We studied the development of glutamatergic neurotransmission in dentate gy
rus granule cells (GCs) in hippocampal slices from 5 to 12-day-old rats. Th
e active postnatal neuronogenesis in dentate permits GCs with staggered bir
thdates to be studied in situ in a single preparation. We recorded evoked r
esponses to medial perforant path stimulation using visually-guided whole-c
ell patch clamping to select immature GCs, and biocytin filling to correlat
e electrophysiologic responses with maturational stage. Even within this im
mature cell population we found four distinct electrophysiologic patterns.
Type 1 cells had no glutamatergic current; Type 2 cells had only N-methyl-D
-aspartate receptor (NMDA) current; Type 3 cells had both NMDA and alpha -a
mino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) current although t
he NMDA component could be isolated at low stimulus intensity (NMDA thresho
ld<AMPA threshold): Type 4 cells had both AMPA and NMDA currents with NMDA
threshold<greater than or equal to>AMPA threshold. Type 1 cells were least
mature, and Type 4 cells most mature as assessed by cell properties, dendri
tic arborization, and penetration of dendrites into the molecular layer. Th
us NMDA-mediated currents predominate early in GC development as is consist
ent with their role in processes that determine dentate architecture - neur
onal migration, dendritic outgrowth and regression. and synapse stabilizati
on. By analogy with 'silent synapses' (i.e. synapses that contain only NMDA
receptors), Type 2 cells are candidate 'silent cells' that may undergo act
ivity-dependent acquisition of functional fast-conducting AMPA receptors wi
th maturation. (C) 2000 Elsevier Science B.V. All rights reserved.