The role of synchrony and oscillations in the motor output

Abstract There is currently much interest in the synchronisation of neural discharge and the potential role it may play in information coding within the nervous system. We describe some recent results from investigations of synchronisation within the motor system. Local field potentials (LFPs) and identified pyramidal tract neurones (PTNs) were recorded from the primary motor cortex of monkeys trained to perform a precision grip task. The LFPs showed bursts of oscillatory activity at 20–30 Hz, which were coherent with the rectified electromyographs (EMG) of contralateral hand and forearm muscles. This oscillatory synchronisation showed a highly specific task dependence, being present only during the part of the task when the animal maintained a steady grip and not during the movement phases before or after it. PTNs were phase-locked to LFP oscillations, implying that at least part of the coherence between cortical activity and EMG was mediated by corticospinal fibres. The phase locking of the PTNs to LFP oscillations produced task-dependent oscillatory synchronisation between PTN pairs, as assessed by the single-unit cross-correlation histogram. Recordings were also made from normal human subjects performing a precision grip similar to that used in the monkey recordings. Pairs of EMGs recorded from intrinsic hand and forearm muscles showed 20–30 Hz coherence, which modulated during task performance, being present only during periods of steady contraction. We suggest that these changes in EMG-EMG synchronisation reflect changing levels of synchronous drive from the corticospinal system. The generation of oscillations in the cortex is discussed in the light of results from a model of local cortical circuits. Other modelling work has shown that synchrony in the corticospinal inputs could act to recruit motoneurones more efficiently, producing more output force from a muscle than asynchronous inputs firing at the same mean rate. A speculative hypothesis is presented on the role of synchronous oscillations in the motor system, which is consistent with experimental observations to date.

[1]  E. Adrian,et al.  THE BERGER RHYTHM: POTENTIAL CHANGES FROM THE OCCIPITAL LOBES IN MAN , 1934 .

[2]  W PENFIELD,et al.  Mechanisms of voluntary movement. , 1954, Brain : a journal of neurology.

[3]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. I. The single spike train. , 1967, Biophysical journal.

[4]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[5]  E. Evarts,et al.  Relation of pyramidal tract activity to force exerted during voluntary movement. , 1968, Journal of neurophysiology.

[6]  E. Fetz,et al.  Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. , 1980, Journal of neurophysiology.

[7]  E. Fetz,et al.  Functional classes of primate corticomotoneuronal cells and their relation to active force. , 1980, Journal of neurophysiology.

[8]  George L. Gerstein,et al.  Design of a laboratory for multineuron studies , 1983, IEEE Transactions on Systems, Man, and Cybernetics.

[9]  G. Loeb,et al.  R. Lemon , 1985, Neuroscience.

[10]  R. Lemon,et al.  Corticospinal facilitation of hand muscles during voluntary movement in the conscious monkey. , 1986, The Journal of physiology.

[11]  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.

[12]  J. Eggermont.  The Correlative Brain: Theory and Experiment in Neural Interaction , 1990 .

[13]  Jos J. Eggermont.  The Correlative Brain , 1990 .

[14]  P König,et al.  Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Christof Koch,et al.  Cortical Cells Should Fire Regularly, But Do Not , 1999, Neural Computation.

[16]  G. Pfurtscheller,et al.  Simultaneous EEG 10 Hz desynchronization and 40 Hz synchronization during finger movements. , 1992, Neuroreport.

[17]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[18]  R. Eckhorn,et al.  A new method for the insertion of multiple microprobes into neural and muscular tissue, including fiber electrodes, fine wires, needles and microsensors , 1993, Journal of Neuroscience Methods.

[19]  J. Wessberg,et al.  Organization of motor output in slow finger movements in man. , 1993, The Journal of physiology.

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

[21]  R. Porter,et al.  Corticospinal Function and Voluntary Movement , 1993 .

[22]  E. Vaadia,et al.  Spatiotemporal firing patterns in the frontal cortex of behaving monkeys. , 1993, Journal of neurophysiology.

[23]  Conrad V. Kufta,et al.  Event-related desynchronization and movement-related cortical potentials on the ECoG and EEG. , 1994, Electroencephalography and clinical neurophysiology.

[24]  William R. Softky,et al.  Sub-millisecond coincidence detection in active dendritic trees , 1994, Neuroscience.

[25]  R. Hari,et al.  Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement , 1994, Neuroscience.

[26]  T J Ebner,et al.  8-12 Hz rhythmic oscillations in human motor cortex during two-dimensional arm movements: evidence for representation of kinematic parameters. , 1994, Electroencephalography and clinical neurophysiology.

[27]  Eberhard E. Fetz,et al.  Effects of Input Synchrony on the Firing Rate of a Three-Conductance Cortical Neuron Model , 1994, Neural Computation.

[28]  Michael N. Shadlen,et al.  Noise, neural codes and cortical organization , 1994, Current Opinion in Neurobiology.

[29]  O. Prospero-Garcia,et al.  Reliability of Spike Timing in Neocortical Neurons , 1995 .

[30]  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.

[31]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[32]  G. Pfurtscheller,et al.  Human cortical 40 Hz rhythm is closely related to EMG rhythmicity , 1996, Neuroscience Letters.

[33]  C. Gray,et al.  Chattering Cells: Superficial Pyramidal Neurons Contributing to the Generation of Synchronous Oscillations in the Visual Cortex , 1996, Science.

[34]  Christof Koch,et al.  Temporal Precision of Spike Trains in Extrastriate Cortex of the Behaving Macaque Monkey , 1999, Neural Computation.

[35]  G. Pfurtscheller,et al.  Post-movement beta synchronization. A correlate of an idling motor area? , 1996, Electroencephalography and clinical neurophysiology.

[36]  G. Deuschl,et al.  Clinical neurophysiology of tremor. , 1996, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[37]  Muscle sound during wrist movements in patients with Parkinson's disease , 1996 .

[38]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[39]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

[40]  E. Fetz,et al.  Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. , 1996, Journal of neurophysiology.

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

[42]  G. Buzsáki,et al.  Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. , 1996, The Journal of physiology.

[43]  G. Pfurtscheller,et al.  The effects of external load on movement-related changes of the sensorimotor EEG rhythms. , 1997, Electroencephalography and clinical neurophysiology.

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

[45]  Quantitative assessment of phase locking in discharge of identified pyramidal tract neurones during 25 Hz oscillations in monkey motor cortex , 1997 .

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

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

[48]  C. Marsden,et al.  Frequency peaks of tremor, muscle vibration and electromyographic activity at 10 Hz, 20 Hz and 40 Hz during human finger muscle contraction may reflect rhythmicities of central neural firing , 1997, Experimental Brain Research.

[49]  G. Pfurtscheller,et al.  On the existence of different types of central beta rhythms below 30 Hz. , 1997, Electroencephalography and clinical neurophysiology.

[50]  J. Donoghue,et al.  Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. , 1998, Journal of neurophysiology.

[51]  Ehud Ahissar,et al.  Temporal-Code to Rate-Code Conversion by Neuronal Phase-Locked Loops , 1998, Neural Computation.

[52]  S. Baker,et al.  Computer simulation of post-spike facilitation in spike-triggered averages of rectified EMG. , 1998, Journal of neurophysiology.

[53]  J. R. Rosenberg,et al.  Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans , 1998, Neuroscience Letters.

[54]  M. Hallett,et al.  Task-related coherence and task-related spectral power changes during sequential finger movements. , 1998, Electroencephalography and clinical neurophysiology.

[55]  S N Baker,et al.  Emergent oscillations in a realistic network: the role of inhibition and the effect of the spatiotemporal distribution of the input. , 1999, Journal of computational neuroscience.