Synchronous population activity is prevalent in CNS neurons and experimentally captured as oscillatory electric fields, the frequency of which can represent the state of the neural circuit, e.g., theta (~5 Hz) and gamma (~40 Hz). Such field oscillations, however, have been hypothesized to be not merely a result of coherent neuronal activity but may also play an active role for information processing in the brain. In cultured hippocampal slices, CA3 pyramidal cells responded to a single-pulse stimulus with monosynaptic and polysynaptic potentials and fired spikes with highly variable latencies. The jitter of spike latency was stabilized by applying weak electric field oscillations that per se induced only small fluctuations in subthreshold membrane potential. This effect was specific for the gamma-band frequency range and prevented by blockade of NMDA receptor activity. Strikingly, the latency of spike output was predictable from stimulus timings relative to the phase of the imposed gamma cycle. These results suggest that local field oscillations serve as an extracellular time reference and assure accurate and stable decoding of a memory trace present in cortical feedback networks.