Memory Reconsolidation

1

The Discovery of Memory Reconsolidation

Karim Nader, McGill University, Montreal, Canada

This is an exciting time to be studying learning and memory. Prior to the year 2000, only initial acquisition and memory stabilization, or synaptic consolidation (Dudai, 2004; Kandel, 2001; Martin, Grimwood, & Morris, 2000), were so-called active processes, in that they required neurons to implement metabolic and morphological changes that are thought to depend on the synthesis of new RNA and proteins. Once these changes were in place, so it was commonly believed, all other memory processing phases were essentially akin to passive readouts of long-term memory (LTM). Although this was the mainstream opinion, there were some who did not agree with this model, pointing to the possibility that phases of plasticity may be present not just at the birth of a new memory (Lewis, 1979; Miller & Marlin, 1984; Spear & Mueller, 1984).

It is somewhat ironic that this once minority opinion has become the new de facto standard within the past 12 years, as described in more detail later. First, largely through the pioneering work of Todd Sacktor, we now know that memory maintenance appears to be maintenance as an active biological mechanism. There may be a continuous battle being played out between the forces of memory erasure versus maintenance (Migues et al., 2010; Pastalkova et al., 2006; Sacktor, 2010, Shema et al., 2011). This body of work has identified the constitutively active protein kinase M zeta (PKMζ), an atypical isoform of protein kinase C, as critical for sustaining many types of LTM (Sacktor, 2008). It has been shown in many tasks and brain regions that transient inactivation of PKMζ results in the loss of established LTM. Work has shown that the persistent action of PKMζ keeps GluA2-containing AMPA receptors (GluA2 AMPARs) at the postsynaptic density (Migues et al., 2010) and that this continuous regulation of GluA2 AMPAR trafficking maintains LTM (AMPARs are a core part of the biological substrate of memory, mediating the vast majority of excitatory neurotransmission in the brain).

Second, retrieval is now firmly established as the opposite of the once envisioned passive readout of memory, and its mechanisms and consequences are the topic of much exciting research, to which the body of work assembled in this book gives testimony. All this work is based on the peculiar phenomenon that a fully consolidated memory, when recalled, can return to an unstable state from which, in order to persist, it has to be restabilized. This process of restabilization, which was first demonstrated by Lewis and Sherman’s group (Misanin, Miller, & Lewis, 1968; Schneider & Sherman, 1968), is now referred to as reconsolidation. Now, for the second time in the history of our field, there is accumulating evidence that this memory process does indeed exist (Alberini, 2011; Dudai, 2012; Hardt, Wang, & Nader, 2009; Lewis, 1979; Miller & Springer, 1973; Nader & Hardt, 2009; Sara, 2000; Spear, 1973): Retrieval can cause the retrieved memory to reconsolidate, and disrupting this process will impair it.

Consolidation theory is a tale of two gradients describing conceptually related phenomena. On the one hand, there is the concept now referred to as synaptic consolidation. For more than 100 years, it has been known that new memories pass through qualitatively distinct phases over time (Ebbinghaus, 1885; Müller & Pilzecker, 1900; Ribot, 1881): Memories are unstable after acquisition and progressively stabilize over time. Müller and Pilzecker suggested that a perseveration–consolidation process mediates this stabilization. This process is now called synaptic consolidation, which is thought to be a ubiquitous property of neurons throughout the brain (Dudai & Morris 2000; Kandel, 2001; Martin et al., 2000). When this process is interrupted before completion, memory will be impaired.

The other time-dependent memory stabilization process was initially described by Theodule-Armand Ribot (1881). Studying patients suffering from amnesia, Ribot reported that patients could not recall recent events but had intact memories from the more remote past (Burnham, 1903; Ribot, 1881). Describing similar cases of retrograde amnesia, Russell and Nathan (1946) commented on the dynamic nature of memory as follows: It seems likely that memory of events is not a static process and the normal activity of the brain must steadily strengthen distant memories so that with the passage of time these become less vulnerable to the effects of brain injury (p. 299).

Another temporal gradient forms the basis for what is called systems consolidation. This notion, proposing that prolonged consolidation reflected memory reorganization over brain systems, began to emerge in studies showing that damage to the medial temporal lobe (MTL) resulted in severe global amnesia, but mostly for recently acquired memories. In a landmark paper, the memory impairments were described for patient HM (the late Henry Molaison), who had most of his MTL removed to relieve intractable epilepsy (Scoville & Milner, 1957). Although Henry Molaison’s intellectual abilities remained intact, the operation left him with a profound impairment in forming new episodic memories (memories of events) and an extensive loss of such memories extending back years before his surgery. He also suffered from anterograde amnesia, the inability to form new memories, which, interestingly, was not global. For instance, he was able to acquire new motor skills, the learning of which he had no conscious recollection. Results from this amnesic patient and others with similar MTL damage suggested that MTL structures, specifically the hippocampus, play a role in episodic, explicit, or declarative memory but not in implicit or nondeclarative memories, such as procedural memories, priming, and conditioned responses. Based on such dissociations provided by many case studies, the presence of a systems consolidation process was proposed in which the hippocampal region served to prime activity in cortical areas, where permanent storage took place (Milner, 1966; Squire, Stark, & Clark, 2004). Thus, the hippocampus was thought to be critical during the early, but not later, life of explicit, or episodic, memories.

It is important to note that the neurobiological mechanisms involved in systems consolidation likely engage synaptic consolidation mechanisms (Frankland & Bontempi, 2005). Therefore, reports of reconsolidation at the synaptic level have implications not just for theories of synaptic consolidation but also for theories of systems consolidation.

All consolidation theories posit that once consolidation is complete, a memory will remain in the consolidated state—that is, fixed and stable. In contrast to this expectation, overwhelming evidence suggests that consolidated memories can be transferred again into a labile state, from which they are restabilized by a reconsolidation process. Retrieval appears to be the key process that transfers memory from the stable to the unstable state. This idea is not new to cognitive psychology, in which memory malleability phenomena such as the misinformation effect and hindsight bias have been prominently studied for quite some time. The concept of memory reconsolidation now offers neurobiologically plausible mechanisms that might explain the molecular, cellular, circuit, and brain system processes that underpin these effects (Hardt, Einarsson, & Nader, 2010; Loftus & Yuille, 1984).

1.1 A brief history

Three lines of evidence support the existence of a stabilization period on the order of hours after the acquisition of new memories. First, performance can be impaired if amnesic treatments such as electroconvulsive shock (Duncan, 1949) or protein synthesis inhibitors (Flexner, Flexner, & Stellar, 1965) are given after learning. Second, performance can be impaired if new competing learning occurs after the initial learning (Gordon & Spear, 1973). Third, retention can be enhanced by administration of various compounds after the initial learning, such as strychnine (McGaugh & Krivanek, 1970). Critically, all three manipulations are effective only when given soon after new learning and not when given after a delay. These findings gave rise to theories of synaptic consolidation (Glickman, 1961; Hebb, 1949; McGaugh, 1966).

The initial unstable trace is called short-term memory, lasting on the order of hours. With time, the trace enters LTM, at which point it is considered to be consolidated and can no longer be affected by treatments such as those mentioned previously. Thus, if a memory is susceptible to enhancement or impairment, it is considered to be in a labile, nonconsolidated state, and if it is insensitive to administration of these amnesic treatments, then the memory is, by definition, consolidated (Dudai, 2004; McGaugh, 1966). Once a memory has become consolidated, it remains in the fixed state.

Consolidation theory became the central tenet around which the field of systems neuroscience of memory has evolved. Since that time, the field has enjoyed numerous successes in creating models at different levels of analysis to describe the changes that occur when a memory is converted from labile trace to a fixed one. These include long-term potentiation (Bliss & Lomo, 1973; Martin et al., 2000) and the identification of transcription factors that act as gateways to LTM (Bourtchuladze et al., 1994; Dash, Hochner, & Kandel, 1990; Kandel, 2001; Yin et al., 1994).

Since its inception, there have been some challenges to consolidation theory. One emerged from a small number of studies demonstrating that a consolidated memory could destabilize and restabilize on the order of minutes to hours when reactivated. Again, there were three lines of evidence to support the existence of a restabilization period. First, performance can be impaired if amnesic treatments such as electroconvulsive shock (Misanin et al., 1968; Schneider & Sherman, 1968) are given after reactivation. Second, performance can be impaired if new competing learning occurs after the reactivation (Gordon, 1977a). Third, retention can be enhanced by administration of various compounds, such as strychnine, after reactivation (Gordon 1977b). Critically, all three manipulations are effective only when given soon after reactivation but not when given after a delay. As had been the case for the consolidation concept, these findings gave rise to a theory to explain them, and new theories of memory were proposed (Lewis, 1979; Miller & Marlin, 1984; Miller & Springer, 1973; Spear & Mueller, 1984).

The implications of these findings, called, among other terms, cue-dependent amnesia, were that LTM was not the end of the road in terms of plasticity. Plasticity was merely momentarily paused when a memory was not used, but it could return when memory was reactivated. According to a model proposed by Lewis (1979), memory was in essence a dynamic process that took two states—the active state and the inactive state. The inactive state comprised dormant memories that were not being used, and in it they were insensitive to disruption. New and reactivated memories were in the active state and, as such, unstable and contained both new and reactivated traces. The model endowed memory with a principal dynamic nature. It could explain both the data on which consolidation theory was founded and the cue-dependent amnesia studies that consolidation theory could not explain. For reasons that remain unclear (Dudai, 2004), in the years following the first reconsolidation documentation in the 1970s, research on the phenomenon was very modestly present as a widely unrecognized small steady undercurrent in the mainstream of research on memory dynamics (Land, Bunsey, & Riccio, 2000; Litvin & Anokhin, 2000; Mactutus, Riccio, & Ferek, 1979; Przybyslawski & Sara, 1997; Quartermain, McEwen, & Azmitia, 1972; Rodriguez, Rodriguez, Phillips, & Martinez, 1993; for a careful review of this literature, see Sara, 2000). In fact, no contemporary textbook on memory consolidation even made note of these earlier studies.

Research on the reconsolidation effect was greatly revitalized by the systematic demonstration of memory reconsolidation in a well-defined behavioral protocol: auditory fear conditioning in the rat (Nader, Schafe, & LeDoux, 2000). Directly targeting the brain circuitry critically mediating the behavior and its consolidation (basolateral nucleus of the amygdala) and using a drug with well-documented amnesic effects on memory consolidation (inhibition of protein synthesis with the antibiotic anisomycin), we showed that reminders could bring well-consolidated fear memories back to an unstable state, in which these reactivated memories could be disrupted by inhibiting protein synthesis in the amygdala. Also, as in the original finding, such impairments were not observed in the absence of reactivation. The conclusion using the definitions of the field of consolidation was that consolidated reactivated memories return to an unstable state from which they must restabilize in order to persist (Nader & Hardt, 2009).

Since publication of this study, reconsolidation has been demonstrated using a range of species, tasks, and amnesic agents (Table 1.1). The modern evidence for the existence of a reconsolidation period is once again based on the same three lines of evidence on which consolidation theory is rooted. First, performance can be impaired if amnesic treatments such as targeted infusions of protein synthesis inhibitors (Litvin & Anokhin, 2000; Milekic & Alberini, 2002; Nader et al., 2000) are given soon after reactivation. Second, performance can be impaired if new competing learning occurs in short temporal proximity to reactivation (Walker, Brakefield, Hobson, & Stickgold, 2003). Third, retention can be enhanced by administration of various compounds, such as activators of signaling pathways important for consolidation, after reactivation of the memory (Tronson, Wiseman, Olausson, & Taylor, 2006).

TABLE 1.1

Examples of Paradigms in which Reconsolidation Has Been Reporteda

aThis table lists examples from various experimental paradigms, treatments, and species for studies reporting evidence for a reconsolidation process since the year 2000.

Source: Modified from Nader and Hardt (2009).

Evidence for reconsolidation does not derive solely from behavioral studies. Specifically, cellular and molecular correlates of reconsolidation have been found. For example, a cellular phenomenon akin to reconsolidation was shown for late long-term potentiation (Fonseca, Nagerl, & Bonhoeffer, 2006). The authors report that reactivation of the consolidated potentiated pathway returned it to an unstable state. If anisomycin was added at this point, then the potentiation was lost (Fonseca et al., 2006; Doyere, Debiec, Monfils, Schafe, & LeDoux, 2007). At the molecular level of analysis, a number of studies have demonstrated that blockade of reconsolidation leads to a reversal of molecular correlates of LTM (Miller & Marshall, 2005; Rose & Rankin, 2006; Valjent, Corbille, Bertran-Gonzalez, Hervé, & Girault, 2006). One elegant study used Caenorhabditis elegans and a nonassociative task (habituation of the tap withdrawal effect) (Rose & Rankin, 2006). One molecular correlate of habituation in this system is a decrease in the number of postsynaptic AMPARs in the mechanosensory neuron mediating tap withdrawal (Rose, Kaun, Chen, & Rankin, 2003). When reconsolidation in this model was blocked by amnesic treatments, the amnesic animals had AMPAR levels comparable to those of naive animals in the mechanosensory neuron. This is striking evidence for the specificity of the impairments. Lastly, based on unpublished results from Lucas Johnson’s lab, it appears that the same cells express a memory after reconsolidation has taken place as the ones that had consolidated it (Bergstrom et al., 2011).

Given the richness of the data on reconsolidation mentioned previously, including the original findings, alternative interpretations are incapable of readily explaining the data set. Among these are nonspecific drug effects such as lesions (Rudy, Biedenkapp, Moineau, & Bolding, 2006), state-dependent learning (Millin, Moody, & Riccio, 2001), new learning (Eisenhardt & Menzel, 2007), facilitated extinction (Myers & Davis, 2002), and retrieval impairment (Cahill, McGaugh, & Weinberger, 2001; Squire, 2006; Vianna, Szapiro, McGaugh, Medina, & Izquierdo, 2001). All of these issues have been explicitly addressed in a review and have been refuted (Nader & Hardt, 2009). Indeed, Nader and Hardt described, and then applied, the traditional standards used to conclude that a consolidation period exists to the reactivation-induced phenomenon. They concluded that the reactivation data set met the standard to be considered a time-dependent stabilization period.

Of course, there remain different perspectives on reconsolidation that have been generating more experiments and more findings (Alberini, 2005; Dudai & Eisenberg, 2004; Lee, 2008; Tronson & Taylor, 2007; Walker & Stickgold, 2006). None of these new insights have challenged the basic fact that via reactivation, consolidated memory may return to an unstable state from which it must restabilize. Reconsolidation has been established as a fundamental memory process. Indeed, it seems that new information employs consolidation mechanisms to be stored. All subsequent modifications to these memories seem to engage reconsolidation mechanisms (Lee, 2008, 2009). Thus, consolidation is the exception, and reconsolidation is the memory process most prominently engaged throughout the lifetime of a memory.

It is a testament to the quality of the science performed by the original discoverers of reconsolidation that so many of the effects described approximately 30–40 years ago have now been rediscovered (Nader & Hardt, 2009). It is heartening that, as shown in Figure 1.1, as a consequence of this revival the classic papers that originally described these effects (Lewis, 1979; Misanin et al., 1968; Schneider & Sherman, 1968) have experienced renewed reception, as their rate of citation has been steadily increasing.

FIGURE 1.1 The number of citations per 4-year period for the two original papers reporting reconsolidation by Misanin et al. (1968) and Schneider et al. (1968). In addition, the rate of citations for Lewis (1970), reported in a conceptual paper in which he formulates a new model of memory processing, is also shown.

The term reconsolidation was introduced to the field as early as 1973 by Spear. Asking how consolidation theory would deal with the dynamic effects reported by Lewis and others, Skip Spear stated, How will the dynamic aspects of memory be handled, that is, with successive learning trials or related successive experiences does the entire memory reconsolidate anew or merely the new information? Since the publication of Nader et al. (2000), approximately 540 papers on the topic of reconsolidation have been published. Consistent with the impressions reported by Serge Laroche and colleagues, those domains are healthy and growing exponentially (Besnard, Caboche, & Laroche, 2012).

The authors of the chapters of this book are main contributors to this great wealth of knowledge and represent many of the leading thinkers in their fields. Many were at the forefront of the exciting debates and scientific discourses that arose after publication of our study in the year 2000. Thanks to Cristina Alberini’s efforts, they are all united in this book, which, I have no doubt, will become one of the historic markers of our field that future generations will revisit to guide their own efforts in understanding more about this peculiar phenomenon of memory.

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