The acquisition of skilled motor performance: Fast and slow experience-driven changes in primary motor cortex

Abstract

Behavioral and neurophysiological studies suggest that skill learning can be mediated by discrete, experience-driven changes within specific neural representations subserving the performance of the trained task. We have shown that a few minutes of daily practice on a sequential finger opposition task induced large, incremental performance gains over a few weeks of training. These gains did not generalize to the contralateral hand nor to a matched sequence of identical component movements, suggesting that a lateralized representation of the learned sequence of movements evolved through practice. This interpretation was supported by functional MRI data showing that a more extensive representation of the trained sequence emerged in primary motor cortex after 3 weeks of training. The imaging data, however, also indicated important changes occurring in primary motor cortex during the initial scanning sessions, which we proposed may ref lect the setting up of a task-specific motor processing routine. Here we provide behavioral and functional MRI data on experience-dependent changes induced by a limited amount of repetitions within the first imaging session. We show that this limited training experience can be sufficient to trigger performance gains that require time to become evident. We propose that skilled motor performance is acquired in several stages: "fast" learning, an initial, withinsession improvement phase, followed by a period of consolidation of several hours duration, and then "slow" learning, consisting of delayed, incremental gains in performance emerging after continued practice. This time course may ref lect basic mechanisms of neuronal plasticity in the adult brain that subserve the acquisition and retention of many different skills.The performance of many tasks improves, throughout life, with repetition and practice. Even in adulthood simple tasks such as reaching to a target or rapidly and accurately tapping a short sequence of finger movements, which appear, when mastered, to be effortlessly performed, often require extensive training before skilled performance develops. What changes occur in the adult brain when a new skill is acquired through practice? When, and after how much practice, do these changes occur? Functional reorganization of adult mammalian sensory and motor cortical representations has been found to occur in many different animal models of brain plasticity in the last two decades, advancing the idea that throughout life the functional properties of central nervous system neurons, as well as the neural circuitry within different brain areas, are malleable and retain a functionally significant degree of plasticity (e.g., refs. 1-4). These representational changes have been shown to be induced not only in response to lesions of peripheral or central sensory input or motor output pathways but also, in normal individuals, as a result of practice and experience. The advent of new brain imaging techniques, especially functional MRI (fMRI) (5), which allows repeated mapping of cor...

Neurofeedback fMRI‐mediated learning and consolidation of regional brain activation during motor imagery

“…Meanwhile, both the ROI analysis (Fig.3) and the subjective evaluation score (Fig.5) showed the two-week practice period did not result in any further increase in either the level of BOLD signal or the perception of task performance. The seemingly plateaued level of activation that we have seen in this study is in accordance with other behavioral/neuroimaging studies whereby newly acquired motor skill, once rapidly consolidated ('fast learning'), tapers off in terms of both performance and functional representation in the long term [Karni et al, 1998;Muellbacher et al, 2002;Krakauer and Shadmehr 2006]. However the current study does not provide enough data to examine this 'learning curve' effect and calls for the examination of the longitudinal studies extending to longer terms beyond the tested two-week practice period.…”

The effects of acute experimental hip muscle pain on dynamic single-limb balance performance in healthy middle-aged adults

“…This design also allowed us to determine whether performance of novel motor tasks improves with repetition in middle-aged adults. We hypothesised that performance would improve in Group-2 (consistent with short-term adaptions in motor performance with repetition [17]), but that the presence of pain would be associated with worse performance in Group-1.…”

Distinct Contribution of the Striatum and Cerebellum to Motor Learning

“…The latter findings are consistent with other studies which suggest that a striatal dysfunction does not affect the learning of an incremental perceptual-motor skill at the very beginning (i.e., Session 1, fast learning stage), but does so in the later (i.e., slow learning phase) stages of the acquisition process (Doyon et al, 1997a(Doyon et al, , 1997b(Doyon et al, , 1998(Doyon et al, , 1996b. Thus, this suggests that PD does not impair performance during the fast learning stage in which considerable improvement in performance can be seen within a single training session, but, instead, that it produces a deficit in the slow learning stage during which further gains are usually observed across several sessions of practice (Karni, 1996;Karni, Meyer, Rey-Hipolito, Jezzard, Adams, Turner, & Ungerleider, 1998).…”