Characteristics of a long-term procedural skill in the monkey

Rand, Miya K.; Hikosaka, Okihide; Miyachi, Shigehiro; Lu, Xiaofeng; Miyashita, Kae

doi:10.1007/s002210050284

Cited by 57 publications

(41 citation statements)

References 15 publications

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“…These results are consistent with previous studies, which demonstrated that the accuracy and speed of movement may be acquired and retained in different brain regions (15,40). Areas contributing to new learning, such as the pre-SMA (18,38,41,42) and the associative striatum (2, 13), would be related to the accuracy of motor memory.…”

Section: Discussionsupporting

confidence: 92%

Distinct basal ganglia territories are engaged in early and advanced motor sequence learning

Lehericy

Benali

Moortele

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

548

449

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In this study, we used functional MRI (fMRI) at high field (3T) to track the time course of activation in the entire basal ganglia circuitry, as well as other motor-related structures, during the explicit learning of a sequence of finger movements over a month of training. Fourteen right-handed healthy volunteers had to practice 15 min daily a sequence of eight moves using the left hand. MRI sessions were performed on days 1, 14 and 28. In both putamen, activation decreased with practice in rostrodorsal (associative) regions. In contrast, there was a significant signal increase in more caudoventral (sensorimotor) regions of the putamen. Subsequent correlation analyses between signal variations and behavioral variables showed that the error rate (movement accuracy) was positively correlated with signal changes in areas activated during early learning, whereas reaction time (movement speed) was negatively correlated with signal changes in areas activated during advanced learning stages, including the sensorimotor putamen and globus pallidus. These results suggest the possibility that motor representations shift from the associative to the sensorimotor territories of the striato-pallidal complex during the explicit learning of motor sequences, suggesting that motor skills are stored in the sensorimotor territory of the basal ganglia that supports a speedy performance.functional MRI ͉ human ͉ subthalamic nucleus T here is now ample evidence from a number of sources that indicates that the basal ganglia are implicated in the formation of motor skills (1). In human studies using brain-imaging techniques, for example, changes of activity have been observed in the basal ganglia at different stages of the acquisition of motor abilities. Decreases of activity in the basal ganglia were reported during the early phase of trial-and-error learning of sequential movements (2). Using a similar task, Toni et al. (3) also reported a decrease of activity in the caudate nucleus, pre-supplementary motor area (SMA), and prefrontal cortex during the first hour of the acquisition process (3). By contrast, studies of implicit motor learning showed that the striatum was more active when subjects reached asymptotic performance, thus suggesting that this structure may be critical for the long-term storage of motor sequences (4-7). However, other investigations (8, 9) failed to document the presence of a greater increase in activity during the execution of well-learned sequential movements compared with the early learning phase.Although still conjectural, differences in the patterns of activation described above may reflect the involvement of different cortico-basal ganglia circuits during the acquisition process, because it is now known that cortical areas project to the striatum in separate associative, premotor, and sensorimotor circuits (10, 11). Indeed, previous imaging works have shown that rostral striatal areas are activated during learning of new motor sequences (2, 3) whereas the execution of well learned sequential movements invo...

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Section: Discussionsupporting

confidence: 92%

Distinct basal ganglia territories are engaged in early and advanced motor sequence learning

Lehericy

Benali

Moortele

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

548

449

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“…Contrary to the notion of skills as corresponding to more general performance routines (42), our results, in agreement with others (6,7,12,17,43), clearly show that more training resulted in more specific gains. Thus, practice makes transfer imperfect.…”

Section: Discussionsupporting

confidence: 90%

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

Korman

Raz

Flash

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

336

395

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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...

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“…Hikosaka and colleagues (Hikosaka et al 1995;Nakamura et al 1998;Rand et al 1998Rand et al , 2000 taught their monkeys long sequences of 10 movements by teaching them series of five short 2-movement sequences or sets. They referred to the entire 10-movement sequence as a hyperset.…”

Section: Role Of the Pre-sma In Updating Sequence Chunksmentioning

confidence: 99%

Organization of Action Sequences and the Role of the Pre-SMA

Kennerley¹,

Sakai²,

Rushworth³

2004

Journal of Neurophysiology

193

196

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Kennerley, Steve W., K. Sakai, and M.F.S. Rushworth. Organization of action sequences and the role of the pre-SMA. J Neurophysiol 91: 978-993, 2004. First published October 22, 2003 10.1152/jn.00651.2003. To understand the contribution of the human presupplementary motor area (pre-SMA) in sequential motor behavior, we performed a series of finger key-press experiments. Experiment 1 revealed that each subject had a spontaneous tendency to organize or "chunk" a long sequence into shorter components. We hypothesized that the pre-SMA might have a special role in initiating each chunk but not at other points during the sequence. Experiment 2 therefore examined the effect of 0.5-s, 10-Hz repetitive transcranial magnetic stimulation (rTMS) directed over the pre-SMA. As hypothesized, performance was disrupted when rTMS was delivered over the pre-SMA at the beginning of the second chunk but not when it was delivered in the middle of a chunk. Contrary to the hypothesis, TMS did not disrupt sequence initiation. Experiments 3 and 4 examined whether the very first movement of a sequence could be disrupted under any circumstances. Pre-SMA TMS did disrupt the initiation of sequences but only when subjects had to switch between sequences and when the first movement of each sequence was not covertly instructed by a learned visuomotor association. In conjunction, the results suggest that for overlearned sequences the pre-SMA is primarily concerned with the initiation of a sequence or sequence chunk and the role of the pre-SMA in sequence initiation is only discerned when subjects must retrieve the sequence from memory as a superordinate set of movements without the aid of a visuomotor association. Control experiments revealed such effects were not present when rTMS was applied over the left dorsal premotor cortex.

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Characteristics of a long-term procedural skill in the monkey

Cited by 57 publications

References 15 publications

Distinct basal ganglia territories are engaged in early and advanced motor sequence learning

Distinct basal ganglia territories are engaged in early and advanced motor sequence learning

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

Organization of Action Sequences and the Role of the Pre-SMA

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