Reflexes with intraoral afferents in human lip musculature

EXPERIMENTAL

Reflexes

NEUROLOGY

with

37,

179-187

Intraoral

(1972)

Afferents iif..

in Human

Lip Musculature

BRATZLAVSKY~

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The effect of intraoral stimuli on the lip musculature was studied in healthy subjects and in patients with an unilateral retrogasserian neurotomy. A brisk tap of the tongue surface, predominantly near its tip, evoked in the m. orbicularis oris an uncrossed reflex response with a latency of 11-15 msec. It was not affected by anesthesia of the tongue surface but abolished after lingual nerve anesthesia. It was concluded that deep submucosal mechanoreceptors of the tongue are responsible for this reflex. During voluntary activation of the m. orbicularis oris, a powerful facilitation of this reflex was noticed, which seemed not attributable to the cortical depolarization of the corresponding motoneurons. It was postulated therefore that the cortical inputs excite interneurons of the reflex path. Lingual nerve anesthesia failed to produce a substantial alternation of the pattern of activation of the m. orbicularis oris during chewing. Besides this early reflex response, a crossed reflex, with a variable latency of between 28 and 80 msec, was elicitable in the m. orbicularis oris upon nociceptive stimulation of the intraoral mucosa especially in areas exposed to external noxious stimuli. Introduction

The oral motor functions in man which are concerned with the production of speech, mastication, and the initial stage of deglutition. require highly coordinated tnovements of the tongue, jaws, and lips, It has been known for a long time that some basic patterns of chewing and swallowing are reflex in nature. In cats the tongue and jaw muscles are controlled by exteroceptive oral afferents, through the lingual and glossopharyngealhypoglossal reflexes (4, 5, 34, 40) and through the lingual-mandibular reflexes (17, 18, 32, 44, 47) which have also been reported in man ( 10. 25 ). Besides the neural information from the cutaneous input from orofacial areas, reflex integration of oral motor activities is mediated by periodontal ligament and tooth pulp afferents (3, 16. 22, 28 31), by vagal afferents (11) and by the proprioceptive input from jaw muscles (35, 37. 41-43, 45, 46), from the temporomandibular joint (20) and probably from tongue muscles as well (19, 36, 38). Most of the available experimental data con1 This Scientific

work was Research.

supported

by a grant

<‘opyrIght All rights

0 1972 by .Academic Press, of reproduction in any form

from

179 Inc. reserred.

the Belgian

National

Foundation

for

180

BRATZLAVSKY

cerning this subject has dealt with jaw and tongue musculature and no studies have been reported to our knowledge on influences on the lip musculature. Since closure of the mouth is an important activity during mastication, the present study was undertaken to find out whether the perioral facial muscles were involved in some reflex mechanisms arising at an intraoral level. The results presented in this paper show that the buccal cavity is the afferent source of at least two different reflex responses in the human m. orbicularis oris. Their origin and possible function are briefly discussed. Methods

Fifteen healthy subjects and six patients with an unilateral retrogasserian neurotomy (performed for release from severe trigeminal neuralgia) were examined in a room which had a temperature of 23 C. During the examination the patients were asked to stick out their tongue which was held between the examiner’s thumb and index finger while mechanical stimulation of the tongue was performed by tapping its surface. Other mechanical stimuli included sustained pressure of the tongue between two fingers and stretching the tongue. The taps were given with a reflex hammer which triggered the suppressed sweep of a cathode ray oscilloscope at the moment of contact with the tapped area. Electrical stimulation of intraoral afferents was performed with single shocks of 1-msec duration and of 5- to 90-v intensity. The shocks were delivered through a bipolar percutaneous electrode or through a pair of steel needles inserted into the tongue approximately 2 cm apart to a depth of about 5 mm. In four subjects the lingual nerve was infiltrated with 4 ml xylocaine 270 and in five subjects a superficial tongue anesthesia was performed with a xylocaine spray 10%. The evoked responses were recorded with coaxial needle electrodes inserted into the m. orbicularis oris at the level of the corner of the mouth. The evoked and voluntary muscular activities were displayed on the oscilloscope of a Medelec MS6 electromyograph and filmed on a direct print paper. Results

L\ tap on the tongue elicited in the m. orbicularis oris a reflex response with a latency of between 11 and 15 msec and a duration of 6-15 msec (Fig. 1A). It was most easily evoked by taps near the tongue tip. No appreciable decrement in the response was noticed during continuous stimulation for 10 set at a frequency of 1-2 /sec. Application of lOy$ xylocaine to the tongue surface so as to just eliminate tactile sensation did not abolish the reflex. Neither sustained pressure on the tongue nor low-intensity electrical stimulation of the tongue surface with single shocks was successful in evoking this reflex response. It could, therefore, be assumed to origi-

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FIG. 1. Reflex responses recorded with coaxial needle electrodes in the m. orbicularis oris of a healthy subject. (A) Weak tap on the tongue with the m. orbicularis oris relaxed (R) and during its voluntary activation (V). (B) Weak tap on the tongue during sustained moderate activation of the m. orbicularis oris: in 1 before and in 2 after a homolateral lingual nerve anesthesia. (C) Electrical stimulation of the intrinsic tongue muscle through steel needles, with the IN. orbicularis oris relaxed t R) and during its voluntary activation (V). (D) Repeated painful electrical stimulation of the tongue surface at a frequency of l/set.

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nate in deeply located rapidly adapting mechanosensitive units. Since muscle spindles have been observed in both the extrinsic and intrinsic tongue muscles of primates (6, 12, 48), the question arose as to whether they contributed to this reflex. Although the exact pathway of the lingual proprioceptive afferents in man is not yet clear, the work of several investigators (1, 49) indicates that these afferents travel in the hypoglossal nerve beyond its connection with the lingual nerve (15). Experimental data supporting this assumption were reported in monkeys (7, 8, 13). In the present study an unilateral lingual nerve anesthesia caused the reflex response to disappear in the homolateral m. orbicularis oris (Fig. lB), and in patients with an unilateral retrogasserian neurotomy the reflex was abolished on the operated side. This indicates its uncrossed character and allows us to exclude with some certainty the participation of tongue spindles in its elicitation. Proprioceptive inflow from the tongue muscles could not in fact play any important role as the reflex was easily elicitable by short taps applied on the tongue tip in the axial direction of the tongue ; this procedure leads to no stretching of the intrinsic tongue muscles. Muscle spindles are very few in number at the level of the tongue tip (12). Effective stretching of the tongue, on the other hand, was unable to evoke any reflex response. Furthermore, a clear reflex response could be often induced in the m. orbicularis oris (with an increased latency of between 15 and 22 msec) by active contraction of the intrinsic tongue muscles following electrical stimulation through needle electrodes inserted into the tongue or strong percutaneous tongue stimulation (Fig. 1C). A powerful facilitation of this “linguolabial” reflex was observed during voluntary activation of the m. orbicularis oris (Fig. lA, C). It appeared to be an essential feature of this reflex since it was frequently either abolished or only abortively elicitable when the m. orbicularis oris was completely relaxed. No such facilitatory effect was noticed upon the early reflex component evoked in the m. orbicularis oris by perioral mechanical or electrical stimulation (14)) which is likely to have a cutaneous origin (9). This makes it improbable that the depolarization of the m. orbicularis oris motoneurons by the cortical inputs is the chiefly involved mechanism of the observed facilitation. The physiological EMG activity of the m. masseter and the m. orbicularis oris has been studied during the active phase of chewing in an attempt to evaluate the importance of this “linguolabial” reflex. Both muscles usually exhibited a rythmical alternating pattern of activity (Fig. 2). The temporal sequence and the duration of the bursts of activity were less rigid in the m. orbicularis oris than in the m. masseter and on rare occasions coactivation of both muscles could even be noticed. Some background activity often persisted in the m. orbicularis oris between two bursts, con-

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MUSCLE

FIG. 2. EMG activit:recorded during chewin g in the tn. masscter m. orhicularis oris (0.0.) on the right (R) and on the left (L) subject after a right lingual nerve anesthesia.

183

(X.) and in the side in a healthy

trasting with the clear motor pauses in the m. masseter whose close relationship with tooth-contact has been demonstrated (2, 21, 23). In both muscles the duration of the bursts varied between 200 and 500 msec and the motor pauses lasted 300-700 msec. When comparing the right and the left side after an unilateral lingual nerve anesthesia there was never any visible impairment of this temporal pattern, and as shown in Fig. 2 the activation of the m. orbicularis oris during chewing was apparently LUchanged on the anesthetized side. Painful electrical or mechanical stimulation of the anterior tongue mucosa and of the mandibular and masillar labial gums evoked in both the ipsilateral and contralateral m. orbicularis oris a reflex response with a variable latency of between 28 and 80 msec, lasting S-40 msec (Fig. 1D). It showed habituation when evoked repeatedly (Fig. 1D) and it was clearly potentiated by fear of a painful stimulus. In patients with an unilateral retrogasserian neurotomy it was abolished when the stimulus was applied on the operated side. This reflex seemed thus mediated by nociceptive trigeminal afferents with bilateral projection. In the same way as the early refles response described above, it showed a strong facilitation during voluntary activation of the m. orbicularis oris. A similar late reflex response appeared to he evokable upon stimulation of the entire intraoral mucosa. but its threshold raised markedly in areas other than the anterior tongue mucosa and the labial gums. Discussion

The present investigation has shown that the human tongue, predominantly near its tip, is the afferent source of a short latency reflex response in the m. orbicularis oris. The adequate stimulus to evoke this reflex seems

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to he a brisk distortion of the tongue surface consecutive either to an esternal pressure stimulus or to a tongue movement. The reflex is uncrossed and reaches the brain stem through the trigeminal sensory root. Since its latency exceeds that of the monosynaptic jaw jerk (29) by several msec, it appears to have a polysynaptic pathway. It may be attributed to escitation of deep probably submucosal, mechanoreceptors since it is not affected by anesthesia of the tongtie surface but abolished after lingual nerve anesthesia. No evidence has been obtained for the participation of lingual muscle spindles or chorda tympani fibers in this reflex. Afferent impulses triggered by mechanoreceptors situated in the submucosa of the tongue, sensitive both to pressure stimuli and to phasic movements of the tongue, were recorded in the lingual nerve of cats by several authors (4. 39). Their possible role in the reflex control of tongue movements has been emphasized (4, 26, 39) particularly in view of the lack of tongue muscle spindles in this species (4, 12, 30). The present results suggest that similar reflex mechanisms exist in man and thus contradict the assumption which tends to ascribe to the afferent message of the tongue muscle spindles in primates (6, 12, 48) an exclusive proprioceptive function ( 7 ). Impulses behaving like muscle spindle afferents were recently reported in the cat’s hypoglossal nerve (24, 33, SO), the possibility being excluded of recording from peripheral connections with the lingual nerve (15). In the light of the earlier experimental data these findings support the view that in cats both deep submucosal mechanoreceptors and mechanoreceptors situated in the tongue muscle itself (30) participate in the reflex control of oral motor activities. A possible function of the present linguolabial reflex could be to control the activity of the m. orbicularis oris during chewing. This may esplain its strong facilitation during voluntary activation of this muscle. Our results suggest that there is a specific spatial convergence of the excitatory impulses from the cortex and from the tongue mechanoreceptors involved in this reflex and its seems justifiable therefore to make the assumption that impulses in the pyramidal tract excite interneurones of the refles path. The experiments with lingual nerve anesthesia have not revealed any significant impairment of the mode in which the m. orbicularis oris and the m. masseter are activated during chewing, failing thus to provide evidence that this reflex is of dominating importance for activation of the tn. orbicularis oris. These negative findings do not exclude that the reflex plays a role in chewing, since there can be several systems which overlap in the muscular control. Besides this early reflex a crossed, less synchronized. excitatory response with longer latency could be evoked in the m. orbicularis oris LIpon nociceptive stimulation of the intraoral mucosa. Nociceptive \vithdrawal re-

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flexes arising in the buccal cavity have been described in hypoglossal motoneurons (24) and in jaw muscle motoneurons (25, 27, 31, 47). Although stimulation of the A delta fibers in the tooth pulp nerve does not evoke any refles response in the facial musculature (27), facial motoneurons were shown to respond to stimulation of similar fibers in the hypoglossal nerve (24j. The optintal area of elicitation of the present reties was the anterior tongue mucosa and the labial gums, suggesting that it is organized to protect intraoral structures against external noxious stimuli. References 1.

2. 3. 3. 5. 6. 7.

S. 9.

10. 11. 12. 13. 14. 15. 16. 17.

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KELLER, O., L. VYKLICKY, and E. SYKOVA. 1972. Reflexes from A delta and A alpha trigeminal afferents. Brain Res. 37 : 33b-332. KIDOKORO, Y., K. KIJBOTA, S. SHUTO, and R. SUMINO. 1968. Reflex organization of cat masticatory muscles. J. Nezcrophysiol. 31: 695-708. KUGUBERG, E. 1952. Facial reflexes. Brain 75 : 385-396. LAW, M. E. 1954. Lingual proprioception in pig, dog, and cat. Nature (Lortdon) 174 : 1107-1108. MAHAN, P. E., and K. V. ANDERSON. 1970. Jaw depression elicited by tooth pull stimulation. Exp. Newel. 26 : 439-448. MILLER, F. R., and C. S. SHERRINGTON. 1916. Some observations on the bucco. pharyngeal stage of reflex deglutition in the cat. @tart. J. Exp. Physiol. 6 147-186. MORIMOTO, T., and Y. KAWAMURA. 1971. Discharge patterns of hypoglossal affer ents in a cat. Brain Res. 35 : 539-542. MORIMOTO, T., M. TAKATA, and Y. KAWAMURA. 1968. Effect of lingual nerv stimulation on hypoglossal motoneurons. Exp. Nerrrol. 22 : 174-190. NAKAMURA, Y., and C. Y. WV. 1970. Presynaptic inhibition of jaw opening refle: by high threshold afferents from the masseter muscle of the cat. Brain Res. 23 193-211.

NAKAMURA, Y., L. J. GOLDBERG,N. MIZUNO, and C. D. CLEMENTE. 1970. Masse teric reflex inhibition induced by afferent impulses in the hypoglossal nerve Brain Res. 16 : 241-25.5. 37. NAKAMURA, Y., C. Y. WV, H. NAGASHIMA, and S. MORI. 1971. Bilaterally sym metrical effects of high threshold afferents from the masseter muscle on the jai movement. Brain. Res. 26: 200-203. 38. PORTER, R. 1965. Synaptic potentials in hypoglossal motoneurones. J. Physio 36.

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