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.

Reconsolidation‐induced rescue of a remote fear memory blocked by an early cortical inhibition: Involvement of the anterior cingulate cortex and the mediation by the thalamic nucleus reuniens

“…This would put the prefrontal cortex in the control of CA1 synaptic strength after LTP induction, a potential mechanism for the progressive hippocampal‐cortical communication that may underly the memory systems consolidation process. This is consistent, for instance, with the suggested memory trace formation mechanism based upon reverberation of excitation in closed neuronal circuits established in the hippocampus and entorhinal cortex (Buzsáki and Gage, ; Zosimovskii and Korshunov, ). To this point this proposed mechanism to explain our findings is highly speculative, and to be settled, depend on future experiments.…”