Abstract
Over the past four decades, a “standard framework” has emerged to explain the neural mechanisms of episodic memory storage. This framework has been instrumental in driving hippocampal research forward and now dominates the design and interpretation of experimental and theoretical studies. It postulates that cortical inputs drive plasticity in the recurrent cornu ammonis 3 (CA3) synapses to rapidly imprint memories as attractor states in CA3. Here we review a range of experimental studies and argue that the evidence against the standard framework is mounting, notwithstanding the considerable evidence in its support. We propose CRISP as an alternative theory to the standard framework. CRISP is based on Context Reset by dentate gyrus (DG), Intrinsic Sequences in CA3, and Pattern completion in cornu ammonis 1 (CA1). Compared to previous models, CRISP uses a radically different mechanism for storing episodic memories in the hippocampus. Neural sequences are intrinsic to CA3, and inputs are mapped onto these intrinsic sequences through synaptic plasticity in the feedforward projections of the hippocampus. Hence, CRISP does not require plasticity in the recurrent CA3 synapses during the storage process. Like in other theories DG and CA1 play supporting roles, however, their function in CRISP have distinct implications. For instance, CA1 performs pattern completion in the absence of CA3 and DG contributes to episodic memory retrieval, increasing the speed, precision, and robustness of retrieval. We propose the conceptual theory, discuss its implications for experimental results and suggest testable predictions. It appears that CRISP not only accounts for those experimental results that are consistent with the standard framework, but also for results that are at odds with the standard framework. We therefore suggest that CRISP is a viable, and perhaps superior, theory for the hippocampal function in episodic memory.
Highlights
The human hippocampus is important for episodic memories (Scoville and Milner, 1957)
Mutants showed a deficit when tested 3 h after conditioning, but performed as well as controls when tested after 24 h. While this and the previous study suggest a role of plasticity at the recurrent cornu ammonis 3 (CA3) synapse in the learning of some aspects of the tasks, they argue against the notion that plasticity in CA3 is required for single-trial memory storage per se because mutants were able to store and retrieve one-trial memories in some conditions
dentate gyrus (DG) inputs are more likely to drive downstream CA3 spike, if the DG cell spikes at a high rate (Urban et al, 2001; Henze et al, 2002; Mori et al, 2004) and there are suggestions that firing rates are higher in novel than in familiar environments, at least in cornu ammonis 1 (CA1) (Karlsson and Frank, 2008)
Summary
Over the past four decades, a “standard framework” has emerged to explain the neural mechanisms of episodic memory storage. This framework has been instrumental in driving hippocampal research forward and dominates the design and interpretation of experimental and theoretical studies. It postulates that cortical inputs drive plasticity in the recurrent cornu ammonis 3 (CA3) synapses to rapidly imprint memories as attractor states in CA3. We propose the conceptual theory, discuss its implications for experimental results and suggest testable predictions.
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