Neural correlates of motor learning: Network communication versus local oscillations

Abstract Learning new motor skills through training, also termed motor learning, is central for everyday life. Current training strategies recommend intensive task-repetitions aimed at inducing local activation of motor areas, associated with changes in oscillation amplitudes (“event-related power”) during training. More recently, another neural mechanism was suggested to influence motor learning: modulation of functional connectivity (FC), that is, how much spatially separated brain regions communicate with each other before and during training. The goal of the present study was to compare the impact of these two neural processing types on motor learning. We measured EEG before, during, and after a finger-tapping task (FTT) in 20 healthy subjects. The results showed that training gain, long-term expertise (i.e., average motor performance), and consolidation were all predicted by whole-brain alpha- and beta-band FC at motor areas, striatum, and mediotemporal lobe (MTL). Local power changes during training did not predict any dependent variable. Thus, network dynamics seem more crucial than local activity for motor sequence learning, and training techniques should attempt to facilitate network interactions rather than local cortical activation.

• Publication year

  2024

• Venue

  Network Neuroscience

• Publication date

  2024-04-10

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1162/netn_a_00374PMID 39355447PMCID 11340994
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Neurophysiological and behavioural effects of conventional and high definition tDCS

  2021cited by this paper
• Effects of rTMS on the brain: is there value in variability?

  2021cited by this paper
• Stepwise synaptic plasticity events drive the early phase of memory consolidation

  2021cited by this paper
• Separating Neural Oscillations from Aperiodic 1/f Activity: Challenges and Recommendations

  2021cited by this paper
• Theta but not beta power is positively associated with better explicit motor task learning

  2021cited by this paper
• Resting-state functional brain connectivity is related to subsequent procedural learning skills in school-aged children

  2021cited by this paper
• Disrupted resting-state EEG alpha-band interactions as a novel marker for the severity of visual field deficits after brain lesion.

  2021cited by this paper
• The Functional Relevance of Task-State Functional Connectivity

  2020cited by this paper
• Can EEG and MEG detect signals from the human cerebellum?

  2020cited by this paper
• Comparison of Phase Synchronization Measures for Identifying Stimulus-Induced Functional Connectivity in Human Magnetoencephalographic and Simulated Data

  2020cited by this paper
• Spontaneous Network Coupling Enables Efficient Task Performance without Local Task-Induced Activations

  2020influential reference
• Automated anatomical labelling atlas 3

  2020influential reference
• Human Hippocampal Neurons Track Moments in a Sequence of Events

  2020cited by this paper
• Localization of deep brain activity with scalp and subdural EEG

  2020cited by this paper
• The Medial Temporal Lobe Is Critical for Spatial Relational Perception

  2020influential reference
• Mechanisms of systems memory consolidation during sleep

  2019cited by this paper
• High Definition Transcranial Direct Current Stimulation Does Not Modulate Implicit Task Sequence Learning and Consolidation.

  2019cited by this paper
• Large-Scale Communication in the Human Brain Is Rhythmically Modulated through Alpha Coherence.

  2019cited by this paper
• Modulation of large-scale cortical coupling by transcranial alternating current stimulation.

  2019cited by this paper
• Task-evoked activity quenches neural correlations and variability across cortical areas

  2019cited by this paper
• Cortical beta oscillations are associated with motor performance following visuomotor learning

  2019cited by this paper
• Intelligence and uncertainty: Implications of hierarchical predictive processing for the neuroscience of cognitive ability

  2018cited by this paper
• The role of engram cells in the systems consolidation of memory

  2018cited by this paper
• Motor sequence learning

  2018cited by this paper
• Modulating functional connectivity after stroke with neurofeedback: Effect on motor deficits in a controlled cross-over study

  2018cited by this paper
• Resting‐state connectivity predicts visuo‐motor skill learning

  2018influential reference
• Comparison of Neuroplastic Responses to Cathodal Transcranial Direct Current Stimulation and Continuous Theta Burst Stimulation in Subacute Stroke.

  2017cited by this paper
• Beta band oscillations in motor cortex reflect neural population signals that delay movement onset

  2017cited by this paper
• Sparsity enables estimation of both subcortical and cortical activity from MEG and EEG

  2017cited by this paper
• The Cognitive Psychology of Sleep and Memory

  2017cited by this paper
• Dynamics of EEG functional connectivity during statistical learning.

  2017cited by this paper
• MarsAtlas: A cortical parcellation atlas for functional mapping

  2016cited by this paper
• Resting-state Functional Connectivity is an Age-dependent Predictor of Motor Learning Abilities

  2016cited by this paper
• A Systematic Review and Meta-Analysis of the Effects of Transcranial Direct Current Stimulation (tDCS) Over the Dorsolateral Prefrontal Cortex in Healthy and Neuropsychiatric Samples: Influence of Stimulation Parameters

  2016cited by this paper
• Transcranial Electrical Stimulation

  2016cited by this paper
• Ongoing dynamics in large-scale functional connectivity predict perception

  2015cited by this paper
• Functional connectivity in the resting‐state motor networks influences the kinematic processes during motor sequence learning

  2015cited by this paper
• Evolution of cerebral cortico-cortical communication during visuomotor adaptation to a cognitive-motor executive challenge.

  2015cited by this paper
• Neurofeedback training of alpha-band coherence enhances motor performance.

  2015cited by this paper
• Evidence that transcranial direct current stimulation (tDCS) generates little-to-no reliable neurophysiologic effect beyond MEP amplitude modulation in healthy human subjects: A systematic review.

  2015cited by this paper
• Striatal-cerebellar networks mediate consolidation in a motor sequence learning task: An fMRI study using dynamic causal modelling

  2015cited by this paper
• Rhythms for Cognition: Communication through Coherence.

  2015influential reference
• Stroke Rehabilitation.

  2015cited by this paper
• Do sensorimotor β-oscillations maintain muscle synergy representations in primary motor cortex?

  2015cited by this paper
• Practice changes beta power at rest and its modulation during movement in healthy subjects but not in patients with Parkinson's disease

  2015cited by this paper
• Coherent neural oscillations predict future motor and language improvement after stroke.

  2015cited by this paper
• The Consolidation and Transformation of Memory.

  2015cited by this paper
• Two Intrinsic Coupling Types for Resting-State Integration in the Human Brain

  2014influential reference
• Prestimulus oscillatory power and connectivity patterns predispose conscious somatosensory perception

  2014cited by this paper
• Resting state connectivity immediately following learning correlates with subsequent sleep-dependent enhancement of motor task performance

  2014cited by this paper
• Changes of motor-cortical oscillations associated with motor learning.

  2014cited by this paper
• Resting-state cortical connectivity predicts motor skill acquisition

  2014influential reference
• The Time Course of Task-Specific Memory Consolidation Effects in Resting State Networks

  2014cited by this paper
• Assessment of Subcortical Source Localization Using Deep Brain Activity Imaging Model with Minimum Norm Operators: A MEG Study

  2013cited by this paper
• Neurocognitive biases and the patterns of spontaneous correlations in the human cortex.

  2013cited by this paper
• Origins of specificity during tDCS: anatomical, activity-selective, and input-bias mechanisms

  2013cited by this paper
• Network mechanisms of responsiveness to continuous theta‐burst stimulation

  2013cited by this paper
• The behavioral significance of coherent resting-state oscillations after stroke

  2012cited by this paper
• Neural correlates of performance variability during motor sequence acquisition

  2012cited by this paper
• The importance of timing in segregated theta phase-coupling for cognitive performance.

  2012cited by this paper
• Alpha-band oscillations, attention, and controlled access to stored information

  2012cited by this paper
• The organization of physiological brain networks.

  2012cited by this paper
• Spectral fingerprints of large-scale neuronal interactions

  2012cited by this paper
• Removal of Spurious Coherence in MEG Source-Space Coherence Analysis

  2011cited by this paper
• Resting-State Functional Connectivity Indexes Reading Competence in Children and Adults

  2011cited by this paper
• Stroke rehabilitation.

  2011cited by this paper
• MEG/EEG Source Reconstruction, Statistical Evaluation, and Visualization with NUTMEG

  2011influential reference
• Neuroplasticity subserving motor skill learning.

  2011cited by this paper
• α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking

  2011cited by this paper
• Localization of cortico-peripheral coherence with electroencephalography

  2011influential reference
• Rapid consolidation and the human hippocampus: Intracranial recordings confirm surface EEG

  2011cited by this paper
• Dynamic reconfiguration of human brain networks during learning

  2010cited by this paper
• Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition

  2010cited by this paper
• Beta-band oscillations--signalling the status quo?

  2010cited by this paper
• Movement-related desynchronization of alpha rhythms is lower in athletes than non-athletes: a high-resolution EEG study.

  2010cited by this paper
• Dynamics of motor-related functional integration during motor sequence learning

  2010cited by this paper
• Contributions of the basal ganglia and functionally related brain structures to motor learning.

  2009influential reference
• The whats and whens of sleep-dependent memory consolidation.

  2009cited by this paper
• The Resting Human Brain and Motor Learning

  2009cited by this paper
• Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage.

  2008cited by this paper
• Mapping functional connectivity in patients with brain lesions

  2008cited by this paper
• Both the hippocampus and striatum are involved in consolidation of motor sequence memory.

  2008cited by this paper
• A Matlab library for solving quasi-static volume conduction problems using the boundary element method

  2007cited by this paper
• Multivariate time-frequency analysis of electromagnetic brain activity during bimanual motor learning

  2007cited by this paper
• Neural dynamics for facial threat processing as revealed by gamma band synchronization using MEG

  2007cited by this paper
• The dynamics of hippocampal activation during encoding of overlapping sequences.

  2006cited by this paper
• Functional connectivity of cortical networks involved in bimanual motor sequence learning.

  2006cited by this paper
• A mechanism for cognitive dynamics: neuronal communication through neuronal coherence.

  2005cited by this paper
• The Neural Correlates of Motor Skill Automaticity

  2005cited by this paper
• Distinct basal ganglia territories are engaged in early and advanced motor sequence learning.

  2005cited by this paper
• Sleep-dependent memory consolidation

  2005cited by this paper
• Analysis of weighted networks.

  2004cited by this paper
• Asymptotic SNR of scalar and vector minimum-variance beamformers for neuromagnetic source reconstruction

  2004cited by this paper
• Identifying true brain interaction from EEG data using the imaginary part of coherency.

  2004cited by this paper
• Current concepts in procedural consolidation

  2004cited by this paper
• Learned material content and acquisition level modulate cerebral reactivation during posttraining rapid-eye-movements sleep

  2003cited by this paper
• An FMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning.

  2003cited by this paper
• Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning.

  2003cited by this paper
• Central mechanisms of motor skill learning.

  2002cited by this paper
• Practice with sleep makes perfect: sleep-dependent motor skill learning.

  2002cited by this paper

• Towards Network-Based Neurofeedback of Visual Areas to Enhance Visual Perception

  2026cites this paper
• Exploring the Impact of Declarative Learning on the Consolidation of Acquired Motor Skills Under Valence Feedback

  2025cites this paper
• Oscillatory dynamics of motor learning across adulthood life span: a systematic review

  2025cites this paper
• Characterizing Autism Spectrum Disorder Through Fusion of Local Cortical Activation and Global Functional Connectivity Using Game-Based Stimuli and a Mobile EEG System

  2024cites this paper