In the mammalian hippocampus, the dentate gyrus (DG) is characterized by sparse and powerful unidirectional projections to CA3 pyramidal cells, the so-called mossy fibers (MF). The MF form a distinct type of synapses, rich in zinc, that appear to duplicate, in terms of the information they convey, what CA3 cells already receive from entorhinal cortex layer II cells, which project both to the DG and to CA3. Computational models have hypothesized that the function of the MF is to enforce a new, well-separated pattern of activity onto CA3 cells, to represent a new memory, prevailing over the interference produced by the traces of older memories already stored on CA3 recurrent collateral connections. Although behavioral observations support the notion that the MF are crucial for decorrelating new memory representations from previous ones, a number of findings require that this view be reassessed and articulated more precisely in the spatial and temporal domains. First, neurophysiological recordings indicate that the very sparse dentate activity is concentrated on cells that display multiple but disorderly place fields, unlike both the single fields typical of CA3 and the multiple regular grid-aligned fields of medial entorhinal cortex. Second, neurogenesis is found to occur in the adult DG, leading to new cells that are functionally added to the existing circuitry, and may account for much of its ongoing activity. Third, a comparative analysis suggests that only mammals have evolved a DG, despite some of its features being present also in reptiles, whereas the avian hippocampus seems to have taken a different evolutionary path. Thus, we need to understand both how the mammalian dentate operates, in space and time, and whether evolution, in other vertebrate lineages, has offered alternative solutions to the same computational problems.