Dissociation between sustained single-neuron spiking and transient β-LFP oscillations in primate motor cortex

Determining the relationship between single-neuron spiking and transient (20 Hz) beta-local field potential (beta-LFP) oscillations is an important step for understanding the role of these oscillations in motor cortex. We show that whereas motor cortex firing rates and beta spiking rhythmicity remain sustained during steady-state movement preparation periods,beta-LFP oscillations emerge, in contrast, as short transient events. Single-neuron mean firing rates within and outside transient beta-LFP events showed no differences, and no consistent correlation was found between the beta oscillation amplitude and firing rates, as was the case for movement- and visual cue-related beta-LFP suppression. Importantly, well-isolated single units featuring beta-rhythmic spiking (43%, 125/292) showed no apparent or only weak phase coupling with the transient beta-LFP oscillations. Similar results were obtained for the population spiking. These findings were common in triple microelectrode array recordings from primary motor (M1), ventral (PMv), and dorsal premotor (PMd) cortices in nonhuman primates during movement preparation. Although beta spiking rhythmicity indicates strong membrane potential fluctuations in the beta band, it does not imply strong phase coupling with beta-LFP oscillations. The observed dissociation points to two different sources of variation in motor cortex beta-LFPs: one that impacts single- neuron spiking dynamics and another related to the generation of mesoscopic beta-LFP signals. Furthermore, our findings indicate that rhythmic spiking and diverse neuronal firing rates, which encode planned actions during movement preparation, may naturally limit the ability of different neuronal populations to strongly phase-couple to a single dominant oscillation frequency, leading to the observed spiking and beta-LFP dissociation. NEW & NOTEWORTHY We show that whereas motor cortex spiking rates and beta (similar to 20 Hz) spiking rhythmicity remain sustained during steady-state movement preparation periods, beta-local field potential (beta-LFP) oscillations emerge, in contrast, as transient events. Furthermore, the beta-LFP phase at which neurons spike drifts: phase coupling is typically weak or absent. This dissociation points to two sources of variation in the level of motor cortex beta: one that impacts single- neuron spiking and and another related to the generation of measured mesoscopic beta-LFPs.