Return of Excitatory Waves from Field CA1 to the Hippocampal Formation Is Facilitated after Tetanization of Schäffer Collaterals during Sleep

Abstract

Current concepts hold that during learning in waking animals, new information is transmitted from the neocortex to the hippocampus, where it leaves a temporary trace in the form of a mosaic of modified synapses. During sleep, reactivation of the neuron population initially activated by the new stimulus has the result that this information is returned to the neocortex, ensuring consolidation of a permanent memory trace. Exchange of information between the neocortex and hippocampal formation is mediated mainly by the entorhinal cortex, whose internal connections, in principle, allow "messages" from the output of the hippocampal formation to return to its inputs. Our experiments in awake and sleeping rabbits demonstrated that waves of excitation can return to hippocampal field CA1 and the dentate gyrus via fibers of the perforant path, these waves having initially entered field CA1 via potentiated synapses of Schäffer collaterals; during sleep, re-entrant waves of excitation reach a maximum and have a high probability of evoking discharges of dentate gyrus neurons. Thus, the new stimulus, potentiating synaptic connections in the hippocampus and, probably, the entorhinal cortex during waking, create conditions for reactivation of the corresponding hippocampal neuron populations during sleep by waves of excitation returning via the entorhinal cortex.