Although studies in animals and patients have demonstrated that brain oscillations play a role in declarative memory encoding and retrieval, little has been done to investigate the temporal dynamics and sources of brain activity in healthy human subjects performing such tasks. In a magnetoencephalography study using pictorial stimuli, we have now identified oscillatory activity in the gamma (60 -90 Hz) and theta (4.5-8.5 Hz) band during declarative memory operations in healthy participants. Both theta and gamma activity was stronger for the later remembered compared with the later forgotten items (the "subsequent memory effect"). In the retrieval session, theta and gamma activity was stronger for recognized items compared with correctly rejected new items (the "old/new effect"). The gamma activity was also stronger for recognized compared with forgotten old items (the "recognition effect"). The effects in the theta band were observed over right parietotemporal areas, whereas the sources of the effects in the gamma band were identified in Brodmann area 18/19. We propose that the theta activity is directly engaged in mnemonic operations. The increase in neuronal synchronization in the gamma band in occipital areas may result in a stronger drive to subsequent areas, thus facilitating both memory encoding and retrieval. Alternatively, the gamma synchronization might reflect representations being reinforced by top-down activity from higherlevel memory areas. Our results provide additional insight on human declarative memory operations and oscillatory brain activity that complements previous electrophysiological and brain imaging studies.
Retrieval of recently acquired declarative memories depends on the hippocampus, but with time, retrieval is increasingly sustainable by neocortical representations alone. This process has been conceptualized as system-level consolidation. Using functional magnetic resonance imaging, we assessed over the course of three months how consolidation affects the neural correlates of memory retrieval. The duration of slow-wave sleep during a nap͞rest period after the initial study session and before the first scan session on day 1 correlated positively with recognition memory performance for items studied before the nap and negatively with hippocampal activity associated with correct confident recognition. Over the course of the entire study, hippocampal activity for correct confident recognition continued to decrease, whereas activity in a ventral medial prefrontal region increased. These findings, together with data obtained in rodents, may prompt a revision of classical consolidation theory, incorporating a transfer of putative linking nodes from hippocampal to prelimbic prefrontal areas.hippocampus ͉ retrograde amnesia ͉ sleep ͉ ventral medial prefrontal cortex ͉ recognition W e are able to recall memories from the remote past, suggesting a high-capacity system for long-term storage of declarative memories. Lesion studies suggest that declarative memory retrieval initially depends on the hippocampus, although, with time, stored information becomes reorganized in a way that makes retrieval gradually less dependent on the hippocampus (1-3). This pattern of findings has been conceptualized as system-level consolidation, a mnemonic process that leads to a shift from the hippocampus toward distributed neocortical traces (4-8). Although memory consolidation is a fundamental mnemonic operation, its neural correlates at the human brain-system level are not well understood. In particular, it is unknown whether the hippocampus participates under normal circumstances in remote memory retrieval or whether other brain regions take over putative linking nodes created initially in the hippocampus where they are used for recent memory retrieval.Sleep, in particular slow-wave sleep, appears to play a role in declarative memory consolidation in humans (9-15; but see ref.16). Moreover, animal studies have shown that during sleep, hippocampal and neocortical cell-assemblies reflecting recent events exhibit spontaneous coordinated reactivation (17)(18)(19)(20), that, thereby, may strengthen and͞or refine neocortical assemblies so that they can be used for retrieval without hippocampal engagement.The time course of declarative memory consolidation in humans is poorly defined. Estimates reach up to several decades, based on retrospective lesion and functional neuroimaging studies (1, 21). When investigated on a shorter time scale, prospective studies in rodents and nonhuman primates have revealed upperbound estimates of a few weeks (22-25); however, it remains to be determined whether these findings are related to a similar set of process...
Information that is congruent with prior knowledge is generally remembered better than incongruent information. This effect of congruency on memory has been attributed to a facilitatory influence of activated schemas on memory encoding and consolidation processes, and hypothesised to reflect a shift between processing in medial temporal lobes (MTL) towards processing in medial prefrontal cortex (mPFC). To investigate this shift, we used functional magnetic resonance imaging (fMRI) to compare brain activity during paired-associate encoding across three levels of subjective congruency of the association with prior knowledge. Participants indicated how congruent they found an object-scene pair during scanning, and were tested on item and associative recognition memory for these associations one day later. Behaviourally, we found a monotonic increase in memory performance with increasing congruency for both item and associative memory. Moreover, as hypothesised, encoding-related activity in mPFC increased linearly with increasing congruency, whereas MTL showed the opposite pattern of increasing encoding-related activity with decreasing congruency. Additionally, mPFC showed increased functional connectivity with a region in the ventral visual stream, presumably related to the binding of visual representations. These results support predictions made by a recent neuroscientific framework concerning the effects of schema on memory. Specifically, our findings show that enhanced memory for more congruent information is mediated by the mPFC, which is hypothesised to guide integration of new information into a pre-existing schema represented in cortical areas, while memory for more incongruent information relies instead on automatic encoding of arbitrary associations by the MTL.
The standard model of system-level consolidation posits that the hippocampus is part of a retrieval network for recent memories. According to this theory, the memories are gradually transferred to neocortical circuits with consolidation, where the connections within this circuit grow stronger and reorganized so that redundant and/or contextual details may be lost. Thus, remote memories are based on neocortical networks and can be retrieved independently of the hippocampus. To test this model, we measured regional brain activity and connectivity during retrieval with functional magnetic resonance imaging. Subjects were trained on two sets of face-location association and were tested with two different delays, 15 min and 24 h including a whole night of sleep. We hypothesized that memory traces of the locations associated with specific faces will be linked through the hippocampus for the retrieval of recently learned association, but with consolidation, the activity and the functional connectivity between the neocortical areas will increase. We show that posterior hippocampal activity related to high-confidence retrieval decreased and neocortical activity increased with consolidation. Moreover, the connectivity between the hippocampus and the neocortical regions decreased and in turn, cortico-cortical connectivity between the representational areas increased. The results provide mechanistic support for a two-level process of the declarative memory system, involving initial representation of new associations in a network including the hippocampus and subsequent consolidation into a predominantly neocortical network.
"System-level memory consolidation theory" posits that the hippocampus an initially links the neocortical representations, followed by a shift to a hippocampus-independent neocortical network. With consolidation, an increase in activity in the human subgenual ventromedial prefrontal cortex (vmPFC) has repeatedly been shown. Previously we and others have proposed that this area might link the neocortical representational areas in remote memory, similarly as has been proposed for the rodent anterior cingulate cortex (ACC). Here, we review literature involving the human vmPFC to investigate if the results in other cognitive domains are in line with this proposal. We have taken into account reports on patients with lesions in this area, findings in reward and valuation, fear extinction, and confabulation studies, and integrated these with findings in consolidation studies. We conclude: Firstly, it is unlikely that the rodent ACC is homolog to the human subgenual vmPFC. It is more likely that the rodent infralimbic cortex is, as proposed in the fear extinction literature. Secondly, we propose that the function of the subgenual vmPFC is to integrate information which is represented in separate parts of the limbic system (the hippocampus, the amygdala, and the ventral striatum) and that the integrated representation in the subgenual vmPFC might subsequently be used to suppress irrelevant representations in the limbic system. With the progression of time, the importance of the integrated representation in the subgenual vmPFC increases, because it may replace some direct connectivity across the limbic areas which decays with time.
a b s t r a c tNovel words can be recalled immediately and after little exposure, but require a post-learning consolidation period to show word-like behaviour such as lexical competition. This pattern is thought to reflect a qualitative shift from episodic to lexical representations. However, several studies have reported immediate effects of meaningful novel words on semantic processing, suggesting that integration of novel word meanings may not require consolidation. The current study synthesises and extends these findings by showing a dissociation between lexical and semantic effects on the electrophysiological (N400, LPC) response to novel words. The difference in N400 amplitude between novel and existing words (a lexical effect) decreased significantly after a 24-h consolidation period, providing novel support for the hypothesis that offline consolidation aids lexicalisation. In contrast, novel words preceded by semantically related primes elicited a more positive LPC response (a semantic-priming effect) both before and after consolidation, indicating that certain semantic effects can be observed even when words have not been fully lexicalised. We propose that novel meanings immediately start to contribute to semantic processing, but that the underlying neural processes may shift from strategic to more automatic with consolidation.
During a post-encoding delay period, the ongoing consolidation of recently acquired memories can suffer interference if the delay period involves encoding of new memories, or sensory stimulation tasks. Interestingly, two recent independent studies suggest that (i) autobiographical thinking also interferes markedly with ongoing consolidation of recently learned wordlist material, while (ii) a 2-Back task might not interfere with ongoing consolidation, possibly due to the suppression of autobiographical thinking. In this study, we directly compare these conditions against a quiet wakeful rest baseline to test whether the promotion (via familiar sound-cues) or suppression (via a 2-Back task) of autobiographical thinking during the post-encoding delay period can affect consolidation of studied wordlists in a negative or a positive way, respectively. Our results successfully replicate previous studies and show a significant interference effect (as compared to the rest condition) when learning is followed by familiar sound-cues that promote autobiographical thinking, whereas no interference effect is observed when learning is followed by the 2-Back task. Results from a post-experimental experience-sampling questionnaire further show significant differences in the degree of autobiographical thinking reported during the three post-encoding periods: highest in the presence of sound-cues and lowest during the 2-Back task. In conclusion, our results suggest that varying levels of autobiographical thought during the post-encoding period may modulate episodic memory consolidation.
The last decade has brought forth convincing evidence for a role of sleep in non-declarative memory. A similar function of sleep in episodic memory is supported by various correlational studies, but direct evidence is limited. Here we show that cued recall of face-location associations is significantly higher following a 12-h retention interval containing sleep than following an equally long period of waking. Furthermore, retention is significantly higher over a 24-h sleep-wake interval than over an equally long wake-sleep interval. This difference occurs because retention during sleep was significantly better when sleep followed learning directly, rather than after a day of waking. These data demonstrate a beneficial effect of sleep on memory that cannot be explained solely as a consequence of reduced interference. Rather, our findings suggest a competitive consolidation process, in which the fate of a memory depends, at least in part, on its relative stability at sleep onset: Strong memories tend to be preserved, while weaker memories erode still further. An important aspect of memory consolidation may thus result from the removal of irrelevant memory "debris."In recent years, compelling evidence has been found to support a role of sleep in the consolidation of non-declarative memory (Stickgold et al. 2000;Walker et al. 2002;Fenn et al. 2003;Wagner et al. 2004). A coherent body of theoretical (Crick and Mitchison 1983; Alvarez and Squire 1994;McClelland et al. 1995;Meeter and Murre 2005) and physiological (Wilson and McNaughton 1994;Buzsaki 1996;Izquierdo et al. 1997) evidence suggests that sleep might also have an important role in consolidation of hippocampus-dependent episodic memories. According to these studies, sleep may be used to recode these memories from a highly plastic store, the hippocampus, to a more stable one with larger capacity, involving the neocortex. Such recoding would protect memories from fast degradation through interference and passive forms of decay.While a significant body of work indirectly supports the above notion (e.g., Peigneux et al. 2004;Schmidt et al. 2006;Takashima et al. 2006; for review, see Stickgold 2005), direct evidence for a causal role of sleep in episodic memory consolidation is scarce. Indeed, many studies that tapped directly into the effect of sleep are confounded by unspecific effects of sleep deprivation and circadian effects on memory performance. Moreover, beneficial effects of sleep on episodic memory have been attributed, by some, to a lack of interference during sleep, rather than to active consolidation (Wixted 2004).One possible way to control for the time of day effect is to make use of a daytime nap. A recent study based on this approach demonstrated sleep-related declarative memory benefits (Tucker et al. 2006). When using this approach, however, the difference in amount of sleep and interference between the nap and the control group might still introduce a confound. A few other recent studies have shown beneficial effects on memory of a full night's...
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