Double nerve intraneural interface implant on a human amputee for robotic hand control

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Abstract

Objectives

The principle underlying this project is that, despite nervous reorganization following upper limb amputation, original pathways and CNS relays partially maintain their function and can be exploited for interfacing prostheses.

Aim of this study is to evaluate a novel peripheral intraneural multielectrode for multi-movement prosthesis control and for sensory feed-back, while assessing cortical reorganization following the re-acquired stream of data.

Methods

Four intrafascicular longitudinal flexible multielectrodes (tf-LIFE4) were implanted in the median and ulnar nerves of an amputee; they reliably recorded output signals for 4 weeks. Artificial intelligence classifiers were used off-line to analyse LIFE signals recorded during three distinct hand movements under voluntary order.

Results

Real-time control of motor output was achieved for the three actions. When applied off-line artificial intelligence reached >85% real-time correct classification of trials. Moreover, different types of current stimulation were determined to allow reproducible and localized hand/fingers sensations. Cortical organization was observed via TMS in parallel with partial resolution of symptoms due to the phantom-limb syndrome (PLS).

Conclusions

tf-LIFE4s recorded output signals in human nerves for 4 weeks, though the efficacy of sensory stimulation decayed after 10 days. Recording from a number of fibres permitted a high percentage of distinct actions to be classified correctly. Reversal of plastic changes and alleviation of PLS represent corollary findings of potential therapeutic benefit.

Significance

This study represents a breakthrough in robotic hand use in amputees.

Introduction

One of the most intriguing fields for translational medicine deals with the application of robotics technologies to human health. In particular, the ability to interface a robotic device with a human brain after a given damage opens up a number of exciting applications in replacing lost function. An important chapter in translational research within the field of bio-engineering and bio-materials aiming to restore lost abilities in humans, deals with the development of a robotic hand to replace the missing limb following amputation.

Upper limb amputees compensate for cosmetic and functional deficits using prostheses whose present performance is poor for dexterity, control features, anthropomorphism and interface efficacy (e.g., information transfer rate, rate of correct classification and quality/amount of feed-back) (Micera et al., 2006, Tonet et al., 2007). In fact, commercially available hand prostheses are little more than unidimensional pincers operating under electromyographic (EMG) and sight control, without natural or artificial sensory feed-back. Current research focuses on bionic anthropomorphic prostheses connected to the peripheral nervous system (PNS) via bidirectional neural interfaces, which can restore physiological conditions to some extent (Dhillon et al., 2004, Jia et al., 2007), or on nerve transposition for targeted reinnervation (Kuiken et al., 2007, Kuiken et al., 2009). Peripheral nerve interfaces aim to detect electrical activity of the nerve fibres and/or to excite them as selectively as possible (Navarro et al., 2005, Stieglitz et al., 2005, Tesfayesus and Durand, 2007, Micera et al., 2008). Recently, a novel thin film longitudinal intrafascicular flexible multielectrode (tf-LIFE4), assuring biocompatibility and flexibility for long-term use, has been developed for multiple-site recordings (Hoffmann and Kock, 2005, Citi et al., 2008) and tested in experimental models (Lago et al., 2007). In the present study, the first implant of tf-LIFE4s was carried out on a human volunteer with the following aims:

  • o

    to test reliability and compatibility of tf-LIFE4s for the 4 week period allowed by the European Health Authorities;

  • o

    to record electroneurographic (ENG) signals from motor fibres during rest and voluntary emitted commands for three distinct movements dispatched to the missing hand/fingers

  • o

    to implement classifiers to correctly interpret commands and govern a robotic hand;

  • o

    to deliver sensory feed-back as a surrogate of action-driven perception;

  • o

    to correlate performance and training-related changes with topographical reorganization of sensorimotor brain areas and with clinical modifications.

Section snippets

Subject and methods

A 26-year-old right-handed male university graduate had suffered trans-radial amputation of left arm in a car accident in 2007. He had previously tried aesthetic and myoelectric prostheses. Forearm stump muscles were entirely atrophied and non-functional on EMG evaluation. Previous medical history was unremarkable. Full neurological and neurographic/electromyographic examinations were normal. Neuropsychological and neuropsychiatric tests (MMPI-2, WAIS) demonstrated normal comprehension and

Results

A progressive improvement of the tf-LIFE4s signal-to-noise ratio was observed in the post-surgery period, stabilising after 10 days. All the contacts of the 4 electrodes recorded properly during the entire 4-week experimental period. Three of the four electrodes elicited sensations with appropriate stimulation settings for 10 days. Before implantation, the patient experienced a moderate PLS, perceived as if, ‘…the missing hand is still attached to the stump and tightly fastened and immobilized by

Discussion

Limb amputation triggers anterograde/retrograde changes to and from the stump nerves extending to the contralateral cortex (Merzenich et al., 1984, Calford and Tweedale, 1988), as well as functional reorganization of the relevant CNS areas. In the de-efferented motor cortex, there is an increase in size and excitability of the representation of stump muscles, while the de-afferented S1 cortex progressively responds to inputs from skin and muscles adjacent to the stump (Cohen et al., 1991, Kaas,

Acknowledgements

This study was partially supported by the Commission of the European Community within the projects NEUROBOTICS (Contract No. FP6-IST-001917 – The fusion of NEUROscience and roBOTICS) and TIME (Contract No.: FP7-ICT-224012 – Transverse, Intrafascicular Multichannel Electrode system for induction of sensation and treatment of phantom limb pain in amputees). None of these funding sources had a role in study design, data collection, data analysis, data interpretation, or writing of the report. None

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    These authors contributed equally to this work.

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