Ripples make waves: binding structured activity and plasticity in hippocampal networks

Abstract

Establishing novel episodic memories and stable spatial representations depends on an exquisitely choreographed, multistage process involving the online encoding and offline consolidation of sensory information, a process that is largely dependent on the hippocampus. Each step is influenced by distinct neural network states that influence the pattern of activation across cellular assemblies. In recent years, the occurrence of hippocampal sharp wave ripple (SWR) oscillations has emerged as a potentially vital network phenomenon mediating the steps between encoding and consolidation, both at a cellular and network level by promoting the rapid replay and reactivation of recent activity patterns. Such events facilitate memory formation by optimising the conditions for synaptic plasticity to occur between contingent neural elements. In this paper, we explore the ways in which SWRs and other network events can bridge the gap between spatiomnemonic processing at cellular/synaptic and network levels in the hippocampus.

Figure 1

Proposed means of online encoding of spatial trajectories in the rat hippocampus. Place cells in CA3 and CA1 exhibit partial or entire place field overlap. During exploration, hippocampal networks undergo strong 4–7 Hz theta modulation. Overlapping CA3 place cells fire sequentially within the same theta cycle, establishing the conditions necessary for synaptic plasticity to occur between CA3 cell assemblies associated in time and space. Synaptic plasticity could also take place between CA3 and CA1 place cells with the same receptive field as both would fire near simultaneously and are anatomically coupled via the Schaffer collateral to CA1 pathway.

Figure 2

Patterns of activity reflecting spatial exploration during the online state are recapitulated during offline epochs including quiet waking immediately following activity, REM sleep, and slow wave sleep. The greatest degree of temporal overlap in firing patterns occurs between cells with overlapping place fields.