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High Amplitude EEG Motor Potential during Repetitive Foot Movement: Possible Use and Challenges for Futuristic BCIs That Restore Mobility after Spinal Cord Injury

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      Abstract

      Recent advances in neuroprostheses provide us with promising ideas of how to improve the quality of life in people suffering from impaired motor functioning of upper and lower limbs. Especially for patients after spinal cord injury (SCI), futuristic devices that are controlled by thought via brain-computer interfaces (BCIs) might be of tremendous help in managing daily tasks and restoring at least some mobility. However, there are certain problems arising when trying to implement BCI technology especially in such a heterogenous patient group. A plethora of processes occurring after the injuries change the brain's structure as well as its functionality collectively referred to as neuroplasticity. These changes are very different between individuals, leading to an increasing interest to reveal the exact changes occurring after SCI. In this study we investigated event-related potentials (ERPs) derived from electroencephalography (EEG) signals recorded during the (attempted) execution and imagination of hand and foot movements in healthy subjects and patients with SCI. As ERPs and especially early components are of interest for BCI research we aimed to investigate differences between 22 healthy volunteers and 7 patients (mean age = 51.86, SD = 15.49) suffering from traumatic or non-traumatic SCI since 2–314 months (mean = 116,57, SD = 125,55). We aimed to explore differences in ERP responses as well as the general presence of component that might be of interest to further consider for incorporation into BCI research. In order to match the real-life situation of BCIs for controlling neuroprostheses, we worked on small trial numbers (<25), only. We obtained a focal potential over Pz in ten healthy participants but in none of the patients after lenient artifact rejection. The potential was characterized by a high amplitude, it correlated with the repeated movements (6 times in 6 s) and in nine subjects it significantly differed from a resting condition. Furthermore, there are strong arguments against possible confounding factors leading to the potential's appearance. This phenomenon, occurring when movements are repeatedly conducted, might represent a possible potential to be used in futuristic BCIs and further studies should try to investigate the replicability of its appearance.

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      Most cited references 75

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      Nonparametric statistical testing of EEG- and MEG-data.

      In this paper, we show how ElectroEncephaloGraphic (EEG) and MagnetoEncephaloGraphic (MEG) data can be analyzed statistically using nonparametric techniques. Nonparametric statistical tests offer complete freedom to the user with respect to the test statistic by means of which the experimental conditions are compared. This freedom provides a straightforward way to solve the multiple comparisons problem (MCP) and it allows to incorporate biophysically motivated constraints in the test statistic, which may drastically increase the sensitivity of the statistical test. The paper is written for two audiences: (1) empirical neuroscientists looking for the most appropriate data analysis method, and (2) methodologists interested in the theoretical concepts behind nonparametric statistical tests. For the empirical neuroscientist, a large part of the paper is written in a tutorial-like fashion, enabling neuroscientists to construct their own statistical test, maximizing the sensitivity to the expected effect. And for the methodologist, it is explained why the nonparametric test is formally correct. This means that we formulate a null hypothesis (identical probability distribution in the different experimental conditions) and show that the nonparametric test controls the false alarm rate under this null hypothesis.
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        Reach and grasp by people with tetraplegia using a neurally controlled robotic arm

        Paralysis following spinal cord injury (SCI), brainstem stroke, amyotrophic lateral sclerosis (ALS) and other disorders can disconnect the brain from the body, eliminating the ability to carry out volitional movements. A neural interface system (NIS) 1–5 could restore mobility and independence for people with paralysis by translating neuronal activity directly into control signals for assistive devices. We have previously shown that people with longstanding tetraplegia can use an NIS to move and click a computer cursor and to control physical devices 6–8 . Able-bodied monkeys have used an NIS to control a robotic arm 9 , but it is unknown whether people with profound upper extremity paralysis or limb loss could use cortical neuronal ensemble signals to direct useful arm actions. Here, we demonstrate the ability of two people with long-standing tetraplegia to use NIS-based control of a robotic arm to perform three-dimensional reach and grasp movements. Participants controlled the arm over a broad space without explicit training, using signals decoded from a small, local population of motor cortex (MI) neurons recorded from a 96-channel microelectrode array. One of the study participants, implanted with the sensor five years earlier, also used a robotic arm to drink coffee from a bottle. While robotic reach and grasp actions were not as fast or accurate as those of an able-bodied person, our results demonstrate the feasibility for people with tetraplegia, years after CNS injury, to recreate useful multidimensional control of complex devices directly from a small sample of neural signals.
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          High-performance neuroprosthetic control by an individual with tetraplegia.

          Paralysis or amputation of an arm results in the loss of the ability to orient the hand and grasp, manipulate, and carry objects, functions that are essential for activities of daily living. Brain-machine interfaces could provide a solution to restoring many of these lost functions. We therefore tested whether an individual with tetraplegia could rapidly achieve neurological control of a high-performance prosthetic limb using this type of an interface. We implanted two 96-channel intracortical microelectrodes in the motor cortex of a 52-year-old individual with tetraplegia. Brain-machine-interface training was done for 13 weeks with the goal of controlling an anthropomorphic prosthetic limb with seven degrees of freedom (three-dimensional translation, three-dimensional orientation, one-dimensional grasping). The participant's ability to control the prosthetic limb was assessed with clinical measures of upper limb function. This study is registered with ClinicalTrials.gov, NCT01364480. The participant was able to move the prosthetic limb freely in the three-dimensional workspace on the second day of training. After 13 weeks, robust seven-dimensional movements were performed routinely. Mean success rate on target-based reaching tasks was 91·6% (SD 4·4) versus median chance level 6·2% (95% CI 2·0-15·3). Improvements were seen in completion time (decreased from a mean of 148 s [SD 60] to 112 s [6]) and path efficiency (increased from 0·30 [0·04] to 0·38 [0·02]). The participant was also able to use the prosthetic limb to do skilful and coordinated reach and grasp movements that resulted in clinically significant gains in tests of upper limb function. No adverse events were reported. With continued development of neuroprosthetic limbs, individuals with long-term paralysis could recover the natural and intuitive command signals for hand placement, orientation, and reaching, allowing them to perform activities of daily living. Defense Advanced Research Projects Agency, National Institutes of Health, Department of Veterans Affairs, and UPMC Rehabilitation Institute. Copyright © 2013 Elsevier Ltd. All rights reserved.
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            Author and article information

            Affiliations
            1Department of Neurology, Christian Doppler Medical Center, Paracelsus Medical University Salzburg, Austria
            2Spinal Cord Injury and Tissue Regeneration Center Salzburg Salzburg, Austria
            3Department of Psychology, Paris-Lodron University of Salzburg Salzburg, Austria
            4Center for Cognitive Neuroscience Salzburg Salzburg, Austria
            Author notes

            Edited by: Mikhail Lebedev, Duke University, United States

            Reviewed by: Christos Frantzidis, Aristotle University of Thessaloniki, Greece; Carlos Alberto Cuellar, Mayo Clinic, United States; Quentin Noirhomme, Maastricht University, Netherlands

            *Correspondence: Aljoscha Thomschewski a.thomschewski@ 123456salk.at

            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
            23 June 2017
            2017
            : 11
            5481367
            10.3389/fnins.2017.00362
            Copyright © 2017 Thomschewski, Höller, Höller, Leis and Trinka.

            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) or licensor 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: 7, Tables: 3, Equations: 0, References: 77, Pages: 12, Words: 8885
            Categories
            Neuroscience
            Original Research

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