Rule Michael E, Vargas-Irwin Carlos, Donoghue John P, Truccolo Wilson
Department of Neuroscience, Brown University , Providence, Rhode Island.
Institute for Brain Science, Brown University , Providence, Rhode Island.
J Neurophysiol. 2018 Jun 1;119(6):2212-2228. doi: 10.1152/jn.00525.2017. Epub 2018 Feb 14.
Previous studies on the origin and properties of spatial patterns in motor cortex β-local field potential (β-LFP) oscillations have focused on planar traveling waves. However, it is unclear 1) whether β-LFP waves are limited to plane waves, or even 2) whether they are propagating waves of excito-excitatory activity, i.e., primarily traveling waves in excitable media; they could reflect, instead, reorganization in the relative phases of transient oscillations at different spatial sites. We addressed these two problems in β-LFPs recorded via microelectrode arrays implanted in three adjacent motor cortex areas of nonhuman primates during steady-state movement preparation. Our findings are fourfold: 1) β-LFP wave patterns emerged as transient events, despite stable firing rates of single neurons concurrently recorded during the same periods. 2) β-LFP waves showed a richer variety of spatial dynamics, including rotating and complex waves. 3) β-LFP wave patterns showed no characteristic wavelength, presenting instead a range of scales with global zero-lag phase synchrony as a limiting case, features surprising for purely excito-excitatory waves but consistent with waves in coupled oscillator systems. 4) Furthermore, excito-excitatory traveling waves induced by optogenetic stimulation in motor cortex showed, in contrast, a characteristic wavelength and reduced phase synchrony. Overall, β-LFP wave statistics differed from those of induced traveling waves in excitable media recorded under the same microelectrode array setup. Our findings suggest phase reorganization in neural coupled oscillators contribute significantly to the origin of transient β-LFP spatial dynamics during preparatory steady states and outline important constraints for spatially extended models of β-LFP dynamics in motor cortex. NEW & NOTEWORTHY We show that a rich variety of transient β-local field potential (β-LFP) wave patterns emerge in motor cortex during preparatory steady states, despite stable neuronal firing rates. Furthermore, unlike optogenetically induced traveling waves, β-LFP waves showed no characteristic wavelength, presenting instead a range of scales with global phase synchrony as a limiting case. Overall, our statistical analyses suggest that transient phase reorganization in neural coupled oscillators, beyond purely excito-excitatory traveling waves, contribute significantly to the origin of motor cortex β-LFP wave patterns.
先前关于运动皮层β-局部场电位（β-LFP）振荡空间模式的起源和特性的研究主要集中在平面行波上。然而，目前尚不清楚：1）β-LFP波是否仅限于平面波；甚至2）它们是否是兴奋-兴奋活动的传播波，即主要是可兴奋介质中的行波；相反，它们可能反映的是不同空间位置处瞬态振荡相对相位的重新组织。我们通过植入非人类灵长类动物三个相邻运动皮层区域的微电极阵列记录β-LFP，解决了这两个问题，记录过程处于稳态运动准备阶段。我们的发现有四点：1）尽管在同一时期同时记录的单个神经元放电率稳定，但β-LFP波模式表现为瞬态事件。2）β-LFP波表现出更丰富多样的空间动态，包括旋转波和复杂波。3）β-LFP波模式没有特征波长，而是呈现出一系列尺度，以全局零滞后相位同步作为极限情况，这些特征对于纯粹的兴奋-兴奋波来说令人惊讶，但与耦合振荡器系统中的波一致。4）此外，相比之下，运动皮层中光遗传学刺激诱发的兴奋-兴奋行波具有特征波长且相位同步性降低。总体而言，β-LFP波的统计特性与在相同微电极阵列设置下记录的可兴奋介质中诱发的行波不同。我们的发现表明神经耦合振荡器中的相位重新组织对准备稳态期间瞬态β-LFP空间动态的起源有显著贡献，并为运动皮层中β-LFP动态的空间扩展模型勾勒出重要限制。新发现与值得注意之处我们表明，尽管神经元放电率稳定，但在准备稳态期间运动皮层中会出现丰富多样的瞬态β-局部场电位（β-LFP）波模式。此外，与光遗传学诱发的行波不同，β-LFP波没有特征波长，而是呈现出一系列尺度，以全局相位同步作为极限情况。总体而言，我们的统计分析表明，神经耦合振荡器中的瞬态相位重新组织，而非纯粹的兴奋-兴奋行波，对运动皮层β-LFP波模式的起源有显著贡献。
