LFP beta amplitude is linked to mesoscopic spatio-temporal phase patterns

Michael Denker,Lyuba Zehl,Markus Diesmann,Alexa Riehle,Sonja Grün,Thomas Brochier,Bjørg E Kilavik

doi:10.1038/s41598-018-22990-7

Abstract

Beta oscillations observed in motor cortical local field potentials (LFPs) recorded on separate electrodes of a multi-electrode array have been shown to exhibit non-zero phase shifts that organize into planar waves. Here, we generalize this concept to additional classes of salient patterns that fully describe the spatial organization of beta oscillations. During a delayed reach-to-grasp task we distinguish planar, synchronized, random, circular, and radial phase patterns in monkey primary motor and dorsal premotor cortices. We observe that patterns correlate with the beta amplitude (envelope): Coherent planar/radial wave propagation accelerates with growing amplitude, and synchronized patterns are observed at largest amplitudes. In contrast, incoherent random or circular patterns are observed almost exclusively when beta is strongly attenuated. The occurrence probability of a particular pattern modulates with behavioral epochs in the same way as beta amplitude: Coherent patterns are more present during movement preparation where amplitudes are large, while incoherent phase patterns are dominant during movement execution where amplitudes are small. Thus, we uncover a trigonal link between the spatial arrangement of beta phases, beta amplitude, and behavior. Together with previous findings, we discuss predictions on the spatio-temporal organization of precisely coordinated spiking on the mesoscopic scale as a function of beta power.

Highlights

The local field potential (LFP) has long served as a readily available brain signal to monitor the average input activity that reaches the neurons in the vicinity of extracellular recording electrodes[1,2,3]
Three monkeys were trained in a delayed reach-to-grasp task (Fig. 1A) in which the animal had to grasp, pull and hold an object using either a side grip (SG) or a precision grip (PG), and either with a low force (LF) or high force (HF), resulting in a total of 4 pseudo-randomly presented trial types
The monkey was first presented with a cue for 300 ms which provided partial prior information either about the grip type (SG or PG) in grip-first trials, or the amount of force (LF or HF) in force-first trials, to be used in the upcoming movement

Summary

Introduction

The local field potential (LFP) has long served as a readily available brain signal to monitor the average input activity that reaches the neurons in the vicinity of extracellular recording electrodes[1,2,3]. LFP signals recorded in motor cortex from electrodes separated by up to several millimeters are typically highly correlated[19], the analysis of the instantaneous phase of the oscillation[20] revealed a non-zero temporal shift between electrodes[21] Such shifts may be expressed by the formation of dynamic spatial patterns propagating along preferred directions across the cortical surface, referred to as traveling waves[22]. Even though an individual beta spindle lasts far longer than the occurrence of a planar wave, their dynamic properties suggest that amplitude and spatial organization of beta activity are correlated This hypothesis is further supported by the finding that when considering data of different trials, both traveling waves[22] and beta power[16] are most prominent during an instructed delay of a motor task. Taken together with previous findings relating planar waves to sequential spike patterns[42] and linking the phase of beta oscillations to the occurrence of precise synchronous events[21], LFP beta power could be indicative of communication by means of activity propagation on the level of single spikes

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