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. 2006 Oct;27(10):789-98.
doi: 10.1002/hbm.20220.

Coherent corticomuscular oscillations originate from primary motor cortex: evidence from patients with early brain lesions

Christian Gerloff  1 , Christoph Braun, Martin Staudt, Yiwen Li Hegner, Johannes Dichgans, Ingeborg Krägeloh-Mann
Affiliations

Coherent corticomuscular oscillations originate from primary motor cortex: evidence from patients with early brain lesions

Christian Gerloff et al. Hum Brain Mapp. 2006 Oct.

Abstract

Coherent oscillations of neurons in the primary motor cortex (M1) have been shown to be involved in the corticospinal control of muscle activity. This interaction between M1 and muscle can be measured by the analysis of corticomuscular coherence in the beta-frequency range (beta-CMCoh; 14-30 Hz). Largely based on magnetoencephalographic (MEG) source-modeling data, it is widely assumed that beta-CMCoh reflects direct coupling between M1 and muscle. Deafferentation is capable of modulating beta-CMCoh, however, and therefore the influence of reafferent somatosensory signaling and corresponding neuronal activity in the somatosensory cortex (S1) has been unclear. We present transcranial magnetic stimulation (TMS) and MEG data from three adult patients suffering from congenital hemiparesis due to pre- and perinatally acquired lesions of the pyramidal tract. In these patients, interhemispheric reorganization had resulted in relocation of M1 to the contralesional hemisphere, ipsilateral to the paretic hand, whereas S1 had remained in the lesioned hemisphere. This topographic dichotomy allowed for an unequivocal topographic differentiation of M1 and S1 with MEG (which is not possible if M1 and S1 are directly adjacent within one hemisphere). In all patients, beta-CMCoh originated from the contralesional M1, in accordance with the TMS-evoked motor responses, and in contrast to the somatosensory evoked fields (SEFs) for which the sources (N20m) were localized in S1 of the lesioned hemisphere. These data provide direct evidence for the concept that beta-CMCoh reflects the motorcortical efferent drive from M1 to the spinal motoneuron pool and muscle. No evidence was found for a relevant contribution of neuronal activity in S1 to beta-CMCoh.

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Figures

Figure 1
Figure 1
T2‐weighted structural MRI of the three patients (Patients 1–3 from left to right).
Figure 2
Figure 2
Power spectra of muscular and cortical activity for Patient 2. A: Power spectra of MEG activity over the right M1 during precision grip with the nonaffected (left) and paretic (right) hand. Spectra of channels with maximal power representing neuronal activity in M1 are superimposed. B: EMG spectra for grip with the nonaffected (left) and paretic (right) hand. Frequencies from 1–40 Hz are displayed.
Figure 3
Figure 3
Summary of β‐CMCoh and N20m results for the three patients (Patients 1–3 from left to right; paretic hand). A: β‐CMCoh for the ED muscle. Topographic maps are presented in the top row, coherence spectra below. The bipolar configuration of the two current maxima (map) indicates 180‐degree phase reversal of inward and outward currents and facilitates robust modeling of the coherent sources. In other words, the two maxima correspond to “sink” and “source” of the electromagnetic field generated in M1. This configuration is characteristic for data obtained with radial gradiometers (Omega MEG system; VSM, Vancouver, Canada). Coherence spectra are plotted for two representative channels. The horizontal line in the coherence spectral plots denotes the statistical 95% confidence limit. Coherence values above this level are considered significant. B: β‐CMCoh for the APB muscle. Same conventions as in A. C: Topography of the N20m components (upper row) and butterfly plots of the individual evoked magnetic responses (bottom row). The red vertical lines indicate the latency of the map and source reconstruction. In the topographic maps, red corresponds to inward currents, blue to outward currents. For mapping, data were normalized and the units (−50 to 50) are arbitrary.
Figure 4
Figure 4
Summary of β‐CMCoh and N20m source reconstructions coregistered with individual anatomy (structural MRI). A: All sources of corticomuscular coupling (β‐CMCoh) were located in the rolandic region of the contralesional hemisphere. No coherence was detected between muscles of the paretic upper limb and the lesioned hemisphere. The sources are represented by the colored dipoles. The color code is given in the insert on the lower right. B: The generators of the N20m were located in the primary somatosensory cortex (S1) contralateral to the hand stimulated, i.e., the N20m source for the paretic hand was located in the lesioned hemisphere in contrast to the source of β‐CMCoh for the same hand, which was located in the primary motor cortex (M1) of the contralesional hemisphere. Note the clear dissociation of M1 and S1 representations of the paretic upper limb in opposite hemispheres. The location of M1 in the contralesional hemisphere was confirmed by transcranial magnetic stimulation.
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