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      The Advantage of Low-Delta Electroencephalogram Phase Feature for Reconstructing the Center-Out Reaching Hand Movements

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          Abstract

          It is an emerging frontier of research on the use of neural signals for prosthesis control, in order to restore lost function to amputees and patients after spinal cord injury. Compared to the invasive neural signal based brain-machine interface (BMI), a non-invasive alternative, i.e., the electroencephalogram (EEG)-based BMI would be more widely accepted by the patients above. Ideally, a real-time continuous neuroprosthestic control is required for practical applications. However, conventional EEG-based BMIs mainly deal with the discrete brain activity classification. Until recently, the literature has reported several attempts for achieving the real-time continuous control by reconstructing the continuous movement parameters (e.g., speed, position, etc.) from the EEG recordings, and the low-frequency band EEG is consistently reported to encode the continuous motor control information. Previous studies with executed movement tasks have extensively relied on the amplitude representation of such slow oscillations of EEG signals for building models to decode kinematic parameters. Inspired by the recent successes of instantaneous phase of low-frequency invasive brain signals in the motor control and sensory processing domains, this study examines the extension of such a slow-oscillation phase representation to the reconstructing two-dimensional hand movements, with the non-invasive EEG signals for the first time. The data for analysis are collected on five healthy subjects performing 2D hand center-out reaching along four directions in two sessions. On representative channels over the cortices encoding the execution information of reaching movements, we show that the low-delta EEG phase representation is characterized by higher signal-to-noise ratio and stronger modulation by the movement tasks, compared to the low-delta EEG amplitude representation. Furthermore, we have tested the low-delta EEG phase representation with two commonly used linear decoding models. The results demonstrate that the low-delta EEG phase based decoders lead to superior performance for 2D executed movement reconstruction to its amplitude based counterparts, as well as the other-frequency band amplitude and power based features. Thus, our study contributes to improve the movement reconstruction from EEG by introducing a new feature set based on the low-delta EEG phase patterns, and demonstrates its potential for continuous fine motion control of neuroprostheses.

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          Most cited references 37

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          Neuronal population coding of movement direction.

          Although individual neurons in the arm area of the primate motor cortex are only broadly tuned to a particular direction in three-dimensional space, the animal can very precisely control the movement of its arm. The direction of movement was found to be uniquely predicted by the action of a population of motor cortical neurons. When individual cells were represented as vectors that make weighted contributions along the axis of their preferred direction (according to changes in their activity during the movement under consideration) the resulting vector sum of all cell vectors (population vector) was in a direction congruent with the direction of movement. This population vector can be monitored during various tasks, and similar measures in other neuronal populations could be of heuristic value where there is a neural representation of variables with vectorial attributes.
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            Bayesian population decoding of motor cortical activity using a Kalman filter.

            Effective neural motor prostheses require a method for decoding neural activity representing desired movement. In particular, the accurate reconstruction of a continuous motion signal is necessary for the control of devices such as computer cursors, robots, or a patient's own paralyzed limbs. For such applications, we developed a real-time system that uses Bayesian inference techniques to estimate hand motion from the firing rates of multiple neurons. In this study, we used recordings that were previously made in the arm area of primary motor cortex in awake behaving monkeys using a chronically implanted multielectrode microarray. Bayesian inference involves computing the posterior probability of the hand motion conditioned on a sequence of observed firing rates; this is formulated in terms of the product of a likelihood and a prior. The likelihood term models the probability of firing rates given a particular hand motion. We found that a linear gaussian model could be used to approximate this likelihood and could be readily learned from a small amount of training data. The prior term defines a probabilistic model of hand kinematics and was also taken to be a linear gaussian model. Decoding was performed using a Kalman filter, which gives an efficient recursive method for Bayesian inference when the likelihood and prior are linear and gaussian. In off-line experiments, the Kalman filter reconstructions of hand trajectory were more accurate than previously reported results. The resulting decoding algorithm provides a principled probabilistic model of motor-cortical coding, decodes hand motion in real time, provides an estimate of uncertainty, and is straightforward to implement. Additionally the formulation unifies and extends previous models of neural coding while providing insights into the motor-cortical code.
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              Prediction of arm movement trajectories from ECoG-recordings in humans.

              Electrocorticographic (ECoG) signals have been shown to contain reliable information about the direction of arm movements and can be used for on-line cursor control. These findings indicate that the ECoG is a potential basis for a brain-machine interface (BMI) for application in paralyzed patients. However, previous approaches to ECoG-BMIs were either based on classification of different movement patterns or on a voluntary modulation of spectral features. For a continuous multi-dimensional BMI control, the prediction of complete movement trajectories, as it has already been shown for spike data and local field potentials (LFPs), would be a desirable addition for the ECoG, too. Here, we examined ECoG signals from six subjects with subdurally implanted ECoG-electrodes during continuous two-dimensional arm movements between random target positions. Our results show that continuous trajectories of 2D hand position can be approximately predicted from the ECoG recorded from hand/arm motor cortex. This indicates that ECoG signals, related to body movements, can directly be transferred to equivalent controls of an external effector for continuous BMI control.
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                Author and article information

                Affiliations
                1Jiangsu Key Lab of Remote Measurement and Control, School of Instrument Science and Engineering, Southeast University , Nanjing, China
                2Mechatronics and Haptics Interfaces Laboratory, Department of Mechanical Engineering, Rice University , Houston, TX, United States
                3College of Automation, Nanjing University of Posts and Telecommunications , Nanjing, China
                4College of Automation Engineering, Nanjing University of Aeronautics and Astronautics , Nanjing, China
                5Guangxi Key Laboratory of Automatic Detecting Technology and Instruments, Guilin University of Electronic Technology , Guilin, China
                Author notes

                Edited by: Mikhail Lebedev, Duke University, United States

                Reviewed by: Tonio Ball, Department of Neurosurgery, University Hospital Freiburg, Germany; Damien Coyle, Ulster University, United Kingdom; Elvira Pirondini, Université de Genève, Switzerland; Yujing Wang, Johns Hopkins University, United States; Marisel Villafañe-Delgado, Applied Physics Laboratory, Johns Hopkins University, United States

                *Correspondence: Hong Zeng hzeng@ 123456seu.edu.cn

                This article was submitted to Neuroprosthetics, a section of the journal Frontiers in Neuroscience

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                15 May 2019
                2019
                : 13
                10.3389/fnins.2019.00480
                6530632
                Copyright © 2019 Zeng, Sun, Xu, Wu, Song, Xu, Li and Hu.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Counts
                Figures: 10, Tables: 5, Equations: 11, References: 37, Pages: 18, Words: 10276
                Categories
                Neuroscience
                Original Research

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