Implicit Learning–Explicit Knowing: A Role for Sleep in Memory System Interaction

Abstract

There is evidence that sleep supports the enhancement of implicit as well as explicit memories (i.e., two memory systems that during learning normally appear to act together). Here, employing a serial reaction time task (SRTT) paradigm, we examined the question whether sleep can provide explicit knowledge on an implicitly acquired skill. At learning, young healthy subjects (n = 20) were first trained on the SRTT. Then, implicit knowledge was assessed on two test blocks, in which grammatically incorrect target positions were occasionally interspersed by the difference in reaction times between grammatically correct and incorrect target positions. To assess explicit sequence knowledge, thereafter subjects performed on a generation task in which they were explicitly instructed to predict the sequential target positions. In half the subjects, learning took place before a 9-hour retention interval filled with nocturnal sleep (sleep group), in the other half, the retention interval covered a 9-hour period of daytime wakefulness (wake group). At subsequent retesting, both testing on the generation task and the SRTT test blocks was repeated. At learning before the retention interval, subjects displayed significant implicit sequence knowledge which was comparable for the sleep and wake groups. Moreover, both groups did not display any explicit sequence knowledge as indicated by a prediction performance not differing from chance on the generation task. However, at retesting, there was a distinct gain in explicit knowledge in the subjects who had slept in the retention interval, whereas generation task performance in the wake group remained at chance level. SRTT performance in the test blocks at retesting did not indicate any further gain in skill (i.e., unchanged reaction time differences between grammatically correct and incorrect target positions) independently of whether subjects had slept or remained awake after learning. Our results indicate a selective enhancement of explicit memory formation during sleep. Because before sleep subjects only had implicit knowledge on the sequence of target transitions, these data point to an interaction between implicit and explicit memory systems during sleep-dependent off-line learning.

Overlapping memory replay during sleep builds cognitive schemata

“…It also builds upon prior suggestions that SWS-based transfer of information might combine with synaptic downscaling to erase memories in which connections have not been sufficiently strengthened by replay [12,30,44]. In sum, although there is ample evidence that abstraction can occur during wake, this process is facilitated by sleep [1][2][3][4][5]. We argue that the unique combination of veridical replay, synaptic downscaling, comparative sensory isolation and favourable neuropharmacology that occurs during SWS could underpin this facilitation.…”

“…It explains why newly learned material becomes increasingly easy to integrate and remember as a conceptual schema takes shape [18,19]. It also explains the observed postsleep enhancements in integration [6][7][8], abstraction [1][2][3][4][5], insight [9] and false memory formation [28].…”

“…In considering this issue we should note that the behavioural studies of integration [6][7][8], abstraction [1][2][3][4][5], insight [9] and false memory formation [28] discussed above all suggest that sleep facilitates the formation of connections between related items. Importantly, performance on these tasks typically improves across both wakefulness and sleep but improvement is greater across the latter.…”

“…Central shared concepts of this type can be thought of as the 'gist' (see Glossary), or essential features, of a set of memories, and taken together can form a cognitive framework of expectations or schema (Box 1). This article proposes a physiological mechanism by which memory replay during sleep could be responsible for the abstraction of gist information from newly encoded memories to form cognitive schemata.Recent research has shown that sleep facilitates abstraction of gist information [1][2][3][4][5] as well as integration across multiple memories [6][7][8], insight into hidden solutions [9], and even the ability to make creative connections between distantly related ideas and concepts [10]. These findings build upon a strong body of work demonstrating that sleep plays a crucial role in memory consolidation (for reviews [11][12][13]), as well as a highly influential model of how memories are re-organised and strengthened by replay during slow wave sleep (SWS) (see [11,12,[14][15][16][17] and Box 2).…”

Sleep in children improves memory performance on declarative but not procedural tasks

“…There is increasing evidence that formation of procedural memories is not achieved as independently from hippocampal function as originally assumed, which holds also for the finger sequence tapping task (S. Corkin, referenced in Diekelmann and . Particularly, at initial stages of skill acquisition and most likely also during consolidation, explicit mechanisms involving hippocampal function interfere with implicit procedural aspects of performance (Jimenez et al 1996;Willingham and Goedert-Eschmann 1999;Wagner et al 2004;Forkstam and Petersson 2005;Fischer et al 2006;Foerde et al 2006). Compared with adults' performance, in our children, finger tapping speed was distinctly slower, and many of the children tended to speak out loud the respective numbers allocated to the bars to be pressed, indicating that they relied strongly on explicit learning strategies involving hippocampal in addition to prefrontal functions.…”