Biological and bionic hands: Natural neural coding and artificial perception

Abstract

One contribution of 15 to a theme issue 'Controlling brain activity to alter perception, behaviour and society'. The first decade and a half of the twenty-first century brought about two major innovations in neuroprosthetics: the development of anthropomorphic robotic limbs that replicate much of the function of a native human arm and the refinement of algorithms that decode intended movements from brain activity. However, skilled manipulation of objects requires somatosensory feedback, for which vision is a poor substitute. For upper-limb neuroprostheses to be clinically viable, they must therefore provide for the restoration of touch and proprioception. In this review, I discuss efforts to elicit meaningful tactile sensations through stimulation of neurons in somatosensory cortex. I focus on biomimetic approaches to sensory restoration, which leverage our current understanding about how information about grasped objects is encoded in the brain of intact individuals. I argue that not only can sensory neuroscience inform the development of sensory neuroprostheses, but also that the converse is true: stimulating the brain offers an exceptional opportunity to causally interrogate neural circuits and test hypotheses about natural neural coding.

Imaging fast neural traffic at fascicular level with electrical impedance tomography: proof of principle in rat sciatic nerve

“…Mathematical models may be constructed of the information processing of spikes and refined and verified using electrophysiological measures of spiking activity using multielectrode arrays [1]. Information is transmitted to the central nervous system through peripheral nerves and any complete description thus requires understanding of spike coding in nerve as well as brain [2]. However, this field is not well developed, which may be attributed to limitations in technology for recording such neural activity within nerves.…”

Key considerations in designing a somatosensory neuroprosthesis

“…One way to mitigate the problem of scalability when it comes to the learnability of the space is to exploit, to the extent possible, existing perceptual representations (Bensmaia, 2015;Saal and Bensmaia, 2015). Indeed, to the extent that we can reproduce the patterns of neuronal activation that would be produced with an intact limb and nervous system, the resulting percepts will be natural and the patient will not have to learn anything.…”

“…For example, a subpopulation of neurons in S1 is strongly selective for the direction in which objects move across the skin (Pei et al, 2011). If stimulation of these neurons evokes percepts of tactile motion, perhaps this phenomenon can be exploited to convey information about objects moving across the prosthetic hand (Bensmaia, 2015;Bensmaia and Miller, 2014).…”

“…However, dexterous use of robotic hands will also necessitate sensory restoration. In light of this, efforts have been underway to develop approaches to convey somatosensory feedback (Bensmaia, 2015;Bensmaia and Miller, 2014;Flesher et al, 2016;Graczyk et al, 2016;Saal and Bensmaia, 2015). One family of approaches -sensory substitution -consists of applying mechanical stimuli, typically skin vibrations, to an intact and sensate patch of skin somewhere on the body and modulate the activation of these tactors according to the movements of the prosthesis and/or its contact with objects (Antfolk et al, 2013).…”

Spatiotemporal Maps of Proprioceptive Inputs to the Cervical Spinal Cord During Three-Dimensional Reaching and Grasping

“…However, restoration of voluntary control of arm and hand movements likely requires even finer integration between stimulation signals, descending drive and natural sensory feedback [22]. Unfortunately, electrical stimulation patterns interfere with natural afferent activity [23] leading to impairment of movement execution and conscious perception of proprioception [24]. Therefore, application of EES protocols to the complex control of the upper limb should rely on precise knowledge of cervical sensorimotor circuit dynamics.…”