Literature DB >> 29442553

Phase reorganization leads to transient β-LFP spatial wave patterns in motor cortex during steady-state movement preparation.

Michael E Rule1, Carlos Vargas-Irwin1, John P Donoghue1,2,3, Wilson Truccolo1,2,3.   

Abstract

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.

Entities:  

Keywords:  beta oscillations; cortical waves; neural dynamics; optogenetically induced oscillations

Mesh:

Year:  2018        PMID: 29442553      PMCID: PMC6032117          DOI: 10.1152/jn.00525.2017

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.714


  59 in total

1.  Extracting spatial-temporal coherent patterns in large-scale neural recordings using dynamic mode decomposition.

Authors:  Bingni W Brunton; Lise A Johnson; Jeffrey G Ojemann; J Nathan Kutz
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2.  Beta rebound after different types of motor imagery in man.

Authors:  G Pfurtscheller; C Neuper; C Brunner; F Lopes da Silva
Journal:  Neurosci Lett       Date:  2005-01-08       Impact factor: 3.046

3.  Propagating waves mediate information transfer in the motor cortex.

Authors:  Doug Rubino; Kay A Robbins; Nicholas G Hatsopoulos
Journal:  Nat Neurosci       Date:  2006-11-19       Impact factor: 24.884

4.  Hippocampal theta oscillations are travelling waves.

Authors:  Evgueniy V Lubenov; Athanassios G Siapas
Journal:  Nature       Date:  2009-05-28       Impact factor: 49.962

5.  Latent state-space models for neural decoding.

Authors:  Mehdi Aghagolzadeh; Wilson Truccolo
Journal:  Conf Proc IEEE Eng Med Biol Soc       Date:  2014

6.  Synchrony, waves and ripple in spatially coupled Kuramoto oscillators with Mexican hat connectivity.

Authors:  Stewart Heitmann; G Bard Ermentrout
Journal:  Biol Cybern       Date:  2015-02-13       Impact factor: 2.086

Review 7.  Oscillations and the basal ganglia: motor control and beyond.

Authors:  John-Stuart Brittain; Peter Brown
Journal:  Neuroimage       Date:  2013-05-25       Impact factor: 6.556

8.  Large-scale spatiotemporal spike patterning consistent with wave propagation in motor cortex.

Authors:  Kazutaka Takahashi; Sanggyun Kim; Todd P Coleman; Kevin A Brown; Aaron J Suminski; Matthew D Best; Nicholas G Hatsopoulos
Journal:  Nat Commun       Date:  2015-05-21       Impact factor: 14.919

9.  Shifts of Gamma Phase across Primary Visual Cortical Sites Reflect Dynamic Stimulus-Modulated Information Transfer.

Authors:  Michel Besserve; Scott C Lowe; Nikos K Logothetis; Bernhard Schölkopf; Stefano Panzeri
Journal:  PLoS Biol       Date:  2015-09-22       Impact factor: 8.029

10.  Contribution of LFP dynamics to single-neuron spiking variability in motor cortex during movement execution.

Authors:  Michael E Rule; Carlos Vargas-Irwin; John P Donoghue; Wilson Truccolo
Journal:  Front Syst Neurosci       Date:  2015-06-22
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  5 in total

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Authors:  Anup Das; John Myers; Joshua Jacobs; Sameer A Sheth; Raissa Mathura; Ben Shofty; Brian A Metzger; Kelly Bijanki; Chengyuan Wu
Journal:  Elife       Date:  2022-05-26       Impact factor: 8.713

2.  Synchronization, Stochasticity, and Phase Waves in Neuronal Networks With Spatially-Structured Connectivity.

Authors:  Anirudh Kulkarni; Jonas Ranft; Vincent Hakim
Journal:  Front Comput Neurosci       Date:  2020-10-19       Impact factor: 2.380

3.  Propagating Motor Cortical Dynamics Facilitate Movement Initiation.

Authors:  Karthikeyan Balasubramanian; Vasileios Papadourakis; Wei Liang; Kazutaka Takahashi; Matthew D Best; Aaron J Suminski; Nicholas G Hatsopoulos
Journal:  Neuron       Date:  2020-03-06       Impact factor: 17.173

4.  Grasp-squeeze adaptation to changes in object compliance leads to dynamic beta-band communication between primary somatosensory and motor cortices.

Authors:  Huy Cu; Laurie Lynch; Kevin Huang; Wilson Truccolo; Arto Nurmikko
Journal:  Sci Rep       Date:  2022-04-26       Impact factor: 4.996

5.  Is there an Intrinsic Relationship between LFP Beta Oscillation Amplitude and Firing Rate of Individual Neurons in Macaque Motor Cortex?

Authors:  Joachim Confais; Nicole Malfait; Thomas Brochier; Alexa Riehle; Bjørg Elisabeth Kilavik
Journal:  Cereb Cortex Commun       Date:  2020-05-13
  5 in total

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