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

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.