Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning
Introduction
In everyday life, we go about activities using a variety of motor skills that have been acquired gradually through practice and interactions with our environment. These include, for example, the use of smooth co-articulation of finger movements into a specific sequence (e.g. when playing a musical instrument like the piano), of regular multi-joint movement synergies (e.g. during reaching and grasping of small objects), and of a smoothly executed eye-body coordinated action (e.g. in playing sports such as golf). To study the time course, the biomechanics, the learning mechanisms (e.g. implicit versus explicit) and the neural substrates mediating our ability to learn such skilled behaviors in the laboratory, investigators have used experimental paradigms that fall into two categories: the first measures the incremental acquisition of movements into a well-executed behavior (motor sequence learning), whereas the second tests our capacity to compensate for environmental changes (motor adaptation) (e.g. [8], [11], [15], [18], [31], [32], [57], [58]). Operationally defined, these two forms of motor skill learning refer to the process by which movements, either produced alone or in a sequence, come to be performed effortlessly through repeated practice [68].
In both animals and humans, motor skill learning is usually measured by a reduction in reaction time and the number of errors, and/or by a change in movement synergy and kinematics (e.g. [5], [6], [7], [24], [30], [57], [60] for reviews). For some skills, such as learning to play a new melody on a musical instrument, early learning can be facilitated using explicit knowledge (i.e. requiring thought). For most motor skills, however, motor performance is ultimately over-learned to a point where it can be performed implicitly (i.e. without conscious recollection). As opposed to other forms of memory (e.g. episodic memory), these changes in performance are known to evolve slowly, requiring many repetitions over several training sessions [30], [60]. Indeed, psychophysical studies have demonstrated that the incremental acquisition of motor skills follows two distinct stages: first, an early, fast learning stage in which considerable improvement in performance can be seen within a single training session; and second, a later, slow stage in which further gains can be observed across several sessions (and even weeks) of practice [4], [32], [42]. In addition to these two stages, an intermediate phase corresponding to a consolidation period of the motor routine has recently been proposed, as gains in performance have been reported following a latent period of more than 6 h after the first training session without additional practice on the task (e.g. [26], [33]). Additionally, there is little or no interference from a competing task, provided it is administered beyond a critical time window of about 4–6 h [4], [49], [57]. Finally, with extended practice, the skilled behavior is thought to become resistant both to interference and to the simple passage of time [45]. Once over-learned, a motor skill can thus be readily retrieved with reasonable performance despite long periods without practice.
Based on animal and human work, several brain structures, including the striatum, cerebellum, and motor cortical regions of the frontal lobe have been thought to be critical for the acquisition and/or retention of motor skilled behaviors (e.g. [2], [5], [9], [10], [14], [19], [30], [53], [62], [64], [65] for reviews). Anatomical studies have demonstrated that these structures form two distinct cortical-subcortical circuits: a cortico-basal ganglia-thalamo-cortical loop and a cortico-cerebello-thalamo-cortical loop [37], [46], [61] (see Fig. 1). Evidence supporting the role of these cortical-subcortical systems in motor skill learning has come from impairments found in patients with striatal dysfunction (e.g. in Parkinson’s or Huntington’s disease), with damage to the cerebellum, or with a circumscribed lesion involving the frontal motor areas (e.g. [1], [6], [7], [13], [22], [44], [52], [69]). Further support has come from neurophysiological studies (e.g. [21], [42], [61]), as well as from lesion experiments in rodents (e.g. [36], [67] for a review) and non-human primates (e.g. [35], [38]). More recently, modern brain imaging techniques have allowed us to confirm not only the functional contribution of both cortico-striatal and cortico-cerebellar systems in motor skill learning, but also to identify in vivo the neural substrates mediating this type of memory and the functional dynamic changes that occur over the entire course of the acquisition process (e.g. see [5], [9], [10], [30], [64], [65] for reviews).
In this review paper, we will discuss the results of studies in healthy human subjects that examined the functional anatomy and the cerebral plasticity associated with the learning, consolidation and retention phases of motor skilled behaviors using brain imaging technology, such as positron emission tomography (PET) and functional magnetic resonance imaging (fMRI). Previous literature reviews have often pointed out the heterogeneity in the results obtained with this methodological approach [5], [10], [15], [65]. However, Doyon and Ungerleider [10] have recently proposed that much of the variability in the pattern of results across studies can be accounted for if one considers the type of motor task and the learning phase at which subjects are scanned. The latter model suggests that the cortico-striatal and cortico-cerebellar systems contribute differentially to motor sequence learning and motor adaptation, respectively, and that this is most apparent during the slow learning phase (i.e. automatization) when subjects achieve asymptotic performance, as well as during reactivation of the new skilled behavior in the retention phase. In support of this model, we will put emphasis on the results of our own series of experiments with tasks designed to investigate the neural substrate mediating motor sequence learning, and will also describe in more detail some of the studies that focused on the neuronal system involved in motor adaptation.
Section snippets
Neural correlates of motor sequence learning
In brain imaging investigations designed to better understand the neuroanatomy of motor skill learning, subjects are typically required to produce a sequence of movements that they know explicitly before scanning [9], [31], [32], [54], [56], to discover a particular sequence by trial and error [27], [28], [29], [50], [63], or to follow the display of visual stimuli appearing sequentially on a screen [6], [9], [15], [23], [47], [48]. The motor responses in those tasks involve finger-to-thumb
Neural correlates of motor adaptation
Several studies have examined the neural systems that are involved in motor adaptation. Tasks have included target reaching with the upper limb, in which the relationship between movements of a manipulandum and cursor on a monitor is reversed [11], [25], and pointing to a target with a robotic arm to which different force fields are applied [34], [58], [59]. In these studies, subjects have been tested during both early in the fast learning process and later when they have achieved asymptotic
Changes in motor representations over the course of learning
A very limited number of imaging studies have investigated the changes in motor representation that occur in the brain over the entire course of motor learning [18], [31], [32], [63]. Consequently, little is known about the neural circuitry mediating the acquisition of new motor skills that become fully mastered. Furthermore, the relative contribution of the cortico-striatal and cortico-cerebellar systems during the consolidation and long-term retention of motor skills remains largely unknown.
Acknowledgements
We wish to thank Katherine Hanratty, Miriam Beauchamp, Eva Gutierrez and Kimberly Montgomery for their technical assistance in preparing the manuscript. This work was supported, in part, by grants from the Natural Sciences and Engineering Research Council of Canada to J.D and V.P, the Canadian Institutes of Health Research to J.D., as well as through funding from the NIMH-IRP to L.G.U.
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