Trends in Neurosciences
OpinionReconsolidation: maintaining memory relevance
Introduction
An introspective analysis of memory clearly suggests that human memories are neither constant in content nor of fixed strength. Memory retrieval is often triggered by a similar experience that subsequently intermeshes with and modifies future recollections. The reconstructive nature of memory retrieval and memory malleability in general is recognized within the domains of cognitive psychology and neuroscience 1, 2. However, this cognitive level of analysis is not immediately reconciled with the molecular neurobiological understanding of learning and memory. The interest generated by the study of synaptic plasticity in both hippocampal slices and simpler invertebrate models has led to a surge in knowledge at the cellular level. Whereas mammalian behavioural studies are equally plentiful, the neurobiological analysis has largely been conducted within the theoretical framework of memory consolidation and the time-dependent stabilization of plasticity [3], an implicit assumption of which is that memories are subsequently stable and fixed.
The phenomenon of ‘memory reconsolidation’ [4] has the potential to bridge the divide between cellular and cognitive accounts of long-term memory. I will not provide a comprehensive review of the extensive literature on the cellular and behavioural mechanisms of memory reconsolidation (reviews of this nature are relatively plentiful, e.g. Refs 5, 6, 7, 8, 9, 10). Instead, I will focus on a particular viewpoint, namely that reconsolidation serves to enable the updating of memories, ultimately to maintain their predictive and adaptive relevance. Therefore, it is important to note that reconsolidation does not simply represent an automatic restabilization of a retrieved memory, but is a special process that presents an opportunity for adaptive modification. Moreover, the numerous negative findings in relation to reconsolidation can be argued to result from the use of experimental conditions that fail to engage a memory updating process (thereby explaining the existence of boundary conditions on memory reconsolidation). Given the emphasis on normal learning and memory processes, it is also possible to integrate ideas on reconsolidation and memory updating with traditional learning theories, and I will focus on the potential role of surprise and prediction error. Finally, I will conclude with the broad implications of a memory updating hypothesis of reconsolidation, both in terms of how reconsolidation itself might be viewed as an epiphenomenon, and the conclusion that experimental amnesia must reflect storage impairments.
Section snippets
Reconsolidation and memory updating
The reconsolidation phenomenon is an increasingly studied area in learning and memory and describes a fundamental finding that the retrieval (or ‘reactivation’) of a previously stable memory renders that memory vulnerable to the disruptive effects of amnestic agents. Thus, retrieval returns memories to a plastic state. Although much has been learned regarding the mechanisms of reconsolidation, the search for an endogenous function of the process remains a fundamental issue. As noted by Dudai
Reconsolidation is a special process and a special state
Much of the research into memory reconsolidation has taken a comparative view, capitalising upon the wealth of knowledge already gained about consolidation, and the degree to which the molecular substrates of the two processes overlaps is of importance. Indeed, although the mechanisms of memory reconsolidation largely recapitulate those of initial consolidation, there are notable dissociations between the two (see Ref. [6] for a comprehensive review). In particular, there is evidence that
Reconsolidation is common, but is it ubiquitous?
An understanding of when reconsolidation does and does not occur is of primary importance in assigning potential functional roles to the process. Reconsolidation has come to be viewed as an almost universal memory process, with reactivation-dependent amnesia indicative of memory reconsolidation having been observed across a variety of species, from C. elegans [31] to humans 12, 13, 32 (see Ref. [10] for a comprehensive review). Moreover, the majority of studies have been conducted in rodents,
Boundary conditions on reconsolidation
Even in paradigms with well-established demonstrations of reactivation-dependent amnesia, there are conditions under which reconsolidation does not take place. Therefore, there exist certain boundary conditions, which, for the purposes of this review, are considered simply to be a description of the boundaries around which reconsolidation might or might not be observed. Boundary conditions are important in the context of the current discussion as it will be argued that the engagement of
Reconsolidation and memory updating: relation to existing theories
The prior sections argue that currently identified boundary conditions on memory reconsolidation, as well as prior failures to demonstrate reconsolidation in contextual and instrumental memories, are consistent with a hypothesis emphasizing the memory-updating properties of the reactivation experience. Thus, reconsolidation might be viewed as a fundamental process in the ongoing modification and storage of memories.
Several positions have been advanced regarding the role of reconsolidation in
Reconsolidation integrated into learning theory
Given that an updating hypothesis places reconsolidation in a central role in memory persistence, it should be possible to integrate reconsolidation into existing theories of learning and memory. As a salient example, I will focus briefly on only one such area: the role of surprise in learning.
Rescorla and Wagner [62] formalised the role of surprise in their model of learning that places crucial emphasis on prediction error. That is, the amount of learning generated on a particular trial
Reconsolidation updates memory storage
It has been fiercely debated whether experimentally induced consolidation and reconsolidation impairments reflect a storage deficit or an inability to retrieve the memory normally [66]. While there is no conclusive evidence to favour either view, the retrieval account is inconsistent with the proposed action of reconsolidation to modify the strength and even content of a memory. An initial novel finding, making use of positive predictions of the storage view, strongly indicates that
Conclusion
Memory reconsolidation is a rapidly expanding field of research, which is becoming widely accepted as a fundamental process in long-term memory. Although advances are continually being made in terms of the pharmacological and cellular mechanisms of reconsolidation, these do not address the fundamental question of the role of memory reconsolidation in memory persistence. In this review, I have proposed that the function of memory reconsolidation might be to mediate the updating of a memory to
References (69)
Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processes?
Trends Neurosci.
(2005)Memory traces unbound
Trends Neurosci.
(2003)- et al.
Rites of passage of the engram: reconsolidation and the lingering consolidation hypothesis
Neuron
(2004) - et al.
Reactivation-induced interference in a short-term retention paradigm
Learn. Motiv.
(1978) Reconsolidation: the advantage of being refocused
Curr. Opin. Neurobiol.
(2006)- et al.
Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala
Neuroscience
(2004) Disrupting reconsolidation of drug memories reduces cocaine seeking behavior
Neuron
(2005)Effects of glucose and fructose on recently reactivated and recently acquired memories
Prog. Neuropsychopharmacol. Biol. Psychiatry
(1999)- et al.
Post-training and post-reactivation administration of amphetamine enhances morphine conditioned place preference
Behav. Brain Res.
(2006) - et al.
Appetitive memory reconsolidation depends upon NMDA receptor-mediated neurotransmission
Neurobiol. Learn. Mem.
(2008)
Memory reconsolidation: sensitivity of spatial memory to inhibition of protein synthesis in dorsal hippocampus during encoding and retrieval
Neuron
Intrahippocampal anisomycin infusions disrupt previously consolidated spatial memory only when memory is updated
Neurobiol. Learn. Mem.
Protein synthesis inhibition in the basolateral amygdala following retrieval does not impair expression of morphine-associated conditioned place preference
Behav. Brain Res.
Temporally graded requirement for protein synthesis following memory reactivation
Neuron
Cellular and systems reconsolidation in the hippocampus
Neuron
Protein synthesis subserves reconsolidation or extinction depending on reminder duration
Neuron
Make mild moments memorable: add a little arousal
Trends Cog. Sci.
Remembering: A study in Experimental and Social Psychology
The cognitive neuroscience of constructive memory
Annu. Rev. Psychol.
Time-dependent processes in memory storage
Science
Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval
Nature
Molecular mechanisms of memory reconsolidation
Nat. Rev. Neurosci.
Retrieval and reconsolidation: toward a neurobiology of remembering
Learn. Mem.
A single standard for memory: the case for reconsolidation
Nat. Rev. Neurosci.
Post-activation state: a critical rite of passage of memories
Dissociable stages of human memory consolidation and reconsolidation
Nature
Reconsolidation of episodic memories: a subtle reminder triggers integration of new information
Learn. Mem.
Arousal and stress effects on consolidation and reconsolidation of recognition memory
Neuropsychopharmacology
Stress impairs reconsolidation of drug memory via glucocorticoid receptors in the basolateral amygdala
J. Neurosci.
The neurobiology of consolidations, or, how stable is the engram?
Annu. Rev. Psychol.
Linking new information to a reactivated memory requires consolidation and not reconsolidation mechanisms
PLoS Biol.
Memory reconsolidation mediates the strengthening of memories by additional learning
Nat. Neurosci.
Independent cellular processes for hippocampal memory consolidation and reconsolidation
Science
The consolidation of new but not reactivated memory requires hippocampal C/EBP beta
Nat. Neurosci.
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