This study investigated whether unilateral deafferentation of the presynaptic neuron is key in the control of morphology and the subunit composition and expression of AMPA type glutamate receptors (GluRs) in neurons of the dorsal cochlear nucleus (DCN). Data showed that there are morphological changes at the postsynaptic sites which precede presynaptic changes at the auditory nerve (AN) synaptic ending in response to peripheral damage, in particular that the postsynaptic densities (PSD) of the AN on fusiform cells (FC) are thicker after denervation. Moreover, GluR2, GluR3 and GluR4 AMPA receptor subunits were redistributed, not only at the synapse of FCs receiving direct contact with the AN, but also at the glutamatergic synapse of the parallel fibers on FC and on cartwheel cells (CwC) which are indirectly innervated by the AN. Interestingly, the same synapses in the DCN contralateral to the lesion and with a normal AN synaptic input also redistributed AMPA receptor subunits at the synapse in respond to deafferentation. In these synapses, there was an increase of immunogold labeling for GluR2/3 subunits but not for GluR2 at 2 days after deafferentation.