Retinogeniculate synaptic properties controlling spike number and timing in relay neurons

Retinal ganglion cells (RGC) transmit visual signals to thalamocortical relay neurons in the lateral geniculate nucleus via retinogeniculate synapses. Relay neuron spike patterns do not simply reflect those of RGCs, but the mechanisms controlling this transformation are not well understood. We therefore examined synaptic properties controlling the strength and precision of relay neuron firing in mouse (p28-33) brain slices using physiological stimulation patterns and a combination of current clamp and dynamic clamp. In tonic mode (-55 mV), activation of single RGC inputs elicited stereotyped responses in a given neuron. In contrast, responses in different neurons varied from unreliable, to faithfully following, to a gain in the number of spikes. Dynamic clamp experiments indicated these different responses primarily reflected variability in the amplitudes of the N-methyl-D-aspartate (NMDA) and AMPA components. Each of these components played a distinct role in transmission. The AMPA component evoked a single precisely timed, short-latency spike per stimulus, but efficacy decreased during repetitive stimulation due to desensitization and depression. The NMDA component elicited longer-latency spikes and multiple spikes per stimulus and became more effective during repetitive stimuli that led to NMDA current summation. We found that in burst mode (-75 mV), where low-threshold calcium spikes are activated, AMPA and NMDA components and synaptic plasticity influenced spike number, but no combination enabled relay cells to faithfully follow the stimulus. Thus the characteristics of AMPA and NMDA currents, the ratio of these currents and use-dependent plasticity interact to shape how RGC activity is conveyed to relay neurons.