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Journal articleIbanez Pereda J, Zicher B, Brown KE, et al., 2023,
Standard intensities of transcranial alternating current stimulation over the motor cortex do not entrain corticospinal inputs to motor neurons
, The Journal of Physiology, Vol: 601, Pages: 3187-3199, ISSN: 0022-3751Transcranial alternating current stimulation (TACS) is commonly used to synchronise a cortical area and its outputs to the stimulus waveform, but evidence for this based on brain recordings in humans is challenging. The corticospinal tract transmits beta oscillations (~21Hz) from motor cortex to tonically contracted limb muscles linearly. Therefore, muscle activity may be used to measure the level of beta entrainment in the corticospinal tract due to TACS over motor cortex. Here, we assessed if TACS is able to modulate the neural inputs to muscles, which would provide indirect evidence for TACS-driven neural entrainment. In the first part of this study, we ran simulations of motor neuron (MN) pools receiving inputs from corticospinal neurons with different levels of beta entrainment. Results suggest that MNs are highly sensitive to changes in corticospinal beta activity. Then, we ran experiments on healthy human subjects (N=10) in which TACS (at 1mA) was delivered over the motor cortex at 21Hz (beta stimulation), or at 7Hz or 40Hz (control conditions) while the abductor digiti minimi or the tibialis anterior muscle were tonically contracted. Muscle activity was measured using high-density electromyography, which allowed us to decompose the activity of pools of motor units innervating the muscles. By analysing motor unit pool activity, we observed that none of the TACS conditions could consistently alter the spectral contents of the common neural inputs received by the muscles. These results suggest that 1mA-TACS over motor cortex given at beta frequencies does not entrain corticospinal activity.
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Journal articleHug F, Avrillon S, Sarcher A, et al., 2023,
Correlation networks of spinal motor neurons that innervate lower limb muscles during a multi-joint isometric task
, The Journal of Physiology, Vol: 601, Pages: 3201-3219, ISSN: 0022-3751Movements are reportedly controlled through the combination of synergies that generate specific motor outputs by imposing an activation pattern on a group of muscles. To date, the smallest unit of analysis of these synergies has been the muscle through the measurement of its activation. However, the muscle is not the lowest neural level of movement control. In this human study (n = 10), we used a purely data-driven method grounded on graph theory to extract networks of motor neurons based on their correlated activity during an isometric multi-joint task. Specifically, high-density surface electromyography recordings from six lower limb muscles were decomposed into motor neurons spiking activity. We analyzed these activities by identifying their common low-frequency components, from which networks of correlated activity to the motor neurons were derived and interpreted as networks of common synaptic inputs. The vast majority of the identified motor neurons shared common inputs with other motor neuron(s). In addition, groups of motor neurons were partly decoupled from their innervated muscle, such that motor neurons innervating the same muscle did not necessarily receive common inputs. Conversely, some motor neurons from different muscles – including distant muscles – received common inputs. Our study supports the theory that movements are produced through the control of small numbers of groups of motor neurons via common inputs and that there is a partial mismatch between these groups of motor neurons and muscle anatomy. We provide a new neural framework for a deeper understanding of the structure of common inputs to motor neurons.Abstract figure legend Ten participants performed an isometric multi-joint task, which consisted in producing force on an instrumented pedal. Adhesive grids of 64 electrodes were placed over six lower limb muscles (gastrocnemius medialis [GM] and lateralis [GL], vastus lateralis [VL] and medialis [VM], biceps femoris [BF], semit
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Journal articleHug F, Avrillon S, Sarcher A, et al., 2023,
Correlation networks of spinal motor neurons that innervate lower limb muscles during a multi-joint isometric task
, JOURNAL OF PHYSIOLOGY-LONDON, Vol: 601, Pages: 3201-3219, ISSN: 0022-3751- Author Web Link
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- Citations: 7
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Journal articleFarina D, Vujaklija I, Branemark R, et al., 2023,
Toward higher-performance bionic limbs for wider clinical use
, Nature Biomedical Engineering, Vol: 7, Pages: 473-485, ISSN: 2157-846XMost prosthetic limbs can autonomously move with dexterity, yet they are not perceived by the user as belonging to their own body. Robotic limbs can convey information about the environment with higher precision than biological limbs, but their actual performance is substantially limited by current technologies for the interfacing of the robotic devices with the body and for transferring motor and sensory information bidirectionally between the prosthesis and the user. In this Perspective, we argue that direct skeletal attachment of bionic devices via osseointegration, the amplification of neural signals by targeted muscle innervation, improved prosthesis control via implanted muscle sensors and advanced algorithms, and the provision of sensory feedback by means of electrodes implanted in peripheral nerves, should all be leveraged towards the creation of a new generation of high-performance bionic limbs. These technologies have been clinically tested in humans, and alongside mechanical redesigns and adequate rehabilitation training should facilitate the wider clinical use of bionic limbs.
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Journal articleVujaklija I, IEEE Member, Ki Jung M, et al., 2023,
Biomechanical analysis of body movements of myoelectric prosthesis users during standardized clinical tests
, IEEE Transactions on Biomedical Engineering, Vol: 70, Pages: 789-799, ISSN: 0018-9294Objective: The objective clinical evaluation of user's capabilities to handle their prosthesis is done using various tests which primarily focus on the task completion speed and do not explicitly account for the potential presence of compensatory motions. Given that the excessive body compensation is a common indicator of inadequate prosthesis control, tests which include subjective observations on the quality of performed motions have been introduced. However, these metrics are then influenced by the examiner's opinions, skills, and training making them harder to standardize across patient pools and compare across different prosthetic technologies. Here we aim to objectively quantify the severity of body compensations present in myoelectric prosthetic hand users and evaluate the extent to which traditional objective clinical scores are still able to capture them. Methods: We have instructed 9 below-elbow prosthesis users and 9 able-bodied participants to complete three established objective clinical tests: Box-and-Blocks-Test, Clothespin-Relocation-Test, and Southampton-Hand-Assessment-Procedure. During all tests, upper-body kinematics has been recorded. Results: While the analysis showed that there are some correlations between the achieved clinical scores and the individual body segment travel distances and average speeds, there were only weak correlations between the clinical scores and the observed ranges of motion. At the same time, the compensations were observed in all prosthesis users and, for the most part, they were substantial across the tests. Conclusion: The sole reliance on the currently available objective clinical assessment methods seems inadequate as the compensatory movements are prominent in prosthesis users and yet not sufficiently accounted for.
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Journal articleShirzadi M, Marateb HRR, McGill KCC, et al., 2023,
An Accurate and Real-Time Method for Resolving Superimposed Action Potentials in MultiUnit Recordings
, IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, Vol: 70, Pages: 378-389, ISSN: 0018-9294- Author Web Link
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- Citations: 1
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Journal articleKoutsoftidis S, Barsakcioglu DY, Petkos K, et al., 2022,
Myolink: A 128-Channel, 18 nV/√Hz, Embedded Recording System, Optimized for High-Density Surface Electromyogram Acquisition
, IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, Vol: 69, Pages: 3389-3396, ISSN: 0018-9294- Cite
- Citations: 2
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Journal articleCaillet A, Phillips ATM, Farina D, et al., 2022,
Mathematical relationships between spinal motoneuron properties
, eLife, Vol: 11, ISSN: 2050-084XOur understanding of the behaviour of spinal alpha-motoneurons (MNs) in mammals partly relies on our knowledge of the relationships between MN membrane properties, such as MN size, resistance, rheobase, capacitance, time constant, axonal conduction velocity and afterhyperpolarization period. We reprocessed the data from 40 experimental studies in adult cat, rat and mouse MN preparations, to empirically derive a set of quantitative mathematical relationships between these MN electrophysiological and anatomical properties. This validated mathematical framework, which supports past findings that the MN membrane properties are all related to each other and clarifies the nature of their associations, is besides consistent with the Henneman’s size principle and Rall’s cable theory. The derived mathematical relationships provide a convenient tool for neuroscientists and experimenters to complete experimental datasets, to explore relationships between pairs of MN properties never concurrently observed in previous experiments, or to investigate inter-mammalian-species variations in MN membrane properties. Using this mathematical framework, modelers can build profiles of inter-consistent MN-specific properties to scale pools of MN models, with consequences on the accuracy and the interpretability of the simulations.
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Journal articleLubel E, Sgambato BG, Barsakcioglu DY, et al., 2022,
Kinematics of individual muscle units in natural contractions measured <i>in vivo</i> using ultrafast ultrasound
, JOURNAL OF NEURAL ENGINEERING, Vol: 19, ISSN: 1741-2560- Author Web Link
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- Citations: 5
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Journal articleDel Vecchio A, Jones RHA, Schofield IS, et al., 2022,
Interfacing motor units in non-human primates identifies a principal neural component for force control constrained by the size principle
, The Journal of Neuroscience, Vol: 42, Pages: 7383-7399, ISSN: 0270-6474Motor units convert the last neural code of movement into muscle forces. The classic view of motor unit control is that the central nervous system sends common synaptic inputs to motoneuron pools and that motoneurons respond in an orderly fashion dictated by the size principle. This view however is in contrast with the large number of dimensions observed in motor cortex which may allow individual and flexible control of motor units. Evidence for flexible control of motor units may be obtained by tracking motor units longitudinally during tasks with some level of behavioural variability. Here we identified and tracked populations of motor units in the brachioradialis muscle of two macaque monkeys during ten sessions spanning over one month with a broad range of rate of force development (1.8 - 38.6 N∙m∙s-1). We found a very stable recruitment order and discharge characteristics of the motor units over sessions and contraction trials. The small deviations from orderly recruitment were fully predicted by the motor unit recruitment intervals, so that small shifts in recruitment thresholds happened only during contractions at high rate of force development. Moreover, we also found that one component explained more than ~50% of the motor unit discharge rate variance, and that the remaining components represented a time-shifted version of the first. In conclusion, our results show that motoneurons recruitment is determined by the interplay of the size principle and common input and that this recruitment scheme is not violated over time nor by the speed of the contractions.
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Journal articleCaillet AH, Phillips ATM, Farina D, et al., 2022,
Estimation of the firing behaviour of a complete motoneuron pool by combining electromyography signal decomposition and realistic motoneuron modelling
, PLoS Computational Biology, Vol: 18, ISSN: 1553-734XOur understanding of the firing behaviour of motoneuron (MN) pools during human voluntary muscle contractions is currently limited to electrophysiological findings from animal experiments extrapolated to humans, mathematical models of MN pools not validated for human data, and experimental results obtained from decomposition of electromyographical (EMG) signals. These approaches are limited in accuracy or provide information on only small partitions of the MN population. Here, we propose a method based on the combination of high-density EMG (HDEMG) data and realistic modelling for predicting the behaviour of entire pools of motoneurons in humans. The method builds on a physiologically realistic model of a MN pool which predicts, from the experimental spike trains of a smaller number of individual MNs identified from decomposed HDEMG signals, the unknown recruitment and firing activity of the remaining unidentified MNs in the complete MN pool. The MN pool model is described as a cohort of single-compartment leaky fire-and-integrate (LIF) models of MNs scaled by a physiologically realistic distribution of MN electrophysiological properties and driven by a spinal synaptic input, both derived from decomposed HDEMG data. The MN spike trains and effective neural drive to muscle, predicted with this method, have been successfully validated experimentally. A representative application of the method in MN-driven neuromuscular modelling is also presented. The proposed approach provides a validated tool for neuroscientists, experimentalists, and modelers to infer the firing activity of MNs that cannot be observed experimentally, investigate the neuromechanics of human MN pools, support future experimental investigations, and advance neuromuscular modelling for investigating the neural strategies controlling human voluntary contractions.
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Journal articleYeung D, Guerra IM, Barner-Rasmussen I, et al., 2022,
Co-Adaptive Control of Bionic Limbs via Unsupervised Adaptation of Muscle Synergies
, IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, Vol: 69, Pages: 2581-2592, ISSN: 0018-9294- Author Web Link
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- Citations: 2
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Journal articleBracklein M, Barsakcioglu DY, Ibanez J, et al., 2022,
The control and training of single motor units in isometric tasks are constrained by a common input signal
, eLife, Vol: 11, ISSN: 2050-084XRecent developments in neural interfaces enable the real-time and non-invasive tracking of motor neuron spiking activity. Such novel interfaces could provide a promising basis for human motor augmentation by extracting potentially high-dimensional control signals directly from the human nervous system. However, it is unclear how flexibly humans can control the activity of individual motor neurons to effectively increase the number of degrees of freedom available to coordinate multiple effectors simultaneously. Here, we provided human subjects (N = 7) with real-time feedback on the discharge patterns of pairs of motor units (MUs) innervating a single muscle (tibialis anterior) and encouraged them to independently control the MUs by tracking targets in a 2D space. Subjects learned control strategies to achieve the target-tracking task for various combinations of MUs. These strategies rarely corresponded to a volitional control of independent input signals to individual MUs during the onset of neural activity. Conversely, MU activation was consistent with a common input to the MU pair, while individual activation of the MUs in the pair was predominantly achieved by alterations in de-recruitment order that could be explained by history-dependent changes in motor neuron excitability. These results suggest that flexible MU recruitment based on independent synaptic inputs to single MUs is unlikely, although de-recruitment might reflect varying inputs or modulations in the neuron’s intrinsic excitability.
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Journal articleBracklein M, Barsakcioglu DY, Del Vecchio A, et al., 2022,
Reading and modulating cortical beta bursts from motor unit spiking activity
, JOURNAL OF NEUROSCIENCE, Vol: 42, ISSN: 0270-6474- Author Web Link
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- Citations: 9
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Journal articleMendez Guerra I, Barsakcioglu DY, Vujaklija I, et al., 2022,
Far-field electric potentials provide access to the output from the spinal cord from wrist-mounted sensors
, Journal of Neural Engineering, Vol: 19, ISSN: 1741-2552OBJECTIVE: Neural interfaces need to become more unobtrusive and socially acceptable to appeal to general consumers outside rehabilitation settings. APPROACH: We developed a non-invasive neural interface that provides access to spinal motor neuron activities from the wrist, which is the preferred location for a wearable. The interface decodes far-field potentials present at the tendon endings of the forearm muscles using blind source separation. First, we evaluated the reliability of the interface to detect motor neuron firings based on far-field potentials, and thereafter we used the decoded motor neuron activity for the prediction of finger contractions in offline and real-time conditions. MAIN RESULTS: The results showed that motor neuron activity decoded from the far-field potentials at the wrist accurately predicted individual and combined finger commands and therefore allowed for highly accurate real-time task classification. SIGNIFICANCE: These findings demonstrate the feasibility of a non-invasive, neural interface at the wrist for precise real-time control based on the output of the spinal cord.
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Journal articleEden J, Bräcklein M, Ibáñez J, et al., 2022,
Principles of human movement augmentation and the challenges in making it a reality
, Nature Communications, Vol: 13, ISSN: 2041-1723Augmenting the body with artificial limbs controlled concurrently to one's natural limbs has long appeared in science fiction, but recent technological and neuroscientific advances have begun to make this possible. By allowing individuals to achieve otherwise impossible actions, movement augmentation could revolutionize medical and industrial applications and profoundly change the way humans interact with the environment. Here, we construct a movement augmentation taxonomy through what is augmented and how it is achieved. With this framework, we analyze augmentation that extends the number of degrees-of-freedom, discuss critical features of effective augmentation such as physiological control signals, sensory feedback and learning as well as application scenarios, and propose a vision for the field.
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Journal articlePuttaraksa G, Muceli S, Barsakcioglu DY, et al., 2022,
Online tracking of the phase difference between neural drives to antagonist muscle pairs in essential tremor patients
, IEEE Transactions on Neural Systems and Rehabilitation Engineering, Vol: 30, Pages: 709-718, ISSN: 1534-4320Transcutaneous electrical stimulation has been applied in tremor suppression applications. Out-of-phase stimulation strategies applied above or below motor threshold result in a significant attenuation of pathological tremor. For stimulation to be properly timed, the varying phase relationship between agonist-antagonist muscle activity during tremor needs to be accurately estimated in real-time. Here we propose an online tremor phase and frequency tracking technique for the customized control of electrical stimulation, based on a phase-locked loop (PLL) system applied to the estimated neural drive to muscles. Surface electromyography signals were recorded from the wrist extensor and flexor muscle groups of 13 essential tremor patients during postural tremor. The EMG signals were pre-processed and decomposed online and offline via the convolution kernel compensation algorithm to discriminate motor unit spike trains. The summation of motor unit spike trains detected for each muscle was bandpass filtered between 3 to 10 Hz to isolate the tremor related components of the neural drive to muscles. The estimated tremorogenic neural drive was used as input to a PLL that tracked the phase differences between the two muscle groups. The online estimated phase difference was compared with the phase calculated offline using a Hilbert Transform as a ground truth. The results showed a rate of agreement of 0.88 ± 0.22 between offline and online EMG decomposition. The PLL tracked the phase difference of tremor signals in real-time with an average correlation of 0.86 ± 0.16 with the ground truth (average error of 6.40° ± 3.49°). Finally, the online decomposition and phase estimation components were integrated with an electrical stimulator and applied in closed-loop on one patient, to representatively demonstrate the working principle of the full tremor suppression system. The results of this study support the feasibility of real-time estimation of the pha
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Journal articleYu T, Akhmadeev K, Le Carpentier E, et al., 2022,
Highly Accurate Real-Time Decomposition of Single Channel Intramuscular EMG
, IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, Vol: 69, Pages: 746-757, ISSN: 0018-9294- Author Web Link
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- Citations: 1
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Journal articleLuft M, Klepetko J, Muceli S, et al., 2021,
Proof of concept for multiple nerve transfers to a single target muscle
, eLife, Vol: 10, Pages: 1-16, ISSN: 2050-084XSurgical nerve transfers are used to efficiently treat peripheral nerve injuries, neuromas,phantom limb pain, or improve bionic prosthetic control. Commonly, one donor nerve is transferredto one target muscle. However, the transfer of multiple nerves onto a single target muscle mayincrease the number of muscle signals for myoelectric prosthetic control and facilitate the treatmentof multiple neuromas. Currently, no experimental models are available. This study describes anovel experimental model to investigate the neurophysiological effects of peripheral double nervetransfers to a common target muscle. In 62 male Sprague-Dawleyrats, the ulnar nerve of the antebrachiumalone (n=30) or together with the anterior interosseus nerve (n=32) was transferred to reinnervatethe long head of the biceps brachii. Before neurotization, the motor branch to the biceps’long head was transected at the motor entry point. Twelve weeks after surgery, muscle responseto neurotomy, behavioral testing, retrograde labeling, and structural analyses were performed toassess reinnervation. These analyses indicated that all nerves successfully reinnervated the targetmuscle. No aberrant reinnervation was observed by the originally innervating nerve. Our observationssuggest a minimal burden for the animal with no signs of functional deficit in daily activities orauto-mutilationin both procedures. Furthermore, standard neurophysiological analyses for nerveand muscle regeneration were applicable. This newly developed nerve transfer model allows for thereliable and standardized investigation of neural and functional changes following the transfer ofmultiple donor nerves to one target muscle.
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Journal articleIbáñez J, Angeli CA, Harkema SJ, et al., 2021,
Recruitment order of motor neurons promoted by epidural stimulation in individuals with spinal cord injury.
, Journal of Applied Physiology, Vol: 131, Pages: 1100-1110, ISSN: 1522-1601Spinal cord epidural stimulation (scES) combined with activity-based training can promote motor function recovery in individuals with motor complete spinal cord injury (SCI). The characteristics of motor neuron recruitment, which influence different aspects of motor control, are still unknown when motor function is promoted by scES. Here, we enrolled five individuals with chronic motor complete SCI implanted with an scES unit to study the recruitment order of motor neurons during standing enabled by scES. We recorded high-density electromyography (HD-EMG) signals on the vastus lateralis muscle and inferred the order of recruitment of motor neurons from the relation between amplitude and conduction velocity of the scES-evoked EMG responses along the muscle fibers. Conduction velocity of scES-evoked responses was modulated over time, whereas stimulation parameters and standing condition remained constant, with average values ranging between 3.0 ± 0.1 and 4.4 ± 0.3 m/s. We found that the human spinal circuitry receiving epidural stimulation can promote both orderly (according to motor neuron size) and inverse trends of motor neuron recruitment, and that the engagement of spinal networks promoting rhythmic activity may favor orderly recruitment trends. Conversely, the different recruitment trends did not appear to be related with time since injury or scES implant, nor to the ability to achieve independent knees extension, nor to the conduction velocity values. The proposed approach can be implemented to investigate the effects of stimulation parameters and training-induced neural plasticity on the characteristics of motor neuron recruitment order, contributing to improve mechanistic understanding and effectiveness of epidural stimulation-promoted motor recovery after SCI.NEW & NOTEWORTHY After motor complete spinal cord injury, the human spinal cord receiving epidural stimulation can promote both orderly and inverse trends o
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