Excitation Waves Returning to the Hippocampus via the Entorhinal Cortex Can Reactivate Populations of “Trained” Field CA1 Neurons during Deep Sleep

Abstract

It is suggested that information on new stimuli from the neocortex is transmitted to the hippocampus, where temporal traces persist in the form of mosaics of modified synapses. During sleep, populations of neurons storing these traces are reactivated and return the information required for consolidation of a permanent memory trace to the neocortex. A possible mechanism for the reactivation of “trained” hippocampal neurons during memory consolidation consists of the reverberation of excitation in the neuron circuits linking the hippocampus and entorhinal cortex. Our studies in rats included recording of responses in hippocampal field CA1 to stimulation of Schaffer collaterals with potentiated synapses during waking and sleep. During deep sleep, discharges of field CA1 neurons were followed by waves of excitation which passed through the entorhinal cortex and reached the hippocampus and dentate gyrus via fibers of the perforant path, evoking neuron discharges in the latter. Repeated neuron discharges in field CA1 occurred on interaction of the early excitation wave returning directly via perforant path fibers and the late wave returning via Schaffer collaterals, not via the trisynaptic path via the dentate gyrus and hippocampal field CA3 but probably via field CA2.