The dentate gyrus (DG), a hippocampal subregion, continuously produces new neurons in the adult mammalian brain that become functionally integrated into existing neural circuits. To what extent this form of plasticity contributes to memory functions remains to be elucidated. Using mapping of activity-dependent gene expression, we visualized in mice injected with the birthdating marker 5-bromo-2 -deoxyuridine the recruitment of new neurons in a set of controlled water maze procedures that engage specific spatial memory processes and require hippocampal-cortical networks. Here, we provide new evidence that adult-generated hippocampal neurons make a specific but differential contribution to the processing of remote spatial memories. First, we show that new neurons in the DG are recruited into neuronal networks that support retrieval of remote spatial memory and that their activation is situation-specific. We further reveal that once selected, new hippocampal neurons are durably incorporated into memory circuits, and also that their recruitment into hippocampal networks contributes predominantly to the updating and strengthening of a previously encoded memory. We find that initial spatial training during a critical period, when new neurons are more receptive to surrounding neuronal activity, favors their subsequent recruitment upon remote memory retrieval. We therefore hypothesize that new neurons activated during this critical period become tagged so that once mature, they are preferentially recruited into hippocampal networks underlying remote spatial memory representation when encountering a similar experience.immediate early gene Í learning Í memory consolidation Í neurogenesis Í plasticity N ew neurons are generated throughout adult life in discrete regions of the mammalian brain, including the dentate gyrus (DG) of the hippocampus. Some of these newborn neurons become integrated into preexisting hippocampal circuits, raising the possibility that they may thereby contribute to behaviorally relevant neuronal assemblies. Supporting this idea, the increasing number of reports that have used correlative and invasive approaches indicates the existence of a functional link between hippocampal-dependent learning and adult hippocampal neurogenesis (1-5). Recently, it was found that new cells contribute to the functional activity patterns elicited in the hippocampus in response to performing memory tasks that solicit hippocampal networks (4, 6, 7).To date, the nature of the specific contributions of adultgenerated neurons to memory processing remains largely unknown. During the second week after birth, new hippocampal cells enter a period during which they show enhanced synaptic plasticity, their functional maturation occurs, and their ultimate survival is determined (8, 9). At this age, depletion of new neurons leads to memory impairment in several hippocampaldependent tasks (1, 3). Based on these observations, we sought to examine in mice injected with the birthdating marker 5-bromo-2Đ-deoxyuridine (BrdU) the contribu...