1. Although synaptic transmission is known to influence many aspects of neuronal development, activity rates are quite low at early ages. The present study describes a long-lasting postsynaptic response to brief periods of synaptic stimulation that may underlie such an influence. Whole-cell patch clamp recordings were made from the lateral superior olive (LSO) in a brain slice preparation from early postnatal gerbils. 2. Stimulation of the excitatory afferent pathway from the cochlear nucleus elicited a prolonged depolarization (PD) in approximately 60% of the LSO neurons tested. Low frequency stimulation (1 Hz) was as effective as tetanic stimulation in producing PDs. These synaptically evoked depolarizations ranged in amplitude from 3 to 32 mV and recovered spontaneously after 0.5-35 min. 3. The LSO neuron input resistance declined during every PD episode and remained significantly lower even after the membrane potential had recovered. These PDs were partially reversed by 2 mM Ni(+2), but 1 microM tetrodotoxin and 10 microM 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) were ineffective. The metabotropic glutamate receptor agonist, trans-1-aminocyclopentane-1,3-dicarboxylic acid (40 microM), produced depolarizations that outlasted the exposure period by an average of 20 min and were also partially repolarized by 2 mM Ni(+2). In contrast, the depolarizations produced by alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid or N-methyl-D-aspartate decayed within a much shorter period of time. 4. To test whether in vivo discharge rates are, in fact, very low during development, spontaneous activity was recorded from neurons of the auditory midbrain in gerbils before and during the onset of sound-evoked responses. The average discharge rate of auditory neurons was quite low (X = 0.4 spikes/s), although many cells displayed brief periods of rapid discharge rate (X = 37 spikes/ s). Together, these results demonstrate a novel form of developmental plasticity elicited by low rates of glutamatergic transmission that may involve a metabotropic pathway and prolonged calcium influx.