Central functional changes after facialspinal-accessory anastomosis in man and facial-hypoglossal anastomosis in the cat
CRISTIAN L. V~:RA, M . D . , MAR('IAI, G. LEWIN, M . D . , JIJAN C. KANE, M . D . , AND MARA D. T. CAI,I)ERON, M . S c .
Laboratorio de Neur()[iviologia Clinica and Servicio de Neurocirugia, Escuela de Medicinea Universidad Catolica, Santiago, Chile A left facial-spinal-accessory anastomosis was performed for peripheral facial paralysis in an 8-year-old boy. By the fourth postoperative year, the corneal reflex showed a normal latency, and left arm and face movements could be executed independently. The possibility of neural plasticity playing a role in establishing new central relationships which enable the achievement of a "normal" latency corneal reflex and independent face and arm movements is discussed. The latency of the corneal reflex recorded as electrical response of the orbicularis oculi muscle to electrical stimulation of the ipsilateral cornea was measured in normal cats and in cats which had undergone a facial-hypoglossal anastomosis 12 to 14 months previously. The latency of the reflex was 8 to 22 msec in normal animals and 200 to 300 msec in the operated cats, while conduction times in the regenerated hypoglossal nerve tibers were found to be within normal limits. This suggests that the long latency of the corneal reflex following the cross anastomosis is due to the time required for transmission across newly-formed connections between the trigeminal terminals and the hypoglossal neurons. K~:vWoRDs
9 nerve
9 anastomosis
hypoglossal
nerve fibers
9 corneal
y
OUN(~42 s t a t e d t h a t " c h a n g e s affecting the c e n t r a l ( n e u r o n a l ) connections as a result o f the new per i p h e r a l c o n n e c t i o n s " c o u l d be a m o n g the processes c o m p l e t i n g nerve r e g e n e r a t i o n . R e c e n t l y , m i c r o e l e c t r o d e studies in kittens h a v e s h o w n c h a n g e s in t h e p a t t e r n o f m o n o s y n a p t i c p a t h w a y s to spinal m o t o -
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spinal-accessory
nerve
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neurons o c c u r r i n g a f t e r r e g e n e r a t i o n t h a t followed c r o s s e d a n a s t o m o s i s o f s o m e nerves to the hind limbs. '3,'' S p i n a l - a c c e s s o r y - f a c i a l a n a s t o m o s i s for the treatment of peripheral facial p a r a l y sis" 4.~.,,2,~,~.2~.~.:J~ :~, r e p r e s e n t s a c r o s s e d nerve a n a s t o m o s i s ; s o m e o f the c e n t r a l functional m o d i f i c a t i o n s o c c u r r i n g a f t e r this 18]
C. L. Vera, M. G. Lewin, J. C. Kase and M. D. T. Calderon operation were pointed out by KennedyTM and Cushing." In a case of seventh nerve paralysis treated with such an operation and followed for 39 months, we have obtained additional data that also suggest the importance of central mechanisms in the ultimate regeneration that occurs following this procedure. For example, recovery of the corneal reflex which exhibited a normal latency by the end of the observation period led us to postulate the formation of functional connections between trigeminal afferents~2,~,3~ and the spinal-accessory motoneurons. The validity of such a possibility is strengthened by the anatomical recognition of secondorder connections between the trigeminal complex and the neurons of both the spinal accessory and the hypoglossal nuclei?~ To provide answers to some of the questions proposed by these observations, a corresponding study was carried out in animals. Recovery of the corneal reflex was investigated in cats following a hypoglossalfacial anastomosis, a procedure also used in humans for the treatment of facial paralysis. t'5,qAS'lg'2~176 Normal latency~1,24,3~,3~did not return. The experimental findings suggest that prolongation of the latency is due to long transmission time across newly functioning paths between trigeminal and hypoglossal nerves rather than slow conduction along regenerated hypoglossal axons. Clinical Material and Methods
Case Report An 8-year-old right-handed boy developed episodes of bilateral ear suppuration at the age of 2 years. During the last episode before admission a left peripheral facial paralysis was noted. He was admitted to a Children's Hospital in Santiago where a left radical mastoidectomy was performed. Three months later he was referred to our service. He had complete left facial paralysis with face asymmetry, Bell's phenomenon, and no left corneal reflexY4 Corneal sensation was intact. Electromyogram (EMG) of the left facial muscles showed only denervation activity, and cathodal stimuli applied behind the left ear lobe failed to elicit a visible or electrically recordable response from left facial muscles. A left facial-spinal-accessory anastomosis was performed. 182
Postoperative Functional Studies Neuromuscular function and voluntary motility of the left side of the patient's face were evaluated 12, 27 and 39 months after the nerve anastomosis. The degree of facial symmetry was recorded photographically. Percutaneous cathodal stimulation of the sutured nerve trunks was carried out with a brass rod (1 • 3 mm tip surface) placed in contact with the skin overlying the nerve suture site, with the anode a large flexible copper plate applied over the opposite side of the neck. Square wave pulses of 1 msec duration were delivered through this pair of electrodes. Electrical activity of the orbicularis oculi (OO) muscle especially in the inferior lid close to its free edge ~ was recorded as EMG through small pairs of needle electrodes insulated except at their tips. They were inserted through the skin at points about 2 mm apart from each other and connected through capacity-coupled amplifiers to a cathode ray oscilloscope (CRO) equipped with a Grass Photo Kymograph camera.* A saline-soaked cotton wisp was used to test the corneal reflex. It was linked with a specially devised circuit which triggered the CRO beam, recording the OO electrical activity whenever the cornea was touched. Thus, the latency of the corneal reflex could be determined accurately.25 The cotton wisp was held for a few seconds near the temporal side of the eye before the cornea was touched so that there was no visual warning before actual mechanical stimulation. Repeated recordings proved the constancy of latency determinations for the OO response. 22'~5 To record the electrical activity of voluntary arm and face movements, pairs of disc electrodes were attached to the skin overlying the superior border of both trapezii muscles (5- to 6-cm separation) and also over upper and lower eyelids or on the cheeks. These electrodes were connected through capacitycoupled amplifiers to the CRO. Records were made during the following face and shoulder movements: *Cathode ray type 565 oscilloscope manufactured by Tektronix, Inc., P.O. Box 500, Beaverton, Oregon 97005. Grass Photo Kymograph camera manufactured by Grass Instrument Company, 101 Old Colony Avenue, Quincy, Massachusetts 02169. J. Neurosurg. / Volume 43 / August, 1975
Changes after facial-spinal-accessory anastomosis
Fic. 1. Photographs and electromyographic recordinss of electrical activity during voluntary face and shoulder movements. LF = left facial muscles; RF = right facial muscles; LT = left trapezius muscle; RT = right trapezius muscle. All records were taken with widely spaced surface electrodes during the following actions: A: Wrinkling left side of face without moving left arm (photograph, LF and LT records); wrinkling right side of face without moving right arm (RF and RT records); B: Left arm raising without moving left side of face (photograph, LF and LT records); rigfit arm raising without moving right side of face (RF and RT records). C: Left arm raising with full force, allowing involuntary contraction of left side of face if it occurred (photograph, LF and LT records); intentional association of movement of right arm and the right side of the face(RF and RT records). Regular continuous artifact is record of electrocardiogram through surface electrodes. Calibrations for all records: 10 Hz and 500 uV.
1. The patient was asked to contract the left side of his face and close his left eye without raising his left arm; the same maneuver was carried out on the right side for control purposes (Fig. 1 A). 2. The patient was asked to raise his left arm without moving the left side of his face; the patient was also asked to raise his right arm without moving the right side of his face as a control (Fig. 1 B). 3, The same maneuver as in 2, but with forceful elevation of the left arm. The right side was tested similarly but the patient was instructed to c o n t r a c t simultaneously the right facial musculature (Fig. 1 C). The patient's face was also observed and photographed when he smiled or cried.
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Case Study: Results Reappearance of the Corneal Reflex The records of electrical activity of the left OO obtained upon ipsilateral mechanical corneal stimulation showed absence of a corneal reflex during the first postoperative year and reappearance of this reflex with a long latency (230 to 240 msec) during the third postoperative year (Fig. 2). During the fourth postoperative year, recordings showed a corneal reflex with a latency of only 40 msec, the value obtained from normally innervated O O (Fig. 3).
Independence of Voluntary Face and Arm Movements Development of complete independence of voluntary face and arm movements was at]83
C. L. Vera, M. G. Lewin, J. C. Kase and M. D. T. Calderon tained gradually during the postoperative period. One year after operation, the left side of the face moved whenever the left arm was raised and it was impossible for the patient to move the left side of his face unless he raised his left arm. At 27 months after operation, the left facial muscle contractions initiated with left arm elevation could be maintained after lowering the arm. Ultimately, during the fourth postoperative year, the left arm and face could be moved voluntarily with complete independence of each other? 3 At this time there was absence of electrical activity of the facial territory when the arm was moved and absence of electrical activity of trapezius when the face was brought into action (Fig. 1 A and B). As reported by other observers, 17 smiling or Flo. 2. Bipolar needle recording (retouched) crying exposed the left facial paralysis even from inferior part of orbicularis muscles made 21/2 when all other testing demonstrated virtual years after crossed nerve suture operation during recovery of facial m o t o r function on that side. tactile corneal stimulation. Initiation of sweep indicates instant of electrical contact between cornea The results of all these observations are sumand cotton wisp. Upper: Operated side; time marized in Table 1. calibration = 30 msec, voltage = 500 ~V. Lower." Normal side; time calibration = 20 msec, Animal Studies: Material and Methods voltage = 100 uV. Nonoperated Animals Young adult cats of both sexes were studied under barbiturate anesthesia. Their heads were held in position by a simple head holder. A pair of silver wires with smooth spherical tips served as stimulating electrodes. The tips were separated by 3 mm and were positioned gently to touch the cornea. Square wave pulses (0.5 msec) were applied to the cornea and the electrical activity of the ipsilateral orbicularis oculi (OO), especially the fasciculi over the lower lid, 16 was recorded bipolarly with fine needles insulated except at their tips and linked to a capacity-coupled amplifier and cathode ray oscilloscope. The stimulus intensities used were supramaximal for the response studied.
Operated Animals Sixty cats were operated on under ether anesthesia. The hypoglossal nerve was carefully dissected free from the surrounding structures in the neck a8 and sectioned as distally as possible. This nerve stump was F~o. 3. Monopolar needle recording from carried under the parotid gland and sutured inferior part of orbicularis muscles made 31/2years end to end with 6-0 silk sutures through the after crossed nerve suture operation. Stimulation as ]n Fig. 2. Upper: Operated side. Lower: epineurium to the distal stump of the ipNormal side. Time calibration = 20 msec; volt- silateral facial nerve which had previously age = 500 uV. been sectioned at its point of emergence from 18,4
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Changes after facial-spinal-accessory anastomosis TABLE 1 Functional changes in patient after facial-spinal-accessory anastomosis* Feature Observed facial symmetry Bell's phenomenon when trying to close both eyes effect of percutaneous cathodal stimulation over suture site
still asymmetric but less than preoperatively very evident on left
visible and recordable activity of OO and other facial muscles on left needle EMG of left OO no fibrillation recorded on left latency of left corneal reflex absent reflex face & shoulder muscles, voluntary movement ability to wrinkle left impossible; elevation of left arm necessary to side of face and to obtain left face motion close left eye without raising left arm
ability to raise left arm without contracting left side of face forced elevation of left arm smiling or crying
Postoperative Period 27 months
12 months
better than at 12 mos less than at 12 mos
39 months
better than at 27 mos but still not perfectly symmetrical less than at 27 mos, but not absent
same
same
same
same
reflex present, 240 msec latency
reflex present, 40 msec latency
feasible if left arm perfectly possible; confirmed raised to initiate by observation & EMG action; left arm could then be lowered while left side of face contraction was maintained impossible; contraction feasible; initiation of perfectly possible; observed of muscles of left movement produced and documented by EMG facial territory always facial contraction occurred contemporaneously inevitable wrinkling of same same; observed and left side of face documented by EMG same evident left facial same paralysis
* o o = orbicularis oculi muscle.
the s t y l o m a s t o i d f o r a m e n . This orifice was sealed with b o n e wax a f t e r the c e n t r a l s t u m p o f the facial nerve was avulsed. Two m o n t h s a f t e r the a n a s t o m o s i s , the a n i m a l s were p l a c e d u n d e r e t h e r a n e s t h e s i a a n d their h e a d s were s e c u r e d in a h e a d h o l d e r to test their c o r n e a l reflexes with the s a m e technique as for the u n o p e r a t e d a n i m a l s . P e r c u t a n e o u s c a t h o d a l s t i m u l a t i o n was a p p l i e d to the s u t u r e d n e r v e t r u n k s with a b r a s s r o d o f 1 • 3 - m m t i p surface. T h e tip was pressed a g a i n s t the s h a v e d skin o f the neck, p r o x i m a l to the n e r v e s u t u r e site. T h e a n o d e was a c o p p e r p l a t e a p p l i e d over the opposite side o f the neck. S q u a r e wave pulses o f 0.5-msec d u r a t i o n a n d m a x i m a l i n t e n s i t y for the response s t u d i e d w e r e d e l i v e r e d t h r o u g h this pair o f electrodes. Twelve to 14 m o n t h s a f t e r the a n a s t o m o s i s , six of the o p e r a t e d a n i m a l s were a n e s t h e t i z e d J. Neurosurg. / Volume 43 / August, 1975
with e t h e r a n d p l a c e d in a B a l t i m o r e stereotaxic instrument's headpiece and frame;* their spinal cords were s e c t i o n e d at the C 3 - 4 level. P r o c a i n e was a p p l i e d to all pressure p o i n t s a n d to the s u r g i c a l w o u n d . Ether a n e s t h e s i a was d i s c o n t i n u e d a n d t h e cornea was stimulated e l e c t r i c a l l y as d e s c r i b e d before. T h e O O a c t i v i t y s u b s e q u e n t to this s t i m u l a t i o n was r e c o r d e d with t h e s a m e e l e c t r o d e s a n d r e c o r d i n g t e c h n i q u e as d e s c r i b e d above. D i r e c t e l e c t r i c a l s t i m u l a t i o n o f the nucleus o f t h e twelfth nerve o f t h e s e a n i m a l s was c a r r i e d out t h r o u g h c o n c e n t r i c electrodes m a d e o f fine i n s u l a t e d h y p o d e r m i c needles with a piece o f i n s u l a t e d wire fitted inside them. T h e s e s t i m u l a t i n g e l e c t r o d e s w e r e
*Stereotaxic instrument made by Baltimore Instruments, Baltimore, Maryland. 185
C. L. Vera, M. G. Lewin, J. C. Kase and M. D. T. Calderon 25 msec were found in 120 responses measured in several different experiments. Response amplitude varied with the level of anesthesia (Fig. 4), and diminished when successive stimulating shocks were delivered at a rate of 8 to 10/sec. The OO response to single test shocks applied to the cornea every 5 to 10 seconds increased in amplitude during 10 to 15 seconds after a 10- to 15-second period of repetitive corneal stimulation (20 to
50/sec).
Fie. 4. Bipolar recordings of orbicularis oculi response to ipsilateral electrical corneal stimuli of supramaximal intensity. Dose of intraperitoneal barbiturate anesthesia is increased in each recording. A: Light anesthesia (0.30 gr Nembutal/kg body weight). B, C, and D: Twenty percent of original dose injected before each recording. Responses were photographed after the effect of the additional anesthetic dose had become stable. Time calibration = 10 msec; voltage = 1 /~V.
Operated Animals
Sixty days after facial-hypoglossal anastomosis the animals showed hemiatrophy of their tongues on the operated side. Facial m o v e m e n t s (both sides) were observed whenever they ate or licked their bodies. The face asymmetry noted in early postoperative period was mild or absent. However, bipolar electrical stimulation of the cornea at this time failed to elicit an electrical response from the ipsilateral OO (Fig. 5 A). Electrical activity of this OO muscle could be obtained upon percutaneous cathodal stimulation of the hypoglossal nerve trunk applied well proximal to the suture site (Fig. 5 B). Twelve months after operation, electrical corneal stimulation on the operated side produced both a visible and an electrical response in the ipsilateral OO. This response had a much longer latency (200 to 300 msec) and was of much longer duration (Fig. 6 C) than the O O response recorded from the nonFl~. 5. Records obtained 3 months after o p e r a t e d animals. This OO response hypoglossal-facial anastomosis in cats. Upper." Absence of orbicularis oculi response to corneal decreased in amplitude with stimulating frestimulation. Time calibration = 10 msec; quencies as low as 3/sec. Sometimes, the voltage = 500 /~V. Lower: Response to per- response could not be elicited by ipsilateral cutaneous cathodal stimulation proximal to suture electrical stimulation with single shocks, but site. Time calibration = 10 msec; voltage = 100 a series of five or six repetitive stimuli at 10 to /zV. 20 Hz did succeed in eliciting a response (Fig. 6 B). Eye closure was also elicited in these cases by projecting a puff of air to the cornea inserted stereotaxically into the medulla, a9 on the operated side, or by touching it with a and electrode placements were verified cotton wisp before anesthetizing and preparhistologically. ing these animals for electrical exploration. Sectioning the twelfth nerve trunk abolished Animal Studies: Results the newly established electrical response of the OO (Fig. 6 D). Nonoperated Animals Single square wave pulses of 0.5-msec The latency of the electrical response duration applied directly to the twelfth nerve recorded from the OO of n o n o p e r a t e d nucleus on the operated side through animals varied from 10 to 22 msec (Fig. 4 A). stereotaxically implanted electrodes elicited This latency was constant for each animal in electrical activity of the ipsilateral OO (Fig. 7 the same testing session but values from 8 to A). This electrical response had a total laten]86
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Changes after facial-spinal-accessory anastomosis cy of around 5 msec and the characteristics of a "direct" neuromuscular response when tested with repetitive stimulation. This response was abolished by section of the sutured twelfth nerve trunk (Fig. 7 B).
Discussion
Clinical Study Latencies in the Corneal-Facial and Corneal-Accessory Reflexes. The long laten-
cy of the corneal reflex during the third postoperative year cannot be attributed to changes affecting its afferent t r i g e m i n a l pathway. 16,~t,~4,st,32 Dysfunction in the efferent path of this reflex (fibers pertaining to the eleventh nerve nucleus neurons, see below) could be a m o r e plausible explanation. At 27 m o n t h s a f t e r surgery, the stage of the regenerating spinal accessory fibers could still have exhibited a slowed conduction, ",3~ and this could have accounted for the long latency of the OO response to corneal stimulation. Against such an explanation are findings in cases of severe facial nerve pathology 31,s2 where the corneal reflex or corresponding physiologically late components of other O O responses to corneal stimulation 2a show much shorter latencies than the 240 msec found in our patient. The possibility that the O O response to corneal stimulation was a voluntary action in which the patient was consciously trying to avoid the touching of his cornea by attempting to move his arm and shoulder defensively was also considered. However, the latencies measured were constant and the patient remained immobile during testing. Furthermore, in animal studies where the a n a s t o m o s i s was p e r f o r m e d between the hypoglossal and facial nerves, a similar long latency O O response was ob-
Fto. 6. Bipolar EMG recordings of orbicularis oculi response to electrical stimulation of ipsilateral cornea as in Fig. 4. A: Single 0.5-msec square wave pulse 12 months after operation. Time calibration = 50 msec; voltage = 500 uV. B: Same as A but six stimulus shocks at 20/sec. Time calibration = 150 msec; voltage = 500 ~V. C = Same as A, 14 months after operation. Time calibration = 50 msec; voltage = 200 ~V. D: Same as C after the sutured nerve was sectioned. Time calibration = 150 msec; voltage = 500 t~V.
rained on electrical corneal stimulation in both lightly anesthetized and unanesthetized preparations. Another possibility is that the corneal afferents could have activated a longer central pathway than that used by the normal corneal reflex. 21,24 H o w e v e r , during the fourth postoperative year, there was a decrease in latency o f the O O r e s p o n s e to c o r n e a l stimulation from the high values just discussed to " n o r m a l " values, t6'2a,z4,al This implies that the trigeminal afferent pathway from the cornea 16,~4'sl activated neurons in the eleventh nerve nucleus through pathways of similar lengths and synaptic numbers to those participating in the normal corneal reflex. The existence of such second order connec-
FI~. 7. Electromyographic response from orbicularis oculi to direct stimulation of twelfth nerve nucleus. A: Twelve months after facial-hypoglossal anastomosis. B: After sectioning the twelfth nerve trunk; stimulus evokes no response.
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C. L. Vera, M. G. Lewin, J. C. Kase and M. D. T. Calderon tions between trigeminal and eleventh nerve neurons was recognized by Ramon y Cajal. 3~ However, the details of these are not known. 24 Conceivably, the long time (39 months) required for the appearance of the cornealaccessory reflex of normal latency could relate to plastic properties of neural pathways, 23 that is, the development of functional neural connections incident to environmental differences or learning. Such a process occurs in more primitive nervous systems where it has been shown that in some pathways there are synapses that function only after a period of forced training. 22 Independent Postoperative Voluntary Arm and Face Movements. Independent voluntary movements of left arm and face became possible during the third and fourth years following facial-accessory anastomosis, and were shown to be performed with electrical silence in the surface recordings of the trapezius muscle when the face was moved and of the face muscles when the arm was elevated (Fig. 1A and B). This indicates that the left arm was not kept immobile during the left facial movement by simultaneous activity of the trapezius muscle and its antagonists (the same can be inferred for left facial muscles during elevation of the left arm). Thus, when asked to move the left side of his face, the patient had learned to activate those eleventh nerve neurons that had re-innervated the left facial musculature while keeping inactive other motor neurons concerned with left arm raising. In explanation of such learned movements, there is experimental evidence which also indicates that the plastic potential of neural pathways plays an important role. Normally, eleventh nerve motor neurons are part of the final common path of voluntary arm elevation and are activated by the shoulder area T M and not by the face area 1~ of the motor cortex. '1 However, Schemm 34 demonstrated in monkeys that had undergone a facial-spinal-accessory anastomosis that direct electrical stimulation of the shoulder area of the motor cortex produced face movement and that similar stimulation of the face area had no motor effect in these animals.
Animal Study In the animals, as in the human, the afferent pathways of the corneal reflex (trigeminal nerve) ~3,~4 should not be significantly 188
altered by a crossed anastomosis between facial and hypoglossal nerve. The results shown in Figs. 5, 6, and 7 indicate that the OO response to corneal stimulation (electrical or mechanical) was mediated by an efferent path of twelfth nerve neurons and that the time involved in traversing the efferent (hypoglossal) path of the newly established corneal reflex observed 1 year after operation takes only a fraction (5 msec) of the total latency (200 to 300 msec). Anesthesia, as a factor that might lengthen the latency of the corneal reflex, was excluded by studying animals under local anesthesia and high cervical cord section. The prolonged discharge time of the OO response on the operated side, the occasional necessity to stimulate the cornea repetitively in order to obtain it, and its long latency are compatible with an explanation that invokes the participation of central pathways involving more synapses than those of the normal corneal reflex. The known existence of second-order relations between the fifth nuclear complex and the eleventh and twelfth nerves a~would be compatible with this suggestion, and it is further suggested that these connections do not become functional until after the nerve anastomosis. 22 The failure of the newly established corneal reflex latency to return to normal 24,31,z2 and the apparent lack of development of independent face and tongue movements constitute the main differences observed between the animal after facial-hypoglossal anastomosis and the human after facial-spinal-accessory anastomosis.
Acknowledgments We want to thank Professor J. V. Luco for opening to us the facilities of the Gabriela G. Gildemeister Laboratories of Neurophysiology at the Catholic University, Santiago, and particularly for his encouragement, criticism, and invaluable advice. We also want to thank Professor Sidney Goldring, Washington University School of Medicine, St. Louis, Missouri, for correcting and criticizing the manuscript.
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34. 35.
centers. Philos Trans R Soc Lond (Bioi Sci) 194:127-162, 1901 Kessler LA, Moldaver J, Pool JL: Hypoglossal-facial anastomosis for treatment of facial paralysis. Neurology (Minneap) 9:118-125, 1959 Korte W: Ein Fall von Nervenpropfung: des Nervus Facialis auf den Nervus Hypoglossus. Dtseh Med Wochenschr 29:293-295, 1903 Kugelberg E: Facial reflexes. Brain 75: 385-396, 1952 Luco JV: Plasticity of neural function in learning and retention, in Brazier MAB (ed): Brain Function, Volume 2. Los Angeles, University of California Press, 1964, pp 135-160 Luco .IV, Aranda LC: An electrical correlate to the process of learning. Experiments in Blatta orientalis. Nature 201:1330-1331, 1964 Magladery JW, Teasdall RD: Corneal reflexes. An electromyographic study in man. Arch Neuroi 5:269-274, 1961 McKenzie KG, Alexander E: Restoration of facial function by anastomosis. Ann Surg 132:411-415, 1950 Olivecrona H: The surgical treatment of intracranial tumors, in Olivecrona H, TSnnis W (eds): Handbuch der Neurochirurgie, Volume 4, Part 4. Berlin/Heidelberg/New York, Springer-Verlag, 1967, pp 219-220 Penfield WG, Jasper H: Epilepsy and the Functional Anatomy of the Human Brain. Boston, Little, Brown and Co, 1954 Penfield WG, Rasmussen T: The Cerebral Cortex of Man. A Clinical Study of Localization of Function. New York, Macmillan, 1950 Poppen J" An Atlas of Neurosurgical Techniques. Philadelphia/London, W B Saunders, 1960, pp 328-329 Ramon y Cajal S: Histologie du systeme nerveux de I'homme et des vertebres. Talleres Graficos Montona Madrid. Instituto Superior de Investigaciones Cientificas. Madrid, Instituto Ramon Cajal, 1952, pp 706, 720 Rushworth G: The effects of cranial nerve pathology on the blink reflexes. Br Ophthaimol U K 82:549-558, 1962 Rushworth G: Observations on blink reflexes. J Neurol Neurosurg Psychiatry 25:93-108, 1962 Sanders FK, Whitteridge D: Conduction velocity and myelin thickness in regenerating nerve fibers. J Physioi (Lond) 105:152-174, 1946 Schemm GW: The pattern of cortical localization following cranial nerve cross anastomosis. J Neurosurg 18:593-596, 1961 Sjoquist O: Surgery of cranial nerves, in Olivecrona H, TSnnis W (eds): Handbuch der Neuroehirurgie, Volume 6, Part 6. Berlin/ Heidelberg/New York, Springer-Verlag, 1957, pp 1-58 "189
C. L. Vera, M. G. Lewin, J. C. Kase and M. D. T. Calderon 36. Svien H J, Karavatis AL: A technique for anastomosis of the facial nerve and spinal accessory nerve. J Neurosarg 11:509-510, 1954 37. Thulin CA, Petersen I, Grandholm L: Follow-up study of spinal accessory-facial anastomosis with special reference to electromyographic findings. J Neural Neurasurg Psychiatry 27:502-506, 1964 38. Vera CL, Vial JD, Luco JV: Reinnervation of the nictitation membrane of cat by cholinergic fibers. J Neuraphysiol 20:365-373, 1957 39. Verhaart WJC: A Stereotaxic Atlas af the Brain Stem of the Cat: Comprising the Cord, the Medulla Oblongata, the Pars, and the Mesencephalon. Assen, Van Gorcum S Comp N V, 1964 40. Welty CF: Anastomosis of facial and hypoglossal nerve for facial paralysis. JAMA 62:612-613, 1914 41. Woolsey CN: Organization of somatic sensory and motor areas of the cerebral cortex, in Harlow HF, Woolsey CN (eds): Biological and Biochemical Bases of Behavior. Madison, Wis, University of Wisconsin Press, 1958, pp 63-81
190
42. Young JZ: The functional repair of nervous tissue. Physiol Rev 22:318-374, 1942
This work was supported in part by the Gildemeister Foundation, Santiago-Chile, and by Grant 61139 of The Rockefeller Foundation, New York. Preliminary results of these observations were read at the Jornadas Anuales de la Sociedad de Neurologia, Psiquiatria y Neurocirugia de Chile in 1967 in Santiago, Chile. Present address for Dr. Lewin: Montreal Neurological Hospital and Institute, 3801 University Street, Montreal, P.Q., Canada. Present address for Dr. Kase: Unidad Neurologica, Catholic University, Santiago, Chile. Present address for Miss Calderon: Department of Psychology, Boston University, Boston, Massachusetts. Address reprint requests to: Cristi~n L. Vera, M.D., Division of Neurological Surgery, Medical University of South Carolina, 80 Barre Street, Charleston, South Carolina 29401.
J. Neurosurg. / Volume 43 / August, 1975
CRISTIAN L. V~:RA, M . D . , MAR('IAI, G. LEWIN, M . D . , JIJAN C. KANE, M . D . , AND MARA D. T. CAI,I)ERON, M . S c .
Laboratorio de Neur()[iviologia Clinica and Servicio de Neurocirugia, Escuela de Medicinea Universidad Catolica, Santiago, Chile A left facial-spinal-accessory anastomosis was performed for peripheral facial paralysis in an 8-year-old boy. By the fourth postoperative year, the corneal reflex showed a normal latency, and left arm and face movements could be executed independently. The possibility of neural plasticity playing a role in establishing new central relationships which enable the achievement of a "normal" latency corneal reflex and independent face and arm movements is discussed. The latency of the corneal reflex recorded as electrical response of the orbicularis oculi muscle to electrical stimulation of the ipsilateral cornea was measured in normal cats and in cats which had undergone a facial-hypoglossal anastomosis 12 to 14 months previously. The latency of the reflex was 8 to 22 msec in normal animals and 200 to 300 msec in the operated cats, while conduction times in the regenerated hypoglossal nerve tibers were found to be within normal limits. This suggests that the long latency of the corneal reflex following the cross anastomosis is due to the time required for transmission across newly-formed connections between the trigeminal terminals and the hypoglossal neurons. K~:vWoRDs
9 nerve
9 anastomosis
hypoglossal
nerve fibers
9 corneal
y
OUN(~42 s t a t e d t h a t " c h a n g e s affecting the c e n t r a l ( n e u r o n a l ) connections as a result o f the new per i p h e r a l c o n n e c t i o n s " c o u l d be a m o n g the processes c o m p l e t i n g nerve r e g e n e r a t i o n . R e c e n t l y , m i c r o e l e c t r o d e studies in kittens h a v e s h o w n c h a n g e s in t h e p a t t e r n o f m o n o s y n a p t i c p a t h w a y s to spinal m o t o -
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9
spinal-accessory
nerve
9
reflex
neurons o c c u r r i n g a f t e r r e g e n e r a t i o n t h a t followed c r o s s e d a n a s t o m o s i s o f s o m e nerves to the hind limbs. '3,'' S p i n a l - a c c e s s o r y - f a c i a l a n a s t o m o s i s for the treatment of peripheral facial p a r a l y sis" 4.~.,,2,~,~.2~.~.:J~ :~, r e p r e s e n t s a c r o s s e d nerve a n a s t o m o s i s ; s o m e o f the c e n t r a l functional m o d i f i c a t i o n s o c c u r r i n g a f t e r this 18]
C. L. Vera, M. G. Lewin, J. C. Kase and M. D. T. Calderon operation were pointed out by KennedyTM and Cushing." In a case of seventh nerve paralysis treated with such an operation and followed for 39 months, we have obtained additional data that also suggest the importance of central mechanisms in the ultimate regeneration that occurs following this procedure. For example, recovery of the corneal reflex which exhibited a normal latency by the end of the observation period led us to postulate the formation of functional connections between trigeminal afferents~2,~,3~ and the spinal-accessory motoneurons. The validity of such a possibility is strengthened by the anatomical recognition of secondorder connections between the trigeminal complex and the neurons of both the spinal accessory and the hypoglossal nuclei?~ To provide answers to some of the questions proposed by these observations, a corresponding study was carried out in animals. Recovery of the corneal reflex was investigated in cats following a hypoglossalfacial anastomosis, a procedure also used in humans for the treatment of facial paralysis. t'5,qAS'lg'2~176 Normal latency~1,24,3~,3~did not return. The experimental findings suggest that prolongation of the latency is due to long transmission time across newly functioning paths between trigeminal and hypoglossal nerves rather than slow conduction along regenerated hypoglossal axons. Clinical Material and Methods
Case Report An 8-year-old right-handed boy developed episodes of bilateral ear suppuration at the age of 2 years. During the last episode before admission a left peripheral facial paralysis was noted. He was admitted to a Children's Hospital in Santiago where a left radical mastoidectomy was performed. Three months later he was referred to our service. He had complete left facial paralysis with face asymmetry, Bell's phenomenon, and no left corneal reflexY4 Corneal sensation was intact. Electromyogram (EMG) of the left facial muscles showed only denervation activity, and cathodal stimuli applied behind the left ear lobe failed to elicit a visible or electrically recordable response from left facial muscles. A left facial-spinal-accessory anastomosis was performed. 182
Postoperative Functional Studies Neuromuscular function and voluntary motility of the left side of the patient's face were evaluated 12, 27 and 39 months after the nerve anastomosis. The degree of facial symmetry was recorded photographically. Percutaneous cathodal stimulation of the sutured nerve trunks was carried out with a brass rod (1 • 3 mm tip surface) placed in contact with the skin overlying the nerve suture site, with the anode a large flexible copper plate applied over the opposite side of the neck. Square wave pulses of 1 msec duration were delivered through this pair of electrodes. Electrical activity of the orbicularis oculi (OO) muscle especially in the inferior lid close to its free edge ~ was recorded as EMG through small pairs of needle electrodes insulated except at their tips. They were inserted through the skin at points about 2 mm apart from each other and connected through capacity-coupled amplifiers to a cathode ray oscilloscope (CRO) equipped with a Grass Photo Kymograph camera.* A saline-soaked cotton wisp was used to test the corneal reflex. It was linked with a specially devised circuit which triggered the CRO beam, recording the OO electrical activity whenever the cornea was touched. Thus, the latency of the corneal reflex could be determined accurately.25 The cotton wisp was held for a few seconds near the temporal side of the eye before the cornea was touched so that there was no visual warning before actual mechanical stimulation. Repeated recordings proved the constancy of latency determinations for the OO response. 22'~5 To record the electrical activity of voluntary arm and face movements, pairs of disc electrodes were attached to the skin overlying the superior border of both trapezii muscles (5- to 6-cm separation) and also over upper and lower eyelids or on the cheeks. These electrodes were connected through capacitycoupled amplifiers to the CRO. Records were made during the following face and shoulder movements: *Cathode ray type 565 oscilloscope manufactured by Tektronix, Inc., P.O. Box 500, Beaverton, Oregon 97005. Grass Photo Kymograph camera manufactured by Grass Instrument Company, 101 Old Colony Avenue, Quincy, Massachusetts 02169. J. Neurosurg. / Volume 43 / August, 1975
Changes after facial-spinal-accessory anastomosis
Fic. 1. Photographs and electromyographic recordinss of electrical activity during voluntary face and shoulder movements. LF = left facial muscles; RF = right facial muscles; LT = left trapezius muscle; RT = right trapezius muscle. All records were taken with widely spaced surface electrodes during the following actions: A: Wrinkling left side of face without moving left arm (photograph, LF and LT records); wrinkling right side of face without moving right arm (RF and RT records); B: Left arm raising without moving left side of face (photograph, LF and LT records); rigfit arm raising without moving right side of face (RF and RT records). C: Left arm raising with full force, allowing involuntary contraction of left side of face if it occurred (photograph, LF and LT records); intentional association of movement of right arm and the right side of the face(RF and RT records). Regular continuous artifact is record of electrocardiogram through surface electrodes. Calibrations for all records: 10 Hz and 500 uV.
1. The patient was asked to contract the left side of his face and close his left eye without raising his left arm; the same maneuver was carried out on the right side for control purposes (Fig. 1 A). 2. The patient was asked to raise his left arm without moving the left side of his face; the patient was also asked to raise his right arm without moving the right side of his face as a control (Fig. 1 B). 3, The same maneuver as in 2, but with forceful elevation of the left arm. The right side was tested similarly but the patient was instructed to c o n t r a c t simultaneously the right facial musculature (Fig. 1 C). The patient's face was also observed and photographed when he smiled or cried.
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Case Study: Results Reappearance of the Corneal Reflex The records of electrical activity of the left OO obtained upon ipsilateral mechanical corneal stimulation showed absence of a corneal reflex during the first postoperative year and reappearance of this reflex with a long latency (230 to 240 msec) during the third postoperative year (Fig. 2). During the fourth postoperative year, recordings showed a corneal reflex with a latency of only 40 msec, the value obtained from normally innervated O O (Fig. 3).
Independence of Voluntary Face and Arm Movements Development of complete independence of voluntary face and arm movements was at]83
C. L. Vera, M. G. Lewin, J. C. Kase and M. D. T. Calderon tained gradually during the postoperative period. One year after operation, the left side of the face moved whenever the left arm was raised and it was impossible for the patient to move the left side of his face unless he raised his left arm. At 27 months after operation, the left facial muscle contractions initiated with left arm elevation could be maintained after lowering the arm. Ultimately, during the fourth postoperative year, the left arm and face could be moved voluntarily with complete independence of each other? 3 At this time there was absence of electrical activity of the facial territory when the arm was moved and absence of electrical activity of trapezius when the face was brought into action (Fig. 1 A and B). As reported by other observers, 17 smiling or Flo. 2. Bipolar needle recording (retouched) crying exposed the left facial paralysis even from inferior part of orbicularis muscles made 21/2 when all other testing demonstrated virtual years after crossed nerve suture operation during recovery of facial m o t o r function on that side. tactile corneal stimulation. Initiation of sweep indicates instant of electrical contact between cornea The results of all these observations are sumand cotton wisp. Upper: Operated side; time marized in Table 1. calibration = 30 msec, voltage = 500 ~V. Lower." Normal side; time calibration = 20 msec, Animal Studies: Material and Methods voltage = 100 uV. Nonoperated Animals Young adult cats of both sexes were studied under barbiturate anesthesia. Their heads were held in position by a simple head holder. A pair of silver wires with smooth spherical tips served as stimulating electrodes. The tips were separated by 3 mm and were positioned gently to touch the cornea. Square wave pulses (0.5 msec) were applied to the cornea and the electrical activity of the ipsilateral orbicularis oculi (OO), especially the fasciculi over the lower lid, 16 was recorded bipolarly with fine needles insulated except at their tips and linked to a capacity-coupled amplifier and cathode ray oscilloscope. The stimulus intensities used were supramaximal for the response studied.
Operated Animals Sixty cats were operated on under ether anesthesia. The hypoglossal nerve was carefully dissected free from the surrounding structures in the neck a8 and sectioned as distally as possible. This nerve stump was F~o. 3. Monopolar needle recording from carried under the parotid gland and sutured inferior part of orbicularis muscles made 31/2years end to end with 6-0 silk sutures through the after crossed nerve suture operation. Stimulation as ]n Fig. 2. Upper: Operated side. Lower: epineurium to the distal stump of the ipNormal side. Time calibration = 20 msec; volt- silateral facial nerve which had previously age = 500 uV. been sectioned at its point of emergence from 18,4
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Changes after facial-spinal-accessory anastomosis TABLE 1 Functional changes in patient after facial-spinal-accessory anastomosis* Feature Observed facial symmetry Bell's phenomenon when trying to close both eyes effect of percutaneous cathodal stimulation over suture site
still asymmetric but less than preoperatively very evident on left
visible and recordable activity of OO and other facial muscles on left needle EMG of left OO no fibrillation recorded on left latency of left corneal reflex absent reflex face & shoulder muscles, voluntary movement ability to wrinkle left impossible; elevation of left arm necessary to side of face and to obtain left face motion close left eye without raising left arm
ability to raise left arm without contracting left side of face forced elevation of left arm smiling or crying
Postoperative Period 27 months
12 months
better than at 12 mos less than at 12 mos
39 months
better than at 27 mos but still not perfectly symmetrical less than at 27 mos, but not absent
same
same
same
same
reflex present, 240 msec latency
reflex present, 40 msec latency
feasible if left arm perfectly possible; confirmed raised to initiate by observation & EMG action; left arm could then be lowered while left side of face contraction was maintained impossible; contraction feasible; initiation of perfectly possible; observed of muscles of left movement produced and documented by EMG facial territory always facial contraction occurred contemporaneously inevitable wrinkling of same same; observed and left side of face documented by EMG same evident left facial same paralysis
* o o = orbicularis oculi muscle.
the s t y l o m a s t o i d f o r a m e n . This orifice was sealed with b o n e wax a f t e r the c e n t r a l s t u m p o f the facial nerve was avulsed. Two m o n t h s a f t e r the a n a s t o m o s i s , the a n i m a l s were p l a c e d u n d e r e t h e r a n e s t h e s i a a n d their h e a d s were s e c u r e d in a h e a d h o l d e r to test their c o r n e a l reflexes with the s a m e technique as for the u n o p e r a t e d a n i m a l s . P e r c u t a n e o u s c a t h o d a l s t i m u l a t i o n was a p p l i e d to the s u t u r e d n e r v e t r u n k s with a b r a s s r o d o f 1 • 3 - m m t i p surface. T h e tip was pressed a g a i n s t the s h a v e d skin o f the neck, p r o x i m a l to the n e r v e s u t u r e site. T h e a n o d e was a c o p p e r p l a t e a p p l i e d over the opposite side o f the neck. S q u a r e wave pulses o f 0.5-msec d u r a t i o n a n d m a x i m a l i n t e n s i t y for the response s t u d i e d w e r e d e l i v e r e d t h r o u g h this pair o f electrodes. Twelve to 14 m o n t h s a f t e r the a n a s t o m o s i s , six of the o p e r a t e d a n i m a l s were a n e s t h e t i z e d J. Neurosurg. / Volume 43 / August, 1975
with e t h e r a n d p l a c e d in a B a l t i m o r e stereotaxic instrument's headpiece and frame;* their spinal cords were s e c t i o n e d at the C 3 - 4 level. P r o c a i n e was a p p l i e d to all pressure p o i n t s a n d to the s u r g i c a l w o u n d . Ether a n e s t h e s i a was d i s c o n t i n u e d a n d t h e cornea was stimulated e l e c t r i c a l l y as d e s c r i b e d before. T h e O O a c t i v i t y s u b s e q u e n t to this s t i m u l a t i o n was r e c o r d e d with t h e s a m e e l e c t r o d e s a n d r e c o r d i n g t e c h n i q u e as d e s c r i b e d above. D i r e c t e l e c t r i c a l s t i m u l a t i o n o f the nucleus o f t h e twelfth nerve o f t h e s e a n i m a l s was c a r r i e d out t h r o u g h c o n c e n t r i c electrodes m a d e o f fine i n s u l a t e d h y p o d e r m i c needles with a piece o f i n s u l a t e d wire fitted inside them. T h e s e s t i m u l a t i n g e l e c t r o d e s w e r e
*Stereotaxic instrument made by Baltimore Instruments, Baltimore, Maryland. 185
C. L. Vera, M. G. Lewin, J. C. Kase and M. D. T. Calderon 25 msec were found in 120 responses measured in several different experiments. Response amplitude varied with the level of anesthesia (Fig. 4), and diminished when successive stimulating shocks were delivered at a rate of 8 to 10/sec. The OO response to single test shocks applied to the cornea every 5 to 10 seconds increased in amplitude during 10 to 15 seconds after a 10- to 15-second period of repetitive corneal stimulation (20 to
50/sec).
Fie. 4. Bipolar recordings of orbicularis oculi response to ipsilateral electrical corneal stimuli of supramaximal intensity. Dose of intraperitoneal barbiturate anesthesia is increased in each recording. A: Light anesthesia (0.30 gr Nembutal/kg body weight). B, C, and D: Twenty percent of original dose injected before each recording. Responses were photographed after the effect of the additional anesthetic dose had become stable. Time calibration = 10 msec; voltage = 1 /~V.
Operated Animals
Sixty days after facial-hypoglossal anastomosis the animals showed hemiatrophy of their tongues on the operated side. Facial m o v e m e n t s (both sides) were observed whenever they ate or licked their bodies. The face asymmetry noted in early postoperative period was mild or absent. However, bipolar electrical stimulation of the cornea at this time failed to elicit an electrical response from the ipsilateral OO (Fig. 5 A). Electrical activity of this OO muscle could be obtained upon percutaneous cathodal stimulation of the hypoglossal nerve trunk applied well proximal to the suture site (Fig. 5 B). Twelve months after operation, electrical corneal stimulation on the operated side produced both a visible and an electrical response in the ipsilateral OO. This response had a much longer latency (200 to 300 msec) and was of much longer duration (Fig. 6 C) than the O O response recorded from the nonFl~. 5. Records obtained 3 months after o p e r a t e d animals. This OO response hypoglossal-facial anastomosis in cats. Upper." Absence of orbicularis oculi response to corneal decreased in amplitude with stimulating frestimulation. Time calibration = 10 msec; quencies as low as 3/sec. Sometimes, the voltage = 500 /~V. Lower: Response to per- response could not be elicited by ipsilateral cutaneous cathodal stimulation proximal to suture electrical stimulation with single shocks, but site. Time calibration = 10 msec; voltage = 100 a series of five or six repetitive stimuli at 10 to /zV. 20 Hz did succeed in eliciting a response (Fig. 6 B). Eye closure was also elicited in these cases by projecting a puff of air to the cornea inserted stereotaxically into the medulla, a9 on the operated side, or by touching it with a and electrode placements were verified cotton wisp before anesthetizing and preparhistologically. ing these animals for electrical exploration. Sectioning the twelfth nerve trunk abolished Animal Studies: Results the newly established electrical response of the OO (Fig. 6 D). Nonoperated Animals Single square wave pulses of 0.5-msec The latency of the electrical response duration applied directly to the twelfth nerve recorded from the OO of n o n o p e r a t e d nucleus on the operated side through animals varied from 10 to 22 msec (Fig. 4 A). stereotaxically implanted electrodes elicited This latency was constant for each animal in electrical activity of the ipsilateral OO (Fig. 7 the same testing session but values from 8 to A). This electrical response had a total laten]86
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Changes after facial-spinal-accessory anastomosis cy of around 5 msec and the characteristics of a "direct" neuromuscular response when tested with repetitive stimulation. This response was abolished by section of the sutured twelfth nerve trunk (Fig. 7 B).
Discussion
Clinical Study Latencies in the Corneal-Facial and Corneal-Accessory Reflexes. The long laten-
cy of the corneal reflex during the third postoperative year cannot be attributed to changes affecting its afferent t r i g e m i n a l pathway. 16,~t,~4,st,32 Dysfunction in the efferent path of this reflex (fibers pertaining to the eleventh nerve nucleus neurons, see below) could be a m o r e plausible explanation. At 27 m o n t h s a f t e r surgery, the stage of the regenerating spinal accessory fibers could still have exhibited a slowed conduction, ",3~ and this could have accounted for the long latency of the OO response to corneal stimulation. Against such an explanation are findings in cases of severe facial nerve pathology 31,s2 where the corneal reflex or corresponding physiologically late components of other O O responses to corneal stimulation 2a show much shorter latencies than the 240 msec found in our patient. The possibility that the O O response to corneal stimulation was a voluntary action in which the patient was consciously trying to avoid the touching of his cornea by attempting to move his arm and shoulder defensively was also considered. However, the latencies measured were constant and the patient remained immobile during testing. Furthermore, in animal studies where the a n a s t o m o s i s was p e r f o r m e d between the hypoglossal and facial nerves, a similar long latency O O response was ob-
Fto. 6. Bipolar EMG recordings of orbicularis oculi response to electrical stimulation of ipsilateral cornea as in Fig. 4. A: Single 0.5-msec square wave pulse 12 months after operation. Time calibration = 50 msec; voltage = 500 uV. B: Same as A but six stimulus shocks at 20/sec. Time calibration = 150 msec; voltage = 500 ~V. C = Same as A, 14 months after operation. Time calibration = 50 msec; voltage = 200 ~V. D: Same as C after the sutured nerve was sectioned. Time calibration = 150 msec; voltage = 500 t~V.
rained on electrical corneal stimulation in both lightly anesthetized and unanesthetized preparations. Another possibility is that the corneal afferents could have activated a longer central pathway than that used by the normal corneal reflex. 21,24 H o w e v e r , during the fourth postoperative year, there was a decrease in latency o f the O O r e s p o n s e to c o r n e a l stimulation from the high values just discussed to " n o r m a l " values, t6'2a,z4,al This implies that the trigeminal afferent pathway from the cornea 16,~4'sl activated neurons in the eleventh nerve nucleus through pathways of similar lengths and synaptic numbers to those participating in the normal corneal reflex. The existence of such second order connec-
FI~. 7. Electromyographic response from orbicularis oculi to direct stimulation of twelfth nerve nucleus. A: Twelve months after facial-hypoglossal anastomosis. B: After sectioning the twelfth nerve trunk; stimulus evokes no response.
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187
C. L. Vera, M. G. Lewin, J. C. Kase and M. D. T. Calderon tions between trigeminal and eleventh nerve neurons was recognized by Ramon y Cajal. 3~ However, the details of these are not known. 24 Conceivably, the long time (39 months) required for the appearance of the cornealaccessory reflex of normal latency could relate to plastic properties of neural pathways, 23 that is, the development of functional neural connections incident to environmental differences or learning. Such a process occurs in more primitive nervous systems where it has been shown that in some pathways there are synapses that function only after a period of forced training. 22 Independent Postoperative Voluntary Arm and Face Movements. Independent voluntary movements of left arm and face became possible during the third and fourth years following facial-accessory anastomosis, and were shown to be performed with electrical silence in the surface recordings of the trapezius muscle when the face was moved and of the face muscles when the arm was elevated (Fig. 1A and B). This indicates that the left arm was not kept immobile during the left facial movement by simultaneous activity of the trapezius muscle and its antagonists (the same can be inferred for left facial muscles during elevation of the left arm). Thus, when asked to move the left side of his face, the patient had learned to activate those eleventh nerve neurons that had re-innervated the left facial musculature while keeping inactive other motor neurons concerned with left arm raising. In explanation of such learned movements, there is experimental evidence which also indicates that the plastic potential of neural pathways plays an important role. Normally, eleventh nerve motor neurons are part of the final common path of voluntary arm elevation and are activated by the shoulder area T M and not by the face area 1~ of the motor cortex. '1 However, Schemm 34 demonstrated in monkeys that had undergone a facial-spinal-accessory anastomosis that direct electrical stimulation of the shoulder area of the motor cortex produced face movement and that similar stimulation of the face area had no motor effect in these animals.
Animal Study In the animals, as in the human, the afferent pathways of the corneal reflex (trigeminal nerve) ~3,~4 should not be significantly 188
altered by a crossed anastomosis between facial and hypoglossal nerve. The results shown in Figs. 5, 6, and 7 indicate that the OO response to corneal stimulation (electrical or mechanical) was mediated by an efferent path of twelfth nerve neurons and that the time involved in traversing the efferent (hypoglossal) path of the newly established corneal reflex observed 1 year after operation takes only a fraction (5 msec) of the total latency (200 to 300 msec). Anesthesia, as a factor that might lengthen the latency of the corneal reflex, was excluded by studying animals under local anesthesia and high cervical cord section. The prolonged discharge time of the OO response on the operated side, the occasional necessity to stimulate the cornea repetitively in order to obtain it, and its long latency are compatible with an explanation that invokes the participation of central pathways involving more synapses than those of the normal corneal reflex. The known existence of second-order relations between the fifth nuclear complex and the eleventh and twelfth nerves a~would be compatible with this suggestion, and it is further suggested that these connections do not become functional until after the nerve anastomosis. 22 The failure of the newly established corneal reflex latency to return to normal 24,31,z2 and the apparent lack of development of independent face and tongue movements constitute the main differences observed between the animal after facial-hypoglossal anastomosis and the human after facial-spinal-accessory anastomosis.
Acknowledgments We want to thank Professor J. V. Luco for opening to us the facilities of the Gabriela G. Gildemeister Laboratories of Neurophysiology at the Catholic University, Santiago, and particularly for his encouragement, criticism, and invaluable advice. We also want to thank Professor Sidney Goldring, Washington University School of Medicine, St. Louis, Missouri, for correcting and criticizing the manuscript.
References 1. Alexander E: Correction of peripheral paralysis of the facial nerve by hypoglossal facial anastomosis. South Med J 47:299-302, 1954 2. Ballance CA, Ballance HA, Steward P: Remarks on the operative treatment of
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3.
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5. 6. 7. 8.
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This work was supported in part by the Gildemeister Foundation, Santiago-Chile, and by Grant 61139 of The Rockefeller Foundation, New York. Preliminary results of these observations were read at the Jornadas Anuales de la Sociedad de Neurologia, Psiquiatria y Neurocirugia de Chile in 1967 in Santiago, Chile. Present address for Dr. Lewin: Montreal Neurological Hospital and Institute, 3801 University Street, Montreal, P.Q., Canada. Present address for Dr. Kase: Unidad Neurologica, Catholic University, Santiago, Chile. Present address for Miss Calderon: Department of Psychology, Boston University, Boston, Massachusetts. Address reprint requests to: Cristi~n L. Vera, M.D., Division of Neurological Surgery, Medical University of South Carolina, 80 Barre Street, Charleston, South Carolina 29401.
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