Propagating waves of local field potentials in motor cortex and their relations to unit spiking activities and motor behavior

Kazutaka Takahashi

University of Chicago, USA

High-frequency oscillations in the beta range (10-45 Hz) are most active in motor cortex during motor preparation and are postulated to reflect the steady postural state or global attentive state of the animal. By simultaneously recorded multiple local field potential (LFP) signals across the primary motor cortex of monkeys (Macaca mulatta) trained to perform an instructed-delay reaching task and a random pursuit target (RTP) task, we found that these oscillations propagated as waves across the surface of the motor cortex along dominant spatial axes characteristic of the local circuitry of the motor cortex under both tasks. Moreover, during the RPT task we preliminary found that the spiking activity of a class of neurons, classified based on the widths of spike waveform, in motor cortical ensembles also exhibit a tendency to propagate as planar waves with statistical properties similar to that of the LFP waves. An evoked LFP for each channel was obtained by averaging LFP signals around each target hit that triggered the next target appearance over all successful target hits. An evoked spike response for each unit was also obtained by binning spike counts into 1 ms bins ranging over the same time window as that for the evoked LFPs. We found that both evoked LFPs and evoked spike rates in the beta frequency range propagate transiently as waves across both cortical areas for ~100-150 ms after the target hit. Furthermore, the distribution of propagation directions of the LFP and spike waves were found to be similar to each other. These results suggest that both aggregate synaptic inputs and spiking outputs share common spatiotemporal structure in motor cortex. Furthermore, we found that at each stable LFP wave occurrence the speed of an LFP wave and the hand speed were correlated with a certain lag range. This may indicate that a cortical LFP wave speed may be a measure of the speed of the recruitment of neurons for an upcoming movement speed. In conclusion, we showed for the first time in cortex that copropagation of evoked planar waves of LFP and spike rates of a certain class of neurons. Furthermore, a relation between individual stable LFP wave speed and hand speed was found to be weakly linear. This speed relation was found only over a certain range of lag. Taken together, the spatiotemporal dynamics in motor cortex integrates the relation among LFP, spiking activities of a class of neurons, and behavioral output.

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