Manipulation of peripheral neural feedback loops alters human corticomuscular coherence

Sensorimotor EEG shows ∼20 Hz coherence with contralateral EMG. This could involve efferent and/or afferent components of the sensorimotor loop. We investigated the pathways responsible for coherence genesis by manipulating nervous conduction delays using cooling. Coherence between left sensorimotor EEG and right EMG from three hand and two forearm muscles was assessed in healthy subjects during the hold phase of a precision grip task. The right arm was then cooled to 10°C for ∼90 min, increasing peripheral motor conduction time (PMCT) by ∼35% (assessed by F‐wave latency). EEG and EMG recordings were repeated, and coherence recalculated. Control recordings revealed a heterogeneous subject population. In 6/15 subjects (Group A), the corticomuscular coherence phase increased linearly with frequency, as expected if oscillations were propagated along efferent pathways from cortex to muscle. The mean corticomuscular conduction delay for intrinsic hand muscles calculated from the phase–frequency regression slope was 10.4 ms; this is smaller than the delay expected for conduction over fast corticospinal pathways. In 8/15 subjects (Group B), the phase showed no dependence with frequency. One subject showed both Group A and Group B patterns over different frequency ranges. Following cooling, averaged corticomuscular coherence was decreased in Group A subjects, but unchanged for Group B, even though both groups showed comparable slowing of nervous conduction. The delay calculated from the slope of the phase–frequency regression was increased following cooling. However, the size of this increase was around twice the rise in PMCT measured using the F‐wave (regression slope 2.33, 95% confidence limits 1.30–3.36). Both afferent and efferent peripheral nerves will be slowed by similar amounts following cooling. The change in delay calculated from the coherence phase therefore better matches the rise in total sensorimotor feedback loop time caused by cooling, rather than just the change in the efferent limb. A model of corticomuscular coherence which assumes that only efferent pathways contribute cannot be reconciled to these results. The data rather suggest that afferent feedback pathways may also play a role in the genesis of corticomuscular coherence.

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

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

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

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

[5]  Stuart N Baker,et al.  Task‐dependent intermanual coupling of 8‐Hz discontinuities during slow finger movements , 2003, The European journal of neuroscience.

[6]  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.

[7]  S. Farmer,et al.  Central nervous pathways underlying synchronization of human motor unit firing studied during voluntary contractions. , 1991, The Journal of physiology.

[8]  R. N. Lemon,et al.  Digital nerve anaesthesia decreases EMG-EMG coherence in a human precision grip task , 2002, Experimental Brain Research.

[9]  J. Rothwell,et al.  Cortical correlate of the Piper rhythm in humans. , 1998, Journal of neurophysiology.

[10]  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.

[11]  P. Matthews Long‐latency stretch reflexes of two intrinsic muscles of the human hand analysed by cooling the arm. , 1989, The Journal of physiology.

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

[13]  C. G. Phillips,et al.  The distribution of monosynaptic excitation from the pyramidal tract and from primary spindle afferents to motoneurones of the baboon's hand and forearm , 1968, The Journal of physiology.

[14]  A. E. Schulman,et al.  Electroencephalographic measurement of motor cortex control of muscle activity in humans , 2000, Clinical Neurophysiology.

[15]  E. Olivier,et al.  Comparison of direct and indirect measurements of the central motor conduction time in the monkey , 2002, Clinical Neurophysiology.

[16]  P. Matthews,et al.  Mammalian muscle receptors and their central actions , 1974 .

[17]  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.

[18]  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.

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

[20]  P. Rack,et al.  Different types of tremor in the human thumb. , 1982, The Journal of physiology.

[21]  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.

[22]  O. Lippold Oscillation in the stretch reflex arc and the origin of the rhythmical, 8–12 c/s component of physiological tremor , 1970, The Journal of physiology.

[23]  G Pfurtscheller,et al.  Mu‐rhythm changes in brisk and slow self‐paced finger movements , 1996, Neuroreport.

[24]  Lemon Rn,et al.  Thalamic pathway for rapid afferent input from hand to motor cortex in the monkey [proceedings]. , 1979 .

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

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

[27]  J. R. Rosenberg,et al.  The unilateral and bilateral control of motor unit pairs in the first dorsal interosseous and paraspinal muscles in man , 1999, The Journal of physiology.

[28]  Karl M Newell,et al.  Amplitude changes in the 8–12, 20–25, and 40 Hz oscillations in finger tremor , 2000, Clinical Neurophysiology.

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

[30]  R. Lemon,et al.  Human Cortical Muscle Coherence Is Directly Related to Specific Motor Parameters , 2000, The Journal of Neuroscience.

[31]  F W Cody,et al.  Effects of ischaemia upon reflex electromyographic responses evoked by stretch and vibration in human wrist flexor muscles. , 1987, The Journal of physiology.

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

[33]  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.

[34]  A. Vighetto,et al.  A selective imaging of tinnitus. , 1999, Neuroreport.

[35]  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.

[36]  D. Halliday,et al.  The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. , 1993, The Journal of physiology.

[37]  J. B. Preston,et al.  Classification and response characteristics of muscle spindle afferents in the primate. , 1976, Journal of neurophysiology.

[38]  C. Nicholas Riddle,et al.  The effect of carbamazepine on human corticomuscular coherence , 2004, NeuroImage.

[39]  R. N. Stiles,et al.  Mechanical factors in human tremor frequency. , 1967, Journal of applied physiology.

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