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


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
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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.
    Full-text · Article · Dec 2015 · Clinical neuroimaging
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    • "Furthermore, previous studies (Di et al. 2012; Di Paola et al. 2013; Bernardi et al. 2013; Walz et al. 2015) revealed an effect of long-term motor skill training on the cerebellum . Di et al. (2012) detected significantly increased gray Table 3 Overview of previous studies on revealing the plasticity of brain functional connectivity (FC) after motor skill learning References Training task Training time fMRI scan Main findings in trainers Hamzei et al. (2012) Left hand practice 30 min/day for 5 days R-fMRI : FC between striatum and cortical regions Ma et al. (2011) Finger movement 15 min/day for 4 weeks R-fMRI : FC between PoCG.R and SupraMarginal_R in 0–2nd week : FC between PoCG.R and SupraMarginal_R in 3rd–4th week Ma et al. (2010) Finger movement 15 min/day for 4 weeks T-fMRI : FC between BG and cortical regions ; FC between CB and cortical regions Coynel et al. (2010) Finger movement 10–20 min/day for 4 weeks T-fMRI ; FC in associative/premotor networks : FC between associate/premotor and SMN Taubet et al. (2011) Dynamic balance 42.5 min once a week for 6 weeks R-fMRI : FC between frontal and parietal regions "
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    ABSTRACT: Long-term motor skill learning can induce plastic structural and functional reorganization of the brain. Our previous studies detected brain structural plasticity related to long-term intensive gymnastic training in world class gymnasts (WCGs). The goal of this study was to investigate brain functional plasticity in WCGs by using network measures of brain functional networks. Specifically, we acquired resting-state fMRI data from 13 WCGs and 14 controls, constructed their brain functional networks, and compared the differences in their network parameters. At the whole brain level, we detected significantly decreased overall functional connectivity (FC) and decreased local and global efficiency in the WCGs compared to the controls. At the modular level, we found intra- and inter-modular reorganization in three modules, the cerebellum, the cingulo-opercular and fronto-parietal networks, in the WCGs. On the nodal level, we revealed significantly decreased nodal strength and efficiency in several non-rich club regions of these three modules in the WCGs. These results suggested that functional plasticity can be detected in the brain functional networks of WCGs, especially in the cerebellum, fronto-parietal network, and cingulo-opercular network. In addition, we found that the FC between the fronto-parietal network and the sensorimotor network was significantly negatively correlated with the number of years of training in the WCGs. These findings may help us to understand the outstanding gymnastic performance of the gymnasts and to reveal the neural mechanisms that distinguish WCGs from controls.
    Full-text · Article · Sep 2015 · Brain Structure and Function
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    • "Thus, it seems that during the slow learning phase, the connection from cerebellum to putamen is weakened by additional practice, and this effect is more robust for sequence material. This observation as well as the general pruning of the network after sleep is in accordance with a study showing decrease in the overall connectivity of the cortico-striatal–cerebellar network with extended practice over 4 weeks (Coynel et al., 2010). It also agrees with a resting-state network analysis which showed recruitment of the cortico-basal ganglia–thalamic–cerebellar network directly after motor learning but not in resting-state measured after 6 h (Sami et al., 2014). "
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    ABSTRACT: The fast and slow learning stages of motor sequence learning are suggested to be realized through plasticity in a distributed cortico-striato-cerebellar network. To better understand the causal interactions within this network in the different phases of motor sequence learning, we investigated the effective connectivity within this network during encoding (Day 1) and after consolidation (Day 2) of a serial reaction time task. Using Dynamic Causal Modelling of fMRI data, we found general changes in network connections reflected in altered input nodes and endogenous connections when comparing the early and fast learning session to the late and slow learning session. Whereas encoding of a motor memory early on modulated several connections in a distributed network, slow learning resulted in a pruned network. More specifically, we found a negative modulation of connections from left M1 to right cerebellum, right premotor cortex to left cerebellum, as well as backward connections from putamen to cerebellum bilaterally in the encoding session. While connections during pre-sleep were significantly modulated by learning per se (i.e., specifically modulated by performance on sequence conditions), the connections observed after sleep were rather modulated by general performance (i.e., modulated by performance on both sequence and random conditions). A forward connection from left cerebellum to right putamen was found to be consistent across participants for the sequence condition only during slow learning. Together these findings suggest that whereas encoding in the fast learning phase requires plasticity in several connections implementing both motor and perceptual learning components, slow learning is mediated through connectivity from left cerebellum to right putamen. Copyright © 2015. Published by Elsevier Inc.
    Full-text · Article · Aug 2015 · NeuroImage
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