Significance Synapses with high probability of neurotransmitter release ( P ᵣ) depress during prolonged activity, which reduces the faithful transfer of information. Auditory nerve synapses onto bushy cells show particularly strong depression at physiologically relevant rates of activity, which raises the question of how bushy cells transmit information when sound levels are high for a prolonged period. After rearing mice in constant, nondamaging noise, auditory nerve synapses changed from high to low P ᵣ, with a corresponding increase in the number of release sites, which increased spike fidelity during high activity. Neither quantal size nor average excitatory postsynaptic current changed. After returning to control conditions, P ᵣ recovered to high. These changes seem to reflect a homeostatic response to enhance fidelity. Information processing in the brain requires reliable synaptic transmission. High reliability at specialized auditory nerve synapses in the cochlear nucleus results from many release sites ( N ), high probability of neurotransmitter release ( P ᵣ), and large quantal size ( Q ). However, high P ᵣ also causes auditory nerve synapses to depress strongly when activated at normal rates for a prolonged period, which reduces fidelity. We studied how synapses are influenced by prolonged activity by exposing mice to constant, nondamaging noise and found that auditory nerve synapses changed to facilitating, reflecting low P ᵣ. For mice returned to quiet, synapses recovered to normal depression, suggesting that these changes are a homeostatic response to activity. Two additional properties, Q and average excitatory postsynaptic current (EPSC) amplitude, were unaffected by noise rearing, suggesting that the number of release sites ( N ) must increase to compensate for decreased P ᵣ. These changes in N and P ᵣ were confirmed physiologically using the integration method. Furthermore, consistent with increased N , endbulbs in noise-reared animals had larger VGlut1-positive puncta, larger profiles in electron micrographs, and more release sites per profile. In current-clamp recordings, noise-reared BCs had greater spike fidelity even during high rates of synaptic activity. Thus, auditory nerve synapses regulate excitability through an activity-dependent, homeostatic mechanism, which could have major effects on all downstream processing. Our results also suggest that noise-exposed bushy cells would remain hyperexcitable for a period after returning to normal quiet conditions, which could have perceptual consequences.