EXPERIMENTAL
NEUROLOGY
Sensory
59,
137-145 (1978)
Fibers in the Nerve and their Functional TADAAKI
Department
SUMI
of the Jaw Opening Property in Rabbits AND SOTARO HANAI
of Physiology, Fujita-Gakucn Toyoake, Nagoya
Received
Allgust
10,1977;
Universiry School 4iO-11,
Muscles
1 of Medicine,
Japan
revision received October
17,1977
In anesthetized and immobilized adult rabbits, the peripheral stump of the mylohyoid nerve innervating musculus mylohyoideus and musculus digastricus was isolated and the activity recorded from its constituent single fibers. The fibers originated from sensory receptors in the skin, muscles, or other noncutaneous structures. The cutaneous afferent fibers had receptive fields of 11 mm’ (average value) distributed roughly in the area covering the relevant muscles. They responded readily to air-blowing, light touch, and/or pressure whereas the muscular afferent fibers responded to stretch of either of the jaw opening muscles. The latter fibers were classified into three groups: (i) low-threshold, tension-dependent, slowly adapting units; (ii) highthreshold, tension-velocity-dependent, rapidly adapting units ; and (iii) “on-otY units. The physiologic significance of these sensory fibers is discussed in relation to the type of their receptors as well as to their central linkages in the brain stem.
INTRODUCTION It is widely believed that the rhythmic activity of mastication originates primarily from the “chewing center” in the brain stem (4, 17). However, the activity has also been considered to be produced through feedback from the jaw opening and closing muscles: The proprioceptive afferents of each functional group of muscles activate the synergic motoneurons, while inhibiting the antagonistic motoneurons, thus leading to reciprocal, rhythmic sequencesof excitation and inhibition of the two jaw muscles (8, 10, 12, 14). In fact, many tension receptors are found in the jaw 1 Thanks are extended to Prof. Robert W. Doty of the University of Rochester for giving suggestions and criticisms, and reading the earlier draft of the manuscript. This investigation was supported in part by a grant in aid for Scientific Research from the Educational Ministry of Japan. 137 0014-4886/78/0591-0137$02.00/O Copyright 0 1978 by Academic Press, Inc. All rights of reproduction in any form reserved.
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closing muscles (6) ; their afferent fibers intermingle with efferent fibers to the muscle (19). On the other hand, there is no or very little evidence for the existence of afferent fibers in the nerves arising from the jaw opening muscles, viz., the digastricus, mylohyoideus, and geniohyoideus (1, 19). In none of these muscles have the tension receptors been fully confirmed histologically (10). However, recent investigations clearly indicate that centripetal stimulation of the mylohyoid nerve inhibits hypoglossal motoneurons (21) and also modifies cortically evoked rhythmic jaw movements (IS). In addition, a brief burst of spikes is produced in the cat mylohyoid nerve only by brisk stretch of the anterior digastric muscle (13). These facts prompted us to examine more fully whether or not sensory fibers exist in the nerve from the jaw opening muscles and, if so, what their origin and nature might be. METHODS Twenty-two adult rabbits, weighing 2.5 to 3.0 kg, were used. They were anesthetized initially with ethyl urethane (1 g/kg, intramuscularly) or with sodium pentobarbital (30 to 50 mg/kg, intraperitoneally. Supplemental anesthesia was administered as necessary. Thirteen of the anesthetized animals were immobilized by gallamine triethiodide (3 mg/kg, intravenously) and respiration was maintained artificially through the tracheal cannula. The animal was placed laterally on a table and the jaws were fixed rigidly with clamps and bars. The masseter muscle and the lower jaw were partially removed unilaterally. The mylohyoid nerve, a branch of the inferior alveolar nerve, was isolated and severed near the bifurcation from the parent nerve trunk. The cutaneous edge along the incision was elevated to form a trough and filled with liquid paraffin kept at 34 to 38°C by an infrared light. After identifying the nerve branch by direct observation of contraction, produced both in the mylohyoideus and in the digastricus by an electrical shock applied to the nerve, the distal end was dissected into single fibers with watchmaker’s forceps under microscopic control. Single nerve fibers were placed on a platinum wire electrode, and the electrical sign of the activity of the fiber was amplified, displayed on a cathode ray oscillograph, and photographed with a kymograph camera. The “indifferent” Iead was sewn subcutaneously around the wound and grounded. Auditory monitoring of the neural activity was used routinely. To determine the peripheral origin and the functional property of the nerve fibers, natural stimuli, such as bending hairs, air-blowing, or lightly touching the skin covering the locus of the jaw opening muscles, as well as pulling each of the muscles, were applied. The contour and extent of the
AFFERENT
B
FIBERS
FROM
---
JAW
OPENING
MUSCLES
139
-
------------------------
C D FIG. 1. Responses of cutaneous sensory fibers of the mylohyoid nerve to touch (A, B, and D) or air-blowing (C) on their receptive fields. Broken lines indicate the durations of cutaneous stimulations; horizontal bars, 0.5 s. Slowly adapting (A) or rapidly adapting (B) discharge to touch in each fiber; steady discharge to airblowing (C) ; “on-off” discharge to touch (D) in the same fiber.
cutaneous receptive field for individual fibers were traced with a small, blunt glass rod and drawn with India ink on the surface of the skin. After each experiment the drawing of the receptive fields were photographed and measured. To apply tension to the muscles, two threads, one attached to the caudal tendon of the digastric muscle and the other to the body of the hyoid bone, were pulled caudally with a force of 10 to 800 g. Using a strain-gauge amplifier, the forces thus applied to the muscle were recorded simultaneously with the activity of the nerve fibers. In two animals, the area and configuration of cutaneous receptive fields for L2 dorsal root fibers were similarly photographed and measured for comparison with those of the mylohyoid afferent fibers. RESULTS More than 100 afferent units were identified and successful records were obtained from 55 units, 35 of which responded to cutaneous stimulation, 10 to muscular traction, and 5 to unspecific, noncutaneous mechanical stimulation such as manipulation of the suprahyoid structures. In general, afferent fibers of cutaneous or muscular origin tended to be gathered respectively in the nerve bundle. Furthermore, the cutaneous fibers
140
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initiating from adjacent receptive fields also ran side by side in the nerve bundle. Responsive Properties and Receptive Field Organization of the Cutaneous Aterent Fibers. No spontaneous activity was observed in this type of afferent fiber, However, these fibers fired a burst of impulses when their receptive fields were stimulated with gentle air-blowing or touching. A repetitive application of the stimulus elicited a brisk burst discharge of impulses. Among those cutaneous afferent fibers, many units responded continuously but with a small decrease in the frequency of discharge (Fig. 1A), whereas several others responded only for a short period at the beginning of light continuous touch (Fig. 1B). In the same unit, a steady discharge (Fig. 1C) to air-blowing was converted into an “on-off” discharge (Fig. 1D) when a light touch was applied to its receptive field. Units with fast-adapting responses to touch discharged 300 or more impulses per second and possessed a small receptive field, very often consisting of a single spot or a few discrete spots, whereas units with slowly adapting responses discharged several tens of impulses per second and had a wider receptive area than did fast-adapting units. The cutaneous receptive fields in the ipsilateral suprahyoid area were delineated by the chin rostrally, the ventral edge of the mandible laterally, and the midline (Fig. 2). The distribution of receptive fields was dense around the center of the area, where many of these fields overlapped. The sizes of the receptive fields were spot-like to 100 mm2, with an average value of 11
FIG. 2. Receptive field organization of cutaneous sensory fibers of the left mylohyoid nerve in the rabbit. The area encompassed by the ,broken line denotes the approximate locus and extent of all receptive fields verified in this study. Dots and circles of various sizes and shapes indicate the receptive fields of single fibers confirmed in one animal.
AFFERENT
FIBERS
FROM
JAW
OPENING
141
MUSCLES
llllllllllc
loo-
.
50 og
50
. . 0-A
’
’
’
’
’
-
T
1
m
50 og
0
5
Time(sec)
10
r?g
FIG. 3. Responses of three sensory fibers of the mylohyoid nerve (upper right, traces of each record) to stretch of the digastric muscle at various strengths (lower right traces of each record calibrated by the scale). Time marks, 0.1-s divisions, In the upper left diagram, the number of impulses per second (ordinate) is plotted against tension (absicca). Plot A represents the unit of small-size spikes, whereas B represents that of medium-size spikes shown in the records to the right. In the lower left diagram, the number of impulses per second (ordinate) is plotted against the time after onset of traction (abscissa) for a unit of small-size spikes exclusively at three different strengths. mm2 for 30 units examined. However, because of methodological limitations, fields smaller than 1 mm2 could be defined only approximately. These values contrast with those obtained for the fields of cutaneous fibers at L2 dorsal roots, which were spot-like to 165 mm2, with an average of 78 mm2. Properties of Agerent Fibers Originating from Deep Structures. Eight afferent fibers found in the mylohyoid nerve trunk gave no response to cutaneous stimulation, but fired specifically and exclusively when the digastric or mylohyoid muscle was mechanically stretched. Both the threshold and the frequency of discharge attained at each intensity of muscular tension differed for each individual unit. In Fig. 3 three units recorded simutlaneously are shown : The unit of small spikes responded at first to tension of about 7.0 g with 16 impulses/s, the unit of middle-
142
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FIG. 4. Responses of a sensory fiber of the mylohyoid nerve (upper right traces of each record) to traction of the digastric muscle at various strengths (lower right traces of each record). Vertical scales are for calibration of tension. Time marks, 0.1-s divisions. In the diagram, the rate of discarge is plotted as a function of the time after onset of traction at three different strengths.
size spikes responded to 250 g with only a few impulses per second. Of these, small-spike and middle-spike units showed a linear relation between the rate of discharge of impulses and the logarithmic value of the tension applied (Fig. 3, A and B in upper left diagram). Other similar units revealed a comparable relation of impulses rate to tension as described above, except for differences in their thresholds. Therefore, when plots were made for these analogous units on the same scale, their lines of representation became parallel, i.e., they had the same slope. In each unit, however, the rate of discharge decreased very slightly after the onset, although the tension was kept constant for 30 s or longer. The decline in the rate of discharge was more obvious at the beginning of a stronger traction (Fig. 3, lower left diagram). Among the units responding to muscular stretch, several possesseda much higher threshold and a lower rate of discharge, even at maximum tension, than those described above, e.g., 250 g for the threshold and 7 impulses/s at 800 g for the unit of large spikes shown in Fig. 3. In units with a high threshold, the rate of discharge was relatively higher initially but rapidly reached its steady value, which varied roughtly with the tension applied (Fig. 4). The rate of discharge during the initial phase of muscular stretch generally depended on the strength of stretch, the rate of increase of tension, and the individual unit
examined.
In three units,
burst
discharges
of impulses
were
produced
only at the moment when stretch was applied or released, and there was no sign of activity during the period when tension was constant (Fig. 5). In these cases, the threshold exceeded 150 g. Corresponding to rhythmically repeated pulling and releasing of the muscle, as would occur actually during the jaw closing and opening of rhythmic mastication, all tension-sensitive units readily gave a rhythmic burst of impulses in phase with an increase
AFFERENT
-
FIRERS
FRO&~
JAW
OPENIKG
143
11~793,~~
500 og
FIG. 5. Example of an “on-off” response of a sensory fiber of the mylohyoid nerve to traction of the digastric muscle. The lower trace indicates the tension of traction calibrated by the scale attached. Horizontal bar 0.5-s. tension (jaw closing). The last type of unit fired in both phases at strong traction. Every unit fired in responseto pulling either the mylohyoid or the digastric muscle, and no unit discharged in response to the isolated manipulation of both muscles. In general, the threshold was lower for units responding to stretch of the diagasticus compared to stretch of the mylohyoid. DISCUSSION in
Abundant muscle spindles are present in the jaw closing muscles, viz., the masseter and the ptyerygoid (6). Sensory nerve fibers arising from these receptors intermingle with motor fibers in the same peripheral nerve trunk and run into the trigeminal mesencephalic tract nucleus where their cell bodies congregate (2). Near the cell bodies, their axons give off a branch which terminates on the motoneurons of jaw closing muscles, thus forming a monosynaptic reflex linkage between the sensory and the motor neurons concerned (7, 21). In the jaw closing muscles, the possible existence of tendon organs was also suggestedby a number of investigators (3, 15, 19) and confirmed directly by histology (10). However, in the jaw opening muscles, viz., the mylohyoid and the digastric, neither the spindles nor the tendon organs have been identified (6, 19). No degeneration of myelinated fibers is observed in the muscles after coagulating the ipsilateral trigeminal mesencephalic tract nucleus (19). These findings may be in line with previous results which show that no reflex effect can be produced either by stretch of the digastric muscle or by stimulation of the digastric nerve electrically (1). Apparently, the results presented in this paper disagree with those described above. This may be attributed to the paucity of such sensory nerve fibers (see Resultsj and presumably to the difference in species of animal studied. becausea few spindles are found in the anterior part of the digastric muscle in man (‘21). Therefore, because so few tension-sensitive afferent fibers exist in the jaw opening muscles, reciprocal inhibition, as seen between the extensors and the flexors of the limb (5), may be poorly expressed between the jaw opening and closing muscles. A slight inhibition of messeteric motoneurons can be produced only when the digastric muscle is pulled intensely (9). It may be tentatively inferred that the low-
144
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threshold, tension-dependent muscular afferents (Fig. 3) arise from muscle spindles: the high-threshold, traction-velocity-dependent unit (Fig. 4) from tendon organs; and the unit responding only at application and removal of the muscular stretch (Fig. 5) from other tension-sensitive receptors (such as those present in the fascia). A single electrical stimulus to the low-threshold afferents of jaw opening muscles exerts an inhibitory influence on the hypoglossal motoneurons in cats. The inhibition begins after a latency of 10 to 15 ms and lasts 200 ms or longer. From this evidence, a polysynaptic linkage is postulated for this inhibitory reflex (20). Stimulation with repetitive electrical pulses to the central stump of the mylohyoid nerve also modifies cortically evoked rhythmic jaw movements. The movement increases in rate and decreases in amplitude, and the lower jaw shifts toward opening (18). All these effects of stimulating the nerve trunk of the jaw opening muscles also indicate the existence of sensory fibers in the nerve concerned, although their peripheral origin would be heterogeneous as shown in the present study. In addition to the afferent fibers of the “deep receptor,” the sensory fibers arise clearly and abundantly from the surface of skin in the area roughly covering the mylohyoid and digastric muscles ipsilaterally (see Results). Judging from the relative richness of such afferent fibers and the long latency in the reflex effect of stimulating the nerve of the jaw opening muscle, the sensory fibers of cutaneous origin may play a major role in producing the modification of rhythmic jaw movements (18) and the inhibition of hypoglossal motoneurons (20). In fact, electrical stimulation of the same skin area produces an effect on the cortically evoked rhythmic jaw movement comparable to that produced by stimulation of the mylohyoid nerve (21). The relative smallnessof the cutaneous receptive fields of this nerve (11 mm?; seeResults) compared to those in the other areas, viz., a few square millimeters on hand and foot (ll), 53 mm2 on thorax (16), 78 mm? on abdominal wall (see Results), and more than 300 mm2 on trunk ( 1l), may imply higher sensory discrimination, becausethe area is close to the perioral region which is known to have high sensitivity. The locus of cell bodies for these sensory fibers which arise from the deep receptors or from the skin is still obscure, although the latter may more likely be the semilunar ganglion instead of the trigeminal mesencephalic tract nucleus. This question, however, requires further investigation. REFERENCES 1.
S,. 1960. Afferent influences on tongue muscle activity. Acta Physiol. Scud. : l-97. CROSBY, E. C., T. HUMPHREY, AND E. W. LAVER. 1962. Correlative Anatomy of the Nervous System, 1st ed. Macmillian, New York. BLOM,
[supp1.]49
2.
AFFERENT
3. 4.
5. 6.
7. 8. 9.
10. 11. 12. 13. 14. 15. 16. 17. 18.
FIBERS
FROM
JAW
OPENING
MUSCLES
145
DALE, SMITH, R. 1969. Location of the neurons innervating tendon spindles of masticator muscles. Exp. Nrurol. 25 : 64M54. DELLOU’, P. G., AND J. P. LUND. 1971. Evid,ence for central timing of rhythmical mastication. J. Physiai. (Lotdow) 215 : l-13. ECCLES, J. C. 1957. The Physiology of Nerve Cells, 2nd ed. Johns Hopkins Press, Baltimore. FREIMANN, V. R. 1954. Untersuchungen iiber Zahl und Anordnung der Muskelspindeln in den Kaumuskefn des Menschen. Agzat. -4.1~. 100: 258-264. HUGELIN, A., AND M. BONVALLET. 1956. Etude klectrophysiologique d’un reflexe monosynaptique trigCmina1. C. K. Sot. Biol. (Paris) 150: 2067-2071. JERGE, C. R. 1964. The neurophysiologic mechanism underlying cyclic jaw movements. J. Prosfhcf. Dent. 14 : 667-681. KAWAMURA, Y., M. FUNAKOSHI, AND M. TAICATA. 1960. Reciprocal relationships in the brain-stem among afferent impulses from each jaw muscle on the cat. Jap. J. Physiol. 10: 585-593. KAWAMURA, Y. 1972. Recent advances in the physiology of mastication. Pages 163-204 in N. EMELIN AND Y. ZOTTERMAN, Eds., Oral Physiology. Pergamon Press, Oxford. PCI.ETTI, F. 1959. Cutaneous tactile units in cats. Physiologist 2 : 96. RIOCH, J. M. 1934. The neural mechanism of mastication. d~z. J. Physiol. 108: 168-176. SAUERLAND, E. K., AND H. THIELE. 1970. Presynaptic depolarization of lingual and glossopharyngeal nerve afferents induced by stimulation of trigeminal proprioceptive fibers. Exp. Ncwol. 28 : 344-355. SHERRINGTON, C. S. 1917. Reflexes elicitable in the cat from pinna, vibrissae and jaws. J. PhysioI. (Lo&on) 51 : 4Oa31. STOREY, A. T. 1962. Physiology of a changing vertical dimension. J. Pr-osthcf. Dent. 12 : 912-921. SvnrI, T. 1963. The segmental reflex relations of cutaneous afferent inflow to thoracic respiratory motoneurons. J. Nezcrophysiol. 26 : 478493. SUMI, T. 1970. Activity in single hypoglossal fibers during cortically induced swallowing and chewing in rabbits. Pjliigers Arch. 314: 329-346. SUMI, T. 1975. Reflex modification of cortically evoked rhythmic jaw movements. J. Physiol.
Sot.
Jap. 37 : 250.
19. SZENTAGOTHAI, J. 1948. Anatomical considerations of monosynaptic reflex arcs. J. Nczrrofihysiol. 11 : 445-454. 20. TAKATA, M., K. ITO, AND Y. KAWAMURA. 1975. Inhibition of hypoglossal motoneurons by stimulation of the jaw-opening muscle afferents. Jap. J. Physiol. 25:
453-465.
21. Voss, H. 1956. Zahl und Anordnung der Muskelspindeln in den oberen Zungenbeinmuskeln, im M. trapezius und M. latissimus dorsi. Anat. Am. 103: 443-446.
NEUROLOGY
Sensory
59,
137-145 (1978)
Fibers in the Nerve and their Functional TADAAKI
Department
SUMI
of the Jaw Opening Property in Rabbits AND SOTARO HANAI
of Physiology, Fujita-Gakucn Toyoake, Nagoya
Received
Allgust
10,1977;
Universiry School 4iO-11,
Muscles
1 of Medicine,
Japan
revision received October
17,1977
In anesthetized and immobilized adult rabbits, the peripheral stump of the mylohyoid nerve innervating musculus mylohyoideus and musculus digastricus was isolated and the activity recorded from its constituent single fibers. The fibers originated from sensory receptors in the skin, muscles, or other noncutaneous structures. The cutaneous afferent fibers had receptive fields of 11 mm’ (average value) distributed roughly in the area covering the relevant muscles. They responded readily to air-blowing, light touch, and/or pressure whereas the muscular afferent fibers responded to stretch of either of the jaw opening muscles. The latter fibers were classified into three groups: (i) low-threshold, tension-dependent, slowly adapting units; (ii) highthreshold, tension-velocity-dependent, rapidly adapting units ; and (iii) “on-otY units. The physiologic significance of these sensory fibers is discussed in relation to the type of their receptors as well as to their central linkages in the brain stem.
INTRODUCTION It is widely believed that the rhythmic activity of mastication originates primarily from the “chewing center” in the brain stem (4, 17). However, the activity has also been considered to be produced through feedback from the jaw opening and closing muscles: The proprioceptive afferents of each functional group of muscles activate the synergic motoneurons, while inhibiting the antagonistic motoneurons, thus leading to reciprocal, rhythmic sequencesof excitation and inhibition of the two jaw muscles (8, 10, 12, 14). In fact, many tension receptors are found in the jaw 1 Thanks are extended to Prof. Robert W. Doty of the University of Rochester for giving suggestions and criticisms, and reading the earlier draft of the manuscript. This investigation was supported in part by a grant in aid for Scientific Research from the Educational Ministry of Japan. 137 0014-4886/78/0591-0137$02.00/O Copyright 0 1978 by Academic Press, Inc. All rights of reproduction in any form reserved.
138
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AND
HANAI
closing muscles (6) ; their afferent fibers intermingle with efferent fibers to the muscle (19). On the other hand, there is no or very little evidence for the existence of afferent fibers in the nerves arising from the jaw opening muscles, viz., the digastricus, mylohyoideus, and geniohyoideus (1, 19). In none of these muscles have the tension receptors been fully confirmed histologically (10). However, recent investigations clearly indicate that centripetal stimulation of the mylohyoid nerve inhibits hypoglossal motoneurons (21) and also modifies cortically evoked rhythmic jaw movements (IS). In addition, a brief burst of spikes is produced in the cat mylohyoid nerve only by brisk stretch of the anterior digastric muscle (13). These facts prompted us to examine more fully whether or not sensory fibers exist in the nerve from the jaw opening muscles and, if so, what their origin and nature might be. METHODS Twenty-two adult rabbits, weighing 2.5 to 3.0 kg, were used. They were anesthetized initially with ethyl urethane (1 g/kg, intramuscularly) or with sodium pentobarbital (30 to 50 mg/kg, intraperitoneally. Supplemental anesthesia was administered as necessary. Thirteen of the anesthetized animals were immobilized by gallamine triethiodide (3 mg/kg, intravenously) and respiration was maintained artificially through the tracheal cannula. The animal was placed laterally on a table and the jaws were fixed rigidly with clamps and bars. The masseter muscle and the lower jaw were partially removed unilaterally. The mylohyoid nerve, a branch of the inferior alveolar nerve, was isolated and severed near the bifurcation from the parent nerve trunk. The cutaneous edge along the incision was elevated to form a trough and filled with liquid paraffin kept at 34 to 38°C by an infrared light. After identifying the nerve branch by direct observation of contraction, produced both in the mylohyoideus and in the digastricus by an electrical shock applied to the nerve, the distal end was dissected into single fibers with watchmaker’s forceps under microscopic control. Single nerve fibers were placed on a platinum wire electrode, and the electrical sign of the activity of the fiber was amplified, displayed on a cathode ray oscillograph, and photographed with a kymograph camera. The “indifferent” Iead was sewn subcutaneously around the wound and grounded. Auditory monitoring of the neural activity was used routinely. To determine the peripheral origin and the functional property of the nerve fibers, natural stimuli, such as bending hairs, air-blowing, or lightly touching the skin covering the locus of the jaw opening muscles, as well as pulling each of the muscles, were applied. The contour and extent of the
AFFERENT
B
FIBERS
FROM
---
JAW
OPENING
MUSCLES
139
-
------------------------
C D FIG. 1. Responses of cutaneous sensory fibers of the mylohyoid nerve to touch (A, B, and D) or air-blowing (C) on their receptive fields. Broken lines indicate the durations of cutaneous stimulations; horizontal bars, 0.5 s. Slowly adapting (A) or rapidly adapting (B) discharge to touch in each fiber; steady discharge to airblowing (C) ; “on-off” discharge to touch (D) in the same fiber.
cutaneous receptive field for individual fibers were traced with a small, blunt glass rod and drawn with India ink on the surface of the skin. After each experiment the drawing of the receptive fields were photographed and measured. To apply tension to the muscles, two threads, one attached to the caudal tendon of the digastric muscle and the other to the body of the hyoid bone, were pulled caudally with a force of 10 to 800 g. Using a strain-gauge amplifier, the forces thus applied to the muscle were recorded simultaneously with the activity of the nerve fibers. In two animals, the area and configuration of cutaneous receptive fields for L2 dorsal root fibers were similarly photographed and measured for comparison with those of the mylohyoid afferent fibers. RESULTS More than 100 afferent units were identified and successful records were obtained from 55 units, 35 of which responded to cutaneous stimulation, 10 to muscular traction, and 5 to unspecific, noncutaneous mechanical stimulation such as manipulation of the suprahyoid structures. In general, afferent fibers of cutaneous or muscular origin tended to be gathered respectively in the nerve bundle. Furthermore, the cutaneous fibers
140
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HANAI
initiating from adjacent receptive fields also ran side by side in the nerve bundle. Responsive Properties and Receptive Field Organization of the Cutaneous Aterent Fibers. No spontaneous activity was observed in this type of afferent fiber, However, these fibers fired a burst of impulses when their receptive fields were stimulated with gentle air-blowing or touching. A repetitive application of the stimulus elicited a brisk burst discharge of impulses. Among those cutaneous afferent fibers, many units responded continuously but with a small decrease in the frequency of discharge (Fig. 1A), whereas several others responded only for a short period at the beginning of light continuous touch (Fig. 1B). In the same unit, a steady discharge (Fig. 1C) to air-blowing was converted into an “on-off” discharge (Fig. 1D) when a light touch was applied to its receptive field. Units with fast-adapting responses to touch discharged 300 or more impulses per second and possessed a small receptive field, very often consisting of a single spot or a few discrete spots, whereas units with slowly adapting responses discharged several tens of impulses per second and had a wider receptive area than did fast-adapting units. The cutaneous receptive fields in the ipsilateral suprahyoid area were delineated by the chin rostrally, the ventral edge of the mandible laterally, and the midline (Fig. 2). The distribution of receptive fields was dense around the center of the area, where many of these fields overlapped. The sizes of the receptive fields were spot-like to 100 mm2, with an average value of 11
FIG. 2. Receptive field organization of cutaneous sensory fibers of the left mylohyoid nerve in the rabbit. The area encompassed by the ,broken line denotes the approximate locus and extent of all receptive fields verified in this study. Dots and circles of various sizes and shapes indicate the receptive fields of single fibers confirmed in one animal.
AFFERENT
FIBERS
FROM
JAW
OPENING
141
MUSCLES
llllllllllc
loo-
.
50 og
50
. . 0-A
’
’
’
’
’
-
T
1
m
50 og
0
5
Time(sec)
10
r?g
FIG. 3. Responses of three sensory fibers of the mylohyoid nerve (upper right, traces of each record) to stretch of the digastric muscle at various strengths (lower right traces of each record calibrated by the scale). Time marks, 0.1-s divisions, In the upper left diagram, the number of impulses per second (ordinate) is plotted against tension (absicca). Plot A represents the unit of small-size spikes, whereas B represents that of medium-size spikes shown in the records to the right. In the lower left diagram, the number of impulses per second (ordinate) is plotted against the time after onset of traction (abscissa) for a unit of small-size spikes exclusively at three different strengths. mm2 for 30 units examined. However, because of methodological limitations, fields smaller than 1 mm2 could be defined only approximately. These values contrast with those obtained for the fields of cutaneous fibers at L2 dorsal roots, which were spot-like to 165 mm2, with an average of 78 mm2. Properties of Agerent Fibers Originating from Deep Structures. Eight afferent fibers found in the mylohyoid nerve trunk gave no response to cutaneous stimulation, but fired specifically and exclusively when the digastric or mylohyoid muscle was mechanically stretched. Both the threshold and the frequency of discharge attained at each intensity of muscular tension differed for each individual unit. In Fig. 3 three units recorded simutlaneously are shown : The unit of small spikes responded at first to tension of about 7.0 g with 16 impulses/s, the unit of middle-
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FIG. 4. Responses of a sensory fiber of the mylohyoid nerve (upper right traces of each record) to traction of the digastric muscle at various strengths (lower right traces of each record). Vertical scales are for calibration of tension. Time marks, 0.1-s divisions. In the diagram, the rate of discarge is plotted as a function of the time after onset of traction at three different strengths.
size spikes responded to 250 g with only a few impulses per second. Of these, small-spike and middle-spike units showed a linear relation between the rate of discharge of impulses and the logarithmic value of the tension applied (Fig. 3, A and B in upper left diagram). Other similar units revealed a comparable relation of impulses rate to tension as described above, except for differences in their thresholds. Therefore, when plots were made for these analogous units on the same scale, their lines of representation became parallel, i.e., they had the same slope. In each unit, however, the rate of discharge decreased very slightly after the onset, although the tension was kept constant for 30 s or longer. The decline in the rate of discharge was more obvious at the beginning of a stronger traction (Fig. 3, lower left diagram). Among the units responding to muscular stretch, several possesseda much higher threshold and a lower rate of discharge, even at maximum tension, than those described above, e.g., 250 g for the threshold and 7 impulses/s at 800 g for the unit of large spikes shown in Fig. 3. In units with a high threshold, the rate of discharge was relatively higher initially but rapidly reached its steady value, which varied roughtly with the tension applied (Fig. 4). The rate of discharge during the initial phase of muscular stretch generally depended on the strength of stretch, the rate of increase of tension, and the individual unit
examined.
In three units,
burst
discharges
of impulses
were
produced
only at the moment when stretch was applied or released, and there was no sign of activity during the period when tension was constant (Fig. 5). In these cases, the threshold exceeded 150 g. Corresponding to rhythmically repeated pulling and releasing of the muscle, as would occur actually during the jaw closing and opening of rhythmic mastication, all tension-sensitive units readily gave a rhythmic burst of impulses in phase with an increase
AFFERENT
-
FIRERS
FRO&~
JAW
OPENIKG
143
11~793,~~
500 og
FIG. 5. Example of an “on-off” response of a sensory fiber of the mylohyoid nerve to traction of the digastric muscle. The lower trace indicates the tension of traction calibrated by the scale attached. Horizontal bar 0.5-s. tension (jaw closing). The last type of unit fired in both phases at strong traction. Every unit fired in responseto pulling either the mylohyoid or the digastric muscle, and no unit discharged in response to the isolated manipulation of both muscles. In general, the threshold was lower for units responding to stretch of the diagasticus compared to stretch of the mylohyoid. DISCUSSION in
Abundant muscle spindles are present in the jaw closing muscles, viz., the masseter and the ptyerygoid (6). Sensory nerve fibers arising from these receptors intermingle with motor fibers in the same peripheral nerve trunk and run into the trigeminal mesencephalic tract nucleus where their cell bodies congregate (2). Near the cell bodies, their axons give off a branch which terminates on the motoneurons of jaw closing muscles, thus forming a monosynaptic reflex linkage between the sensory and the motor neurons concerned (7, 21). In the jaw closing muscles, the possible existence of tendon organs was also suggestedby a number of investigators (3, 15, 19) and confirmed directly by histology (10). However, in the jaw opening muscles, viz., the mylohyoid and the digastric, neither the spindles nor the tendon organs have been identified (6, 19). No degeneration of myelinated fibers is observed in the muscles after coagulating the ipsilateral trigeminal mesencephalic tract nucleus (19). These findings may be in line with previous results which show that no reflex effect can be produced either by stretch of the digastric muscle or by stimulation of the digastric nerve electrically (1). Apparently, the results presented in this paper disagree with those described above. This may be attributed to the paucity of such sensory nerve fibers (see Resultsj and presumably to the difference in species of animal studied. becausea few spindles are found in the anterior part of the digastric muscle in man (‘21). Therefore, because so few tension-sensitive afferent fibers exist in the jaw opening muscles, reciprocal inhibition, as seen between the extensors and the flexors of the limb (5), may be poorly expressed between the jaw opening and closing muscles. A slight inhibition of messeteric motoneurons can be produced only when the digastric muscle is pulled intensely (9). It may be tentatively inferred that the low-
144
SUM1
AND
HANAI
threshold, tension-dependent muscular afferents (Fig. 3) arise from muscle spindles: the high-threshold, traction-velocity-dependent unit (Fig. 4) from tendon organs; and the unit responding only at application and removal of the muscular stretch (Fig. 5) from other tension-sensitive receptors (such as those present in the fascia). A single electrical stimulus to the low-threshold afferents of jaw opening muscles exerts an inhibitory influence on the hypoglossal motoneurons in cats. The inhibition begins after a latency of 10 to 15 ms and lasts 200 ms or longer. From this evidence, a polysynaptic linkage is postulated for this inhibitory reflex (20). Stimulation with repetitive electrical pulses to the central stump of the mylohyoid nerve also modifies cortically evoked rhythmic jaw movements. The movement increases in rate and decreases in amplitude, and the lower jaw shifts toward opening (18). All these effects of stimulating the nerve trunk of the jaw opening muscles also indicate the existence of sensory fibers in the nerve concerned, although their peripheral origin would be heterogeneous as shown in the present study. In addition to the afferent fibers of the “deep receptor,” the sensory fibers arise clearly and abundantly from the surface of skin in the area roughly covering the mylohyoid and digastric muscles ipsilaterally (see Results). Judging from the relative richness of such afferent fibers and the long latency in the reflex effect of stimulating the nerve of the jaw opening muscle, the sensory fibers of cutaneous origin may play a major role in producing the modification of rhythmic jaw movements (18) and the inhibition of hypoglossal motoneurons (20). In fact, electrical stimulation of the same skin area produces an effect on the cortically evoked rhythmic jaw movement comparable to that produced by stimulation of the mylohyoid nerve (21). The relative smallnessof the cutaneous receptive fields of this nerve (11 mm?; seeResults) compared to those in the other areas, viz., a few square millimeters on hand and foot (ll), 53 mm2 on thorax (16), 78 mm? on abdominal wall (see Results), and more than 300 mm2 on trunk ( 1l), may imply higher sensory discrimination, becausethe area is close to the perioral region which is known to have high sensitivity. The locus of cell bodies for these sensory fibers which arise from the deep receptors or from the skin is still obscure, although the latter may more likely be the semilunar ganglion instead of the trigeminal mesencephalic tract nucleus. This question, however, requires further investigation. REFERENCES 1.
S,. 1960. Afferent influences on tongue muscle activity. Acta Physiol. Scud. : l-97. CROSBY, E. C., T. HUMPHREY, AND E. W. LAVER. 1962. Correlative Anatomy of the Nervous System, 1st ed. Macmillian, New York. BLOM,
[supp1.]49
2.
AFFERENT
3. 4.
5. 6.
7. 8. 9.
10. 11. 12. 13. 14. 15. 16. 17. 18.
FIBERS
FROM
JAW
OPENING
MUSCLES
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DALE, SMITH, R. 1969. Location of the neurons innervating tendon spindles of masticator muscles. Exp. Nrurol. 25 : 64M54. DELLOU’, P. G., AND J. P. LUND. 1971. Evid,ence for central timing of rhythmical mastication. J. Physiai. (Lotdow) 215 : l-13. ECCLES, J. C. 1957. The Physiology of Nerve Cells, 2nd ed. Johns Hopkins Press, Baltimore. FREIMANN, V. R. 1954. Untersuchungen iiber Zahl und Anordnung der Muskelspindeln in den Kaumuskefn des Menschen. Agzat. -4.1~. 100: 258-264. HUGELIN, A., AND M. BONVALLET. 1956. Etude klectrophysiologique d’un reflexe monosynaptique trigCmina1. C. K. Sot. Biol. (Paris) 150: 2067-2071. JERGE, C. R. 1964. The neurophysiologic mechanism underlying cyclic jaw movements. J. Prosfhcf. Dent. 14 : 667-681. KAWAMURA, Y., M. FUNAKOSHI, AND M. TAICATA. 1960. Reciprocal relationships in the brain-stem among afferent impulses from each jaw muscle on the cat. Jap. J. Physiol. 10: 585-593. KAWAMURA, Y. 1972. Recent advances in the physiology of mastication. Pages 163-204 in N. EMELIN AND Y. ZOTTERMAN, Eds., Oral Physiology. Pergamon Press, Oxford. PCI.ETTI, F. 1959. Cutaneous tactile units in cats. Physiologist 2 : 96. RIOCH, J. M. 1934. The neural mechanism of mastication. d~z. J. Physiol. 108: 168-176. SAUERLAND, E. K., AND H. THIELE. 1970. Presynaptic depolarization of lingual and glossopharyngeal nerve afferents induced by stimulation of trigeminal proprioceptive fibers. Exp. Ncwol. 28 : 344-355. SHERRINGTON, C. S. 1917. Reflexes elicitable in the cat from pinna, vibrissae and jaws. J. PhysioI. (Lo&on) 51 : 4Oa31. STOREY, A. T. 1962. Physiology of a changing vertical dimension. J. Pr-osthcf. Dent. 12 : 912-921. SvnrI, T. 1963. The segmental reflex relations of cutaneous afferent inflow to thoracic respiratory motoneurons. J. Nezcrophysiol. 26 : 478493. SUMI, T. 1970. Activity in single hypoglossal fibers during cortically induced swallowing and chewing in rabbits. Pjliigers Arch. 314: 329-346. SUMI, T. 1975. Reflex modification of cortically evoked rhythmic jaw movements. J. Physiol.
Sot.
Jap. 37 : 250.
19. SZENTAGOTHAI, J. 1948. Anatomical considerations of monosynaptic reflex arcs. J. Nczrrofihysiol. 11 : 445-454. 20. TAKATA, M., K. ITO, AND Y. KAWAMURA. 1975. Inhibition of hypoglossal motoneurons by stimulation of the jaw-opening muscle afferents. Jap. J. Physiol. 25:
453-465.
21. Voss, H. 1956. Zahl und Anordnung der Muskelspindeln in den oberen Zungenbeinmuskeln, im M. trapezius und M. latissimus dorsi. Anat. Am. 103: 443-446.
