Accurate and representative decoding of the neural drive to muscles in humans with multi-channel intramuscular thin-film electrodes

Abstract

Intramuscular electrodes developed over the past 80 years can record the concurrent activity of only a few motor units active during a muscle contraction. We designed, produced and tested a novel multi-channel intramuscular wire electrode that allows in vivo concurrent recordings of a substantially greater number of motor units than with conventional methods. The electrode has been extensively tested in deep and superficial human muscles. The performed tests indicate the applicability of the proposed technology in a variety of conditions. The electrode represents an important novel technology that opens new avenues in the study of the neural control of muscles in humans. We describe the design, fabrication and testing of a novel multi-channel thin-film electrode for detection of the output of motoneurones in vivo and in humans, through muscle signals. The structure includes a linear array of 16 detection sites that can sample intramuscular electromyographic activity from the entire muscle cross-section. The structure was tested in two superficial muscles (the abductor digiti minimi (ADM) and the tibialis anterior (TA)) and a deep muscle (the genioglossus (GG)) during contractions at various forces. Moreover, surface electromyogram (EMG) signals were concurrently detected from the TA muscle with a grid of 64 electrodes. Surface and intramuscular signals were decomposed into the constituent motor unit (MU) action potential trains. With the intramuscular electrode, up to 31 MUs were identified from the ADM muscle during an isometric contraction at 15% of the maximal force (MVC) and 50 MUs were identified for a 30% MVC contraction of TA. The new electrode detects different sources from a surface EMG system, as only one MU spike train was found to be common in the decomposition of the intramuscular and surface signals acquired from the TA. The system also allowed access to the GG muscle, which cannot be analysed with surface EMG, with successful identification of MU activity. With respect to classic detection systems, the presented thin-film structure enables recording from large populations of active MUs of deep and superficial muscles and thus can provide a faithful representation of the neural drive sent to a muscle.

Figure 1

Thin-film electrode A, the final assembly of the thin-film electrode structure. B, a close-up of the structure tip with the 16 detection sites. C, box for transportation. D, the whole structure. E, FR4 adapter and plug where the polyimide foil is attached. F, dimension of the tip. G, dimension of each oval-shape platinum electrode site at the structure tip.

Figure 2

Schematic diagram of the microfabrication process for development of the thin-film electrode structure Two layers of metal are sandwiched between two layers of polyimide. The polyimide is then opened on the top side to expose the electrode sites.

Figure 3

Impedance measurements Representative example of the impedance of the 16 detection sites before (black) and after (grey) coating with microrough platinum.

Figure 4

Experimental set-up A, Experiment 1: the thin-film electrode was inserted in the abductor digiti minimi muscle and the subject was instructed to abduct the little finger at 10 and 15% of the maximal force. B, Experiment 2: electromyographic signals were recorded from the tibialis anterior muscle with two intramuscular thin-film structures and a grid of surface electrodes while the subject dorsiflexed the ankle exerting 10, 20 and 30% of the maximal force. C, Experiment 3: the subject lay supine and breathed quietly with the thin-film structure inserted into the genioglossus muscle.

Figure 5

Electromyographic signal detection from a thin-film electrode structure implanted in the abductor digiti minimi muscle A, cross-section of a simple muscle with the electrode array within. The array includes 16 detection sites (d₁–d₂– … –d₁₆ from the tip towards the connector). B, four bipolar electromyographic signals obtained during an isometric contraction of the abductor digiti minimi muscle at 15% of the maximal force in Experiment 1. The potential v recorded at channel i is obtained as the difference of the potentials at two adjacent detection sites (with 1 mm inter-site distance): v(ch_i) = v(d_i) − v(d_i+1). Motor unit action potential trains are represented with colour-coded dots. Dots of the same colours are used in A to indicate the location of the motor units inside the muscle. C, a segment of the signal from channel 6 on a large time scale. D, template of the units represented in B, in the channel with the highest amplitude.

Figure 6

Motor unit territory Average action potentials (templates) of two motor units (h and i) detected in Experiment 1 from the abductor digiti minimi muscle during an isometric contraction at 15% of the maximal force across 15 bipolar channels. The number of action potentials included in the average was 104 and 147 for the units h and i, respectively. Spike-triggered averaging resulted in amplitude similar to the background level for electrodes outside the motor unit territory.

Figure 7

Multi-channel representation of motor units Average action potentials (templates) of two motor units (j and k) detected from the abductor digiti minimi muscle during an isometric contraction at 15% of the maximal force in Experiment 1. The number of action potentials included in the average was 147 and 176 for the units j and k, respectively. Signals were high-passed filtered at 500 Hz prior to averaging. The templates of the two units are quite similar in channels 6 and 7 whereas only unit k appears in channels 4 and 5.

Figure 8

Representative firing pattern of motor units from abductor digiti minimi Firing patterns of 31 motor units detected in Experiment 1 during an isometric contraction of the abductor digiti minimi muscle using the thin-film electrode. Force exerted during the contraction is also shown, 15% of maximum.

Figure 9

Representative recordings from tibialis anterior A 1 s segment to show EMG signals acquired from the 16 detection sites on the thin-film electrode inserted in the distal position in the tibialis anterior in Experiment 2. Electromyographic signals are normalized to the maximal peak-to-peak amplitude across the entire contraction relative to each channel. The discharges of the 5 motor units with the highest average action potential peak-to-peak amplitude are shown above each electromyographic trace. Different motor units are represented with different coloured symbols (see legend on the right). The contraction force was 10% of the maximal force. A 200 ms segment of the signal from channel 1 is shown at the lowest part of the figure.

Figure 10

Template similarity across contractions levels Average action potentials (templates) of 7 representative common motor units detected from the tibialis anterior muscle during isometric contractions at 10% (black), 20% (dark grey) and 30% MVC (light grey) in Experiment 2. The templates are highly similar across the three contraction intensities, which indicates that the electromyographic signals were stable over time.

Figure 11

Representative signals from genioglossus A, two channels of electromyographic signals recorded from the genioglossus muscle during quiet breathing through the nose. B, motor unit action potential trains contributing to the composite signals in A. C, electromyographic signals recorded from 15 bipolar channels during a spontaneous swallow. The signals shown in the left and right panels belong to two blocks of data (∼3.5 min) recorded approximately 2.5 h apart.