Abstract
The ability to adapt to new situations involves behavioral changes expressed either from an innate repertoire, or by acquiring experience through memory consolidation mechanisms, by far a much richer and flexible source of adaptation. Memory formation consists of two interrelated processes that take place at different spatial and temporal scales, Synaptic Consolidation, local plastic changes in the recruited neurons, and Systems Consolidation, a process of gradual reorganization of the explicit/declarative memory trace between hippocampus and the neocortex. In this review, we summarize some converging experimental results from our lab that support a normal temporal framework of memory systems consolidation as measured both from the anatomical and the psychological points of view, and propose a hypothetical model that explains these findings while predicting other phenomena. Then, the same experimental design was repeated interposing additional tasks between the training and the remote test to verify for any interference: we found that (a) when the animals were subject to a succession of new learnings, systems consolidation was accelerated, with the disengagement of the hippocampus taking place before the natural time point of this functional switch, but (b) when a few reactivation sessions reexposed the animal to the training context without the shock, systems consolidation was delayed, with the hippocampus prolonging its involvement in retrieval. We hypothesize that new learning recruits from a fixed number of plastic synapses in the CA1 area to store the engram index, while reconsolidation lead to a different outcome, in which additional synapses are made available. The first situation implies the need of a reset mechanism in order to free synapses needed for further learning, and explains the acceleration observed under intense learning activity, while the delay might be explained by a different process, able to generate extra free synapses: depending on the cognitive demands, it deals either with a fixed or a variable pool of available synapses. The Synaptic Occupancy/Reset Theory (SORT) emerged as an explanation for the temporal flexibility of systems consolidation, to encompass the two different dynamics of explicit memories, as well as to bridge both synaptic and systems consolidation in one single mechanism.
Highlights
Reviewed by: Diego Moncada, CONICET Institute of Cell Biology and Neuroscience (IBCN), Argentina Maria-Isabel Miranda, National Autonomous University of Mexico, Mexico
The same experimental design was repeated interposing additional tasks between the training and the remote test to verify for any interference: we found that (a) when the animals were subject to a succession of new learnings, systems consolidation was accelerated, with the disengagement of the hippocampus taking place before the natural time point of this functional switch, but (b) when a few reactivation sessions reexposed the animal to the training context without the shock, systems consolidation was delayed, with the hippocampus prolonging its involvement in retrieval
The first two points were inherited from Multiple Trace Theory (MTT), but the last one is new, and incorporates the very recent paradigm that emphasizes the parallels between HPC/precision and corticalization/generalization, i.e., the supposed connection between the neuroanatomical and the psychological/qualitative points of view
Summary
The ability to adapt to challenging new situations involves both physiological and behavioral changes, and behavior may either be expressed from an innate repertoire of stereotyped responses – which Fuster (1995) calls “phyletic memory” – or by the acquisition of experience through memory mechanisms, or even a combination of both (James, 1890). This would explain memory retrieval without an active HPC, since an extrahippocampal trace, despite weaker, could yet be expressed in some situations This interesting ad hoc hypothesis reintroduces an assumption already present – but frequently understated – in the SMSC (Squire and Alvarez, 1995), that is fully consistent with several other findings from our lab over the years (Jerusalinsky et al, 1994; Sierra et al, 2017 – see below): cortical areas must be recruited simultaneously with the hippocampal system during acquisition/learning in order to, later, support the temporally graded “changing of the guards” between the HPC and the NCTX, i.e., the suggested dual trace seems to exist at last. The first two points were inherited from MTT, but the last one is new, and incorporates the very recent paradigm that emphasizes the parallels between HPC/precision and corticalization/generalization, i.e., the supposed connection between the neuroanatomical and the psychological/qualitative points of view
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