Restoring tactile and proprioceptive sensation through a brain interface

Abstract

Somatosensation plays a critical role in the dexterous manipulation of objects, in emotional communication, and in the embodiment of our limbs. For upper-limb neuroprostheses to be adopted by prospective users, prosthetic limbs will thus need to provide sensory information about the position of the limb in space and about objects grasped in the hand. One approach to restoring touch and proprioception consists of electrically stimulating neurons in somatosensory cortex in the hopes of eliciting meaningful sensations to support the dexterous use of the hands, promote their embodiment, and perhaps even restore the affective dimension of touch. In this review, we discuss the importance of touch and proprioception in everyday life, then describe approaches to providing artificial somatosensory feedback through intracortical microstimulation (ICMS). We explore the importance of biomimicry – the elicitation of naturalistic patterns of neuronal activation – and that of adaptation – the brain's ability to adapt to novel sensory input, and argue that both biomimicry and adaptation will play a critical role in the artificial restoration of somatosensation. We also propose that the documented re-organization that occurs after injury does not pose a significant obstacle to brain interfaces. While still at an early stage of development, sensory restoration is a critical step in transitioning upper-limb neuroprostheses from the laboratory to the clinic.

Introduction

One approach to restoring sensorimotor function to amputees or tetraplegic patients is to equip them with robotic prosthetic arms and have them control these limbs using signals from the motor parts of their brain. To date, a number of patients have been able to control anthropomorphic robotic arms to perform simple motor tasks, such as grasping and moving objects (Collinger et al., 2013, Hochberg et al., 2012). As impressive as these feats are from a scientific and technological standpoint, however, movements generated using these prosthetic limbs are slow and relatively inaccurate; their performance still does not warrant the highly invasive surgery that they would require if they were adopted in the clinic. One important reason for the poor performance is the lack of somatosensory feedback. Indeed, our ability to grasp and manipulate objects is critically dependent on the senses of touch and proprioception. Tactile and proprioceptive signals from the hand convey information about the size, shape, and texture of objects, and indicate when objects are slipping from our grasp (Johansson and Flanagan, 2009). Proprioceptive signals also convey information about the state of our limb and are important to plan and guide movements (Sainburg et al., 1993, Sainburg et al., 1995). Vision is a poor substitute for touch and proprioception as evidenced by the fact that patients with intact motor but impaired somatosensory function struggle to perform activities of daily living, like tying a shoelace or turning a doorknob (Marsden et al., 1984). Touch also plays a critical role in emotional and social communication – we touch the people we care about – and in embodiment – the sense that our body is part of us. Given the importance of somatosensation in intact individuals, a key to improving the performance of prosthetic arms is to incorporate this critical sensory feedback. One approach to restoring somatosensation is to electrically stimulate the somatosensory parts of the brain, specifically primary somatosensory cortex (Fig. 1), in the hopes of eliciting meaningful and informative tactile percepts that can then be used not only to improve the dexterity of these limbs, but also to restore the affective component of touch and promote the embodiment of the prosthesis.