Human cortical prostheses: lost in translation?

Direct brain control of a prosthetic system is the subject of much popular and scientific news. Neural technology and science have advanced to the point that proof-of-concept systems exist for cortically-controlled prostheses in rats, monkeys, and even humans. However, realizing the dream of making such technology available to everyone is still far off. Fortunately today there is great public and scientific interest in making this happen, but it will only occur when the functional benefits of such systems outweigh the risks. In this article, the authors briefly summarize the state of the art and then highlight many issues that will directly limit clinical translation, including system durability, system performance, and patient risk. Despite the challenges, scientists and clinicians are in the desirable position of having both public and fiscal support to begin addressing these issues directly. The ultimate challenge now is to determine definitively whether these prosthetic systems will become clinical reality or forever unrealized.

[1]  Pantaleo Romanelli,et al.  Asymptomatic Transient MRI Signal Changes after Unilateral Deep Brain Stimulation Electrode Implantation for Movement Disorder , 2004, Stereotactic and Functional Neurosurgery.

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

[3]  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.

[4]  E. Fetz,et al.  Operantly conditioned patterns on precentral unit activity and correlated responses in adjacent cells and contralateral muscles. , 1973, Journal of neurophysiology.

[5]  R.R. Harrison,et al.  HermesC: Low-Power Wireless Neural Recording System for Freely Moving Primates , 2009, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

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

[7]  Scott L. Simon,et al.  Complications of Invasive Monitoring Used in Intractable Pediatric Epilepsy , 2002, Pediatric Neurosurgery.

[8]  Gerwin Schalk,et al.  A brain–computer interface using electrocorticographic signals in humans , 2004, Journal of neural engineering.

[9]  Miguel A. L. Nicolelis,et al.  Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex , 1999, Nature Neuroscience.

[10]  D. Humphrey,et al.  Long-term gliosis around chronically implanted platinum electrodes in the Rhesus macaque motor cortex , 2006, Neuroscience Letters.

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

[12]  Joseph J Pancrazio,et al.  Neuroprosthetic devices: how far are we from recovering movement in paralyzed patients? , 2009, Expert review of neurotherapeutics.

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

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

[15]  P R Kennedy,et al.  Direct control of a computer from the human central nervous system. , 2000, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[16]  Stephen I. Ryu,et al.  HermesC: RF wireless low-power neural recording system for freely behaving primates , 2008, 2008 IEEE International Symposium on Circuits and Systems.

[17]  J.P. Donoghue,et al.  Reliability of signals from a chronically implanted, silicon-based electrode array in non-human primate primary motor cortex , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[18]  E. Fetz.  Operant Conditioning of Cortical Unit Activity , 1969, Science.

[19]  W. A. Sarnacki,et al.  Brain–computer interface (BCI) operation: optimizing information transfer rates , 2003, Biological Psychology.

[20]  H. Flor,et al.  A spelling device for the paralysed , 1999, Nature.

[21]  Malcolm Pell,et al.  Postmortem analysis of bilateral subthalamic electrode implants in Parkinson's disease. , 2002, Movement disorders : official journal of the Movement Disorder Society.

[22]  E. Fetz,et al.  Operant Conditioning of Specific Patterns of Neural and Muscular Activity , 1971, Science.

[23]  J. Donoghue,et al.  Neuronal Interactions Improve Cortical Population Coding of Movement Direction , 1999, The Journal of Neuroscience.

[24]  Jaimie M. Henderson,et al.  Venous Air Embolism during Deep Brain Stimulation Surgery in an Awake Supine Patient , 2005, Stereotactic and Functional Neurosurgery.

[25]  Vikash Gilja,et al.  Toward optimal target placement for neural prosthetic devices. , 2008, Journal of neurophysiology.

[26]  Allen Waziri,et al.  INITIAL SURGICAL EXPERIENCE WITH A DENSE CORTICAL MICROARRAY IN EPILEPTIC PATIENTS UNDERGOING CRANIOTOMY FOR SUBDURAL ELECTRODE IMPLANTATION , 2009, Neurosurgery.

[27]  T. Aziz,et al.  Electron microscopy of tissue adherent to explanted electrodes in dystonia and Parkinson's disease. , 2004, Brain : a journal of neurology.

[28]  A B Schwartz,et al.  Direct cortical representation of drawing. , 1994, Science.

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

[30]  Peter E. Konrad,et al.  Postmortem analysis following 71 months of deep brain stimulation of the subthalamic nucleus for Parkinson disease. , 2008, Journal of neurosurgery.

[31]  A. Arya,et al.  Long-term complications of bone-anchored hearing aids: a 14-year experience , 2008, The Journal of Laryngology & Otology.

[32]  Gabriel Curio,et al.  Brain-computer communication and slow cortical potentials , 2004, IEEE Transactions on Biomedical Engineering.

[33]  D. Kipke,et al.  Neural probe design for reduced tissue encapsulation in CNS. , 2007, Biomaterials.

[34]  Gordon H Baltuch,et al.  Deep brain stimulation for movement disorders: morbidity and mortality in 109 patients. , 2003, Journal of neurosurgery.

[35]  Karl A. Sillay,et al.  Deep brain stimulator hardware-related infections: incidence and management in a large series. , 2008, Neurosurgery.

[36]  J. A. Wilson,et al.  Two-dimensional movement control using electrocorticographic signals in humans , 2008, Journal of neural engineering.

[37]  A. Schwartz,et al.  Work toward real-time control of a cortical neural prothesis. , 2000, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[38]  P. Kennedy,et al.  Restoration of neural output from a paralyzed patient by a direct brain connection , 1998, Neuroreport.

[39]  Ayako Ochi,et al.  Complications of invasive subdural grid monitoring in children with epilepsy. , 2003, Journal of neurosurgery.

[40]  R. Andersen,et al.  Neural prosthetic control signals from plan activity , 2003, Neuroreport.

[41]  Daryl R Kipke,et al.  Advanced Neurotechnologies for Chronic Neural Interfaces: New Horizons and Clinical Opportunities , 2008, The Journal of Neuroscience.

[42]  Clement Hamani,et al.  Hardware-Related Complications of Deep Brain Stimulation: A Review of the Published Literature , 2006, Stereotactic and Functional Neurosurgery.

[43]  P. Tresco,et al.  Acute microelectrode array implantation into human neocortex: preliminary technique and histological considerations. , 2006, Neurosurgical focus.

[44]  D R Humphrey,et al.  Predicting Measures of Motor Performance from Multiple Cortical Spike Trains , 1970, Science.

[45]  P. Tresco,et al.  Response of brain tissue to chronically implanted neural electrodes , 2005, Journal of Neuroscience Methods.

[46]  Afsheen Afshar,et al.  Free-paced high-performance brain-computer interfaces. , 2007, Journal of neural engineering.

[47]  U Kramer,et al.  Use of subdural grids and strip electrodes to identify a seizure focus in children. , 1995, Pediatric neurosurgery.

[48]  Orrin Devinsky,et al.  Multistage Epilepsy Surgery: Safety, Efficacy, and Utility of a Novel Approach in Pediatric Extratemporal Epilepsy , 2005, Neurosurgery.

[49]  R. L. Rennaker,et al.  A comparison of chronic multi-channel cortical implantation techniques: manual versus mechanical insertion , 2005, Journal of Neuroscience Methods.

[50]  Jonathan R Wolpaw,et al.  Control of a two-dimensional movement signal by a noninvasive brain-computer interface in humans. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Byron M. Yu,et al.  Detecting neural-state transitions using hidden Markov models for motor cortical prostheses. , 2008, Journal of neurophysiology.

[52]  Teresa H. Y. Meng,et al.  HermesB: A Continuous Neural Recording System for Freely Behaving Primates , 2007, IEEE Transactions on Biomedical Engineering.

[53]  Nicholas Hatsopoulos,et al.  Decoding continuous and discrete motor behaviors using motor and premotor cortical ensembles. , 2004, Journal of neurophysiology.

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

[55]  Christine Haberler,et al.  No tissue damage by chronic deep brain stimulation in Parkinson's disease , 2000, Annals of neurology.

[56]  Parag G. Patil,et al.  Ensemble Recordings Of Human Subcortical Neurons as a Source Of Motor Control Signals For a Brain-Machine Interface , 2004, Neurosurgery.

[57]  Byron M. Yu,et al.  Factor-analysis methods for higher-performance neural prostheses. , 2009, Journal of neurophysiology.

[58]  R.R. Harrison,et al.  A wireless neural interface for chronic recording , 2008, 2008 IEEE Biomedical Circuits and Systems Conference.

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

[60]  John P. Cunningham,et al.  Increasing the Performance of Cortically-Controlled Prostheses , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

[61]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

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

[63]  Jeffrey G Ojemann,et al.  Complications of invasive subdural electrode monitoring at St. Louis Children's Hospital, 1994-2005. , 2006, Journal of neurosurgery.

[64]  G.F. Inbar,et al.  An improved P300-based brain-computer interface , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.