The consequences of deafness on the central auditory nervous system have been examined at many levels, from molecular to functional. However, there has never been a direct and selective measurement of excitatory synaptic function following total hearing loss. In the present study, gerbils were deafened at postnatal day 9, an age at which there is no deafferentation-induced cell death of ventral cochlear nucleus neurons. One to five days after bilateral cochlear ablation, the amplitude of evoked excitatory postsynaptic currents (EPSC) was measured with whole-cell voltage-clamp recordings in an inferior colliculus (IC) brain slice preparation in response to electrical stimulation of the ipsilateral lateral lemniscus (LL) or the commissure of the inferior colliculus (CIC). Deafness resulted in larger LL- and CIC-evoked EPSC amplitudes and durations. This result was observed at a depolarized holding potential. In addition, deafness caused a decrease in excitatory neurotransmitter release at the LL pathway, as assessed with a paired-pulse stimulation protocol. In contrast to its effect on excitatory synapses, bilateral cochlear ablation reduced inhibitory synaptic strength in IC neurons. The effects included a postsynaptic decrease in IPSC conductance, a 25-mV depolarization in the IPSC equilibrium potential and a decrease of neurotransmitter release. Thus normal innervation differentially affects excitatory and inhibitory synaptic strength in IC neurons, and these changes may contribute to alterations in auditory coding properties following sensory deprivation.