Target-specific regulation of presynaptic release properties at auditory nerve terminals in the avian cochlear nucleus

Abstract

Short-term synaptic plasticity (STP) acts as a time- and firing rate-dependent filter that mediates the transmission of information across synapses. In the auditory brain stem, the divergent pathways that encode acoustic timing and intensity information express differential STP. To investigate what factors determine the plasticity expressed at different terminals, we tested whether presynaptic release probability differed in the auditory nerve projections to the two divisions of the avian cochlear nucleus, nucleus angularis (NA) and nucleus magnocellularis (NM). Estimates of release probability were made with an open-channel blocker of N-methyl-d-aspartate (NMDA) receptors. Activity-dependent blockade of NMDA receptor-mediated excitatory postsynaptic currents (EPSCs) with application of 20 μM (+)-MK801 maleate was more rapid in NM than in NA, indicating that release probability was significantly higher at terminals in NM. Paired-pulse ratio (PPR) was tightly correlated with the blockade rate at terminals in NA, suggesting that PPR was a reasonable proxy for relative release probability at these synapses. To test whether release probability was similar across convergent inputs onto NA neurons, PPRs of different nerve inputs onto the same postsynaptic NA target neuron were measured. The PPRs, as well as the plasticity during short trains, were tightly correlated across multiple inputs, further suggesting that release probability is coordinated at auditory nerve terminals in a target-specific manner. This highly specific regulation of STP in the auditory brain stem provides evidence that the synaptic dynamics are tuned to differentially transmit the auditory information in nerve activity into parallel ascending pathways.