Reading and Modulating Cortical β Bursts from Motor Unit Spiking Activity

Abstract

β Oscillations (13–30 Hz) are ubiquitous in the human motor nervous system. Yet, their origins and roles are unknown. Traditionally, β activity has been treated as a stationary signal. However, recent studies observed that cortical β occurs in “bursting events,” which are transmitted to muscles. This short-lived nature of β events makes it possible to study the main mechanism of β activity found in the muscles in relation to cortical β. Here, we assessed whether muscle β activity mainly results from cortical projections. We ran two experiments in healthy humans of both sexes ( N = 15 and N = 13, respectively) to characterize β activity at the cortical and motor unit (MU) levels during isometric contractions of the tibialis anterior muscle. We found that β rhythms observed at the cortical and MU levels are indeed in bursts. These bursts appeared to be time-locked and had comparable average durations (40–80 ms) and rates (approximately three to four bursts per second). To further confirm that cortical and MU β have the same source, we used a novel operant conditioning framework to allow subjects to volitionally modulate MU β. We showed that volitional modulation of β activity at the MU level was possible with minimal subject learning and was paralleled by similar changes in cortical β activity. These results support the hypothesis that MU β mainly results from cortical projections. Moreover, they demonstrate the possibility to decode cortical β activity from MU recordings, with a potential translation to future neural interfaces that use peripheral information to identify and modulate activity in the central nervous system. SIGNIFICANCE STATEMENT We show for the first time that β activity in motor unit (MU) populations occurs in bursting events. These bursts observed in the output of the spinal cord appear to be time-locked and share similar characteristics of β activity at the cortical level, such as the duration and rate at which they occur. Moreover, when subjects were exposed to a novel operant conditioning paradigm and modulated MU β activity, cortical β activity changed in a similar way as peripheral β. These results provide evidence for a strong correspondence between cortical and peripheral β activity, demonstrating the cortical origin of peripheral β and opening the pathway for a new generation of neural interfaces.

The control and training of single motor units in isometric tasks are constrained by a common input signal

“…One possible strategy consistent with such state-dependent control of individual MUs could be relying on an input signal to MUs not directly linked to motor function and non-homogeneously distributed among the MU pool. For example, cortical oscillations could meet these criteria if descending projections of this activity to large and small MUs in a pool differed ( Ibáñez et al, 2021 ; Bräcklein et al, 2021 ; Bräcklein et al, 2022 ). A different alternative that may allow for flexible MU control after initial recruitment is volitional modulation of reciprocal inhibition ( Chen et al, 2006 ; Thompson et al, 2013 ) presumably via direct descending commands ( Jankowska, 1992 ; Nielsen et al, 1995 ).…”

“…Here, we extracted single MU activity from the TA since this muscle has properties (e.g. muscle fibres arrangement, proximity to the skin, distribution of innervation zones) that facilitate a reliable decomposition of MU activity using surface recordings ( Barsakcioglu et al, 2021 ; Bräcklein et al, 2021 ; Bräcklein et al, 2022 ; Negro et al, 2016a ; Dideriksen et al, 2018 ; Del Vecchio et al, 2020 ) and a relatively large number of monosynaptic connections with the motor cortex that could potentially be leveraged for direct independent MU control ( Ibáñez et al, 2021 ; Dideriksen et al, 2018 ). Our results strongly suggest that subjects do not tend to find or opt for a control strategy that relies on flexible MU recruitment order under constraint isometric conditions.…”

Mental fatigue impairs physical performance but not the neural drive to the muscle

“…COHalpha represents the common synaptic input in the alpha band (5–12 Hz), which is usually associated to afferent feedback (Mehrkanoon et al ., 2014). COHbeta represents the common synaptic input in the beta band (15-30 Hz), which is associated to descending inputs from motor cortex during isometric contractions of weak to moderate strength (Brown, 2000; Bräcklein et al ., 2022) as performed in the present study. COHpiper represents the common synaptic input at 40-50 Hz, which is associated to descending inputs from motor cortex during strong isometric contractions or during dynamic movement (Brown, 2000).…”

“…To our knowledge, the effects of MF induced by an acute cognitive task on subsequent muscle endurance, motor unit activity and common inputs to motoneurons have not been explored. This is important since the oscillations carried by the motoneuron have direct link with the motor cortex (Bräcklein et al, 2022) and effective neural drive to the muscle (Farina et al, 2014b), and muscle performance (Del Vecchio et al, 2019a, 2019b.The aim of this study are was to explore the effects of MF on submaximal muscle endurance, RPE and motor unit activity. We hypothesize that MF will impair physical performance while increasing RPE and perceived mental fatigue and reducing the motivation for the subsequent physical task.…”

Measuring the non-selective effects of motor inhibition using isometric force recordings

“…Individual peaks in beta power were detected during single trials, using the imregionalmax Matlab function. A peak in beta power was counted as a burst if its amplitude exceeded 3X the median power for that frequency across all trials, based on methods used in (Bräcklein et al 2022).…”