Effects of Memory Consolidation on Human Hippocampal Activity During Retrieval

Bosshardt, Simone; Schmidt, Conny F.; Jaermann, T.; Degonda, Nadia; Boesiger, Peter; Nitsch, Roger M.; Höck, Christoph; Henke, Katharina

doi:10.1016/s0010-9452(08)70189-8

Cited by 31 publications

(32 citation statements)

References 55 publications

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“…The present data suggest that reactivation following this initial period of consolidation, as compared to more immediate reactivation, renders these memories more resistant to forgetting. Consistent with our behavioral data, some initial studies of human memory consolidation using brain imaging report increased activation of the hippocampus following a 24 hr retention interval as compared to intervals of less than an hour (Bosshardt et al 2005;Litman and Davachi 2007; but see Stark and Squire 2000;Takashima et al 2006;). Our data complement these imaging findings in revealing the behavioral consequences of consolidation, namely a reduced forgetting of relational information.…”

Section: Discussionsupporting

confidence: 87%

Distributed learning enhances relational memory consolidation

Litman

Davachi²

2008

Learn. Mem.

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It has long been known that distributed learning (DL) provides a mnemonic advantage over massed learning (ML). However, the underlying mechanisms that drive this robust mnemonic effect remain largely unknown. In two experiments, we show that DL across a 24 hr interval does not enhance immediate memory performance but instead slows the rate of forgetting relative to ML. Furthermore, we demonstrate that this savings in forgetting is specific to relational, but not item, memory. In the context of extant theories and knowledge of memory consolidation, these results suggest that an important mechanism underlying the mnemonic benefit of DL is enhanced memory consolidation. We speculate that synaptic strengthening mechanisms supporting long-term memory consolidation may be differentially mediated by the spacing of memory reactivation. These findings have broad implications for the scientific study of episodic memory consolidation and, more generally, for educational curriculum development and policy.Over 100 years ago Jost put forth what is now known as his first law: "If two memory traces are of equal strength but different ages, the older one will benefit more from an additional learning trial." This general phenomenon, also known as the distributed learning effect (DL), refers to the finding that memory for items encoded over repeated sessions is better when those sessions are distributed across time rather than massed (ML). While hundreds of studies have now confirmed that DL provides a mnemonic advantage over ML (see Dempster 1988;Janiszewski et al. 2003;Cepeda et al. 2006 for reviews), the cognitive and neural mechanisms behind this effect remain unclear.In this paper we present evidence supporting a consolidation theory account of DL. Consolidation is a neurobiological process involved in long-term stabilization of mnemonic representations, causing memories to strengthen and become less prone to forgetting and interference over time (e.g., Squire and Alvarez 1998;Dudai 2004;Wixted 2004). Historically, the field of psychology has been resistant to embracing consolidation as an explanation for DL memory enhancement. For example, in an influential symposium that captured the zeitgeist, Melton (1970) commented that "I find it comforting that no one in the symposium appealed to consolidation as an explanation of the observed distributed practice effects, but all sought instead to find understanding from hypotheses about the informationprocessing activities of the subject."Instead of proposing neural mechanisms, researchers have favored accounts of DL effects in terms of cognitive factors, such as fatigue and encoding variability (Youtz 1941;Melton 1970;Hintzman 1974). Importantly, however, these theories have been derived from a DL literature that has primarily used very short intersession intervals (ISIs) ranging only from seconds to minutes (Underwood 1961;Melton 1970;Hintzman 1974) that are not likely to be affected by consolidation processes. For example, protein synthesis takes place over many hours (Tully et al...

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Section: Discussionsupporting

confidence: 87%

Distributed learning enhances relational memory consolidation

Litman

Davachi²

2008

Learn. Mem.

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“…Consistent with an increase in the number of GABA-producing neurons, when action potential firing was blocked with tetrodotoxin, miniature IPSC frequencies were also increased in neocortical and hippocampal pyramidal cells 4 weeks after transplantation (cortex, 2.3 Ϯ 0.1 Hz, n ϭ 4; CA1, 2.4 Ϯ 0.2 Hz, n ϭ 3) when compared with controls (cortex, 1.3 Ϯ 0.2 Hz, n ϭ 4; CA1, 1.1 Ϯ 0.1 Hz, n ϭ 3; p Ͻ 0.05). These data demonstrate the potential for MGEderived precursors to modify circuit function in brain regions critical to cognition Amodio and Frith, 2006), epileptogenesis (Prince and Connors, 1984;Prince, 1985), and memory consolidation (Bosshardt et al, 2005). …”

Section: Transplanted Mge Cells Influence Synaptic Function In the Homentioning

confidence: 74%

Cortical Inhibition Modified by Embryonic Neural Precursors Grafted into the Postnatal Brain

et al. 2006

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“…A 3-day interval between sessions might be too short to demonstrate such a transfer effect. Indeed, several previous studies failed to show a diminution of hippocampal involvement in a recognition memory task performed immediately, 1 day or 1 week after learning (44), or even found enhanced retrieval-related hippocampal activity after a consolidation period ranging from 10 min to 1 month (45,46). However, a recent study revealed a progressive disengagement of the hippocampus during declarative memory retrieval over a time course ranging from a few hours to 3 months (25).…”

Section: Discussionmentioning

confidence: 96%

Sleep after spatial learning promotes covert reorganization of brain activity

Orban

Rauchs

Balteau

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

154

130

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Sleep promotes the integration of recently acquired spatial memories into cerebral networks for the long term. In this study, we examined how sleep deprivation hinders this consolidation process. Using functional MRI, we mapped regional cerebral activity during place-finding navigation in a virtual town, immediately after learning and 3 days later, in subjects either allowed regular sleep (RS) or totally sleep-deprived (TSD) on the first posttraining night. At immediate and delayed retrieval, place-finding navigation elicited increased brain activity in an extended hippocamponeocortical network in both RS and TSD subjects. Behavioral performance was equivalent between groups. However, striatal navigation-related activity increased more at delayed retrieval in RS than in TSD subjects. Furthermore, correlations between striatal response and behavioral performance, as well as functional connectivity between the striatum and the hippocampus, were modulated by posttraining sleep. These data suggest that brain activity is restructured during sleep in such a way that navigation in the virtual environment, initially related to a hippocampus-dependent spatial strategy, becomes progressively contingent in part on a response-based strategy mediated by the striatum. Both neural strategies eventually relate to equivalent performance levels, indicating that covert reorganization of brain patterns underlying navigation after sleep is not necessarily accompanied by overt changes in behavior.functional MRI ͉ hippocampus ͉ sleep deprivation ͉ memory consolidation ͉ striatum T he hypothesis that sleep represents a crucial, albeit not always indispensable, neurophysiological state that actively promotes learning-dependent brain plasticity (1-5) has become a main topic of interest in neuroscience. In this view, an active processing of freshly acquired memories may occur in the sleeping brain, supporting the gradual consolidation process by which labile recent memories are restructured and incorporated into stable memories for the long term (6, 7).Memories that can be consciously and symbolically expressed belong to the declarative memory system. At the neuroanatomical level, their encoding and initial maintenance rely upon the integrity of the medial temporal lobe, with the hippocampus at its core (8, 9). Episodic memory for personally experienced events set in a spatiotemporal context is defined as a subclass of declarative memory (10). Animal (11) and human (12) studies suggest that the hippocampus is involved in spatial learning, because encoding is based on a flexible knowledge of relationships between environmental cues. Hippocampus-dependent spatial memory in animals is thus phylogenetically viewed as a homologue of human episodic͞ declarative memory (13,14). However, spatial navigation in a well learned environment may also be mediated by the striatum through the expression of stimulus-response associations (15, 16). Current research further suggests that rodents (17, 18) and humans (19) tend to initially use a hippocampus-de...

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Effects of Memory Consolidation on Human Hippocampal Activity During Retrieval

Cited by 31 publications

References 55 publications

Distributed learning enhances relational memory consolidation

Distributed learning enhances relational memory consolidation

Cortical Inhibition Modified by Embryonic Neural Precursors Grafted into the Postnatal Brain

Sleep after spatial learning promotes covert reorganization of brain activity

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