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Clinical Trial
. 2000 Dec 1;20(23):8838-45.
doi: 10.1523/JNEUROSCI.20-23-08838.2000.

Human cortical muscle coherence is directly related to specific motor parameters

J M Kilner  1 , S N Baker, S Salenius, R Hari, R N Lemon
Affiliations
Clinical Trial

Human cortical muscle coherence is directly related to specific motor parameters

J M Kilner et al. J Neurosci. .

Abstract

Cortical oscillations have been the target of many recent investigations, because it has been proposed that they could function to solve the "binding" problem. In the motor cortex, oscillatory activity has been reported at a variety of frequencies between approximately 4 and approximately 60 Hz. Previous research has shown that 15-30 Hz oscillatory activity in the primary motor cortex is coherent or phase locked to activity in contralateral hand and forearm muscles during isometric contractions. However, the function of this oscillatory activity remains unclear. Is it simply an epiphenomenon or is it related to specific motor parameters? In this study, we investigated task-dependent modulation in coherence between motor cortex and hand muscles during precision grip tasks. Twelve right-handed subjects used index finger and thumb to grip two levers that were under robotic control. Each lever was fitted with a sensitive force gauge. Subjects received visual feedback of lever force levels and were instructed to keep them within target boxes throughout each trial. Surface EMGs were recorded from four hand and forearm muscles, and magnetoencephalography (MEG) was recorded using a 306 channel neuromagnetometer. All subjects showed significant levels of coherence (0.086-0.599) between MEG and muscle in the 15-30 Hz range. Coherence was significantly smaller when the task was performed under an isometric condition (levers fixed) compared with a compliant condition in which subjects moved the levers against a spring-like load. Furthermore, there was a positive, significant relationship between the level of coherence and the degree of lever compliance. These results argue in favor of coherence between cortex and muscle being related to specific parameters of hand motor function.

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Figures

Fig. 1.
Fig. 1.
Averaged data for performance during the precision grip task. A, Schematic of the task showing the forces required to be exerted on the finger and the thumb levers by the subjects. The different phases of the task (Hold 1, Ramp, Hold 2) are indicated, and the ramp phase is highlighted by the pale gray box. B, The force profiles actually recorded from the strain gauge signals for the three conditions in which the levers carried a compliant load (COMP1, COMP2, COMP3) and for the condition in which they were fixed and forces exerted isometrically (ISO). C, The lever position traces calculated from the optical encoder signals for the COMP1, COMP2, COMP3, and ISO tasks. Data for each of these traces were averaged across trials, across subjects, and across levers.
Fig. 2.
Fig. 2.
Single subject data for the COMP1 condition.A, B, Power spectra for MEG signal (A) recorded from a sensor overlying the sensorimotor cortex and the EMG recorded from the 1DI muscle (B), averaged over the whole task and for all trials (n = 75). C, The coherence spectra calculated between the two power spectra shown inA and B. The red lineindicates the 95% significance level. D,E, Frequency versus time power spectra maps for MEG and 1DI EMG activity calculated with respect to the task;below each trace is a schematic of the task.F, Maps of MEG–EMG coherence frequency calculated for the different periods of the precision grip task. The color bar indicates the level of coherence estimated; only values above the 95% significance level are shown. The frequency scale on the ordinate inD applies also to plots E andF.
Fig. 3.
Fig. 3.
Effect of task condition on MEG–EMG coherence.A–D, Coherence frequency versus time maps. Thecolors indicate the percentage of points above significance pooled using the nonparametric method (see Materials and Methods) for data from all nine subjects and four muscles (see color scale bar to the right of D). At any point, 100% would be equal to 36 of 36 points. The levers were most compliant in A (greatest digit displacement required to exert the target force level), and compliance was reduced in the following direction: A, COMP1; B, COMP2;C, COMP3; and D, ISO (no lever movement).E shows the mean percentage of significant points in the 15–30 Hz range for each of the four task conditions with respect to the task (dark blue, COMP1; green, COMP2;red, COMP3; and light blue, ISO). Data for each of these traces were averaged across trials, across muscles, and across subjects. F–K show the same data combined using the parametric method. Below eachcolumn is a schematic of the task.
Fig. 4.
Fig. 4.
Quantitative estimate of the change in MEG–EMG coherence with task condition. Histograms showing differences in coherence in the 15–30 Hz range between task conditions, all expressed relative to the COMP1 condition and plotted for data recorded during the different phases of the task (see Fig. 1A).A, D, and G show the results for Hold 1; B, E, andH show results for Ramp; and C,F, and I show results for Hold 2.A–C show the positive changes summed across all subjects and muscles using the nonparametric method. For each of these plots, the maximum possible number of points greater than significance was 6480. D–F show the same data averaged using the parametric method. G–I show the data for each muscle summed across subjects using the nonparametric method. For each of these plots, the maximum possible number of points greater than significance was 1620.
Fig. 5.
Fig. 5.
Effect of type of movement on MEG–EMG coherence.A, B, Coherence frequency versus time maps. The colors indicate the percentage of points above 95% significance pooled using the nonparametric method across all seven subjects and four muscles (color scale bar to right ofB applies to both maps; at any point, 100% would be equal to 28 of 28 points). A shows the data for the Ramp task, and B shows the data for the Ballistic task.E and F show the mean percentage of significant points in the 15–30 Hz range for Ramp (E) and Ballistic (F;Bal) tasks. Data for each of these traces were averaged across trials, across muscles, and across subjects.C, D, G, andH show the same data for the parametric pooling method.I and J show the schematic of the two tasks; the horizontal bars indicate the periods of the task from which data were used for statistical testing (see K;H1, Hold 1; H2, Hold 2). Kshows the number of points above 95% significance summed over the 15–30 Hz range and the periods marked in I andJ. Maximum number of points was 5040. NS, Not significant (p > 0.05, corrected); * indicates significance (p < 0.05, corrected).
Fig. 6.
Fig. 6.
Comparison of coherence during short versus long precision grips. A, Coherence spectra for MEG–1DI pair for a single subject during the second hold period (solid line) of the standard task, shown schematically inC and averaged from data recorded in 75 successive trials compared with coherence in data recorded during a single long hold period (dashed line) of the Neverending task, which lasted for up to 180 sec shown schematically in D (notebroken time scale). Both tasks were performed under most compliant (COMP1) conditions. B, Coherence spectra for MEG–1DI pair for a single subject during the second hold period averaged across trials (solid line) and during the long hold, Neverending task (dashed line), for the task performed under isometric (ISO) conditions. E, The percentage of points above 95% significance in the 15–30 Hz range for the Hold 2 (filled bar) and Neverending task (open bar) for COMP1 conditions. Fdisplays the same data as E for the ISO task. For bothE and F, 100% would be equal to 532 of 532 points.
Fig. 7.
Fig. 7.
Cortical source analysis of coherent MEG activity.A, B, Single subject data showing the direction and strength of the current dipole on the subject's surface-rendered magnetic resonance image for MEG–1DI EMG coherence during the second hold period for the four task conditions COMP1, COMP2, COMP3, and ISO (A), and the MEG–EMG coherence for the four muscles recorded during the second hold period (B). C shows the distances of the cortical sources of the MEG–1DI coherence spectra during the first hold period relative to those during the second hold period of the task performed under COMP1 conditions. Each point represents a different subject. D, The distance of the sources of the MEG signal with the highest level of coherence signals for MEG–AbPB (×), MEG–FDS (○), and MEG–EDC (⋄) pairs relative to those for the MEG–1DI pair during the second hold period under COMP1 conditions. Each point represents a different subject.E, The distance of cortical sources for the MEG–1DI coherence spectra during Hold 2 under COMP2 (×), COMP3 (○), and ISO (⋄) conditions relative to those for the COMP1 condition. Eachpoint represents a different subject.
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