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Remote Memory and the Hippocampus: a Constructive Critique

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Remote Memory and the Hippocampus: a Constructive Critique TICS 1866 No. of Pages 15 Opinion Remote Memory and the Hippocampus: A Constructive Critique 1 1, Daniel N. Barry and Eleanor A. Maguire * The hippocampus is known to be recruited during the recall of experiences from Highlights our distant past, despite evidence that memory traces in this region vanish over It is widely agreed the hippocampus plays a crucial role in memory time. Extant theories of systems-level consolidation have yet to accommodate encoding. both phenomena. We propose that the hippocampus reconstructs remote The question of how long a hippocam- memories in the absence of the original trace. It accomplishes this by assem- pal trace is required to retrieve a mem- bling consolidated neocortical elements into spatially coherent scenes that ory is unresolved. form the basis of unfolding memory events. This reconstruction is likely facili- Opposing theoretical accounts advo- tated by input from the ventromedial prefrontal cortex. This process-oriented cate either the hippocampus is unne- approach to hippocampal recruitment during remote recollection is consistent cessary for memory retrieval in the with its increasingly acknowledged role in constructing mental representations longer term or that is it required in perpetuity. There is evidence from ani- beyond the domain of memory. mal and human work to support both views; consequently, extant theories A Divergent Debate on Hippocampal-Dependent Memory cannot account for these conflicting fi Hippocampal damage impairs the formation and recall of recent memories in humans [1], non- ndings. human primates [2], and rodents [3]. However, conflicting evidence regarding its necessity for We suggest that the hippocampal role remote memory retrieval has generated two opposing perspectives. There is cross-species in memory retrieval is not simply a evidence of temporally graded retrograde amnesia (see Glossary), the preservation of older question of persistence, but is best memories following hippocampal damage [4–6]. This reinforces the view of the standard characterised as a functional shift over time from retention to reconstruction of consolidation theory that memories are stored in progressively strengthened cortico-cortical the past in the absence of the original connections, known as system-level consolidation, while the hippocampal memory trace/ trace. engram fades, after which the hippocampus is no longer required for retrieval [7] (Figure 1A). This new perspective accounts for existing data and offers a means to However, comparably strong evidence also exists to the contrary. Impairment in the recall of leverage a clearer understanding of memories regardless of their age has been observed following hippocampal damage, particu- the hippocampal-neocortical interac- larly where the retrieval of a specific context is essential, as for episodic/autobiographical tions that support memory retrieval. memories [8,9]. A resultant reformulation, the multiple trace theory (and its recent elabora- tion the trace transformation theory), asserts that episodic memory traces are cumulatively stored in the hippocampus, thus assigning a perpetual role to this region in the retrieval of the original complete representations [10,11] (Figure 1B). Other prominent accounts of hippocam- pal functioning also incorporate the notion that memory retrieval involves the reactivation or recombination of consolidated hippocampal memory traces [12,13]. However, recent compelling evidence in both humans [14] and rodents [15] provides support for the long-standing tenet of the standard consolidation theory that the hippocampus has a 1 Wellcome Centre for Human fi time-limited role in memory storage. To reconcile these ndings with the seemingly perpetual Neuroimaging, Queen Square Institute involvement of the hippocampus in episodic memory retrieval, we propose a reconceptualisa- of Neurology, University College London, 12 Queen Square, London tion of the hippocampal contribution to remote memory. The hippocampus may reconstruct WC1N 3AR, UK past experience in the absence of the original trace (Figure 1C). In light of this hypothesis, we outline the mounting evidence for systems-level consolidation and consider the neocortical- Trends in Cognitive Sciences, Month Year, Vol. xx, No. yy https://doi.org/10.1016/j.tics.2018.11.005 1 © 2018 Elsevier Ltd. All rights reserved. TICS 1866 No. of Pages 15 Time Glossary Consolidation: the strengthening of Recent memory Remote memory Remote memory neuronal connections on both a cellular and a network level, Neocortex Neocortex Neocortex manifesting as the successful (A) subsequent retention of learned information. Delta waves: low-frequency (1–4- Hz) synchronised neural activity that Standard is prevalent during sleep. consolidaƟon Episodic/autobiographical theory memory: the multisensory mental reconstruction of a personally experienced past event from a particular place and time. Long-term potentiation/ Hippocampus Hippocampus Hippocampus depression: the persistent strengthening or weakening of Neocortex Neocortex Neocortex postsynaptic neuronal excitability following presynaptic stimulation, and (B) a long-standing model of memory storage. Memory trace/engram: a MulƟple trace distributed network of inter-neuronal theory/trace structural connections that facilitates transformaƟon subjective re-experiencing of a past event when activated. theory Multiple trace theory: the proposed perpetual dependence of detailed episodic memories on traces Hippocampus Hippocampus Hippocampus stored in the hippocampus; its further elaboration is called the trace transformation theory. Neocortex Neocortex Neocortex N-Methyl-d-aspartic acid (C) receptor: a primarily postsynaptic excitatory receptor, gated by glutamate and implicated in learning and memory. Scene Neurogenesis: the creation of new construcƟon neurons that occurs throughout theory adulthood, predominantly observed in the granule cell layer of the dentate gyrus in the hippocampus. Optogenetics: the targeting of photo-sensitive proteins by light, to Hippocampus Hippocampus Hippocampus either activate or silence a neuron that expresses these proteins. Place cell: hippocampal neurons Figure 1. Three Perspectives on the Hippocampal-Neocortical Connectivity Underlying Systems-Level that increase their firing rate in a Consolidation. (A) Standard consolidation theory [7] proposes that a declarative memory (a past event or factual particular environmental location, information) is initially encoded in a hippocampal-neocortical trace (left, red lines and spheres) but, over time, becomes known as a ‘place field’, irrespective stabilised in a pattern of connectivity between neocortical modules (middle, red lines and spheres). Adapted, with of where an animal is looking. permission [131]. After this consolidation period, the original hippocampal trace is no longer required to reactivate the Reconsolidation: the process by memory (middle). This is true for any subsequent retrieval of this memory (right). (B) Multiple trace theory/trace transforma- which previously consolidated tion theory states that a hippocampal-neocortical trace (left, blue lines and red spheres) is always required for a detailed memories can become destabilised episodic memory (middle, blue lines and red spheres), with repeated retrieval of this memory increasing the number of or strengthened upon reactivation. these permanent hippocampal traces (middle and right, red spheres) [10]. The intrinsic neocortical connectivity that Reinstatement: a spatially emerges over time (middle and right, green lines) supports memories of a more factual and semantic nature that have been distributed or temporal neural pattern derived from repeated recall [11]. (C) Scene construction theory [62] proposes that during the recall of a recent event, the observed during memory retrieval hippocampus constructs a series of coherent scenes from this episode through hippocampal-neocortical interactions (left, that was previously present during blue lines and red spheres). These fade rapidly from the hippocampus as representations are consolidated in the neocortex encoding. (Figure legend continued on the bottom of the next page.) 2 Trends in Cognitive Sciences, Month Year, Vol. xx, No. yy TICS 1866 No. of Pages 15 hippocampal interactions that may facilitate the reconstruction of remote memories during Retrograde amnesia: an retrieval. impairment in recalling the past, affecting either all memories (flat gradient), or disproportionately The Evanescent Hippocampal Engram affecting either recent or remote Theoretical accounts of how memory traces are stored within the hippocampus have been memories (temporal gradient). Scene construction theory: a motivated both by its architecture and neural activity. Initial input to the hippocampal circuit proposal that the hippocampal generates sparse activity in the dentate gyrus, assumed to reduce interference between similar contribution to memory, imagination, memories. These distinct patterns are conveyed to CA3, where intrinsic recurrent connections prospection, and navigation is the are thought to form a complete memory trace. The resultant output produces a sparse pattern construction of naturalistic 3D spatially coherent scene in CA1, and this unique representation is relayed back to the neocortex [16]. This output has representations of the world typically been proposed to index neocortical locations relevant to a specific memory [17]. Therefore, populated by objects and viewed tracking the structural and functional integrity of hippocampal
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