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

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.

The reorganization of corticomuscular coherence during a transition between sensorimotor states

“…This was identical to the time lag that was found in the beta band during static force output. An 11-ms time lag for the beta band is consistent with previously findings, e.g., 15.9 ms (Mima et al, 2000), 9.3 ms (Gerlo↵ et al, 2006) and 7.9 ms (Witham et al, 2011). Similarly, (Scho↵elen et al, 2005) found a positive slope for corticomuscular gamma-band coherence corresponding to a time delay of 7.0 ms.…”

Developmental plasticity connects visual cortex to motoneurons after stroke

“…Persistence of fast-conducting ipsilateral corticospinal projections from the noninfarcted motor cortex, which normally would have been withdrawn during development, 4 and focal corticomuscular coherence over the ipsilateral motor cortex have been demonstrated previously. 6 That the contralateral occipital cortex can also control movement of the paretic hand has not been reported previously in humans or animal models. Therefore, excitation of brainstem motor pathways is an unlikely explanation for our findings, because they lie too far below the scalp to be excited directly and, with the exception of the rubrospinal pathway, which is virtually absent in the human brain, 10 innervate the spinal cord and excite muscles bilaterally.…”

Absence of Gamma-Range Corticomuscular Coherence During Dynamic Force in a Deafferented Patient

“…Although afferent inflow may modulate beta-range CMC, our results reconcile the view that the efferent motor information alone is sufficient to generate beta-band CMC during steady-state force. Recently Gerloff et al (2006), by clearly identifying the primary motor and somatosensory cortex in patients with early brain lesions, also provided evidence that beta-range CMC represents efferent drive from the primary motor and not reafferent feedback processing. This is also in line with Farmer et al (1993), who studied synchronization between single motor units in the first dorsal interosseous muscle of the dominant (right) hand of another deafferented patient (IW) and did not report any FIG.…”