We have examined the microcircuit mechanisms of place field generation using whole-cell voltage recordings from hippocampal CA1 neurons in mice running on a linear track. We found that CA1 cells receive a constant barrage of excitatory input from thousands of presynaptic cells that are tuned to all features of the environment and that a novel form of synaptic plasticity (termed BTSP) enhances the weights of a particular subset of excitatory inputs producing the ramp of depolarization that drives place specific firing. In addition, a constant level of un-tuned inhibition counter acts the barrage of un-potentiated excitatory input thus suppressing a potential source of “noise”. The novel synaptic plasticity is induced in as few as a single trial by dendritic Ca2+ spikes and operates over a many seconds long asymmetric time course. The time course of the plasticity produces predictive place fields whose center of mass and peak are actually tens of centimeters before the location where they were induced. Also the induction mechanism (dendritic plateau potential) appears to make this a non-autonomous form of one-shot learning that allows experience to rapidly shape the CA1 representation. Together these data indicate that the hippocampus functions as an experience-dependent model generating predictions about the environment approximately one second (or 20 cm) ahead of the animal.