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. 2000 Apr 15;524 Pt 2(Pt 2):503-12.
doi: 10.1111/j.1469-7793.2000.00503.x.

Primary afferent synaptic responses recorded from trigeminal caudal neurons in a mandibular nerve-brainstem preparation of neonatal rats

K Onodera  1 , M Hamba, T Takahashi
Affiliations

Primary afferent synaptic responses recorded from trigeminal caudal neurons in a mandibular nerve-brainstem preparation of neonatal rats

K Onodera et al. J Physiol. .

Abstract

1. Whole-cell patch-clamp recordings were made from the neurons in the superficial trigeminal caudal nucleus (substantia gelatinosa) visually identified in a parasagittal brainstem slice of neonatal rat with the mandibular nerve attached. 2. Stimulation of the mandibular nerve at 0.03 Hz evoked compound excitatory postsynaptic potentials (EPSPs) or currents (EPSCs) in trigeminal caudal neurons. When stimulated at higher frequency (> 0.5 Hz), compound synaptic responses were largely attenuated and a small component remained. This component had a monosynaptic nature, following high-frequency stimulation (33-50 Hz) with a stable synaptic latency. 3. The N-methyl-D-aspartate (NMDA) receptor antagonist D(-)-2-amino-5-phosphonopentanoic acid (D-AP5, 50 microM) largely attenuated the slow polysynaptic EPSCs. The AMPA/kainate receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX, 10 microM) largely attenuated monosynaptic EPSCs, but only weakly attenuated slow polysynaptic EPSCs. Simultaneous application of CNQX and D-AP5 completely abolished EPSCs. The monosynaptic EPSCs isolated by repetitive stimulation had both NMDA and non-NMDA components. 4. Monosynaptic EPSCs having high threshold had a relatively long latency. During repetitive stimulation (0.5-5.0 Hz), EPSCs having high threshold and long latency underwent a stepwise potentiation in an activity-dependent manner. The conduction velocity estimated for these EPSCs fell into the range of C-fibres. The activity-dependent potentiation was observed for both non-NMDA and NMDA EPSCs and was accompanied by a significant decrease in the coefficient of variation of EPSC amplitude. 5. We suggest that the activity-dependent potentiation of EPSCs is induced presynaptically and that it may underlie the wind-up phenomenon, an activity-dependent hyperexcitability of the primary afferent C-fibres.

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Figures

Figure 1
Figure 1. Schematic illustrations for the parasagittal brainstem slice and the experimental arrangement
A, dorsal and ventral views of the brainstem attached with mandibular nerve trunks. A parasagittal slice including the trigeminal spinal tract nucleus was trimmed out of the brainstem along the thick line indicated. B, the slice attached to a mandibular nerve trunk was immobilized with its cut surface upward with nylon threads glued onto a U-shaped platinum frame (Edwards et al. 1989). Whole-cell recordings were made from neurons visually identified in substantia gelatinosa in subnucleus caudalis. D, dorsal side; V, ventral side. The middle thread is approximately at the height of the obex in this scheme.
Figure 2
Figure 2. Excitatory postsynaptic responses recorded from trigeminal caudal neurons in response to mandibular nerve stimulation
Excitatory postsynaptic potentials (EPSPs, A and B) and currents (EPSCs, C) evoked in trigeminal caudal neurons. A, mandibular nerves were stimulated at 0.03 Hz with a square pulse (0.3 ms) of different intensities as indicated in two different neurons. A short-latency fast EPSP component (asterisks) had lower threshold than slow components in one cell (a), but vice versa in another cell (b). Resting membrane potential was -64 mV in a and -71 mV in b. B and C, effects of repetitive stimulation on excitatory postsynaptic responses. B, gradual attenuation of EPSPs during 2 Hz stimulation (resting potential, -64 mV). The 1st, 10th, 20th, 25th and 32nd EPSPs are superimposed at a fast time scale (b). Note that an EPSP component with a relatively long latency remains unblocked after the 32nd stimulation. C, suppression of EPSCs during a 3.3 Hz train of stimulation followed by a potentiation in another cell under voltage clamp. The 2nd-6th EPSC was largely attenuated, but potentiated thereafter till the end of stimulation (a). Note that the 10th and 40th EPSCs had a slightly longer latency (13.8 ms) than the 1st, 3rd and 4th EPSCs (10.2 ms) (b). Synaptic responses were evoked with the supra-maximal stimulus intensity.
Figure 7
Figure 7. Activity-dependent potentiation of EPSCs
A, monosynaptic non-NMDA EPSCs recorded in the presence of D-AP5 (50 μM) underwent an abrupt potentiation during repetitive stimulations (0.6-5 Hz). At a stimulus frequency below 0.5 Hz, no potentiation was observed (data not shown). The potentiation occurred earlier at higher stimulus frequency (abscissa, sequence number of stimulation). Sample traces are EPSCs (3 events superimposed) at 0.8 Hz before (a) and after (b) potentiation. B, NMDA EPSCs in the presence of CNQX (10 μM) evoked at 1 and 2 Hz. Only the first NMDA EPSC had a clear polysynaptic component. Monosynaptic NMDA EPSCs showed a potentiation after the 15th (2 Hz) or 16th (1 Hz) event (b). Sample traces are whole time course at 1 Hz stimulation (left) and NMDA EPSCs before (a) and after (b) potentiation (1 Hz) superimposed (right). EPSCs were evoked by the suprathreshold stimulus.
Figure 3
Figure 3. Monosynaptic nature of EPSCs remaining after repetitive stimulation
The latency histograms of EPSCs evoked at 3.3 Hz in two different trigeminal caudal neurons. EPSCs in one neuron (A) had a threshold of 1.8 V and mean latency of 10.1 ms (88 events fitted with a Gaussian distribution, □). These EPSCs persisted up to 50 Hz with a stable latency (3-4 traces superimposed in sample records). EPSCs recorded from another neuron (B) had a threshold of 5.0 V and mean latency of 16.1 ms (105 events fitted as above,formula image) and persisted up to 33 Hz with a stable latency (4 traces superimposed).
Figure 6
Figure 6. Threshold and latency of monosynaptic EPSCs
A, the relationship between the stimulus intensity and amplitude of low threshold (^) and high threshold (•) EPSCs each evoked at 2 Hz in two different trigeminal caudal neurons (superimposed sample traces in the bottom panel are 3 consecutive EPSCs at a and b, respectively). Mean amplitudes and s.e.m.s of EPSCs (10-17 events including failures) are plotted against stimulus intensity (V). B, the relationship between threshold (V) and latency (ms) for EPSCs recorded from 75 trigeminal caudal neurons. Threshold and latency are positively correlated (r = 0.81). A regression line was drawn with the least square method. Filled symbols (•) indicate EPSCs which underwent activity-dependent potentiation during 0.6-5 Hz stimulation (see Fig. 7). The dashed lines separate the high-threshold long-latency EPSCs with activity-dependent potentiation (•) from the low-threshold short-latency EPSCs with no activity-dependent potentiation (^). Most EPSCs (89 %) could be classified into one of these categories.
Figure 4
Figure 4. Voltage dependence of monosynaptic EPSCs
Voltage dependence of EPSCs recorded from two different trigeminal caudal neurons. Aa, EPSCs evoked at 3.3 Hz having a low threshold (1.8 V) and short latency (10.2 ms). Averaged EPSC (from 5 consecutive events in this and following figures) at each holding potential is superimposed. Ab, non-NMDA component isolated by D-AP5 (50 μM, left) and NMDA component isolated by CNQX (10 μM, right) at holding potentials of +45 and -65 mV (4 traces superimposed). An asterisk indicates a spontaneous EPSC. Ba, EPSCs evoked at 5 Hz having a relatively high threshold (6.0 V) and long latency (19.7 ms) superimposed as above. Bb, NMDA component isolated by CNQX (10 μM) at each holding potential superimposed. C, current-voltage relationships for the peaks of non-NMDA EPSCs (Aa, ^; Ba, ▵) and NMDA EPSCs (Bb, ▪).
Figure 5
Figure 5. Pharmacological properties of EPSCs
A, EPSCs evoked at 0.03 Hz in a caudal neuron. The aCSF contained bicuculline (10 μM), strychnine (0.5 μM) and 1 mM Mg2+. Aa, D-AP5 (50 μM) largely attenuated slow EPSC components (AP5) and further addition of CNQX (10 μM) completely abolished the synaptic current (AP5 + CNQX). Averaged records from 5 events each are superimposed. Ab, EPSCs remaining in the presence of D-AP5 evoked at 0.03, 1 and 10 Hz (averaged EPSCs superimposed). Ac, CNQX (10 μM) attenuated EPSCs in a reversible manner. Ad, EPSPs remaining in the presence of CNQX trigger action potentials. Resting potential was -67 mV. B, essentially the same results as above obtained in the absence of bicuculline and strychnine and in aCSF containing 0.5 mM Mg2+.
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