Intracortical Microstimulation Elicits Human Fingertip Sensations

The restoration of cutaneous sensation to fingers and fingertips is critical to achieving dexterous prosthesis control for individuals with sensorimotor dysfunction. However, localized and reproducible fingertip sensations in humans have not been reported via intracortical microstimulation (ICMS) in humans. Here, we show that ICMS in a human participant was capable of eliciting percepts in 7 fingers spanning both hands, including 6 fingertip regions (i.e., 3 on each hand). Median percept size was estimated to include 1.40 finger or palmar segments (e.g., one segment being a fingertip or the section of upper palm below a finger). This was corroborated with a more sensitive manual marking technique where median percept size corresponded to roughly 120% of a fingertip segment. Percepts showed high intra-day consistency, including high performance (99%) on a blinded finger discrimination task. Across days, there was more variability in percepts, with 75.8% of trials containing the modal finger or palm region for the stimulated electrode. These results suggest that ICMS can enable the delivery of localized fingertip sensations during object manipulation by neuroprostheses.

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

[2]  J. Kaas,et al.  Multiple representations of the body within the primary somatosensory cortex of primates. , 1979, Science.

[3]  R. Johansson,et al.  Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. , 1979, The Journal of physiology.

[4]  J C Rothwell,et al.  Manual motor performance in a deafferented man. , 1982, Brain : a journal of neurology.

[5]  J. Gordon,et al.  Impairments of reaching movements in patients without proprioception. II. Effects of visual information on accuracy. , 1995, Journal of neurophysiology.

[6]  J. Gordon,et al.  Impairments of reaching movements in patients without proprioception. I. Spatial errors. , 1995, Journal of neurophysiology.

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

[8]  David C. Alsop,et al.  The Sensory Somatotopic Map of the Human Hand Demonstrated at 4 Tesla , 1999, NeuroImage.

[9]  A. Schleicher,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 1. Microstructural Organization and Interindividual Variability , 1999, NeuroImage.

[10]  M. Leek.  Adaptive procedures in psychophysical research , 2001, Perception & psychophysics.

[11]  R. Johansson,et al.  Somatosensory control of precision grip during unpredictable pulling loads , 2004, Experimental Brain Research.

[12]  Marianne I. Christel,et al.  How Precisely Do Bonobos (Pan paniscus) Grasp Small Objects? , 1998, International Journal of Primatology.

[13]  Frode Ødegaard,et al.  A multiple-site similarity measure , 2007, Biology Letters.

[14]  L. Miller,et al.  Electrical Stimulation of the Proprioceptive Cortex (Area 3a) Used to Instruct a Behaving Monkey , 2008, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

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

[16]  Miguel A. L. Nicolelis,et al.  A Brain-Machine Interface Instructed by Direct Intracortical Microstimulation , 2009, Front. Integr. Neurosci..

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

[18]  Matthew P. Para,et al.  Control System Architecture for the Modular Prosthetic Limb , 2011 .

[19]  Stuart D. Harshbarger,et al.  An Overview of the Developmental Process for the Modular Prosthetic Limb , 2011 .

[20]  S. Francis,et al.  Within-Digit Functional Parcellation of Brodmann Areas of the Human Primary Somatosensory Cortex Using Functional Magnetic Resonance Imaging at 7 Tesla , 2012, The Journal of Neuroscience.

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

[22]  Josef Parvizi,et al.  Hand posture classification using electrocorticography signals in the gamma band over human sensorimotor brain areas , 2013, Journal of neural engineering.

[23]  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.

[24]  Kevin H. Chen,et al.  The effect of chronic intracortical microstimulation on the electrode–tissue interface , 2014, Journal of neural engineering.

[25]  Spencer Kellis,et al.  A cognitive neuroprosthetic that uses cortical stimulation for somatosensory feedback , 2014, Journal of neural engineering.

[26]  Meike A. Schweisfurth,et al.  Individual fMRI maps of all phalanges and digit bases of all fingers in human primary somatosensory cortex , 2014, Front. Hum. Neurosci..

[27]  Bradley Greger,et al.  Acute human brain responses to intracortical microelectrode arrays: challenges and future prospects , 2014, Front. Neuroeng..

[28]  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.

[29]  Joseph E O'Doherty,et al.  A learning–based approach to artificial sensory feedback leads to optimal integration , 2014, Nature Neuroscience.

[30]  S. Bensmaia,et al.  Behavioral assessment of sensitivity to intracortical microstimulation of primate somatosensory cortex , 2015, Proceedings of the National Academy of Sciences.

[31]  Johan Wessberg,et al.  Mapping quantal touch using 7 Tesla functional magnetic resonance imaging and single-unit intraneural microstimulation , 2016, eLife.

[32]  Stephen T. Foldes,et al.  Intracortical microstimulation of human somatosensory cortex , 2016, Science Translational Medicine.

[33]  Heidi Johansen-Berg,et al.  Investigating the Stability of Fine-Grain Digit Somatotopy in Individual Human Participants , 2016, The Journal of Neuroscience.

[34]  N. Ramsey,et al.  Fully Implanted Brain-Computer Interface in a Locked-In Patient with ALS. , 2016, The New England journal of medicine.

[35]  T. Lucas,et al.  The effects of acute cortical somatosensory deafferentation on grip force control , 2016, Cortex.

[36]  Adeen Flinker,et al.  Spatial-temporal functional mapping of language at the bedside with electrocorticography , 2016, Neurology.

[37]  Kapil D. Katyal,et al.  Individual finger control of a modular prosthetic limb using high-density electrocorticography in a human subject , 2016, Journal of neural engineering.

[38]  Benoit P. Delhaye,et al.  The neural basis of perceived intensity in natural and artificial touch , 2016, Science Translational Medicine.

[39]  Z T Irwin,et al.  Neural control of finger movement via intracortical brain–machine interface , 2017, Journal of neural engineering.

[40]  Silvestro Micera,et al.  A somatotopic bidirectional hand prosthesis with transcutaneous electrical nerve stimulation based sensory feedback , 2017, Scientific Reports.

[41]  Wei Wang,et al.  Human perception of electrical stimulation on the surface of somatosensory cortex , 2017, PloS one.

[42]  Nick F. Ramsey,et al.  Detailed somatotopy in primary motor and somatosensory cortex revealed by Gaussian population receptive fields , 2018, NeuroImage.

[43]  Nitish V. Thakor,et al.  Prosthesis with neuromorphic multilayered e-dermis perceives touch and pain , 2018, Science Robotics.

[44]  Franck-Emmanuel Roux,et al.  Functional architecture of the somatosensory homunculus detected by electrostimulation , 2017, The Journal of physiology.

[45]  Daniel R Kramer,et al.  Engineering Artificial Somatosensation Through Cortical Stimulation in Humans , 2018, Front. Syst. Neurosci..

[46]  Daniel R Kramer,et al.  Proprioceptive and cutaneous sensations in humans elicited by intracortical microstimulation , 2018, eLife.

[47]  Benoit P. Delhaye,et al.  Neural Basis of Touch and Proprioception in Primate Cortex. , 2018, Comprehensive Physiology.

[48]  S. Bensmaia,et al.  The frequency of cortical microstimulation shapes artificial touch , 2019, Proceedings of the National Academy of Sciences.

[49]  Daniel R Kramer,et al.  Technical considerations for generating somatosensation via cortical stimulation in a closed-loop sensory/motor brain-computer interface system in humans , 2019, Journal of Clinical Neuroscience.

[50]  Nathan E. Crone,et al.  BCI2000Web and WebFM: Browser-Based Tools for Brain Computer Interfaces and Functional Brain Mapping , 2019, Front. Neurosci..

[51]  Elizaveta V Okorokova,et al.  Biomimetic sensory feedback through peripheral nerve stimulation improves dexterous use of a bionic hand , 2019, Science Robotics.

[52]  Solaiman Shokur,et al.  Creating a neuroprosthesis for active tactile exploration of textures , 2019, Proceedings of the National Academy of Sciences.

[53]  Aneesha K. Suresh,et al.  Neural Coding of Contact Events in Somatosensory Cortex. , 2019, Cerebral cortex.

[54]  Michael L. Boninger,et al.  Restored tactile sensation improves neuroprosthetic arm control , 2019, bioRxiv.

[55]  Spencer Kellis,et al.  Mapping of primary somatosensory cortex of the hand area using a high-density electrocorticography grid for closed-loop brain computer interface. , 2020, Journal of neural engineering.

[56]  Robert A. Gaunt,et al.  Neural stimulation and recording performance in human somatosensory cortex over 1500 days , 2020 .

[57]  Hannes P. Saal,et al.  Tactile innervation densities across the whole body , 2020, bioRxiv.

[58]  David A. Friedenberg,et al.  Restoring the Sense of Touch Using a Sensorimotor Demultiplexing Neural Interface , 2020, Cell.