Hebbian plasticity in parallel synaptic pathways: A circuit mechanism for systems memory consolidation

Abstract Systems memory consolidation involves the transfer of memories across brain regions and the transformation of memory content. For example, declarative memories that transiently depend on the hippocampal formation are transformed into long-term memory traces in neocortical networks, and procedural memories are transformed within cortico-striatal networks. These consolidation processes are thought to rely on replay and repetition of recently acquired memories, but the cellular and network mechanisms that mediate the changes of memories are poorly understood. Here, we suggest that systems memory consolidation could arise from Hebbian plasticity in networks with parallel synaptic pathways — two ubiquitous features of neural circuits in the brain. We explore this hypothesis in the context of hippocampus-dependent memories. Using computational models and mathematical analyses, we illustrate how memories are transferred across circuits and discuss why their representations could change. The analyses suggest that Hebbian plasticity mediates consolidation by transferring a linear approximation of a previously acquired memory into a parallel pathway. Our modelling results are further in quantitative agreement with lesion studies in rodents. Moreover, a hierarchical iteration of the mechanism yields power-law forgetting — as observed in psychophysical studies in humans. The predicted circuit mechanism thus bridges spatial scales from single cells to cortical areas and time scales from milliseconds to years. Author summary After new memories are acquired, they can be transferred over time into other brain areas — a process called systems memory consolidation. For example, new declarative memories, which refer to the conscious memory of facts and events, depend on the hippocampus. Older declarative memories, however, also rely on neocortical networks. The cellular mechanisms underlying such a transfer are poorly understood. In this work, we show that a simple and in the brain ubiquitous connectivity pattern, combined with a standard learning rule, leads to gradual memory transfer. We illustrate our proposed mechanism in numerical simulations and mathematical analyses. At the neurophysiological level, our theory explains experimental findings on memory storage in the hippocampal formation when specific pathways between neural populations are disrupted. At the psychophysical level, we can account for the power-law forgetting curves typically found in humans. A consequence of the proposed model is that consolidated memories can yield faster responses because they are stored in increasingly shorter synaptic pathways between sensory and motor areas. By giving a mechanistic explanation of the consolidation process, we contribute to the understanding of the transfer of memories and the reorganization of memories over time.

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