Dynamics of motor-related functional integration during motor sequence learning

INSERM and UPMC Univ Paris 06, UMR-S 678 Laboratoire d'Imagerie Fonctionnelle, CHU Pitié-Salpêtrière, 91 Boulevard de l'Hôpital, Paris, France.
NeuroImage (Impact Factor: 6.36). 09/2009; 49(1):759-66. DOI: 10.1016/j.neuroimage.2009.08.048
Source: PubMed

ABSTRACT Motor skill learning is associated with profound changes in brain activation patterns over time. Associative and rostral premotor cortical and subcortical regions are mostly recruited during the early phase of explicit motor learning, while sensorimotor regions may increase their activity during the late learning phases. Distinct brain networks are therefore engaged during the early and late phases of motor skill learning. How these regions interact with one another and how information is transferred from one circuit to the other has been less extensively studied. In this study, we used functional MRI (fMRI) at 3T to follow the changes in functional connectivity in the associative/premotor and the sensorimotor networks, during extended practice (4 weeks) of an explicitly known sequence of finger movements. Evolution of functional connectivity was assessed using integration, a measure that quantifies the total amount of interaction within a network. When comparing the integration associated with a complex finger movement sequence to that associated with a simple sequence, we observed two patterns of decrease during the 4 weeks of practice. One was not specific as it was observed for all sequences, whereas a specific decrease was observed only for the execution of the learned sequence. This second decrease was a consequence of a relative decrease in associative/premotor network integration, together with a relative increase in between-network integration. These findings are in line with the hypothesis that information is transferred from the associative/premotor circuit to the sensorimotor circuit during the course of motor learning.

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Available from: David Coynel, Sep 26, 2015
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    • "In the early phase of motor practice, during which sensorimotor representations are built within a single practice session, activation decreases in the associative striatal territory (Floyer-Lea and Matthews, 2004; Jueptner et al., 1997; Laforce and Doyon, 2002; Lehéricy et al., 2005; Toni et al., 1998) and increases in the sensorimotor striatal territory (Doyon et al., 2009; Floyer-Lea and Matthews, 2004; Lehéricy et al., 2005). This functional remapping is associated with the reorganization of functional interactions in the striatocortical networks (Coynel et al., 2010). After sleep or the simple passage of time, a consolidation phase occurs, during which sensorimotor representations are maintained or strengthened (Albouy et al., 2013a, 2013b; Dayan and Cohen, 2011; Doyon et al., 2009; Ungerleider et al., 2002). "
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    ABSTRACT: Sensorimotor representations of movements are created in the sensorimotor network through repeated practice to support successful and effortless performance. Writer's cramp (WC) is a disorder acquired through extensive practice of finger movements, and it is likely associated with the abnormal acquisition of sensorimotor representations. We investigated (i) the activation and connectivity changes in the brain network supporting the acquisition of sensorimotor representations of finger sequences in patients with WC and (ii) the link between these changes and consolidation of motor performance 24 h after the initial practice. Twenty-two patients with WC and 22 age-matched healthy volunteers practiced a complex sequence with the right (pathological) hand during functional MRI recording. Speed and accuracy were measured immediately before and after practice (day 1) and 24 h after practice (day 2). The two groups reached equivalent motor performance on day 1 and day 2. During motor practice, patients with WC had (i) reduced hippocampal activation and hippocampal–striatal functional connectivity; and (ii) overactivation of premotor–striatal areas, whose connectivity correlated with motor performance after consolidation. These results suggest that patients with WC use alternative networks to reach equiperformance in the acquisition of new motor memories.
    Clinical neuroimaging 12/2015; 8. DOI:10.1016/j.nicl.2015.04.013 · 2.53 Impact Factor
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    • "Slow learning has been linked with larger-scale functional reorganization as well. A recent study tracked functional connectivity using fMRI over a period of 4 weeks of training on an explicit motor sequence task (Coynel et al., 2010). Early learning was associated with increased integration, a metric reflecting functional interactions among several brain regions, of a premotorassociative striatum-cerebellar network. "
    Eurohaptics; 06/2014
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    • "The present increase in interactions between regions of the corticostriatal network, as shown with the hypothesis-driven network analysis is in line with previous studies that have demonstrated greater strength in regional brain connectivity during the initial learning phase of a MSL task (Coynel et al., 2010; Ma et al., 2010; Sun et al., 2007). For example, our findings are in accord with those from Ma et al. (2010) who have reported that the connectivity between the basal ganglia and M1 is strengthened across 2 and 4 weeks of learning a sequence of movements . "
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    ABSTRACT: The consolidation of motor sequence learning is known to depend on sleep. Work in our laboratory and others have shown that the striatum is associated with this off-line consolidation process. In this study, we aimed to quantify the sleep-dependent dynamic changes occurring at the network level using a measure of functional integration. We directly compared changes in connectivity before and after sleep or the simple passage of daytime. As predicted, the results revealed greater integration within the cortico-striatal network after sleep, but not an equivalent daytime period. Importantly, a similar pattern of results was also observed using a data-driven approach; the increase in integration being specific to a cortico-striatal network, but not to other known functional networks. These findings reveal, for the first time, a new signature of motor sequence consolidation: a greater between-regions interaction within the cortico-striatal system.
    NeuroImage 05/2014; 99. DOI:10.1016/j.neuroimage.2014.05.022 · 6.36 Impact Factor
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