The human sensorimotor cortex fosters muscle synergies through cortico-synergy coherence

In neuromotor control, the dimensionality of complex muscular activation patterns is effectively reduced through the emergence of muscle synergies. Muscle synergies are tailored to task-specific biomechanical needs. Traditionally, they are considered as low-dimensional neural output of the spinal cord and as such their coherent cortico-muscular pathways have remained underexplored in humans. We investigated whether muscle synergies have a higher-order origin, especially, whether they are manifest in the cortical motor network. We focused on cortical muscle synergy representations involved in balance control and examined changes in cortico-synergy coherence accompanying short-term balance training. We acquired electromyography and electro-encephalography and reconstructed cortical source activity using adaptive spatial filters. The latter were based on three muscle synergies decomposed from the activity of nine unilateral leg muscles using non-negative matrix factorization. The corresponding cortico-synergy coherence displayed phase-locked activity at the Piper rhythm, i.e., cortico-spinal synchronization around 40 Hz. Our study revealed the presence of muscle synergies in the motor cortex, in particular, in the paracentral lobule, known for the representation of lower extremities. We conclude that neural oscillations synchronize between the motor cortex and spinal motor neuron pools signifying muscle synergies. The corresponding cortico-synergy coherence around the Piper rhythm decreases with training-induced balance improvement.

[1]  T. Hortobágyi,et al.  Dose-Response Relationships of Balance Training in Healthy Young Adults: A Systematic Review and Meta-Analysis , 2014, Sports Medicine.

[2]  J. Foley The co-ordination and regulation of movements , 1968 .

[3]  P. Stein Neuronal control of turtle hindlimb motor rhythms , 2005, Journal of Comparative Physiology A.

[4]  B. Conway,et al.  The motor cortex drives the muscles during walking in human subjects , 2012, The Journal of physiology.

[5]  J. Nielsen,et al.  Changes in corticospinal drive to spinal motoneurones following tablet‐based practice of manual dexterity , 2016, Physiological reports.

[6]  Emilio Bizzi,et al.  Representation of Muscle Synergies in the Primate Brain , 2015, The Journal of Neuroscience.

[7]  A. Jackson,et al.  Flexible Cortical Control of Task-Specific Muscle Synergies , 2012, The Journal of Neuroscience.

[8]  Y. Prut,et al.  Do sensorimotor β-oscillations maintain muscle synergy representations in primary motor cortex? , 2015, Trends in Neurosciences.

[9]  Emilio Bizzi,et al.  Combinations of muscle synergies in the construction of a natural motor behavior , 2003, Nature Neuroscience.

[10]  M. Lemay,et al.  Modularity of motor output evoked by intraspinal microstimulation in cats. , 2004, Journal of neurophysiology.

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

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

[13]  J. Lundbye-Jensen,et al.  Changes in corticospinal drive to spinal motoneurones following visuo‐motor skill learning in humans , 2006, The Journal of physiology.

[14]  H. Sebastian Seung,et al.  Algorithms for Non-negative Matrix Factorization , 2000, NIPS.

[15]  J. V. van Dieën,et al.  Learning to balance on one leg: motor strategy and sensory weighting. , 2015, Journal of neurophysiology.

[16]  Francisco J. Valero Cuevas,et al.  Beta Band Corticomuscular Drive Reflects Muscle Coordination Strategies , 2017, Front. Comput. Neurosci..

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

[18]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[19]  Andreas Daffertshofer,et al.  Neural synchrony within the motor system: what have we learned so far? , 2012, Front. Hum. Neurosci..

[20]  Marie-Claude Hepp-Reymond,et al.  Gamma-range corticomuscular coherence during dynamic force output , 2007, NeuroImage.

[21]  Stuart N Baker,et al.  Contributions of descending and ascending pathways to corticomuscular coherence in humans , 2011, The Journal of physiology.

[22]  E. M. Pinches,et al.  The role of synchrony and oscillations in the motor output , 1999, Experimental Brain Research.

[23]  Marie-Claude Hepp-Reymond,et al.  Absence of gamma-range corticomuscular coherence during dynamic force in a deafferented patient. , 2008, Journal of neurophysiology.

[24]  R. Lemon Descending pathways in motor control. , 2008, Annual review of neuroscience.

[25]  S. Swinnen,et al.  Understanding bimanual coordination across small time scales from an electrophysiological perspective , 2014, Neuroscience & Biobehavioral Reviews.

[26]  S. Grillner,et al.  On the central generation of locomotion in the low spinal cat , 1979, Experimental Brain Research.

[27]  P. Brown Cortical drives to human muscle: the Piper and related rhythms , 2000, Progress in Neurobiology.

[28]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[29]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[30]  M. Hallett,et al.  Electroencephalographic analysis of cortico-muscular coherence: reference effect, volume conduction and generator mechanism , 1999, Clinical Neurophysiology.

[31]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[32]  A. d’Avella,et al.  Locomotor Primitives in Newborn Babies and Their Development , 2011, Science.

[33]  Michael Breakspear,et al.  Neural mechanisms of intermuscular coherence: implications for the rectification of surface electromyography. , 2012, Journal of neurophysiology.

[34]  Emilio Bizzi,et al.  The neural origin of muscle synergies , 2013, Front. Comput. Neurosci..

[35]  Richard R Neptune,et al.  Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke. , 2010, Journal of neurophysiology.

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

[37]  Christoph M. Michel,et al.  Head model and electrical source imaging: A study of 38 epileptic patients☆ , 2014, NeuroImage: Clinical.

[38]  Lena H Ting,et al.  Dimensional reduction in sensorimotor systems: a framework for understanding muscle coordination of posture. , 2007, Progress in brain research.

[39]  B. Freriks,et al.  Development of recommendations for SEMG sensors and sensor placement procedures. , 2000, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[40]  E. Bizzi,et al.  Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. , 2001, Journal of neurophysiology.

[41]  Silvestro Micera,et al.  EEG topographies provide subject-specific correlates of motor control , 2017, Scientific Reports.

[42]  J. Schoffelen,et al.  Neuronal Coherence as a Mechanism of Effective Corticospinal Interaction , 2005, Science.

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

[44]  M. Tresch,et al.  The case for and against muscle synergies , 2022 .

[45]  M. Schieber Training and Synchrony in the Motor System , 2002, The Journal of Neuroscience.

[46]  Jose Luis Patino,et al.  Beta-range cortical motor spectral power and corticomuscular coherence as a mechanism for effective corticospinal interaction during steady-state motor output , 2007, NeuroImage.

[47]  Frank Huethe,et al.  Corticomuscular coherence reflects interindividual differences in the state of the corticomuscular network during low-level static and dynamic forces. , 2012, Cerebral cortex.

[48]  S. Scott The role of primary motor cortex in goal-directed movements: insights from neurophysiological studies on non-human primates , 2003, Current Opinion in Neurobiology.

[49]  Bernadette C. M. van Wijk,et al.  Corticomuscular and bilateral EMG coherence reflect distinct aspects of neural synchronization , 2009, Neuroscience Letters.

[50]  Andreas Daffertshofer,et al.  Functional connectivity in the neuromuscular system underlying bimanual coordination. , 2016, Journal of neurophysiology.

[51]  T. Hortobágyi,et al.  Erratum to: Dose-Response Relationships of Balance Training in Healthy Young Adults: A Systematic Review and Meta-Analysis , 2015, Sports Medicine.

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

[53]  S. Grillner Neurobiological bases of rhythmic motor acts in vertebrates. , 1985, Science.