SENSORS Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works Prosthesis with neuromorphic multilayered e-dermis perceives touch and pain Luke E. Osborn 1 *, Andrei Dragomir 2 , Joseph L. Betthauser 3 , Christopher L. Hunt 1 , Harrison H. Nguyen 1 , Rahul R. Kaliki 1,4 , Nitish V. Thakor 1,2,3,5 * The human body is a template for many state-of-the-art prosthetic devices and sensors. Perceptions of touch and pain are fundamental components of our daily lives that convey valuable information about our environment while also providing an element of protection from damage to our bodies. Advances in prosthesis designs and control mechanisms can aid an amputee’s ability to regain lost function but often lack meaningful tactile feedback or per- ception. Through transcutaneous electrical nerve stimulation (TENS) with an amputee, we discovered and quantified stimulation parameters to elicit innocuous (nonpainful) and noxious (painful) tactile perceptions in the phantom hand. Electroencephalography (EEG) activity in somatosensory regions confirms phantom hand activation during stimulation. We invented a multilayered electronic dermis (e-dermis) with properties based on the behavior of mechanoreceptors and nociceptors to provide neuromorphic tactile information to an amputee. Our biologically inspired e-dermis enables a prosthesis and its user to perceive a continuous spectrum from innocuous to noxious touch through a neuromorphic interface that produces receptor-like spiking neural activity. In a pain detection task (PDT), we show the ability of the prosthesis and amputee to differentiate nonpainful or painful tactile stimuli using sensory feedback and a pain reflex feedback control system. In this work, an amputee can use perceptions of touch and pain to discriminate object curvature, including sharpness. This work demonstrates possibilities for creating a more natural sensation spanning a range of tactile stimuli for prosthetic hands. INTRODUCTION One of the primary functions of the somatosensory system is to provide exteroceptive sensations to help us perceive and react to stimuli from outside of our body (1). Our sense of touch is a crucial aspect of the somatosensory system and provides valuable information that enables us to interact with our surrounding environment. Tactile feedback, in conjunction with proprioception, allows us to perform many of our dai- ly tasks that rely on the dexterous manipulation of our hands (2). Me- chanoreceptors and free nerve endings in our skin give us the means to perceive tactile sensation (2). The primary mechanoreceptors in the gla- brous skin that convey tactile information are Meissner corpuscles, Merkel cells, Ruffini endings, and Pacinian corpuscles. The Merkel cells and Ruffini endings are classified as slowly adapting (SA) and respond to sustained tactile loads. Meissner and Pacinian corpuscles are rapidly adapting (RA) and respond to the onset and offset of tactile stimulation (1, 3). More recently, research has shown the role of fingertips in coding tactile information (4) and extracting tactile features (5). A vital component of our tactile perception is the sense of pain. Al- though often undesired, pain provides a protection mechanism when we experience a potentially damaging stimulus. In the event of an injury, increased sensitivity can render even innocuous stimuli as painful (6). Nociceptors are dedicated sensory afferents in both glabrous and non- glabrous skin responsible for conducting tactile stimuli that we perceive as painful (6). Nociceptors, free nerve endings in the epidermal layer of the skin, act as high threshold mechanoreceptors (HTMRs) and re- spond to noxious stimuli through Ab,Ad, and C nerve fibers (1), which enable our perception of tactile pain. It was discovered that Ad fiber HTMRs respond to both innocuous and noxious mechanical stimuli with an increase in impulse frequency while experiencing the noxious stimuli (7). It is also known that mechanoreceptor activation along with nociceptor activation helps inhibit our perception of pain, and our dis- comfort increases when only nociceptors are active (8), which helps to explain our ability to perceive a range of innocuous and noxious sensations. Although novel approaches have improved prosthesis mo- tor control (9), comprehensive sensory perceptions are not available in today’s prosthetic hands. The undoubted importance of our sense of touch, and lack of sen- sory capabilities in today’s prostheses, has spurred research on artificial tactile sensors and restoring sensory feedback to those with upper limb loss. Novel sensor developments use flexible electronics (10–12), self- healing (13, 14) and recyclable materials (15), mechanoreceptor- inspired elements (16, 17), and even optoelectronic strain sensors (18), which will likely affect the future of prosthetic limbs. Local force feedback to a prosthesis is known to improve grasping (19), but in re- cent years, there has been a major push toward providing sensory feedback to the prosthesis and the amputee. Groundbreaking results show that implanted peripheral nerve electrodes (20–23) and non- invasive electrical nerve stimulation methods (24) can successfully elicit sensations of touch in the phantom hand of amputees. Recent approaches aim to mimic the biological behavior of tactile receptors using advanced skin dynamics (25) and what are known as neuromorphic (26) models of tactile receptors for sensory feedback. A neuromorphic system aims to implement components of a neural sys- tem, for example, the representation of touch through spiking activity based on biologically driven models. One reason for using a neuro- morphic approach is to create a biologically relevant representation of tactile information using actual mechanoreceptor characteristics. Neuromorphic techniques have been used to convey tactile sensations for differentiating textures using SA-like dynamics for the stimulation 1 Department of Biomedical Engineering, Johns Hopkins School of Medicine, 720 Rutland Avenue, Baltimore, MD 21205, USA. 2 Singapore Institute for Neurotechnol- ogy, National University of Singapore, 28 Medical Drive, #05-02, Singapore 117456, Singapore. 3 Department of Electrical and Computer Engineering, Johns Hopkins Uni- versity, 3400 North Charles Street, Baltimore, MD 21218, USA. 4 Infinite Biomedical Technologies, Johns Hopkins University Eastern Campus, 1101 East 33rd Street, Suite E305, Baltimore, MD 21218, USA. 5 Department of Neurology, Johns Hopkins Univer- sity, 600 North Wolfe, Baltimore, MD 21205, USA. *Corresponding author. Email: losborn@jhu.edu (L.E.O.); nitish@jhu.edu or eletnv@nus.edu.sg (N.V.T.) SCIENCE ROBOTICS | RESEARCH ARTICLE Osborn et al., Sci. 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