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      Comparison of linear frequency and amplitude modulation for intraneural sensory feedback in bidirectional hand prostheses

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          Abstract

          Recent studies have shown that direct nerve stimulation can be used to provide sensory feedback to hand amputees. The intensity of the elicited sensations can be modulated using the amplitude or frequency of the injected stimuli. However, a comprehensive comparison of the effects of these two encoding strategies on the amputees’ ability to control a prosthesis has not been performed. In this paper, we assessed the performance of two trans-radial amputees controlling a myoelectric hand prosthesis while receiving grip force sensory feedback encoded using either linear modulation of amplitude (LAM) or linear modulation of frequency (LFM) of direct nerve stimulation (namely, bidirectional prostheses). Both subjects achieved similar and significantly above-chance performance when they were asked to exploit LAM or LFM in different tasks. The feedbacks allowed them to discriminate, during manipulation through the robotic hand, objects of different compliances and shapes or different placements on the prosthesis. Similar high performances were obtained when they were asked to apply different levels of force in a random order on a dynamometer using LAM or LFM. In contrast, only the LAM strategy allowed the subjects to continuously modulate the grip pressure on the dynamometer. Furthermore, when long-lasting trains of stimulation were delivered, LFM strategy generated a very fast adaptation phenomenon in the subjects, which caused them to stop perceiving the restored sensations. Both encoding approaches were perceived as very different from the touch feelings of the healthy limb (natural). These results suggest that the choice of specific sensory feedback encodings can have an effect on user performance while grasping. In addition, our results invite the development of new approaches to provide more natural sensory feelings to the users, which could be addressed by a more biomimetic strategy in the future.

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          Coding and use of tactile signals from the fingertips in object manipulation tasks.

          During object manipulation tasks, the brain selects and implements action-phase controllers that use sensory predictions and afferent signals to tailor motor output to the physical properties of the objects involved. Analysis of signals in tactile afferent neurons and central processes in humans reveals how contact events are encoded and used to monitor and update task performance.
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            Restoring natural sensory feedback in real-time bidirectional hand prostheses.

            Hand loss is a highly disabling event that markedly affects the quality of life. To achieve a close to natural replacement for the lost hand, the user should be provided with the rich sensations that we naturally perceive when grasping or manipulating an object. Ideal bidirectional hand prostheses should involve both a reliable decoding of the user's intentions and the delivery of nearly "natural" sensory feedback through remnant afferent pathways, simultaneously and in real time. However, current hand prostheses fail to achieve these requirements, particularly because they lack any sensory feedback. We show that by stimulating the median and ulnar nerve fascicles using transversal multichannel intrafascicular electrodes, according to the information provided by the artificial sensors from a hand prosthesis, physiologically appropriate (near-natural) sensory information can be provided to an amputee during the real-time decoding of different grasping tasks to control a dexterous hand prosthesis. This feedback enabled the participant to effectively modulate the grasping force of the prosthesis with no visual or auditory feedback. Three different force levels were distinguished and consistently used by the subject. The results also demonstrate that a high complexity of perception can be obtained, allowing the subject to identify the stiffness and shape of three different objects by exploiting different characteristics of the elicited sensations. This approach could improve the efficacy and "life-like" quality of hand prostheses, resulting in a keystone strategy for the near-natural replacement of missing hands.
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              A neural interface provides long-term stable natural touch perception.

              Touch perception on the fingers and hand is essential for fine motor control, contributes to our sense of self, allows for effective communication, and aids in our fundamental perception of the world. Despite increasingly sophisticated mechatronics, prosthetic devices still do not directly convey sensation back to their wearers. We show that implanted peripheral nerve interfaces in two human subjects with upper limb amputation provided stable, natural touch sensation in their hands for more than 1 year. Electrical stimulation using implanted peripheral nerve cuff electrodes that did not penetrate the nerve produced touch perceptions at many locations on the phantom hand with repeatable, stable responses in the two subjects for 16 and 24 months. Patterned stimulation intensity produced a sensation that the subjects described as natural and without "tingling," or paresthesia. Different patterns produced different types of sensory perception at the same location on the phantom hand. The two subjects reported tactile perceptions they described as natural tapping, constant pressure, light moving touch, and vibration. Changing average stimulation intensity controlled the size of the percept area; changing stimulation frequency controlled sensation strength. Artificial touch sensation improved the subjects' ability to control grasping strength of the prosthesis and enabled them to better manipulate delicate objects. Thus, electrical stimulation through peripheral nerve electrodes produced long-term sensory restoration after limb loss.
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                Author and article information

                Contributors
                silvestro.micera@epfl.ch
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                12 November 2018
                12 November 2018
                2018
                : 8
                : 16666
                Affiliations
                [1 ]ISNI 0000000121839049, GRID grid.5333.6, Bertarelli Foundation Chair in Translational Neuroengineering, Centre for Neuroprosthetics and Institute of Bioengineering, School of Engineering, , École Polytechnique Fédérale de Lausanne (EPFL), ; Lausanne, Switzerland
                [2 ]ISNI 0000 0004 1762 600X, GRID grid.263145.7, Center for Neuroscience, Neurotechnology, and Bioelectronic Medicine and BioRobotics Institute, , Scuola Superiore Sant’Anna, ; Pisa, Italy
                [3 ]Institute of Neurology, Catholic University of The Sacred Heart, Policlinic A. Gemelli Foundation, Roma, Italy
                [4 ]GRID grid.5963.9, Laboratory for Biomedical Microtechnology, Department of Microsystems Engineering–IMTEK, Bernstein Center, BrainLinks-BrainTools Cluster of Excellence, , University of Freiburg, ; Freiburg, D-79110 Germany
                [5 ]ISNI 0000 0001 2156 2780, GRID grid.5801.c, Department of Health Sciences and Technology, , Institute for Robotics and Intelligent Systems, ; ETH Zürich, 8092 Zürich Switzerland
                Author information
                http://orcid.org/0000-0002-2637-8007
                http://orcid.org/0000-0003-0971-8783
                http://orcid.org/0000-0002-4365-5328
                http://orcid.org/0000-0003-1299-4957
                http://orcid.org/0000-0002-7349-4254
                http://orcid.org/0000-0002-9632-1831
                Article
                34910
                10.1038/s41598-018-34910-w
                6232130
                30420739
                9f8e2b91-5650-455e-b68e-50a6d437267a
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 18 April 2018
                : 28 October 2018
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