Differential inhibition onto developing and mature granule cells generates high-frequency filters with variable gain

Abstract

Adult hippocampal neurogenesis provides the dentate gyrus (DG) with heterogeneous populations of granule cells (GC) originated at different times. The specific contribution of these cells to the encoding of information arriving to the hippocampus is under current investigation. Here we show that spike trains arriving to the DG are channeled into activation of different populations of GC determined by the stimulation frequency and GC age. Immature GC respond to a wider range of afferent stimuli arriving at 1-40 Hz, whereas mature GC are less effective in following higher frequencies. This difference is dictated by the activation of feed forward inhibition, which predominantly restricts mature GC activation. Although it restricts frequency responsiveness, the stronger inhibition of mature GC results in a higher temporal fidelity compared to that of immature GC. Thus, activity arriving to the hippocampus at different frequencies activates two populations of neurons with variable frequency filters: immature cells, with wide range of responses, that are reliable transmitters of the incoming frequency, and mature neurons, with narrow responses to frequency, that are precise at informing the beginning of the stimulus, but with a sparse activity.