Updating memories—The role of prediction errors in memory reconsolidation

Exton-McGuinness, Marc T. J.; Lee, Jonathan; Reichelt, Amy C.

doi:10.1016/j.bbr.2014.10.011

Cited by 175 publications

(162 citation statements)

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“…However, with increasing nonreinforced stimulus reexposure, it is unlikely that there is a sufficient qualitative or quantitative change in the prediction error signal to explain the transition to the null point and beyond to the NMDA receptor-dependent extinction phase. Moreover, it is not obvious how the instantiation of prediction error-mediated learning, for example, within the Rescorla-Wagner rule (Rescorla and Wagner 1972), is consistent with the new learning that is characteristic of extinction, rather than prediction error-mediated memory weakening (Exton-McGuinness et al 2015). Indeed, it is possible, and perhaps likely, that there are independent mechanisms controlling destabilization and NMDA-receptor dependent extinction (Exton-McGuinness et al 2015).…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, it is not obvious how the instantiation of prediction error-mediated learning, for example, within the Rescorla-Wagner rule (Rescorla and Wagner 1972), is consistent with the new learning that is characteristic of extinction, rather than prediction error-mediated memory weakening (Exton-McGuinness et al 2015). Indeed, it is possible, and perhaps likely, that there are independent mechanisms controlling destabilization and NMDA-receptor dependent extinction (Exton-McGuinness et al 2015). While a sharp transition between reconsolidation and extinction might suggest a direct Cold Spring Harbor Laboratory Press on May 9, 2018 -Published by learnmem.cshlp.org Downloaded from interaction between the two, the three-phase transition with an intermediate null point may reflect the independent control of reconsolidation and extinction.…”

Section: Discussionmentioning

confidence: 99%

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On the transition from reconsolidation to extinction of contextual fear memories

et al. 2017

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Retrieval of an associative memory can lead to different phenomena. Brief reexposure sessions tend to trigger reconsolidation, whereas more extended ones trigger extinction. In appetitive and fear cued Pavlovian memories, an intermediate "null point" period has been observed where neither process seems to be engaged. Here we investigated whether this phenomenon extends to contextual fear memory. Adult rats were subjected to a contextual fear conditioning paradigm, reexposed to the context 2 d later for 3, 5, 10, 20, or 30 min, with immediate injections of MK-801 or saline following reexposure, and tested on the following day. We observed a significant effect of MK-801 with the 3-and 30-min sessions, impairing reconsolidation and extinction, respectively. However, it did not have significant effects with 5-, 10-, or 20-min sessions, even though freezing decreased from reexposure to test. Further analyses indicated that this is not likely to be due to a variable transition point at the population level. In conclusion, the results show that in contextual fear memories there is a genuine "null point" between the parameters that induce reconsolidation and extinction, as defined by the effects of MK-801, although NMDA receptor-independent decreases in freezing can still occur in these conditions.[Supplemental material is available for this article.]The retrieval of an associative memory can result in different outcomes. Retrieval in the absence of further reinforcement can destabilize a memory, requiring a process of reconsolidation (Nader and Hardt 2009), or can cause memory extinction through new inhibitory learning (Giustino and Maren 2015). The balance between destabilization and extinction appears to be influenced by the relative strength of learning and extent of nonreinforced retrieval (Eisenberg et al. 2003;Suzuki et al. 2004;Lee et al. 2006;de la Fuente et al. 2011;Flavell and Lee 2013). More extensive stimulus reexposure (i.e., extinction training), or weaker initial conditioning is more likely to result in extinction, whereas more restricted stimulus reexposure preferentially engages memory destabilization. This apparent competition between destabilization and extinction manifests as a bidirectional effect of amnestic treatment, depending of the parameters of conditioning and retrieval. Either reconsolidation is impaired to reduce subsequent memory expression, or extinction is disrupted to maintain expression of the original memory (Eisenberg et al. 2003;Suzuki et al. 2004;Lee et al. 2006;de la Fuente et al. 2011;Flavell and Lee 2013).In both appetitive Pavlovian and conditioned fear memories, recent evidence has indicated that extinction per se does not prevent memory destabilization and reconsolidation. In cue-sucrose, cue-fear, and context-fear settings, there appears to be a reexposure period between the parameters that engage destabilization and extinction, in which there is no behavioral effect of amnestic treatment (Flavell and Lee 2013;Merlo et al. 2014;Alfei et al. 2015). This "limbo" or "null poin...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

On the transition from reconsolidation to extinction of contextual fear memories

et al. 2017

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“…A similar two-trace approach, but focused on attention was initially developed by Pearce and Hall (1980). It is not entirely clear, however, how this model handles the lack of sensitivity to amnestics observed under both training conditions following intermediate amounts of exposure (also see Exton-McGuinness et al 2014a for a potential explanation in terms of attentional processes to the CS). This finding is consistent with a report by Flavell and Lee (2013), using an appetitive learning task and MK-801 as amnesic agent.…”

Section: Discussionmentioning

confidence: 99%

Prediction error and trace dominance determine the fate of fear memories after post-training manipulations

et al. 2015

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Different mnemonic outcomes have been observed when associative memories are reactivated by CS exposure and followed by amnestics. These outcomes include mere retrieval, destabilization-reconsolidation, a transitional period (which is insensitive to amnestics), and extinction learning. However, little is known about the interaction between initial learning conditions and these outcomes during a reinforced or nonreinforced reactivation. Here we systematically combined temporally specific memories with different reactivation parameters to observe whether these four outcomes are determined by the conditions established during training. First, we validated two training regimens with different temporal expectations about US arrival. Then, using Midazolam (MDZ) as an amnestic agent, fear memories in both learning conditions were submitted to retraining either under identical or different parameters to the original training. Destabilization (i.e., susceptibly to MDZ) occurred when reactivation was reinforced, provided the occurrence of a temporal prediction error about US arrival. In subsequent experiments, both treatments were systematically reactivated by nonreinforced context exposure of different lengths, which allowed to explore the interaction between training and reactivation lengths. These results suggest that temporal prediction error and trace dominance determine the extent to which reactivation produces the different outcomes.

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“…Similarly, the idea that 'reconsolidation is the mechanistic instantiation of memory updating' (J. L. Lee, 2009, p. 418), has received widespread attention (e.g., Besnard et al, 2012;Exton-McGuinness, Lee, & Reichelt, 2015;Hardt et al, 2010;Nader et al, 2000b;Sara, 2000b;Tronson & Taylor, 2007). According to this account, the reconsolidation process that is triggered upon trace retrieval opens a transient window of plasticity during which the trace can be updated with incoming environmental information.…”

Section: Overview Of Thesismentioning

confidence: 99%

“…Although physiological interventions are intended to directly disrupt the putative molecular substrates of reconsolidation, considerable ambiguity surrounds the envisioned mechanism by which a behavioral intervention might influence these same processes. Indeed, reconsolidation-updating claims are typically cast in broad terms (Dudai, 2009;Exton-McGuinness et al, 2015;Hardt et al, 2010;J. L. Lee, 2009), and the qualitative nature of empirical outcomes taken to support these claims varies considerably.…”

Section: Overview Of Thesismentioning

confidence: 99%

Persistence and plasticity in the human memory system: An empirical investigation of the overwriting hypothesis

Hardwicke¹

2017

Preprint

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The human memory system must resolve a critical tension, ensuring that knowledge endures over time (persistence), whilst simultaneously retaining a capacity for updating when knowledge is outdated or erroneous (plasticity). In this thesis, I examine the provocative idea that memory traces can be overwritten with new information, especially during transient periods of retrieval-induced plasticity that occur when a trace undergoes reconsolidation. A systematic review of human reconsolidation studies finds that the evidentiary support for this claim is remarkably tenuous. Furthermore, the theory fails to survive several strong empirical tests. In Experiments 1-7, I do not replicate a previous finding that is widely cited as a convincing demonstration of human reconsolidation. In Experiments 8-10, I revisit the ‘destructive updating’ account of the classic ‘misinformation effect’ in the context of reconsolidation theory. These experiments show that the effect can be eliminated when an appropriate recognition test is used, demonstrating that event traces are not irrecoverably lost, and therefore cannot have been overwritten during reconsolidation. In Experiment 11, I examine whether prior retrieval will help or hinder the correction of naturally occurring semantic misconceptions. Contrary to reconsolidation theory, I find that knowledge updating is not contingent on memory retrieval, nor does it result in the overwriting of prior knowledge.Finally, in the context of media ‘breaking news’ reports (Experiment 12), I find that the provision of an explicit retraction message, coupled with an alternative account with high causal coverage, is insufficient to eliminate reliance on false information. Finally, I contend that the widespread proliferation of ad hoc hypotheses, and the absence of systematic direct replication, has caused the field of reconsolidation to descend into a theoretical quagmire.I make several recommendations based on the principles of open science that may help to restore mechanisms of self-correction and foster genuine theoretical progress.

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Updating memories—The role of prediction errors in memory reconsolidation

Cited by 175 publications

References 130 publications

On the transition from reconsolidation to extinction of contextual fear memories

On the transition from reconsolidation to extinction of contextual fear memories

Prediction error and trace dominance determine the fate of fear memories after post-training manipulations

Persistence and plasticity in the human memory system: An empirical investigation of the overwriting hypothesis

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