Afferent impulses from the teeth due to pressure and noxious

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J. Physiol. (I939) 97, 207-2I9 . "''6I2.3I.I :6I2.83

AFFERENT IMPULSES FROM THE TEETH DUE TOPRESSURE AND NOXIOUS STIMULATION

BY CARL PFAFFMANN1From the Physiological Laboratory, Cambridge

(Received 5 August 1939)

THAT the tooth has a rich sensory endowment is a matter of commonobservation and clinical experience. Nevertheless, most controlledstudies of this subject have been largely histological in emphasis and thepresent study is concerned with a more physiological approach makinguse of electro-physiological methods to register the action potentials inthe dental nerves of the cat.

HISTORICAL2The 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 impulseswhich were transmitted to the pulp. Clinical observations by Duval [1833] and ThomasBell [1835] showed that the dentine itself was acutely sensitive to pain. This has been thegenerally accepted view up to the present time.

Peaselee [1857] mentions that various forms of pressure can be detected and to someextent localized by the teeth. Friinkel [1871] pointed out that this power of localizationwas due to the nerves of the periodontal membrane and was still present after removal ofthe pulp. Black [1887] clearly recognized that both the pulp and periodontal nerves werenecessary to complete the sensory complex of the tooth. The nerves of the periodontalmembrane responded to the slightest pressure, whereas the pulp nerves gave rise to painwhatever the stimulus.

The demonstration by Stewart [1927] that the tactile thresholds of teeth were practicallyunchanged after extirpation of the pulp strongly suggests that the tactile sensitivity islimited to the periodontal membrane, although it has been maintained that there is aconsiderable amount of tactile sensibility over and above pressure which is affected byremoval of the pulp [Woods, 1914]. Others have suggested that alterations in the calibreof 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 fibresand 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1 George Henry Lewes Student.2 For historical references, see Stewart [1927].

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ANATOMICALIn the cat the tooth pulp is supplied essentially with medullated

nerve fibres of small size, between 2 and 10 in diameter, with few if anyunmyelinated fibres [Windle, 1927; Brashear, 1936]. On the other hand,the exact nature of the termination of these fibres is not clear. As thefibres proceed up through the pulp, they progressively lose their myelinsheaths and pass into the region of odontoblast cells and, according tosome [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 varyingdistances.

The nerve supply to the periodontal membrane, on the other hand,is more heterogeneous including unmyelinated as well as myelinatedfibres up to 14,u. in diameter [Windle, 1927; Brashear, 1936]. These arederived from the apical nerves, as well as from various bundles penetratingthe 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 thecathave specialized spindle-like terminations formed by the fibre becomingtwisted like a spiral spring, and finer ones which pass to the deeper partsof the periodontal membrane and there break up into fine arborizationswithout terminal organs.

APPARATUS AND PROCEDURE

The recording apparatus consisted of a resistance capacity-coupledamplifier, loud-speaker, and Matthews oscillograph arranged for visualscanning as well as photography.

Nerves supplying the incisor, canine and premolar teeth of the upperjaw were obtained in cats anaesthetized under dial after first removingthe eye and then locating the dental branches of the maxillary divisionof the trigeminal nerve as they cross the floor of the orbit. The head wasrigidly held by a clamp which engaged the upper jaw by the infra-orbitalmargin of the opposite maxilla superiorly and the opposite molar teethinferiorly. This clamp was applied directly without reflexion of the skin.

The whole animal was placed in a heated box fitted with a slidingglass front. Temperature and humidity could be independently controlledand maintained to keep the nerve in good condition. Silver-silver chloridewick electrodes were used.

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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.1 5-72 2-33 14 0*55 0-25

Heavier weights were applied by means of a simple lever, one end ofwhich could be fastened to the tooth by plasticine, while the appropriateweights were attached to the other. This could be arranged to work eitherin the vertical or horizontal planes.

EFFECTS OF PRESSURE

When the intact tooth is touched with an insulated rod, there is amarked discharge of nerve impulses. At the moment of contact there isan initial high voltage spike (250-600 ,V.) which is followed by a steady

...

Fig. 1. Response to pressure showing the initial high-voltage spikes produced at themoment of contact, followed by the low-voltage asynchronous discharge. Both recordsfrom the same preparation. A. Calibration, 40 ,uV. Note that the initial spikes areoff the record. B. Calibration, 400,uV. Time 01 sec.

Fig. 2. Response of the whole nerve to maintained pressure (100 g.) on the canine toothThe 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 asthe pressure is maintained (Fig. 1). Over a period of time this steady

C. PFAFFMANN

discharge shows a gradual diminution in potential magnitude and incomplexity due both to a decrease in the frequency of response in somefibres and to a cessation of activity in others (Fig. 2).

Touching neighbouring teeth and regions of the gum and lower jawwhose nerves are not on the electrodes shows that this initial responseis not an artefact resulting from the mere contact, but is nervous in originand 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 animmediate cessation of the response. In two cases, after the pressure hadbeen maintained for a considerable period of time, there was a slightdischarge of a few fibres for a short period after its removal. Only oncedid a single fibre (judging from the potential record) of the large numberactive during normal tactile stimulation give rise to a short series ofimpulses upon removal of the stimulus.

Many, if not most, of the endings responsive to tactile or pressurestimulation are located in the periodontal membrane and receive theirnerve supply through alveolar bone, since the response diminished little,if at all, after removal of the pulp and destruction of the nerves in theapical canal by a cautery. After severe fracture of the tooth and removalof all but a small portion of the root, pressure on this remaining fragmentstill gave rise to a vigorous response. In other experiments, where singlefibres or only a few fibres were obtained, removal of the pulp and apicalcanal nerves by pulp canal cleaners did not affect the response to pressure.

Determinations of thresholds were made with the series of gradedhairs. In most adult cats, the threshold value for the canine tooth was2-3 g. In one very young animal a pressure of 0 5 g. was found to beeffective, whereas for all cases 0-25 g. was found to be supraliminal forthe 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 insome cases only one fibre. Different fibres in the same and differentpreparations gave varying adaptation times (i.e. time to cessation of theresponse with a maintained pressure) with the same stimulus. Thesedifferences in adaptation time were also apparent for supraliminal stimuliin experiments in which single fibres were obtained by dissection. Witha 100 g. stimulus some endings gave only a few impulses (five or six orless), whereas others continued to discharge for 5 min. or longer. Noattempt was made to follow the response for longer than 5 min.

The response of any one ending to pressure consists of a regularlyspaced train of impulses (Fig. 5 A). With greater pressures the frequency

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of response is higher and usually adaptation time is longer (Fig. 3). Therelationship between the frequency of response and the stimulus over the

200 g.

70

50

0 2 _.vowCUo 40 sec

Fig. 3. Showing the frequency of response in the same fibre for different pressures.

f req160-

1-3 17 20 2-3 log0 stim.

Fig. 4. The relation between frequency of response and log of the stimulus for two differentexperiments. 16 a is based on the frequency during the first sec. of the response shownin Fig. 3. 16 b is a similar plot from another experiment.

limited range used in these experiments (20-200 g.) is approximatelylogarithmic as indicated in Fig. 4. Since in both cases only four points

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were obtained and since the experiments were not especially designed totest this aspect of the response, the results are included merely to showthat 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 notedthat pressures applied against any surface of the tooth elicited responsesof about the same magnitude. With single fibres, however, it was foundthat pressures against only one surface were effective for that particularfibre. Thus, in Fig. 5, the upper record illustrates the response to a stimulusapplied to the canine tooth in the cephalo-caudal direction. The secondrecord shows that the opposite direction does not stimulate the sameending, 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 otherfibres. Time 0.2sec.

the maximal position, there is a decrease in stimulating efficiency untila position of about 900 on either side is reached where the stimulus is nolonger effective for that particular fibre. This suggests that, since mostof the endings are in the periodontal membrane, only one type of deforma-tion of the ending, as the tooth moves slightly in the alveolus, is effective.From the case reported above, where a fragment of the tooth wasstimulated by pressure, it might be argued that pressure only and nottension is the adequate stimulus, although it must be remembered thatconditions were abnormal.

The nerve branches to the teeth may also contain fibres supplyingthe adjacent gums and even lips. These, too, may be activated individuallyby localized stimulation with a graded bristle, and seem to resemble

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physiologically those endings found in the periodontal membrane, showingon the whole slow adaptation and individual variations in time to com-plete adaptation. In some cases a spontaneously discharging ending maybe encountered which can be made to stop after maintained pressureover the sensitive area. When the stimulus is released, there is a cessationof all response for a time, followed by a gradual return to the level of theprevious resting discharge. This has also been observed occasionally ina tooth and is reminiscent of the same behaviour reported for muscleendings [Adrian & Zotterman, 1926 a; Matthews, 1933]. These slowlyadapting pressure endings are also found in the tongue when the afferentimpulses from that organ are recorded from the lingual nerve.

In both the periodontal and mucous membrane endings, the frequencyof discharge was found to be influenced not only by the final tension orpressure applied, but also by the rate of application of that tension. Itwas only qualitatively noted that with more rapid changes higher initialfrequencies 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 pressurethan could be obtained from the endings in soft tissues. This is probablydue to the damping effect of the soft tissues which prevent sudden changesfrom being directly applied to the end-organ in question. The highestinitial frequency obtained to such sudden changes in pressure was1200 per sec., although this high rate of discharge lasted for only a fewimpulses. This maximum frequency will be discussed later in connexionwith the response to a vibratory stimulus.

It is of interest to consider another type of ending found in the tonguecharacterized by a rapid rate of adaptation. This ending is not stimulatedby steady pressure, but only by changes of pressure, and so may respondeither upon the application or removal of the stimulus. In this case, thefrequency of discharge is also determined by the rate of application ofthe stimulus. Slow applications may call out impulses at about 25 orless per sec. Sudden deformations caused by tapping the skin with atactile bristle or other light instrument may call out groups of 5-10regularly spaced impulses at a frequency of nearly 1000 per sec. Thistype 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 about5 mm. in diameter as determined by the tactile bristle. The pressureendings of the tongue have a smaller sensitive region on the surface andusually have a higher threshold.

PI. XCVII. 14

C. PFAFFMANN

DiscussionThe 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 theirtactile sensitivity. In fact, the pressure thresholds of teeth before andafter removal of the pulp is little changed as measured by an aesthesio-meter. A peripheral basis for the ability to localize fairly accurately thestimulus when applied to the tooth [Stewart, 1927] is provided in theunidirectional sensitivity of the periodontal endings. Furthermore, thefact that such a rich tactile response may be obtained after destructionof the apical nerves agrees with the histological finding that a majorityof the nerves to the membrane come from the alveolar plate itself[Lewinsky & Stewart, 1937].

The extreme development of this pressure sensitivity can be relatedto the reflex control of mastication. In the decerebrate preparationSherrington [1917] demonstrated that pressure stimulation of the gumsbordering the teeth of both the upper and lower jaws, of the teeth them-selves, as well as of the front part of the hard palate, caused reflex openingof the tonically closed jaw, which involved a reflex inhibition of the jaw-closing muscles as well as a stimulation of the opener muscles. Faradiza-tion of the central end of the severed superior alveolar nerve had asimilar result. These effects could also be demonstrated in the anaesthe-tized animal, and in the present experiments it has often been observedthat when the maxillary branch of the trigeminal was cut, there waspractically always a very stiong and sudden movement of the mandible.

The finding of two definite types of ending in the mucosa of the tongueagrees with the results of Adrian & Zotterman [1926 b] who describerapidly adapting touch and more slowly adapting pressure endings ofthe skin. In the present experiments, the fact that the touch endingshave a lower threshold suggests that they are not so deeply situated asthe pressure endings.

The fact that frequencies up to 1000 per sec. can be elicited in thecase of the touch ending and even higher in the case of the tooth endingagrees with the proof by Matthews [1931] that the sensory ending over-laps the nerve fibre with respect to its capacity for response.

RESPONSE TO NOXIOUS STIMULIObservation of the impulses related to noxious stimuli is complicated

by the fact that any manipulation of the tooth causes a pronounceddischarge from the pressure endings which quite effectively masks

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anything else that may be going on. On the other hand, it is possible totreat the tooth with agents that are definitely related to pain in thehuman and to avoid this complication.

The best agents for this purpose are hot or cold water. The intactcanine tooth can be immersed in the fluid contained in a small beaker orvessel without causing any pressure discharge. Water at room temperaturehas little effect, but water of 70 or 00 C. will call out a marked dischargeof impulses which for the most part are more slowly conducted than thoseelicited by pressure. Since both cold and hot water produced theseimpulses and since pressure impulses retained their normal form whenthe tooth was immersed in ice water, it is not likely that these slowerrates 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. Interelectrodedistance 4-4 mm. Time 0 01 sec.

nerve. Comparison of the diphasic impulses resulting from both typesof stimuli also show that the potentials related to "painful" agents areof longer duration at the electrodes, due to the slower rate of conductionas indicated by the thickness of the potential spike (Fig. 6).

Water of 70° C. seems a more effective stimulus than ice water, fornot only are the recognizable impulses called out, but there is also anincreased irregularity of the base-line which would indicate that numerouspotentials of small magnitude are being produced. For both hot andcold, the impulses continue as long as the stimulus is applied, althoughthere seems to be a diminution in the response as time proceeds.

It might be argued that these stimuli were activating endings specifi-cally sensitive to temperature changes. Injury to the tooth, however,gives rise to impulses of the same type. Clipping off the end of the toothwith a bone forceps also gives rise to a series of slowly conducted impulseswhich gradually decrease in number with time. It has only been possibleto estimate this "adaptation" qualitatively, yet it is quite clear that the

14-2

C. PFAFFMANN

response continues for some minutes after the injury. In certain cases,a large number of small, yet moderately fast impulses have been calledup by noxious agents as well. In one case where strong acetic acid wasplaced on the bared dentine and pulp, there was also a marked dischargewhich gradually built up and then declined over a period of severalminutes. In another case, mere exposure of the dentine elicited a dis-charge of moderately fast impulses which could be diminished by coveringthe exposed area with cotton-wool soaked in warm Ringer's solution.

On the whole, however, this response has been disappointingly meagrefor a region known to be as sensitive as the tooth. The technical limitationsare considered to be responsible for this, since many of the potentials arebarely greater than the noise level of the amplifier. In some experiments,where the base-line was particularly bad, no indication of a response toany noxious agent could be detected at all.

Discussion

Estimations of conduction velocity can be made from the form of thediphasic impulses if the interelectrode distance is known. The time ofconduction from one electrode to the second is then given by the intervalfrom the beginning of the rising phase of the negative deflexion to thepoint 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 resultin large errors if this distance is small. Furthermore, in agreement withothers, it has been noted that the slowly conducted impulses are oftentriphasic in form. Adrian [1931] attributes this to axon branching, whileBishop [1934] points out that often, particularly in fibres, there is a largepositive after-potential which gives a triphasic form to the recordedimpulse. Both factors would vitiate measurements based on the begin-ning of the second phase.

Analysis of the records themselves is complicated by the difficulty ofdetermining the beginning of the positive phase. Comparison of the fastmonophasic spikes with the fast diphasic spikes show that there is adefinite break in the rising phase of these potentials. In the slowerpotentials, however, there seems to be little difference in the spikedurations of the monophasic and diphasic impulses, so that the beginningof the second phase is combined with the end of the monophasic potential.Nevertheless, calculations based on the form of the potential have beenmade. The rates for the fast impulses of 24-60 m./sec. are probably near

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the correct value, while those for the slow impulses of 4-21 m./sec. areprobably too fast.

Since the errors of measurement seem to be less significant for thefast impulses it seems permissible to make certain correlations by placingthem among the slower components of the A group of Erlanger & Gasser[1930]. It seems quite definite that this group is made up of fibres oflarge size, although the exact relation between velocity and fibre diameteris not yet settled [Erlanger & Gasser, 1937; Douglass, Davenport,Heinbecker & Bishop, 1934]. Histological studies have shown that thenerves to the periodontal membrane in the cat include all sizes but with20 % fibres between 10 and 14,u in diameter. In this region large fibresare related to the spindle endings. The fast conduction rates of thepressure impulses are consistent with all these facts.

All the pulp nerves are myelinated, but of smaller size ranging from2 to 9 ,u in diameter with 64 % less than 6 tt in diameter. Noxious stimuli,which presumably activate these fibres, call out impulses of slowerconduction rates. This agrees with the results of others that "painful"stimulation gives rise to slowly conducted potentials presumably relatedto 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 painsensitivity, is supplied only with small myelinated fibres is of interestwith regard to the relation between fibre types and their function.Histological considerations alone have shown that nerves subserving thesame cutaneous qualities may have quite different fibre constitutionswith respect to the smaller fibres. The trigeminal, as a whole, has a muchsmaller unmyelinated component than have the spinal nerves [Windle,1926]. The pulp nerves of the tooth are essentially myelinated containingmany fibres of the B group, yet the quality of the sensation aroused inman 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 ofthe body. Indeed, this innervation of moderately sized fibres wouldaccount for the finding of v. Werz [1932] that the chronaxie of the toothfor pain indicated fast excitabilities of the irritable tissue concerned.Stimulation in this case probably involved direct activation of themedullated pulp fibres.

C. PFAFFMANN

SUMMARY AND CONCLUSIONS

1. Touch or pressures applied to the intact tooth gave rise to anintense discharge of nerve impulses in the dental nerves.

2. Most of the endings responsible for this discharge are located inthe periodontal membrane.

3. Threshold values for the canine tooth are about 2-3 g. using abristle calibrated to bend at that pressure.

4. The endings to pressure showed great individual differences inadaptation times. Times to complete cessation of the response variedfrom a fraction of a second to more than 5 min.

5. Individual pressure endings of the periodontal membrane dis-played properties agreeing with those elucidated for other afferent endingsand are physiologically similar to the pressure endings of the mucousmembrane.

6. Force applied only in one general direction stimulates the singleending. It seems that pressure rather than tension is the adequatestimulus for the single ending.

7. Frequencies as high as 1200 per sec. in a single fibre from the toothhave been recorded with very rapid applications of pressure.

8. The touch endings of the mucous membrane (tongue) respondwith short bursts of impulses to changes in pressure, but not to steadydeformations. Frequencies of nearly 1000 per sec. have been obtainedwith rapid deformations of the mucous membrane. These endings havea lower threshold than have the pressure endings of the tongue.

9. Noxious agents such as extremes of temperature or fracture of thetooth give rise to impulses typically of lower voltage and slower conduc-tion rate than those initiated by pressure on the intact tooth.

The writer wishes to thank Prof. Adrian for his constant help and encouragement andDr 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.

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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.

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Afferent impulses from the teeth due to pressure and noxious