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Conduction velocities in afferent fibers from feline tooth pulp
ESPERIMEKTAL
NEUROLOGY
43, 281-283
(19i4)
RESEARCH Conduction
Velocities KENNETH
Departwent
NOTE
in Afferent V.
of Anatomy,
Fibers from
ANDERSON Emory
Received
AND University,
Decewber
GARY Atlanta,
S.
Feline
Tooth
PEARL
1
Georgia
30322
Pulp
21,1973
In analyzing the anatomy and physiology of sensory systems, it is often necessary to activate the particular system being studied with appropriate stimulation. In experiments in which this is necessary, the stimulation presented should be specific to the sensory system under study. With the pain system, however, this is most difficult, since most stimuli that activate nociceptive pathways also activate other pathways, such as those that mediate touch and pressure sensations. Activation of the tooth pulp would appear to be a type of stimulation that might be either primarily or exclusively noxious in quality, since, in man at least, the tooth pulp is a structure which has been demonstrated to give rise only to pain or prepain sensations when stimulated, whether the stimulation consisted of thermal changes, mechanical pressure, or electric pulses (9). In the present study, which is part of a broad program of research designated to study nociceptive mechanisms systematically, we have attempted to determine whether tooth pulp stimulation might be a relatively specific way to activate nociceptive pathways. To accomplish this we have determined the degree to which A-delta and C fibers, which are thought to play an important role in mediating nociceptive information (1, 4, 7), are activated by stimulation of the tooth pulp. Conduction velocities within the maxillary and mandibular nerves were determined in cats after stimulation of the appropriate teeth. All cats in this experiment were anesthetized with pentobarbital sodium (35 mg/kg) and immobilized with Flaxedil (3-5 mg/kg). The animals were artificially respirated and body temperature was maintained with a 1 This investigation was supported by Grant MH23499 from NIMH and by Grant MH16077, a Research Scientist Award, to KVA, also from NIMH. Publication No. 1188, Department of Anatomy, Division of Basic Health Sciences, Emory University. The authors express their appreciation to Mr. Clegg Honeycutt for his assistance in this research. 281 Copyright 0 1974 by Academic Press, Inc. All rights of reproduction in any l~rn rexrved
282
ANDERSON
AND
PEARI.
thermostatically controlled heating pad. Cardiac rate, pupil size, and appearance of peripheral vessels were periodically monitored to ensure that the physiological condition of the animal was satisfactory. Bipolar electrodes were implanted in the tooth pulp of upper or lower canine teeth (or both). The electrodes were made of Teflon-coated, 29-gauge copper wire and were fixed in place with dental impression compound, The details of the electrode implantation technique have been described (8). Recordings from the mandibular and maxillary nerves were made with concentric, bipolar electrodes that were positioned stereotaxically. In some cases, the nerves themselves were stimulated and recordings were made from the tooth electrodes. This enabled us to compare orthodromically and antidromically elicited conduction velocities. In some cases responses were averaged using a PDP S/L computer in order to assure an accurate assessment of small-amplitude components in the compound action potentials and to allow latencies to be determined as precisely as possible. At the end of each experiment, the nerves studied were dissected free and the distance between various stimulating and recording electrodes measured to enable conduction velocities to be calculated. Evoked potentials were readily recorded in every animal in the first-order trigeminal fibers after stimulation of the canine teeth. Each evoked potential that resulted from stimulation of the teeth had two relatively distinct peaks; the first peak usually had a larger amplitude and shorter duration than the second peak (Fig. 1) . The conduction velocities in the maxillary nerves of 21 cats ranged from 1.74-61.0 m/set, with an average of 15.2 m/set. The conduction velocities in the mandibular nerves of eight cats ranged from 2.28 to 55.2 m/set, with an average of 12.3 m/set. Orthodromic and
FIG. 1. Orthodromic (Frame A) and antidromic (Frame B) responses in first-order trigeminal afferent fibers after stimulation of the canine teeth. Note that responses evoked antidromically were recorded at a slower sweep speed than those evoked orthodromically. This was done so that responses recorded in the teeth could be easily observed and measured, since they were typically of smaller amplitude and of longer duration than those recorded in the nerve. Time calibration represents 2 msec in A and 10 msec in B. Amplitude calibration is 50 pv.
TOOTH
PULP
AFFERENTS
283
anticlromic conduction velocities were similar in all cases (Fig. 1). These data indicate that stimulation of the teeth results primarily in the activation of small-diameter fibers and that much of the information traveling to the central nervous system from the teeth is carried by A-delta and C fibers, with most being carried by A-delta fibers. The findings from our electrophysiological study, and from other similar studies reported previously (3, 6, 10, 11)) are consistent with the findings in anatomical studies (2, 5, 12, 13), which have demonstrated that about 64% of the fibers entering the tooth pulp are less than 6 pm in diameter and none has a diameter greater than 10pm. Since stimulation of the teeth results primarily in the activation of small-diameter afferent fibers, it would appear that tooth pulp stimulation is an effective and relatively selective means of activating cranial nociceptive pathways. REFERENCES 1. BESSOU, P., and E. PERL. 1969. Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli. J. Neurophysiol. 32: 1025-1043. 2. BRASHEAR, A. 1936. The innervation of the teeth. J. Covnp. Neural. 64: 169-185. 3. BROOKHART, J., W. LIVINGSTON, and F. HAUGEN. 1953. The functional characteristics of afferent fibers from tooth pulp of cat. J. Nezlrophysiol. 16: 634-642. 4. COLLINS, W., and F. NULSEN. 1962. Studies on sensation interpreted as pain: Central nervous system pathways. Ch. Neurosurg. 8 : 271-278. 5. DELAKGE, A., A. HANNAI\I, and B. MATTHEWS. 1969. The diameters and conduction velocities of fibers in the terminal branches of the inferior dental nerve. ‘lrch. Oral Biol. 14: 513-520. 6. GREENWOOD, F., H. HORIUCHI, and B. MATTHEWS. 1972. Electrophysiological evidence on the types of nerve fibers excited by electrical stimulation of teeth with a pulp tester. .Irch. Oral Biol. 17: 701-709. 7. HEINBECKER, P., G. BISHOP, and J. O’LEARY. 1933. Pain and touch fibers in peripheral nerves. Arch. Neural. Psychiat. 29 : 771-789. 8. MAHAN, P. E., and R. V. ANDERSON. 1970. Activation of pain pathways in animals. Amv-. J. .411nt. 128: 235-238. 9. MU~~FORD, J. M. 1965. Pain perception threshold and adaptation of normal human teeth. drch. Oral Biol. 10: 957-968. 10. PFAFFMAN, C. 1939. Afferent impulses from the teeth due to pressure and noxious stimulation. J. Physiol. 97 : 207-219. 11. WAGERS, P., and C. SMITH. 1960. Responses in dental nerves of dogs to tooth stimulation and the effects of systemically administered procaine, lidocaine, and morphine. J. Pkarwacol. E.rp. Ther. 130: 89-105. 12. WINDLE, W. 1927. Experimental proof of the types of neurons that innervate the tooth pulp. J. Coriip. Ncrwol. 43 : 347-356. 13. YOUNG, R. F., and R. B. KING. 1973. Fiber spectrum of the trigeminal sensory root of the baboon determined by electron microscopy. J. Neurosurg. 38: 65-72.
NEUROLOGY
43, 281-283
(19i4)
RESEARCH Conduction
Velocities KENNETH
Departwent
NOTE
in Afferent V.
of Anatomy,
Fibers from
ANDERSON Emory
Received
AND University,
Decewber
GARY Atlanta,
S.
Feline
Tooth
PEARL
1
Georgia
30322
Pulp
21,1973
In analyzing the anatomy and physiology of sensory systems, it is often necessary to activate the particular system being studied with appropriate stimulation. In experiments in which this is necessary, the stimulation presented should be specific to the sensory system under study. With the pain system, however, this is most difficult, since most stimuli that activate nociceptive pathways also activate other pathways, such as those that mediate touch and pressure sensations. Activation of the tooth pulp would appear to be a type of stimulation that might be either primarily or exclusively noxious in quality, since, in man at least, the tooth pulp is a structure which has been demonstrated to give rise only to pain or prepain sensations when stimulated, whether the stimulation consisted of thermal changes, mechanical pressure, or electric pulses (9). In the present study, which is part of a broad program of research designated to study nociceptive mechanisms systematically, we have attempted to determine whether tooth pulp stimulation might be a relatively specific way to activate nociceptive pathways. To accomplish this we have determined the degree to which A-delta and C fibers, which are thought to play an important role in mediating nociceptive information (1, 4, 7), are activated by stimulation of the tooth pulp. Conduction velocities within the maxillary and mandibular nerves were determined in cats after stimulation of the appropriate teeth. All cats in this experiment were anesthetized with pentobarbital sodium (35 mg/kg) and immobilized with Flaxedil (3-5 mg/kg). The animals were artificially respirated and body temperature was maintained with a 1 This investigation was supported by Grant MH23499 from NIMH and by Grant MH16077, a Research Scientist Award, to KVA, also from NIMH. Publication No. 1188, Department of Anatomy, Division of Basic Health Sciences, Emory University. The authors express their appreciation to Mr. Clegg Honeycutt for his assistance in this research. 281 Copyright 0 1974 by Academic Press, Inc. All rights of reproduction in any l~rn rexrved
282
ANDERSON
AND
PEARI.
thermostatically controlled heating pad. Cardiac rate, pupil size, and appearance of peripheral vessels were periodically monitored to ensure that the physiological condition of the animal was satisfactory. Bipolar electrodes were implanted in the tooth pulp of upper or lower canine teeth (or both). The electrodes were made of Teflon-coated, 29-gauge copper wire and were fixed in place with dental impression compound, The details of the electrode implantation technique have been described (8). Recordings from the mandibular and maxillary nerves were made with concentric, bipolar electrodes that were positioned stereotaxically. In some cases, the nerves themselves were stimulated and recordings were made from the tooth electrodes. This enabled us to compare orthodromically and antidromically elicited conduction velocities. In some cases responses were averaged using a PDP S/L computer in order to assure an accurate assessment of small-amplitude components in the compound action potentials and to allow latencies to be determined as precisely as possible. At the end of each experiment, the nerves studied were dissected free and the distance between various stimulating and recording electrodes measured to enable conduction velocities to be calculated. Evoked potentials were readily recorded in every animal in the first-order trigeminal fibers after stimulation of the canine teeth. Each evoked potential that resulted from stimulation of the teeth had two relatively distinct peaks; the first peak usually had a larger amplitude and shorter duration than the second peak (Fig. 1) . The conduction velocities in the maxillary nerves of 21 cats ranged from 1.74-61.0 m/set, with an average of 15.2 m/set. The conduction velocities in the mandibular nerves of eight cats ranged from 2.28 to 55.2 m/set, with an average of 12.3 m/set. Orthodromic and
FIG. 1. Orthodromic (Frame A) and antidromic (Frame B) responses in first-order trigeminal afferent fibers after stimulation of the canine teeth. Note that responses evoked antidromically were recorded at a slower sweep speed than those evoked orthodromically. This was done so that responses recorded in the teeth could be easily observed and measured, since they were typically of smaller amplitude and of longer duration than those recorded in the nerve. Time calibration represents 2 msec in A and 10 msec in B. Amplitude calibration is 50 pv.
TOOTH
PULP
AFFERENTS
283
anticlromic conduction velocities were similar in all cases (Fig. 1). These data indicate that stimulation of the teeth results primarily in the activation of small-diameter fibers and that much of the information traveling to the central nervous system from the teeth is carried by A-delta and C fibers, with most being carried by A-delta fibers. The findings from our electrophysiological study, and from other similar studies reported previously (3, 6, 10, 11)) are consistent with the findings in anatomical studies (2, 5, 12, 13), which have demonstrated that about 64% of the fibers entering the tooth pulp are less than 6 pm in diameter and none has a diameter greater than 10pm. Since stimulation of the teeth results primarily in the activation of small-diameter afferent fibers, it would appear that tooth pulp stimulation is an effective and relatively selective means of activating cranial nociceptive pathways. REFERENCES 1. BESSOU, P., and E. PERL. 1969. Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli. J. Neurophysiol. 32: 1025-1043. 2. BRASHEAR, A. 1936. The innervation of the teeth. J. Covnp. Neural. 64: 169-185. 3. BROOKHART, J., W. LIVINGSTON, and F. HAUGEN. 1953. The functional characteristics of afferent fibers from tooth pulp of cat. J. Nezlrophysiol. 16: 634-642. 4. COLLINS, W., and F. NULSEN. 1962. Studies on sensation interpreted as pain: Central nervous system pathways. Ch. Neurosurg. 8 : 271-278. 5. DELAKGE, A., A. HANNAI\I, and B. MATTHEWS. 1969. The diameters and conduction velocities of fibers in the terminal branches of the inferior dental nerve. ‘lrch. Oral Biol. 14: 513-520. 6. GREENWOOD, F., H. HORIUCHI, and B. MATTHEWS. 1972. Electrophysiological evidence on the types of nerve fibers excited by electrical stimulation of teeth with a pulp tester. .Irch. Oral Biol. 17: 701-709. 7. HEINBECKER, P., G. BISHOP, and J. O’LEARY. 1933. Pain and touch fibers in peripheral nerves. Arch. Neural. Psychiat. 29 : 771-789. 8. MAHAN, P. E., and R. V. ANDERSON. 1970. Activation of pain pathways in animals. Amv-. J. .411nt. 128: 235-238. 9. MU~~FORD, J. M. 1965. Pain perception threshold and adaptation of normal human teeth. drch. Oral Biol. 10: 957-968. 10. PFAFFMAN, C. 1939. Afferent impulses from the teeth due to pressure and noxious stimulation. J. Physiol. 97 : 207-219. 11. WAGERS, P., and C. SMITH. 1960. Responses in dental nerves of dogs to tooth stimulation and the effects of systemically administered procaine, lidocaine, and morphine. J. Pkarwacol. E.rp. Ther. 130: 89-105. 12. WINDLE, W. 1927. Experimental proof of the types of neurons that innervate the tooth pulp. J. Coriip. Ncrwol. 43 : 347-356. 13. YOUNG, R. F., and R. B. KING. 1973. Fiber spectrum of the trigeminal sensory root of the baboon determined by electron microscopy. J. Neurosurg. 38: 65-72.