A cognitive neuroprosthetic that uses cortical stimulation for somatosensory feedback

OBJECTIVE Present day cortical brain-machine interfaces (BMIs) have made impressive advances using decoded brain signals to control extracorporeal devices. Although BMIs are used in a closed-loop fashion, sensory feedback typically is visual only. However medical case studies have shown that the loss of somesthesis in a limb greatly reduces the agility of the limb even when visual feedback is available. APPROACH To overcome this limitation, this study tested a closed-loop BMI that utilizes intracortical microstimulation to provide 'tactile' sensation to a non-human primate. MAIN RESULT Using stimulation electrodes in Brodmann area 1 of somatosensory cortex (BA1) and recording electrodes in the anterior intraparietal area, the parietal reach region and dorsal area 5 (area 5d), it was found that this form of feedback can be used in BMI tasks. SIGNIFICANCE Providing somatosensory feedback has the poyential to greatly improve the performance of cognitive neuroprostheses especially for fine control and object manipulation. Adding stimulation to a BMI system could therefore improve the quality of life for severely paralyzed patients.

[1]  S. Hathaway,et al.  MMPI-2 : Minnesota Multiphasic Personality Inventory-2 : manual for administration and scoring , 1989 .

[2]  R. Andersen,et al.  Cognitive Control Signals for Neural Prosthetics , 2004, Science.

[3]  K. Horch,et al.  Object Discrimination With an Artificial Hand Using Electrical Stimulation of Peripheral Tactile and Proprioceptive Pathways With Intrafascicular Electrodes , 2011, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[4]  Michael J. Black,et al.  Multi-state decoding of point-and-click control signals from motor cortical activity in a human with tetraplegia , 2007, 2007 3rd International IEEE/EMBS Conference on Neural Engineering.

[5]  T S Davis,et al.  Multiple factors may influence the performance of a visual prosthesis based on intracortical microstimulation: nonhuman primate behavioural experimentation , 2011, Journal of neural engineering.

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

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

[8]  J G Ojemann,et al.  Cortical stimulation mapping of phantom limb rolandic cortex. Case report. , 1995, Journal of neurosurgery.

[9]  Shamim Nemati,et al.  Biomimetic Brain Machine Interfaces for the Control of Movement , 2007, The Journal of Neuroscience.

[10]  D. Durand,et al.  Functionally selective peripheral nerve stimulation with a flat interface nerve electrode , 2002, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[11]  Victor Pikov,et al.  Neuronal loss due to prolonged controlled-current stimulation with chronically implanted microelectrodes in the cat cerebral cortex , 2010, Journal of neural engineering.

[12]  R. Romo,et al.  Sensing without Touching Psychophysical Performance Based on Cortical Microstimulation , 2000, Neuron.

[13]  Hannes Bleuler,et al.  Active tactile exploration enabled by a brain-machine-brain interface , 2011, Nature.

[14]  J. Donoghue,et al.  Primary Motor Cortex Tuning to Intended Movement Kinematics in Humans with Tetraplegia , 2008, The Journal of Neuroscience.

[15]  R A Normann,et al.  Chronic intracortical microstimulation (ICMS) of cat sensory cortex using the Utah Intracortical Electrode Array. , 1999, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[16]  Andrew S. Whitford,et al.  Cortical control of a prosthetic arm for self-feeding , 2008, Nature.

[17]  N A Fitzsimmons,et al.  Primate Reaching Cued by Multichannel Spatiotemporal Cortical Microstimulation , 2007, The Journal of Neuroscience.

[18]  Wolfgang Rosenstiel,et al.  Coupling BCI and cortical stimulation for brain-state-dependent stimulation: methods for spectral estimation in the presence of stimulation after-effects , 2012, Front. Neural Circuits.

[19]  Wei Wu,et al.  Neural Decoding of Cursor Motion Using a Kalman Filter , 2002, NIPS.

[20]  S. Cogan.  Neural stimulation and recording electrodes. , 2008, Annual review of biomedical engineering.

[21]  Byron M. Yu,et al.  A high-performance brain–computer interface , 2006, Nature.

[22]  M. Mehrali,et al.  A review on powder-based additive manufacturing for tissue engineering: selective laser sintering and inkjet 3D printing , 2015, Science and technology of advanced materials.

[23]  D. McCreery,et al.  Histopathologic evaluation of prolonged intracortical electrical stimulation , 1986, Experimental Neurology.

[24]  F. Grover,et al.  Amplitudes of background fast activity characteristic of specific brain sites. , 1970, Journal of neurophysiology.

[25]  Mikhail A Lebedev,et al.  Future developments in brain-machine interface research , 2011, Clinics.

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

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

[28]  Keehoon Kim,et al.  Robotic touch shifts perception of embodiment to a prosthesis in targeted reinnervation amputees. , 2011, Brain : a journal of neurology.

[29]  D. L. Adams,et al.  A biocompatible titanium headpost for stabilizing behaving monkeys. , 2007, Journal of neurophysiology.

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

[31]  Hugh M Herr,et al.  Horizons in Prosthesis Development for the Restoration of Limb Function , 2006, The Journal of the American Academy of Orthopaedic Surgeons.

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

[33]  Michael J. Black,et al.  Neural control of computer cursor velocity by decoding motor cortical spiking activity in humans with tetraplegia , 2008, Journal of neural engineering.

[34]  Vikash Gilja,et al.  A closed-loop human simulator for investigating the role of feedback control in brain-machine interfaces. , 2011, Journal of neurophysiology.

[35]  Eran Stark,et al.  Predicting Movement from Multiunit Activity , 2007, The Journal of Neuroscience.

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

[37]  J. Burdick,et al.  Integrated parylene-cabled silicon probes for neural prosthetics , 2008, 2008 IEEE 21st International Conference on Micro Electro Mechanical Systems.

[38]  W. Penfield,et al.  The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1968 .

[39]  Eun Jung Hwang,et al.  Brain Control of Movement Execution Onset Using Local Field Potentials in Posterior Parietal Cortex , 2009, The Journal of Neuroscience.

[40]  Jerald D. Kralik,et al.  Real-time prediction of hand trajectory by ensembles of cortical neurons in primates , 2000, Nature.

[41]  R.N.Dej.,et al.  Epilepsy and the Functional Anatomy of the Human Brain , 1954, Neurology.

[42]  Bradley Greger,et al.  The functional consequences of chronic, physiologically effective intracortical microstimulation. , 2011, Progress in brain research.

[43]  Michael J. Black,et al.  Point-and-Click Cursor Control With an Intracortical Neural Interface System by Humans With Tetraplegia , 2011, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[44]  Nicolas Y. Masse,et al.  Reach and grasp by people with tetraplegia using a neurally controlled robotic arm , 2012, Nature.

[45]  David M. Santucci,et al.  Learning to Control a Brain–Machine Interface for Reaching and Grasping by Primates , 2003, PLoS biology.

[46]  Blair A. Lock,et al.  Redirection of cutaneous sensation from the hand to the chest skin of human amputees with targeted reinnervation , 2007, Proceedings of the National Academy of Sciences.

[47]  Wei Wu,et al.  Bayesian Population Decoding of Motor Cortical Activity Using a Kalman Filter , 2006, Neural Computation.

[48]  D.B. McCreery,et al.  Charge density and charge per phase as cofactors in neural injury induced by electrical stimulation , 1990, IEEE Transactions on Biomedical Engineering.

[49]  I. Kaufman.  The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1951 .

[50]  R R Riso,et al.  Strategies for providing upper extremity amputees with tactile and hand position feedback--moving closer to the bionic arm. , 1999, Technology and health care : official journal of the European Society for Engineering and Medicine.

[51]  M. Mozetič,et al.  Titanium nanostructures for biomedical applications , 2015, Nanotechnology.

[52]  Guy Bouvier,et al.  Stimulation of human somatosensory cortex: tactile and body displacement perceptions in medial regions , 2004, Experimental Brain Research.

[53]  Dawn M. Taylor,et al.  Direct Cortical Control of 3D Neuroprosthetic Devices , 2002, Science.

[54]  Nicholas G. Hatsopoulos,et al.  Brain-machine interface: Instant neural control of a movement signal , 2002, Nature.

[55]  Jon A. Mukand,et al.  Neuronal ensemble control of prosthetic devices by a human with tetraplegia , 2006, Nature.

[56]  Michael J. Black,et al.  Neural control of cursor trajectory and click by a human with tetraplegia 1000 days after implant of an intracortical microelectrode array , 2011 .

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

[58]  H. Vaughan,et al.  Averaged multiple unit activity as an estimate of phasic changes in local neuronal activity: effects of volume-conducted potentials , 1980, Journal of Neuroscience Methods.

[59]  S. Meagher.  Instant neural control of a movement signal , 2002 .

[60]  H. Jasper,et al.  Epilepsy and the functional anatomy of the human brain , 1985 .

[61]  B. Libet.  Brain stimulation in the study of neuronal functions for conscious sensory experiences. , 1982, Human neurobiology.

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

[63]  Eun Jung Hwang,et al.  Spiking and LFP activity in PRR during symbolically instructed reaches. , 2012, Journal of neurophysiology.

[64]  Gerald E Loeb,et al.  Cognitive signals for brain–machine interfaces in posterior parietal cortex include continuous 3D trajectory commands , 2012, Proceedings of the National Academy of Sciences.

[65]  F F R E Y G. Oj,et al.  Cortical stimulation mapping of phantom limb rolandic cortex , 1995 .

[66]  John P. Cunningham,et al.  A High-Performance Neural Prosthesis Enabled by Control Algorithm Design , 2012, Nature Neuroscience.