Two-stage, input-specific synaptic maturation in a nucleus essential for vocal production in the zebra finch

In most songbirds, vocal learning occurs through two experience-dependent p hases, culminating in a reduction of behavioral plasticity called song crys tallization. At ends of developmentally plastic periods in other systems, s ynaptic properties change in a fashion appropriate to limit plasticity. Mat uration of glutamatergic synapses often involves a reduction in duration of NMDA receptor (NMDAR)-mediated synaptic responses and a coincident reducti on in the contribution of NMDARs to synaptic transmission. We hypothesized that similar changes in the zebra finch song system help limit behavioral p lasticity during song development. Nucleus robustus archistriatalis (RA) is a key nucleus in the forebrain song motor pathway and receives glutamaterg ic input from the motor nucleus HVc. RA also receives glutamatergic input, mediated primarily by NMDARs, from the lateral magnocellular nucleus of the anterior neostriatum, which is part of a circuit essential for learning bu t not song production. We examined whether synaptic maturation occurs in ei ther input to RA by recording synaptic currents in brain slices prepared fr om zebra finches of different ages. We find the motor input from HVc to RA uses both AMPA receptors (AMPARs) and NMDARs, and synaptic maturation occur s in two phases: an early reduction in duration of NMDAR-mediated synaptic currents in both inputs, and a later reduction in the NMDAR contribution to synaptic responses in the motor pathway. Although NMDAR kinetics change to o early to account for crystallization, the reduction of the relative NMDAR contribution to synaptic transmission could contribute to the onset of cry stallization. Thus, synaptic maturation events can be temporally distinct a nd input-specific and may play different roles in behavioral plasticity.