Presynaptic depolarization of lingual and glossopharyngeal nerve afferents induced by stimulation of trigeminal proprioceptive fibers

EXPERIMENTAL

NEUROLOGY

28, 344-355

(1970)

of lingual and Aff erents Induced by Proprioceptive Fibers

Presynaptic Depolarization Glossopharyngeal Nerve Stimulation of Trigeminal E. K.

SAUERLAND

AND

H.

THIELE

1

Departments of Axatowy alzd Oral Medicine and the Brain Research Institute, Center for Health Sciences, University of California at Los Angeles, Los Angeles, California 90024 Received

April

24,197O

The effect of trigeminal proprioceptive input from masticatory muscles on the level of polarization of lingual and glossopharyngeal nerve afferents was studied in cats with complete precollicular transection of the brain, A modification of Wall’s technique was utilized to determine excitability changes of the central terminals of lingual and glossopharyngeal fibers in nucleus oralis and nucleus parasolitarius, respectively. Primary afferent depolarization of these sensory nerves could be induced by electrical stimulation of the masseteric nerve, anterior digastric nerve, or the trigeminal mesencephalic nucleus. Primary afferent depolarization of lingual and glossopharyngeal fibers was also produced by brisk tension of jaw elevator muscles as well as of jaw openers, whereas moderate sustained tension of these muscles had no effect on the level of terminal polarization. It was concluded that masticatory proprioceptive activities, excluding those mediated in group IA fibers from spindle organs, are responsible for the observed primary afferent depolarization. It appears that the depolarization of presynaptic terminals of lingual and glossopharyngeal fibers plays an important role in the control of reflexly induced tongue movements. Introduction

As was shown by Sauerland and Mizuno (13), electrical conditioning stimulation of the severed masseteric nerve or the nerve to the anterior digastric muscle induces a marked, long-lasting depression of the linguohypoglossal reflex. Similarly, the glossopharyngico-hypoglossal reflex, if conditioned by stimulation of the masseteric or anterior digastric nerve, is subjected to a long-lasting inhibitory phase (Sauerland and Mizuno, unpublished data). The remarkable duration of the depressive effect (300-400 msec) suggests the involvement of a presynaptic inhibitory mechanism. One can hypothesize that the activation of proprioceptive 1 This research was supported by a grant from the United Service, NS 06819-04. Horst Thiele, candidate of medicine, from the University of Hamburg, Germany. 344

States Public was a visiting

Health student

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afferent fibers in the masseteric or anterior digastric nerve induces presynaptic depolarization of the central terminals of lingual and glossopharyngeal afferents and thereby effects presynaptic inhibition of tongue reflexes elicited by stimulation of these sensory nerves. It was the purpose of the present study to verify this assumption. Electrical stimulation of the masseteric or anterior digastric nerve leads to antidromic volleys in trigeminal motor fibers and to orthodromic volleys in proprioceptive afferents. &\ntidromic discharges of motoneurons in the spinal cord may induce increased excitability of presynaptic terminals impinging upon these motoneurons (3). If one assumes a similar situation in the brain stem, antidromic volleys in the masseteric or anterior digastric nerve could lead to heightened excitability of presynaptic terminals contacting trigeminal motoneurons. However, it is unlikely that antidromic discharges in trigeminal motor fibers would exert depolarizing influences on sensory nuclei in the brain stem. Furthermore, there is no morphological evidence for the existence of recurrent collaterals of trigeminal motor fibers (12). On the other hand, orthodromic volleys in trigeminal proprioceptive afferents reach the trigeminal mesencephalic nucleus, and from there via Probst’s tract, a variety of brain stem structures including the reticular formation, the hypoglossal nucleus, and the cervical ventral gray column 2, 9, lS, 19). Smith, Marcarian, and Niemer (16, 17) have reviewed and added to the important electrophysiological aspects of trigeminal proprioceptive input. There is no question that the jaw elevator muscles contain neuromuscular spindles, and that the somata of primary afferents from these proprioceptive organs are located in the trigeminal mesencephalic nucleus (2, 3, 7, 16, 17, 19). On the basis of the available literature and their own experiments, Smith et al. ( 17) hypothesized that the somata of other afferent fibers, such as those from tendon organs, are located in the trigeminal ganglion. We have successfully utilized this assumption as a working hypothesis for our present experimental approaches. As far as the jaw depressors are concerned, virtually nothing is known about their proprioceptive innervation. There are no muscle spindles in the anterior belly of the digastric muscle (l), and no positive proof has been obtained that its nerve has any direct connection to the trigeminal mesencephalic tract or nucleus (5). However, our previous electrophysiological work ( 13) indicates that the nerve of the anterior digastricus contains proprioceptive afferents. Although it is generally assumed that Golgi tendon organs are found in the tendons of all mammalian muscles (11)) no morphological work has been done to prove the existence of proprioceptive organs in the anterior digastric muscle. In the present study, further electrophysiological evidence will be introduced to demonstrate that proprioceptive afferent activity can actually be generated in the anterior digastric muscle. In the

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following, evidence will be presented that activation of masticatory proprioceptive afferents by electrical or natural stimulation leads to primary afferent depolarization of lingual and glossopharyngeal nerve terminals. Methods Seventeen adult cats were used for this study. General anesthesia was induced by ether inhalation and subsequently maintained by short-acting sodium methohexital (Brevital, 5 mg/kg) whenever necessary. Following complete precollicular transection of the brain, the administration of anesthetics was discontinued, and gallamine triethiodide (Flaxedil) was intravenously injected as a muscle relaxant. The method of proper ventilation of immobilized preparations was described earlier (15). The body temperature was kept constant at 36-37 C with radiant heat. Peripheral nerves were carefully dissected and suspended in a small pool of mineral oil. For recording and stimulating purposes, bipolar silver hook electrodes were applied to the proximal portion of the severed nerves. The following nerves were prepared : lingual nerve (14 experiments), glossopharyngeal nerve branches to tongue mucosa (6 experiments), masseteric nerve (10 experiments), and the nerve to the anterior belly of the digastricus ( 11 experiments). A modification of Wall’s technique (20) was utilized to determine the excitability of the central terminals of lingual and glossopharyngeal afferents in the spinal nucleus of the trigeminal tract (nucleus oralis) and nucleus parasolitarius, respectively. Monopolar, stainless steel electrodes with a tip diameter of 0.1 mm were inserted stereotaxically int,o nucleus oralis (coordinates : P 9.5 ; L 4.4 ; H -6.2) or nucleus parasolitarius (coordinates: P13.5; L 2.5; H -6.3), or into both. The stimulation and recording procedures have been described in detail previously ( 14, 15). Test stimuli (0.1 msec duration) were delivered to the central terminals of lingual or glossopharyngeal nerve afferents at the rate of 0.5-l/set, and the resulting antidromic compound potentials were recorded from the respective sensory nerves. Excitability changes in sensory nerve terminals were induced by applying conditioning stimulation via an isolation unit to either the masseteric nerve, the anterior digastric nerve, or the nucleus of the trigeminal mesencephalic tract (stereotaxic coordinates : P 2.5 ; L2.2 ; H -0.4). The optimal conditioning stimulus consisted of a burst of three pulses (5OO/sec, 0.3 msec pulse duration, 7 v). The conditioning interval is defined as the time elapsed between the beginning of the conditioning stimulus and the beginning of the test stimulus. The effects of mechanical stimulation of trigeminal muscle proprioceptors on the excitability of lingual and glossopharyngeal afferents was investigated in six animals. Proprioceptors in jaw elevator muscles (masseter,

temporalis, medial pterygoid) were activated by manual depression of the mandible. In these experiments the mylohyoid and lingual nerves were severed bilaterally. Discharges in the ipsilateral trigeminal ganglion (stereotaxic coordinates : A 6.0; L 6.0 ; H -9.0) were recorded monopolarly with a small concentric stainless steel electrode. On the other hand, proprioceptors in a jaw opener were activated by manual tension on the intertendon of the anterior digastric muscle. In these experiments, the posterior digastric muscle was detached from the intertendon, and the jaw elevator muscles together with the mandible were rendered immobile by means of a tight string around the snout of the animal. The mylohyoid muscle was denervated. Discharges in proprioceptive afferents were recorded from the mylohyoid nerve with fine bipolar gold hook electrodes. The manually induced activity in trigeminal proprioceptive afferents served as the conditioning stimulus. The test stimulus to nucleus oralis or nucleus parasolitarius was generated 30 msec after the occurrence of the first discharge in proprioceptive fibers. Detailed schematics of the experimental arrangements are shown in the upper parts of Figs. 3 and 4. Following the electrophysiological part of the experiments, the electrode positions were verified either macroscopically (trigeminal ganglion) or histologically. Results

Trigeminal proprioceptive input from masticatory muscles produced primary afferent depolarization (PAD) of the central terminals of lingual and glossopharyngeal nerve fibers. Activity in trigeminal proprioceptive afferents was induced by two different methods: by electrical stimulation and hy mechanical stimulation (muscle tension). Lingual and Glossopharyngeal PAD Induced by Electrical Stiwmlation of Trigemicznl Pt-oprioceptive A.ferents. The effects of electrical stimulation of trigeminal proprioceptive afferents on the excitability of lingual nerve terminais in the spinal trigeminal nucleus are demonstrated in Fig. 1. Antidromic compound potentials were evoked by test stimuli to the central processes of lingual nerve fibers in nucleus oralis and recorded distally from the lingual nerve (Fig. lB, controls). Conditioning stimulation to either the ipsilateral masseteric nerve, anterior digastric nerve, or proprioceptive fibers and nerve cells within the trigeminal mesencephalic nucleus induced substantial increases in amplitude of the antidromic potentials (Fig. lB, conditioned). Irrespective to the locus of conditioning stimulation, all time courses of excitability changes showed common characteristics (Fig. l-4) : The latency of onset of the induced PAD was approximately 10 msec; the peak of the time course was observed at 30-40 msec; the declining phase lasted 100-130 msec, and the total duration of the time

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1. Effect of electrical stimulation to trigeminal proprioceptive afferents on oralis. A. Time courses of the excitability of lingual nerve terminals in nucleus excitability changes evoked by stimulation of the ipsilateral masseteric nerve (A), anterior disgastric nerve (0)) or trigeminal mesencephalic nucleus (0). B. Examples of antidromically conducted compound potentials evoked by a test stimulus to nucleus oralis and recorded from the proximal portion of the severed lingual nerve. If conditioning stimulation to ipsilateral trigeminal proprioceptive afferents (A, 0, 0) preceded the test stimulus by the optimal conditioning interval of 37 msec, the antidromic spike was markedly increased in amplitude (see “conditioned” responses) over the control value. Each record depicts three superimposed responses. The data were obtained from two separate experiments (0; and 0, A). Calibrations : time, 2 msec ; amplitude, 80 pv. FIG.

course was approximately 150-170 msec. Conditioning stimulation to the anterior digastric nerve was consistently more effective in producing the lingual PAD than was equally intense conditioning stimulation to the masseteric nerve. Conditioning stimulation to the contralateral masseteric or anterior digastric nerve (three experiments) induced weaker PAD than ipsilateral conditioning. Figure 2 illustrates the effect of electrical stimulation of trigeminal proprioceptive afferents on the excitability of glossopharyngeal nerve terminals. Antidromic compound potentials were evoked by test stimuli to the central processes of glossopharyngeal nerve fibers in nucleus parasolitarius and recorded distally from the glossopharyngeal nerve (Fig 2B, controls). Conditioning stimulation to either the ipsilateral masseteric nerve, anterior digastric nerve, or the trigeminal mesencephalic nucleus induced substantial increases in amplitude of the antidromic spikes (Fig. 2B, condi-

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FIG. 2. Effect of electrical stimulation to trigeminal proprioceptive afferents on the excitability of glossopharyngeal nerve terminals in nucleus parasolitarius. A. Time courses of excitability changes evoked by stimulation of the ipsilateral anterior digastric nerve (a) or the trigeminal mesencephalic nucleus (0). B. Examples of antidromically conducted compound potentials evoked by a test stimulus to nucleus parasolitarius and recorded from the proximal end of the severed glossopharyngeal nerve. If conditioning stimulation to ipsilateral trigeminal proprioceptive afferents (0, 0, masseteric nerve A) preceded the test stimulus by the optimal conditioning interval of 37 msec, the antidromic spike was markedly increased in amplitude (see “conditioned” responses) over the control value. The data were obtained from two separate experiments (0; and @, a). Calibrations : time, 2 msec; amplitude, 60 pv. tioned). The titne courses of excitability changes, evoked by conditioning stimulation to the anterior digastric nerve or the mesencephalic nucleus (Fig ZA), showed similar characteristics as those illustrated in Fig. 1A. Lingual and Glossopharyngeal PAD Induced by Mechanical Stivnulation of Pvoprioceptors in Masticatory Muscles. Figure 3 illustrates the effects of tension of the jaw elevator muscles on the excitability of lingual and glossopharyngeal nerve terminals in nucleus oralis and nucleus parasolitarius, respectively. Brisk depression of the mandible (i.e., brisk tension of the jaw elevator muscles) led to a burst of spikes in the trigeminal ganglion. In analogy to electrical conditioning stimulation, these spikes were used as the afferent conditioning volley. After a latency of 30 msec (corresponding to the conditioning interval), the test stimulus was generated and delivered to the sensory nucleus of either the lingual or glossopharyngeal nerve. Since no spikes were recorded from the trigeminal ganglion during elevation of the mandible (control) or during moderate sustained depres-

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Mandible elevoted

lrom sensory nerve

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1 SEQUENCEOF EVENTSF BRISK DEPRESSI< OF MANOIELE ~figs. C and FI

Brisk depression of mandible

LINGUAL NERVE (Antidromic potential) . Trigeminol Ganglion

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NERVE IX (Antidromic potentiol) c Trigeminol Ganglion

FIG. 3. Effect of depression of mandible (tension of jaw elevator muscles) on the excitability of lingual and glossopharyngeal nerve terminals in nucleus oralis and nucleus parasolitarius, respectively. The experimental arrangement is illustrated in the upper part of the figure. Brisk depression of the mandible led to a brief burst of spikes (conditioning input) in the trigeminal ganglion (lower trace of C and F). The first spike triggered the lower beam of the oscilloscope and a delay unit. After a delay (conditioning interval) of 30 msec, the test stimulus was generated and delivered to the sensory nucleus. The resulting antidromic potential was obtained from the sensory nerve and displayed on the upper beam of the oscilloscope (upper trace of C and F; generated 30 msec after the beginning of the lower beam). During elevation (closed mouth) or sustained depression of the mandible, the test stimuli were triggered externally. Discharges in the trigeminal ganglion and subsquent increases in amplitude of the antidromic potentials were only observed during brisk depression (C, F), whereas no changes over the control values (A, D) were noted during moderate sustained depression of the mandible (B, E). Time bar : 2 msec for upper traces A-F; 10 msec for all lower traces. Amplitude bars : 60 and 20 pv for upper and lower traces of A-C, respectively; 40 and 20 pv for upper and lower traces of D-F, respectively.

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sion of the jaw, test stimuli to sensory nuclei were triggered externally; and no differences in size of the antidromic compound potentials were observed. In contrast, during brisk depression of the mandible, the burst of spikes in the trigeminal ganglion induced substantial increases in amplitude of the antidromic potentials. The effects of tension of the anterior digastric muscle on the excitability of lingual nerve terminals in nucleus oralis are demonstrated in Fig. 4. Brisk tension of the anterior digastric muscle led to a burst of spikes in the mylohyoid nerve (analog to afferent conditioning voliey). After a latency of 30 msec, the test stimulus was delivered to nucleus oralis. Since no spikes were recorded from the mylohyoid nerve during relaxation of the muscle (control) or during moderate sustained tension, test stimuli to nucleus oralis were triggered externally; and no differences in size of the antidromic compound potentials were observed. In contrast, during brisk tension of the anterior digastric muscle, the burst of spikes in the mylolyoid nerve induced a substantial increase in amplitude of the antidromic potential. Similarly, brisk tension of the anterior digastric muscle produced PAD in glossopharyngeal terminals (one experiment). Discussion

The preceding experimental observations have shown that activation of masticatory proprioceptive afferents by electrical or natural stimulation leads to primary afferent depolarization (PAD) of lingual and glossopharyngeal nerve terminals. During the preparation of this paper it was learned that Nakamura and Wu (10) had performed experiments closely related to our present work. In their study of the jaw opening reflex, these investigators demonstrated that electrical stimulation of the masseteric nerve or of the trigeminal mesencephalic nucleus induces depolarization of lingual nerve afferents. Their time courses of excitability changes are in good agreement with the time courses illustrated in this paper (Fig. 1) . It was shown that electrical conditioning stimulation to the anterior digastric nerve was consistently more effective in producing the lingual PAD than was equally intense (supramaximal) conditioning stimulation to the masseteric nerve. This phenomenon could be explained if the various types of proprioceptive muscle afferents are considered. The masseter muscle contains neuromuscular spindles as well as Golgi tendon organs (IS) ; in addition, there may be atypical, rather primitive types of endings which are characteristic for many cranial nerve regions (5 j. Thus, the masseteric nerve contains group IA and group II afferents from spindle organs, group IB fibers from tendon organs, and possibly also group III fibers from more primitive endings. Since electrical supramaximal stimulation will excite all afferent fibers simultaneously, antagonistic effects

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between IA and other afferents (11) may occur and result in less effective PAD. In contrast, stimulation of the anterior digastric nerve, which does not contain IA fibers from muscle spindles, will lead to excitation of proprioceptive fibers with synergistic functions, and hence to stronger PAD. Irigger; 0

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4. Effect of tension of the anterior belly of the digastric muscle on the excitability of lingual nerve terminals in the spinal trigeminal nucleus (nucleus oralis). The experimental arrangement is shown in the upper part of the figure. The mandible was rendered immobile by means of a tight string around the snout of the animal. Brisk tension of the anterior digastric muscle led to a brief burst of spikes (conditioning input) in the mylohyoid nerve (lower trace of C). The first spike triggered the lower beam of the oscilloscope and a delay unit. After a delay (conditioning interval) of 30 msec, the test stimulus was generated and delivered to nucleus oralis. The resulting antidromic potential was obtained from the lingual nerve and displayed on the upper beam of the oscilloscope (upper trace cf C ; generated 30 msec following the beginning of the lower beam). During contr& (no tension) or during moderate sustained tension of the anterior digastric muscle, the test stimuli were triggered externally. Discharges in the mylohyoid nerve and subsequent increases in amplitude of the antidromic spike were only observed during brisk tension (C), whereas no changes over the control value (A) were noted during moderate sustained tension of the anterior digastric muscle (B). Time bar : 2 msec for upper traces ; 10 msec for lower traces. Amplitude bars : 60 /.LLV for upper traces; 40 .UV for lower FIG.

traces.

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The question as to the type or types of proprioceptors in the anterior digastric muscle remains to be answered. The existence of Golgi tendon organs is likely ( 11) ; the presence of atypical endings is entirely possible. Our experiments (Fig. 4) showed that brisk tension of the anterior digastric muscle leads to a burst of discharges in the mylohyoid nerve (mylohyoid muscle denervated). Similar discharges are found in group IB afferents after relatively intense muscle stretch (6, 8, 11). Thus, it appears that proprioceptive organs with characteristics similar to those of tendon organs are located in the anterior digastric muscle. Brisk muscle stretch of the jaw elevator muscles produced a burst of discharges in the trigeminal ganglion. whereas no discharges were ohserved during moderate sustained tension (Fig. 3). Thus, regular rhythmic spindle discharges which are typically produced by moderate sustained muscle stretch (6) were not recorded from the trigeminal ganglion. These ohscrvations suggest that the proprioceptive afferent activities recorded from the trigeminal ganglion did not originate from neuromuscular spindles. This assumption is in agreement with the proposed concept that the somata of certain afferent fibers, other than those from muscle spindles, are located in the trigeminal ganglion (17). We cannot state with certainty that group IB fihers from tendon organs are solely or partially involved in the observed lingual and glossopharyngeal PAD. The participation of group II or group III afferents in this masseterically induced process cannot he excluded. In fact, Nakamura and 1Vu (IO) hold these types of afferents responsible for preterminal depolarization of lingual nerve fihers. It can he inferred from our experiments that during mastication proprioceptive afferent activities from masticatory muscles reach the hrain stem and induce presynaptic depolarization of the central terminals of lingual and glossopharyngeal nerve fillers. Thus, tongue reflexes elicited by lingual or glossopharyngeal input should he presynaptically inhibited during mastication. This postulate is also supported hy out previous work (13). The inhibition of lingually and glossopharyngically induced reflexes to the tongue protruder (genioglossus) is of particular importance in order to avoid injuries to the tongue during mastication. Addendum

Recently Smith (Smith, R. D. 1969. Location of the neurons innervating tendon spindles of masticator muscles. E‘xptl. .2Tr~r~ol. 25: 646-654) concluded that, in the cat, cell bodies of afferent neurons from tendon organs of the masseter muscleare located in the trigeminal mesencephalic nucleus. This conclusion is not incompatible with our finding that spikes could be recorded from the trigeminal ganglion during brisk depression of the mandible (Fig. 3). The reasons for this statement are as follows :

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(1) Only afferents from tendon organs of the masseter muscle were investigated by Smith. In our experiments (Fig. 3), additional proprioceptive input from other jaw elevators (medial pterygoid ; temporalis) must be considered. (2) There is no evidence that all cell bodies of tendon organ afferents are located in the trigeminal mesencephalicnucleus. (3) It is possible that the spikes recorded from the trigeminal ganglion (Fig. 3) were obtained from afferent fibers merely traversing the ganglion. (4) As pointed out in the discussion, it is conceivable that the discharges recorded from the trigeminal ganglion originated in group III afferents. References

1. BAUM, J. 1900. Beitrige 2. 3.

zur Kenntnis der Muskelspindeln.

Anat. Hefte

Abt.

1, 13 :

249-30s. CORBIN, K. CORBIN, K.

B. 1942. Probst’s tract in the cat. J. Camp. Neural. 77: 455467. B., and F. HARRISON. 1940. Function of mesencephalic root of fifth cranial nerve. J. Neztrophysiol. 3: 423-435. 4. DECIMA, E. E. 1969. An effect of postsynaptic neurons upon presynaptic teminals. Proc.

Nat.

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63:

58-64.

5. HOSOKAWA, H. 1961. Proprioceptive innervation of striated muscles in the territory of the cranial nerves. Tex. Rej. Biol. Med. 19: 405-464. 6. HUNT, C. C., and S. W. KUFFLER. 1951. Stretch receptor discharges during muscle contraction. J. Physiol. London 113: 298-315. 7. JERGE, C. R. 1962 Organization and function of the trigeminal mesencephalic nucleus J. Neurophysiol., 26 : 379-392. 8. MATTHEWS, B. H. C. 1933. Nerve endings in mammalian muscle. J. Physiol. London 76 : l-53. 9. MIZUNO, N., and E. K. SAUERLAND. (in press, 1970). Trigeminal Proprioceptive projections to the hypoglossal nucleus and the cervical ventral gray column. J. Camp. Neurol. 10. NAKAMURA, Y., and C. Y. Wu. (in press, 1970). Presynaptic inhibition of jaw opening reflex by high threshold afferents from masseter muscle of cat. Brain Res.

11. PATTON, H. D. 1965. Reflex regulation of movement and posture, pp. 181-206. Zn “Physiology and Biophysics.” T. C. Ruth and H. D. Patton teds.] W. B. Saunders, Philadelphia. 12. RAM~N Y CAJAL, S. 1909. “Histologie du Systeme Nerveux de I’Homme et des VertCbrCs,” Vol. 1. A. Maloine, Paris. 13. SAWERLAND, E. K., and N. MIZUNO. 1969a. Effect of trigeminal proprioceptive input on the linguo-hypoglossal reflex. Anat. Rec. 163: 322-323. 14. SAUERLAND, E. K., and N. MIZUNO. 1969b. Cortically induced presynaptic inhibition of trigeminal proprioceptive afferents. Brain Res. 13: 556-568. 1.5. SAUERLAND, E. K., N. MIZUNO, and R. M. HARPER. (1970). Presynaptic depolarization of trigeminal cutaneous afferent fibers induced by ethanol. Erp. Neural. 27 : 1232. 16. SMITH, R. D., H. Q. MARCARIAN, and W. T. NIEIIEX. 1967. Bilateral relationships of the trigeminal mesencephalic nuclei and mastication. J. Comb. Neural. 131: 79-92.

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17. SMITH, R. D., H. Q. MARCARIAN, and W. T. NIEMER. 1968. Direct projections from the masseteric nerve to the mesencephalic nucleus. J. Cowp. Ncnrol. 133: 495-502. 18. SZENTACOTHAI, J. 1949. Anatomical considerations of monosynaptic reflex arcs. J. ,Vcwophysiol. 11 : 445354. 19. THELANIIER, H. E. 1924. The course and distribution of the radix mesencephalica trigemini in the cat. J. Courp. iVfu~o1. 37 : 207-220. 20. \\‘ALL, P. D. 1958. Excitability changes in afferent libre terminations and their relation to slow potentials. J. Physiol. Londo~r. 142 : l-21.