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NE35CH11-Dudai ARI 21 May 2012 8:22 The Restless Engram: Consolidations Never End Yadin Dudai Department of Neurobiology, Weizmann Institute of Science, Rehovot 76100, Israel; email: [email protected] Annu. Rev. Neurosci. 2012. 35:227–47 Keywords First published online as a Review in Advance on memory trace, long-term memory, behavioral plasticity, memory March 20, 2012 systems, episodic memory, internal representations The Annual Review of Neuroscience is online at neuro.annualreviews.org Abstract This article’s doi: Memory consolidation is the hypothetical process in which an item 10.1146/annurev-neuro-062111-150500 in memory is transformed into a long-term form. It is commonly ad- Copyright c 2012 by Annual Reviews. by Weizmann Institute of Science on 06/20/12. For personal use only. dressed at two complementary levels of description and analysis: the All rights reserved cellular/synaptic level (synaptic consolidation) and the brain systems 0147-006X/12/0721-0227$20.00 Annu. Rev. Neurosci. 2012.35:227-247. Downloaded from www.annualreviews.org level (systems consolidation). This article focuses on selected recent advances in consolidation research, including the reconsolidation of long-term memory items, the brain mechanisms of transformation of the content and of cue-dependency of memory items over time, as well as the role of rest and sleep in consolidating and shaping memories. Taken together, the picture that emerges is of dynamic engrams that are formed, modified, and remodified over time at the systems level by using synaptic consolidation mechanisms as subroutines. This implies that, contrary to interpretations that have dominated neuroscience for a while, but similar to long-standing cognitive concepts, consolidation of at least some items in long-term memory may never really come to an end. 227 NE35CH11-Dudai ARI 21 May 2012 8:22 over time. The study of memory consolidation Contents provides an intriguing example. Since first pro- posed by Muller & Pilzecker (1900), the term INTRODUCTION.................. 228 consolidation has acquired multiple usages and CONCEPTS AND CRITERIA . 228 meanings. It even budded off new terminology How Is Consolidation Identified? . 229 by acquiring a prefix (reconsolidation). Given RE-CONSOLIDATION, OR the recent impressive advance of research ISIT?............................. 229 on this topic, it seems apt to explore what Boundary Conditions for memory consolidation currently means and Reconsolidation. 230 the implications concerning our understating Reconsolidation as an Opportunity of memory at large. for Memory Enhancement . 231 Imaginative and resourceful as they were, Reconsolidation in the Real Muller and Pilzecker were not the first to iden- World.......................... 231 tify consolidation. Roman orators already knew Are Consolidation and about it (Quintillian 1C AD/1921). Though not Reconsolidation the Same? . 232 yet so termed, consolidation entered the clini- THE ENGRAM TRANSFORMED . 232 cal discourse as a consequence of observations The Standard Model of Systems of amnesic patients (Ribot 1882). This and ad- Consolidation . 233 ditional findings that preceded and coincided The Multiple-Trace and the with the studies by Muller and Pilzecker are Trace-Transformation not reiterated here (Dudai 2004). Many im- Models......................... 233 pressive advances in molecular, cellular, and The Schema Assimilation Model. 234 systems neuroscience that relate to memory WORKINGATREST............... 234 mechanisms are also not discussed. Instead, the A Reminder Concerning Sleep. 235 present discussion focuses on selected recent Which Memory Systems Benefit developments that have changed our view on from Consolidation in Sleep? . 235 how memories become long-term and on their Which Properties of Memory subsequent fate. Increase the Benefit from Consolidation in Sleep? . 235 WhenandHowinSleep........... 236 CONCEPTS AND CRITERIA HowItMightWork............... 238 Memory consolidation is the hypothetical CONSOLIDATIONS process in which a memory item is transformed INTEGRATED................... 239 by Weizmann Institute of Science on 06/20/12. For personal use only. into a long-term form. It is commonly ad- ON THE RECONSOLIDATION OF dressed at two levels of description and analysis: TERMSANDIDEAS............. 241 Annu. Rev. Neurosci. 2012.35:227-247. Downloaded from www.annualreviews.org the cellular/synaptic level and the brain systems level. Synaptic consolidation refers to the post- encoding transformation of information into a long-term form at local nodes in the neural INTRODUCTION circuit that encodes the memory. The current Those who consider In principio erat verbum (“in central dogma of synaptic consolidation is Memory consolidation: the beginning there was the word”) as a biblical that it involves stimulus (“teacher”)-induced hypothetical process in aphorism only, philosophical connotations activation of intracellular signaling cascades, which a memory item notwithstanding, may be gratified to discover resulting in posttranslational modifications, is transformed into a that it applies to scientific research as well. modulation of gene expression, and synthesis long-term or remote Occasionally, scientific practice is shaped by of gene products that alter synaptic efficacy. form terms whose original meaning has mutated Synaptic consolidation is traditionally assumed 228 Dudai NE35CH11-Dudai ARI 21 May 2012 8:22 to draw to a close within hours of its initiation. engram (Bartlett 1932), but proponents of The stimulus that triggers it in the local node the consolidation hypothesis drew a distinc- may represent perceptually or internally driven tion between the postulated immutability of Synaptic information. Synaptic consolidation is found consolidated memory items and the dynamic consolidation: throughout the animal kingdom. nature of behavior (McGaugh 1966). The hypothetical process in Systems consolidation refers to the posten- view that consolidation occurs just once per which information is coding reorganization of long-term memory item was, however, challenged by the late transformed into a (LTM) over distributed brain circuits. The 1960s. Researchers reported that presentation long-term form at local nodes in the process may last days to years, depending of a reminder cue (RC) rendered a seemingly neural circuits that on the memory system, task, and author. consolidated memory item labile to amnesic encode the memory The conventional taxonomy of LTM systems agents (Misanin et al. 1968). The prototypical Systems (Squire 2004) distinguishes between declarative experimental protocol goes like this: Training consolidation: memory, which is memory for facts (semantic) is followed by time to complete the postulated hypothetical process in or events (episodic) that requires conscious consolidation period. An RC, usually the which an experience- awareness for retrieval, and nondeclarative conditioned stimulus (CS), is then presented dependent internal representation is memory, a collection of memory faculties to reactivate the memory. An amnesic agent converted into a that do not require conscious awareness for is administered simultaneously or immediately long-term form and retrieval. Systems consolidation commonly afterward. LTM is then retested. Under these reorganized over refers to declarative memory, but may exist in conditions, LTM may be blocked. No such distributed brain nondeclarative memory as well. effect is detected if retrieval is not followed circuits “Reconsolidation” refers to a consolida- by the amnesic agent or the amnesic agent is Reconsolidation: tion process that is initiated by reactivation of not preceded by retrieval. This reactivation- postulated consolidation process LTM. The process is assumed to transiently induced reopening of a consolidation-like initiated by destabilize LTM. window challenged the unidirectional mem- reactivation of a long- ory maturation view (Spear 1973) and was term memory item in termed reconsolidation (Rodriguez et al. 1993, the system that already How Is Consolidation Identified? Przybyslawski & Sara 1997). stores this item Although certain changes detected in the brain Reservations concerning interpretations Long-term memory may reflect consolidation, none can so far be as well as paradigmatic drives diverted the (LTM): item lasting long after it is used as a definitive signature of consolidation. exploration of reconsolidation away from encoded; in behavioral Currently, the only accepted criterion to infer mainstream memory research. Although a neuroscience, “long” is consolidation is the existence of a time window few groups pursued the topic (reviewed in conventionally of susceptibility to amnesic agents. An amnesic Sara 2000), the notion lost favor, as reflected, considered more than one day by Weizmann Institute of Science on 06/20/12. For personal use only. agent that does not exhibit time-dependent de- for example, in the number of publications: crease in efficacy is assumed to affect main- Of the 27,061 papers relating to “memory” Declarative memory: requires conscious Annu. Rev. Neurosci. 2012.35:227-247. Downloaded from www.annualreviews.org tenance or expression of memory rather than published in the psychobiology literature awareness for retrieval, consolidation (Shema et al. 2007). from 1993 to 1999, only 6 referred to “re- usually classified into consolidation” (Thomson Reuters Science Web of memory for facts Knowledge). The notion of reconsolidation was (semantic) and RE-CONSOLIDATION, OR IS IT? ultimately revitalized
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