The contribution of the basal ganglia and cerebellum to motor learning: A neuro-computational approach

Baladron, Javier; Vitay, Julien; Fietzek, Torsten; Hamker, Fred H.

doi:10.1371/journal.pcbi.1011024

Cited by 13 publications

(3 citation statements)

References 109 publications

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“…Although both studies represent essential milestones towards a better understanding of both PD and motor learning, they differ from our model in some crucial aspects: although the network in ( 51) is composed of multiple cortical nodes leveraging the "TVB" framework, however, it does not model the cerebellar contribution explicitly, nor investigates functional motor learning impairments in PD. (52), on the other hand, provide a precise functional interpretation of the BG-cerebellum interplay and their model can produce complex motor responses that are close to human motor adaptation data. Still, their system-level design abstracts remarkably from the brain regions it represents and the authors do not consider any pathological scenario.…”

Section: Discussionmentioning

confidence: 66%

Dopamine-dependent cerebellar dysfunction enhances beta oscillations and disrupts motor learning in a multiarea model

Gambosi,

Sheiban,

Biasizzo

et al. 2023

Preprint

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Parkinson's disease (PD) is a chronic degenerative disorder of the central nervous system that affects the motor system. The discovery that PD motor symptoms result from the death of dopaminergic cells in the substantia nigra led to focus most of PD research on the basal ganglia. However, recent findings point to an active involvement of the cerebellum in PD. Here, we have developed a multiscale computational model of the rodent brain's basal ganglia-cerebellar network. Simulations showed that a direct effect of dopamine depletion on the cerebellum must be taken into account to reproduce the alterations of PD neural activity, particularly the increased beta oscillations widely reported in PD patients. Moreover, dopamine depletion indirectly impacted spike-time-dependent plasticity at the parallel fiber-Purkinje cell synapses, degrading associative motor learning as observed in PD. Overall, these results suggest a relevant involvement of cerebellum in PD motor symptoms.

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Section: Discussionmentioning

confidence: 66%

Dopamine-dependent cerebellar dysfunction enhances beta oscillations and disrupts motor learning in a multiarea model

Gambosi,

Sheiban,

Biasizzo

et al. 2023

Preprint

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“…One study in animals showed contralateral cortical to striate connections, not evaluated in our study, with implications in compensatory mechanisms with lesion, it is also a consideration to add such regions to the model moving forward ( Borra et al, 2022 ). Additionally, we opted to include the entire cerebellum, rather than specific cerebellar motor regions, as broader areas are involved in motor learning ( Baladron et al, 2023 ). However, such narrowing is a consideration for future studies.…”

Section: Discussionmentioning

confidence: 99%

Motor network dynamic resting state fMRI connectivity of neurotypical children in regions affected by cerebral palsy

Boerwinkle,

Sussman,

de Lima Xavier

et al. 2024

Front. Hum. Neurosci.

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BackgroundNormative childhood motor network resting-state fMRI effective connectivity is undefined, yet necessary for translatable dynamic resting-state-network-informed evaluation in pediatric cerebral palsy.MethodsCross-spectral dynamic causal modeling of resting-state-fMRI was investigated in 50 neurotypically developing 5- to 13-year-old children. Fully connected six-node network models per hemisphere included primary motor cortex, striatum, subthalamic nucleus, globus pallidus internus, thalamus, and contralateral cerebellum. Parametric Empirical Bayes with exhaustive Bayesian model reduction and Bayesian modeling averaging informed the model; Purdue Pegboard Test scores of hand motor behavior were the covariate at the group level to determine the effective-connectivity-functional behavior relationship.ResultsAlthough both hemispheres exhibited similar effective connectivity of motor cortico-basal ganglia-cerebellar networks, magnitudes were slightly greater on the right, except for left-sided connections of the striatum which were more numerous and of opposite polarity. Inter-nodal motor network effective connectivity remained consistent and robust across subjects. Age had a greater impact on connections to the contralateral cerebellum, bilaterally. Motor behavior, however, affected different connections in each hemisphere, exerting a more prominent effect on the left modulatory connections to the subthalamic nucleus, contralateral cerebellum, primary motor cortex, and thalamus.DiscussionThis study revealed a consistent pattern of directed resting-state effective connectivity in healthy children aged 5–13 years within the motor network, encompassing cortical, subcortical, and cerebellar regions, correlated with motor skill proficiency. Both hemispheres exhibited similar effective connectivity within motor cortico-basal ganglia-cerebellar networks reflecting inter-nodal signal direction predicted by other modalities, mainly differing from task-dependent studies due to network differences at rest. Notably, age-related changes were more pronounced in connections to the contralateral cerebellum. Conversely, motor behavior distinctly impacted connections in each hemisphere, emphasizing its role in modulating left sided connections to the subthalamic nucleus, contralateral cerebellum, primary motor cortex, and thalamus. Motor network effective connectivity was correlated with motor behavior, validating its physiological significance. This study is the first to evaluate a normative effective connectivity model for the pediatric motor network using resting-state functional MRI correlating with behavior and serves as a foundation for identifying abnormal findings and optimizing targeted interventions like deep brain stimulation, potentially influencing future therapeutic approaches for children with movement disorders.

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“…Research has identified that the basal ganglia are central to timing and time perception, crucial for teleoperation tasks that require millisecond to second precision (Merchant et al, 2013 ; McElvain et al, 2021 ; Baladron et al, 2023 ). Additionally, the supplementary motor area (SMA) and pre-SMA are involved in integrating temporal and motor information, essential for planning and timing movements (Halsband et al, 1993 ; Mondok and Wiener, 2023 ).…”

Section: Literature Reviewmentioning

confidence: 99%

Neural dynamics of delayed feedback in robot teleoperation: insights from fNIRS analysis

Zhou,

Ye,

Zhu

et al. 2024

Front. Hum. Neurosci.

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IntroductionAs robot teleoperation increasingly becomes integral in executing tasks in distant, hazardous, or inaccessible environments, operational delays remain a significant obstacle. These delays, inherent in signal transmission and processing, adversely affect operator performance, particularly in tasks requiring precision and timeliness. While current research has made strides in mitigating these delays through advanced control strategies and training methods, a crucial gap persists in understanding the neurofunctional impacts of these delays and the efficacy of countermeasures from a cognitive perspective.MethodsThis study addresses the gap by leveraging functional Near-Infrared Spectroscopy (fNIRS) to examine the neurofunctional implications of simulated haptic feedback on cognitive activity and motor coordination under delayed conditions. In a human-subject experiment (N = 41), sensory feedback was manipulated to observe its influences on various brain regions of interest (ROIs) during teleoperation tasks. The fNIRS data provided a detailed assessment of cerebral activity, particularly in ROIs implicated in time perception and the execution of precise movements.ResultsOur results reveal that the anchoring condition, which provided immediate simulated haptic feedback with a delayed visual cue, significantly optimized neural functions related to time perception and motor coordination. This condition also improved motor performance compared to the asynchronous condition, where visual and haptic feedback were misaligned.DiscussionThese findings provide empirical evidence about the neurofunctional basis of the enhanced motor performance with simulated synthetic force feedback in the presence of teleoperation delays. The study highlights the potential for immediate haptic feedback to mitigate the adverse effects of operational delays, thereby improving the efficacy of teleoperation in critical applications.

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The contribution of the basal ganglia and cerebellum to motor learning: A neuro-computational approach

Cited by 13 publications

References 109 publications

Dopamine-dependent cerebellar dysfunction enhances beta oscillations and disrupts motor learning in a multiarea model

Dopamine-dependent cerebellar dysfunction enhances beta oscillations and disrupts motor learning in a multiarea model

Motor network dynamic resting state fMRI connectivity of neurotypical children in regions affected by cerebral palsy

Neural dynamics of delayed feedback in robot teleoperation: insights from fNIRS analysis

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