Upregulation of cortico-cerebellar functional connectivity after motor learning

Interactions between the cerebellum and primary motor cortex are crucial for the acquisition of new motor skills. Recent neuroimaging studies indicate that learning motor skills is associated with subsequent modulation of resting-state functional connectivity in the cerebellar and cerebral cortices. The neuronal processes underlying the motor-learning-induced plasticity are not well understood. Here, we investigate changes in functional connectivity in source-reconstructed electroencephalography (EEG) following the performance of a single session of a dynamic force task in twenty young adults. Source activity was reconstructed in 112 regions of interest (ROIs) and the functional connectivity between all ROIs was estimated using the imaginary part of coherence. Significant changes in resting-state connectivity were assessed using partial least squares (PLS). We found that subjects adapted their motor performance during the training session and showed improved accuracy but with slower movement times. A number of connections were significantly upregulated after motor training, principally involving connections within the cerebellum and between the cerebellum and motor cortex. Increased connectivity was confined to specific frequency ranges in the mu- and beta-bands. Post hoc analysis of the phase spectra of these cerebellar and cortico-cerebellar connections revealed an increased phase lag between motor cortical and cerebellar activity following motor practice. These findings show a reorganization of intrinsic cortico-cerebellar connectivity related to motor adaptation and demonstrate the potential of EEG connectivity analysis in source space to reveal the neuronal processes that underpin neural plasticity.

[1]  Heidi Johansen-Berg,et al.  The rate of visuomotor adaptation correlates with cerebellar white‐matter microstructure , 2009, Human brain mapping.

[2]  S. Kinomura,et al.  A PET Study of Visuomotor Learning under Optical Rotation , 2000, NeuroImage.

[3]  J. Doyon,et al.  Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[4]  L. Cohen,et al.  Neuroplasticity Subserving Motor Skill Learning , 2011, Neuron.

[5]  A. Luft,et al.  Stages of motor skill learning , 2005, Molecular Neurobiology.

[6]  Moritz Grosse-Wentrup,et al.  Multisubject Learning for Common Spatial Patterns in Motor-Imagery BCI , 2011, Comput. Intell. Neurosci..

[7]  Habib Benali,et al.  Dynamics of motor-related functional integration during motor sequence learning , 2010, NeuroImage.

[8]  A. Kelly,et al.  Human functional neuroimaging of brain changes associated with practice. , 2005, Cerebral cortex.

[9]  C. Miniussi,et al.  New insights into rhythmic brain activity from TMS–EEG studies , 2009, Trends in Cognitive Sciences.

[10]  Scott T. Grafton,et al.  Motor sequence learning with the nondominant left hand , 2002, Experimental Brain Research.

[11]  T. Milner,et al.  Functionally Specific Changes in Resting-State Sensorimotor Networks after Motor Learning , 2011, The Journal of Neuroscience.

[12]  Darren Price,et al.  Investigating the electrophysiological basis of resting state networks using magnetoencephalography , 2011, Proceedings of the National Academy of Sciences.

[13]  Kae Nakamura,et al.  Central mechanisms of motor skill learning , 2002, Current Opinion in Neurobiology.

[14]  Anthony Randal McIntosh,et al.  Partial least squares analysis of neuroimaging data: applications and advances , 2004, NeuroImage.

[15]  Hiroshi Imamizu,et al.  Human cerebellar activity reflecting an acquired internal model of a new tool , 2000, Nature.

[16]  J Mazziotta,et al.  A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[17]  Andreas Daffertshofer,et al.  Neural changes induced by learning a challenging perceptual-motor task , 2008, NeuroImage.

[18]  J. Doyon,et al.  Reorganization and plasticity in the adult brain during learning of motor skills , 2005, Current Opinion in Neurobiology.

[19]  Thomas F. Münte,et al.  Delineating the cortico-striatal-cerebellar network in implicit motor sequence learning , 2014, NeuroImage.

[20]  P. Celnik,et al.  Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. , 2011, Cerebral cortex.

[21]  B. Kowalski,et al.  Partial least-squares regression: a tutorial , 1986 .

[22]  A. Karni,et al.  The time course of learning a visual skill , 1993, Nature.

[23]  Heidi Haavik,et al.  A novel protocol to investigate motor training-induced plasticity and sensorimotor integration in the cerebellum and motor cortex. , 2014, Journal of neurophysiology.

[24]  M. Corbetta,et al.  Large-scale cortical correlation structure of spontaneous oscillatory activity , 2012, Nature Neuroscience.

[25]  BrunetDenis,et al.  Spatiotemporal analysis of multichannel EEG , 2011 .

[26]  Edward T. Bullmore,et al.  Network-based statistic: Identifying differences in brain networks , 2010, NeuroImage.

[27]  Markus Butz,et al.  Task-dependent oscillations during unimanual and bimanual movements in the human primary motor cortex and SMA studied with magnetoencephalography , 2005, NeuroImage.

[28]  Peter T. Fox,et al.  Changes occur in resting state network of motor system during 4weeks of motor skill learning , 2011, NeuroImage.

[29]  Rhea R. Kimpo,et al.  Cerebellar Purkinje cell activity drives motor learning , 2013, Nature Neuroscience.

[30]  Bradley D. Hatfield,et al.  Electroencephalographic Coherence During Visuomotor Performance: A Comparison of Cortico-Cortical Communication in Experts and Novices , 2009, Journal of motor behavior.

[31]  Juliane Britz,et al.  EEG microstate sequences in healthy humans at rest reveal scale-free dynamics , 2010, Proceedings of the National Academy of Sciences.

[32]  Michael Breakspear,et al.  Intrinsic Coupling Modes in Source-Reconstructed Electroencephalography , 2014, Brain Connect..

[33]  R. Ivry,et al.  Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements. , 2005, Journal of neurophysiology.

[34]  J. Donoghue,et al.  Plasticity and primary motor cortex. , 2000, Annual review of neuroscience.

[35]  E. Formisano,et al.  Phase coupling in a cerebro-cerebellar network at 8-13 Hz during reading. , 2007, Cerebral cortex.

[36]  G. Fink,et al.  Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches , 2011, Brain : a journal of neurology.

[37]  Alfons Schnitzler,et al.  Modality specific functional interaction in sensorimotor synchronization , 2009, Human brain mapping.

[38]  P. Matthews,et al.  Distinguishable brain activation networks for short- and long-term motor skill learning. , 2005, Journal of neurophysiology.

[39]  Ernst Fernando Lopes Da Silva Niedermeyer,et al.  Electroencephalography, basic principles, clinical applications, and related fields , 1982 .

[40]  B. Murphy,et al.  Do pursuit movement tasks lead to differential changes in early somatosensory evoked potentials related to motor learning compared with typing tasks? , 2015, Journal of neurophysiology.

[41]  V. Krause,et al.  Changes of motor-cortical oscillations associated with motor learning , 2014, Neuroscience.

[42]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[43]  U. Halsband,et al.  Motor learning in man: A review of functional and clinical studies , 2006, Journal of Physiology-Paris.

[44]  Dimitrios Pantazis,et al.  Coherent neural representation of hand speed in humans revealed by MEG imaging , 2007, Proceedings of the National Academy of Sciences.

[45]  M. Hallett,et al.  Dynamic cortical involvement in implicit and explicit motor sequence learning. A PET study. , 1998, Brain : a journal of neurology.

[46]  R. Shadmehr,et al.  Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degeneration. , 2005, Journal of neurophysiology.

[47]  Andreas Daffertshofer,et al.  Non-identical smoothing operators for estimating time-frequency interdependence in electrophysiological recordings , 2013, EURASIP J. Adv. Signal Process..

[48]  Heidi Johansen-Berg,et al.  Structural and functional bases for individual differences in motor learning , 2011, Human brain mapping.

[49]  Martin J. McKeown,et al.  Altered directional connectivity in Parkinson's disease during performance of a visually guided task , 2011, NeuroImage.

[50]  Simon B. Eickhoff,et al.  A quantitative meta-analysis and review of motor learning in the human brain , 2013, NeuroImage.

[51]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[52]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[53]  D. Yarnitsky,et al.  Neurophysiology of the cortical pain network: revisiting the role of S1 in subjective pain perception via standardized low-resolution brain electromagnetic tomography (sLORETA). , 2008, Journal of Pain.

[54]  O. Hikosaka,et al.  Presupplementary Motor Area Activation during Sequence Learning Reflects Visuo-Motor Association , 1999, The Journal of Neuroscience.

[55]  Daniel S. Margulies,et al.  Long-term effects of motor training on resting-state networks and underlying brain structure , 2011, NeuroImage.

[56]  L. Merabet,et al.  The plastic human brain cortex. , 2005, Annual review of neuroscience.

[57]  J. Doyon,et al.  Contributions of the basal ganglia and functionally related brain structures to motor learning , 2009, Behavioural Brain Research.

[58]  Michael Breakspear,et al.  Low-Dimensional Dynamics of Resting-State Cortical Activity , 2013, Brain Topography.

[59]  Michael Breakspear,et al.  The reorganization of corticomuscular coherence during a transition between sensorimotor states , 2014, NeuroImage.

[60]  R Chris Miall,et al.  The Time Course of Task-Specific Memory Consolidation Effects in Resting State Networks , 2014, The Journal of Neuroscience.

[61]  Leslie G. Ungerleider,et al.  Imaging Brain Plasticity during Motor Skill Learning , 2002, Neurobiology of Learning and Memory.

[62]  Christoph M. Michel,et al.  Spatiotemporal Analysis of Multichannel EEG: CARTOOL , 2011, Comput. Intell. Neurosci..

[63]  B. Ross,et al.  Internalized Timing of Isochronous Sounds Is Represented in Neuromagnetic Beta Oscillations , 2012, The Journal of Neuroscience.

[64]  M. Hallett,et al.  Identifying true brain interaction from EEG data using the imaginary part of coherency , 2004, Clinical Neurophysiology.

[65]  S. Lisberger,et al.  The Cerebellum: A Neuronal Learning Machine? , 1996, Science.

[66]  A. Schnitzler,et al.  The neural basis of intermittent motor control in humans , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[67]  Andreas Daffertshofer,et al.  Multivariate time–frequency analysis of electromagnetic brain activity during bimanual motor learning , 2007, NeuroImage.

[68]  G. Buzsáki,et al.  Cerebellar neuronal activity correlates with spike and wave EEG patterns in the rat , 1993, Epilepsy Research.

[69]  Mahmoud Hassan,et al.  EEG Source Connectivity Analysis: From Dense Array Recordings to Brain Networks , 2014, PloS one.

[70]  Anthony Randal McIntosh,et al.  Partial Least Squares (PLS) methods for neuroimaging: A tutorial and review , 2011, NeuroImage.

[71]  Keshab K. Parhi,et al.  Semiblind frequency-domain timing synchronization and channel estimation for OFDM systems , 2013, EURASIP J. Adv. Signal Process..

[72]  Volkmar Glauche,et al.  Dynamic gray matter changes within cortex and striatum after short motor skill training are associated with their increased functional interaction , 2012, NeuroImage.

[73]  Ethan R. Buch,et al.  Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation , 2009, Proceedings of the National Academy of Sciences.

[74]  M. Nitsche,et al.  Modulating functional connectivity patterns and topological functional organization of the human brain with transcranial direct current stimulation , 2011, Human brain mapping.

[75]  Y. Dudai The neurobiology of consolidations, or, how stable is the engram? , 2004, Annual review of psychology.

[76]  O. Bertrand,et al.  Oscillatory activity of the human cerebellum: The intracranial electrocerebellogram revisited , 2013, Neuroscience & Biobehavioral Reviews.

[77]  Guanghua Xiao,et al.  Alterations in resting functional connectivity due to recent motor task , 2013, NeuroImage.

[78]  Leslie G. Ungerleider,et al.  The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[79]  Leslie G. Ungerleider,et al.  Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning , 2003, Neuropsychologia.

[80]  M. Breakspear,et al.  Multi-frequency phase locking in human somatosensory cortex. , 2011, Progress in biophysics and molecular biology.

[81]  R D Pascual-Marqui,et al.  Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. , 2002, Methods and findings in experimental and clinical pharmacology.

[82]  J. Cardoso Infomax and maximum likelihood for blind source separation , 1997, IEEE Signal Processing Letters.

[83]  J. Krakauer,et al.  Human sensorimotor learning: adaptation, skill, and beyond , 2011, Current Opinion in Neurobiology.

[84]  J. Krakauer,et al.  Sensory prediction errors drive cerebellum-dependent adaptation of reaching. , 2007, Journal of neurophysiology.

[85]  H. Haavik,et al.  Selective changes in cerebellar-cortical processing following motor training , 2013, Experimental Brain Research.