Long-term potentiation of primary afferent neurotransmission at trigeminal synapses of juvenile rats

Abstract

Primary afferent monosynaptic and polysynaptic excitatory postsynaptic currents (EPSCs) were recorded from brainstem trigeminal neurons by stimulation of the mandibular nerve attached to the brainstem preparation of juvenile rats. A high-frequency conditioning stimulus induced long-term potentiation (LTP) of high-threshold EPSCs in the majority of trigeminal caudal neurons in substantia gelatinosa, where both A- and C-fibres terminate. However, the same conditioning stimulus did not potentiate low-threshold EPSCs in caudal neurons or EPSCs recorded from neurons in the middle part of trigeminal interpolar nucleus, where C-fibres rarely terminate. LTP in caudal neurons could be induced after blocking N-methyl-D-aspartate (NMDA) receptors with D(-)-2-amino-5-phosphonopentanoic acid (D-AP5, 50 microM), after postsynaptic loading of the Ca2+ chelator BAPTA (10 mM), or even after completely blocking excitatory transmission with kynurenic acid during conditioning. However, LTP was blocked by the metabotropic glutamate receptor antagonist (+)-alpha-methyl-4-carboxyphenylglycine (1 mM). We suggest that LTP of the trigeminal primary afferent EPSCs is induced preferentially in the C-fibre inputs and that the induction mechanism involves metabotropic glutamate receptors, possibly at the presynaptic terminals.