Residual Motor Signal in Long-Term Human Severed Peripheral Nerves and Feasibility of Neural Signal-Controlled Artificial Limb

doi:10.1016/j.jhsa.2007.02.021

The Journal of Hand Surgery

Volume 32, Issue 5, May–June 2007, Pages 657-666

https://doi.org/10.1016/j.jhsa.2007.02.021 Get rights and content

Purpose

The residual motor pathways after amputation have not been fully elucidated. We sampled potentials from peripheral nerve stumps with intrafascicular electrodes to study residual motor transmission and explore the feasibility of nerve signal-controlled artificial limbs.

Methods

Six intrafascicular electrodes were inserted into the ulnar, radial, and median nerves in the stump of an amputee. An electrode was placed outside the fascicle as a reference. Potentials from 4 of the 6 electrodes per trial were monitored using a 4-channel electromyogram machine, and 32 groups of electrophysiologic tests were conducted under volitional control. Actions included finger extension and flexion, forearm pronation and supination, and wrist extension and flexion. Each action was carried out with light, intermediate, and full efforts. Then, 2 of 6 electrodes randomly chosen per trial were interfaced to a nerve signal-controlled artificial limb. Finger extension and flexion of the prosthesis were tested under volitional control.

Results

The volitional motor nerve potentials uniquely associated with the missing limb were recorded successfully with intrafascicular electrodes. The signal amplitude from the radial nerve was 5.5 μV ± 0.8 (mean ± SD), which was greater than the amplitudes from the ulnar (2.5 μV ± 0.4) and median (2.2 μV ± 0.3) nerves. Under volitional control of the subject, finger extension of the artificial limb was triggered by the radial nerve signal, but the remaining actions were unsuccessful.

Conclusions

The long-term amputee was able to generate motor neuron activity related to phantom limb movement. Intrafascicular electrodes can be used to monitor residual motor nerve activity in the stump, and the amplitude may predict successful control of artificial limbs.

Section snippets

Clinical Data and Experimental Materials

In November 2002, a 31-year-old man was admitted 2 years, 5 months after a severe injury. The patient’s left hand and wrist were crushed by an industrial machine. Salvage was not possible, and his hand was amputated 8 cm proximal to the wrist. He was given a 1 degree of freedom (DOF) myoelectric artificial hand 1 month after the amputation. After written consent and approval by the institutional review board, he took part in this study as a volunteer. On physical examination, he was healthy and

Results

Real electric nerve signaling was recorded by intrafascicular electrodes when volitional actions associated with the missing limb were made. Related muscle groups contracted simultaneously proximal to the amputation site. A total of 32 groups of 6 actions (ie, finger extension, finger flexion, wrist extension, wrist flexion, forearm pronation, forearm supination) were successfully recorded. Stable nerve signal harvested by intrafascicular electrodes was displayed on the EMG instrument (Fig. 4).

Discussion

The key issue of motor control in bionic prosthesis research, especially for prostheses with multiple DOF, is reliably and reproducibly recording and transmitting neural signals. Collecting information from peripheral nerves for prosthesis control may be preferred over myoelectric sources for reasons including a lack of stable open-loop or essential closed-loop feedback,³⁶ muscle fatigue,³ and control limited to one movement at a time.³⁷

Potential impediments to interfacing artificial limbs to

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Recovering motor activation signals from peripheral nerve fascicles is the most acknowledged strategy for the control of prostheses driven by electroneurogram. Yet, restoring signals capturing correct muscular co-activation dynamics is still a challenge. This study aims to identify, through a novel hybrid paradigm, a reference model for muscular co-activation dynamics, whose parameters could be controlled by electroneurogram. A dataset related to an animal study was exploited. Muscular co-activation was modelled in the phase space using the Poincaré plot. The information of a selected electroneurogram channel about gait events was extracted and employed for the first time to design the Poincaré section. Utilising the intersection points, proposed iterated maps, X- and Y-maps, were trained to develop a reference model. The cross-validated prediction error of the model was 2.06 × 10^-4 ± 0.0011 and 7.17 × 10^-6 ± 4.59 × 10^-5 for the X- and Y-maps, respectively. Analogous large- and small-scale patterns of the recurrence plots corresponding to sample model-generated and true data verified their similar dynamical regimes. Low variability of the model parameters, intra- and inter-trially, corroborated generalisability of the model. The viability of exploiting electroneurogram for modelling and predicting muscular co-activation was established. Leveraging reference model not only simplifies, but also opens up new possibilities for near-natural control of prostheses.
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Alternative approaches such as non-invasive haptic feedback (vibro- or electro-tactile stimulation) were proved to be effective (Antfolk et al., 2013), but they are just an expedient to signal the prosthetic users that they are interacting with the environment, since they do not mimic the real behaviour of the sensorial fibres like the electrical stimulation of the nerves. To date, only a few studies have provided evidence of the feasibility to use the ENG recorded from peripheral nerves to control a prosthetic device (Dhillon et al., 2004; Jia et al., 2007; Rossini et al., 2010; Micera et al., 2011; Wendelken et al., 2017; Noce et al., 2018). In Fig. 1 a functional scheme of the neural control of a prosthesis is shown.
This paper proposes a new approach for neural control of hand prostheses, grounded on pattern recognition applied to the envelope of neural signals (eENG).
The ENG envelope was computed by taking into account the amplitude and the occurrence of the spike in the neural recording. A pattern recognition algorithm applied on muscular signals was defined as a reference and a comparative analysis with traditionally adopted Spike Sorting Algorithms (SSA) for neural signals has been carried out. Method validation was divided in two parts: firstly, neural signals recorded from one amputee subject through intraneural electrodes were offline analyzed to discriminate between the two performed gestures; secondly, algorithm performance decay with the increase of the number of classes was studied through synthetic data.
An accuracy of 98.26% with real data was reached with the pattern recognition applied to eENG. SSA reached an accuracy of 70%. Increasing the number of classes worsens the accuracy of this algorithm. Additionally, computational time for the pattern recognition applied to eENG is very low (32.6 μs for each sample in the data window analyzed).
The eENG was proved to be more reliable in decoding the user intention than the SSA algorithm and it is computationally efficient.
It was demonstrated that it is possible to apply the well-known techniques of EMG pattern recognition to a conveniently processed neural signal and can pave the way to the application of neural gesture decoding in upper limb prosthetics.
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Being able to control an upper limb prosthesis by means of the signals recorded from the peripheral nerves is not a trivial task. New generations of neural electrodes are able to record this information but the quality of the signal can make difficult the extraction of the useful information. Several techniques have been adopted both for central and peripheral acquisitions in order to remove the noise and/or enhance the electrical activity generated by the brain or carried by the nerves.
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MAA outperforms the other techniques because it is capable of detecting a high amount of RPs and, compared to NEO, with a reduced number of FPs.
MAA needs only the information of the duration of the action potential while the NEO and the WD require the frequency and/or the shape of the action potentials.
NEO and WD are algorithms requiring information about the signal, not a priori known. MAA, then, seems most suitable for online applications.
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Transverse cryostat sections (10 μm thick) were prepared from the middle parts of the conduits for immunohistochemical staining and histomorphometric analysis. In the stimulation groups, after nerve repair, 2 modified intrafascicular electrodes were implanted in both sides of the sciatic nerve stump 0.5 cm from the suture site, as we previously described [28–31]. The insulated electrodes were led to a stimulator (Grass S48 Square Pulse stimulator, Astro-Med Inc, West Warwick, RI).
Peripheral nerve injuries often lead to incomplete recovery and contribute to significant disability to approximately 360,000 people in the USA each year. Stem cell therapy holds significant promise for peripheral nerve regeneration, but maintenance of stem cell viability and differentiation potential in vivo are still major obstacles for translation. Using a made-in-house 96-well vertical electrical stimulation (ES) platform, we investigated the effects of different stimulating pulse frequency, duration and field direction on human neural crest stem cell (NCSC) differentiation. We observed dendritic morphology with enhanced neuronal differentiation for NCSCs cultured on cathodes subject to 20 Hz, 100μs pulse at a potential gradient of 200 mV/mm. We further evaluated the effect of a novel cell-based therapy featuring optimized pulsatile ES of NCSCs for in vivo transplantation following peripheral nerve regeneration. 15 mm critical-sized sciatic nerve injuries were generated with subsequent surgical repair in sixty athymic nude rats. Injured animals were randomly assigned into five groups (N = 12 per group): blank control, ES, NCSC, NCSC + ES, and autologous nerve graft. The optimized ES was applied immediately after surgical repair for 1 h in ES and NCSC + ES groups. Recovery was assessed by behavioral (CatWalk gait analysis), wet muscle-mass, histomorphometric, and immunohistochemical analyses at either 6 or 12 weeks after surgery (N = 6 per group). Gastrocnemius muscle wet mass measurements in ES + NCSC group were comparable to autologous nerve transplantation and significantly higher than other groups (p < 0.05). Quantitative histomorphometric analysis and catwalk gait analysis showed similar improvements by ES on NCSCs (p < 0.05). A higher number of viable NCSCs was shown via immunochemical analysis, with higher Schwann cell (SC) differentiation in the NCSC + ES group compared to the NCSC group (p < 0.05). Overall, ES on NCSC transplantation significantly enhanced nerve regeneration after injury and repair, and was comparable to autograft treatment. Thus, ES can be a potent alternative to biochemical and physical cues for modulating stem cell survival and differentiation. This novel cell-based intervention presents an effective and safe approach for improved outcomes after peripheral nerve repair.
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Despite that, most of the invasive neural interfaces developmental process almost completely relies on the conjunct efforts of bioengineers and neurophysiologists, whereas the figure of the surgeon is considered quite marginal and involved only at the moment of the implant. So far, intrafascicular electrodes implanted in amputees were able to record volitional motor activity used by the patient to control the grip of a single degree of freedom, tongs-like, hand prosthesis [26], and the flexion-extension of a robotic finger [27]. Our group performed the first implant of multiple intraneural multielectrodes in multiple peripheral nerves of the stump of a human amputee, with the aim of controlling a sensorized cybernetic hand prosthesis and to deliver artificial afferent stimulations [28,29].
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Invasive neural interfaces developmental process almost completely relies on the efforts of bioengineers and neurophysiologists; however, the surgeon is responsible for intra and perioperative factors. Therefore, he deserves to play a major role also at the stage of specifying the requirements, to satisfy the requisites of a safe, stable, and long-lasting implant.
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: No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

¹: X.J., X.Z., J.Z., T.C., and Z.C. were supported by the Key Program of the National Natural Science Foundation of the People’s Republic of China (39930070).

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NerveResidual Motor Signal in Long-Term Human Severed Peripheral Nerves and Feasibility of Neural Signal-Controlled Artificial Limb

Purpose

Methods

Results

Conclusions

Section snippets

Clinical Data and Experimental Materials

Results

Discussion

Phys Med Rehabil Clin N Am

J Hand Surg

J Hand Surg

Brain Res Bull

J Neurosci Methods

Brain Res

Functional outcome of patients with proximal upper limb deficiency—acquired and congenital

Clin Rehabil

Myoelectric prosthesesA long-term follow-up and a study of the use of alternate prostheses

J Bone Joint Surg

Prosthetic rehabilitation of upper limb amputees: a five year review

Clin Rehabil

Prosthesis rejection in children with a unilateral congenital arm defect

Clin Rehabil

Myoelectric prostheses for below-elbow amputees: the Trent experience

Int Disabil Stud

Electrically powered prostheses for the adult with an upper limb amputation

J Bone Joint Surg

Prescription of the first prosthesis and later use in children with congenital unilateral upper limb deficiency: a systematic review

Prosthet Orthot Int

Clinical detection and movement recognition of neuro signals

J Zhejiang Univ Sci B

Direct neural sensory feedback and control of a prosthetic arm

IEEE Trans Neural Syst Rehabil Eng

Effects of short-term training on sensory and motor function in severed nerves of long-term human amputees

J Neurophysiol

Regeneration microelectrode array for peripheral nerve recording and stimulation

IEEE Trans Biomed Eng

Silicon-substrate microelectrode arrays for parallel recording of neural activity in peripheral and cranial nerves

IEEE Trans Biomed Eng

Neural interfaces for regenerated nerve stimulation and recording

IEEE Trans Rehabil Eng

Acute peripheral nerve recording characteristics of polymer-based longitudinal intrafascicular electrodes

IEEE Trans Neural Syst Rehabil Eng

Selective motor unit recruitment via intrafascicular multielectrode stimulation

Can J Physiol Pharmacol

Metallized polymer fibers as leadwires and intrafascicular microelectrodes

J Neurosci Methods

Nerve
Residual Motor Signal in Long-Term Human Severed Peripheral Nerves and Feasibility of Neural Signal-Controlled Artificial Limb