Abstract
Accurate prediction of motor output based on neural signals is critical in human–machine interactions. The objective was to evaluate the performance of predicting individual finger forces through an estimation of the descending neural drive to the spinal motoneuron pool. High-density surface electromyogram (EMG) signals of the extensor digitorum communis muscle were obtained, and were then decomposed into individual motor unit discharge events. The frequency of the composite discharge events at the population level was used to derive the descending neural drive, which was then used to predict the finger forces. The global EMG-based approach was used as a control condition. Compared with the EMG-based approach, the experimental results show that the neural-drive-based approach can better predict the individual finger forces with higher R2 values across different force levels and across different force trajectories (steady and varying forces). These findings indicate that the neural drive estimation based on motoneuron firing activities can be used as a reliable neural-machine interface signal involving individual fingers. However, real-time implementation of this approach is needed for future clinical translation.
Similar content being viewed by others
Change history
29 April 2019
Due to an error in production, Figure 4 in the original paper shows the root mean squared error (RMSE) between the force and the neural drive estimation. The <Emphasis Type="Italic">R</Emphasis><Superscript>2</Superscript> heat map as a function of the number of motor units and the accuracy is illustrated below.
Abbreviations
- MU:
-
Motor unit
- MUAP:
-
Motor unit action potential
- EMG:
-
Electromyogram
- sEMG:
-
Surface electromyogram
- HD:
-
High density
- EDC:
-
Extensor digitorum communis
- MVC:
-
Maximal voluntary contraction
- SNR:
-
Signal to noise ratio
- ANOVA:
-
Analysis of variance
References
Al-Timemy, A. H., G. Bugmann, J. Escudero, and N. Outram. Classification of finger movements for the dexterous hand prosthesis control with surface electromyography. IEEE J. Biomed. Health. Inform. 17:608–618, 2013.
Boretius, T., J. Badia, A. Pascual-Font, M. Schuettler, X. Navarro, K. Yoshida, and T. Stieglitz. A transverse intrafascicular multichannel electrode (TIME) to interface with the peripheral nerve. Biosens. Bioelectron. 26:62–69, 2010.
Callier, T., E. W. Schluter, G. A. Tabot, L. E. Miller, F. V. Tenore, and S. J. Bensmaia. Long-term stability of sensitivity to intracortical microstimulation of somatosensory cortex. J. Neural Eng. 12:56010, 2015.
Chen, M., and P. Zhou. A novel framework based on FastICA for high density surface EMG decomposition. IEEE Trans. Neural Syst. Rehabil. Eng. 24:117–127, 2016.
Clancy, E. A., and N. Hogan. Probability density of the surface electromyogram and its relation to amplitude detectors. IEEE Trans. Biomed. Eng. 46:730–739, 1999.
Dai, C., and X. Hu. Extracting and classifying spatial muscle activation patterns in forearm flexor muscles using high-density electromyogram recordings. Int. J. Neural Syst. 29:1850025, 2019.
Dai, C., H. Shin, B. Davis, and X. Hu. Origins of common neural inputs to different compartments of the extensor digitorum communis muscle. Sci. Rep. 7:13960, 2017.
Dai, C., Y. Zheng, and X. Hu. Estimation of muscle force based on neural drive in a hemispheric stroke survivor. Front. Neurol. 9:187, 2018.
Davoodi, R., C. Urata, M. Hauschild, M. Khachani, and G. E. Loeb. Model-based development of neural prostheses for movement. IEEE Trans. Biomed. Eng. 54:1909–1918, 2007.
De Luca, C. J., and R. Merletti. Surface myoelectric signal cross-talk among muscles of the leg. Electroencephalogr. Clin. Neurophysiol. 69:568–575, 1988.
Farina, D., L. Mesin, S. Martina, and R. Merletti. A surface EMG generation model with multilayer cylindrical description of the volume conductor. IEEE Trans. Biomed. Eng. 51:415–426, 2004.
Farina, D., I. Vujaklija, M. Sartori, T. Kapelner, F. Negro, N. Jiang, K. Bergmeister, A. Andalib, J. Principe, and O. C. Aszmann. Man/machine interface based on the discharge timings of spinal motor neurons after targeted muscle reinnervation. Nat. Biomed. Eng. 1:25, 2017.
Fuglevand, A. J., D. A. Winter, and A. E. Patla. Models of recruitment and rate coding organization in motor-unit pools. J. Neurophysiol. 70:2470–2488, 1993.
Gemperline, J. J., S. Allen, D. Walk, and W. Z. Rymer. Characteristics of motor unit discharge in subjects with hemiparesis. Muscle Nerve 18:1101–1114, 1995.
Glaser, V., A. Holobar, and D. Zazula. Real-time motor unit identification from high-density surface EMG. IEEE Trans. Neural Syst. Rehabil. Eng. 21:949–958, 2013.
Hu, X., W. Z. Rymer, and N. L. Suresh. Reliability of spike triggered averaging of the surface electromyogram for motor unit action potential estimation. Muscle Nerve 48:557–570, 2013.
Hu, X., A. K. Suresh, W. Z. Rymer, and N. L. Suresh. Altered motor unit discharge patterns in paretic muscles of stroke survivors assessed using surface electromyography. J. Neural Eng. 13:46025, 2016.
Hu, X., N. L. Suresh, C. Xue, and W. Z. Rymer. Extracting extensor digitorum communis activation patterns using high-density surface electromyography. Front. Physiol. 6:279, 2015.
Hyvärinen, A., and E. Oja. Independent component analysis: algorithms and applications. Neural Netw. 13:411–430, 2000.
Keenan, K. G., D. Farina, K. S. Maluf, R. Merletti, and R. M. Enoka. Influence of amplitude cancellation on the simulated surface electromyogram. J. Appl. Physiol. 98:120–131, 2005.
Kuiken, T. A., G. A. Dumanian, R. D. Lipschutz, L. A. Miller, and K. A. Stubblefield. The use of targeted muscle reinnervation for improved myoelectric prosthesis control in a bilateral shoulder disarticulation amputee. Prosthet. Orthot. Int. 28:245–253, 2004.
LeFever, R. S., A. P. Xenakis, and C. J. De Luca. A procedure for decomposing the myoelectric signal into its constituent action potentials-part II: execution and test for accuracy. IEEE Trans. Biomed. Eng. 29:158–164, 1982.
Merletti, R., and P. Di Torino. Standards for reporting EMG data. J Electromyogr. Kinesiol. 9:3–4, 1999.
Negro, F., S. Muceli, A. M. Castronovo, A. Holobar, and D. Farina. Multi-channel intramuscular and surface EMG decomposition by convolutive blind source separation. J. Neural Eng. 13:26027, 2016.
Richard, P. D., R. E. Gander, P. A. Parker, and R. N. Scott. Multistate myoelectric control: the feasibility of 5-state control. J. Rehabil. R&D 20:84–86, 1983.
Santello, M., and C. E. Lang. Are movement disorders and sensorimotor injuries pathologic synergies? When normal multi-joint movement synergies become pathologic. Front. Hum. Neurosci. 8:1050, 2015.
Thompson, C. K., F. Negro, M. D. Johnson, M. R. Holmes, L. M. McPherson, R. K. Powers, D. Farina, and C. J. Heckman. Robust and accurate decoding of motoneuron behaviour and prediction of the resulting force output. J. Physiol. 596:2643–2659, 2018.
van Beek, N., D. F. Stegeman, J. C. Van Den Noort, D. H. E. J. Veeger, and H. Maas. Activity patterns of extrinsic finger flexors and extensors during movements of instructed and non-instructed fingers. J. Electromyogr. Kinesiol. 38:187–196, 2018.
Yao, W., R. J. Fuglevand, and R. M. Enoka. Motor-unit synchronization increases EMG amplitude and decreases force steadiness of simulated contractions. J. Neurophysiol. 83:441–452, 2000.
Zatsiorsky, V. M., Z.-M. Li, and M. L. Latash. Enslaving effects in multi-finger force production. Exp. Brain Res. 131:187–195, 2000.
Conflict of interest
The authors have no financial relationships that may cause a conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Associate Editor Jane Grande-Allen oversaw the review of this article.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Dai, C., Cao, Y. & Hu, X. Prediction of Individual Finger Forces Based on Decoded Motoneuron Activities. Ann Biomed Eng 47, 1357–1368 (2019). https://doi.org/10.1007/s10439-019-02240-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10439-019-02240-1