A Mismatch-Based Model for Memory Reconsolidation and Extinction in Attractor Networks

Oşan, Remus; Tort, Adriano Bretanha Lopes; Amaral, Olavo B.

doi:10.1371/journal.pone.0023113

Cited by 57 publications

(98 citation statements)

References 100 publications

(175 reference statements)

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“…Previous studies have suggested a critical role for prediction error in triggering reconsolidation across a number of paradigms (Reichelt and Lee 2012;Díaz-Mataix et al 2013;Reichelt et al 2013;Sevenster et al 2013;Alfei et al 2015), a finding that has also been incorporated by computational models (Osan et al 2011;Gershman et al 2017). 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.…”

Section: Discussionmentioning

confidence: 96%

“…This has led to the suggestion that there is a trace dominance effect, with the trace that is dominantly activated by memory retrieval being the one impaired by amnestic treatment, such as NMDA receptor antagonism or protein synthesis inhibition (Eisenberg et al 2003). Mechanisms for such trace dominance have been postulated by computational models, in which different degrees of similarity between training and reexposure lead to reconsolidation or extinction-like phenomena (Osan et al 2011;Gershman et al 2017). However, these models do not predict a null point in which neither reconsolidation nor extinction is dominantly activated, leading to the lack of effect of MK-801.…”

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: 96%

Section: Discussionmentioning

confidence: 99%

On the transition from reconsolidation to extinction of contextual fear memories

et al. 2017

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“…With respect to reactivation of memory during wakefulness, it has been argued that the induced cycle of labilization and reconsolidation enables the updating of items in memory (Forcato et al, 2014;Hupbach et al, 2008;. Thus, reactivating cues producing stronger mismatch may be more effective in labilizing a memory representation (Osan et al, 2011). Yet, during sleep there is naturally no external stimulus input that could be used for meaningfully updating a representation.…”

Section: Systems Consolidation During Sleep: Unsupervised Learning?mentioning

confidence: 99%

The Consolidation and Transformation of Memory

Dudai

Karni

Born

2015

Neuron

498

464

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Memory consolidation refers to the transformation over time of experience-dependent internal representations and their neurobiological underpinnings. The process is assumed to be embodied in synaptic and cellular modifications at brain circuits in which the memory is initially encoded and to proceed by recurrent reactivations, both during wakefulness and during sleep, culminating in the distribution of information to additional locales and integration of new information into existing knowledge. We present snapshots of our current knowledge and gaps in knowledge concerning the progress of consolidation over time and the cognitive architecture that supports it and shapes our long-term memories.

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“…We showed that memory reactivation induces simple retrieval, reconsolidation or new learning (Osan et al 2011;Piñeyro et al 2014), as a function of the number of reactivation trials. Our data showed that in the absence of PE, the retrieved memory remained intact, although a single PE was required for memory destabilization.…”

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confidence: 93%

Prediction error demarcates the transition from retrieval, to reconsolidation, to new learning

2014

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Although disrupting reconsolidation is promising in targeting emotional memories, the conditions under which memory becomes labile are still unclear. The current study showed that post-retrieval changes in expectancy as an index for prediction error may serve as a read-out for the underlying processes engaged by memory reactivation. Minor environmental changes define whether retrieval induces memory reconsolidation or the initiation of a new memory trace even before fear extinction can be observed.[Supplemental material is available for this article.]The recent appreciation of memory as a dynamic rather than static process inspires new fundamental questions about memory malleability. After the formation of associative fear memory, a reencounter with the feared stimulus can lead to various outcomes; retrieval only, reconsolidation, or new learning. Insights into how the system determines whether a memory trace should be updated or an additional memory trace should be formed are essential not only for our understanding of the fundamentals of learning and memory but also for the development of reconsolidation based treatment.Prediction error (PE)-a mismatch between what is expected based on previous experiences and the actual state of events (Rescorla and Wagner 1972)-is a necessary condition for inducing reconsolidation of human associative fear memory upon retrieval (Sevenster et al. 2013). Previously, we have shown the utility of retrieval-induced changes in the expectancy ratings of the unconditioned stimulus (US) during presentation of the conditioned stimulus (CS) as a measure of PE (Sevenster et al. 2013). This behavioral and noninvasive index of PE may indicate whether the original memory trace was destabilized by the retrieval experience, independent of the outcome of the reconsolidation process itself. It may, however, be questioned whether PE is a sufficient condition for reconsolidation, given that PE can also give rise to new learning instead (e.g., extinction learning) (Rescorla and Wagner 1972). For example, extinction training, which involves the formation of a new inhibitory memory trace (Bouton 2002), puts a constraint on reconsolidation (Eisenberg et al. 2003;Lee et al. 2006;Bos et al. 2012). During extinction training, repeated or prolonged unreinforced exposure generates multiple PEs, which eventually reduces both threat expectancy and fear responding. However, the transition from updating of the original memory trace to the formation of a new memory trace may occur long before the expression of the inhibitory extinction memory can be observed. Until now, the restraint that new learning puts on reconsolidation could only be inferred from extinction of the fear behavior itself. In the current study, we tested whether changes in threat expectancy could serve not only as an index of memory destabilization, but could also reveal a boundary condition of reconsolidation independent from the fear reduction itself. Hereto, we established the optimal parameters for fear acquisition and memory reactivati...

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A Mismatch-Based Model for Memory Reconsolidation and Extinction in Attractor Networks

Cited by 57 publications

References 100 publications

On the transition from reconsolidation to extinction of contextual fear memories

On the transition from reconsolidation to extinction of contextual fear memories

The Consolidation and Transformation of Memory

Prediction error demarcates the transition from retrieval, to reconsolidation, to new learning

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