Silent synapses onto interneurons in the rat CA1 stratum radiatum.

Glutamate transmission to gamma-aminobutyric acid (GABA)ergic interneurons and to principal neurons differs in various important respects. Whether these differences exist from an early developmental stage, or result from differential development from a more common state, is unclear. In the hippocampal CA1 area, glutamate transmission to the developing, but not to the adult, principal neurons is characterized by the presence of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) silent synapses and of AMPA silencing induced by test pulse stimulation (0.03-1 Hz). In the present study, we examined whether this developmental difference in AMPA signaling is also true for glutamate transmission to CA1 stratum radiatum interneurons. We found that AMPA silent synapses onto these interneurons also exist, and that they can be generated by test pulse stimulation. In marked contrast to AMPA silencing in principal neurons, AMPA silencing in interneurons was not developmentally restricted, but was observed to the same extent after the first postnatal month as in the second postnatal week. In addition, we found that glutamate synapses onto these interneurons can also be N-methyl-d-aspartate (NMDA)-silent, that is, only AMPA-signaling. After test pulse stimulation, the AMPA-silent, the NMDA-silent and the AMPA/NMDA-signaling synapses onto the developing interneurons were estimated to be about equally frequent. These results highlight a diversity of glutamate signaling to CA1 stratum radiatum interneurons, and they indicate that the glutamate synapses onto pyramidal neurons and to interneurons can mature differentially.