Abstract
The hippocampus plays important roles in memory formation and retrieval through sharp-wave-ripples. Recent studies have shown that certain neuron populations in the prefrontal cortex (PFC) exhibit coordinated reactivations during awake ripple events. These experimental findings suggest that the awake ripple is an important biomarker, through which the hippocampus interacts with the neocortex to assist memory formation and retrieval. However, the computational mechanisms of this ripple based hippocampal-cortical coordination are still not clear due to the lack of unified models that include both the hippocampal and cortical networks. In this work, using a coupled biophysical model of both CA1 and PFC, we investigate possible mechanisms of hippocampal-cortical memory trace transfer and the conditions that assist reactivation of the transferred memory traces in the PFC. To validate our model, we first show that the local field potentials generated in the hippocampus and PFC exhibit ripple range activities that are consistent with the recent experimental studies. Then we demonstrate that during ripples, sequence replays can successfully transfer the information stored in the hippocampus to the PFC recurrent networks. We investigate possible mechanisms of memory retrieval in PFC networks. Our results suggest that the stored memory traces in the PFC network can be retrieved through two different mechanisms, namely the cell-specific input representing external stimuli and non-specific spontaneous background noise representing spontaneous memory recall events. Importantly, in both cases, the memory reactivation quality is robust to network connection loss. Finally, we find out that the quality of sequence reactivations is enhanced by both increased number of SWRs and an optimal background noise intensity, which tunes the excitability of neurons to a proper level. Our study presents a mechanistic explanation for the memory trace transfer from the hippocampus to neocortex through ripple coupling in awake states and reports two different mechanisms by which the stored memory traces can be successfully retrieved.
Highlights
The hippocampus (HPC) plays important roles in memory consolidation and sharp-wave ripples (SWR) are believed to transfer the compressed temporary information stored in the hippocampus to the distributed cortical networks (Buzsáki, 1989; Diekelmann and Born, 2010) through the abundant connections between the hippocampus and the cortex
We demonstrate that the sequence can be transferred and stored in the recurrent connections of the prefrontal cortex (PFC) network through spike-timingdependent plasticity (STDP) between PFC neurons
Our model suggests the existence of cortical ripples in PFC network coupled to the hippocampal ripples
Summary
The hippocampus (HPC) plays important roles in memory consolidation and sharp-wave ripples (SWR) are believed to transfer the compressed temporary information stored in the hippocampus to the distributed cortical networks (Buzsáki, 1989; Diekelmann and Born, 2010) through the abundant connections between the hippocampus and the cortex. Systems consolidation theory hypothesizes that memory consolidation process redistribute the hippocampal-dependent memories to support integration of the newly acquired memories with the related existing ones by reorganizing the cortical networks (Squire and Alvarez, 1995; Dudai et al, 2015) In support of this idea, it has been shown that during sleep, the neurons in prefrontal cortex (PFC) display learning-dependent reactivations when SWR are generated (Peyrache et al, 2009). During sleep the neurons in PFC can exhibit fast sequential reactivations with a compression factor of 6–7 compared to that during behavioral states (Euston et al, 2007) These experimental findings support the view that HPC SWR play important roles in memory consolidation during sleep
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