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Research ArticleResearch Article: New Research, Novel Tools and Methods

Larger and Denser: An Optimal Design for Surface Grids of EMG Electrodes to Identify Greater and More Representative Samples of Motor Units

Arnault H. Caillet, Simon Avrillon, Aritra Kundu, Tianyi Yu, Andrew T. M. Phillips, Luca Modenese and Dario Farina
eNeuro 1 September 2023, 10 (9) ENEURO.0064-23.2023; https://doi.org/10.1523/ENEURO.0064-23.2023
Arnault H. Caillet
1Department of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom
2Department of Civil and Environmental Engineering, Imperial College London, London SW7 2AZ, United Kingdom
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Simon Avrillon
1Department of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom
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Aritra Kundu
1Department of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom
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Tianyi Yu
1Department of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom
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Andrew T. M. Phillips
2Department of Civil and Environmental Engineering, Imperial College London, London SW7 2AZ, United Kingdom
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Luca Modenese
3Graduate School of Biomedical Engineering, University of New South Wales, Sydney, New South Wales 1466, Australia
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Dario Farina
1Department of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom
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Figures

  • Extended Data
  • Figure 1.
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    Figure 1.

    The eight grid configurations considered in this study. From the first grid of 256 electrodes (A, grid size: 36 cm2, interelectrode distance (IED): 4 mm), six shallower and smaller grids (B–G) were artificially obtained by discarding the relevant electrodes. B–D, Density analysis: 8-, 12-, and 16-mm IED. E–G, Size analysis: 7.7, 3.6, and 2 cm2 surface area. H, The ultradense prototyped grid of 256 electrodes (grid size: 9 cm2, IED: 2 mm).

  • Figure 2.
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    Figure 2.

    Results from the 200 simulated motor units (MUs) with 84 configurations of grids of electrodes. A, Each solid line represents a motor unit territory, the scatters being the muscle fibers. Blues lines are the theoretically identifiable motor units with a grid of 21.6 cm2 and an interelectrode distance (IED) of 18 mm, while the orange lines are the motor units revealed with a grid of 21.6 cm2 and an IED of 2 mm. Gray lines represent the nonidentifiable motor units. The percentage of theoretically identifiable motor units (B) and their distance from the skin (C) are reported for the 84 configurations.

  • Figure 3.
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    Figure 3.

    Discharge times of the maximum number of motor units identified in one participant (S1) at 30% (A) and 50% maximal voluntary contraction (MVC) (B), with 79 and 58 identified motor units, respectively. The motor units were identified with separated decompositions of the four grids of 64 electrodes (4-mm interelectrode distance). C, Discharge times of the 30 first recruited motor units during the ascending ramp of force (black curve) at 30% MVC (black box in A).

  • Figure 4.
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    Figure 4.

    Effect of the electrode density on the number of identified motor units N at 30% (A, B) and 50% maximal voluntary contraction (MVC) (C, D). The boxplots in the left column report the absolute number N of identified motor units per participant (gray dots) and the median (orange line), quartiles, and 95% range across participants. In the right column, the normalized number of motor units N¯ logarithmically decreases with interelectrode distance d (4, 8, 12, and 16 mm in abscissa) as N¯=195−68log(d)(r2=1.0,p=2.5⋅10−5) at 30% MVC (B) and N¯=196−71log(d)(r2=0.99,p=0.001) at 50% MVC (D). The standard deviation of N¯ across subjects is displayed with vertical bars. Moreover, the quality of the motor unit pulse trains (i.e., decomposition accuracy, estimated by the PNR) increased when increasing the density of electrodes (Extended Data Fig. 4-3 for more details). Two decomposition procedures were considered for the 256-electrode condition; the grid of 256 black electrodes indicates that the 256 signals were simultaneously decomposed and the grid of 256 electrodes of four different colors indicates that four subsets of 64 electrodes were decomposed. To maintain consistency with the computational study, the trendlines were fitted with the 4*64 condition, which returned the higher number of identified motor units (Extended Data Fig. 4-1 for the other fitting condition). It is worth noting that computationally increasing the density of electrodes by resampling the EMG signals with a spatial interpolation did not reveal any previously hidden motor units (Extended Data Fig. 4-2).

  • Figure 5.
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    Figure 5.

    Effect of the size of the grid on the number of identified motor units N at 30% (A, B) and 50% maximal voluntary contraction (MVC) (C, D). The boxplots in the left column report the absolute number N of identified motor units per participant (gray dots) and the median (orange line), quartiles, and 95% range across participants. In the right column, the normalized number of motor units N¯ logarithmically decreases with the size of the grid s (2, 3.8, 7.7, and 36 cm2 in abscissa) as N¯=−20+33log(s)(r2=0.99,p=3.0⋅10−4) at 30% MVC (B), and N¯=−19+32log(s)(r2=0.98,p=0.001) at 50% MVC (D). The standard deviation of N¯ across subjects is displayed with vertical bars. Moreover, the quality of the identified motor unit pulse trains (i.e., decomposition accuracy, estimated by the pulse-to-noise ratio) increased when increasing the size of the grid (Extended Data Fig. 4-3 for more details). Two decomposition procedures were considered for the 256-electrode condition; the grid of 256 black electrodes indicates that the 256 signals were simultaneously decomposed and the grid of 256 electrodes of four different colors indicates that four subsets of 64 electrodes were decomposed. To maintain consistency with the computational study, the trendlines were fitted with the 4*64 condition, which returned the higher number of identified motor units (Extended Data Fig. 4-1 for the other fitting condition).

  • Figure 6.
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    Figure 6.

    Effect of the number n of electrodes on the normalized number N¯ of identified motor units at 30% (A) and 50% maximal voluntary contraction (MVC) (B). The discrete results per participant are displayed with gray data points. The average values N¯ per condition are displayed with black crosses. Weighted logarithmic trendlines were fitted to the data and returned (A) N¯=−104+37log(n)(r2=0.98,p=0.018) , and (B) N¯=−113+38log(n)(r2=0.95,p=0.016) . Two decomposition procedures were considered for the 256-electrode condition; the grid of 256 black electrodes indicates that the 256 signals were simultaneously decomposed and the grid of 256 electrodes of four different colors indicates that four subsets of 64 electrodes were decomposed. To maintain consistency with the computational study, the trendlines were fitted with the 4*64 condition, which returned the higher number of identified motor units (Extended Data Fig. 4-1 for the other fitting condition).

  • Figure 7.
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    Figure 7.

    A, Typical frequency distribution of motor unit force recruitment thresholds in a human TA. The black dashed lines denote the theoretical portions of the population of motor units recruited at 30% and 50% maximal voluntary contraction (MVC). Effect of the grid density (B, D, F) and grid size (C, E, G) on the percentage of early recruited motor units identified at 30% (B, C, F, G) and 50% MVC (D, E). The boxplots report the results per participant (gray dots) and the median (orange line), quartiles, and 95% range across participants. (F) At 30% MVC, the percentage of early recruited identified motor units logarithmically decreases with interelectrode distance d (4, 8, 12, and 16 mm in abscissa) as 44.6−13.1log(d)(r2=0.91,p=2.8⋅10−3) . (G) At 30% MVC, the percentage of early recruited identified motor units does not vary with the size of the grid s (2, 3.8, 7.7, and 36 cm2 in abscissa), the logarithmic trendline fitting (20.5+1.2log(s) ) returning a negligible slope and low r2=0.28(p=8⋅10−4) . The standard deviation across subjects is displayed with vertical bars. Two decomposition procedures were considered for the 256-electrode condition; the grid of 256 black electrodes indicates that the 256 signals were simultaneously decomposed and the grid of 256 electrodes of four different colors indicates that four subsets of 64 electrodes were decomposed. To maintain consistency with the computational study, the trendlines were fitted with the 4*64 condition, which returned the higher number of identified motor units (Extended Data Fig. 4-1 for the other fitting condition). We did not report the results when five or fewer motor units were identified in one condition for three or more participants.

  • Figure 8.
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    Figure 8.

    Effect of the electrode density on the correlation ρ between the profiles of motor unit action potentials (MUAP) detected over adjacent electrodes (A) at 30% (B) and 50% maximal voluntary contraction (MVC) (C). The profile of the MUAP detected over the red electrode was compared with those detected over the four adjacent electrodes separated by a 4 mm (orange), 8 mm (blue), 12 mm (green), and 16 mm (purple) interelectrode distance (A). The boxplots denote the correlation coefficient ρ per participant (gray dots) and the median (orange line), quartiles, and 95% range across participants.

  • Figure 9.
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    Figure 9.

    Results for the ultradense prototyped grid (2-mm interelectrode distance (IED), 5 × 1.8 cm, 256 electrodes). A, Description of the ultradense grid, where gray circles represent the electrodes. On average, the correlation between the profiles of MUAPs detected over electrodes separated by an IED of 2 mm (orange), 4 mm (blue), and 8 mm (purple) reached ρ = 0.98, 0.96, and 0.92 at 30% maximal voluntary contraction (MVC), respectively, and 0.93, 0.88, and 0.85 at 50% MVC, respectively. B, Series of discharge times for motor units identified at 30% (left) and 50% MVC (right). The dark ticks represent the discharge times identified with a grid of electrodes with an 8-mm IED. The discharge times in blue were additionally identified with a grid of electrodes with a 4-mm IED, and the discharge times in red were additionally identified with a grid of electrodes with a 2-mm IED. All the pulse trains identified with one grid were also identified with the denser grids. C, Effect of electrode density on the number of identified motor units at 30% (scatters) and 50% MVC (triangles). The trendlines from the density analysis in Figure 4B,D are also reported (red dotted lines). To maintain consistency with the other results, the grid was decomposed as four independent subsets of 64 electrodes, as explained in Materials and Methods, to identify the higher number of motor units.

Extended Data

  • Figures
  • Extended Data Figure 4-1

    Effect of the density of the grid (A, D), the size of the grid (B, D), and the number of electrodes (C, F) on the normalized number N¯ of identified motor units at 30% (A–C) and 50% MVC (D–F). N¯ was estimated after decomposing the full grid of 256 electrodes and manually editing the motor unit pulse trains. Vertical bars (A, B, D, E) are the standard deviation of N¯ across subjects, scatters are the individual data points, and crosses are their mean (C, F). Logarithmic trendlines were fitted between the averaged values N¯ and IED, grid size, and number of channels, as in Figures 4-6 of the main document. Here, the trendlines were fitted with the values obtained from the decomposition of the full grid of 256 electrodes. Consistent with the results provided in the main document, N¯ increased with electrode density ( d), grid size (s) , and with the number of electrodes (n) following statistically significant logarithmic trendlines (p < 0.05). At 30% MVC, N¯=198−67log⁡(d)(r2=0.92) , N¯=−10+31log⁡(s)(r2=0.98) , andN¯=−78+32log⁡(n)(r2=0.90) . At 50% MVC, N¯=204−69log⁡(d)(r2=0.92) , N¯=5+28log⁡(s)(r2=0.98) , and N¯=−57+29log⁡(n)(r2=0.90) . It is noteworthy that the trendlines exhibited more pronounced plateaus (lower b value in the y=a+b⋅log⁡(x) trendlines) with the decomposition of the full grid of 256 electrodes than with the decomposition of subsets of 64 electrodes. Download Figure 4-1, TIF file.

  • Extended Data Figure 4-2

    Correlation ρ between experimentally recorded (left, black) and interpolated (right, green) EMG signals (right, black). Using the ultradense grid of 256 electrodes (2-mm IED) at 30% MVC, we spatially interpolated down-sampled montages of 4 × 9 electrodes with an IED of 8 mm and 5 × 13 electrodes with an IED of 4 mm to generate 5 × 13 (4-mm IED) and 10 × 26 (2-mm IED) grids of electrodes, respectively. In these interpolated grids, 25% of the signals were therefore experimentally recorded (right, black) and 75% interpolated (right, green). After comparing interpolated and experimentally recorded grids of electrodes, we observed that a better signal reconstruction was obtained with the 2-mm IED, with a correlation coefficient of ρ = 0.93 ± 0.09 between recorded and interpolated signals. We identified 4 and 19 motor units from the interpolated grid with a 4- and 2-mm IED, respectively, versus 19 and 24 motor units with the experimentally recorded signals. We only identified the same motor units as identified with the original less dense grids used to generate the interpolation. These results indicate that interpolation is not sufficient to reconstruct signals from a lower spatial sampling. This may be due to the spatial bandwidth which is greater than the inverse of the minimal interelectrode distance used or to the edge effects of the interpolation due to the relatively small size of the grid. Download Figure 4-2, TIF file.

  • Extended Data Figure 4-3

    Effect of the electrode density (A, C) and grid size (B, D) on the average PNR across the identified spike trains at 30% MVC (A, B) and 50% MVC (C, D). The boxplots report the average PNRs per participant (grey dots) and the median (orange line), quartiles, and 95% range across participants. We calculated the average PNR value for the motor unit spike trains (PNR > 28 dB) identified in each subject and condition. The average PNR across identified motor units increased together with both the density and the size of the grid. The lowest PNR values were observed with 16 mm-IED (30 ± 1.8 dB at 30% MVC and 29 ± 1.2 dB at 50% MVC) and with a grid of 2 cm2 (31 ± 0.9 dB at 30% MVC and 30 ± 0.9 dB at 50% MVC). The highest PNR was observed with 4 mm-IED and a grid of 36 cm2 (36 ± 0.7 dB at 30% MVC and 37 ± 0.7 dB at 50% MVC), enabling the operators to quickly edit the identified motor units. Download Figure 4-3, TIF file.

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Larger and Denser: An Optimal Design for Surface Grids of EMG Electrodes to Identify Greater and More Representative Samples of Motor Units
Arnault H. Caillet, Simon Avrillon, Aritra Kundu, Tianyi Yu, Andrew T. M. Phillips, Luca Modenese, Dario Farina
eNeuro 1 September 2023, 10 (9) ENEURO.0064-23.2023; DOI: 10.1523/ENEURO.0064-23.2023

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Larger and Denser: An Optimal Design for Surface Grids of EMG Electrodes to Identify Greater and More Representative Samples of Motor Units
Arnault H. Caillet, Simon Avrillon, Aritra Kundu, Tianyi Yu, Andrew T. M. Phillips, Luca Modenese, Dario Farina
eNeuro 1 September 2023, 10 (9) ENEURO.0064-23.2023; DOI: 10.1523/ENEURO.0064-23.2023
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Keywords

  • action potentials
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