Distinct sensorimotor feedback loops for dynamic and static control of primate precision grip

Volitional limb motor control involves dynamic and static muscle actions. It remains elusive how such distinct actions are controlled through separated or shared neural circuits. Here we explored the potential separation for dynamic and static controls in primate hand actions, by investigating the neuronal coherence between local field potentials (LFPs) of the spinal cord and the forelimb electromyographic activity (EMGs), and LFPs of the motor cortex and the EMGs during the performance of a precision grip in macaque monkeys. We observed the emergence of beta-range coherence with EMGs at spinal cord and motor cortex in the separated phases; spinal coherence during the grip phase and cortical coherence during the hold phase. Further, both of the coherences were influenced by bidirectional interactions with reasonable latencies as beta oscillatory cycles. These results indicate that dedicated feedback circuits comprising spinal and cortical structures underlie dynamic and static controls of dexterous hand actions. Using a precision grip model in macaque monkeys, Oya, Takei et al. show that the emergence of beta-range coherence with the forelimb electromyographic activity at spinal cord and motor cortex in separate phases. This study suggests that dedicated feedback circuits comprising spinal and cortical structures underlie dynamic and static controls of hand actions.

[1]  David A. Robinson,et al.  Models of the saccadic eye movement control system , 1973, Kybernetik.

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

[3]  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.

[4]  Herman van der Kooij,et al.  Face to phase: pitfalls in time delay estimation from coherency phase , 2013, Journal of Computational Neuroscience.

[5]  Stuart N Baker,et al.  Synchronization in monkey motor cortex during a precision grip task. II. effect of oscillatory activity on corticospinal output. , 2003, Journal of neurophysiology.

[6]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[7]  R. Lemon Recent advances in our understanding of the primate corticospinal system , 2019, F1000Research.

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

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

[10]  B. Conway,et al.  Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. , 1995, The Journal of physiology.

[11]  E. Fetz,et al.  Response patterns and force relations of monkey spinal interneurons during active wrist movement. , 1998, Journal of neurophysiology.

[12]  E. Todorov Optimality principles in sensorimotor control , 2004, Nature Neuroscience.

[13]  Yoshikazu Isomura,et al.  Directional organization of sensorimotor oscillatory activity related to the electromyogram in the monkey , 2009, Clinical Neurophysiology.

[14]  Stuart N Baker,et al.  Cells in somatosensory areas show synchrony with beta oscillations in monkey motor cortex , 2007, The European journal of neuroscience.

[15]  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.

[16]  Radford M. Neal Pattern Recognition and Machine Learning , 2007, Technometrics.

[17]  H. Freund,et al.  Cortico‐muscular synchronization during isometric muscle contraction in humans as revealed by magnetoencephalography , 2000, The Journal of physiology.

[18]  R N Lemon,et al.  A novel algorithm to remove electrical cross‐talk between surface EMG recordings and its application to the measurement of short‐term synchronisation in humans , 2002, The Journal of physiology.

[19]  Steven W. Smith,et al.  The Scientist and Engineer's Guide to Digital Signal Processing , 1997 .

[20]  J. Kalaska,et al.  Differential relation of discharge in primary motor cortex and premotor cortex to movements versus actively maintained postures during a reaching task , 1996, Experimental Brain Research.

[21]  K. J. Cole,et al.  Autogenic and nonautogenic sensorimotor actions in the control of multiarticulate hand movements , 2004, Experimental Brain Research.

[22]  R N Lemon,et al.  Synchronization in monkey motor cortex during a precision grip task. I. Task-dependent modulation in single-unit synchrony. , 2001, Journal of neurophysiology.

[23]  Stuart N. Baker,et al.  Convergence of Pyramidal and Medial Brain Stem Descending Pathways Onto Macaque Cervical Spinal Interneurons , 2010, Journal of neurophysiology.

[24]  J. Andrew Pruszynski,et al.  Primary motor cortex underlies multi-joint integration for fast feedback control , 2011, Nature.

[25]  Uri Shalit,et al.  Descending systems translate transient cortical commands into a sustained muscle activation signal. , 2012, Cerebral cortex.

[26]  Alfred C Schouten,et al.  Directional coherence disentangles causality within the sensorimotor loop, but cannot open the loop , 2012, The Journal of physiology.

[27]  R. Hari,et al.  Cortical control of human motoneuron firing during isometric contraction. , 1997, Journal of neurophysiology.

[28]  Luiz A. Baccalá,et al.  Partial directed coherence: a new concept in neural structure determination , 2001, Biological Cybernetics.

[29]  E E Fetz,et al.  Corticomotoneuronal cells contribute to long‐latency stretch reflexes in the rhesus monkey. , 1984, The Journal of physiology.

[30]  P. Strick,et al.  Subdivisions of primary motor cortex based on cortico-motoneuronal cells , 2009, Proceedings of the National Academy of Sciences.

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

[32]  E. Olivier,et al.  Coherent oscillations in monkey motor cortex and hand muscle EMG show task‐dependent modulation , 1997, The Journal of physiology.

[33]  Ingeborg Krägeloh-Mann,et al.  Coherent corticomuscular oscillations originate from primary motor cortex: Evidence from patients with early brain lesions , 2006, Human brain mapping.

[34]  J. Valls-Solé The circuitry of the human spinal cord: Its role in motor control and movement disorders Pierrot-Deseilligny E, Burke D, editors. Hardback. Cambridge University Press; 2005. 642 p. [ISBN: 13978052182581]. , 2008, Clinical Neurophysiology.

[35]  Arnold Neumaier,et al.  Algorithm 808: ARfit—a matlab package for the estimation of parameters and eigenmodes of multivariate autoregressive models , 2001, TOMS.

[36]  S. Bressler,et al.  Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[37]  V. Jousmäki,et al.  Task‐dependent modulation of 15‐30 Hz coherence between rectified EMGs from human hand and forearm muscles , 1999, The Journal of physiology.

[38]  Yifat Prut,et al.  Firing Properties of Spinal Interneurons during Voluntary Movement. II. Interactions between Spinal Neurons , 2003, The Journal of Neuroscience.

[39]  S. Scott,et al.  Random change in cortical load representation suggests distinct control of posture and movement , 2005, Nature Neuroscience.

[40]  J. Schoffelen,et al.  Nonparametric statistical testing of coherence differences , 2007, Journal of Neuroscience Methods.

[41]  Stephen H Scott,et al.  Long-latency responses during reaching account for the mechanical interaction between the shoulder and elbow joints. , 2009, Journal of neurophysiology.

[42]  L. Pinneo On noise in the nervous system. , 1966, Psychological review.

[43]  K. Seki,et al.  Spinomuscular coherence in monkey performing a precision grip task , 2007, Neuroscience Research.

[44]  D. Hoffman,et al.  Corticomotoneuronal cells are “functionally tuned” , 2015, Science.

[45]  K. Seki,et al.  Spinomuscular coherence in monkeys performing a precision grip task. , 2008, Journal of neurophysiology.

[46]  Daniel M. Wolpert,et al.  Signal-dependent noise determines motor planning , 1998, Nature.

[47]  Katarzyna J. Blinowska,et al.  A new method of the description of the information flow in the brain structures , 1991, Biological Cybernetics.

[48]  Dewen Hu,et al.  Hemodynamic and electrophysiological spontaneous low-frequency oscillations in the cortex: Directional influences revealed by Granger causality , 2014, NeuroImage.

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

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

[51]  Reza Shadmehr,et al.  Distinct neural circuits for control of movement vs. holding still. , 2017, Journal of neurophysiology.

[52]  H. Kornhuber,et al.  Natural and drug-induced variations of velocity and duration of human saccadic eye movements: Evidence for a control of the neural pulse generator by local feedback , 2004, Biological Cybernetics.

[53]  Kazuhiko Seki,et al.  Spinal Premotor Interneurons Mediate Dynamic and Static Motor Commands for Precision Grip in Monkeys , 2013, The Journal of Neuroscience.

[54]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[55]  Nikhil V. Divekar,et al.  Neurophysiological, behavioural and perceptual differences between wrist flexion and extension related to sensorimotor monitoring as shown by corticomuscular coherence , 2013, Clinical Neurophysiology.

[56]  R. Lemon,et al.  The influence of single monkey cortico‐motoneuronal cells at different levels of activity in target muscles. , 1994, The Journal of physiology.

[57]  R. Lemon,et al.  Contribution of the monkey corticomotoneuronal system to the control of force in precision grip. , 1993, Journal of neurophysiology.

[58]  A. M. Smith,et al.  Relation of activity in precentral cortical neurons to force and rate of force change during isometric contractions of finger muscles , 1975, Experimental Brain Research.

[59]  Stephen H. Scott,et al.  A Functional Taxonomy of Bottom-Up Sensory Feedback Processing for Motor Actions , 2016, Trends in Neurosciences.

[60]  Kazuhiko Seki,et al.  Synaptic and functional linkages between spinal premotor interneurons and hand-muscle activity during precision grip , 2013, Front. Comput. Neurosci..

[61]  J. A. Pruszynski,et al.  Optimal feedback control and the long-latency stretch response , 2012, Experimental Brain Research.

[62]  Stuart N Baker,et al.  Afferent encoding of central oscillations in the monkey arm. , 2006, Journal of neurophysiology.

[63]  E. Fetz,et al.  Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. , 1996, Journal of neurophysiology.

[64]  William A. MacKay,et al.  Synchronized neuronal oscillations and their role in motor processes , 1997, Trends in Cognitive Sciences.

[65]  A. Aertsen,et al.  Spike synchronization and rate modulation differentially involved in motor cortical function. , 1997, Science.

[66]  S. Scott The computational and neural basis of voluntary motor control and planning , 2012, Trends in Cognitive Sciences.

[67]  S. Votaw,et al.  Roles of primate spinal interneurons in preparation and execution of voluntary hand movement , 2002, Brain Research Reviews.