Neuronal network coherent with hand kinematics during fast repetitive hand movements

We quantified the coupling between magnetoencephalographic (MEG) cortical signals and the kinematics of fast repetitive voluntary hand movements monitored by a 3-axis accelerometer. Ten healthy right-handed adults performed self-paced flexion-extension movements of right-hand fingers at ~3Hz with either touching the thumb during flexions (TOUCH) or not (noTOUCH). At the sensor level, we found in all subjects and conditions significant coherence at the movement frequency (F0) and its first harmonic (F1). Coherence values were significantly higher in TOUCH compared to noTOUCH. At the group level, dynamic imaging of coherent sources localized the main source of coherent activity at the left primary motor (M1) hand area, except at F0 TOUCH were the main source was localized at the left primary sensory (S1) hand area. Other coherent brain areas were also identified at right S1-M1 cortices (F0), left dorsolateral prefrontal cortex (F1), left posterior parietal cortex (F0 TOUCH and F1 noTOUCH) and left medial S1-M1 areas (TOUCH). This study highlights the prominent role of rhythmic neuronal activity phase-locked to movements for the encoding and the integration of key sensori-motor features of limb kinematics. This study also suggests that somatosensory afferences play a key role to sustain a high synchronization level between the neuronal activity in coherent brain areas and hand acceleration. Some coherent brain regions differed between F0 and F1 in both conditions, suggesting that distinct cortical areas are involved in different features of hand kinematics.

[1]  Toshio Inui,et al.  Separating brain regions involved in internally guided and visual feedback control of moving effectors: An event-related fMRI study , 2006, NeuroImage.

[2]  Richard B. Ivry,et al.  Cerebellar activation during discrete and not continuous timed movements: An fMRI study , 2007, NeuroImage.

[3]  Gregor Leicht,et al.  The free choice whether or not to respond after stimulus presentation , 2009, Human brain mapping.

[4]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[5]  Wolfgang Prinz,et al.  The role of the primary somatosensory cortex in an auditorily paced finger tapping task , 2004, Experimental Brain Research.

[6]  Stuart N Baker,et al.  The effect of diazepam on motor cortical oscillations and corticomuscular coherence studied in man , 2003, The Journal of physiology.

[7]  Alvaro Pascual-Leone,et al.  Ipsilateral motor cortex activation on functional magnetic resonance imaging during unilateral hand movements is related to interhemispheric interactions , 2003, NeuroImage.

[8]  Pavel Sovka,et al.  Approximation of statistical distribution of magnitude squared coherence estimated with segment overlapping , 2007, Signal Process..

[9]  Joachim Gross,et al.  The cerebral oscillatory network associated with auditorily paced finger movements , 2005, NeuroImage.

[10]  M. Schieber.  Constraints on somatotopic organization in the primary motor cortex. , 2001, Journal of neurophysiology.

[11]  Luca Faes,et al.  Surrogate data analysis for assessing the significance of the coherence function , 2004, IEEE Transactions on Biomedical Engineering.

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

[13]  A B Schwartz,et al.  Motor cortical representation of speed and direction during reaching. , 1999, Journal of neurophysiology.

[14]  A M Amjad,et al.  A framework for the analysis of mixed time series/point process data--theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. , 1995, Progress in biophysics and molecular biology.

[15]  A. P. Georgopoulos,et al.  Movement parameters and neural activity in motor cortex and area 5. , 1994, Cerebral cortex.

[16]  D. Wolpert,et al.  Maintaining internal representations: the role of the human superior parietal lobe , 1998, Nature Neuroscience.

[17]  K. Zilles,et al.  Functional neuroanatomy of the primate isocortical motor system , 2000, Anatomy and Embryology.

[18]  M. Hallett,et al.  Hemispheric asymmetry of ipsilateral motor cortex activation during unimanual motor tasks: further evidence for motor dominance , 2001, Clinical Neurophysiology.

[19]  Takashi Hanakawa,et al.  Functional coupling underlying motor and cognitive functions of the dorsal premotor cortex , 2009, Behavioural Brain Research.

[20]  Terrence D. Lagerlund,et al.  Cortical potentials at the frequency of absolute wrist velocity become phase-locked during slow sinusoidal tracking movements , 1999, Experimental Brain Research.

[21]  Richard A Andersen,et al.  Forward estimation of movement state in posterior parietal cortex , 2008, Proceedings of the National Academy of Sciences.

[22]  José Luis Contreras-Vidal,et al.  Decoding center-out hand velocity from MEG signals during visuomotor adaptation , 2009, NeuroImage.

[23]  C. Mehring,et al.  Inference of hand movements from local field potentials in monkey motor cortex , 2003, Nature Neuroscience.

[24]  Riitta Hari,et al.  Functional motor-cortex mapping using corticokinematic coherence , 2011, NeuroImage.

[25]  S. Taulu,et al.  Applications of the signal space separation method , 2005, IEEE Transactions on Signal Processing.

[26]  A. Schwartz,et al.  On the relationship between joint angular velocity and motor cortical discharge during reaching. , 2001, Journal of neurophysiology.

[27]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. II. Coding of the direction of movement by a neuronal population , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  J. R. Rosenberg,et al.  The Fourier approach to the identification of functional coupling between neuronal spike trains. , 1989, Progress in biophysics and molecular biology.

[29]  Takashi Hanakawa,et al.  Finger and face representations in the ipsilateral precentral motor areas in humans. , 2005, Journal of neurophysiology.

[30]  David M. Santucci,et al.  Learning to Control a Brain–Machine Interface for Reaching and Grasping by Primates , 2003, PLoS biology.

[31]  Eran Stark,et al.  Distinct movement parameters are represented by different neurons in the motor cortex , 2007, The European journal of neuroscience.

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

[33]  Katsuya Ogata,et al.  Functional network of the basal ganglia and cerebellar motor loops in vivo: Different activation patterns between self-initiated and externally triggered movements , 2006, NeuroImage.

[34]  R. Andersen,et al.  The posterior parietal cortex: Sensorimotor interface for the planning and online control of visually guided movements , 2006, Neuropsychologia.

[35]  R. Ivry,et al.  Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. , 2005, Journal of neurophysiology.

[36]  S. Baker,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[37]  F. Binkofski,et al.  The role of ipsilateral primary motor cortex in movement control and recovery from brain damage , 2010, Experimental Neurology.

[38]  R. Passingham,et al.  Self-initiated versus externally triggered movements. II. The effect of movement predictability on regional cerebral blood flow. , 2000, Brain : a journal of neurology.

[39]  P Baraldi,et al.  Ipsilateral involvement of primary motor cortex during motor imagery , 2000, The European journal of neuroscience.

[40]  J. Semmler,et al.  Motor unit discharge and force tremor in skill- and strength-trained individuals , 1998, Experimental Brain Research.

[41]  M. Hallett,et al.  Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. , 1999, Journal of neurophysiology.

[42]  Stephen M. Rao,et al.  Motor Sequence Complexity and Performing Hand Produce Differential Patterns of Hemispheric Lateralization , 2004, Journal of Cognitive Neuroscience.

[43]  C. Kennard,et al.  Functional role of the supplementary and pre-supplementary motor areas , 2008, Nature Reviews Neuroscience.

[44]  R. Passingham,et al.  The sensory guidance of movement: a comparison of the cerebellum and basal ganglia , 1996, Experimental Brain Research.

[45]  B R Rosen,et al.  Activation of distinct motor cortex regions during ipsilateral and contralateral finger movements. , 1999, Journal of neurophysiology.

[46]  Alan Sunderland,et al.  fMRI signal decreases in ipsilateral primary motor cortex during unilateral hand movements are related to duration and side of movement , 2005, NeuroImage.

[47]  A. Schnitzler,et al.  The cerebral oscillatory network of voluntary tremor , 2004, The Journal of physiology.

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

[49]  T. Ebner,et al.  Cerebellar Purkinje Cell Simple Spike Discharge Encodes Movement Velocity in Primates during Visuomotor Arm Tracking , 1999, The Journal of Neuroscience.

[50]  Timothy J Ebner,et al.  Past, present, and emerging principles in the neural encoding of movement. , 2009, Advances in experimental medicine and biology.

[51]  H. Zelaznik,et al.  Disrupted Timing of Discontinuous But Not Continuous Movements by Cerebellar Lesions , 2003, Science.

[52]  A. Georgopoulos,et al.  Parietal representation of hand velocity in a copy task. , 2005, Journal of neurophysiology.

[53]  Scott T. Grafton,et al.  Motor subcircuits mediating the control of movement velocity: a PET study. , 1998, Journal of neurophysiology.

[54]  Shigeru Muraki,et al.  Cortical activity in multiple motor areas during sequential finger movements: An application of independent component analysis , 2005, NeuroImage.

[55]  Peter Brown,et al.  Transient increases of synchronized neural activity during movement preparation: influence of cognitive constraints , 2003, Experimental Brain Research.

[56]  R. J. Ilmoniemi,et al.  Bilateral changes in excitability of sensorimotor cortices during unilateral movement: Combined electroencephalographic and transcranial magnetic stimulation study , 2008, Neuroscience.

[57]  Seong-Gi Kim,et al.  Cerebellar activation during copying geometrical shapes. , 2003, Journal of neurophysiology.

[58]  Paul B. Johnson,et al.  Making arm movements within different parts of space: dynamic aspects in the primate motor cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[59]  Paul Van Hecke,et al.  Internal vs external generation of movements: differential neural pathways involved in bimanual coordination performed in the presence or absence of augmented visual feedback , 2003, NeuroImage.

[60]  D. Hoffman,et al.  Muscle and movement representations in the primary motor cortex. , 1999, Science.

[61]  Stephan Salenius,et al.  Modulation of cortex-muscle oscillatory interaction by ischaemia-induced deafferentation , 2003, Neuroreport.

[62]  J Gross,et al.  REPRINTS , 1962, The Lancet.

[63]  Michael Alexander,et al.  Age-Related Differences in Movement Representation , 2002, NeuroImage.