During sinusoidal rotation or translation, primary vestibular afferents modulate their discharge rates at the frequency of motion, effectively transmitting frequency-modulated (FM) signals. This study indicates a possible role for excitatory synapses in the processing of FM signals by vestibular brainstem pathways. Inputs to medial vestibular neurons were activated with FM pulse trains, while inhibitory transmission was blocked. The relationship between the presynaptic pulse rate and the postsynaptic membrane potential was found to be linear within a range of pulse rates. Short-term plasticity was a factor contributing to sensitivity at higher modulating frequencies. The amount of low-pass filtering was correlated with excitatory postsynaptic potential (EPSP) shape, which affected temporal summation during the train. Although the NMDA component of glutamatergic transmission affected EPSP shape, it made only a minor contribution to the dynamics of synaptic transmission. Most responses showed low-pass filtering over the entire 1–16 Hz range. Overall, excitatory synapses in the medial vestibular nucleus contribute a low-pass filter to central vestibular processing and complement the high-pass filtering that is introduced both by peripheral vestibular dynamics and by the intrinsic dynamics of secondary vestibular neurons.