Brain Research, 113 ( 1976) 83-94
83
© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
SENSORY A N D R E F L E X RESPONSES TO T O O T H PULP S T I M U L A T I O N IN MAN
BRUCE MATTHEWS, JILL BAXTER and STEVEN WATTS Department of Physiology, The Medical School, University Walk, Bristol BS8 1TD (Great Britain)
(Accepted January 22nd, 1976)
SUMMARY Experiments have been carried out to investigate whether all tooth pulp afferent nerves are capable of producing pain. Monopolar and bipolar stimuli were applied to teeth in human subjects and sensory thresholds determined. EMGs were recorded from the masseter and the anterior digastric muscles. With stimuli up to three times the sensory threshold, no response could be detected in the digastric but at, or just above, the sensory threshold, inhibitory effects were produced in masseter muscle. The latency of the muscle respons~ with bipolar stimulation was 18-22 msec. There was no evidence of stimulus spread to nerves outside the teeth. Bipolar and monopolar stimulation both produced the same sensation but this was not described as painful. It is concluded that some pulpal afferent nerves may not be capable of producing pain, and that the sensory and reflex responses at threshold were probably produced by the same fibres.
INTRODUCTION Most of the evidence from human experiments indicates that pain is the only sensation produced by thermal, osmotic or chemical stimulation of dentine or the dental pulp 1,9 and for this reason electrical stimulation of teeth is often used as a convenient test stimulus in experiments designed to investigate pain mechanisms. However, it has not been established that such a stimulus excites only nerves which produce pain; some pulpal afferents may subserve functions unrelated to pain while others may be involved in pain, in that they can cause facilitation or inhibition of transmission through the pain pathway, without forming the primary excitatory input which evokes the sensation. An additional uncertainty arises in some experiments in which monopolar stimulation of teeth has been used, since with this there is a risk of exciting nerves around the teeth, due to stimulus spread, as well as in the pulpg,16,4o.
84 The experiments to be described were carried out to determine if electrical stimulation of pulpal nerves in man produces a jaw opening reflex similar to that which is produced in the cat 22,27,2s. If so, it was thought that a comparison between the threshold of the reflex and the sensory threshold to pulp stimulation might provide some information on the types of fibres involved in the two responses. Experiments were also carried out to assess the risk of stimulus spread to the tissues around the teeth. METHODS EMGs were recorded with surface electrodes from the right masseter and the region of the anterior belly of the right digastric in three subjects, and from just the right masseter in a further 8 subjects. The subjects were aged between 20 and 30 years. In each subject, recordings were made both with the jaw muscles relaxed and with a constant level of background activity in the masseter muscle which was achieved by the subject biting on a rubber bung between his left posterior teeth. To help the subject maintain a stable level of activity in the muscle, either the masseter E M G was reproduced through a loudspeaker or the pressure in a cavity in the bung was displayed in front of him on a manometer. Bipolar or monopolar stimuli were applied once a second to the upper left or right central incisor using a constant current stimulator which produced rectangular pulses with an amplitude of up to 500 #A and a duration of 10 msec. A stimulus duration of 10 msec was selected because this appeared to place minimal demands on the voltage which had to be made available for applying bipolar, constant current pulses through intact teeth. The stimulator was of the same type as that used in a previous study 31. The electrodes used for bipolar stimulation consisted of two pieces of 1.5 mm diameter stainless steel rod with flat ends which were insulated with sleeving down to their tips and mounted with their centres 4 mm apart on an insulated holder. Each tooth was dried carefully with cotton wool before stimulation. The tips of the electrodes were covered with a thin layer of toothpaste to ensure good electrical contact with the tooth and were applied to the labial surface of the tooth, one on either side of its long axis, midway between the incisal edge and the gingival margin. The tooth electrode used for monopolar stimulation had a diameter of 2,5 mm and was applied to the centre of the crown of the tooth and the indifferent electrode (the anode) was held in the subject's hand. With both forms of stimulation, the sensory threshold was determined by applying stimuli continuously while increasing and decreasing the stimulus intensity several times through threshold. The threshold was defined as the minimum intensity which consistently produced a sensation when the stimulus was being increased from below threshold. The subject indicated when the stimulus was felt either by a prearranged hand signal or by pressing a button which produced a signal on the oscilloscope. The loudspeaker used to monitor the E M G was disconnected during sensory threshold determinations and the subject could not see the oscilloscope or the stimulus control. With each positioning of the stimulating electrode, the sensory and reflex thresholds and the latency of the muscle response
85 were determined. These meaurements were repeated several times for each tooth with the electrode repositioned each time. To look for evidence of stimulus spread, bipolar and monopolar stimuli were applied to the dried mucous membrane 3-4 mm above the gingival margin over the root of the right central incisor. These tests were carried out on three of the subjects used in the experiments described above. The electrodes were the same as those used for stimulating the teeth except that their tips were modified by the addition of a short length of soft plastic tubing to avoid discomfort from pressure on the mucous membrane. The tubing projected beyond the end of the electrode to form a small cup which was filled with saline electrode jelly. In another subject, bipolar and monopolar stimuli were applied to a pulpless, root-filled upper right central incisor and to the vital tooth on the other side. RESULTS With a relaxed subject, there was no detectable response in either the masseter or the digastric muscles to tooth stimulation at intensities up to three times the sensory threshold. However, if stimuli were applied while the subject contracted his masseter muscle, inhibitory effects could be demonstrated which had a threshold which was about the same as the sensory threshold to the same form of stimulus. A typical result obtained with bipolar stimulation of the ipsilateral upper central incisor is shown in Fig. 1. As the stimulus intensity increased, the subject first reported a sensation at 9 #A but with this stimulus there was no evidence of a response in the masseter EMG. However, when the stimulus intensity was increased to 10 #A, a consistent silent period was produced in the EMG. As the stimulus was increased further from 10 to 15 #A, this silencing of the muscle became more complete and a second silent period became apparent. Betweeen the two silent periods the amplitude of the E M G often exceeded that present in control sweeps and, in other subjects, there was sometimes evidence of synchronisation of the waveform in successive oscilloscope sweeps at this time. Occasionally there was evidence of a similar synchronized component immediately preceding the first silent period, as for example with stimuli of 10 #A in Fig. 1. The threshold of the muscle response was defined as the smallest stimulus which produced an obvious decrease in the amplitude of the E M G in at least 3 out of 5 successive traces stored on the oscilloscope screen. The latency of the first silent period was difficult to measure because its onset could not be defined precisely. Measurements were made to the point at which the envelope produced by several superimposed traces showed an abrupt decrease in width and in the example shown in Fig. 1 this was at approximately 21 msec. The latency did not decrease significantly with increase in stimulus intensity up to 1.5 times threshold. The latency of the second silent period was about 55 msec. In all 5 subjects tested, the thresholds of the masseter inhibition with bipolar stimulation of the ipsilateral tooth were significantly greater than the corresponding sensory thresholds, although the differences were not large (Table I). The significance of differences between paired observations was determined using the t-test. Provided
86
9~A
10 uA
12 pA
15 IJA
t
0,2 my
10 m s
Fig. 1. E M G s recorded from the right masseter muscle during voluntary contraction o f the muscle. Bipolar electrical stimuli at the intensities shown were applied once a second t o the upper right central incisor 5 msec after the oscilloscope sweep was triggered. Five successive traces were superimposed in each record.
the electrodes remained in a constant position on the tooth, the thresholds were generally stable and any variation between repeated determinations appeared to be due principally to inconsistencies in repositioning the electrodes on the tooth and affected both the sensory and reflex thresholds equally. The latency of the first silent period was 18-22 msec. Bipolar stimulation of the contralateral teeth gave essentially the same results although in 3 of the 9 subjects the difference was not significant. With monopolar stimulation (Table II) the reflex thresholds were significantly higher than the sensory thesholds for 6 of the 10 teeth, although again the differences were not large. In another 3 teeth, the thresholds were not significantly different and, in one, the sensory thesholds were on average the higher by a small amount. The latency of the first silent period was 15-20 msec. The latency o f the second silent period with both forms of stimulation was 50-60 msec. Out of a total of 198 threshold determinations, in 142 the reflex threshold was higher than the sensory threshold by a factor of up to 1.3; in 40 no difference between
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83
© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
SENSORY A N D R E F L E X RESPONSES TO T O O T H PULP S T I M U L A T I O N IN MAN
BRUCE MATTHEWS, JILL BAXTER and STEVEN WATTS Department of Physiology, The Medical School, University Walk, Bristol BS8 1TD (Great Britain)
(Accepted January 22nd, 1976)
SUMMARY Experiments have been carried out to investigate whether all tooth pulp afferent nerves are capable of producing pain. Monopolar and bipolar stimuli were applied to teeth in human subjects and sensory thresholds determined. EMGs were recorded from the masseter and the anterior digastric muscles. With stimuli up to three times the sensory threshold, no response could be detected in the digastric but at, or just above, the sensory threshold, inhibitory effects were produced in masseter muscle. The latency of the muscle respons~ with bipolar stimulation was 18-22 msec. There was no evidence of stimulus spread to nerves outside the teeth. Bipolar and monopolar stimulation both produced the same sensation but this was not described as painful. It is concluded that some pulpal afferent nerves may not be capable of producing pain, and that the sensory and reflex responses at threshold were probably produced by the same fibres.
INTRODUCTION Most of the evidence from human experiments indicates that pain is the only sensation produced by thermal, osmotic or chemical stimulation of dentine or the dental pulp 1,9 and for this reason electrical stimulation of teeth is often used as a convenient test stimulus in experiments designed to investigate pain mechanisms. However, it has not been established that such a stimulus excites only nerves which produce pain; some pulpal afferents may subserve functions unrelated to pain while others may be involved in pain, in that they can cause facilitation or inhibition of transmission through the pain pathway, without forming the primary excitatory input which evokes the sensation. An additional uncertainty arises in some experiments in which monopolar stimulation of teeth has been used, since with this there is a risk of exciting nerves around the teeth, due to stimulus spread, as well as in the pulpg,16,4o.
84 The experiments to be described were carried out to determine if electrical stimulation of pulpal nerves in man produces a jaw opening reflex similar to that which is produced in the cat 22,27,2s. If so, it was thought that a comparison between the threshold of the reflex and the sensory threshold to pulp stimulation might provide some information on the types of fibres involved in the two responses. Experiments were also carried out to assess the risk of stimulus spread to the tissues around the teeth. METHODS EMGs were recorded with surface electrodes from the right masseter and the region of the anterior belly of the right digastric in three subjects, and from just the right masseter in a further 8 subjects. The subjects were aged between 20 and 30 years. In each subject, recordings were made both with the jaw muscles relaxed and with a constant level of background activity in the masseter muscle which was achieved by the subject biting on a rubber bung between his left posterior teeth. To help the subject maintain a stable level of activity in the muscle, either the masseter E M G was reproduced through a loudspeaker or the pressure in a cavity in the bung was displayed in front of him on a manometer. Bipolar or monopolar stimuli were applied once a second to the upper left or right central incisor using a constant current stimulator which produced rectangular pulses with an amplitude of up to 500 #A and a duration of 10 msec. A stimulus duration of 10 msec was selected because this appeared to place minimal demands on the voltage which had to be made available for applying bipolar, constant current pulses through intact teeth. The stimulator was of the same type as that used in a previous study 31. The electrodes used for bipolar stimulation consisted of two pieces of 1.5 mm diameter stainless steel rod with flat ends which were insulated with sleeving down to their tips and mounted with their centres 4 mm apart on an insulated holder. Each tooth was dried carefully with cotton wool before stimulation. The tips of the electrodes were covered with a thin layer of toothpaste to ensure good electrical contact with the tooth and were applied to the labial surface of the tooth, one on either side of its long axis, midway between the incisal edge and the gingival margin. The tooth electrode used for monopolar stimulation had a diameter of 2,5 mm and was applied to the centre of the crown of the tooth and the indifferent electrode (the anode) was held in the subject's hand. With both forms of stimulation, the sensory threshold was determined by applying stimuli continuously while increasing and decreasing the stimulus intensity several times through threshold. The threshold was defined as the minimum intensity which consistently produced a sensation when the stimulus was being increased from below threshold. The subject indicated when the stimulus was felt either by a prearranged hand signal or by pressing a button which produced a signal on the oscilloscope. The loudspeaker used to monitor the E M G was disconnected during sensory threshold determinations and the subject could not see the oscilloscope or the stimulus control. With each positioning of the stimulating electrode, the sensory and reflex thresholds and the latency of the muscle response
85 were determined. These meaurements were repeated several times for each tooth with the electrode repositioned each time. To look for evidence of stimulus spread, bipolar and monopolar stimuli were applied to the dried mucous membrane 3-4 mm above the gingival margin over the root of the right central incisor. These tests were carried out on three of the subjects used in the experiments described above. The electrodes were the same as those used for stimulating the teeth except that their tips were modified by the addition of a short length of soft plastic tubing to avoid discomfort from pressure on the mucous membrane. The tubing projected beyond the end of the electrode to form a small cup which was filled with saline electrode jelly. In another subject, bipolar and monopolar stimuli were applied to a pulpless, root-filled upper right central incisor and to the vital tooth on the other side. RESULTS With a relaxed subject, there was no detectable response in either the masseter or the digastric muscles to tooth stimulation at intensities up to three times the sensory threshold. However, if stimuli were applied while the subject contracted his masseter muscle, inhibitory effects could be demonstrated which had a threshold which was about the same as the sensory threshold to the same form of stimulus. A typical result obtained with bipolar stimulation of the ipsilateral upper central incisor is shown in Fig. 1. As the stimulus intensity increased, the subject first reported a sensation at 9 #A but with this stimulus there was no evidence of a response in the masseter EMG. However, when the stimulus intensity was increased to 10 #A, a consistent silent period was produced in the EMG. As the stimulus was increased further from 10 to 15 #A, this silencing of the muscle became more complete and a second silent period became apparent. Betweeen the two silent periods the amplitude of the E M G often exceeded that present in control sweeps and, in other subjects, there was sometimes evidence of synchronisation of the waveform in successive oscilloscope sweeps at this time. Occasionally there was evidence of a similar synchronized component immediately preceding the first silent period, as for example with stimuli of 10 #A in Fig. 1. The threshold of the muscle response was defined as the smallest stimulus which produced an obvious decrease in the amplitude of the E M G in at least 3 out of 5 successive traces stored on the oscilloscope screen. The latency of the first silent period was difficult to measure because its onset could not be defined precisely. Measurements were made to the point at which the envelope produced by several superimposed traces showed an abrupt decrease in width and in the example shown in Fig. 1 this was at approximately 21 msec. The latency did not decrease significantly with increase in stimulus intensity up to 1.5 times threshold. The latency of the second silent period was about 55 msec. In all 5 subjects tested, the thresholds of the masseter inhibition with bipolar stimulation of the ipsilateral tooth were significantly greater than the corresponding sensory thresholds, although the differences were not large (Table I). The significance of differences between paired observations was determined using the t-test. Provided
86
9~A
10 uA
12 pA
15 IJA
t
0,2 my
10 m s
Fig. 1. E M G s recorded from the right masseter muscle during voluntary contraction o f the muscle. Bipolar electrical stimuli at the intensities shown were applied once a second t o the upper right central incisor 5 msec after the oscilloscope sweep was triggered. Five successive traces were superimposed in each record.
the electrodes remained in a constant position on the tooth, the thresholds were generally stable and any variation between repeated determinations appeared to be due principally to inconsistencies in repositioning the electrodes on the tooth and affected both the sensory and reflex thresholds equally. The latency of the first silent period was 18-22 msec. Bipolar stimulation of the contralateral teeth gave essentially the same results although in 3 of the 9 subjects the difference was not significant. With monopolar stimulation (Table II) the reflex thresholds were significantly higher than the sensory thesholds for 6 of the 10 teeth, although again the differences were not large. In another 3 teeth, the thresholds were not significantly different and, in one, the sensory thesholds were on average the higher by a small amount. The latency of the first silent period was 15-20 msec. The latency o f the second silent period with both forms of stimulation was 50-60 msec. Out of a total of 198 threshold determinations, in 142 the reflex threshold was higher than the sensory threshold by a factor of up to 1.3; in 40 no difference between
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