Muscle responses to motor cortical stimulation: can we get more out of surface electromyography?

It is now close to 40 years since Anthony Barker and colleagues demonstrated that a pulsed magnetic field can be delivered through the scalp to the motor cortex of awake human volunteers and evoke brief movements in a contralateral hand muscle (Barker et al., 1985). Since then, the use of transcranial magnetic stimulation (TMS) to study the human motor cortex and corticospinal pathway has exploded, and TMS has greatly improved our understanding of the neural control of movement across healthy and clinical populations. Motor cortical TMS activates corticospinal cells directly, or indirectly through the activation of intracortical neurons that directly synapse onto these cells, thus generating descending volleys capable of recruiting spinal motoneurones. The near synchronous recruitment of motoneurones causes the activation of muscle fibres and generates a compound muscle action potential conventionally recorded with a single channel of surface electromyography (EMG), i.e. as a motor evoked potential (MEP). Importantly, the MEP provides an index of ‘excitability’ for the entire motor pathway and the size of the MEP is thus influenced by excitability changes at both the motor cortex and the spinal cord. The surface interference EMG signal, i.e. the voltage difference between two electrodes overlying a muscle belly, sums activity of the underlying motor units. Hence, if more motor units are recruited by a TMS pulse, and/or more units fire at the same time in response to the stimulus, the MEP recorded with surface interference EMG will have a larger peak-to-peak amplitude or area. Although the MEP is a useful measure of corticospinal-motoneuronal excitability, it is difficult to identify the individual motor unit action potentials comprising the MEP using a single channel of surface EMG. Motor units have different sizes, recruitment thresholds, conduction velocities along their axons and muscle fibres, and biochemical and twitch characteristics of their muscle fibres, and inputs to a motoneurone pool are non-uniform (Heckman & Enoka, 2012). Consequently, individual motor units across a pool may affect the MEP differently. To this end, intramuscular EMG has a better capacity to identify the recruitment and discharge patterns of individual motor units and has hence been used to study the responses of individual units to motor cortical stimulation. Yet, intramuscular EMG can only identify the activity of a small number of motor units (often only one or two units at a time). Considering that there can be hundreds of motor units for a given muscle, the recruitment and discharge patterns within this small sample of motor units does not always represent the recruitment and discharge patterns of units across an entire motor pool. In more recent years, high-density surface EMG (HDsEMG) has been used to study the firing patterns of a larger sample of voluntarily recruited motor units (Del Vecchio et al., 2020). With HDsEMG, multi-electrode surface arrays sample multi-channel EMG across a sizeable portion of the muscle. HDsEMG recordings are typically analysed offline with specialised decomposition algorithms that identify, track and quantify the firing patterns of individual motor units recruited during voluntary isometric contractions, often identifying tens of motor units at a time. Yet, to date, the combined use of HDsEMG with TMS as a technique to identify the individual discharges of TMS-recruited motor units has been limited by the inability of the decomposition algorithms to reliably identify individual units and their associated firings during the very brief, highly synchronised contractions evoked by motor cortical stimulation. Can we use HDsEMG to study TMS-induced firings of individual motor units?