Remote Memory and the Hippocampus: A Constructive Critique

The hippocampus is known to be recruited during the recall of experiences from our distant past, despite evidence that memory traces in this region vanish over time. Extant theories of systems-level consolidation have yet to accommodate both phenomena. We propose that the hippocampus reconstructs remote memories in the absence of the original trace. It accomplishes this by assembling consolidated neocortical elements into spatially coherent scenes that form the basis of unfolding memory events. This reconstruction is likely facilitated by input from the ventromedial prefrontal cortex. This process-oriented approach to hippocampal recruitment during remote recollection is consistent with its increasingly acknowledged role in constructing mental representations beyond the domain of memory. It is widely agreed the hippocampus plays a crucial role in memory encoding. The question of how long a hippocampal trace is required to retrieve a memory is unresolved. Opposing theoretical accounts advocate either the hippocampus is unnecessary for memory retrieval in the longer term or that is it required in perpetuity. There is evidence from animal and human work to support both views; consequently, extant theories cannot account for these conflicting findings. We suggest that the hippocampal role in memory retrieval is not simply a question of persistence, but is best characterised as a functional shift over time from retention to reconstruction of the past in the absence of the original trace. This new perspective accounts for existing data and offers a means to leverage a clearer understanding of the hippocampal-neocortical interactions that support memory retrieval.