Corticomuscular synchronization with small and large dynamic force output

BackgroundOver the last few years much research has been devoted to investigating the synchronization between cortical motor and muscular activity as measured by EEG/MEG-EMG coherence. The main focus so far has been on corticomuscular coherence (CMC) during static force condition, for which coherence in beta-range has been described. In contrast, we showed in a recent study [1] that dynamic force condition is accompanied by gamma-range CMC. The modulation of the CMC by various dynamic force amplitudes, however, remained uninvestigated. The present study addresses this question. We examined eight healthy human subjects. EEG and surface EMG were recorded simultaneously. The visuomotor task consisted in isometric compensation for 3 forces (static, small and large dynamic) generated by a manipulandum. The CMC, the cortical EEG spectral power (SP), the EMG SP and the errors in motor performance (as the difference between target and exerted force) were analyzed.ResultsFor the static force condition we found the well-documented, significant beta-range CMC (15–30 Hz) over the contralateral sensorimotor cortex. Gamma-band CMC (30–45 Hz) occurred in both small and large dynamic force conditions without any significant difference between both conditions. Although in some subjects beta-range CMC was observed during both dynamic force conditions no significant difference between conditions could be detected. With respect to the motor performance, the lowest errors were obtained in the static force condition and the highest ones in the dynamic condition with large amplitude. However, when we normalized the magnitude of the errors to the amplitude of the applied force (relative errors) no significant difference between both dynamic conditions was observed.ConclusionThese findings confirm that during dynamic force output the corticomuscular network oscillates at gamma frequencies. Moreover, we show that amplitude modulation of dynamic force has no effect on the gamma CMC in the low force range investigated. We suggest that gamma CMC is rather associated with the internal state of the sensorimotor system as supported by the unchanged relative error between both dynamic conditions.

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

[2]  M. Hepp-Reymond,et al.  Neuronal coding of static force in the primate motor cortex. , 1978, Journal de physiologie.

[3]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[4]  M. Hepp-Reymond,et al.  Sensorimotor cortical control of isometric force in the monkey. , 1989, Progress in brain research.

[5]  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.

[6]  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.

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

[8]  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.

[9]  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.

[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]  D. Tucker,et al.  EEG coherency. I: Statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales. , 1997, Electroencephalography and clinical neurophysiology.

[12]  J. Ashe Force and the motor cortex , 1997, Behavioural Brain Research.

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

[14]  J. Ashe Erratum to “Force and the motor cortex” [Behavioural Brain Research 86 (1997) 1–15] 1 PII of original article: S0166-4328(96)00145-3 1 , 1997, Behavioural Brain Research.

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

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

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

[19]  P. Ashby,et al.  Organization of Cortical Activities Related to Movement in Humans , 2000, The Journal of Neuroscience.

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

[21]  R N Lemon,et al.  Modulation of synchrony between single motor units during precision grip tasks in humans , 2002, The Journal of physiology.

[22]  R. Kristeva-Feige,et al.  Effects of attention and precision of exerted force on beta range EEG-EMG synchronization during a maintained motor contraction task , 2002, Clinical Neurophysiology.

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

[24]  Karl M. Newell,et al.  Perceived effort in force production as reflected in motor-related cortical potentials , 2004, Clinical Neurophysiology.

[25]  Riitta Hari,et al.  Reproducibility of cortex–muscle coherence , 2005, NeuroImage.

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

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

[28]  Stuart N. Baker,et al.  Digit displacement, not object compliance, underlies task dependent modulations in human corticomuscular coherence , 2006, NeuroImage.

[29]  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.

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