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Spatiotemporal dissociation of fMRI activity in the caudate nucleus underlies human de novo motor skill learning.

ABSTRACT: Motor skill learning involves a complex process of generating novel movement patterns guided by evaluative feedback, such as a reward. Previous literature has suggested anteroposteriorly separated circuits in the striatum to be implicated in early goal-directed and later automatic stages of motor skill learning, respectively. However, the involvement of these circuits has not been well elucidated in human de novo motor skill learning, which requires learning arbitrary action-outcome associations and value-based action selection. To investigate this issue, we conducted a human functional MRI (fMRI) experiment in which participants learned to control a computer cursor by manipulating their right fingers. We discovered a double dissociation of fMRI activity in the anterior and posterior caudate nucleus, which was associated with performance in the early and late learning stages. Moreover, cognitive and sensorimotor cortico-caudate interactions predicted individual learning performance. Our results suggest parallel cortico-caudate networks operating in different stages of human de novo motor skill learning.

SUBMITTER: Choi Y

PROVIDER: S-EPMC7519330 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Spatiotemporal dissociation of fMRI activity in the caudate nucleus underlies human de novo motor skill learning.

Choi Yera Y Shin Emily Yunha EY Kim Sungshin S

Proceedings of the National Academy of Sciences of the United States of America 20200908 38

Motor skill learning involves a complex process of generating novel movement patterns guided by evaluative feedback, such as a reward. Previous literature has suggested anteroposteriorly separated circuits in the striatum to be implicated in early goal-directed and later automatic stages of motor skill learning, respectively. However, the involvement of these circuits has not been well elucidated in human de novo motor skill learning, which requires learning arbitrary action-outcome associations ...[more]

PMID: 32900934

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Project description:Many studies have used functional magnetic resonance imaging to unravel the neuronal underpinnings of motor system abnormalities in Parkinson's disease, indicating functional inhibition at the level of basal ganglia-thalamo-cortical motor networks. The study aim was to extend the characterization of functional motor changes in Parkinson's Disease by dissociating between two phases of action (i.e. motor planning and motor execution) during an automated unilateral finger movement sequence with the left and right hand, separately. In essence, we wished to identify neuronal dysfunction and potential neuronal compensation before (planning) and during (execution) automated sequential motor behavior in unmedicated early stage Parkinson's Disease patients. Twenty-two Parkinson's Disease patients (14 males; 53 ± 11 years; Hoehn and Yahr score 1.4 ± 0.6; UPDRS (part 3) motor score 16 ± 6) and 22 healthy controls (14 males; 49 ± 12 years) performed a pre-learnt four finger sequence (index, ring, middle and little finger, in order), either self-initiated (FREE) or externally triggered (REACT), within an 8-second time window. Findings were most pronounced during FREE with the clinically most affected side, where motor execution revealed significant underactivity of contralateral primary motor cortex, contralateral posterior putamen (sensorimotor territory), ipsilateral anterior cerebellum / cerebellar vermis, along with underactivity in supplementary motor area (based on ROI analyses only), corroborating previous findings in Parkinson's Disease. During motor planning, Parkinson's Disease patients showed a significant relative overactivity in dorsolateral prefrontal cortex (DLPFC), suggesting a compensatory overactivity. To a variable extent this relative overactivity in the DLPFC went along with a relative overactivity in the precuneus and the ipsilateral anterior cerebellum/cerebellar vermis Our study illustrates that a refined view of disturbances in motor function and compensatory processes can be gained from experimental designs that try to dissociate motor planning from motor execution, emphasizing that compensatory mechanisms are triggered in Parkinson's Disease when voluntary movements are conceptualized for action.

Project description:BackgroundThe definitive pathogenic mechanisms underlying chronic migraine (CM) remain unclear. Mounting evidence from functional and structural magnetic resonance imaging (MRI) studies suggests that the caudate nucleus (CN) plays a role in the cognitive, sensory, and emotional integration of pain information in patients with migraine. However, evidence concerning the role played by CN in CM patients is limited. Here, we used the CN as the seed to explore patterns of functional connectivity (FC) among healthy controls (HCs), patients with episodic migraine (EM), and patients with CM.MethodsWe included 25 HCs, 23 EM patients, and 46 CM patients in this study. All participants underwent resting-state functional MRI scans on a GE 3.0T MRI system. We performed seed-based FC analyses among the three groups using the bilateral CNs as seeds. We also compared the subgroups of CM (with and without medication overuse headache, males and females) and performed Pearson's correlation analyses between FC values and the clinical features of CM patients.ResultsFC values between the right CN and five clusters (mainly involved in emotion, cognition, and sensory-related brain regions) were higher in CM patients than in HCs. Compared to EM patients, enhanced FC values between the bilateral precuneus, left anterior cingulate gyrus, right middle cingulate cortex, right lingual gyrus, and right CN were shown in the CM patients. There were no significant differences between CM patients with and without MOH, males and females. FC values between the bilateral calcarine cortex, lingual gyrus, and right CN were positively correlated with body mass index. Moreover, right CN-related FC values in the left calcarine cortex and right lingual gyrus were inversely correlated with visual analogue scale scores for headaches.ConclusionOur results revealed abnormal right CN-based FC values in CM patients, suggesting dysfunction of brain networks associated with pain perception and multi-regulation (emotion, cognition, and sensory). Aberrant FC of the CN can provide potential neuroimaging markers for the diagnosis and treatment of CM.

Dataset Information

Spatiotemporal dissociation of fMRI activity in the caudate nucleus underlies human de novo motor skill learning.

Publications

Spatiotemporal dissociation of fMRI activity in the caudate nucleus underlies human de novo motor skill learning.

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