Trends in Cognitive Sciences
OpinionRemote Memory and the Hippocampus: A Constructive Critique
Section snippets
A Divergent Debate on Hippocampal-Dependent Memory
Hippocampal damage impairs the formation and recall of recent memories in humans [1], non-human primates [2], and rodents [3]. However, conflicting evidence regarding its necessity for remote memory retrieval has generated two opposing perspectives. There is cross-species evidence of temporally graded retrograde amnesia (see Glossary), the preservation of older memories following hippocampal damage 4, 5, 6. This reinforces the view of the standard consolidation theory that memories are stored
The Evanescent Hippocampal Engram
Theoretical accounts of how memory traces are stored within the hippocampus have been motivated both by its architecture and neural activity. Initial input to the hippocampal circuit generates sparse activity in the dentate gyrus, assumed to reduce interference between similar memories. These distinct patterns are conveyed to CA3, where intrinsic recurrent connections are thought to form a complete memory trace. The resultant output produces a sparse pattern in CA1, and this unique
A Consensus on Consolidation
Systems-level consolidation is a hypothesised time-dependent process of hippocampal-facilitated strengthening of neocortical neural connections post-learning 64, 65. Supporting evidence in humans arises from hippocampal [66] and neocortical [67] reinstatement of activity patterns present at encoding during subsequent quiescence and sleep. This regional activity is synchronised [68], with bursts of hippocampal activity being entrained by slower oscillations in the neocortex [69]. Memory replay
Reconstruction of the Past by the Hippocampus
Hippocampal damage in humans can impair the recollection of specific autobiographical memories from any period of life before the damage occurred 8, 9 (Figure 2C), and neuroimaging studies in healthy individuals reveal hippocampal engagement during the recollection of both recent and remote autobiographical memories [95]. This implies that no duration of systems-level consolidation will relieve the hippocampus of a role in retrieval. Likewise, hippocampal lesions in rodents yield a flat
The Remote Control of Memory
Time-dependent strengthening of connectivity between neocortical modules is thought to form the basis of systems-level consolidation. The medial prefrontal cortex becomes an increasingly important hub during this process, with lesions selectively disrupting remote memories in animals [131]. Likewise, in humans, memory-specific activity patterns emerge in the ventromedial prefrontal cortex (vmPFC) over the course of consolidation 93, 94, 132 while vmPFC damage impairs autobiographical memory
Concluding Remarks and Future Perspectives
A proliferation of evidence challenges the notion of permanent hippocampal memory traces. Core assumptions underlying extant perspectives on systems-level consolidation and the fundamental role of the hippocampus may need to be reassessed. The hippocampus is unlikely to be a permanent indexer of memories. Given the extraordinary demands placed upon the hippocampus for continuous encoding of experience, and the required representational flexibility involved in imagination and future-thinking,
Acknowledgements
The authors are supported by a Wellcome Principal Fellowship to E.A.M. (210567/Z/18/Z).
Glossary
- Consolidation
- the strengthening of neuronal connections on both a cellular and a network level, manifesting as the successful subsequent retention of learned information.
- Delta waves
- low-frequency (1–4-Hz) synchronised neural activity that is prevalent during sleep.
- Episodic/autobiographical memory
- the multisensory mental reconstruction of a personally experienced past event from a particular place and time.
- Long-term potentiation/depression
- the persistent strengthening or weakening of postsynaptic
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