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Effect of tooth temperature on activities of slowly adapting periodontal mechanoreceptors in the cat
CGO3-9969 92 SS.OO+O.oO Copyright c 1992 Pergamon Press Ltd
.drchs ord Bid.Vol.37,No. 11, pp. 875-881, 1992 Printed in Great Britain. All rights reserved
EFFECT OF TOOTH TEMPERATURE ON ACTIVITIES OF SLOWLY ADAPTING PERIODONTAL MECHANORECEPTORS IN THE CAT T. TABATA
and K. KARITA
Department of Physiology, Tohoku University School of Dentistry, Seiryo-machi. Aoba-ku, Sendai 980, Japan (Accepred 12 June 1992)
Summary-The mass response of a nerve bundle and the unitary discharges from a functional single nerve fibre evoked by mechanical stimulation of the upper canine tooth were recorded from the superior alveolar nerves of 10 anaesthetized cats. When the pulpal cavity of the mechanically stimulated tooth was perfused with a 0.9% NaCl solution at temperatures from 10 to 45”C, the mass response of the nerve bundle to that stimulation increased linearly with the rise in perfusate temperature (hereafter, tooth temperature). In the unitary discharge recordings, the activities of 30 (88%) of 34 slowly adapting periodontal mechanosensitive units were modulated by tooth temperature. The optimal temperature, at which the periodontal mechanoreceptor shows extreme excitation by mechanical tooth stimulation, was distributed widely from 10 lo <45”C with a peak at <45”C. A shift in tooth temperature away from the optimal value caused a decrease in, or sometimes the disappearance of, the response. This decrease was the result of the decrease in the excitability of the periodontal mechanoreceptor; i.e. an increase in threshold stimulus intensity and a shortening of the adaptation time to sustained pressure applied to the tooth. Key words: periodontal ligament, mechanoreceptor,
INTRODUCTION The PM neurones of the primary afferent nerve have been classified as one of four types: rapidly
adapting, slowly adapting, very slowly adapting and spontaneously active (Hannam, 1970). Cash and Linden (1982) and Linden and Millar (1987, 1988a,b), however, speculated that there may be only one type of mechanoreceptor within the periodontal ligament and that the rate of adaptation and the threshold of a particular receptor depend on the location of that receptor within the periodontal ligament from fulcrum to apex. Hannam (1982), Linden and Millar (1987), Millar, Halata and Linden (1989) and Linden (1990) reported that the response characteristics of periodontal mechanoreceptors are similar to those of the type II endings (Ruffini endings) in hairy skin described by Chambers et al. (1972). These findings are supported by morphological observations that all periodontal mechanoreceptors are of slowly adapting type II (Ruffini endings) (Byers, 1985; Byers et al., 1986; Halata, 1988). The type II (Ruffini) endings in hairy skin are sensitive to rapid changes in temperature (Iggo, 1969; Chambers ef al., 1972; Burton, Terashima and Clark, 1972). Similar thermosensitive mechanoreceptors in the skin, reported in several animal species (Weddel and Miller, 1962), have been described as ‘spurious thermoreceptors’ by Iggo (1969) or ‘non-specific neurones’. Whether periodontal mechanoreceptors like the type II endings are sensitive to rapid temperature change has yet to be established. In preliminary Abbreciution: PM, periodontal mechanosensitive (neurone). 875
tooth temperature.
experiments (Tabata and Karita, 1984), we found that the responses (spikes/stimulus) of periodontal mechanoreceptors elicited by mechanical tooth stimulation were influenced by tooth temperature. Millar et al. (1989) also reported that the excitability of the periodontal mechanoreceptor changes with temperature. At what temperature are receptors most excitable and what kind of response properties are most modulated by tooth temperature, however, have yet to be determined. We therefore recorded the neuronal discharges from the primary afferent fibres (superior alveolar nerve) evoked by mechanical stimulation of the canine tooth of the cat and investigated the effects of tooth temperature on the following properties or components of the response: the most vigorous excitation temperature (optimal tooth temperature for excitation) for the periodontal receptor, threshold stimulus intensity, dynamic and static phases of the response to mechanical stimulation in a trapezoidal waveform, and the adaptation rate to a sustained stimulus. MATERIALS AND 5lETHODS
Ten adult cats weighing 2.5-4.5 kg were sedated with ketamine hydrochloride (25 mg/kg i.m.). After cannulation of the cephalic vein, the animals were anaesthetized with pentobarbitone sodium (initial dose 50mg/kg, i.v.; maintenance dose 5 mg/kg/h, i.v.), and their ECG recordings were monitored continuously. Additional anaesthetic was given when spontaneous muscular activity took place or when the pupil of the right eye was insufficiently constricted. The animal’s body temperature was kept at 37-38’C with a bag filled with hot water.
876
T. TAFIATAand K. KAR~TA
ST
ST
0.9% NaCl
Fig. 1. (A) Diagram showing the recording method for the mass response elicited from a nerve bundle of the superior alveolar nerve (I’$)and for unitary discharges from a functional single nerve fibre caused by mechanical stimulation of the upper canine tooth (ST) of the cat. The pulpal cavity of the stimulated tooth was perfused with a 0.9% NaCl solution at various temperatures (IWYC). R, R’, recording electrodes. (B) Mass response (R) and integrated response curve (IR) of R. (C) Unitary discharges (R’) of a PM unit. ST. 0.2N in B and 0.04N in C. The animal’s head was fixed horizontally in a stereotaxic device, after which the left eyeball was
removed from the orbit. The anterior branch of the superior alveolar nerve was exposed and cut centrally. The neuronal discharges elicited by mechanical stimulation of the ipsilateral maxillary canine tooth were recorded from the peripheral nerve bundle (N) or from a functional single nerve fibre isolated from the bundle [Fig. l(A)]. Force-controlled mechanical stimulation was applied to the tooth in the most vigorously discharging direction on the horizontal plane at a point 8 mm from the gingiva. Stimuli of trapezoidal waveform were produced by an electromagnetic force generator (duration 6 s, rising phase 1 s, plateau phase 5 s). The stimulus intensity was monitored with a mechano-
electric transducer. It constituted a negative feedback system designed to improve the fidelity of the stimulator’s response to the driving signal. Tooth temperature was changed slowly at the rate of 0.3”C/min by perfusing the pulpal cavity with a 0.9% NaCl solution at temperatures ranging from 10 to 45°C. The tooth was cut 4 mm from the gingiva, then the pulpal cavity was widened with a dental reamer after pulp extirpation. A polyethylene tube 1 mm dia was then inserted in the dental cavity to let in the perfusate. It was fixed to the tooth with dental cement. To drain off the perfusate, another tube was installed through a small hole opened on the labial side of the tooth 2 mm from the gingiva. The temperature of the perfusate measured from a thermometer was taken as the tooth temperature.
100
.
80
10 -I
l
20 20
30 30
40
:
40
(Periodontium)
Temperature('C) Fig. 2. Thermal effect on the mass response elicited from a nerve bundle by mechanical stimulation of the canine tooth (0.2 N) of the cat. Results recorded for two cats are shown. The magnitude of the mass response (R) measured from the amplitude of the integrated response curve is given as a percentage of the maximum response. Abscissa: tooth and periodontium temperature. Linear regression lines: R = 56 + 0.7. 7”(solid line, solid circles) and R = 29 + 1.5. T (broken line, open circles) where T is the tooth temperature.
877
Thermal effect on periodontal receptors In two cats, the temperatures of the perfusate and the periodontium were measured simultaneously after the experiment. The periodontium temperature was obtained with a fine thermocouple (0.5 mm dia) installed through a hole drilled with a dental bur in the periodontal ligament space on the labial side of the tooth. The periodontium temperature is shown in Fig. 2 with tooth temperature to give a rough estimate of the temperature of the periodontal mechanoreceptor area. Nerve discharges were recorded with a silver-wire electrode (200pm) placed in a liquid-paraffin pool on the floor of the orbit under a surgical microscope. The unitary discharges of a functional single fibre fulfilled the consistency criteria for spike size and shape, for an all-or-none response and for a spike interval of more than 5 ms. Discharges were displayed on an oscilloscope (Nihonkoden, VC-10) by the use of a preamplifier with high-input impedance (WPI, M701) and they were also fed to an audiomonitor. Typical discharges were recorded on magnetic tape (TEAC, R-SO) for later analysis.
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RESULTS
Relation between tooth andperiodontium
temperatures
Tooth and periodontium temperatures were recorded simultaneously in two cats. A rise in the tooth temperature induced a rise in periodontium temperature (Fig. 2). The tooth temperature was lower than the periodontium temperature at < 31 ‘C, the reverse being true at > 3 1‘C with a cross-over at 31’C in both cases. Discharges from
the nerve bundle
Examples of the mass response recorded from a nene bundle and an integrated curve (time constant = 0.1 s) for the response to mechanical stimulation of the canine tooth are shown in Fig. l(B). The magnitude of the mass response increased linearly with a rise in the tooth temperature from 10 to 45YZ. Examples of the linear relation between tooth temperature (or periodontium temperature) and the magnitude of the response in two cats are shown in Fig. 2. The slope of the simple linear-regression line of the tooth temperature and mass-response relation shows the degree of the thermal effect; 1.2 5 0.4%/“C (mean + SD. n = 6 for two cats). Discharges from a single nerve jbre
Unitary discharges from a functional single nerve fibre evoked by stimulation of the canine tooth are shown in Fig. l(C). A total of 34 slowly adapting PM units were detected in 10 cats, The optimal tooth temperature, at which periodontal afferents are most vigorously excited by mechanical tooth stimulation, varied in the PM unit. Three typical thermal effects on the responses (spikes/stimulus) and on the threshold intensities of mechanical stimuli are shown in Fig. 3. The optimal tooth temperature was 39°C for A, 29°C for B and 18’C for C. The threshold intensity was measured from the stimulus intensity at the time of the first spike-firing of the response during the ramp phase of stimulation. In all the cats, threshold stimulus intensities were low in the vicinity of the optimal
Tooth temperature (‘C) Fig. 3. Typical examples of the thermal effect on the unitary discharges elicited from PM units by mechanical stimulation of the canine tooth of the cat and on the threshold stimulus intensity. (A) High-temperature unit. (B) Intermediatetemperature unit. (C) Low-temperature unit. The optimal tooth temperature at which the maximum response occurred is 39’C (A). 28’C (B) and 18°C (C). tooth temperature. A shift of the tooth temperature away from the optimum produced a decrease in the response. The extent of the thermal effect differed in the PM unit. Eighteen PM units (53%) had optimal tooth temperatures above 35°C as shown in A (hightemperature type), eight units (24%) had optima from 20-35’C as shown in B (intermediate-temperature type) and four units (12%) had optima below 2O’C as shown in C (low-temperature type). The activities of four units (12%) were not affected by the tooth temperature. The distribution of optimal tooth temperatures for 30 PM units is shown in Fig. 4. Thirteen (43%) of the 30 had optimum tooth temperatures at 645°C. In four units (13%), spontaneous discharges were induced at about 10°C in the vicinity of the optimal tooth temperatures of these units. Responses
in the rising, transient
and static phases
When the canine tooth of the cat was stimulated mechanically in a trapezoidal waveform, the firing frequency of the PM units increased with the increase in stimulus intensity during the rising phase, reached the maximum response at the start of the plateau phase, then decreased slightly. To determine which phase of the response is most influenced by the tooth temperature, we chose three representative parts [a, b and c in Fig. 5(A ), 0.5 s duration] of a time course of mechanical stimulation. Parts a and b are just before and after the start of the plateau phase of the stimulus, and c is just before the end of the stimulus.
T. TABATAand K.
878
IO
Tooth
20
30
temperature
40
50
(‘c)
Fig. 4. Distribution of the optimal tooth temperature for 30 PM units recorded from the superior alveolar nerve of the cat. For convenience, the responses during periods a, b and c are represented as rising (a, a’), transient (b, b’) and static (c, c’) phase responses. An example of the thermal effect on each phase in one of the high-temperature units is shown in Fig. 5(B). The extent of the thermal effect calculated from the slope of the linear regression line is given as the thermodependent coefficient. The mean coefficient
A
KARITA
was 0.44 spikes/“C in the rising phase (a), 0.45 spikes/ “C in the transient phase (b) and 0.49 spikes/“C in the static phase (c) (Table 1). There was no significant difference among the coefficients for the three phases (paired t test, P < 0.05). The thermal effect observed for one of the intermediate-temperature units is shown in Fig. S(C), in which the regression lines for each phase are given as a, b and c in the low temperature range and as a’, b’ and c’ in the high temperature range. Spike frequencies decreased sharply with a shift of the tooth temperature away from the optimum. Thermodependent coefficients for eight units are shown in Table 2(A). The mean coefficient was between 0.78 and 0.96 spikes/“C in the low temperature range and between - I. 10 and - 1.21 spikes/% in the high temperature range. The coefficients did not differ significantly for the rising, transient and static phases in the low or in the high temperature range (paired t test, p c 0.05). The coefficients of these PM units were significantly higher than those of the hightemperature units (two sample r test with Welch’s correction, p < 0.05). The thermal effect observed for one of four lowtemperature units is shown in Fig. 5(D). Two units were not responsive to mechanical tooth stimulation
R’ ST
Tooth
temperature (T;C)
Fig. 5. Thermal effect on the rising- (n), transient- (b) and static- (c) phase responses (R) elicited by mechanical stimulation of the canine tooth of the cat. (A) Unitary discharges (R’) and mechanical stimulation (ST, 0.04 N) in a trapezoidal waveform. (I, b: 0.5 s period just before or after the start of the plateau phase of the stimulus. c: 0.5 s period just before the end of the stimulus. Arrow head: onset of the mechanical stimulus. (B) Example of the thermal effect on each phase response (a, b and c) in a high-temperature PM unit with the optimal tooth temperature of 645°C. Linear regression lines: a, R = -0.2 + 0.89 . T (sold circles, solid line); b,R = - 1.6f0.93 T (solid triangles, broken line); c, R = - 1.5 + 0.88 . T (open squares, dotted line). (C) Example of the thermal effect in an intermediatetemperature type unit with the optimal tooth temperature of 25°C. Linear regression lines: a and a’, R = 1.0 + 0.70. T and R = 53.5 - 1.12. T (solid circles, solid lines); b and b’, R = -2.0 + 0.90. T and R = 56.5 - 1.16’ T(solid triangles, broken lines); c and c’, R = - 10.4+ 1.18. Tand R = 52.0- 1.10’ T (open squares, dotted lines). (D) Example of the thermal effect in a low-temperature type unit with the optimal T.Temp of 20°C. Linear regression lines: o and (I’, R = Il.5 + 0.5. T and R = 63.3 - 1.9. T (solid circles, solid lines); b and b’, R = 13.0 + 0.4 Tand R = 73.7 - 2.2. T(solid triangles, broken lines); c and c’, R = 12.2 + 0.5 . T and R = 76.7 - 2.3. T (open squares, dotted lines).
879
Thermal effect on periodontal receptors Table 1. Thermal effect on the rising- (a), transient- (6) and static- (c) phase responses of the high-temperature PM units when the canine tooth of the cat was stimulated mechanically in a trapezoidal waveform Response phase Unit
a
b
c
1 2 3 4 5 6 7 8 9 IO II 12 13 14 I5 16 17 18
1.12 0.89 0.86 0.84 0.82 0.72 0.41 0.37 0.37 0.30 0.23 0.22 0.21 0.21 0.14 0.13 0.09 0.07
1.09 0.93 0.97 0.82 0.84 0.88 0.40 0.43 0.37 0.29 0.17 0.24 0.25 0.22 0.17 0.07 0.12 -0.08
0.95 0.88 0.98 0.83 0.94 1.04 0.47 0.47 0.22 0.34 0.14 0.25 0.51 0.23 0.13 0.15 0.12 0.13
0.44 + 0.33
0.45 f 0.36
0.49 * 0.35
Mean k SD
The thermodependent coefficient was calculated from the slope of the linear regression line. at temperatures higher than 3OC [Fig. 5(D)], and the response of two units decreased linearly with the rise in temperature. The thermodependent coefficients are shown in Table 2(B). There was no significant
difference among the three phases in the low or high temperature range (paired f test, p c 0.05). Table 2. Thermal effect on the rising- (a, a’), transient- (6, b’) and static-(c, c’) phase responses of the intermediate- (A) and low temperature (B) PM units on mechanical stimulation of the canine tooth of the cat in a trapezoidal waveform Low range Unit No. 19 20 21 22 23 24 25 26 Mean &
a
b
(A) 1.60 1.38 0.70 0.56 0.50 0.42 0.56 0.50 0.78 * 0.45
High range C
a’
0.83 Zb 0.36
0.96 O?S
-1.21 k 0.72
Low range Unit No.
a
27 28 29 30
0.42 0.50 -
Mean
0.46 f 0.06
8%
b’
Intermediate-temperature units 1.40 1.60 -0.98 -0.78 1.34 1.30 -2.70 -2.80 0.90 1.18 -1.12 -1.16 0.44 0.46 -0.98 - 1.00 0.58 0.90 -1.86 -1.58 0.78 0.92 -0.64 -1.02 0.58 0.62 -0.90 -0.50 0.60 0.70 -0.52 -0.50
b
c’ -0.80 -2.30 -1.10 -0.82 -1.36 -1.00 -0.90 -0.50
-1.17
-1.10
0;s
0:s
High range C
a’
(B) Low-temperature units 0.18 0.36 -3.00 0.40 0.50 -1.90 -0.21 -0.14 0.29
0.43
0:6
o:o
-1.31 I!Z 1.39
b’
c’
-3.20 -2.20 -0.28 -0.14
-2.00 -2.30 -0.25 -0.16
-1.46 -1.18 + 1.50 I?3
The thermodependent coefficient was calculated from the slope of the linear regression line.
DISCUSSION
A rise in the tooth temperature induced a rise in periodontium temperature, but there was a slight difference between them. This difference may result from the thickness and thermal conductivities of the dentine and cementum present between the pulpal cavity and periodontal ligament. Conceivably, if the temperature of the pulpal cavity were changed rapidly or transiently, it would have no effect on the periodontal mechanoreceptor. The tooth temperature was therefore changed very slowly at the rate of 0.3”C/min. The cross-over point of the tooth and periodontium temperatures was 31°C; lower than the cat’s body temperature of 37-38°C. Because the animal’s mouth was open during the experiments and the room temperature was 17-18°C the low periodontium temperature may be the result of the low room temperature. There is also the possibility that the response properties of PM units examined when the mouth was kept open during the long period of experimentation differ somewhat from those examined when the mouth was closed, during which latter period the periodontium temperature nearly equalled the body temperature. The response of a superior alveolar nerve bundle evoked by mechanical tooth stimulation increased linearly with the rise in the tooth temperature between 10 and 45°C. A similar thermal effect on the spike frequency of a single nerve fibre was found in only 43% of the PM units affected by the tooth temperature. In more than half (57%) of PM units, the optimal tooth temperatures were distributed almost equally over the wide range of 15-45°C. These PIM units had their own peculiar thermodependent properties, which differed from those of the nerve bundle. A similar thermal modulation has been reported for several types of mechanoreceptors: the touch receptor (Hunt and McIntyre, 1960; Wall, 1960; Casey and Hahn, 1970) Pacinian corpuscle (Ishiko and Loewenstein, 1960, 1961; Inman and Peruui, 1961), muscle spindle (Lippold, Nicholls and Redfearn, 1960; Ottoson, 1965; Sato, 1983) and periosteum free-fibre ending (Sakada and Nemoto, 1972). In preliminary experiments (Tabata and Karita, 1984), we classified PM units into one of three groups on the basis of whether the optimal tooth temperature was high, intermediate or low. In the present experiments, about half of the PM units were the high-temperature type, the majority of these units having optimal tooth temperatures 6 45’C. Miller et al. (1989) studied the thermal effect on responses of periodontal mechanoreceptors evoked by mechanical tooth stimulation. They pared the alveolar bone that overlays the mechanoreceptor down to a tissuepaper thin layer and changed the temperature of the receptor by perfusing isotonic saline at various temperatures over the receptor site. The optimal temperature ranged from about 39-43’C. Those mechanoreceptors may correspond to the hightemperature PM units found in our experiments. Functionally, it is logical that PM units which fire most actively at near body temperature should be the most abundant. In the type II endings of hairy skin, however, the frequency of spontaneously discharging
T. TABATAand
880
spikes is maximal at 29°C (Burton et al., 1972) and the response elicited by sustained pressure also is maximal at 27°C (Chambers et al., 1972). Therefore, the optimal temperature of the periodontal mechanoreceptors is considered to be about 10°C higher than that of the type II receptors. Unlike the type II endings, the PM units did not produce thermodependent spontaneous discharges. The threshold stimulus intensity of the PM units was low in the vicinity of the optimal tooth temperature. This low intensity is similar to that of the muscle spindle (Lippold et al., 1960) but differs from that of type I receptors whose threshold intensities were unchanged at various skin temperatures (Tapper, 1965). The elevation of the stimulus-response curve of the PM units with a rise in temperature, however, was similar to that of the cutaneous type I receptor (Tapper, 1965; Casey and Hahn, 1970). Tapper (1965) and Casey and Hahn (1970) reported that the response of type I receptors evoked by mechanical ramp or sinusoidal stimulation increased with temperature. Because these responses of type I receptors correspond to the rising-phase responses of the PM units in our experiments, the thermal modulation of type I receptors must be similar to that in high-temperature PM units. The thermal effect on rising-, transient- and static-phase responses of type II endings, however, is not known. In the PM units, the thermodependent coefficients were nearly the same in the rising, transient and static phases of individual units, although the optima1 tooth temperature and thermodependent coefficients differed. The mean coefficient value for the intermediate-temperature units was higher than that of the high-temperature units. The thermodependent response pattern of the intermediate-temperature units resembled that of the type II endings in the skin (Burton et al., 1972; Chambers et al., 1972). The mean conduction velocity of PM units is reported to range from 28 to 83 m/s, most fibres conducting at rates between 44 and 50m/s; i.e. the range of A fibres (Pfaffmann, 1939; Hannam, 1968; Mei, Hartmann and Aubert, 1977; Linden, 1978). The PM units in our experiments therefore are thought to differ from non-specific, nociceptive C fibres (Weddel and Miller, 1962; Burgess and Perl, 1973). Thirteen % of the PM units affected by the tooth temperature discharged spontaneously at temperatures near the optimal tooth temperature. These PM units seem to correspond to the non-specific A fibre group responsive to both mechanical and thermal stimuli (Weddell and Miller, 1962). Our findings on the thermal effect on the activity of PM units suggest that the periodontal sensation to mechanical tooth stimulation changes with the tooth temperature. Psychophysical observations in support of our findings, such as change in the hardness sensation when a human bites foods at different temperatures, have yet to be reported.
K.
KARITA
Burton H., Terashima S. and Clark J. (1972) Response properties of slowly adapting mechanoreceptors to temperature stimulation in cats. Brain Res. 45, 401-416.
Byers M. R. (1985) Sensory innervation of periodontal ligament of rat molars consists of unencapsulated Ruffinilike mechanoreceptors and free nerve endings. J. camp. Neurol. 231, 500-5 18.
Byers M. R., O’Connor T. A., Martin R. F. and Dong W. K. (1986) Mexncephalic trigeminal sensory neurons of cat: axon pathways and structure of mechanoreceptive endings in periodontal ligament. J. camp. Neurol. 250, 181-191. Cash R. M. and Linden R. W. A. (1982) The distribution of mechano-receptors in the periodontal ligament of the mandibular canine tooth of the cat. J. Physiol., Lond. 330, 439-447.
Casey D. E. and Hahn J. F. (1970) Thermal effects on response of cat touch corpuscle. Expl Neurol. 28, 35-45.
Chambers M. R., Andres K. H., Duering V. M. and Iggo A. (1972) The structure and function of the slowly adapting type II mechanoreceptor in the hairy skin. Q. Jl Exp. Physiol. 57, 417-415.
Halata Z. (1988) RuiTini corpuscles-a stretch receptor in the connective tissue of the skin and locomotion apparatus. Pro. Brain Res. 74, 221-229. Hannam A. Ci. (1968) The conduction velocity of nerve impulses from dental mechanoreceptors in the dog. Archs oral Biol. 13, 1377-1383.
Hannam A. G. (1970) Receptive fields of periodontal mechanosensitive units in the dog. Archs oral Biol. 15, 971-978. Hannam A. G. (1982) The innervation of the periodontal ligament. In The Periodontal Ligament in Health and Disease (Eds Berkovitz B. K. B., Maxham B. J. and Neuman H. N.), pp. 173-196. Pergamon Press, Oxford. Hunt C. C. and McIntyre A. K. (1960) Properties of cutaneous touch receptors in the cat. J. Physiol., Lond. 153, 88-98.
Iggo A. (1969) Cutaneous thermoreceptors in primates and subprimates. J. PhIsiol., Lond. 200, 403-430. Inman D. R. and Peruzzi P. (1961) The effects of temperature on the responses of Pacinian corpuscles. J. Physiol., Lond. 155, 280-301.
Ishiko N. and Loewenstein W. R. (1960) Temperature and change transfer in a receptor membrane. Science 132, 1841-1842. Ishiko N. and Loewenstein W. R. (1961) Effects of temperature on the generator and action potentials of a sense organ. J. gen. Ph.vsiol. 45, 105-124. Linden R. W. A. (1978) Properties of intraoral mechanoreceptors represented in the mesencephalic nucleus of the fifth nerve in the cat. J. PhTsiol., Lond. 279, 395-408. Linden R. W. A. (1990) Periodontal mechanoreceptors and their functions. In Neurophysiology of the Jaws and Teerh (Ed. Taylor A.), pp. 52-95. MacMillan Press, New York. Linden R. W. A. and Millar B. J. (1987) Effect of temperature on the discharge of periodontal ligament mechanoreceptors in cat canme tooth. J. dent. Res. 66, 862, Abstract No. 247. Linden R. W. A. and Millar B. J. (1988a) The response characteristics of mechanoreceptors related to their position in the cat canine periodontal ligament. Archs oral Biol. 33, 52-56.
REFERENCES
Linden R. W. A. and Millar B. J. (1988b) The effect of rate of force application on the threshold of periodontal ligament mechanoreceptors in the canine tooth. Archs
Burgess P. R. and Per1 E. R. (1973) Cutaneous mechanoreceptors and nociceptors. In Handbook of Sensory Physiology, II. Somatosensory System (Ed. Iggo A.), pp. 29-78. Springer, Berlin.
Lippold 0. C. J., Sicholls J. G. and Redfearn J. W. T. (1960) A study of the afferent discharge produced by cooling a mammalian muscle spindle. J. Physiol., Lond. 153, 2 18-23 1.
oral Biol. 33, 715-719.
Thermal effect on periodontal receptors Mei N., Hartmann F. and Aubert M. (1977) Periodontal mechanoreceptors involved in pain. In Pain in rhe Trigeminal Region (Eds Anderson D. J. and Matthews B.), pp. 103-I 10. Elsevier/North-holland Biomedical Press, Amsterdam. Millar B. J., Halata Z. and Linden R. W. A. (1989) The structure of physiologically located periodontal ligament mechanoreceptors of the cat canine tooth. J. Anat. 167, 117-127. Ottoson D. (1965) The effects of temperature on the isolated muscle spindle. J. Physiol., Land. 180, 636-648. Pfaffmann C. (1939) Afferent impulses from the teeth due to pressure and noxious stimulation. J. Physiol., Land. 97, 207-219.
Sakada S. and Nemoto T. (1972) Response to thermal stimulation of fast- and slow-adapting free-fiber ending
881
units in the cat mandibular periosteum. Bull. Tokyo dent. CON. 13, 227-250. Sato H. (1983) Effects of skin cooling and warming on stretch responses of the muscle spindle primary and secondary afferent fibers from the cat’s tibialis anterior. Expl Neurol. 81, 446-458. Tabata T. and Karita K. (1984) The effect of tooth temperature on the activity of the periodontal mechanoreceptor in the cat. J. Physiol. Sot. Japan 46 (Suppl.), s455. Tapper D. N. (1965) Stimulus-response relationships in the cutaneous slowly-adapting mechanoreceptor in hairy skin of the cat. Expl Neurol. 13, 364-385. Wall P. D. (1960) Cord cells responding to touch, damage, and temperature of skin. J. keurophjsiol. 23, 197-210. Weddeil G. and Miller S. (1962) Cutaneous sensibility. A. Rev. Physiol. 24, 199-222.
.drchs ord Bid.Vol.37,No. 11, pp. 875-881, 1992 Printed in Great Britain. All rights reserved
EFFECT OF TOOTH TEMPERATURE ON ACTIVITIES OF SLOWLY ADAPTING PERIODONTAL MECHANORECEPTORS IN THE CAT T. TABATA
and K. KARITA
Department of Physiology, Tohoku University School of Dentistry, Seiryo-machi. Aoba-ku, Sendai 980, Japan (Accepred 12 June 1992)
Summary-The mass response of a nerve bundle and the unitary discharges from a functional single nerve fibre evoked by mechanical stimulation of the upper canine tooth were recorded from the superior alveolar nerves of 10 anaesthetized cats. When the pulpal cavity of the mechanically stimulated tooth was perfused with a 0.9% NaCl solution at temperatures from 10 to 45”C, the mass response of the nerve bundle to that stimulation increased linearly with the rise in perfusate temperature (hereafter, tooth temperature). In the unitary discharge recordings, the activities of 30 (88%) of 34 slowly adapting periodontal mechanosensitive units were modulated by tooth temperature. The optimal temperature, at which the periodontal mechanoreceptor shows extreme excitation by mechanical tooth stimulation, was distributed widely from 10 lo <45”C with a peak at <45”C. A shift in tooth temperature away from the optimal value caused a decrease in, or sometimes the disappearance of, the response. This decrease was the result of the decrease in the excitability of the periodontal mechanoreceptor; i.e. an increase in threshold stimulus intensity and a shortening of the adaptation time to sustained pressure applied to the tooth. Key words: periodontal ligament, mechanoreceptor,
INTRODUCTION The PM neurones of the primary afferent nerve have been classified as one of four types: rapidly
adapting, slowly adapting, very slowly adapting and spontaneously active (Hannam, 1970). Cash and Linden (1982) and Linden and Millar (1987, 1988a,b), however, speculated that there may be only one type of mechanoreceptor within the periodontal ligament and that the rate of adaptation and the threshold of a particular receptor depend on the location of that receptor within the periodontal ligament from fulcrum to apex. Hannam (1982), Linden and Millar (1987), Millar, Halata and Linden (1989) and Linden (1990) reported that the response characteristics of periodontal mechanoreceptors are similar to those of the type II endings (Ruffini endings) in hairy skin described by Chambers et al. (1972). These findings are supported by morphological observations that all periodontal mechanoreceptors are of slowly adapting type II (Ruffini endings) (Byers, 1985; Byers et al., 1986; Halata, 1988). The type II (Ruffini) endings in hairy skin are sensitive to rapid changes in temperature (Iggo, 1969; Chambers ef al., 1972; Burton, Terashima and Clark, 1972). Similar thermosensitive mechanoreceptors in the skin, reported in several animal species (Weddel and Miller, 1962), have been described as ‘spurious thermoreceptors’ by Iggo (1969) or ‘non-specific neurones’. Whether periodontal mechanoreceptors like the type II endings are sensitive to rapid temperature change has yet to be established. In preliminary Abbreciution: PM, periodontal mechanosensitive (neurone). 875
tooth temperature.
experiments (Tabata and Karita, 1984), we found that the responses (spikes/stimulus) of periodontal mechanoreceptors elicited by mechanical tooth stimulation were influenced by tooth temperature. Millar et al. (1989) also reported that the excitability of the periodontal mechanoreceptor changes with temperature. At what temperature are receptors most excitable and what kind of response properties are most modulated by tooth temperature, however, have yet to be determined. We therefore recorded the neuronal discharges from the primary afferent fibres (superior alveolar nerve) evoked by mechanical stimulation of the canine tooth of the cat and investigated the effects of tooth temperature on the following properties or components of the response: the most vigorous excitation temperature (optimal tooth temperature for excitation) for the periodontal receptor, threshold stimulus intensity, dynamic and static phases of the response to mechanical stimulation in a trapezoidal waveform, and the adaptation rate to a sustained stimulus. MATERIALS AND 5lETHODS
Ten adult cats weighing 2.5-4.5 kg were sedated with ketamine hydrochloride (25 mg/kg i.m.). After cannulation of the cephalic vein, the animals were anaesthetized with pentobarbitone sodium (initial dose 50mg/kg, i.v.; maintenance dose 5 mg/kg/h, i.v.), and their ECG recordings were monitored continuously. Additional anaesthetic was given when spontaneous muscular activity took place or when the pupil of the right eye was insufficiently constricted. The animal’s body temperature was kept at 37-38’C with a bag filled with hot water.
876
T. TAFIATAand K. KAR~TA
ST
ST
0.9% NaCl
Fig. 1. (A) Diagram showing the recording method for the mass response elicited from a nerve bundle of the superior alveolar nerve (I’$)and for unitary discharges from a functional single nerve fibre caused by mechanical stimulation of the upper canine tooth (ST) of the cat. The pulpal cavity of the stimulated tooth was perfused with a 0.9% NaCl solution at various temperatures (IWYC). R, R’, recording electrodes. (B) Mass response (R) and integrated response curve (IR) of R. (C) Unitary discharges (R’) of a PM unit. ST. 0.2N in B and 0.04N in C. The animal’s head was fixed horizontally in a stereotaxic device, after which the left eyeball was
removed from the orbit. The anterior branch of the superior alveolar nerve was exposed and cut centrally. The neuronal discharges elicited by mechanical stimulation of the ipsilateral maxillary canine tooth were recorded from the peripheral nerve bundle (N) or from a functional single nerve fibre isolated from the bundle [Fig. l(A)]. Force-controlled mechanical stimulation was applied to the tooth in the most vigorously discharging direction on the horizontal plane at a point 8 mm from the gingiva. Stimuli of trapezoidal waveform were produced by an electromagnetic force generator (duration 6 s, rising phase 1 s, plateau phase 5 s). The stimulus intensity was monitored with a mechano-
electric transducer. It constituted a negative feedback system designed to improve the fidelity of the stimulator’s response to the driving signal. Tooth temperature was changed slowly at the rate of 0.3”C/min by perfusing the pulpal cavity with a 0.9% NaCl solution at temperatures ranging from 10 to 45°C. The tooth was cut 4 mm from the gingiva, then the pulpal cavity was widened with a dental reamer after pulp extirpation. A polyethylene tube 1 mm dia was then inserted in the dental cavity to let in the perfusate. It was fixed to the tooth with dental cement. To drain off the perfusate, another tube was installed through a small hole opened on the labial side of the tooth 2 mm from the gingiva. The temperature of the perfusate measured from a thermometer was taken as the tooth temperature.
100
.
80
10 -I
l
20 20
30 30
40
:
40
(Periodontium)
Temperature('C) Fig. 2. Thermal effect on the mass response elicited from a nerve bundle by mechanical stimulation of the canine tooth (0.2 N) of the cat. Results recorded for two cats are shown. The magnitude of the mass response (R) measured from the amplitude of the integrated response curve is given as a percentage of the maximum response. Abscissa: tooth and periodontium temperature. Linear regression lines: R = 56 + 0.7. 7”(solid line, solid circles) and R = 29 + 1.5. T (broken line, open circles) where T is the tooth temperature.
877
Thermal effect on periodontal receptors In two cats, the temperatures of the perfusate and the periodontium were measured simultaneously after the experiment. The periodontium temperature was obtained with a fine thermocouple (0.5 mm dia) installed through a hole drilled with a dental bur in the periodontal ligament space on the labial side of the tooth. The periodontium temperature is shown in Fig. 2 with tooth temperature to give a rough estimate of the temperature of the periodontal mechanoreceptor area. Nerve discharges were recorded with a silver-wire electrode (200pm) placed in a liquid-paraffin pool on the floor of the orbit under a surgical microscope. The unitary discharges of a functional single fibre fulfilled the consistency criteria for spike size and shape, for an all-or-none response and for a spike interval of more than 5 ms. Discharges were displayed on an oscilloscope (Nihonkoden, VC-10) by the use of a preamplifier with high-input impedance (WPI, M701) and they were also fed to an audiomonitor. Typical discharges were recorded on magnetic tape (TEAC, R-SO) for later analysis.
- (0)
OWL0 IO
,#B
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B 100 : 50
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,,O.__O. . . . 0.’
,’
10
20
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2 g
d r
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ifi
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- 0.03
30
40
Lo
RESULTS
Relation between tooth andperiodontium
temperatures
Tooth and periodontium temperatures were recorded simultaneously in two cats. A rise in the tooth temperature induced a rise in periodontium temperature (Fig. 2). The tooth temperature was lower than the periodontium temperature at < 31 ‘C, the reverse being true at > 3 1‘C with a cross-over at 31’C in both cases. Discharges from
the nerve bundle
Examples of the mass response recorded from a nene bundle and an integrated curve (time constant = 0.1 s) for the response to mechanical stimulation of the canine tooth are shown in Fig. l(B). The magnitude of the mass response increased linearly with a rise in the tooth temperature from 10 to 45YZ. Examples of the linear relation between tooth temperature (or periodontium temperature) and the magnitude of the response in two cats are shown in Fig. 2. The slope of the simple linear-regression line of the tooth temperature and mass-response relation shows the degree of the thermal effect; 1.2 5 0.4%/“C (mean + SD. n = 6 for two cats). Discharges from a single nerve jbre
Unitary discharges from a functional single nerve fibre evoked by stimulation of the canine tooth are shown in Fig. l(C). A total of 34 slowly adapting PM units were detected in 10 cats, The optimal tooth temperature, at which periodontal afferents are most vigorously excited by mechanical tooth stimulation, varied in the PM unit. Three typical thermal effects on the responses (spikes/stimulus) and on the threshold intensities of mechanical stimuli are shown in Fig. 3. The optimal tooth temperature was 39°C for A, 29°C for B and 18’C for C. The threshold intensity was measured from the stimulus intensity at the time of the first spike-firing of the response during the ramp phase of stimulation. In all the cats, threshold stimulus intensities were low in the vicinity of the optimal
Tooth temperature (‘C) Fig. 3. Typical examples of the thermal effect on the unitary discharges elicited from PM units by mechanical stimulation of the canine tooth of the cat and on the threshold stimulus intensity. (A) High-temperature unit. (B) Intermediatetemperature unit. (C) Low-temperature unit. The optimal tooth temperature at which the maximum response occurred is 39’C (A). 28’C (B) and 18°C (C). tooth temperature. A shift of the tooth temperature away from the optimum produced a decrease in the response. The extent of the thermal effect differed in the PM unit. Eighteen PM units (53%) had optimal tooth temperatures above 35°C as shown in A (hightemperature type), eight units (24%) had optima from 20-35’C as shown in B (intermediate-temperature type) and four units (12%) had optima below 2O’C as shown in C (low-temperature type). The activities of four units (12%) were not affected by the tooth temperature. The distribution of optimal tooth temperatures for 30 PM units is shown in Fig. 4. Thirteen (43%) of the 30 had optimum tooth temperatures at 645°C. In four units (13%), spontaneous discharges were induced at about 10°C in the vicinity of the optimal tooth temperatures of these units. Responses
in the rising, transient
and static phases
When the canine tooth of the cat was stimulated mechanically in a trapezoidal waveform, the firing frequency of the PM units increased with the increase in stimulus intensity during the rising phase, reached the maximum response at the start of the plateau phase, then decreased slightly. To determine which phase of the response is most influenced by the tooth temperature, we chose three representative parts [a, b and c in Fig. 5(A ), 0.5 s duration] of a time course of mechanical stimulation. Parts a and b are just before and after the start of the plateau phase of the stimulus, and c is just before the end of the stimulus.
T. TABATAand K.
878
IO
Tooth
20
30
temperature
40
50
(‘c)
Fig. 4. Distribution of the optimal tooth temperature for 30 PM units recorded from the superior alveolar nerve of the cat. For convenience, the responses during periods a, b and c are represented as rising (a, a’), transient (b, b’) and static (c, c’) phase responses. An example of the thermal effect on each phase in one of the high-temperature units is shown in Fig. 5(B). The extent of the thermal effect calculated from the slope of the linear regression line is given as the thermodependent coefficient. The mean coefficient
A
KARITA
was 0.44 spikes/“C in the rising phase (a), 0.45 spikes/ “C in the transient phase (b) and 0.49 spikes/“C in the static phase (c) (Table 1). There was no significant difference among the coefficients for the three phases (paired t test, P < 0.05). The thermal effect observed for one of the intermediate-temperature units is shown in Fig. S(C), in which the regression lines for each phase are given as a, b and c in the low temperature range and as a’, b’ and c’ in the high temperature range. Spike frequencies decreased sharply with a shift of the tooth temperature away from the optimum. Thermodependent coefficients for eight units are shown in Table 2(A). The mean coefficient was between 0.78 and 0.96 spikes/“C in the low temperature range and between - I. 10 and - 1.21 spikes/% in the high temperature range. The coefficients did not differ significantly for the rising, transient and static phases in the low or in the high temperature range (paired t test, p c 0.05). The coefficients of these PM units were significantly higher than those of the hightemperature units (two sample r test with Welch’s correction, p < 0.05). The thermal effect observed for one of four lowtemperature units is shown in Fig. 5(D). Two units were not responsive to mechanical tooth stimulation
R’ ST
Tooth
temperature (T;C)
Fig. 5. Thermal effect on the rising- (n), transient- (b) and static- (c) phase responses (R) elicited by mechanical stimulation of the canine tooth of the cat. (A) Unitary discharges (R’) and mechanical stimulation (ST, 0.04 N) in a trapezoidal waveform. (I, b: 0.5 s period just before or after the start of the plateau phase of the stimulus. c: 0.5 s period just before the end of the stimulus. Arrow head: onset of the mechanical stimulus. (B) Example of the thermal effect on each phase response (a, b and c) in a high-temperature PM unit with the optimal tooth temperature of 645°C. Linear regression lines: a, R = -0.2 + 0.89 . T (sold circles, solid line); b,R = - 1.6f0.93 T (solid triangles, broken line); c, R = - 1.5 + 0.88 . T (open squares, dotted line). (C) Example of the thermal effect in an intermediatetemperature type unit with the optimal tooth temperature of 25°C. Linear regression lines: a and a’, R = 1.0 + 0.70. T and R = 53.5 - 1.12. T (solid circles, solid lines); b and b’, R = -2.0 + 0.90. T and R = 56.5 - 1.16’ T(solid triangles, broken lines); c and c’, R = - 10.4+ 1.18. Tand R = 52.0- 1.10’ T (open squares, dotted lines). (D) Example of the thermal effect in a low-temperature type unit with the optimal T.Temp of 20°C. Linear regression lines: o and (I’, R = Il.5 + 0.5. T and R = 63.3 - 1.9. T (solid circles, solid lines); b and b’, R = 13.0 + 0.4 Tand R = 73.7 - 2.2. T(solid triangles, broken lines); c and c’, R = 12.2 + 0.5 . T and R = 76.7 - 2.3. T (open squares, dotted lines).
879
Thermal effect on periodontal receptors Table 1. Thermal effect on the rising- (a), transient- (6) and static- (c) phase responses of the high-temperature PM units when the canine tooth of the cat was stimulated mechanically in a trapezoidal waveform Response phase Unit
a
b
c
1 2 3 4 5 6 7 8 9 IO II 12 13 14 I5 16 17 18
1.12 0.89 0.86 0.84 0.82 0.72 0.41 0.37 0.37 0.30 0.23 0.22 0.21 0.21 0.14 0.13 0.09 0.07
1.09 0.93 0.97 0.82 0.84 0.88 0.40 0.43 0.37 0.29 0.17 0.24 0.25 0.22 0.17 0.07 0.12 -0.08
0.95 0.88 0.98 0.83 0.94 1.04 0.47 0.47 0.22 0.34 0.14 0.25 0.51 0.23 0.13 0.15 0.12 0.13
0.44 + 0.33
0.45 f 0.36
0.49 * 0.35
Mean k SD
The thermodependent coefficient was calculated from the slope of the linear regression line. at temperatures higher than 3OC [Fig. 5(D)], and the response of two units decreased linearly with the rise in temperature. The thermodependent coefficients are shown in Table 2(B). There was no significant
difference among the three phases in the low or high temperature range (paired f test, p c 0.05). Table 2. Thermal effect on the rising- (a, a’), transient- (6, b’) and static-(c, c’) phase responses of the intermediate- (A) and low temperature (B) PM units on mechanical stimulation of the canine tooth of the cat in a trapezoidal waveform Low range Unit No. 19 20 21 22 23 24 25 26 Mean &
a
b
(A) 1.60 1.38 0.70 0.56 0.50 0.42 0.56 0.50 0.78 * 0.45
High range C
a’
0.83 Zb 0.36
0.96 O?S
-1.21 k 0.72
Low range Unit No.
a
27 28 29 30
0.42 0.50 -
Mean
0.46 f 0.06
8%
b’
Intermediate-temperature units 1.40 1.60 -0.98 -0.78 1.34 1.30 -2.70 -2.80 0.90 1.18 -1.12 -1.16 0.44 0.46 -0.98 - 1.00 0.58 0.90 -1.86 -1.58 0.78 0.92 -0.64 -1.02 0.58 0.62 -0.90 -0.50 0.60 0.70 -0.52 -0.50
b
c’ -0.80 -2.30 -1.10 -0.82 -1.36 -1.00 -0.90 -0.50
-1.17
-1.10
0;s
0:s
High range C
a’
(B) Low-temperature units 0.18 0.36 -3.00 0.40 0.50 -1.90 -0.21 -0.14 0.29
0.43
0:6
o:o
-1.31 I!Z 1.39
b’
c’
-3.20 -2.20 -0.28 -0.14
-2.00 -2.30 -0.25 -0.16
-1.46 -1.18 + 1.50 I?3
The thermodependent coefficient was calculated from the slope of the linear regression line.
DISCUSSION
A rise in the tooth temperature induced a rise in periodontium temperature, but there was a slight difference between them. This difference may result from the thickness and thermal conductivities of the dentine and cementum present between the pulpal cavity and periodontal ligament. Conceivably, if the temperature of the pulpal cavity were changed rapidly or transiently, it would have no effect on the periodontal mechanoreceptor. The tooth temperature was therefore changed very slowly at the rate of 0.3”C/min. The cross-over point of the tooth and periodontium temperatures was 31°C; lower than the cat’s body temperature of 37-38°C. Because the animal’s mouth was open during the experiments and the room temperature was 17-18°C the low periodontium temperature may be the result of the low room temperature. There is also the possibility that the response properties of PM units examined when the mouth was kept open during the long period of experimentation differ somewhat from those examined when the mouth was closed, during which latter period the periodontium temperature nearly equalled the body temperature. The response of a superior alveolar nerve bundle evoked by mechanical tooth stimulation increased linearly with the rise in the tooth temperature between 10 and 45°C. A similar thermal effect on the spike frequency of a single nerve fibre was found in only 43% of the PM units affected by the tooth temperature. In more than half (57%) of PM units, the optimal tooth temperatures were distributed almost equally over the wide range of 15-45°C. These PIM units had their own peculiar thermodependent properties, which differed from those of the nerve bundle. A similar thermal modulation has been reported for several types of mechanoreceptors: the touch receptor (Hunt and McIntyre, 1960; Wall, 1960; Casey and Hahn, 1970) Pacinian corpuscle (Ishiko and Loewenstein, 1960, 1961; Inman and Peruui, 1961), muscle spindle (Lippold, Nicholls and Redfearn, 1960; Ottoson, 1965; Sato, 1983) and periosteum free-fibre ending (Sakada and Nemoto, 1972). In preliminary experiments (Tabata and Karita, 1984), we classified PM units into one of three groups on the basis of whether the optimal tooth temperature was high, intermediate or low. In the present experiments, about half of the PM units were the high-temperature type, the majority of these units having optimal tooth temperatures 6 45’C. Miller et al. (1989) studied the thermal effect on responses of periodontal mechanoreceptors evoked by mechanical tooth stimulation. They pared the alveolar bone that overlays the mechanoreceptor down to a tissuepaper thin layer and changed the temperature of the receptor by perfusing isotonic saline at various temperatures over the receptor site. The optimal temperature ranged from about 39-43’C. Those mechanoreceptors may correspond to the hightemperature PM units found in our experiments. Functionally, it is logical that PM units which fire most actively at near body temperature should be the most abundant. In the type II endings of hairy skin, however, the frequency of spontaneously discharging
T. TABATAand
880
spikes is maximal at 29°C (Burton et al., 1972) and the response elicited by sustained pressure also is maximal at 27°C (Chambers et al., 1972). Therefore, the optimal temperature of the periodontal mechanoreceptors is considered to be about 10°C higher than that of the type II receptors. Unlike the type II endings, the PM units did not produce thermodependent spontaneous discharges. The threshold stimulus intensity of the PM units was low in the vicinity of the optimal tooth temperature. This low intensity is similar to that of the muscle spindle (Lippold et al., 1960) but differs from that of type I receptors whose threshold intensities were unchanged at various skin temperatures (Tapper, 1965). The elevation of the stimulus-response curve of the PM units with a rise in temperature, however, was similar to that of the cutaneous type I receptor (Tapper, 1965; Casey and Hahn, 1970). Tapper (1965) and Casey and Hahn (1970) reported that the response of type I receptors evoked by mechanical ramp or sinusoidal stimulation increased with temperature. Because these responses of type I receptors correspond to the rising-phase responses of the PM units in our experiments, the thermal modulation of type I receptors must be similar to that in high-temperature PM units. The thermal effect on rising-, transient- and static-phase responses of type II endings, however, is not known. In the PM units, the thermodependent coefficients were nearly the same in the rising, transient and static phases of individual units, although the optima1 tooth temperature and thermodependent coefficients differed. The mean coefficient value for the intermediate-temperature units was higher than that of the high-temperature units. The thermodependent response pattern of the intermediate-temperature units resembled that of the type II endings in the skin (Burton et al., 1972; Chambers et al., 1972). The mean conduction velocity of PM units is reported to range from 28 to 83 m/s, most fibres conducting at rates between 44 and 50m/s; i.e. the range of A fibres (Pfaffmann, 1939; Hannam, 1968; Mei, Hartmann and Aubert, 1977; Linden, 1978). The PM units in our experiments therefore are thought to differ from non-specific, nociceptive C fibres (Weddel and Miller, 1962; Burgess and Perl, 1973). Thirteen % of the PM units affected by the tooth temperature discharged spontaneously at temperatures near the optimal tooth temperature. These PM units seem to correspond to the non-specific A fibre group responsive to both mechanical and thermal stimuli (Weddell and Miller, 1962). Our findings on the thermal effect on the activity of PM units suggest that the periodontal sensation to mechanical tooth stimulation changes with the tooth temperature. Psychophysical observations in support of our findings, such as change in the hardness sensation when a human bites foods at different temperatures, have yet to be reported.
K.
KARITA
Burton H., Terashima S. and Clark J. (1972) Response properties of slowly adapting mechanoreceptors to temperature stimulation in cats. Brain Res. 45, 401-416.
Byers M. R. (1985) Sensory innervation of periodontal ligament of rat molars consists of unencapsulated Ruffinilike mechanoreceptors and free nerve endings. J. camp. Neurol. 231, 500-5 18.
Byers M. R., O’Connor T. A., Martin R. F. and Dong W. K. (1986) Mexncephalic trigeminal sensory neurons of cat: axon pathways and structure of mechanoreceptive endings in periodontal ligament. J. camp. Neurol. 250, 181-191. Cash R. M. and Linden R. W. A. (1982) The distribution of mechano-receptors in the periodontal ligament of the mandibular canine tooth of the cat. J. Physiol., Lond. 330, 439-447.
Casey D. E. and Hahn J. F. (1970) Thermal effects on response of cat touch corpuscle. Expl Neurol. 28, 35-45.
Chambers M. R., Andres K. H., Duering V. M. and Iggo A. (1972) The structure and function of the slowly adapting type II mechanoreceptor in the hairy skin. Q. Jl Exp. Physiol. 57, 417-415.
Halata Z. (1988) RuiTini corpuscles-a stretch receptor in the connective tissue of the skin and locomotion apparatus. Pro. Brain Res. 74, 221-229. Hannam A. Ci. (1968) The conduction velocity of nerve impulses from dental mechanoreceptors in the dog. Archs oral Biol. 13, 1377-1383.
Hannam A. G. (1970) Receptive fields of periodontal mechanosensitive units in the dog. Archs oral Biol. 15, 971-978. Hannam A. G. (1982) The innervation of the periodontal ligament. In The Periodontal Ligament in Health and Disease (Eds Berkovitz B. K. B., Maxham B. J. and Neuman H. N.), pp. 173-196. Pergamon Press, Oxford. Hunt C. C. and McIntyre A. K. (1960) Properties of cutaneous touch receptors in the cat. J. Physiol., Lond. 153, 88-98.
Iggo A. (1969) Cutaneous thermoreceptors in primates and subprimates. J. PhIsiol., Lond. 200, 403-430. Inman D. R. and Peruzzi P. (1961) The effects of temperature on the responses of Pacinian corpuscles. J. Physiol., Lond. 155, 280-301.
Ishiko N. and Loewenstein W. R. (1960) Temperature and change transfer in a receptor membrane. Science 132, 1841-1842. Ishiko N. and Loewenstein W. R. (1961) Effects of temperature on the generator and action potentials of a sense organ. J. gen. Ph.vsiol. 45, 105-124. Linden R. W. A. (1978) Properties of intraoral mechanoreceptors represented in the mesencephalic nucleus of the fifth nerve in the cat. J. PhTsiol., Lond. 279, 395-408. Linden R. W. A. (1990) Periodontal mechanoreceptors and their functions. In Neurophysiology of the Jaws and Teerh (Ed. Taylor A.), pp. 52-95. MacMillan Press, New York. Linden R. W. A. and Millar B. J. (1987) Effect of temperature on the discharge of periodontal ligament mechanoreceptors in cat canme tooth. J. dent. Res. 66, 862, Abstract No. 247. Linden R. W. A. and Millar B. J. (1988a) The response characteristics of mechanoreceptors related to their position in the cat canine periodontal ligament. Archs oral Biol. 33, 52-56.
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Burgess P. R. and Per1 E. R. (1973) Cutaneous mechanoreceptors and nociceptors. In Handbook of Sensory Physiology, II. Somatosensory System (Ed. Iggo A.), pp. 29-78. Springer, Berlin.
Lippold 0. C. J., Sicholls J. G. and Redfearn J. W. T. (1960) A study of the afferent discharge produced by cooling a mammalian muscle spindle. J. Physiol., Lond. 153, 2 18-23 1.
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Thermal effect on periodontal receptors Mei N., Hartmann F. and Aubert M. (1977) Periodontal mechanoreceptors involved in pain. In Pain in rhe Trigeminal Region (Eds Anderson D. J. and Matthews B.), pp. 103-I 10. Elsevier/North-holland Biomedical Press, Amsterdam. Millar B. J., Halata Z. and Linden R. W. A. (1989) The structure of physiologically located periodontal ligament mechanoreceptors of the cat canine tooth. J. Anat. 167, 117-127. Ottoson D. (1965) The effects of temperature on the isolated muscle spindle. J. Physiol., Land. 180, 636-648. Pfaffmann C. (1939) Afferent impulses from the teeth due to pressure and noxious stimulation. J. Physiol., Land. 97, 207-219.
Sakada S. and Nemoto T. (1972) Response to thermal stimulation of fast- and slow-adapting free-fiber ending
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units in the cat mandibular periosteum. Bull. Tokyo dent. CON. 13, 227-250. Sato H. (1983) Effects of skin cooling and warming on stretch responses of the muscle spindle primary and secondary afferent fibers from the cat’s tibialis anterior. Expl Neurol. 81, 446-458. Tabata T. and Karita K. (1984) The effect of tooth temperature on the activity of the periodontal mechanoreceptor in the cat. J. Physiol. Sot. Japan 46 (Suppl.), s455. Tapper D. N. (1965) Stimulus-response relationships in the cutaneous slowly-adapting mechanoreceptor in hairy skin of the cat. Expl Neurol. 13, 364-385. Wall P. D. (1960) Cord cells responding to touch, damage, and temperature of skin. J. keurophjsiol. 23, 197-210. Weddeil G. and Miller S. (1962) Cutaneous sensibility. A. Rev. Physiol. 24, 199-222.