Spectral changes of interhemispheric crosstalk during movement instabilities.

Bimanual coordination requires the functional integration of the activity in various cortical, subcortical, spinal, and peripheral neural structures. We challenged this functional integration by destabilizing bimanual 5:8 tapping through an increase in movement tempo, while measuring brain and muscle activity using magnetoencephalography and electromyography. Movement instabilities were characterized by a drop in frequency locking. Time-frequency analysis revealed movement-related beta amplitude modulation in bilateral motor areas as well as movement-related corticospinal entrainment. Both of these synchronization patterns depended on movement tempo suggesting that the timescale needed for the upregulation and downregulation of beta synchrony in rhythmic tapping poses constraints on motor performance. Bilateral phase locking over movement cycles appeared to be mediated by beta-frequency oscillations and constrained by its phase dynamics. The timescale of beta synchrony thus seems to play a key role in achieving timed phase synchrony in the motor cortex and along the neural axis. Once event-related desynchronization-synchronization cycles cannot be build up properly, inhibition may become inadequate, resulting in a reduction of the stability of performance, which may eventually become unstable.

[1]  A. Fuchs,et al.  Event‐related changes in neuromagnetic activity associated with syncopation and synchronization timing tasks , 2001, Human brain mapping.

[2]  B. Day,et al.  Interhemispheric inhibition of the human motor cortex. , 1992, The Journal of physiology.

[3]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[4]  S. Baker.  Oscillatory interactions between sensorimotor cortex and the periphery , 2007, Current Opinion in Neurobiology.

[5]  Jens Frahm,et al.  Topography of the human corpus callosum revisited—Comprehensive fiber tractography using diffusion tensor magnetic resonance imaging , 2006, NeuroImage.

[6]  P. Brown,et al.  The functional role of interhemispheric synchronization in the control of bimanual timing tasks , 2002, Experimental Brain Research.

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

[8]  J. Stephens,et al.  A neurophysiological study of mirror movements in adults and children , 1999, Annals of neurology.

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

[10]  L. Cohen,et al.  Kinematically specific interhemispheric inhibition operating in the process of generation of a voluntary movement. , 2005, Cerebral cortex.

[11]  B U Meyer,et al.  Central motor pathways in patients with mirror movements. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[12]  C. Vaughan,et al.  Rectification and non-linear pre-processing of EMG signals for cortico-muscular analysis , 2003, Journal of Neuroscience Methods.

[13]  L. Deecke,et al.  Neuromagnetic fields accompanying unilateral and bilateral voluntary movements: topography and analysis of cortical sources. , 1991, Electroencephalography and clinical neurophysiology.

[14]  A. Villringer,et al.  Rolandic alpha and beta EEG rhythms' strengths are inversely related to fMRI‐BOLD signal in primary somatosensory and motor cortex , 2009, Human brain mapping.

[15]  Maureen Dennis,et al.  Impaired sensory and motor differentiation with corpus callosum agenesis: A lack of callosal inhibition during ontogeny? , 1976, Neuropsychologia.

[16]  F. Mormann,et al.  Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients , 2000 .

[17]  Peter J. Beek,et al.  Frequency-induced phase transitions in bimanual tapping , 1995, Biological Cybernetics.

[18]  J C de Munck,et al.  The use of an MEG device as 3D digitizer and motion monitoring system. , 2001, Physics in medicine and biology.

[19]  D. Cheyne,et al.  Spatiotemporal mapping of cortical activity accompanying voluntary movements using an event‐related beamforming approach , 2006, Human brain mapping.

[20]  H. Shibasaki,et al.  Mirror movement: Application of movement‐related cortical potentials , 1984, Annals of neurology.

[21]  Arthur W. Toga,et al.  A Probabilistic Atlas of the Human Brain: Theory and Rationale for Its Development The International Consortium for Brain Mapping (ICBM) , 1995, NeuroImage.

[22]  Andreas Daffertshofer,et al.  Stabilization of bimanual coordination due to active interhemispheric inhibition: a dynamical account , 2005, Biological Cybernetics.

[23]  Andreas Daffertshofer,et al.  A dynamical model for mirror movements , 1999 .

[24]  Viktor K. Jirsa,et al.  Connecting Cortical and Behavioral Dynamics: Bimanual Coordination , 1998, Neural Computation.

[25]  Mark Hallett,et al.  Movement rate effect on activation and functional coupling of motor cortical areas. , 2002, Journal of neurophysiology.

[26]  P Girlanda,et al.  Paired associative stimulation of left and right human motor cortex shapes interhemispheric motor inhibition based on a Hebbian mechanism. , 2009, Cerebral cortex.

[27]  J. Vrba,et al.  Signal processing in magnetoencephalography. , 2001, Methods.

[28]  Tatsuya Asai,et al.  Hemispheric Asymmetry of Frequency-Dependent Suppression in the Ipsilateral Primary Motor Cortex During Finger Movement: A Functional Magnetic Resonance Imaging Study , 2008, Cerebral cortex.

[29]  L. Cohen,et al.  Transitions between dynamical states of differing stability in the human brain , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  G. Ermentrout.  Dynamic patterns: The self-organization of brain and behavior , 1997 .

[31]  D. Cheyne,et al.  Dynamic cortical activity in the human brain reveals motor equivalence , 1998, Nature.

[32]  B. W. van Dijk,et al.  MEG-compatible force sensor , 2005, Journal of Neuroscience Methods.

[33]  C. Gerloff,et al.  Bimanual coordination and interhemispheric interaction. , 2002, Acta psychologica.

[34]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[35]  Andrea Tacchino,et al.  Callosal Contributions to Simultaneous Bimanual Finger Movements , 2008, The Journal of Neuroscience.

[36]  Andreas Daffertshofer,et al.  Spatio-temporal patterns of encephalographic signals during polyrhythmic tapping , 2000 .

[37]  M. Honda,et al.  Neural correlates of the spontaneous phase transition during bimanual coordination. , 2006, Cerebral cortex.

[38]  S. Swinnen.  Intermanual coordination: From behavioural principles to neural-network interactions , 2002, Nature Reviews Neuroscience.

[39]  D. Cheyne,et al.  Supplementary motor area activation while tapping bimanually different rhythms in musicians , 2004, Experimental Brain Research.

[40]  Kanti V. Mardia,et al.  Statistics of Directional Data , 1972 .

[41]  L. Deecke,et al.  Movement-related potentials accompanying unilateral and bilateral finger movements with different inertial loads. , 1990, Electroencephalography and clinical neurophysiology.

[42]  G. Pfurtscheller,et al.  Patterns of cortical activation during planning of voluntary movement. , 1989, Electroencephalography and clinical neurophysiology.

[43]  K. Heilman,et al.  Ipsilateral motor activation during unimanual and bimanual motor tasks , 2007, Clinical Neurophysiology.

[44]  Viktor K. Jirsa,et al.  Theory of the Relation between Human Brain Activity (MEG) and Hand Movements , 2000, NeuroImage.

[45]  Andreas Daffertshofer,et al.  Spectral analyses of event-related encephalographic signals , 2000 .