Myelination of axons greatly increases the conduction velocity and fidelity of impulse propagation in the mammalian CNS. The auditory brainstem is a useful model to test the importance of proper myelination because its circuits rely on very fast, precise, and reliable synaptic relays to process auditory information. To determine the fundamental role of myelination in auditory brainstem function, we recorded the sound evoked auditory brainstem response (ABR) from Long Evans Shaker (LES) rats, which lack myelin due to a genetic deletion of myelin basic protein. Control and LES rats were anesthetized and maintained with 2 % isoflurane (1 L/min O2 flow rate) during ABR recording. In control, the ABR evoked by a click consisted of five well-defined waves (denoted wave I-V), whereas in LES rats waves II and III could not be distinguished and the latency to wave I and IV was greatly increased. In addition, the sound threshold of the ABR was increased in LES rats using tone stimulations of 8 kHz or higher. The central conduction time of the auditory pathway increased significantly in the LES rats, while control showed a significant reduction of conduction time during development. To identify mechanisms by which central demyelination impairs the transmission of auditory signals, alterations in synaptic transmission were explored using whole-cell patch clamp at the synapse formed by the calyx of Held nerve terminal in the Medial Nucleus of the Trapezoid Body (MNTB) in the auditory brainstem. In LES rats, postsynaptic neurons from the MNTB displayed a delayed action potential and an increase in the number of action potential failures during high frequency stimulation when compared to controls. Voltage clamp experiments revealed that the size of the EPSC and the degree of EPSC depression during high frequency stimulation was similar in control and LES MNTB, but both the conduction delay and the synaptic delay were increased in LES rats. Taken together our results suggest that the defects observed in evoked auditory potentials in LES rats is related to the reduction in the temporal fidelity and the reliability of synaptic transmission, which is critical for the accurate processing of sound signals in auditory brainstem involved in sound localization.