Discriminability of Single and Multichannel Intracortical Microstimulation within Somatosensory Cortex

The addition of tactile and proprioceptive feedback to neuroprosthetic limbs is expected to significantly improve the control of these devices. Intracortical microstimulation (ICMS) of somatosensory cortex is a promising method of delivering this sensory feedback. To date, the main focus of somatosensory ICMS studies has been to deliver discriminable signals, corresponding to varying intensity, to a single location in cortex. However, multiple independent and simultaneous streams of sensory information will need to be encoded by ICMS to provide functionally relevant feedback for a neuroprosthetic limb (e.g., encoding contact events and pressure on multiple digits). In this study, we evaluated the ability of an awake, behaving non-human primate (Macaca mulatta) to discriminate ICMS stimuli delivered on multiple electrodes spaced within somatosensory cortex. We delivered serial stimulation on single electrodes to evaluate the discriminability of sensations corresponding to ICMS of distinct cortical locations. Additionally, we delivered trains of multichannel stimulation, derived from a tactile sensor, synchronously across multiple electrodes. Our results indicate that discrimination of multiple ICMS stimuli is a challenging task, but that discriminable sensory percepts can be elicited by both single and multichannel ICMS on electrodes spaced within somatosensory cortex.

[1]  Henning Scheich,et al.  Auditory Cortical Activity after Intracortical Microstimulation and Its Role for Sensory Processing and Learning , 2009, The Journal of Neuroscience.

[2]  Anna W Roe,et al.  Optical imaging of cortical networks via intracortical microstimulation. , 2013, Journal of neurophysiology.

[3]  J. Randall Flanagan,et al.  Coding and use of tactile signals from the fingertips in object manipulation tasks , 2009, Nature Reviews Neuroscience.

[4]  Benjamin Libet,et al.  Electrical Stimulation of Cortex in Human Subjects, and Conscious Sensory Aspects , 1993 .

[5]  S I Helms Tillery,et al.  Computational modeling of direct neuronal recruitment during intracortical microstimulation in somatosensory cortex , 2013, Journal of neural engineering.

[6]  Peter J. Ifft,et al.  Active tactile exploration enabled by a brain-machine-brain interface , 2011, Nature.

[7]  E. J. Tehovnik,et al.  Phosphene induction and the generation of saccadic eye movements by striate cortex. , 2005, Journal of neurophysiology.

[8]  Andrew B. Schwartz,et al.  Brain-Controlled Interfaces: Movement Restoration with Neural Prosthetics , 2006, Neuron.

[9]  B LIBET,et al.  PRODUCTION OF THRESHOLD LEVELS OF CONSCIOUS SENSATION BY ELECTRICAL STIMULATION OF HUMAN SOMATOSENSORY CORTEX. , 1964, Journal of neurophysiology.

[10]  Luca Citi,et al.  Restoring Natural Sensory Feedback in Real-Time Bidirectional Hand Prostheses , 2014, Science Translational Medicine.

[11]  Eric E. Thomson,et al.  Perceiving Invisible Light through a Somatosensory Cortical Prosthesis , 2013, Nature Communications.

[12]  C. Sollerman,et al.  Sollerman hand function test. A standardised method and its use in tetraplegic patients. , 1995, Scandinavian journal of plastic and reconstructive surgery and hand surgery.

[13]  George L. Gerstein,et al.  Reorganization in the auditory cortex of the rat induced by intracortical microstimulation: a multiple single-unit study , 1996, Experimental Brain Research.

[14]  Kapil D. Katyal,et al.  Behavioral Demonstration of a Somatosensory Neuroprosthesis , 2013, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[15]  Max Ortiz-Catalan,et al.  An osseointegrated human-machine gateway for long-term sensory feedback and motor control of artificial limbs , 2014, Science Translational Medicine.

[16]  Lloyd H. Michael,et al.  The Guide for the Care and Use of Laboratory Animals. , 2016, ILAR journal.

[17]  C. K. Overstreet Intracortical Microstimulation of Somatosensory Cortex: Functional Encoding and Localization of Neuronal Recruitment , 2013 .

[18]  M. Keith,et al.  A neural interface provides long-term stable natural touch perception , 2014, Science Translational Medicine.

[19]  G. F. Shannon,et al.  A comparison of alternative means of providing sensory feedback on upper limb prostheses , 2006, Medical and biological engineering.

[20]  B. Rosén Recovery of sensory and motor function after nerve repair. A rationale for evaluation. , 1996, Journal of hand therapy : official journal of the American Society of Hand Therapists.

[21]  A. Rowan Guide for the Care and Use of Laboratory Animals , 1979 .

[22]  Marcia Kilchenman O'Malley,et al.  Tactile Feedback of Object Slip Facilitates Virtual Object Manipulation , 2015, IEEE Transactions on Haptics.

[23]  Sliman J. Bensmaia,et al.  Sensitivity to microstimulation of somatosensory cortex distributed over multiple electrodes , 2015, Front. Syst. Neurosci..

[24]  Dudley S. Childress,et al.  Closed-loop control in prosthetic systems: Historical perspective , 2006, Annals of Biomedical Engineering.

[25]  W. Penfield,et al.  Instability of response to stimulation of the sensorimotor cortex of man , 1949, The Journal of physiology.

[26]  P. Rossini,et al.  Intraneural stimulation elicits discrimination of textural features by artificial fingertip in intact and amputee humans , 2016, eLife.

[27]  R. Romo,et al.  Somatosensory discrimination based on cortical microstimulation , 1998, Nature.

[28]  D. Kipke,et al.  Cortical microstimulation in auditory cortex of rat elicits best-frequency dependent behaviors , 2005, Journal of neural engineering.

[29]  E. G. Jones,et al.  The distribution of intrinsic cortical axons in area 3b of cat primary somatosensory cortex , 2004, Experimental Brain Research.

[30]  C. Kufta,et al.  Feasibility of a visual prosthesis for the blind based on intracortical microstimulation of the visual cortex. , 1996, Brain : a journal of neurology.

[31]  G. Loeb,et al.  Visual sensations produced by intracortical microstimulation of the human occipital cortex , 1990, Medical and Biological Engineering and Computing.

[32]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[33]  Mikhail A Lebedev,et al.  Virtual Active Touch Using Randomly Patterned Intracortical Microstimulation , 2012, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[34]  R. M. McAndrew,et al.  Individualized recording chambers for non-human primate neurophysiology , 2012, Journal of Neuroscience Methods.

[35]  R. J. Vogelstein,et al.  Restoring the sense of touch with a prosthetic hand through a brain interface , 2013, Proceedings of the National Academy of Sciences.

[36]  Vernon B. Mountcastle,et al.  The sensory hand : neural mechanisms of somatic sensation , 2005 .

[37]  G.S. Dhillon,et al.  Direct neural sensory feedback and control of a prosthetic arm , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.