Edinburgh Research Explorer Dissociation between sustained single-neuron spiking rhythmicity and transient -LFP oscillations in primate motor cortex

Determining the relationship between single-neuron spiking and transient ( ∼ 20 Hz) beta local 21 field potential (β-LFP) oscillations is an important step for understanding the role of these oscillations 22 in motor cortex. We show that while motor cortex firing rates and beta spiking rhythmicity remain 23 sustained during steady-state movement preparation periods, β-LFP oscillations emerge, in contrast, 24 as short transient events. Single-neuron mean firing rates within and outside transient β-LFP events 25 showed no differences, and no consistent correlation was found between the beta oscillations’ amplitude 26 and firing rates, as was the case for movement and visual-cue related β-LFP suppression. Importantly, 27 well-isolated single units featuring beta-rhythmic spiking (43%, 125/292) showed no apparent or only 28 weak phase-coupling with the transient β-LFP oscillations. Similar results were obtained for the 29 population spiking. These findings were common in triple microelectrode-array recordings from 30 primary motor (M1), ventral (PMv) and dorsal (PMd) premotor cortices in non-human primates 31 during movement preparation. Although beta spiking rhythmicity indicates strong membrane potential 32 fluctuations in the beta band, it does not imply strong phase coupling with β-LFP oscillations. The 33 observed dissociation points to two different sources of variation in motor cortex β-LFPs: one that 34 impacts single-neuron spiking dynamics, and another related to the generation of mesoscopic β-LFP 35 signals. Furthermore, our findings indicate that rhythmic spiking and diverse neuronal firing rates, 36 which encode planned actions during movement preparation, may naturally limit the ability of different 37 neuronal populations to strongly phase-couple to a single dominant oscillation frequency, leading to 38 the observed spiking and β-LFP dissociation. was computed on the +-5 433 Hz band around β-LFP peak (multi-taper PSD, 10 Hz bandwidth). We used linear discriminant analysis (LDA) with leave-one-out cross validation. Chance levels and p-values were determined by sampling 435 from a null hypothesis distribution generated by randomly permuting the grip and object labels for each 436 trial. We have found no statistically significant classification (p-values > 0.05) of the object or upcoming 437 grip movement from β-LFP power during the examined steady-state movement preparation periods. We examined the possibility that the phase coupling between spiking and the transient β-LFP oscillations could be too weak to be detected, but much stronger if assessed at the level of the population spiking activity. Population spiking activity was defined here as the total number of spikes (1 ms time bins) summed across the well-isolated single units within a given motor area, smoothed by a 25 ms boxcar 443 filter (Methods). For each motor area we computed the cross-correlation function between the population 444 spiking activity and the β-LFP averaged across the channels in the area. Cross-correlation functions 445 were computed for time lags ranging over one beta cycle ( ± 25 ms). A cross-correlation function was 446 computed for each area, epoch, session and subject. 447 Our findings contribute the of the statistical properties of signals recorded via