EXPERIMENTAL

Pulpal

NEUROLOGY

Anodal

Ii. WAYNE

47, 22%239

(1975)

Blockade of Trigeminal by Tooth Stimulation FIELDS,

RICHARD

Biophysics Laboratwy, Ilcnltlz Sciences

Field Potentials in the Cat

B. TACKE,

AND BHIM

Child Study Clinic, Center, Portlaud,

Rccciwd

Nowlnhcr

University Oregon,

Elicited

SEN SAVARA 1 of Oregon 97201

5, 1974

Trigeminal field potentials elicited by monopolar and bipolar stimulation of the canine tooth pulp in the barbiturate-anesthetized cat were recorded to characterize the effects of direct current anodal blocks on pulpal excitability. Anodal blocking currents ranging as high as 50 w result in a dose-dependent attenuation of pulp excitability. An induction time, inversely related to the blocking current and lasting up to several minutes, is required for the establishment of a new steady-state level of excitability. Blocks of these low current intensities or of short duration are rapidly (seconds) reversible upnn block cessation. In general, blocking currents greater than 50 /la further attenuate pulpal excitability in a dose-dependent manner and if terminated immediately were also rapidly reversible. However, following any prolonged administration of these more intense blocking currents, pulpal excitability did not return to control values but was seen to fall within tens of seconds to some intermmediate value which was then maintained for the duration of the monitoring interval (10 min). For all intensities, application of the blocking current to the occlusal end of the tooth was required for the effects to be widespread throughout the pulp chamber.

INTRODUCTION There are both contemoprary and historical references to the use of electrical currents (d-c) for the control of orofacial pain. In the early twentieth century, studies are reported in which currents in the range of 30 ma were employed in the treatment of trigeminal neuralgia or at somewhat lower levels (2-S ma) for gingival anesthesia (1s). Other reports 1 This research was supported by the Dental Branch, United States Army Medical Research and Development Command, Contract No. DADA17-70-C-0075. We are indebted to Dr. Raymond Tsui for his expertise in experimental surgery and tooth preparations, to Mr. Reid Parkhurst for engineering support, and to Mrs. Virigina Varela for conduct of anesthesia. 229 Copyright All rights

0 1975 by Academic Press, of reproduction in any form

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show that direct currents similar to the latter intensities were used during the iontophoretic application of anesthetic agents (15, IS), a procedure which has recently been revived for the extraction of retained deciduous teeth (7). More modern studies indicate that direct currents have been widely employed in ionic desensitization procedures for treating hypersensitive teeth, as reviewed elsewhere (5). The most contemporary application of direct currents involved the incorporation of a power source and intensity control in a dental handpiece. A monoplar anodal current (indifferent electrode on the patient’s hand) is passed from the dental drill bit through the tooth to anesthetize the local site of electrode contact during cavity preparation (4, 14). The rationale is to create an anodal blockade (membrane hyperpolarization) of pulpal nerves or receptors, thus rendering these tissues inexcitable. The latter reports document moderate success using currents of 4-15 pa and even better results are shown using a similar electrode configuration and intensity but a monopolar periodically interrupted wave form ( 1). Quite recently, the results of a preliminary study using a Russian commercial device are reported in which anodal direct currents ranging to 60 pa applied through a dental drill are shown to be totally effective in eliminating pain during drilling tests (13). The latter findings are subsequently supported by the results of a behavioral experimental paradigm using similar current intensities but employing a reflexed as opposed to a perceptual index of pulp activation ( 16). The above studies seem to demonstrate the complete reversibility of anodal blockade of pulp afferent activity, since there are no reports of after-affects, and the behavioral tests are repeatable on multiple occasions. Nevertheless, there is reason to suspect that currents of especially 60 pa and possibly less, when passed through the unique structural architecture of the dental hard tissues to the pulp, may result in rather extreme, potentially damaging current densities (5). The present study reports the initial results of experiments designed to elucidate the neurophysiological characteristics and mechanisms of dental anodal blockade. METHODS The methodology used in the present study differs from that of a previous report (6) only in details of the particular experimental tests performed. Twenty-six young adult cats weighing 2-4 kg were anesthetized with sodium pentobarbital administered to effect with supplementary doses given as required. The animal was ventilated using a Bird Mark VIII system which provided auotmatic artificial ventilation on the animal’s demand (rarely triggered). Neuromuscular blocking agents were not employed. Intra-esophogeal temperature was maintained at 38 + 0.5 C by

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means of a heating pad with thermostatically controlled circulating water (Temp-Pump system, Gaymar Industries) and an esophogeal temperature monitor (YSI Model 43TA). A Beckman Model LB-2 Medical Gas Analyzer was used to monitor end-tidal CO2 for maintenance at 38 -C 2 mm Hg. Systolic and diastolic pressures were recorded noninvasively (Hoffman LaRoche Model 1010). Stimulation. Stimulation of the tooth pulp to test excitability was accomplished through electrodes placed in three gently prepared shallow cavities introduced just through the enamel to minimize disturbance of the pulpal environment. Electrode tips were hooked and surrounded by saline-agar filling the cavity floor to increase the effective electrode surface area, and the agar-electrode combination was sealed in place by means of non-conducive adhesive. Stimuli for excitability tests were monophasic pulses of 0.1 msec duration and of an intensity appropriate to the particular test. For excitability tests, the driving voltage to the isolated output stage (labconstructed photically-isolated constant-current generator, driven by one channel of a Grass Model S88 stimulator) was recorded rather than the actual output current, but an approximate conversion can be estimated by reference to our previous report (6). The excitability test stimuli were applied in the monoplar configuration through one of the tooth electrodes or biopolarfy using two tooth electrodes. The anodal direct blocking currents were applied in a monoplar electrode configuration to the third tooth electrode, using the second channel of the Model S88 stimulator driving an identical photically-isolated constant-current generator. In this case, the output current was directly measured using an electrometer (Keithley, Model 601C). Both the monopolar excitability test and anodal blocking stimuli were referenced to a 1 cm length of platinum wire inserted subcutaneously in the contralateral cheek. The electrode for the anodal blocking currents was placed near the occlusal tip of the tooth, while the two stimulating electrodes were located at an intermediate level, unless noted otherwise. Platinum electrodes were universally employed to reduce the effect of electrode polarization (8). Recording. The animal’s head was mounted in a stereotaxic apparatus (Model 1504, David Kopf Instruments), and all contact points were periodically infiltrated locally with Iidocaine to eliminate extraneous inputs of probable noxious quality. The arch of the first cervical vertebra, an area of skull extending bilaterally from the foramen magnum to the tentorium cerebelli, and the cerebellum were removed bilaterally to expose the dorsal aspect of the pontine and medullary brain stem. The latter remained exposed during recording, as we have found previously that further precautions were unnecessary (6). Concentric bipolar electrodes with a tip separation of 0.5 mm were used for recording (Model NE-100, Rhodes

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Medical Instruments). Electrode penetrations were angled 30” to the vertical to gain access to rostra1 levels of the trigeminal sensory complex under the tentorium cerebelli. Stereotaxic reference was from the obex along rostrocaudal and medio-lateral coordinates and by subsurface depth. The recording electrodes were led to a nearby differential preamplifier (lab-constructed) and from there to a bandpass-limiting amplifier (Tektronix Model 3A9), and were viewed oscillographically (Tektronix 564-B). Permanent recordings were obtained using a scope-mounted, continousrecording camera (Nihon Kohden Model PC-2A). Erperimental Protocol. Following exploration of the rostra1 sensory trigeminal complex in a rostrocaudal and mediolateral grid of 1 mm steps and at frequent subsurface depths, the electrode was placed for the remainder of the experiment at the point of maximal field potential amplitude elicited by supramaximal stimulation of the test tooth (4 V, 0.1 msec) . One or more of the following protocols were then examined in detail. Series of trials were conducted in which the effects on the trigeminal field potentials of a particular intensity of anodal blocking current were tested using a constant intensity of test stimulation (Individual Trace Series). For this series, the level of test stimulation was chosen to be that intensity which was just sufficient to produce maximal pulp responses in the absence of blocking currents. Series were also conducted in which pulp excitability (stimulus threshold of the trigeminal field potential) was followed as the anodal blocking current was successively raised from zero in 10 pa steps ranging to a total current as high as 100 F (Anodal Block Stepping Series). The current was maintained at each level for a time sufficient to conduct ten independent threshold determinations (3-5 min) which was also ample time for the threshold to stablize under the new conditions. Monopolar cathodal test stimulation was used in the two series described above to avoid any test stimulus facilitation of the anodal blocking current. In addition, an experimental series was conducted in which field potentials elicited by both monopolar and bipolar stimuli of successively greater intensity ranging to maximal responses (or 150 v) were recorded to characterize the nature and extent of the anodal block relative to excitable pulp elements (Strength-Response Series). Finally, in a few cases, the latter Strength-Response characterizations were supplemented with trials in which bipolar antidromic field potentials were qualitatively observed from two of the tooth electrodes just following termination of the blocking current. The antidromic potentials were evoked by using the brainstem electrode for bipolar stimulation. Criteria as identified in an earlier publication (6) were applied to all orthodromic field potentials to rule out spread of current to extrapulpal structures. It is assumed further that the recording sites were all in or near the rostra1 subdivisions of the trigeminal sensory complex (nucleus principalis and subnucleus oralis) due to the

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similarity of response characteristics and stereotaxic coordinates with a previous study which included histological characterizations (6). RESULTS Individual Trace Series. As stimulus strength is raised above threshold, a point is reached (2-3~ threshold) where the trigeminal field potential amplitude no longer shows a corresponding increase (response maxium ; Ref. (6)). Stimuli of an intensity just sufficient to induce response maximum activity in the absence of blocking currents were administered once every second during and following anodal blocks of various intensities ranging up to 100 pa. The application of the blocking current was continued until the field potential amplitude stabilized at some new value or until the potentials just disappeared, and was then termintaed. Figure 1 illustrates the results, typical of ten experiments, which were found for a particular test involving a 50 pa anodal blocking current. It will be noticed that the block exhibits a definite induction phase (in this case equal to 50 set) indicated by a progressive decreasein pulp excitability with time. Upon termination of the blocking current, responsesimmediately (less than 1-2 set) returned to control values. In general, blocking currents equal to or greater than 50 w eventually resulted in complete obliteration of the trigeminal field potentials at the excitability test intensities used. Higher

FIG. 1. Temporal series of field potentials recorded in the rostra1 trigeminal complex elicited by pulp stimulation at response-maximum intensity prior to (A), during (B) and following (C) 50 pa anodal direct current block of the tooth pulp. The indicated traces are at 5 set intervals as every fifth trace is shown.

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SAVARA

T

Current

_

(/A)

FIG. 2. Averaged results of pulpal thresholds to monopolar cathodal test stimulation from the anodal block stepping experiments. The brackets delineate the Standard Error of the Mean of the averaged values for individual experiments. For each of ten experiments, ten threshold determinations were made at each level of blocking current. intensities resulted in more rapid blocks, having induction times as low as a few seconds at 100 pa. All low-intensity (30 pa or less) and many intermediate blocking intensities reached a steady-state threshold value less than that of a complete block with induction times to steady-state values of many minutes at lower levels. The effects of multiple blocks were cumulative as successive blocks required less current. The blocking effect extended equally to all tooth electrodes if applied at the occlusal end of the pulp chamber but was limited in extent if applied elsewhere. Anodal Block Stepping Series. When the intensity of anodal blocking current was suddenly increased from zero or some intermediate value, the threshold rose in a curvilinear fashion with time until a new stable value was reached in a manner as documented in Fig. 1. The use of small step changes in blocking current permitted the sequential repetition of this maneuver several times. The averaged results of a series of ten experiments in which the threshold was followed through sequential steps of 10 pa from zero to 100 ,ua (or until “irreversible” processes ensued ; see below) is indicated in Fig. 2. The steady-state values of threshold were found to be a direct function of the anodal blocking current over the range of values investigated. In general, for any given experiment, the threshold reached its new steady-state value following a 10 e blocking current increase usually within 1 min. Very occasionally, a step shift in threshold appeared, either up or down, which was not phased-locked nor appeared otherwise related to the blocking current. The latter phenomena was not pronounced and had little effect on the general trends of the experimental data. Finally, each experimental series was without exception conducted in an ascending (increasing intensity) order of blocking currents, and thus any accumulative effects of lower levels of block were carried along and appeared

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incorporated in later readings. The ascending order of presentation was necessary because high levels of stimulation for prolonged times resulted in a lack of the immediate return of threshold to control levels upon block cessation. In the latter case, thresholds rapidly (within tens of seconds) fell to intermediate values (2-3 x control threshold) upon termination of individual Anodal Block Stepping Series but then remained at the latter level for at least 10 min (longer intervals were not esamined due to experimental time constraints). Strength-Response Series. Since the nature of Strength-Response characterizations for both monopolar and bipolar electrode configurations are known (6) and quite different distributions of current through the pulp are expected for these two stimulus geometries (10, ll), Strength-Response tests provide a practical means to delineate the extent of tissue blocked by the anodal blocking currents under investigation. Figure 3-A indicates an example of typical threshold responses to monopolar (cathodal) test stimulation of the pulp before, during an ascending stepping series, and after the administration of blocking currents ranging to high (greater than 50 pa) values (15 experiments). As illustrated, the results showed that the threshold steady-state values increased with increasing blocking current, and following the cessation of block, the threshold did not return to control values but remained at the intermediate level for at least 10 min, the interval over which the tests were continued. Figure 3-B shows the stimulus intensities and respective traces for the minimal conditions necessary for response-maximum activity using monopolar (cathodal) test stimulation. These results closely parallel the threshold determinations of Fig. 3-A including the retention of elevated values following cessation of block. Anodal blocks exhibited no effects on mono-

FIG. 3. Monopolar cathodal Strength-Response characterizations of the effects of anodal blockade on pulp excitability. A, thresholds (volts) and respective threshold responses prior to (top trace), during 20, 50 and 80 pa anodal block (middle three traces in descending order) and 1 min following block cessation (lower trace). B, analogous series depicting minimal stimulus intensities and respective traces required to elicit response-maximum activity.

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‘30-

30 L,++-

4. Bipolar Strength-Response characterizations of the effects of anzdal blockade on pulp excitability. A, thresholds (volts) and respective threshold responses prior to (top trace), during 20, 50 and 80 pa anodal block (middle three traces in detending order) and one minute following block cessation (lower trace). B, analogous series depicting minimal stmiulus intensities and respective traces required to elicit response-maximum activity. The data is from the same anodal stepping series as the data of Fig. 3. FIG.

polar response latencies, although some temporal dispersion was occasionally noted (see Fig. 3). Figure 4 indicates typical results of bioplar Strength-Response determinations analogous to the monopolar tests of Fig. 3 (the same 15 experiments). The results indicated that thresholds for initial activity (Fig. 4-A) and for response-maximum activity (Fig. 4-B) rose with increasing blocking current by amounts relatively much greater than the monopolar threshold elevations. However, following termination of the block, there was little tendency for either threshold to return to’ even intermediate values, as they remained at the grossly elevated state found during high levels of anodal block. This situation remains for at least ten minutes over which the Strength-Response tests were continued. As with the monopolar tests, blocking currents had no effect on bipolar response latencies. In four experiments, bipolar antidromic responses recorded from the tooth electrodes were qualitatively compared before and after various levels of blocking currents. The results indicated that low levels of block (30 H or less) did not alter antidromic responsesrecorded within 1 min following its cessation from responses recorded prior to its initiation, whereas high levels of blocking current (in general, 50 pa or greater, depending on the experiment) resulted in the obliteration of post-block antidromic responses if the orthodromic threshold also remained at an intermediate value instead of dropping to control levels. DISCUSSION The present results indicate that the application of anodal blocking currents

at low

to moderate

levels

or even

high

blocking

intensities

for

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short periods of time produce significant alterations in pulp excitability while being quickly reversible upon block cessation. These results are consistent with the findings of several recent reports which show that dc blocks applied to peripheral nerve are capable of blocking various components of the compound action potential (2, 3, 9, 13) and of activity in single fibers (2, 3), and that these effects are reversible within a few seconds after termination of the block (3, 13). However, the present results also showed that the effects of high blocking intensities or moderate to high blocks for prolonged time periods were not readily reversible, and that successive blocks showed accumulative effects since less blocking current was required to generate equivalent response attenuation. The notation of accumulative effects confirms a previous finding involving anodal blockade of the tooth pulp in the awake cat using a reflex index of pulp excitability (16). Although the nature of the accumulative effects and short-term irreversibility were not revealed by the present or prior work, both phenomena suggest effects on the nervous tissue of the pulp other since membrane time constants than simple membrane hyperpolarization, are expected to be quite short (19). Nevertheless, these results do not necessarily imply long-term irreversibility since behavioral studies show the day-to-day repeatability of blocking procedures using currents as high as60pa (16). The use of field potential recordings in the present study is similar to recording nerve compound action potentials in that the responses of a large and distributed population of unit elements is involved. It is known that the disappearance of the compound action potential does not necessarily imply that all activity is blocked, since desynchronization of unit activity would have the same result and in fact has been shown to occur (2, 3). Ho’wever, the latter workers also show that preliminary to such an apparent block changes in latency are apparent, as would be expected in the case of a mere desynchronization of the remaining responsive elements (17). The present findings are therefore likely to be the result of a true block of afferent conduction rather than mere desynchronization as attested by the lack of changes in latency in the Strength-Response data during or following the administration of anodal blocking currents. The present results indicate that levels of anodal blocking currents of several tens of microamperes, sufficient to block human perceptual (13) and cat reflex (16) responsiveness, produce a widespread influence on pulp excitability when applied at the occlusal end of the pulp chamber in the cat. Both the pulp excitability and the antidromic recording tests revealed similar alterations in pulpal excitability regardless of whether the blocking electrode or one of the other tooth electrodes was employed for the excitability test. These results rule out an effect of anodal blockade

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localized to the immediate vicinity of the blocking electrode. Also, the fact that anodal blocking currents resulted in quite large (e.g., 30 X in Fig. 4) bipolar threshold elevations indicates that the excitability changes were distributed throughout the main pulp chamber, the area through which such bipolar currents are distributed. The use of the monopolar electrode configuration is known to provide only an ambiguous interpretation in terms of localizing the actual point of nervous stimulation, since the site of excitation may include structures in the root canal or in the periapical locations in addition to the pulp chamber proper (6). The fact that monopolar Strength-Response tests also revealed elevated thresholds but not to the same extent as in bioplar trials suggests that the monopolar test stimulus may have been spreading to structures outside of the pulp chamber whose excitability may also have been affected by the blocking current but not to the same degree as the main pulp chamber. Also, the monopolar Strength-Response results showed that the blocking current had to be applied at the occlusal end of the pulp chamber for widespread effectiveness, in spite of the fact that it seems plausible to expect blocks in the root canal where high current densities are anticipated (12). This may imply that the blocking currents exert their effects on more vulnerable receptor or terminal nerve fiber regions at the pulp periphery rather than on main nerve fibers in the pulp or root canal. In any case, experiments involving electrical stimulation techniques of the present form cannot be used to define precisely the localization of the block, in spite of a recent claim to the contrary (16), since it is not possible to distinguish activation of nerve terminals and/or receptors at the pulp periphery from the direct stimulation of main nerve fibers in central areas of the pulp chamber. In conclusion, the results show that anodal direct blocking currents ranging to the order of 50 pa result in the reversible attenuation of pulp excitability in a dose-dependent manner. Blocking currents of higher intensities further attenuate pulp excitability but also result in physiological changes which are not immediately reversible. Delineation of the mechanisms of the latter effects will require further experimentation. REFERENCES 1.

BROOKS,

J. Dent.

B.,

R.

REISS,

and

R.

UMANS.

1970. Local electroanesthesia

in dentistry.

Res. 49 : 298-300.

B., and M. Y. Woo. 1966. Further studies on asynchronous firing and block of peripheral nerve conduction. Effect of galvanic polarization. Bull. Los Angeles Neural. Sot. 31. 63-71. 3. CASEY, K. L., and M. BLICK. 1969. Observations on anodal polarization of cutaneous nerve. Brain Res. 13 : 155-167. 4. DOUGLAS, B. L. 1955. Anesthesia by electricity. N. Y. State Dottal J. 21 : 28-29. 2. CAMPBELL,

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R. W., B. S. SAVARA, and R. B. TACKE. Regional electroanalgesia and its potentialities in control of orofacial pain. Oral Szbrg. 34: 694-703. FIELDS, R. W., R. B. TACKE, and B. S. SAVARA. The origin of trigeminal response components elicited by electrical stimulation of the tooth pulp of the cat. A&. Oral Biol., in press. GANGAROSA, L. P. 1973. Iontophoresis for surface local anesthesia. /. Amer. Dent. Ass. 88 : 125-128. GREATBATCH, W., B. PIERSMA, F. D. SHANNON, and S. W. CALHOUN, JR., 1969. Polarization phenomena relating to physiological electrodes. Ann. N. Y. Acad. Sci. 167 : 722-744. MANFREDI, M. 1970. Differential block of conduction of large fibers in peripheral nerve by direct current. Arch. Ital. Biol. 108: 52-71. MUMFORD, J. M. 1959. Path of direct current in electric pulp testing using one coronal electrode. Brit. Dent. J. 106: 23-25. MUMFORD, J. M. 1959. Path of direct current in electric pulp testing using two coronal electrodes. Brit. Dent .I. 106: 243-245. MUMFORD, J. M. and A. V. NEWTON. 1969. Zone of excitation when electrically stimulating human teeth. Arch. Oral Biol. 14: 1383-1388. NEWMAN, P. P. 1973. Electrical method for controlling pain. Nature (London) 243 : 474-475. OCHIAI, S. 1959. Improvements on apparatus of electroanesthesia. Bull. Tokyo

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15. OGUR, C. 1940. Anesthesia of the dental pulp by electrolysis. Drvatal Outlook 27 : 253-254. 16. REID, K. H. 1974. Mechanism of action of dental electroanesthesia. Natzkre (Lolcdon) 247 : 150-151. 17. SAVARA, B. S., R. W. FIELDS, R. B. TACKE, and R. S. H. TSUI. 1974. Modulation of cortical inputs from tooth pulp by electrical stimulation of adjacent gingiva. Oral Surg. 37 : 17-25. 18. STURRIDCE, E. 1918. “Dental Electra-Therapeutics.” 2nd ed. Lea and Febiger, NW York. 19. WOODBURY, J. W. 1960. Action potential cable and excitable properties of the cell membrane. Zft “Medical Physiology and Biophysics.” 18th ed., p. 52. T. C. Ruth and J. F. Fulton [Eds.]. W. B. Saunders, Philadelphia.

Pulpal anodal blockade of trigeminal field potentials elicited by tooth stimulation in the cat.

EXPERIMENTAL Pulpal NEUROLOGY Anodal Ii. WAYNE 47, 22%239 (1975) Blockade of Trigeminal by Tooth Stimulation FIELDS, RICHARD Biophysics Labor...
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