Synaptic NMDA currents andshort-term plasticity influence spike generation in neurons of the ventral nucleus of the lateral lemniscus
Neurons in the ventral part of the ventral nucleus of the lateral lemniscus (VNLL) receive large glutamatergic, somatic synapses that underlie the temporal precise generation of action potentials (APs). It remains unclear which synaptic components contribute to the precision and output generation during resting states as well as during ongoing activity. To determine the different synaptic contributions to the generation of APs, we recorded from VNLL neurons in acute brain slices from gerbils aged between postnatal day 19 and 30. We found that fast glutamatergic synaptic transmission in VNLL neurons was based exclusively on AMPA and NMDA receptor currents. The small NMDA component increased the EPSC time course at potentials close to rest. During synaptic 20-pulse stimulation trains, EPSCs exhibited short-term plasticity with paired pulse facilitation at initial pulses for stimulus frequencies above 50 Hz, and a subsequent frequency-dependent depression. Using dynamic clamp recordings, the effects of NMDA currents and short-term plasticity on AP generation were decomposed. During more than 6 seconds of simulated ongoing activity with random frequencies, short-term depression reduced AP generation and prevented a single synapse to become permanently supra-threshold. The depression effectively low-pass filtered the input and only permitted reliable onset APs to input transients presented at frequencies below 50 Hz. Above 100 Hz stimulation, frequency ongoing generation of APs was supported by the NMDA component. Thus, interplay of short-term plasticity and NMDA currents form the physiological basis for prominent onset response to simulated activity transients and ongoing action potential generation during high frequency input stimulations.