Sleep-dependent Neurophysiological Processes in Implicit Sequence Learning

Abstract

Abstract■ Behavioral studies have cast doubts about the role that posttraining sleep may play in the consolidation of implicit sequence learning. Here, we used event-related fMRI to test the hypothesis that sleep-dependent functional reorganization would take place in the underlying neural circuits even in the possible absence of obvious behavioral changes. Twenty-four healthy human adults were scanned at Day 1 and then at Day 4 during an implicit probabilistic serial RT task. They either slept normally (RS) or were sleep-deprived (SD) on the first posttraining night. Unknown to them, the sequential structure of the material was based on a probabilistic finite-state grammar, with 15% chance on each trial of replacing the rules-based grammatical (G) stimulus with a nongrammatical (NG) one. Results indicated a gradual differentiation across sessions between RTs (faster RTs for G than NG), together with NG-related BOLD responses reflecting sequence learning. Similar behavioral patterns were observed in RS and SD participants at Day 4, indicating time-but not sleep-dependent consolidation of performance. Notwithstanding, we observed at Day 4 in the RS group a diminished differentiation between G-and NG-related neurophysiological responses in a set of cortical and subcortical areas previously identified as being part of the network involved in implicit sequence learning and its offline processing during sleep, indicating a sleep-dependent processing of both regular and deviant stimuli. Our results suggest the sleep-dependent development of distinct neurophysiological processes subtending consolidation of implicit motor sequence learning, even in the absence of overt behavioral differences. ■

Does sleep facilitate the consolidation of allocentric or egocentric representations of implicitly learned visual-motor sequence learning?

“…This may be due in-part to the observed stabilization rather than offline gains in performance. While speculative, our results are consistent with the notion that increased REM is thought to be a state of motor memory stabilization and integration (Maquet et al 2000;Peigneux et al 2003;Urbain et al 2013;Debas et al 2014), even without overt gains in SRTT training skill.…”

“…At present, there is little consensus about whether newly learned implicit motor sequences are enhanced over a period of sleep when compared with wake. Whether a similar dissociation (e.g., spatial versus motor) exists for implicitly learned sequences, is unclear, and could help to resolve existing controversies in the literature concerning whether sleep actively consolidates implicit motor sequence learning (Maquet et al 2000;Peigneux et al 2003;Cohen et al 2005;Destrebecqz et al 2005;Fischer et al 2006;Urbain et al 2013) or not (Keisler et al 2007;Song et al 2007;Nemeth et al 2010Nemeth et al , 2012Hallgató et al 2013;Pan and Rickard 2015). Some of the earlier studies using classic motor learning tasks, such as the serial reaction time task (SRTT) (Nissen and Bullemer 1987), have provided evidence for sleep-dependent memory consolidation of implicit motor learning, in terms of behavioral gains, as well as changes in sleep electrophysiology and brain activation (Cohen et al 2005;Fischer et al 2006;Maquet et al 2000;Peigneux et al 2000Peigneux et al , 2003.…”

The Consolidation of Implicit Sequence Memory in Obstructive Sleep Apnea

“…Previous studies that focused on healthy populations found greater improvement in a procedural sequence learning task after a period of sleep than after an equivalent time of wakefulness [10] , [11] . By contrast, several recent studies failed to find sleep-related improvement in sequence learning [12] – [15] . The controversial results might be explained by task complexity, for example varying in sequence length and structure.…”

The multi-component nature of statistical learning

“…1 It has been suggested that NREM sleep may be important for SL through: (i) restoration of cellular homeostasis after the energy-rich processing of statistical regularities during waking periods, and (ii) consolidation and integration of learning via offline sampling of statistical regularities collected during waking periods [80]. See also [81] for discussion of sleep-dependent brain processes relating to SL. Future studies could use polysomnography to determine whether there is a link between individual differences in NREM sleep, SL and language proficiency in ASD.…”