Electromyography: Accessing populations of motor units
A new device improves the way scientists can record the activity of motor units in a wide range of animals and settings.
- Department of Neurosciences, School of Medicine, Case Western Reserve University, United States
Active, purposeful movement is a defining feature of animal life and requires precise coordination between the nervous system and muscles. Specialized nerve cells, known as motoneurons, constitute the final output of the central nervous system, and are responsible for activating muscle. Each motoneuron can innervate multiple muscle fibers, and a single electrical impulse in the motoneuron induces a corresponding impulse in these fibers, causing them to contract. Together, a single motoneuron and the muscle fibers it innervates are referred to as a motor unit (Sherrington, 1925).
Recording the electrical activity of individual motor units during voluntary contractions became possible in the 1920s with the development of needle electrodes that could be inserted into muscles. This approach has revealed many fundamental properties of the neuromuscular system by allowing indirect yet accurate and relatively non-invasive measurement of impulse times in spinal motoneurons (Adrian and Bronk, 1929; Farina and Gandevia, 2023). But it also has many limitations, such as needle electrodes getting displaced during movement and only being able to record a small number of motor units at a time. In addition, it is often challenging to assign a given impulse to a specific unit using this method because an individual electrode may detect impulses with similar electrical profiles from multiple motor units.
However, scientists can bypass some of these limitations. For example, it is possible to reliably isolate the activity of multiple individual units during movement by using a large number of electrodes organized into an array, as each motor unit will produce a unique pattern of waveforms across the electrodes. In recent decades, new techniques have been developed to record from larger numbers of motor units, including high-density electrode arrays that can be implanted into muscle, and arrays that record relatively smaller signals at many sites across the surface of the skin (Muceli et al., 2022; Negro et al., 2016).
While each of these methods has distinct strengths and limitations, there remains a need for a widely available device that is capable of the following: providing stable recordings during natural movements, when muscles rapidly lengthen, shorten, and twist; being used in a broad range of experimental preparations, muscles, and animal groups; recording many motor units simultaneously; and working for weeks or even months after implantation. Now, in eLife, Samuel Sober and colleagues at various institutions in the United States, Canada, Portugal and Germany – including Bryce Chung (Emory University) and Muneeb Zia (Georgia Institute of Technology) as joint first authors – report how they have successfully developed versatile devices called Myomatrix arrays that meet these criteria (Chung et al., 2023).
The instruments consist of four long, flexible threads that each terminate in eight electrodes (Zia et al., 2020; Lu et al., 2022). These threads can either be inserted directly into a muscle or attached to the overlying connective tissue, enabling the electrodes to move with the muscle and maintain stable recordings. Chung et al. first tested the device in freely behaving mice, showing that it provided better recordings of the activity of individual motor units than traditional wire electrodes. The team was then able to demonstrate that Myomatrix arrays could record well-isolated motor units across a wide range of muscle morphologies, species and behaviors: this included the vocal and respiratory muscles of songbirds as they breathed, the hip muscles of bullfrogs during reflex contractions, and the abdominal muscles of hawkmoth larvae undergoing a protocol commonly used in locomotion studies.
Next, Chung et al. showed that their approach could simultaneously provide stable recordings from multiple motor units, including for large muscles and during active movement (for example, for the forelimb muscles of rhesus macaques performing a reaching task). Finally, they successfully confirmed that Myomatrix arrays could be used for long-term recordings, including over at least two months after implantation in mice. Overall, this study presents a compelling validation of a novel device for high-quality, large-scale, long-term motor unit recordings in a broad range of applications.
Investigating how the nervous system controls movement often requires large-scale recordings from the motor unit population. For example, it is still unclear to what extent the brain has the flexibility to voluntarily recruit individual motor units. Under typical experimental conditions, motor units are normally activated in a fixed order as force increases, from the smallest motoneurons to the largest (Henneman et al., 1965). Even with significant training and effort, human subjects have difficulty reversing this recruitment order voluntarily, and activating larger units while suppressing smaller ones (Bräcklein et al., 2022). However, recent work in nonhuman primates suggests that the motor cortex may be capable of independently controlling individual motor units in certain contexts (Marshall et al., 2022). Recent advances in electrode design, such as the Myomatrix arrays described by Chung et al., are expected to accelerate our understanding of flexible recruitment and other major research questions in the coming years.
References
-
The neural control of movement: a century of in vivo motor unit recordings is the legacy of Adrian and BronkThe Journal of Physiology 7:JP285319.https://doi.org/10.1113/JP285319
-
Functional significance of cell size in spinal motoneuronsJournal of Neurophysiology 28:560–580.https://doi.org/10.1152/jn.1965.28.3.560
-
ConferenceHigh-performance flexible microelectrode array with PEDOT:PSS coated 3D micro-cones for electromyographic recordingAnnual International Conference of the IEEE Engineering in Medicine and Biology Society. pp. 5111–5114.https://doi.org/10.1109/EMBC48229.2022.9871052
-
Flexible neural control of motor unitsNature Neuroscience 25:1492–1504.https://doi.org/10.1038/s41593-022-01165-8
-
Multi-channel intramuscular and surface EMG decomposition by convolutive blind source separationJournal of Neural Engineering 13:026027.https://doi.org/10.1088/1741-2560/13/2/026027
-
Remarks on some aspects of reflex inhibitionProceedings of the Royal Society of London. Series B. 97:519–545.
-
Flexible multielectrode arrays with 2-D and 3-D contacts for in vivo electromyography recordingIEEE Transactions on Components, Packaging, and Manufacturing Technology 10:197–202.https://doi.org/10.1109/tcpmt.2019.2963556
Article and author information
Author details
Britton A Sauerbrei
Publication history
- Version of Record published: January 4, 2024 (version 1)
Copyright
© 2024, Kirk and Sauerbrei
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 885
- views
-
- 72
- downloads
-
- 0
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Electromyography: Accessing populations of motor units
eLife 13:e94764.
https://doi.org/10.7554/eLife.94764
Further reading
-
- Medicine
- Neuroscience
Retinitis pigmentosa (RP) is an inherited retinal disease in which there is a loss of cone-mediated daylight vision. As there are >100 disease genes, our goal is to preserve cone vision in a disease gene-agnostic manner. Previously we showed that overexpressing TXNIP, an α-arrestin protein, prolonged cone vision in RP mouse models, using an AAV to express it only in cones. Here, we expressed different alleles of Txnip in the retinal pigmented epithelium (RPE), a support layer for cones. Our goal was to learn more of TXNIP’s structure-function relationships for cone survival, as well as determine the optimal cell type expression pattern for cone survival. The C-terminal half of TXNIP was found to be sufficient to remove GLUT1 from the cell surface, and improved RP cone survival, when expressed in the RPE, but not in cones. Knock-down of HSP90AB1, a TXNIP-interactor which regulates metabolism, improved the survival of cones alone and was additive for cone survival when combined with TXNIP. From these and other results, it is likely that TXNIP interacts with several proteins in the RPE to indirectly support cone survival, with some of these interactions different from those that lead to cone survival when expressed only in cones.
-
- Neuroscience
Vesicles within presynaptic terminals are thought to be segregated into a variety of readily releasable and reserve pools. The nature of the pools and trafficking between them is not well understood, but pools that are slow to mobilize when synapses are active are often assumed to feed pools that are mobilized more quickly, in a series. However, electrophysiological studies of synaptic transmission have suggested instead a parallel organization where vesicles within slowly and quickly mobilized reserve pools would separately feed independent reluctant- and fast-releasing subdivisions of the readily releasable pool. Here, we use FM-dyes to confirm the existence of multiple reserve pools at hippocampal synapses and a parallel organization that prevents intermixing between the pools, even when stimulation is intense enough to drive exocytosis at the maximum rate. The experiments additionally demonstrate extensive heterogeneity among synapses in the relative sizes of the slowly and quickly mobilized reserve pools, which suggests equivalent heterogeneity in the numbers of reluctant and fast-releasing readily releasable vesicles that may be relevant for understanding information processing and storage.
