Systems consolidation, transformation and reorganization: Multiple Trace Theory, Trace Transformation Theory and their Competitors

We review the literature on systems consolidation by providing a brief history of the field to place the current research in proper perspective. We cover the literature on both humans and non-humans, which are highly related despite the differences in techniques and tasks that are used. We argue that understanding the interactions between hippocampus and neocortex (and other structures) that underlie systems consolidation, depend on appreciating the close correspondence between psychological and neural representations of memory, as postulated by Multiple Trace Theory and Trace Transformation Theory. We end by evaluating different theories of systems consolidation in light of the evidence we reviewed and suggest that the concept of systems consolidation, with its central concern with the time-limited role the hippocampus plays in memory, may have outlived its usefulness. We suggest replacing it with a program of research on the psychological processes and neural mechanisms that underlie changes in memory across the lifetime – a natural history of memory change.

Transfer effects in auditory temporal preparation occur using an unfilled but not filled foreperiod

How quickly participants respond to a “go” after a “warning” signal is partly determined by the time between the two signals (the foreperiod) and the distribution of foreperiods. According to Multiple Trace Theory of Temporal Preparation (MTP), participants use memory traces of previous foreperiods to prepare for the upcoming go signal. If the processes underlying temporal preparation reflect general encoding and memory principles, transfer effects (the carryover effect of a previous block’s distribution of foreperiods to the current block) should be observed regardless of the sensory modality in which signals are presented. Despite convincing evidence for transfer effects in the visual domain, only weak evidence for transfer effects has been documented in the auditory domain. Three experiments were conducted to examine whether such differences in results are due to the modality of the stimulus or other procedural factors. In each experiment, two groups of participants were exposed to different foreperiod distributions in the acquisition phase and to the same foreperiod distribution in the transfer phase. Experiment 1 used a choice-reaction time (RT) task, and the warning signal remained on until the go signal, but there was no evidence for transfer effects. Experiments 2 and 3 used a simple- and choice-RT task, respectively, and there was silence between the warning and go signals. Both experiments revealed evidence for transfer effects, which suggests that transfer effects are most evident when there is no auditory stimulation between the warning and go signals.

The mysteries of remote memory

Long-lasting memories form the basis of our identity as individuals and lie central in shaping future behaviours that guide survival. Surprisingly, however, our current knowledge of how such memories are stored in the brain and retrieved, as well as the dynamics of the circuits involved, remains scarce despite seminal technical and experimental breakthroughs in recent years. Traditionally, it has been proposed that, over time, information initially learnt in the hippocampus is stored in distributed cortical networks. This process—the standard theory of memory consolidation—would stabilize the newly encoded information into a lasting memory, become independent of the hippocampus, and remain essentially unmodifiable throughout the lifetime of the individual. In recent years, several pieces of evidence have started to challenge this view and indicate that long-lasting memories might already ab ovo be encoded, and subsequently stored in distributed cortical networks, akin to the multiple trace theory of memory consolidation. In this review, we summarize these recent findings and attempt to identify the biologically plausible mechanisms based on which a contextual memory becomes remote by integrating different levels of analysis: from neural circuits to cell ensembles across synaptic remodelling and epigenetic modifications. From these studies, remote memory formation and maintenance appear to occur through a multi-trace, dynamic and integrative cellular process ranging from the synapse to the nucleus, and represent an exciting field of research primed to change quickly as new experimental evidence emerges. This article is part of a discussion meeting issue ‘Of mice and mental health: facilitating dialogue between basic and clinical neuroscientists’.

Autonoetic Consciousness in Autobiographical Memories after Medial Temporal Lobe Resection

This study aims to investigate autonoetic consciousness associated with episodic autobiographical memory in patients who had undergone unilateral medial temporal lobe resection for intractable epilepsy. Autonoetic consciousness, defined as the conscious feeling of mentally travelling back in time to relive a specific event, was assessed using the Remember/Know (R/K) paradigm across different time periods as proposed in the autobiographical memory task developed by Piolino et al. (TEMPau task). Results revealed that the two patient groups (left and right temporal resection) gave reduced sense of reliving (R) responses and more familiarity (K) responses than healthy controls. This poor autonoetic consciousness was highlighted when patients were asked to justify their Remember responses by recalling sensory-perceptive, affective or spatiotemporal specific details across all life periods. These results support the bilateral MTL contribution to episodic autobiographical memory covering the entire lifespan, which is consistent with the multiple trace theory of MTL function [7,9]. This study also demonstrates the bilateral involvement of MTL structures in recalling specific details of personal events characterized by autonoetic consciousness.

Autobiographical Memory Retrieval and Hippocampal Activation as a Function of Repetition and the Passage of Time

Multiple trace theory (MTT) predicts that hippocampal memory traces expand and strengthen as a function of repeated memory retrievals. We tested this hypothesis utilizing fMRI, comparing the effect of memory retrieval versus the mere passage of time on hippocampal activation. While undergoing fMRI scanning, participants retrieved remote autobiographical memories that had been previously retrieved either one month earlier, two days earlier, or multiple times during the preceding month. Behavioral analyses revealed that the number and consistency of memory details retrieved increased with multiple retrievals but not with the passage of time. While all three retrieval conditions activated a similar set of brain regions normally associated with autobiographical memory retrieval including medial temporal lobe structures, hippocampal activation did not change as a function of either multiple retrievals or the passage of time. However, activation in other brain regions, including the precuneus, lateral prefrontal cortex, parietal cortex, lateral temporal lobe, and perirhinal cortex increased after multiple retrievals, but was not influenced by the passage of time. These results have important implications for existing theories of long-term memory consolidation.

The loss of episodic memories in retrograde amnesia: single–case and group studies

Retrograde amnesia in neurological disorders is a perplexing and fascinating research topic. The severity of retrograde amnesia is not well correlated with that of anterograde amnesia, and there can be disproportionate impairments of either. Within retrograde amnesia, there are various dissociations which have been claimed—for example, between the more autobiographical (episodic) and more semantic components of memory. However, the associations of different types of retrograde amnesia are also important, and clarification of these issues is confounded by the fact that retrograde amnesia seems to be particularly vulnerable to psychogenic factors. Large frontal and temporal lobe lesions have been postulated as critical in producing retrograde amnesia. Theories of retrograde amnesia have encompassed storage versus access disruption, physiological processes of ‘consolidation’, the progressive transformation of episodic memories into a more ‘semantic’ form, and multiple–trace theory. Single–case investigations, group studies and various forms of neuroimaging can all contribute to the resolution of these controversies.