Reading and Modulating Cortical β Bursts from Motor Unit Spiking Activity

• Published in: The Journal of neuroscience Vol. 42; no. 17; pp. 3611 - 3621
• Main Authors: Bräcklein, Mario, Barsakcioglu, Deren Y., Del Vecchio, Alessandro, Ibáñez, Jaime, Farina, Dario
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 27.04.2022
• Subjects: Beta Rhythm - physiology; Bursts; Central nervous system; Electromyography; Female; Firing pattern; Humans; Interfaces; Isometric Contraction - physiology; Learning; Male; Muscle contraction; Muscle, Skeletal - physiology; Muscles; Nervous system; Operant conditioning; Oscillations; Skeletal muscle; Tibialis anterior muscle; neural interfaces; real-time decomposition; neural oscillations; motor units; β oscillations
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.1885-21.2022

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.