Discharge patterns of hypoglossal afferents in a cat

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539

Discharge patterns of hypoglossal afferents in a cat In the previous paper 10 we reported that the activity of a few neurons in the cat hypoglossal nucleus was influenced by forward stretch of the tongue. This finding indicates the possible existence of afferent fibers that transmit impulses from some mechano-receptors in the tongue muscle to the brain. The question remains, which are the nerves responsible for these afferent discharges. Several authors have reported the existence of mechano-receptive afferent fibers in the lingual nerve1,9,10, ~s, in the glossopharyngeal nerveg, ~0, and in the hypoglossal nerve2,4, s. The present experiments identify the response of afferent fibers in the hypoglossal nerve by stretch of the tongue. Some physiological properties of these nerve fibers are analyzed. The experiments were performed under pentobarbital anesthesia (Nembutal, 40 mg/kg, i.p.) in 13 cats. After an animal was fixed in a supine position, the hypoglossal nerve was exposed by the ventral approach. To exclude the possibility of recording from the peripheral connection between the lingual and hypoglossal nerves 6, the latter nerve was sectioned about 15 mm proximal to where the nerve divides into two branches. The cut peripheral end of the hypoglossal nerve was carefully isolated under observation through a stereoscopic microscope to provide a functional single unit of the nerve fiber. A monopolar silver wire electrode 000/zm) was used for recording nerve discharges, and a small silver plate (7 m m × 7 mm) was fixed to the surrounding tissue as an indifferent electrode.

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Fig. 1. Samples of discharge patterns of hypoglossal afferent fibers which respond to stretch of the tongue. A, In response to stretch of the tongue, afferent fibers increased the firing frequency. On release of the stretch, the frequency of discharge of the units often fell slightly below the resting rate. This type of fiber showed continuous and regular spontaneous discharges at rest. 28 units out of 35 recorded belonged to this type. B, A few fibers were highly sensitive to stretch of the tongue. On release of the stretch, there was a short pause. C, Several fibers showed irregular and low frequency discharges responding to stretch. These units had few irregular spontaneous discharges.

Brain Research, 35 (1971) 539-542

540

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With a surgical thread, the tip o f the tongue was connected to a force displacem e n t transducer ( N i h o n K o d e n SB-IT) or to the m i c r o m a n i p u l a t o r which was used as a puller a n d could measure accurately the length of stretch o f the tongue. F o r p r o d u c i n g active tongue contraction, electrical stimulation was applied to the cut peripheral end o f the hypoglossal nerve t h r o u g h a sleeve stimulating electrode or directly to the tongue muscle t h r o u g h a pair o f needle electrodes inserted into the tongue. Succinylcholine, which fires muscle spindles selectively7, was injected t h r o u g h a c a n n u l a inserted in the left femoral vein. Artificial ventilation was used. I n the hypoglossal nerve o f a cat, some fibers showed s p o n t a n e o u s discharges which were either regular a n d c o n t i n u o u s or sporadic. The rates of these discharges 3 1oo

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Fig. 2. 1, Frequency of discharges of units plotted against extension of the tongue in ram. Ordinate, impulse frequency; abscissa, extension length of the tongue. A, B, and C represent each type of fiber shown in Fig. 1.2, Effect of succinylcholine (100/tg/kg). In type B fibers and some type A fibers, the rate of discharge frequency was increased, but in type C fibers, succinylcholine had no effect. Time calibration: 1 sec. 3, Active tongue contraction, produced by electrical stimulation of the cut peripheral end of the hypoglossal nerve, suppressed the firing of spontaneous discharges of one of type A fiber. The left column is a control record and the right column shows the effect of electrical stimulation. In each record, the lower trace is a nerve fiber activity, and the upper is a mechanogram recording, downward deflection showing tongue muscle contraction. Time calibration: i00 msec. 4, The peakto-peak duration of the recorded diphasic potential is the conduction time of impulse transmission from one pole to another. Potentials were recorded on moving film. Time calibration: 1 msec.

Brain Research, 35 (1971) 539-542

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were changed by stretching the tongue. Sample records of the responses of these fibers are shown in Fig. 1. Records were obtained from 35 single units. Twenty-eight units of the 35 stretch-sensitive fibers had regular and continuous spontaneous discharges with 13-46 imp./sec. The frequency of discharges increased with increasing tongue stretch, as illustrated in Fig. 1A. These units showed no apparent dynamic phase, and, when the tongue was held at a certain length of stretch, the rate of discharge remained constant; that is, these discharges were slow to adapt. No silent period was seen after the stretch was released, but the discharge frequency was slightly below the resting rate before return to its initial frequency. In Fig. 2 la the discharge rate of this type of unit at a time 4-5 sec after the onset of stretch is plotted against stretch of the tongue in ram. The average frequency of these units per mm stretch was 1.2 imp./mm (0.8-1.9 imp./mm). Evidently these units were less sensitive than spindle afferents of limb muscles. Injection of succinylcholine chloride (100 #g/kg) into the femoral vein produced a slight increase of discharge frequency of some of these fibers (Fig. 2 2A). Active tongue muscle contraction induced inhibition of spontaneous discharges in 8 units, and, during a recovery phase after the contraction, there was a transient increase of spikes (Fig. 2 z). For measuring approximate conduction velocity, the bipolar recording method was used. In this method, action potentials are recorded as diphasic potentials, and the peak-to-peak duration of the potential is considered as the conduction time for impulse transmission from one pole to another (5 mm). The average conduction velocity thus obtained from 7 units was 21.5 m/sec (16.5-28.5 m/sec). The above-described properties of these fibers are similar to the afferents from secondary endings of the limb muscle lz, although the conduction velocity is slower than that of Group II fibers. Three of the 35 fibers showed some resemblance to Group Ia fibers, and they had a short period of silence on release of stretch (Fig. 1B). The threshold of these units was very low, and discharges were increased by only 1 mm stretch of the tongue from the initial position. These were highly sensitive to stretch, and the maximal increase of one of them was 10 impulses per 1 mm stretch (Fig. 2 1B). The firing frequency was distinctly increased by administration of succinylcholine (100 #g/kg) (Fig. 2 2B). Active tongue contraction also induced inhibition of spontaneous discharge of one of this type of fiber. These properties of the fiber are similar to the stretch-sensitive unit in the hypoglossal afferent reported by Hanson and Wid6n s who strongly suggest that this type of fibers were from muscle spindles. The discharge patterns of the remaining 4 units were different from the abovedescribed units. Three of these 4 units had sporadic spontaneous discharges and showed irregular and very low frequency discharge in response to stretch of the tongue (Fig. 1C). The average frequency of these units to stretch length was 0.8 imp./mm. Another one had no spontaneous discharges but responded to strong tongue stretch. The threshold of this fiber was high, and 6 mm stretch was necessary to produce rapidly adapting discharges. The discharge pattern of this fiber was similar to that of Group III fibers induced by stretch 14. Succinylcholine did not affect

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this t y p e o f fiber, and active c o n t r a c t i o n o f the t o n g u e muscle also h a d no effect on this type o f fiber. O u r present results suggest that there are at least 3 types o f afferent fiber in the h y p o g l o s s a l nerve t h a t r e s p o n d to stretch o f the tongue. Discharge p a t t e r n s o f m o s t o f the stretch-sensitive units o b t a i n e d in this e x p e r i m e n t resemble those o f muscle spindles. H o w e v e r , m a n y previous papersZ,4,12,16, with the exception o f L a n g w o r t h y ' s 1-1, have r e p o r t e d t h a t there were no muscle spindles in the tongue muscles o f the cat. Therefore, it is a s s u m e d t h a t afferent fibers f r o m atypical p r o p r i o c e p t o r s in the tongue show similar discharge p a t t e r n s to those o f the spindle afferents o f the l i m b muscles, in a m a n n e r similar to afferents f r o m the e x t r a o c u l a r muscle in the cat r e p o r t e d by C o o p e r a n d FillenzL The physiological basis o f the l o w sensitivity o f m a n y fibers to tongue stretch is n o t clear. T h e direction o f the stretch m a y be concerned with this p h e n o m e n o n because some afferent fibers in the hypoglossal nerve o f a m o n k e y r e s p o n d better to lateral stretch t h a n to a n t e r o - p o s t e r i o r stretch 3. A s we could n o t recognize a n y stretch-sensitive units after dissection o f the lateral b r a n c h o f the h y p o g l o s s a l nerve in 4 cats, the units r e c o r d e d in the experiments m a y have been o b t a i n e d f r o m the lateral b r a n c h which innervated the tongue retractive muscles, such as the styloglossa! a n d h y p o g l o s s a l muscles. Department of Oral Physiology, Dental School, Osaka University, Kitaku, Osaka (Japan)

TOSHIFUMI MORIMOTO YOJIRO KAWAMURA

I BARRON,D. H., A note on the course of the proprioceptor fibers from the tongue, Anat. Rec., 66 (1936) 11-15. 2 BLOM, S., Afferent influences on tongue muscle activity, Aetaphysiol. stand., 49, Suppl. 170 (1960) 1-97. 3 BOWMAN,J. P., AND COM~S, C. M., Discharge patterns of lingual spindle afferent fibers in the hypoglossal nerves of the rhesus monkey, Exp. Neurol., 21 (1969) 105-119. 4 COOPER,S., Afferent impulses in the hypoglossal nerve on stretching the cat's tongue, J. Physiol. (Lond.), 126 (1954) 32P. 5 COOPER, S., AND FrLL~NZ, M., Afferent discharges in response to stretch from the extraocular muscle of the cat and monkey and the innervation of these muscles, J. Physiol. (Lond.), 127 (1955) 400-413. 6 F~TZGERALD,M. J. T., AND LAW, M.E., The peripheral connections between the lingual and hypoglossal nerve, J. Anat. (Lond.), 92 (1958) 178-188. 7 GRANIT, R.~ The Basis o f Motor Control, Academic Press, London, 1970, p. 61. 8 HANSON,J., AND Wm~N, L., Afferent fibers in the hypoglossal nerve of cat, Aeta physioL stand., 79 (1970) 24-36. 9 KAWAMURA,Y., FUNAKOSHI,M., NISHIYAMA,T., AND MAMMA,T., Afferent impulses from tongue for autogenetic regulation of tongue muscle activity, J. physiol. Soe. Japan, 27 (1965) 436-445. 10 KAWAMURA,Y., FUNAKOSH1,M., NISHIYAMA,T., AND MORIMOTO,T., Auto-regulatory neuromechanism of the tongue muscle activity, Jap. J. Physiol., 17 (1967) 123-134. I 1 LANGWORTHY,O. R., A study of the innervation of the tongue musculature with particular reference to the proprioceptive mechanism, J. comp. NeuroL, 36 (1924) 273-297. 12 LAW, M. E., Lingual proprioception in pig, dog and cat, Nature (Lond.), 174 (1954) 1107-1108, 13 MATTHEWS,P. B. C,, Muscle spindles and their motor control, PhysioL Rev., 44 (1964) 219--288. 14 PAtNTaL,A. S., Functional analysis of Group III afferent fibers of mammalian muscles, J. Physiol. (Lond.), 152 (1960) 250-270. 15 PORTER,R., Lingual mechanoreceptors activated by muscle twitch, J. Physiol. (Lond.), 183 (1966) I01-111. 16 SHERRINGTON,C. S., On the anatomical constitution of nerves of skeletal muscles: with remarks on recurrent fibers in the ventral spinal cord, J. Physiol. (Lond.), 17 (1894) 211-258. (Accepted October 12th, 1971)