Sleep-dependent learning and motor-skill complexity

Abstract

Learning of a procedural motor-skill task is known to progress through a series of unique memory stages. Performance initially improves during training, and continues to improve, without further rehearsal, across subsequent periods of sleep. Here, we investigate how this delayed sleep-dependent learning is affected when the task characteristics are varied across several degrees of difficulty, and whether this improvement differentially enhances individual transitions of the motor-sequence pattern being learned. We report that subjects show similar overnight improvements in speed whether learning a five-element unimanual sequence (17.7% improvement), a nine-element unimanual sequence (20.2%), or a five-element bimanual sequence (17.5%), but show markedly increased overnight improvement (28.9%) with a nine-element bimanual sequence. In addition, individual transitions within the motor-sequence pattern that appeared most difficult at the end of training showed a significant 17.8% increase in speed overnight, whereas those transitions that were performed most rapidly at the end of training showed only a non-significant 1.4% improvement. Together, these findings suggest that the sleep-dependent learning process selectively provides maximum benefit to motor-skill procedures that proved to be most difficult prior to sleep.

Offline consolidation in implicit sequence learning

“…We reasoned that, as information would be integrated across the left and right brain hemispheres, consolidation of bimanual learning might be enhanced compared to unimanual. Indeed, after an interval of 24 hours, Kuriyama et al (2004) found enhanced consolidation in bimanual compared to unimanual finger-tapping performance, but this was only when the sequence was complex. A number of fMRI studies have shown that bimanual and unimanual tasks recruit somewhat different neural systems in the early stages of motor training, but it is not yet clear if this has any lasting effect on memory consolidation in sequence-specific learning (Bapi, Doya, & Harner, 2000;Gerloff & Andres, 2002;Sun, Miller, Rao, & D'Esposito, 2007).…”

“…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.…”

Sleep-dependent motor memory plasticity in the human brain

“…Demonstrations of overnight, sleep-dependent learning have now been reported across both sensory (Karni et al, 1994;Gais et al, 2000;Stickgold et al, 2000a,b;Fenn et al, 2003;Atienza et al, 2004;Gaab et al, 2004) and motor (Smith and MacNeill, 1994;Fischer et al, 2002;Walker et al, 2002Walker et al, , 2003aKorman et al, 2003;Huber et al, 2004;Robertson et al, 2004;Kuriyama et al, 2004) skill memory domains.…”