Sleep forms memory for finger skills

Abstract

Practicing a motor skill triggers a process of memory consolidation that continues for hours after practice has ended, and becomes manifest in an improved skill at later testing. We used a sequential motor task (finger-to-thumb opposition task) to show that, in humans, the formation of motor skill memories essentially benefits from sleep. Independent of whether placed during daytime or nighttime, sleep after practice enhanced speed of sequence performance on average by 33.5% and reduced error rate by 30.1% as compared with corresponding intervals of wakefulness. The effect of sleep after learning proved to be stable when retesting was postponed for another night, to exclude effects of sleep loss and to assure that all subjects had sufficient sleep before retrieval testing. Also, the consolidating effect of sleep was specific for the motor sequence learned. It did not generalize to a similar sequence containing identical movement segments in a different order. Retention periods of wakefulness improved performance only moderately and only if placed during daytime. The observations demonstrate a critical role of sleep for storing and optimizing motor skills.

Motor sequence consolidation: constrained by critical time windows or competing components

“…8pm to 8pm) allows only 3.5-hr awake then goal-based improvements develop. Previous studies have shown that similar improvements develop provided sleep occurs within a critical time after initial practice (Fischer et al 2002;Walker et al 2003). Some procedural memories also remain susceptible to interference for a critical time following acquisition (Brashers-Krug et al 1996;Muellbacher et al 2002;Walker et al 2003).…”

Sleep-dependent motor memory plasticity in the human brain

“…Furthermore, these overnight learning gains correlated with the amount of stage two non-rapid eye movement (NREM) sleep, particularly late in the night (Walker et al, 2002). Adding to these findings, it also appears that there is no transfer of sleep-dependent procedural learning to either new motor sequences, or to performance of the same sequence using the opposite hand (Fischer et al, 2002;Korman et al, 2003), suggesting that the influence of sleep is highly specific. But while the behavioral characteristics of sleep-dependent motor learning are increasingly well characterized, the underlying neural basis of these overnight improvements remains unknown.…”

Offline consolidation in implicit sequence learning

“…wakefulness and time of day (Brawn, Fenn, Nusbaum, & Margoliash, 2010;Cajochen et al, 2004;Della-Maggiore, 2005;Doyon et al, 2009;Fischer, Hallschmid, Elsner, & Born, 2002;Keisler, Ashe, & Willingham, 2007;Kuriyama, Stickgold, & Walker, 2004;Manoach et al, 2004;Maquet, Schwartz, Passingham, & Frith, 2003 The purpose of the present study was to investigate the separate contributions of general motor skill learning and sequence-specific memory consolidation in implicit sequence learning. General motor skill learning refers to faster responses as a result of practice.…”

“…wakefulness and time of day (Brawn, Fenn, Nusbaum, & Margoliash, 2010;Cajochen et al, 2004;Della-Maggiore, 2005;Doyon et al, 2009;Fischer, Hallschmid, Elsner, & Born, 2002;Keisler, Ashe, & Willingham, 2007;Kuriyama, Stickgold, & Walker, 2004;Manoach et al, 2004;Maquet, Schwartz, Passingham, & Frith, 2003;Peigneux et al, OFFLINE CONSOLIDATION 4 2003;Spencer, Sunm, & Ivry, 2006), and degree of explicit awareness (Ghilardi et al, 2009;Hotermans, Peigneux, Maertens de Noordhout, Moonen, & Maquet, 2006;Robertson, Pascual-Leone, & Press, 2004). It is not yet clear how sequence learning per se changes from a labile state to a more stable one, although there is a large body of work on motor memory consolidation (see Krakauer & Shadmehr, 2006, for a review).…”

“…In the present study, we use the first definition (i.e., further improvement or enhancement). For related reviews see Doyon et al (2009) Offline consolidation of sequence learning may depend on a variety of factors, such as training session intervals (Albouy et al, 2008;Press, Casement, Pascual-Leone, & Robertson, 2005;, practice (Korman, Raz, Flash, & Karni, 2003;Shanks & Cameron, 2000;Steele & Penhune, 2010), sleep vs.,wakefulness and time of day (Brawn, Fenn, Nusbaum, & Margoliash, 2010;Cajochen et al, 2004;Della-Maggiore, 2005;Doyon et al, 2009;Fischer, Hallschmid, Elsner, & Born, 2002;Keisler, Ashe, & Willingham, 2007;Kuriyama, Stickgold, & Walker, 2004;Manoach et al, 2004;Maquet, Schwartz, Passingham, & Frith, 2003 The purpose of the present study was to investigate the separate contributions of general motor skill learning and sequence-specific memory consolidation in implicit sequence learning. General motor skill learning refers to faster responses as a result of practice.…”