,ks-;'* -~) 207. (Received 5 August 1939) observation and clinical experience. Nevertheless, most controlled

Transcription

1 ,ks-;'* -~) 207 ~~ ~.8I3 J. Physiol. (I939) 97, 207-2I9. "''6I2.3I. I :6I2.83 AFFERENT IMPULSES FROM THE TEETH DUE TO PRESSURE AND NOXIOUS STIMULATION BY CARL PFAFFMANN1 From the Physiological Laboratory, Cambridge (Received 5 August 1939) THAT the tooth has a rich sensory endowment is a matter of common observation and clinical experience. Nevertheless, most controlled studies of this subject have been largely histological in emphasis and the present study is concerned with a more physiological approach making use of electro-physiological methods to register the action potentials in the dental nerves of the cat. HISTORICAL2 The earliest workers, Hunter & Charles Bell [1811], believed that the dentine was insensitive to pain and that its apparent response to stimuli was due to mechanical impulses which were transmitted to the pulp. Clinical observations by Duval [1833] and Thomas Bell [1835] showed that the dentine itself was acutely sensitive to pain. This has been the generally accepted view up to the present time. Peaselee [1857] mentions that various forms of pressure can be detected and to some extent localized by the teeth. Friinkel [1871] pointed out that this power of localization was due to the nerves of the periodontal membrane and was still present after removal of the pulp. Black [1887] clearly recognized that both the pulp and periodontal nerves were necessary to complete the sensory complex of the tooth. The nerves of the periodontal membrane responded to the slightest pressure, whereas the pulp nerves gave rise to pain whatever the stimulus. The demonstration by Stewart [1927] that the tactile thresholds of teeth were practically unchanged after extirpation of the pulp strongly suggests that the tactile sensitivity is limited to the periodontal membrane, although it has been maintained that there is a considerable amount of tactile sensibility over and above pressure which is affected by removal of the pulp [Woods, 1914]. Others have suggested that alterations in the calibre of the dentinal tubules from occlusive stress may be transmitted to the pulp nerves [Sprenkel, 1936]. At the present time, it is most generally accepted that pain is related to the pulp fibres and touch to the periodontal membrane, although pain may arise from this region as well. 1 George Henry Lewes Student. 2 For historical references, see Stewart [1927].

2 208 C. PFAFFMANN ANATOMICAL In the cat the tooth pulp is supplied essentially with medullated nerve fibres of small size, between 2 and 10 in diameter, with few if any unmyelinated fibres [Windle, 1927; Brashear, 1936]. On the other hand, the exact nature of the termination of these fibres is not clear. As the fibres proceed up through the pulp, they progressively lose their myelin sheaths and pass into the region of odontoblast cells and, according to some [Tiegs, 1932, 1938] may end in that region in special endings or, according to others [Sealey, 1932; Lewinsky & Stewart, 1936; v. d. Sprenkel, 1936], may continue into the dentine as fine fibres for varying distances. The nerve supply to the periodontal membrane, on the other hand, is more heterogeneous including unmyelinated as well as myelinated fibres up to 14,u. in diameter [Windle, 1927; Brashear, 1936]. These are derived from the apical nerves, as well as from various bundles penetrating the numerous foramina in the alveolar bone [Lewinsky & Stewart, 1937]. These latter divide into two fasciculi, one of which runs toward the apex, the other toward the gingival margin, and consist of two types of fibre, thick ones confined to the peripheral part of the membrane, which in the cat have specialized spindle-like terminations formed by the fibre becoming twisted like a spiral spring, and finer ones which pass to the deeper parts of the periodontal membrane and there break up into fine arborizations without terminal organs. APPARATUS AND PROCEDURE The recording apparatus consisted of a resistance capacity-coupled amplifier, loud-speaker, and Matthews oscillograph arranged for visual scanning as well as photography. Nerves supplying the incisor, canine and premolar teeth of the upper jaw were obtained in cats anaesthetized under dial after first removing the eye and then locating the dental branches of the maxillary division of the trigeminal nerve as they cross the floor of the orbit. The head was rigidly held by a clamp which engaged the upper jaw by the infra-orbital margin of the opposite maxilla superiorly and the opposite molar teeth inferiorly. This clamp was applied directly without reflexion of the skin. The whole animal was placed in a heated box fitted with a sliding glass front. Temperature and humidity could be independently controlled and maintained to keep the nerve in good condition. Silver-silver chloride wick electrodes were used.

3 IMPULSES DUE TO PRESSURE, ETC. ON TEETH 209 For threshold measurements of pressure, a series of bristles was made, calibrated on a balance to bend at the following values: Bristle g * Heavier weights were applied by means of a simple lever, one end of which could be fastened to the tooth by plasticine, while the appropriate weights were attached to the other. This could be arranged to work either in the vertical or horizontal planes. EFFECTS OF PRESSURE When the intact tooth is touched with an insulated rod, there is a marked discharge of nerve impulses. At the moment of contact there is an initial high voltage spike ( ,V.) which is followed by a steady... Fig. 1. Response to pressure showing the initial high-voltage spikes produced at the moment of contact, followed by the low-voltage asynchronous discharge. Both records from the same preparation. A. Calibration, 40,uV. Note that the initial spikes are off the record. B. Calibration, 400,uV. Time 01 sec. Fig. 2. Response of the whole nerve to maintained pressure (100 g.) on the canine tooth The four strips of record reading from the left illustrate the response at the beginning, after 15, 45 and 180 sec. of stimulation respectively. Time 0 05 sec. asynchronous discharge of much lower voltage (15-40,uV.) as long as the pressure is maintained (Fig. 1). Over a period of time this steady

4 210 C. PFAFFMANN discharge shows a gradual diminution in potential magnitude and in complexity due both to a decrease in the frequency of response in some fibres and to a cessation of activity in others (Fig. 2). Touching neighbouring teeth and regions of the gum and lower jaw whose nerves are not on the electrodes shows that this initial response is not an artefact resulting from the mere contact, but is nervous in origin and represents presumably a single synchronous volley in the nerve. Single taps give rise to the large spikes only. When the stimulus is removed after maintained pressure, there is an immediate cessation of the response. In two cases, after the pressure had been maintained for a considerable period of time, there was a slight discharge of a few fibres for a short period after its removal. Only once did a single fibre (judging from the potential record) of the large number active during normal tactile stimulation give rise to a short series of impulses upon removal of the stimulus. Many, if not most, of the endings responsive to tactile or pressure stimulation are located in the periodontal membrane and receive their nerve supply through alveolar bone, since the response diminished little, if at all, after removal of the pulp and destruction of the nerves in the apical canal by a cautery. After severe fracture of the tooth and removal of all but a small portion of the root, pressure on this remaining fragment still gave rise to a vigorous response. In other experiments, where single fibres or only a few fibres were obtained, removal of the pulp and apical canal nerves by pulp canal cleaners did not affect the response to pressure. Determinations of thresholds were made with the series of graded hairs. In most adult cats, the threshold value for the canine tooth was 2-3 g. In one very young animal a pressure of 0 5 g. was found to be effective, whereas for all cases 0-25 g. was found to be supraliminal for the skin of the nose or the mucous membrane of the gums and tongue. In the tooth, the threshold bristle often stimulated only a few and in some cases only one fibre. Different fibres in the same and different preparations gave varying adaptation times (i.e. time to cessation of the response with a maintained pressure) with the same stimulus. These differences in adaptation time were also apparent for supraliminal stimuli in experiments in which single fibres were obtained by dissection. With a 100 g. stimulus some endings gave only a few impulses (five or six or less), whereas others continued to discharge for 5 min. or longer. No attempt was made to follow the response for longer than 5 min. The response of any one ending to pressure consists of a regularly spaced train of impulses (Fig. 5 A). With greater pressures the frequency

5 IMPULSES DUE TO PRESSURE, ETC. ON TEETH 211 of response is higher and usually adaptation time is longer (Fig. 3). The relationship between the frequency of response and the stimulus over the 200 g Fig _.vow CUo 40 sec Showing the frequency of response in the same fibre for different pressures. f req log0 stim. Fig. 4. The relation between frequency of response and log of the stimulus for two different experiments. 16 a is based on the frequency during the first sec. of the response shown in Fig b is a similar plot from another experiment. limited range used in these experiments ( g.) is approximately logarithmic as indicated in Fig. 4. Since in both cases only four points

6 212 C. PFAFFMANN were obtained and since the experiments were not especially designed to test this aspect of the response, the results are included merely to show that they are in keeping with the properties of other afferent endings [Matthews, 1931; Hartline & Graham, 1932]. When the full nerve trunk was placed on the electrodes, it was noted that pressures applied against any surface of the tooth elicited responses of about the same magnitude. With single fibres, however, it was found that pressures against only one surface were effective for that particular fibre. Thus, in Fig. 5, the upper record illustrates the response to a stimulus applied to the canine tooth in the cephalo-caudal direction. The second record shows that the opposite direction does not stimulate the same ending, but that this direction is adequate for several other fibres. From Fig. 5. Showing different fibres active with pressures applied in opposite directions. A. Cephalo-caudal direction. One fibre. B. Caudo-cephalic direction. Several other fibres. Time 0.2 sec. the maximal position, there is a decrease in stimulating efficiency until a position of about 900 on either side is reached where the stimulus is no longer effective for that particular fibre. This suggests that, since most of the endings are in the periodontal membrane, only one type of deformation of the ending, as the tooth moves slightly in the alveolus, is effective. From the case reported above, where a fragment of the tooth was stimulated by pressure, it might be argued that pressure only and not tension is the adequate stimulus, although it must be remembered that conditions were abnormal. The nerve branches to the teeth may also contain fibres supplying the adjacent gums and even lips. These, too, may be activated individually by localized stimulation with a graded bristle, and seem to resemble

7 IMPULSES DUE TO PRESSURE, ETC. ON TEETH 213 physiologically those endings found in the periodontal membrane, showing on the whole slow adaptation and individual variations in time to complete adaptation. In some cases a spontaneously discharging ending may be encountered which can be made to stop after maintained pressure over the sensitive area. When the stimulus is released, there is a cessation of all response for a time, followed by a gradual return to the level of the previous resting discharge. This has also been observed occasionally in a tooth and is reminiscent of the same behaviour reported for muscle endings [Adrian & Zotterman, 1926 a; Matthews, 1933]. These slowly adapting pressure endings are also found in the tongue when the afferent impulses from that organ are recorded from the lingual nerve. In both the periodontal and mucous membrane endings, the frequency of discharge was found to be influenced not only by the final tension or pressure applied, but also by the rate of application of that tension. It was only qualitatively noted that with more rapid changes higher initial frequencies were obtained, and since others [Adrian & Zotterman, 1926 a, b; Matthews, 1931] have already carefully elucidated this effect, no further analysis was made. It was noticed, however, that in the tooth, higher frequencies were obtained with sudden applications of pressure than could be obtained from the endings in soft tissues. This is probably due to the damping effect of the soft tissues which prevent sudden changes from being directly applied to the end-organ in question. The highest initial frequency obtained to such sudden changes in pressure was 1200 per sec., although this high rate of discharge lasted for only a few impulses. This maximum frequency will be discussed later in connexion with the response to a vibratory stimulus. It is of interest to consider another type of ending found in the tongue characterized by a rapid rate of adaptation. This ending is not stimulated by steady pressure, but only by changes of pressure, and so may respond either upon the application or removal of the stimulus. In this case, the frequency of discharge is also determined by the rate of application of the stimulus. Slow applications may call out impulses at about 25 or less per sec. Sudden deformations caused by tapping the skin with a tactile bristle or other light instrument may call out groups of 5-10 regularly spaced impulses at a frequency of nearly 1000 per sec. This type of ending has never been found in the tooth in these experiments. On the tongue, such endings may be related to a sensitive area of about 5 mm. in diameter as determined by the tactile bristle. The pressure endings of the tongue have a smaller sensitive region on the surface and usually have a higher threshold. PI. XCVII. 14

8 214 C. PFAFFMANN Discussion The finding that the periodontal membrane is so richly supplied with nerve endings, the adequate stimulus for which is mere pressure or touch, is in keeping with the observations in man that pulpless teeth retain their tactile sensitivity. In fact, the pressure thresholds of teeth before and after removal of the pulp is little changed as measured by an aesthesiometer. A peripheral basis for the ability to localize fairly accurately the stimulus when applied to the tooth [Stewart, 1927] is provided in the unidirectional sensitivity of the periodontal endings. Furthermore, the fact that such a rich tactile response may be obtained after destruction of the apical nerves agrees with the histological finding that a majority of the nerves to the membrane come from the alveolar plate itself [Lewinsky & Stewart, 1937]. The extreme development of this pressure sensitivity can be related to the reflex control of mastication. In the decerebrate preparation Sherrington [1917] demonstrated that pressure stimulation of the gums bordering the teeth of both the upper and lower jaws, of the teeth themselves, as well as of the front part of the hard palate, caused reflex opening of the tonically closed jaw, which involved a reflex inhibition of the jawclosing muscles as well as a stimulation of the opener muscles. Faradization of the central end of the severed superior alveolar nerve had a similar result. These effects could also be demonstrated in the anaesthetized animal, and in the present experiments it has often been observed that when the maxillary branch of the trigeminal was cut, there was practically always a very stiong and sudden movement of the mandible. The finding of two definite types of ending in the mucosa of the tongue agrees with the results of Adrian & Zotterman [1926 b] who describe rapidly adapting touch and more slowly adapting pressure endings of the skin. In the present experiments, the fact that the touch endings have a lower threshold suggests that they are not so deeply situated as the pressure endings. The fact that frequencies up to 1000 per sec. can be elicited in the case of the touch ending and even higher in the case of the tooth ending agrees with the proof by Matthews [1931] that the sensory ending overlaps the nerve fibre with respect to its capacity for response. RESPONSE TO NOXIOUS STIMULI Observation of the impulses related to noxious stimuli is complicated by the fact that any manipulation of the tooth causes a pronounced discharge from the pressure endings which quite effectively masks

9 IMPULSES DUE TO PRESSURE, ETC. ON TEETH 215 anything else that may be going on. On the other hand, it is possible to treat the tooth with agents that are definitely related to pain in the human and to avoid this complication. The best agents for this purpose are hot or cold water. The intact canine tooth can be immersed in the fluid contained in a small beaker or vessel without causing any pressure discharge. Water at room temperature has little effect, but water of 70 or 00 C. will call out a marked discharge of impulses which for the most part are more slowly conducted than those elicited by pressure. Since both cold and hot water produced these impulses and since pressure impulses retained their normal form when the tooth was immersed in ice water, it is not likely that these slower rates of conduction were the result of temperature changes affecting the A B Fig. 6. Comparison of fast and slow impulses. A. Pressure. B. Ice water. Interelectrode distance 4-4 mm. Time 0 01 sec. nerve. Comparison of the diphasic impulses resulting from both types of stimuli also show that the potentials related to "painful" agents are of longer duration at the electrodes, due to the slower rate of conduction as indicated by the thickness of the potential spike (Fig. 6). Water of 70 C. seems a more effective stimulus than ice water, for not only are the recognizable impulses called out, but there is also an increased irregularity of the base-line which would indicate that numerous potentials of small magnitude are being produced. For both hot and cold, the impulses continue as long as the stimulus is applied, although there seems to be a diminution in the response as time proceeds. It might be argued that these stimuli were activating endings specifically sensitive to temperature changes. Injury to the tooth, however, gives rise to impulses of the same type. Clipping off the end of the tooth with a bone forceps also gives rise to a series of slowly conducted impulses which gradually decrease in number with time. It has only been possible to estimate this "adaptation" qualitatively, yet it is quite clear that the 14-2

10 216 C. PFAFFMANN response continues for some minutes after the injury. In certain cases, a large number of small, yet moderately fast impulses have been called up by noxious agents as well. In one case where strong acetic acid was placed on the bared dentine and pulp, there was also a marked discharge which gradually built up and then declined over a period of several minutes. In another case, mere exposure of the dentine elicited a discharge of moderately fast impulses which could be diminished by covering the exposed area with cotton-wool soaked in warm Ringer's solution. On the whole, however, this response has been disappointingly meagre for a region known to be as sensitive as the tooth. The technical limitations are considered to be responsible for this, since many of the potentials are barely greater than the noise level of the amplifier. In some experiments, where the base-line was particularly bad, no indication of a response to any noxious agent could be detected at all. Discussion Estimations of conduction velocity can be made from the form of the diphasic impulses if the interelectrode distance is known. The time of conduction from one electrode to the second is then given by the interval from the beginning of the rising phase of the negative deflexion to the point where this is first affected by the beginning of the opposite phase. Such estimations possess doubtful accuracy for a number of reasons. Inaccuracies in measurement of the interelectrode distance would result in large errors if this distance is small. Furthermore, in agreement with others, it has been noted that the slowly conducted impulses are often triphasic in form. Adrian [1931] attributes this to axon branching, while Bishop [1934] points out that often, particularly in fibres, there is a large positive after-potential which gives a triphasic form to the recorded impulse. Both factors would vitiate measurements based on the beginning of the second phase. Analysis of the records themselves is complicated by the difficulty of determining the beginning of the positive phase. Comparison of the fast monophasic spikes with the fast diphasic spikes show that there is a definite break in the rising phase of these potentials. In the slower potentials, however, there seems to be little difference in the spike durations of the monophasic and diphasic impulses, so that the beginning of the second phase is combined with the end of the monophasic potential. Nevertheless, calculations based on the form of the potential have been made. The rates for the fast impulses of m./sec. are probably near

11 IMPULSES DUE TO PRESSURE, ETC. ON TEETH 217 the correct value, while those for the slow impulses of 4-21 m./sec. are probably too fast. Since the errors of measurement seem to be less significant for the fast impulses it seems permissible to make certain correlations by placing them among the slower components of the A group of Erlanger & Gasser [1930]. It seems quite definite that this group is made up of fibres of large size, although the exact relation between velocity and fibre diameter is not yet settled [Erlanger & Gasser, 1937; Douglass, Davenport, Heinbecker & Bishop, 1934]. Histological studies have shown that the nerves to the periodontal membrane in the cat include all sizes but with 20 % fibres between 10 and 14,u in diameter. In this region large fibres are related to the spindle endings. The fast conduction rates of the pressure impulses are consistent with all these facts. All the pulp nerves are myelinated, but of smaller size ranging from 2 to 9,u in diameter with 64 % less than 6 tt in diameter. Noxious stimuli, which presumably activate these fibres, call out impulses of slower conduction rates. This agrees with the results of others that "painful" stimulation gives rise to slowly conducted potentials presumably related to fibres of smaller diameter [Adrian, 1932; Bishop & Heinbecker, 1935; Clark, Hughes & Gasser, 1935; Erlanger & Gasser, 1937; Zotterman, 1939]. The fact that an organ like the tooth, so richly endowed with pain sensitivity, is supplied only with small myelinated fibres is of interest with regard to the relation between fibre types and their function. Histological considerations alone have shown that nerves subserving the same cutaneous qualities may have quite different fibre constitutions with respect to the smaller fibres. The trigeminal, as a whole, has a much smaller unmyelinated component than have the spinal nerves [Windle, 1926]. The pulp nerves of the tooth are essentially myelinated containing many fibres of the B group, yet the quality of the sensation aroused in man by stimulation of that organ can hardly be called "pricking pain". This kind of correlation may hold for any given preparation of the skin [Zotterman, 1939], but cannot be extended generally to other regions of the body. Indeed, this innervation of moderately sized fibres would account for the finding of v. Werz [1932] that the chronaxie of the tooth for pain indicated fast excitabilities of the irritable tissue concerned. Stimulation in this case probably involved direct activation of the medullated pulp fibres.

12 218 C. PFAFFMANN SUMMARY AND CONCLUSIONS 1. Touch or pressures applied to the intact tooth gave rise to an intense discharge of nerve impulses in the dental nerves. 2. Most of the endings responsible for this discharge are located in the periodontal membrane. 3. Threshold values for the canine tooth are about 2-3 g. using a bristle calibrated to bend at that pressure. 4. The endings to pressure showed great individual differences in adaptation times. Times to complete cessation of the response varied from a fraction of a second to more than 5 min. 5. Individual pressure endings of the periodontal membrane displayed properties agreeing with those elucidated for other afferent endings and are physiologically similar to the pressure endings of the mucous membrane. 6. Force applied only in one general direction stimulates the single ending. It seems that pressure rather than tension is the adequate stimulus for the single ending. 7. Frequencies as high as 1200 per sec. in a single fibre from the tooth have been recorded with very rapid applications of pressure. 8. The touch endings of the mucous membrane (tongue) respond with short bursts of impulses to changes in pressure, but not to steady deformations. Frequencies of nearly 1000 per sec. have been obtained with rapid deformations of the mucous membrane. These endings have a lower threshold than have the pressure endings of the tongue. 9. Noxious agents such as extremes of temperature or fracture of the tooth give rise to impulses typically of lower voltage and slower conduction rate than those initiated by pressure on the intact tooth. The writer wishes to thank Prof. Adrian for his constant help and encouragement and Dr Matthews for his ever-willing advice. REFERENCES Adrian, E. D. [1931]. Proc. Roy. Soc. B, 109, 1. Adrian, E. D. [1932]. The Mechanism of Nervous Action. Philadelphia: Univ. Penn. Press. Adrian, E. D. & Zotterman, Y. [1926 a]. J. Physiol. 61, 151. Adrian, E. D. & Zotterman, Y. [1926 b]. J. Physiol. 61, 465. Bishop, G. H. [1934]. J. cell. comp. Physiol. 5, 151. Bishop, G. H. & Heinbecker, P. [1935]. Amer. J. Physiol. 114, 179. Brashear, A. D. [1936]. J. comp. Neurol. 64, 169. Clark, D., Hughes, J. & Gasser, H. S. [1935]. Amer. J. Physiol. 114, 69.

13 IMPULSES DUE TO PRESSURE, ETC. ON TEETH 219 Douglass, T. C., Davenport, H. A., Heinbecker, P. & Bishop, G. H. [1934]. Amer. J. Physiol. 110, 165. Erlanger, J. & Gasser, H. S. [1930]. Amer. J. Physiol. 92, 43. Erlanger, J. & Gasser, H. S. [1937]. Electrical Signe of Nervous Activity. Philadelphia: Univ. Penn. Press. Hartline, H. K. & Graham, C. H. [1932]. J. ceu. comp. Physiol. 1, 277. Lewinsky, W. & Stewart, D. [1936]. J. Anat., Lond., 70, 349. Lewinsky, W. & Stewart, D. [1937]. J. Anat., Lond., 71, 98 and 232. Matthews, B. H. C. [1931]. J. Phy8iol. 71, 64. Matthews, B. H. C. [1933]. J. Phy8iol. 78, 1. Sealey, V. T. [1932]. Aust. J. Dent. 36, 1. Sherrington, C. S. [1917]. J. Physiol. 51, 420. Sprenkel, H. B. van der [1936]. J. Anat., Lond., 70, 233. Stewart, D. [1927]. Proc. Roy. Soc. Med. 20, 55. Tiegs, 0. W. [1932]. J. Anat., Lond., 66, 622. Tiegs, 0. W. [1938]. J. Anat., Lond., 72, 234. Werz, R. v. [1932]. Arch. exp. Path. Pharmak. 167, 191. Windle, W. F. [1926]. J. comp. Neurol. 41, 453. Windle, W. F. [1927]. J. comp. Neurol. 43, 347. Zotterman, Y. [1939]. J. Physiol. 95, 1.