Schema-conformant memories are preferentially consolidated during REM sleep

Abstract

Please cite this article as: Durrant, S.J., Cairney, S.A., McDermott, C., Lewis, P.A., Schema-Conformant Memories are Preferentially Consolidated During REM Sleep, Neurobiology of Learning and Memory (2015), doi: http:// dx.doi.org/10.1016/j.nlm. 2015.02.011 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. AbstractMemory consolidation is most commonly described by the standard model, which proposes an initial binding role for the hippocampus which diminishes over time as intracortical connections are strengthened. Recent evidence suggests that slow wave sleep (SWS) plays an essential role in this process. Existing animal and human studies have suggested that memories which fit tightly into an existing knowledge framework or schema might use an alternative consolidation route in which the medial prefrontal cortex takes on the binding role. In this study we sought to investigate the role of sleep in this process using a novel melodic memory task. Participants were asked to remember 32 melodies, half of which conformed to a tonal schema present in all enculturated listeners, and half of which did not fit with this schema. After a 24-hour consolidation interval, participants were asked to remember a further 32 melodies, before being given a recognition test in which melodies from both sessions were presented alongside some previously unheard foils. Participants remembered schema-conformant melodies better than non-conformant ones. This was much more strongly the case for consolidated melodies, suggesting that consolidation over a 24-hour period preferentially consolidated schema-conformant items. Overnight sleep was monitored between the sessions, and the extent of the consolidation benefit for schema-conformant items was associated with both the amount of REM sleep obtained and EEG theta power in frontal and central regions during REM sleep. Overall our data suggest that REM sleep plays a crucial role in the rapid consolidation of schemaconformant items. This finding is consistent with previous results from animal studies and the SLIMM model of van Kesteren et al (2012), and suggest that REM sleep, rather than SWS, may be involved in an alternative pathway of consolidation for schema-conformant memories.

The Consolidation and Transformation of Memory

“…The rapid schema-dependent learning was associated with upregulation of immediate-early genes in the medial prefrontal cortex, commonly indicative of ongoing cellular consolidation processes (Tse et al, 2011;and see above). The recently reported preferential consolidation of schema conformant information during sleep in humans, noted above (Durrant et al, 2015), is also in line with the schema assimilation model of systems consolidation.…”

“…Behavioral studies likewise provide a mixed picture. REM sleep seems to benefit particularly memory that is not dependent on cortico-hippocampal circuitry, including procedural skills, object recognition memory, and amygdalamediated cued fear conditioning (Karni et al, 1994;Plihal and Born, 1997;McDevitt et al, 2014;Popa et al, 2010; also see below), as well as stimuli conforming with preexisting schemas (Durrant et al, 2015). These observations could indeed be parsimoniously explained by assuming a stabilization effect mediated via local, synaptic consolidation.…”

“…Hence, one may hypothesize that, instead of external cues, reactivated pre-existing schemas in neocortical sites direct sleep-dependent consolidation, for example, by favoring the hippocampal reactivation of that memory information that fits the pre-existing schema. Schemaguided consolidation has been revealed during wakefulness (see above) but evidence for a similar action of schemas on sleep-dependent consolidation is lacking Durrant et al, 2015).…”

The differential effects of emotional salience on direct associative and relational memory during a nap

“…However, REM sleep is thought to facilitate integration of new information into existing stores (Stickgold, Whidbee, Schirmer, Patel, & Hobson, 2000; but see Tamminen, Payne, Stickgold, Wamsley, & Gaskell, 2010), creative associations (Cai, Mednick, Harrison, Kanady, & Mednick, 2009), problem solving (Walker, Liston, Hobson, & Stickgold, 2002) and other forms of memory transformation, being a state favorable for associative learning (Hasselmo & Bower, 1993;Landmann et al, 2015). Because creating relational associations involves integrating overlapping new and old pairs and extracting their shared relationship, REM sleep could foster the type of intracortical communication needed for this schematic reorganization (Cai et al, 2009;Durrant, Cairney, McDermott, & Lewis, 2015). The current study aimed, in part, to investigate the role of sleep in both negative and neutral direct associative and relational memory formation to provide further evidence and clarify the sleep physiology involved (e.g., SWS or REM sleep).…”

Kreativität und Schlaf

“…Neurobiologisch gelten Gedächtnisschemata als wesentlich durch den ventromedialen Präfrontalkortex vermittelt [97], also einer Hirnstruktur, die sowohl während der Ideengeneration [53] als auch im REM-Schlaf [9] starke Aktivierung aufweist. Es wird weiterhin diskutiert, inwiefern Gedächtnisschema-ta im Schlaf aufgebaut werden [59] und ihre konsolidierungsfördernde Wirkung insbesondere im REM-Schlaf vermitteln [29]. [74].…”