Multiple shifts in the representation of a motor sequence during the acquisition of skilled performance

Abstract

Several lines of evidence support the notion that the brain exhibits a significant degree of experience-dependent functional plasticity even in adulthood (1-10). This plasticity may underlie the acquisition and long-term retention of skills (procedural memory) (11-13). There is growing evidence, however, indicating that different brain areas are involved in the initial, compared with subsequent, phases of learning after practice in a given motor as well as nonmotor task (14-22). These practicerelated changes in the set of brain areas engaged by a repeating task were reported to occur mostly within a single session. However, recent behavioral data have shown that the acquisition of skilled performance occurs on a time scale of hours, days, and weeks (2, 5, 7, 11-13, 18, 21-24). A leading notion, the ''power law of practice,'' suggests that the evolution of skilled performance is determined solely by the number of task repetitions (1-5, 7, 11-13, 25, 26); there are, nevertheless, compelling indications that the passage of time is also an important factor in the acquisition of skills (2,24,(27)(28)(29).Based on behavioral and imaging studies, two distinct stages in skill acquisition were proposed: early, relating to withinsession improvement, and late, slow changes in performance that can be observed across several (daily) sessions of practice (1,2,5,7,10,12,13,28). To account for robust delayed gains in performance that emerged after a latent period of more than a few hours after a single-session training, the notion of an intermediate phase corresponding to the posttraining hours has been proposed (2, 7, 13, 27-31). The conjecture is that a process of memory consolidation requiring time to become effective (in terms of performance) can be triggered by the training experience under certain conditions and requires time to become effective (in terms of performance) in both perceptual and motor tasks [but also in the acquisition of cognitive skills (12)].Recent studies further suggest that sleep may contribute significantly to the development of the delayed gains in this type of learning (28,30,32).It is not clear, however, whether the effects of a single training session, with ample time given for the evolution of delayed gains, can be conceptualized as the unit of skill acquisition, i.e., that multisession training gain constitutes but the sum of incremental gains of a number of single sessions. An earlier study (2) showed that all gains in speed of performance after completing longterm training on a sequence of movements were highly restricted by the physical parameters of the training experience, with no transfer to the untrained hand or to different arrangements of the trained movement components comprising the sequence. Here we show that this remarkable specificity evolves in a stepwise manner both within and between sessions. Within a given session, large performance gains occurred only for newly introduced conditions irrespective of the absolute level of performance. Although after a single session qualitativ...

Sleep-dependent motor memory plasticity in the human brain

“…vs. 0.10 [0.02ϮS.E.M. ]), consistent with previous reports of overnight sleep-dependent consolidation enhancements (Fischer et al, 2002;Korman et al, 2003;Walker et al, 2003aWalker et al, ,b, 2002 although this paced task configuration may limit the full expression of such learning.…”

“…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.…”

“…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.…”

Offline consolidation in implicit sequence learning

“…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.…”

“…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.…”