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Postsynaptic potentials in the jaw-opening motoneurons by stimulation of the trigeminal nerves
Brain Research, 163 (1979) 161-164 © Elsevier/North-Holland Biomedical Press
161
Postsynaptic potentials in the jaw-opening motoneurons by stimulation of the trigeminal nerves
MITSURU TAKATA Department of Physiology, School of Dentistry, Tokushima University, Tokushima (Japan)
(Accepted November 2nd, 1978)
It has been reported that the inhibitory postsynaptic potentials (IPSPs) produced in the jaw-closing motoneurons by lingual nerve stimulation were the composite of a strychnine-sensitive and an insensitive IPSP 1,2,s. With regard to the jaw-opening motoneurons, there are no detailed studies on properties of postsynaptic potentials (PSPs) set up by stimulation of the trigeminal nerves. In this paper, experiments are presented in which PSPs produced in the jawopening motoneurons by stimulation of either the lingual nerves or the infra-orbital nerve were explored, and the properties of PSPs set up by lingual nerve stimulation are discussed. Ten adult cats weighing 2.5-3.5 kg were used. Experiments were performed on decerebrated and decerebellated cats anesthetized with pentobarbital sodium (Nembutal, Abbott) 30 mg/kg. They were immobilized by intravenous injection of Flaxedil and respiration was maintained artificially. Sleeve electrodes were used to stimulate the cut central ends of ipsilateral labial fibers of the infra-orbital nerve (IO), bilateral lingual nerves (ipsi-L and contra-L) and the ipsilateral digastric nerve innervating the anterior belly of digastric muscles. In most cases, both digastric and mylohyoid nerves ( D + M nerves) were stimulated simultaneously for antidromic stimulation and therefore, motoneurons identified in this manner are described as jaw-opening motoneurons. Glass micropipettes filled with 2 M potassium citrate were used for recording. The threshold-stimulus of the afferent fibers which contribute to the PSPs in jawopening motoneurons were examined on both the ipsi-IO and the ipsi-L (Fig. 1A). The threshold-stimulus for the nerves was determined by recording the incoming nerve volley at the semilunar ganglion 4. In Fig. 1A-a is shown the antidromic spike of a jawopening motoneuron evoked by stimulation of D-[-M nerves. By repetitive stimuli of D-~M nerves, the IS and the SD component were separated. In series of Fig. 1A-b and 1A-c are illustrated responses of a motoneuron to the ipsi-IO and the ipsi-L stimulus. Numerals in both series are the stimulus intensity expressed as multiples of the nerve threshold ( x T). In both cases it was found that a stimulus intensity of 1.2 times the nerve threshold ( 1 . 2 x T ) was just suprathreshold for generating the excitatory
162
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Fig. 1. Responses of a jaw-opening Mn to trigeminal nerve stimulation. A-a: antidromic spike. In series A-b and A-c are shown the PSPs set up by ipsi-IO and ipsi-L stimulation. B : firing of a jawopening Mn to stimulation of either the ipsi-L (a) or the eontra-L (b). The stimulus intensity was increased from 1 to 3. C: response of a Dig Mn. C-a: antidromic spike. Responses of a Dig Mn to stimulation (3.2 × T) of either the ipsi-L (b-l) or contra-L (b-2) are shown. postsynaptic potentials (EPSPs). At a stimulus intensity of 1.7 x T, a hyperpolarizing potential followed the EPSP. With increasing stimulus strength, the PSPs gradually increased in size, reaching a maximum at 3.3 x T and remained constant in spite of further increase of stimulus Strength. The top record in both series is of a response of this cell to the ipsi-IO (A-b) and the ipsi-L (A-c) stimulus, recorded with low amplification. The latency of the EPSP caused either by the ipsi-IO or by the ipsi-L stimulus was about 4.0 msec and 3.5 msec, respectively. These results indicate that the low threshold afferents in both the ipsi-IO and the ipsi-L contribute to the EPSP. The afferent fibers which contribute to the hyperpolarizing potential appear to be smaller in diameter than the afferent fibers generating the EPSP. Similar results were obtained from the digastric motoneuron (Dig Mn) innervating the anterior belly of the digastric muscles. In order to investigate the synaptic link of lingual nerve afferents of both sides on the jaw-opening motoneurons, the following experiments were performed. In Fig. 1B
163
A
io MSEC
20 T,ISE C
Fig. 2. Effect of strychnine on the PSPs. A-a: antidromic spike. Responses of a jaw-opening Mn to stimulation of either the ipsi-L (b-1 and 2) or the contra-L (b-3 and 4) before injection of strychnine. Stimulus intensity applied to the nerve was 1.5 × T (b- 1 and b-3) and 5 × T (b-2 and b-4). A-c: responses of this cell to stimulation at 5 x T of either the ipsi-L (c-l) or contra-L (c-3) after strychnine injection (0.08 mg/kg), c-2 and c-4: recordings of c-1 and c-3 at slower speeds and low magnification. B : strychnine insensitive IPSP. Stimulation of D ÷ M nerves produced an antidromic spike followed by EPSPs (a). b-1 and b-2, strychnine insensitive IPSP produced by stimulation of the ipsi-L and contra-L, b-3 : strychnine insensitive IPSP produced by D ÷ M nerves stimulation. are shown the firing of a M n to graded stimulation of either the ipsi-L (B-a) or contraL (B-b). The stimulus strength applied to the nerve was increased f r o m record 1 to 3 in b o t h series. With weak stimulation of either the ipsi-L (Fig. 1Ba-1) or the contra-L (b1) only an EPSP was obtained. With increasing stimulus strength, spikes followed by a hyperpolarizing potential were produced (a-2 and b-2). To supramaximal stimulation this cell responded with three spikes to the ipsi-L (a-3) and with two spikes to the contra-L stimulus (b-3). A Dig M n (Fig. 1C) stimulation of either the ipsi-L (b-l) or contra-L (b-2) with stimulus intensity of 3.2 x T also produced three spikes. The latency of the EPSP set up by the ipsi-L and contra-L stimulus was a b o u t 3.5 msec and 4.0 msec, respectively. In Fig. 1C-a is shown an antidromic spike of a Dig M n evoked by digastric nerve stimulation. F r o m these results it was suggested that some high threshold afferents in the lingual nerve also contribute to the triggering of the spikes. In order to investigate the properties of a hyperpolarizing potential produced in a jaw-opening M n by stimulation of the lingual nerve, the effect of strychnine was examined (Fig. 2A). In A-a is shown an antidromic spike. W e a k stimulation of either the ipsi-L (b-l) or c o n t r a - L (b-3) produced only an EPSP. A single shock applied to either the ipsi-L (b-2) or the c o n t r a - L (b-4) with stimulus intensity of 5 x T evoked three spikes followed by a hyperpolarizing potential. Injection of strychnine (0.08
164 mg/kg, i.v.) increased the number of spikes to four (c-1 and c-3). The records c-1 and c-3 are also shown at slower sweep speeds in c-2 and c-4, respectively. In the following experiment the duration of a strychnine insensitive IPSP was measured in a jawopening Mn showing spontaneous discharges (Fig. 2B). The duration of the strychnine insensitive IPSP produced by stimulation of either the ipsi-L (b-l) or the contra-L (b2) was about 120 msec or 100 msec. Spontaneous discharges were completely depressed during the IPSP. In Fig. 2B-a is shown an antidromic spike. An EPSP was produced when D + M nerves were stimulated with an intensity of about 3 times the threshold of m o t o r fibers. This EPSP may be originated f r o m afferent fibers in (D + M) nerves. In strychninized cats, stimulation of the D + M nerves also produced a strychnine-insensitive IPSP of 100 msec duration (b-3). In this record the 1st spike was an antidromic spike and the 2nd one the orthodromic spike. In a spike-inactivated neuron by depolarization, stimulation of the lingual nerve also produced a strychnineinsensitive IPSP following an EPSP. It is concluded that hyperpolarizing potentials produced in jaw-opening motoneurons by lingual nerve stimulation are composed of strychnine-sensitive and insensitive IPSP and that stimulation of either the ipsi-L or the contra-L produces the same patterns of PSPs. The author wishes to thank Prof. Y. Kawamura, Department of Oral Physiology, Osaka University, for his encouragement and Prof. G. Somjen, Department of Physiology, Duke University, for his helpful criticism in preparing this manuscript.
1 Kidokoro, Y., Kubota, K., Shuto, S. and Sumino, R., Reflex organization of cat masticatory muscles, J. Neurophysiol., 31 (1968) 695-708. 2 Kidokoro, Y., Kubota, K., Shuto, S. and Sumino, R., Possible interneurons responsible for reflex inhibition of motoneurons of jaw-closing muscles from the inferior dental nerve, J. Neurophysiol., 31 (1968) 709-716. 3 Takata, M. and Kawamura, Y., Studies on the postsynaptic potential of masseter motoneurons. In R. Dubner and Y. Kawamura (Eds.), Oral-FacialSensory andMotor Mechanisms, Appleton Century Crofts, New York, 1971, pp. 205-215. 4 Takata, M., Ito, K. and Kawamura, Y., Inhibition ofhypoglossal motoneurons by stimulation of the jaw-opening muscle afferents, Jap. J. Physiol., 25 (1975) 453~465.
161
Postsynaptic potentials in the jaw-opening motoneurons by stimulation of the trigeminal nerves
MITSURU TAKATA Department of Physiology, School of Dentistry, Tokushima University, Tokushima (Japan)
(Accepted November 2nd, 1978)
It has been reported that the inhibitory postsynaptic potentials (IPSPs) produced in the jaw-closing motoneurons by lingual nerve stimulation were the composite of a strychnine-sensitive and an insensitive IPSP 1,2,s. With regard to the jaw-opening motoneurons, there are no detailed studies on properties of postsynaptic potentials (PSPs) set up by stimulation of the trigeminal nerves. In this paper, experiments are presented in which PSPs produced in the jawopening motoneurons by stimulation of either the lingual nerves or the infra-orbital nerve were explored, and the properties of PSPs set up by lingual nerve stimulation are discussed. Ten adult cats weighing 2.5-3.5 kg were used. Experiments were performed on decerebrated and decerebellated cats anesthetized with pentobarbital sodium (Nembutal, Abbott) 30 mg/kg. They were immobilized by intravenous injection of Flaxedil and respiration was maintained artificially. Sleeve electrodes were used to stimulate the cut central ends of ipsilateral labial fibers of the infra-orbital nerve (IO), bilateral lingual nerves (ipsi-L and contra-L) and the ipsilateral digastric nerve innervating the anterior belly of digastric muscles. In most cases, both digastric and mylohyoid nerves ( D + M nerves) were stimulated simultaneously for antidromic stimulation and therefore, motoneurons identified in this manner are described as jaw-opening motoneurons. Glass micropipettes filled with 2 M potassium citrate were used for recording. The threshold-stimulus of the afferent fibers which contribute to the PSPs in jawopening motoneurons were examined on both the ipsi-IO and the ipsi-L (Fig. 1A). The threshold-stimulus for the nerves was determined by recording the incoming nerve volley at the semilunar ganglion 4. In Fig. 1A-a is shown the antidromic spike of a jawopening motoneuron evoked by stimulation of D-[-M nerves. By repetitive stimuli of D-~M nerves, the IS and the SD component were separated. In series of Fig. 1A-b and 1A-c are illustrated responses of a motoneuron to the ipsi-IO and the ipsi-L stimulus. Numerals in both series are the stimulus intensity expressed as multiples of the nerve threshold ( x T). In both cases it was found that a stimulus intensity of 1.2 times the nerve threshold ( 1 . 2 x T ) was just suprathreshold for generating the excitatory
162
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.
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B
)pmpl 1MV i0 MSEC
c
2
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i 0 MSEC
2 ,.,,~
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5 MSEC
Fig. 1. Responses of a jaw-opening Mn to trigeminal nerve stimulation. A-a: antidromic spike. In series A-b and A-c are shown the PSPs set up by ipsi-IO and ipsi-L stimulation. B : firing of a jawopening Mn to stimulation of either the ipsi-L (a) or the eontra-L (b). The stimulus intensity was increased from 1 to 3. C: response of a Dig Mn. C-a: antidromic spike. Responses of a Dig Mn to stimulation (3.2 × T) of either the ipsi-L (b-l) or contra-L (b-2) are shown. postsynaptic potentials (EPSPs). At a stimulus intensity of 1.7 x T, a hyperpolarizing potential followed the EPSP. With increasing stimulus strength, the PSPs gradually increased in size, reaching a maximum at 3.3 x T and remained constant in spite of further increase of stimulus Strength. The top record in both series is of a response of this cell to the ipsi-IO (A-b) and the ipsi-L (A-c) stimulus, recorded with low amplification. The latency of the EPSP caused either by the ipsi-IO or by the ipsi-L stimulus was about 4.0 msec and 3.5 msec, respectively. These results indicate that the low threshold afferents in both the ipsi-IO and the ipsi-L contribute to the EPSP. The afferent fibers which contribute to the hyperpolarizing potential appear to be smaller in diameter than the afferent fibers generating the EPSP. Similar results were obtained from the digastric motoneuron (Dig Mn) innervating the anterior belly of the digastric muscles. In order to investigate the synaptic link of lingual nerve afferents of both sides on the jaw-opening motoneurons, the following experiments were performed. In Fig. 1B
163
A
io MSEC
20 T,ISE C
Fig. 2. Effect of strychnine on the PSPs. A-a: antidromic spike. Responses of a jaw-opening Mn to stimulation of either the ipsi-L (b-1 and 2) or the contra-L (b-3 and 4) before injection of strychnine. Stimulus intensity applied to the nerve was 1.5 × T (b- 1 and b-3) and 5 × T (b-2 and b-4). A-c: responses of this cell to stimulation at 5 x T of either the ipsi-L (c-l) or contra-L (c-3) after strychnine injection (0.08 mg/kg), c-2 and c-4: recordings of c-1 and c-3 at slower speeds and low magnification. B : strychnine insensitive IPSP. Stimulation of D ÷ M nerves produced an antidromic spike followed by EPSPs (a). b-1 and b-2, strychnine insensitive IPSP produced by stimulation of the ipsi-L and contra-L, b-3 : strychnine insensitive IPSP produced by D ÷ M nerves stimulation. are shown the firing of a M n to graded stimulation of either the ipsi-L (B-a) or contraL (B-b). The stimulus strength applied to the nerve was increased f r o m record 1 to 3 in b o t h series. With weak stimulation of either the ipsi-L (Fig. 1Ba-1) or the contra-L (b1) only an EPSP was obtained. With increasing stimulus strength, spikes followed by a hyperpolarizing potential were produced (a-2 and b-2). To supramaximal stimulation this cell responded with three spikes to the ipsi-L (a-3) and with two spikes to the contra-L stimulus (b-3). A Dig M n (Fig. 1C) stimulation of either the ipsi-L (b-l) or contra-L (b-2) with stimulus intensity of 3.2 x T also produced three spikes. The latency of the EPSP set up by the ipsi-L and contra-L stimulus was a b o u t 3.5 msec and 4.0 msec, respectively. In Fig. 1C-a is shown an antidromic spike of a Dig M n evoked by digastric nerve stimulation. F r o m these results it was suggested that some high threshold afferents in the lingual nerve also contribute to the triggering of the spikes. In order to investigate the properties of a hyperpolarizing potential produced in a jaw-opening M n by stimulation of the lingual nerve, the effect of strychnine was examined (Fig. 2A). In A-a is shown an antidromic spike. W e a k stimulation of either the ipsi-L (b-l) or c o n t r a - L (b-3) produced only an EPSP. A single shock applied to either the ipsi-L (b-2) or the c o n t r a - L (b-4) with stimulus intensity of 5 x T evoked three spikes followed by a hyperpolarizing potential. Injection of strychnine (0.08
164 mg/kg, i.v.) increased the number of spikes to four (c-1 and c-3). The records c-1 and c-3 are also shown at slower sweep speeds in c-2 and c-4, respectively. In the following experiment the duration of a strychnine insensitive IPSP was measured in a jawopening Mn showing spontaneous discharges (Fig. 2B). The duration of the strychnine insensitive IPSP produced by stimulation of either the ipsi-L (b-l) or the contra-L (b2) was about 120 msec or 100 msec. Spontaneous discharges were completely depressed during the IPSP. In Fig. 2B-a is shown an antidromic spike. An EPSP was produced when D + M nerves were stimulated with an intensity of about 3 times the threshold of m o t o r fibers. This EPSP may be originated f r o m afferent fibers in (D + M) nerves. In strychninized cats, stimulation of the D + M nerves also produced a strychnine-insensitive IPSP of 100 msec duration (b-3). In this record the 1st spike was an antidromic spike and the 2nd one the orthodromic spike. In a spike-inactivated neuron by depolarization, stimulation of the lingual nerve also produced a strychnineinsensitive IPSP following an EPSP. It is concluded that hyperpolarizing potentials produced in jaw-opening motoneurons by lingual nerve stimulation are composed of strychnine-sensitive and insensitive IPSP and that stimulation of either the ipsi-L or the contra-L produces the same patterns of PSPs. The author wishes to thank Prof. Y. Kawamura, Department of Oral Physiology, Osaka University, for his encouragement and Prof. G. Somjen, Department of Physiology, Duke University, for his helpful criticism in preparing this manuscript.
1 Kidokoro, Y., Kubota, K., Shuto, S. and Sumino, R., Reflex organization of cat masticatory muscles, J. Neurophysiol., 31 (1968) 695-708. 2 Kidokoro, Y., Kubota, K., Shuto, S. and Sumino, R., Possible interneurons responsible for reflex inhibition of motoneurons of jaw-closing muscles from the inferior dental nerve, J. Neurophysiol., 31 (1968) 709-716. 3 Takata, M. and Kawamura, Y., Studies on the postsynaptic potential of masseter motoneurons. In R. Dubner and Y. Kawamura (Eds.), Oral-FacialSensory andMotor Mechanisms, Appleton Century Crofts, New York, 1971, pp. 205-215. 4 Takata, M., Ito, K. and Kawamura, Y., Inhibition ofhypoglossal motoneurons by stimulation of the jaw-opening muscle afferents, Jap. J. Physiol., 25 (1975) 453~465.