the electrical records obtained from the accessory and motor bundles after complete division of the main sensory root in Cases 2, 3, 4, 6, and 7 also represented evoked potentials conducted by sensory nerve fibers lying within these nerve structures. The loss of the negative spike with preservation of only positive or approaching potential, clearly seen in Cases 5, 8, and 9 (Figs. 2, 3, and 4), probably results from the damage caused by repeated application of electrodes. We think that the response recorded from the proximal stump of the divided main sensory root in Case 9 (Fig 4 J) represented a pickup of shunted potentials generated in the spared accessory and motor rootlets entering the pons only a few millimeters away (Fig. 1 upper right).
TABLE 3
Sensory loss after microsurgical division of main sensory root of trigeminal nerve by posterior approach
Type and Distribution of Anesthesia total in 3 divisions partial in 3 divisions fractional (in 1 or 2 divisions) no sensoryloss total
No. of Cases
%
6* 15 10 1 32
18.8 46.8 31.3 3.1
* Two had had previous partial anesthesia from Frazier's operation and three from preoperative studies with electrodes. root." We believe these are the fiber bundles we spared while operating with the microscope through the posterior approach. A few clinical aspects of this study seem important. In 80% of the 32 patients who survived an operation in which we totally divided the dorsal root of the fifth nerve close to the pontine conus under the microscope, a variable amount and extent of sensation was spared over the trigeminal area (Table 3), almost twice as much trigeminal sensation was preserved as in our previously reported series of 29 patients operated on without the microscope. 11 However, the distribution of sparing was similar in both; the areas retaining most sensation were the forehead and the peripheral boundaries of the third division as reported by Pertuiset, et al. ~5 To assess the average loss of sensibility after transection, we plotted the sensory perception of pin-prick and light touch, graded from 4 to 0, into a conventional graph of 244 squares showing the cutaneous distribution of the trigeminal nerve. This study was restricted to the 19 cases in which there had been no previous phenolization of the Gasserian ganglia, root section by the transtemporal route, nor peroperative manipulation with electrodes. In the nine cases in which electrodes were used, the proportion showing complete anesthesia (33%) had been more than twice as great as that found in the remaining 23 cases (Table 3) probably because of trauma to the nerve bundles. The results of the 19 cases were processed in a Digital laboratory 8/e computer* and the resulting averages presented
The ability to produce blink reflex following section of the main sensory root in most cases (Table 2) affords additional evidence of the existence of sensory fibers in the accessory and motor branches. If we were to assume that afferent conduction in the trigeminal system is restricted to proprioceptive impulses from muscles of mastication, as asserted by Pelletier, et al.? 4 it would be difficult to explain why the supraorbital electrode could stimulate these muscles; this would lead to the alternative hypothesis that proprioceptive fibers arise from spindles of facial muscles that as far as we know have not yet been demonstrated in man. However, in their latest paper, Pelletier, et al.? s refer to " . . . occasional splinters of fibers from the sensory root which were seen entering the pons separately at the root entry zone," and later they seem to agree with the *Digital laboratory 8/3 computer made by finding by Gudmundsson, et al., 6 of " . . . Digital Equipment Corporation, 146 Main Street, bundles that were clearly part of the sensory Maynard, Massachusetts 01754. J. Neurosurg. / Volume 42 / May, 1975
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F. B a c c i a n d A. L e y , J r .
Fro. 5. Graphic representation of the computerized average loss of sensibility in 19 patients after operation. Grading of sensation is from 4 (normal) to 0 (anesthesia). See also cover illustration. graphically in Fig. 5. (See cover illustration, also.) The mean values for each of the accepted cutaneous areas of distribution of the three main branches of the trigeminal nerve were 2.4 for the ophthalmic, 1.6 for the maxillary, and 1.8 for the mandibular branch. We should like to emphasize that with the posterior approach the surgeon can always be certain of the boundaries of the main sensory root, thus making an unintentional partial section very unlikely? ,x9 This would even be true in the presence of vascular or other abnormalities, because the component fiber bundles are bounded by a well-defined common pia-arachnoidal covering (Fig. 1 lower right). A second clinical deduction is that there seems to be a definite correlation between the pattern of sensory sparing and the relatively somatotopic arrangement of the motor and accessory rootlets around the main sensory division? ,6 This seems to confirm the findings of Emmons and Rhoton, who in their degeneration experiments in apes found that after section of the rostral fibers adjacent to 520
the motor root, the degeneration was more intense in those regions shown by selective rhizotomy to come from the ophthalmic division. And after section of the caudal fibers adjacent to the brain stem, degeneration was more extensive in those regions that came from the mandibular division. Unfortunately, we were not aware of this study until recently, and so did not make precise references on that matter in the operation records. However, it was obvious that, in accordance with the findings of Gudmundsson, et al., 6 in most of our cases the accessory and anastomotic rootlets were found near the rostral portion of the main root, the region where the fibers from the first division are located. This may also explain why the blink reflexes were usually preserved. Finally, it is important to realize that the term "selective rhizotomy of the trigeminal nerve" merely means section of some particular root. It does not mean that any particular type of sensibility has been spared because, contrary to what was assumed by early investigators, modern research has J. Neurosurg. / Volume 42 / May, 1975
Sensory conduction by accessory nerve rootlets repeatedly demonstrated that within the trigeminal nerve roots there is no specific location for each sensory modality2 ,e Nevertheless, as in most areas of the body, sharp pin-prick and light touch are the first and most seriously impaired senses following nerve injuries of any sort. All of these findings prove how appropriate was Dandy's choice of the term "aberrant" to designate these rootlets.
10.
Acknowledgments
12.
We should like to thank our anesthetist Antonio Castells, M.D.; Maria C. Lizuain, Ph.D., for her invaluable assistance in processing and computerizing the electrophysiological data and the sensory findings; and Rafael Papi, M.D., Chief of the Service of Electrophysiology, for all the facilities and assistance given to us.
References 1. Alvarez-Carregal E, Crue BL Jr, Todd EM: Further observations of trigeminal antidromic potentials. Possible physiological function of sensory antidromic potentials. J Neurosurg 20:277-288, 1963 2. Dandy WE: An operation for the cure of tic douloureux: partial section of the sensory root at the pons. Arch Surg 18:687-734, 1929 3. Darian-Smith I: The neural coding of "tactile" stimulus parameters in different trigeminal nuclei, in Hassler R, Walker AE (eds): Trigeminal Neuralgia. Stuttgart, Georg Thieme Verlag, 1970 4. Davis L, Haven HA: Surgical anatomy of the sensory root of the trigeminal nerve. Arch Neurol Psychiatry 29:1-18, 1933 5. Emmons WF, Rhoton AL Jr: Subdivision of the trigeminal sensory root. Experimental study in the monkey. J Neurosurg 35:585-591, 1971 6. Gudmundsson K, Rhoton AL Jr, Rushton JG: Detailed anatomy of intracranial portion of the trigeminal nerve. J Neurosurg 35: 592-600, 1971 7. Jannetta P J, Rand RW: Transtentorial retrogasserian rhizotomy in trigeminal neuralgia by microneurosurgical technique. Bull Los Angeles Neural Sac 31:93-99, 1966 8. King RB, Barnett JC: Studies of trigeminal nerve potentials: overreaction to tactile facial
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stimulation in acute laboratory preparations. J Neurosurg 14:617-627, 1957 King RB, Meagher JN: Studies of trigeminal nerve potentials. J Neurasurg 12:393-402, 1955 King RB, Meagher JN, Barnett JC: Studies of trigeminal nerve potentials in normal compared to abnormal experimental preparations. J Neurasarg 13:176-183, 1956 Ley A, Guitart JM: Clinical observations on sensory effects of trigeminal dorsal root section. J Neural Neurosurg Psychiatry 34:260-264, 1971 Ley A, Guitart JM, Bacci F: Microsurgical procedure for the selective neurotomy of the Vth nerve root by the suboccipital approach, in Purkyn~ JE (ed): Abstracts Fourth European Congress of Neurosurgery. Prague, Avicenum Czechoslovak Medical Press, 1971, abstract No. 155 Pelletier VA, Poulos DA, Lende RA: Functional localization in the trigeminal root. J Neurasurg 40:504-513, 1974 Pelletier V, Poulos DA, Lende RA: Localization in the trigeminal root. Presented at the Annual Meeting of American Association of Neurological Surgeons, Washington DC, 1970 Pertuiset B, Philippon J, Fohanno D, et al: Traitement microchirurgical de la nevralgie faciale essentielle par neurotomie r6trogass6rienne s61ective transtentorielle. Rev Neural (Paris) 126:97-106, 1972 Provost J, Hardy J: Microchirurgie du trijumeau: anatomie fonctionelle. Neurachirurgie 16:459-470, 1970 Rushworth G: Observations on blink reflexes. J Neurol Neurosarg Psychiatry 25:93-109, 1962 Saunders RL, Sachs E Jr: Relation of the accessory rootlets of the trigeminal nerve to its motor root. A microsurgical autopsy study. J Neurosurg 33:317-324, 1970 Stookey B, Ransohoff J: Trigeminai Neuralgia, Its History and Treatment. Springfield, I11, Charles C Thomas, 1959 Struppler A, Dobbelstein H: Elektromyographische Untersuchung des Glabellareflexes bei verschiedenen neurologischen StSrungen. Nervenartz 34:347-352, 1963
Address reprint requests to: Adolfo Ley, M.D., Services of Neurosurgery and Electrophysiology, Ciudad Sanitaria de la Seguridad Social, Universidad Aut6noma, Barcelona, Spain.
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