Frontiers in Systems Neuroscience (Mar 2014)
A cellular mechanism for system memory consolidation
Abstract
Declarative memories initially depend on the hippocampus. Over a period of weeks to years, however, these memories become hippocampus-independent through a process called system memory consolidation. The underlying cellular mechanisms are unclear. Here, we suggest a consolidation mechanism, which is based on STDP and a ubiquitous anatomical network motif. As a first step in the memory consolidation process, we consider pyramidal neurons in the hippocampal CA1 area. These cells receive Schaffer collateral (SC) input from the CA3 area at the proximal dendrites, and perforant path (PP) input from entorhinal cortex at the distal dendrites. Both pathways carry sensory information that has been processed by cortical networks and that enters the hippocampus through the entorhinal cortex. Hence, information from entorhinal cortex reaches CA1 cells through an indirect pathway (via CA3 and SC) and a direct pathway (PP). Memories are assumed to be initially stored in the recurrent CA3 network and the SC synapses during the awake, exploratory state. During a subsequent consolidation phase (during slow-wave sleep) SC-dependent memories are partly transferred to the PP synapses. Through mathematical analysis and numerical simulations we show that this consolidation process occurs as a natural result from the combination of (1) STDP at PP synapses and (2) the temporal correlations between SC and PP activities, since the (indirect) SC input is delayed compared to the (direct) PP input by about 5-10 ms. With a detailed compartmental model we then show that the spatial tuning of a CA1 cell is copied from the proximal SC-synaptic inputs to the distal PP-inputs. Next, we repeated the network motif across many levels in a hierarchical network model: each direct connection at one level is part of the indirect pathway of the next level. Analysis and simulations of this hierarchical system demonstrate that memories gradually move from hippocampus into neocortex. Moreover, the memories show power-law forgetting, as seen with psychophysical forgetting functions. Hence, our work proposes a novel mechanism to underlie system memory consolidation, allowing us to bridge spatial scales from single cells to cortical areas, and time scales from milliseconds to years.
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