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Memory Consolidation Memory Consolidation Larry R. Squire1,2,3, Lisa Genzel4, John T. Wixted3, and Richard G. Morris4 1VA San Diego Healthcare System, San Diego, California 92161 2Departments of Psychiatry and Neurosciences, University of California, San Diego, La Jolla, California 92093 3Department of Psychology, University of California, San Diego, La Jolla, California 92093 4Centre for Cognitive and Neural Systems, The University of Edinburgh, Edinburgh EH8 9JZ, United Kingdom Correspondence: [email protected] Conscious memory for a new experience is initially dependent on information stored in both the hippocampus and neocortex. Systems consolidation is the process by which the hippo- campus guides the reorganization of the information stored in the neocortex such that it eventually becomes independent of the hippocampus. Early evidence for systems consoli- dation was provided by studies of retrograde amnesia, which found that damage to the hippocampus-impaired memories formed in the recent past, but typically spared memories formed in the more remote past. Systems consolidation has been found to occur for both episodic and semantic memories and for both spatial and nonspatial memories, although empirical inconsistencies and theoretical disagreements remain about these issues. Recent work has begun to characterize the neural mechanisms that underlie the dialogue between the hippocampus and neocortex (e.g., “neural replay,” which occurs during sharp wave ripple activity). New work has also identified variables, such as the amount of preexisting knowledge, that affect the rate of consolidation. The increasing use of molecular genetic tools (e.g., optogenetics) can be expected to further improve understanding of the neural mech- anisms underlying consolidation. emory consolidation refers to the process Ribot (1881). The key observation was that re- Mby which a temporary, labile memory is cent memories are more vulnerable to injury or transformed into a more stable, long-lasting disease than remote memories, and the signifi- form. Memory consolidation was first proposed cance of this finding for consolidation was im- in 1900 (Mu¨ller and Pilzecker 1900; Lechner mediately appreciated. et al. 1999) to account for the phenomenon of retroactive interference in humans, that is, the In normal memory a process of organization is finding that learned material remains vulnera- continually going on—a physical process of or- ganization and a psychological process of repe- ble to interference for a period of time after tition and association. In order that ideas may learning. Support for consolidation was already become a part of permanent memory, time must available in the facts of retrograde amnesia, es- elapse for these processes of organization to be pecially as outlined in the earlier writings of completed. (Burnham 1903, p. 132) Editors: Eric R. Kandel, Yadin Dudai, and Mark R. Mayford Additional Perspectives on Learning and Memory available at www.cshperspectives.org Copyright # 2015 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a021766 Cite this article as Cold Spring Harb Perspect Biol 2015;7:a021766 1 L.R. Squire et al. It is useful to note that the term consolidation hippocampal system. This information directs has different contemporary usages that derive the training of a “slow learning” neocortex, from the same historical sources. For example, whereby the hippocampus gradually guides the term is commonly used to describe events at the development of connections between the the synaptic/cellular level (e.g., protein synthe- multiple cortical regions that are active at the sis), which stabilize synaptic plasticity within time of learning and that represent the memory. hours after learning. In contrast, systems con- Training of the neocortex by the hippocampus solidation, which is the primary focus of this (termed “interleaved” training) allows new in- review, refers to gradual reorganization of the formation to be assimilated into neocortical brain systems that support memory, a process networks with a minimum of interference. In that occurs within long-term memory itself simulations (McClelland et al. 1995), rapid (Squire and Alvarez 1995; Dudai and Morris learning of new information, which was incon- 2000; Dudai 2012). sistent with prior knowledge, was shown to Systems consolidation is typically, and accu- cause interference and disrupt previously estab- rately, described as the process by which mem- lished representations (“catastrophic interfer- ories, initially dependent on the hippocampus, ence”). The gradual incorporation of informa- are reorganized as time passes. By this process, tion into the neocortex during consolidation the hippocampus gradually becomes less im- avoids this problem. In a recent revision of this portant for storage and retrieval, and a more framework (McClelland 2013), neocortical permanent memory develops in distributed re- learning is characterized, not so much as fast gions of the neocortex. The idea is not that or slow, but as dependent on prior knowledge. memory is literally transferred from the hippo- If the information to be learned is consistent campus to the neocortex, for information is en- with prior knowledge, neocortical learning can coded in the neocortex as well as in hippocam- be more rapid. pus at the time of learning. The idea is that This review considers several types of evi- gradual changes in the neocortex, beginning at dence that illuminate the nature of the consol- the time of learning, establish stable long-term idation process: studies of retrograde amnesia in memory by increasing the complexity, distribu- memory-impaired patients, studies of healthy tion, and connectivity among multiple cortical volunteers with neuroimaging, studies of sleep regions. Recent findings have enriched this per- and memory, studies of experimental animals, spective by emphasizing the dynamic nature of both with lesions or other interventions, and long-term memory (Dudai and Morris 2013). studies that track neural activity as time passes Memory is reconstructive and vulnerable to after learning. error, as in false remembering (Schacter and Dodson 2001). Also, under some conditions, STUDIES OF RETROGRADE AMNESIA long-term memory can transiently return to a IN MEMORY-IMPAIRED PATIENTS labile state (and then gradually stabilize), a phe- nomenon termed reconsolidation (Nader et al. One useful source of information about mem- 2000; Sara 2000; Alberini 2005). In addition, the ory consolidation comes from studies in mem- rate of consolidation can be influenced by the ory-impaired patients of memory for past news amount of prior knowledge that is available events or other public facts. In an early study about the material to be learned (Tse et al. of memory for television programs that had 2007; van Kesteren et al. 2012). broadcast for only a single season, patients re- Neurocomputational models of consolida- ceiving electroconvulsive therapy for depressive tion (McClelland et al. 1995; McClelland 2013) illness showed temporally limited retrograde describe how the acquisition of new knowledge amnesia extending back 1–3 years (Squire might proceed and suggest a purpose for con- et al. 1975). This phenomenon was slow to be solidation. As originally described, elements of related to neuroanatomy because of the need to information are first stored in a fast-learning test patients with well-characterized lesions who 2 Cite this article as Cold Spring Harb Perspect Biol 2015;7:a021766 Memory Consolidation developed a memory impairment at a known from studies of autobiographical memory are time. In one of the first studies to meet these mixed. In several studies, patients with restrict- requirements, six memory-impaired patients ed hippocampal lesions, or larger medial tem- with bilateral damage limited to the hippocam- poral lobe lesions, successfully recalled detailed pus were given a test of 250 news events cover- memories from early life (Eslinger 1998; Bayley ing 50 years (Manns et al. 2003). The patients et al. 2003; Buchanan et al. 2005; Kirwan et al. showed a similar graded memory loss extending 2008; Kopelman and Bright 2012). Squire and just a few years into the premorbid period (for Bayley (2007) offer additional discussion of sin- two additional patients, see Kapur and Brooks gle-case reports. Whether assessed by counting 1999). Similar results have been obtained in the details in tape-recorded narratives, rating neuroimaging studies of hippocampal activity, the quality of narratives, or scoring responses for example, when volunteers recalled past news to a few standardized questions (on a 0–9 events that had occurred 1–30 years ago (Smith scale), patients performed like controls (Fig. and Squire 2009). These results suggest a con- 1). Recall of episodes from the recent past was solidation process whereby the human hippo- impaired (see also Thaiss and Petrides 2008). campus can be needed to support memory for Yet, other patients produced fewer details about factual information (semantic memory) for as past events, even events from early life (Rosen- long as a few years after learning, but is not baum et al. 2005; Steinvorth et al. 2005; Race needed after that time. et al. 2011). Patients with damage that not only includes Why are the findings mixed? A lingering and the hippocampus but larger regions of the me- challenging issue concerns the locus and extent dial temporal (and sometimes lateral temporal) of brain damage and the possibility that damage lobes as well can have severe retrograde
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