Principal neurons of the medial nucleus of the trapezoid body (MNTB) receive a synaptic input from a single giant calyx terminal that generates a fast-rising, large excitatory postsynaptic current (EPSC), each of which are supra-threshold for postsynaptic action potential generation. Here, we present evidence that MNTB principal neurons receive multiple excitatory synaptic inputs generating slow-rising, small EPSCs that are also capable of triggering postsynaptic action potentials but are of non-calyceal origin. Both calyceal and non-calyceal EPSCs are mediated by α-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA) and N-methyl-d-aspartate (NMDA) receptor activation; however, the NMDA receptor-mediated response is proportionally larger at the non-calyceal synapses. Non-calyceal synapses generate action potentials in MNTB principal neurons with a longer latency and a lower reliability than the large calyceal input. They constitute an alternative low fidelity synaptic input to the fast and secure relay transmission via the calyx of Held synapse.