Biological, mechanical, and technological considerations affecting the longevity of intracortical electrode recordings

Critical Reviews in Biomedical Engineering

Volumn 41, Issue 6, 2014, Pages 435-456

  Harris, James P ^a   Tyler, Dustin J ^b  

^a Case Western Reserve University   (United States)

^b LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

Author keywords

BCI; BMI; Glial scar; Intracortical electrode; Tissue response

Indexed keywords

PROFESSIONAL ASPECTS; TISSUE;

BCI; BMI; GLIAL SCAR; INTRACORTICAL ELECTRODE; TISSUE RESPONSE;

ELECTRODES;

ANIMALS; BIOMEDICAL ENGINEERING; BRAIN-COMPUTER INTERFACES; CEREBRAL CORTEX; ELECTRODES, IMPLANTED; ELECTROENCEPHALOGRAPHY; GUINEA PIGS; HAPLORHINI; HUMANS; MICE; RATS;

EID: 84899946970     PISSN: 0278940X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (149)

1. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, Carnethon MR, Dai S, de Simone G, Ford ES, Fox CS, Fullerton HJ, Gillespie C, Greenlund KJ, Hailpern SM, Heit JA, Ho PM, Howard VJ, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Makuc DM, Marcus GM, Marelli A, Matchar DB, McDermott MM, Meigs JB, Moy CS, Mozaffarian D, Mussolino ME, Nichol G, Paynter NP, Rosamond WD, Sorlie PD, Stafford RS, Turan TN, Turner MB, Wong ND, Wylie-Rosett J; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics--2011 update: a report from the American Heart Association. Circulation. 2011;123(4):e18-209.
2. About epilepsy. Incidence and prevalence. Epilepsy and seizure statistics. Landover (MD): Epilepsy Foundation. c2012 [updated 2012 April 3; cited 2014 Jan 20]. Available from: http://www.epilepsyfoundation.org/aboutepilepsy/whatisepilepsy/statistics.cfm
3. Who gets ALS? Washington, DC: ALS Association. c2010 [updated 2011 Feb; cited 2014 Jan 20]. Available from: http://www.alsa.org/about-als/who-gets-als.html
4. Spinal cord injury facts and figures at a glance. Birmingham (AL): National Spinal Cord Injury Statistical Center. c2012 [updated 2012 Feb; cited 2014 Jan 20]. Available from: https://www.nscisc.uab.edu/PublicDocuments/fact_figures_docs/Facts%202012%20Feb%20Final.pdf
5. Alves OL, Bullock R, Clausen T, Reinert M, Reeves TM. Concurrent monitoring of cerebral electrophysiology and metabolism after traumatic brain injury: an experimental and clinical study. J Neurotrauma. 2005;22(7):733-749.
6. Buzsáki G. Large-scale recording of neuronal ensembles. Nat Neurosci. 2004;7(5):446-451.
7. Ortinski PI, Dong J, Mungenast A, Yue C, Takano H, Watson DJ, Haydon PG, Coulter DA. Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat Neurosci. 2010;13(5):584-591.
8. Churchland MM, Yu BM, Cunningham JP, Sugrue LP, Cohen MR, Corrado GS, Newsome WT, Clark AM, Hosseini P, Scott BB, Bradley DC, Smith MA, Kohn A, Movshon JA, Armstrong KM, Moore T, Chang SW, Snyder LH, Lisberger SG, Priebe NJ, Finn IM, Ferster D, Ryu SI, Santhanam G, Sahani M, Shenoy KV. Stimulus onset quenches neural variability: a widespread cortical phenomenon. Nat Neurosci. 2010;13(3):369-378.
9. Scherberger H, Jarvis MR, Andersen RA. Cortical local field potential encodes movement intentions in the posterior parietal cortex. Neuron. 2005;46(2):347-354.
10. Wolf JA, Finkel LH, Contreras D. Sublinear summation of afferent inputs to the nucleus accumbens in the awake rat. J Physiol. 2009;587(8):1695-1704.
11. Bjornsson CS, Oh SJ, Al-Kofahi YA, Lim YJ, Smith KL, Turner JN, De S, Roysam B, Shain W, Kim SJ. Effects of insertion conditions on tissue strain and vascular damage during neuroprosthetic device insertion. J Neural Eng. 2006;3(3):196-207.
12. Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci. 2006;7(1):41-53.
13. Abbott NJ. Astrocyte-endothelial interactions and bloodbrain barrier permeability. J Anat. 2002;200(6):629-38.
14. Turner JN, Shain W, Szarowski DH, Andersen M, Martins S, Isaacson M, Craighead H. Cerebral astrocyte response to micromachined silicon implants. Exp Neurol. 1999;156(1):33-49.
15. Edell DJ, Toi VV, McNeil VM, Clark LD. Factors influencing the biocompatibility of insertable silicon microshafts in cerebral cortex. IEEE Trans Biomed Eng. 1992;39(6):635-643.
16. Kozai TD, Marzullo TC, Hooi F, Langhals NB, Majewska AK, Brown EB, Kipke DR. Reduction of neurovascular damage resulting from microelectrode insertion into the cerebral cortex using in vivo two-photon mapping. J Neural Eng. 2010;7(4):046011.
17. Kozai TDY, Langhals NB, Patel PR, Deng X, Zhang H, Smith KL, Lahann J, Kotov NA, Kipke DR. Ultrasmall implantable composite microelectrodes with bioactive surfaces for chronic neural interfaces. Nat Mater. 2012;11(12):1065-1073.
18. Tsai PS, Kaufhold JP, Blinder P, Friedman B, Drew PJ, Karten HJ, Lyden PD, Kleinfeld, D. Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of nuclei and vessels. J Neurosci. 2009;29(46):14553-14570.
19. Sharp AA, Panchawagh HV, Ortega A, Artale R, Richardson-Burns S, Finch DS, Gall K, Mahajan RL, Restrepo D.Toward a self-deploying shape memory polymer neuronal electrode. J Neural Eng. 2006;3(4):L23-30.
20. Gilgunn PJ, Khilwani R, Kozai TDY, Weber DJ, Cui XT, Erdos G, Ozdoganlar OB, Fedder GK. editors. An ultracompliant, scalable neural probe with molded biodissolvable delivery vehicle. Micro Electro Mechanical Systems (MEMS), 2012 IEEE 25th International Conference on; 2012 Jan 29-Feb 2. p. 56-59.
21. Richardson-Burns SM, Hendricks JL, Martin DC. Electrochemical polymerization of conducting polymers in living neural tissue. J Neural Eng. 2007;4(2):L6-13.
22. Llinas RR, Walton KD, Nakao M, Hunter I, Anquetil PA. Neuro-vascular central nervous recording/stimulating system: using nanotechnology probes. J Nanopart Res. 2005;7(2-3):111-127.
23. Carson MJ, Cameron Thrash J, Walter B. The cellular response in neuroinflammation: the role of leukocytes, microglia and astrocytes in neuronal death and survival. Clin Neurosci Res. 2006;6(5):237-245.
24. Biran R, Martin DC, Tresco PA. Neuronal cell loss accompanies the brain tissue response to chronically implanted silicon microelectrode arrays. Exp Neurol. 2005;195(1):115-126.
25. Johnson M, Otto K, Williams J, Kipke D. Bias voltages at microelectrodes change neural interface properties in vivo. Conf Proc IEEE Eng Med Biol Soc. 2004;6:4103-4106.
26. McConnell GC. Chronic inflammation surrounding intracortical electrodes is correlated with a local neurodegenerative state [dissertation]. Atlanta: Georgia Institute of Technology; 2008.
27. Renault-Mihara F, Okada S, Shibata S, Nakamura M, Toyama Y, Okano H. Spinal cord injury: emerging beneficial role of reactive astrocytes' migration. Int J Biochem Cell Biol. 2008;40(9):1649-1653.
28. McConnell GC, Schneider TM, Bellamkonda RV, editors. Acute spatiotemporal changes in neuronal density surrounding microelectrode arrays implanted in rat motor cortex. Neural Engineering, 2007 CNE '07. 3rd International IEEE/EMBS Conference on; 2007 May 2-5. p. 137-40.
29. Kettenmann H. Neuroscience: the brain's garbage men. Nature. 2007;446(7139):987-989.
30. Anderson JM, Rodriguez A, Chang DT. Foreign body reaction to biomaterials. Semin Immunol. 2008;20(2):86-100.
31. Raghavendra Rao VL, Rao AM, Dogan A, Bowen KK, Hatcher J, Rothstein JD, Dempsey RJ. Glial glutamate transporter GLT-1 down-regulation precedes delayed neuronal death in gerbil hippocampus following transient global cerebral ischemia. Neurochem Int. 2000;36(6):531-537.
32. Sofroniew MV. Reactive astrocytes in neural repair and protection. Neuroscientist. 2005;11(5):400-407.
33. Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci. 2004;24(9):2143-2155.
34. Lenzlinger P, Morganti-Kossmann M-C, Laurer H, McIntosh T. The duality of the inflammatory response to traumatic brain injury. Mol Neurobiol. 2001;24(1):169-181.
35. David S, Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci. 2011;12(7):388-399.
36. Mokarram N, Merchant A, Mukhatyar V, Patel G, Bellamkonda RV. Effect of modulating macrophage phenotype on peripheral nerve repair. Biomaterials. 2012;33(34):8793-8801.
37. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci. 2009;29(43):13435-13444.
38. Elkabes S, DiCicco-Bloom EM, Black IB. Brain microglia macrophages express neurotrophins that selectively reglulate microglial proliferaction and function. J Neurosci. 1996;16:2508-2521.
39. Nakajima K, Honda S, Tohyama Y, Imai Y, Kohsaka S, Kurihara T. Neurotrophin secretion from cultured microglia. J Neurosci Res. 2001;65:322-331.
40. Munoz-Fernandez MA, Fresno M. The role of tumor necrosis factor, interlukin-6, interfuron-gamma, and inducible nitric oxide synthase in the development and pathology of the nervous system. Prog Neurobiol. 1998;56:307-340.
41. Koizumi S, Shigemoto-Mogami Y, Nasu-Tada K, Shinozaki Y, Ohsawa K, Tsuda M, Joshi BV, Jacobson KA, Kohsaka S, Inoue K. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature. 2007;446(7139):1091-1095.
42. Salińska E, Danysz W, Łazarewicz JW. The role of excitotoxicity in neurodegeneration. Folia Neuropathol. 2005;43(4):322-339.
43. Szarowski DH, Andersen MD, Retterer S, Spence AJ, Isaacson M, Craighead HG, Turner JN, Shain W. Brain responses to micro-machined silicon devices. Brain Res. 2003;983(1-2):23-35.
44. McConnell GC, Rees HD, Levey AI, Gutekunst CA, Gross RE, Bellamkonda RV. Implanted neural electrodes cause chronic, local inflammation that is correlated with local neurodegeneration. J Neural Eng. 2009;6(5):56003.
45. Rennaker RL, Miller J, Tang H, Wilson DA. Minocycline increases quality and longevity of chronic neural recordings. J Neural Eng. 2007;4(2):L1-5.
46. Zhong Y, Bellamkonda RV. Dexamethasone-coated neural probes elicit attenuated inflammatory response and neuronal loss compared to uncoated neural probes. Brain Res. 2007;1148:15-27.
47. Zhong Y, McConnell GC, Ross JD, DeWeerth SP, Bellamkonda RV. A novel dexamethasone-releasing, anti-inflammatory coating for neural implants. Neural Engineering, 2005 Conference Proceedings 2nd International IEEE EMBS Conference on; 2005 March 16-19. p. 522-525.
48. Purcell EK, Thompson DE, Ludwig KA, Kipke DR. Flavopiridol reduces the impedance of neural prostheses in vivo without affecting recording quality. J Neurosci Methods. 2009;183(2):149-157.
49. Sriram K, Miller DB, O'Callaghan JP. Minocycline attenuates microglial activation but fails to mitigate striatal dopaminergic neurotoxicity: role of tumor necrosis factor-α. J Neurochem. 2006;96(3):706-718.
50. Anderson DJ. Penetrating multichannel stimulation and recording electrodes in auditory prosthesis research. Hear Res. 2008;242(1-2):31-41.
51. Nisbet DR, Rodda AE, Horne MK, Forsythe JS, Finkelstein DI. Neurite infiltration and cellular response to electrospun polycaprolactone scaffolds implanted into the brain. Biomaterials. 2009;30(27):4573-4580.
52. Karumbaiah L, Saxena T, Carlson D, Patil K, Patkar R, Gaupp EA, Betancur M, Stanley GB, Carin L, Bellamkonda RV. Relationship between intracortical electrode design and chronic recording function. Biomaterials. 2013;34(33):8061-8074.
53. Skousen JL, Merriam SM, Srivannavit O, Perlin G, Wise KD, Tresco PA. Reducing surface area while maintaining implant penetrating profile lowers the brain foreign body response to chronically implanted planar silicon microelectrode arrays. Prog Brain Res. 2011;194:167-180.
54. Potter KA, Buck AC, Self WK, Capadona JR. Stab injury and device implantation within the brain results in inversely multiphasic neuroinflammatory and neurodegenerative responses. J Neural Eng. 2012;9(4):046020.
55. Tanaka R, Komine-Kobayashi M, Mochizuki H, Yamada M, Furuya T, Migita M, Shimada T, Mizuno Y, Urabe T. Migration of enhanced green fluorescent protein expressing bone marrow-derived microglia/macrophage into the mouse brain following permanent focal ischemia. Neuroscience. 2003;117(3):531-539.
56. Subbaroyan J. Investigations of tethering induced injury response in brain tissue by intracortical implants through modeling and in vivo experiments [dissertation]. Ann Arbor: University of Michigan; 2007.
57. Biran R, Martin DC, Tresco PA. The brain tissue response to implanted silicon microelectrode arrays is increased when the device is tethered to the skull. J Biomed Mater Res A. 2007;82(1):169-178.
58. Markwardt NT, Stokol J, Rennaker RL 2nd. Sub-meninges implantation reduces immune response to neural implants. J Neurosci Methods. 2013;214(2):119-125.
59. Roitbak T, Sykova E. Diffusion barriers evoked in the rat cortex by reactive astrogliosis. Glia. 1999;28(1):40-48.
60. Fawcett JW, Asher RA. The glial scar and central nervous system repair. Brain Res Bull. 1999;49(6):377-391.
61. Liang J, Takeuchi H, Doi Y, Kawanokuchi J, Sonobe Y, Jin S, Yawata I, Li H, Yasuoka S, Mizuno T, Suzumura A. Excitatory amino acid transporter expression by astrocytes is neuroprotective against microglial excitotoxicity. Brain Res. 2008;1210:11-19.
62. Yin J, Sakamoto K, Zhang H, Ito Z, Imagama S, Kishida S, Natori T, Sawada M, Matsuyama Y, Kadomatsu K. Transforming growth factor-beta1 upregulates keratan sulfate and chondroitin sulfate biosynthesis in microglias after brain injury. Brain Res. 2009;1263:10-22.
63. McKeon RJ, Jurynec MJ, Buck CR. The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar. J Neurosci. 1999;19(24):10778-10788.
64. Shearer MC, Niclou SP, Brown D, Asher RA, Holtmaat AJ, Levine JM, Verhaagen J, Fawcett JW. The astrocyte/meningeal cell interface is a barrier to neurite outgrowth which can be overcome by manipulation of inhibitory molecules or axonal signalling pathways. Mol Cell Neurosci. 2003;24(4):913-925.
65. Silver J, Miller JH. Regeneration beyond the glial scar. Nature Rev. 2004;5(2):146-156.
66. Busch SA, Horn KP, Cuascut FX, Hawthorne AL, Bai L, Miller RH, Silver J. Adult NG2+ cells are permissive to neurite outgrowth and stabilize sensory axons during macrophage- induced axonal dieback after spinal cord injury. J Neurosci. 2010;30(1):255-265.
67. Woolley AJ, Desai HA, Steckbeck MA, Patel NK, Otto KJ. In situ characterization of the brain-microdevice interface using Device Capture Histology. J Neurosci Methods. 2011;201(1):67-77.
68. Grill WM, Mortimer JT. Electrical properties of implant encapsulation tissue. Ann Biomed Eng. 1994;22(1):23-33.
69. Lu P, Jones LL, Tuszynski MH. Axon regeneration through scars and into sites of chronic spinal cord injury. Exp Neurol. 2007;203(1):8-21.
70. Hampton DW, Rhodes KE, Zhao C, Franklin RJ, Fawcett JW. The responses of oligodendrocyte precursor cells, astrocytes and microglia to a cortical stab injury, in the brain. Neuroscience. 2004;127(4):813-820.
71. Winslow BD, Christensen MB, Yang WK, Solzbacher F, Tresco PA. A comparison of the tissue response to chronically implanted Parylene-C-coated and uncoated planar silicon microelectrode arrays in rat cortex. Biomaterials. 2010;31(35):9163-9172.
72. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126(4):677-689.
73. Georges PC, Miller WJ, Meaney DF, Sawyer ES, Janmey PA. Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys J. 2006;90(8):3012-3018.
74. Leach JB, Brown XQ, Jacot JG, Dimilla PA, Wong JY. Neurite outgrowth and branching of PC12 cells on very soft substrates sharply decreases below a threshold of substrate rigidity. J Neural Eng. 2007;4(2):26-34.
75. Zaman MH, Trapani LM, Sieminski AL, Mackellar D, Gong H, Kamm RD, Wells A, Lauffenburger DA, Matsudaira P. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci U S A. 2006;103(29):10889-10894.
76. Li GN, Livi LL, Gourd CM, Deweerd ES, Hoffman-Kim D. Genomic and morphological changes of neuroblastoma cells in response to three-dimensional matrices. Tissue Eng. 2007;13(5):1035-1047.
77. Flanagan LA, Ju YE, Marg B, Osterfield M, Janmey PA. Neurite branching on deformable substrates. Neuroreport. 2002;13(18):2411-2415.
78. Lu YB, Franze K, Seifert G, Steinhauser C, Kirchhoff F, Wolburg H, Guck J, Janmey P, Wei E, Käs J, Reichenback A. Viscoelastic properties of individual glial cells and neurons in the CNS. Proc Natl Acad Sci U S A. 2006;103(47):17759-17764.
79. Ostrow LW, Sachs F. Mechanosensation and endothelin in astrocytes-hypothetical roles in CNS pathophysiology. Brain Res Brain Res Rev. 2005;48(3):488-508.
80. Cullen DK, Simon CM, LaPlaca MC. Strain rate-dependent induction of reactive astrogliosis and cell death in three-dimensional neuronal-astrocytic co-cultures. Brain Res. 2007;1158:103-115.
81. Ludwig KA, Uram JD, Yang J, Martin DC, Kipke DR. Chronic neural recordings using silicon microelectrode arrays electrochemically deposited with a poly(3,4- ethylenedioxythiophene) (PEDOT) film. J Neural Eng. 2006;3(1):59-70.
82. Hochberg LR, Serruya MD, Friehs GM, Mukand JA, Saleh M, Caplan AH, Branner A, Chen D, Penn RD, Donoghue JP. Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature. 2006;442(7099):164-171.
83. Subbaroyan J, Martin DC, Kipke DR. A finite-element model of the mechanical effects of implantable microelectrodes in the cerebral cortex. J Neural Eng. 2005;2(4):103-113.
84. Harris JP, Capadona JR, Miller RH, Healy BC, Shanmuganathan K, Rowan SJ, Weder C, Tyler DJ. Mechanically adaptive intracortical implants improve the proximity of neuronal cell bodies. J Neural Eng. 2011;8(6):066011.
85. Gilletti A, Muthuswamy J. Brain micromotion around implants in the rodent somatosensory cortex. J Neural Eng. 2006;3(3):189-195.
86. Seymour JP, Kipke DR. Neural probe design for reduced tissue encapsulation in CNS. Biomater. 2007;28(25):3594-3607.
87. Sanchez JC, Alba N, Nishida T, Batich C, Carney PR. Structural modifications in chronic microwire electrodes for cortical neuroprosthetics: a case study. IEEE Trans Neural Syst Rehabil Eng. 2006;14(2):217-221.
88. Yamato H, Ohwa M, Wernet W. Stability of polypyrrole and poly(3,4-ethylenedioxythiophene) for biosensor application. J Electroanal Chem (Lausanne Switz). 1995;397(1- 2):163-170.
89. Stensaas SS, Stensaas LJ. Histopathological evaluation of materials implanted in the cerebral cortex. Acta Neuropathologica. 1978 Feb 20;41(2):145-155.
90. Lee K, He J, Clement R, Massia S, Kim B. Biocompatible benzocyclobutene (BCB)-based neural implants with micro-fluidic channel. Biosens Bioelectron. 2004;20(2):404-407.
91. Nikles SA, Pellinen DS, Kitagawa J, Bradley RM, Kipke DR, Najafi K, editors. Long term in vitro monitoring of polyimide microprobe electrical properties. Engineering in Medicine and Biology Society, 2003, Proceedings of the 25th Annual International Conference of IEEE; 2003. vol. 4. p. 3340-3343.
92. Wester BA, Lee RH, LaPlaca MC. Development and characterization of in vivo flexible electrodes compatible with large tissue displacements. J Neural Eng. 2009;6(2):024002.
93. Takeuchi S, Ziegler D, Yoshida Y, Mabuchi K, Suzuki T. Parylene flexible neural probes integrated with microfluidic channels. Lab Chip. 2005;5(5):519-523.
94. Ware T, Simon D, Liu C, Musa T, Vasudevan S, Sloan A, Keefer EW, Rennaker RL 2nd, Voit W. Thiol-ene/acrylate substrates for softening intracortical electrodes. J Biomed Mater Res B Appl Biomater. 2013 May 13. [Epub ahead of print]
95. Ingber DE. Cellular mechanotransduction: putting all the pieces together again. Faseb J. 2006;20(7):811-827.
96. Peyton SR, Ghajar CM, Khatiwala CB, Putnam AJ. The emergence of ECM mechanics and cytoskeletal tension as important regulators of cell function. Cell Biochem Biophys. 2007;47(2):300-320.
97. Chen KD, Li YS, Kim M, Li S, Yuan S, Chien S, Shyy JY. Mechanotransduction in response to shear stress. Roles of receptor tyrosine kinases, integrins, and Shc. J Biol Chem. 1999;274(26):18393-18400.
98. Clark K, Langeslag M, Figdor CG, van Leeuwen FN. Myosin II and mechanotransduction: a balancing act. Trends Cell Biol. 2007;17(4):178-186.
99. Williams JC, Rennaker RL, Kipke DR. Long-term neural recording characteristics of wire microelectrode arrays implanted in cerebral cortex. Brain Res Protoc. 1999;4(3):303-313.
100. Vetter RJ, Williams JC, Hetke JF, Nunamaker EA, Kipke DR. Chronic neural recording using silicon-substrate microelectrode arrays implanted in cerebral cortex. IEEE Trans Biomed Eng. 2004;51(6):896-904.
101. Simeral JD, Kim SP, Black MJ, Donoghue JP, Hochberg LR. Neural control of cursor trajectory and click by a human with tetraplegia 1000 days after implant of an intracortical microelectrode array. J Neural Eng. 2011;8(2):025027.
102. Hochberg LR, Bacher D, Jarosiewicz B, Masse NY, Simeral JD, Vogel J, Haddadin S, Liu J, Cash SS, van der Smagt P, Donoghue JP. Reach and grasp by people with tetraplegia using a neurally controlled robotic arm. Nature. 2012;485(7398):372-375.
103. Collinger JL, Wodlinger B, Downey JE, Wang W, Tyler- Kabara EC, Weber DJ, McMorland AJC, Velliste M, Boninger ML, Schwartz AB. High-performance neuroprosthetic control by an individual with tetraplegia. Lancet. 2013;381(9866):557-564.
104. Velliste M, Perel S, Spalding MC, Whitford AS, Schwartz AB. Cortical control of a prosthetic arm for self-feeding. Nature. 2008;453(7198):1098-1101.
105. Taylor DM, Tillery SIH, Schwartz AB. Direct cortical control of 3D neuroprosthetic devices. Science. 2002;296(5574):1829-1832.
106. Nicolelis MA, Dimitrov D, Carmena JM, Crist R, Lehew G, Kralik JD, Wise SP. Chronic, multisite, multielectrode recordings in macaque monkeys. Proc Natl Acad Sci U S A. 2003;100(19):11041-11046.
107. Taylor DM, Tillery SIH, Schwartz AB. Information conveyed through brain-control: cursor versus robot. IEEE Trans Neural Syst Rehabil Eng. 2003;11(2):195-199.
108. Kennedy PR, Bakay RA, Moore MM, Adams K, Goldwaithe J. Direct control of a computer from the human central nervous system. IEEE Trans Rehabil Eng. 2000;8(2):198-202.
109. Jones KE, Campbell PK, Normann RA. A glass/silicon composite intracortical electrode array. Ann Biomed Eng. 1992;20(4):423-437.
110. Schwartz AB. Cortical neural prosthetics. Annu Rev Neurosci. 2004;27:487-507.
111. Tonet O, Marinelli M, Citi L, Rossini PM, Rossini L, Megali G, Dario P. Defining brain-machine interface applications by matching interface performance with device requirements. J Neurosci Methods. 2008;167(1):91-104.
112. Fitts PM. The information capacity of the human motor system in controlling the amplitude of movement. J Exp Psychol. 1954;47(6):381-391.
113. Wolpaw JR, Ramoser H, McFarland DJ, Pfurtscheller G. EEG-based communication: improved accuracy by response verification. IEEE Trans Rehabil Eng. 1998;6(3):326-333.
114. Kronegg J, Voloshynovskiy S, Pun T, editors. Analysis of bit-rate definitions for brain computer interfaces. 2005 International Conference on Human-computer interaction; 2005.
115. Wolpaw JR, Birbaumer N, McFarland DJ, Pfurtscheller G, Vaughan TM. Brain-computer interfaces for communication and control. Clin Neurophysiol. 2002 Jun;113(6):767-791.
116. Simpson T, Broughton C, Gauthier MJ, Prochazka A. Tooth-click control of a hands-free computer interface. IEEE Trans Biomed Eng. 2008;55(8):2050-2056.
117. Ryu SI, Shenoy KV. Human cortical prostheses: lost in translation? Neurosurg Focus. 2009;27(1):E5.
118. Williams MR, Kirsch RF. Evaluation of head orientation and neck muscle EMG signals as command inputs to a human-computer interface for individuals with high tetraplegia. IEEE Trans Neural Syst Rehabil Eng. 2008;16(5):485-496.
119. Simpson T, Gauthier M, Prochazka A. Evaluation of toothclick triggering and speech recognition in assistive technology for computer access. Neurorehab Neural Repair. 2010;24(2):188-194.
120. Huo X, Ghovanloo M. Evaluation of a wireless wearable tongue-computer interface by individuals with high-level spinal cord injuries. J Neural Eng. 2010;7(2):26008.
121. Kherlopian AR, Gerrein JP, Yue M, Kim KE, Kim JW, Sukumaran M, Sajda P. Electrooculogram based system for computer control using a multiple feature classification model. Conf Proc IEEE Eng Med Biol Sci. 2006;1:1295-1298.
122. Mateo JC, Agustin JS, Hansen JP. Gaze beats mouse: hands-free selection by combining gaze and emg. CHI '08 extended abstracts on human factors in computing systems; 2008; Florence, Italy. New York: ACM; 2008. p. 3039-3044.
123. Surakka V, Illi M, Isokoski P. Gazing and frowning as a new human-computer interaction technique. ACM Trans Appl Percept. 2004;1(1):40-56.
124. Abbott WW, Faisal AA. Ultra-low-cost 3D gaze estimation: an intuitive high information throughput compliment to direct brain-machine interfaces. J Neural Eng. 2012;9(4):046016.
125. Schwartz AB, Kettner RE, Georgopoulos AP. Primate motor cortex and free arm movements to visual targets in three-dimensional space. I. Relations between single cell discharge and direction of movement. J Neurosci. 1988;8(8):2913-2927.
126. Kettner RE, Schwartz AB, Georgopoulos AP. Primate motor cortex and free arm movements to visual targets in three-dimensional space. III. Positional gradients and population coding of movement direction from various movement origins. J Neurosci. 1988;8(8):2938-2947.
127. Georgopoulos AP, Kettner RE, Schwartz AB. Primate motor cortex and free arm movements to visual targets in three-dimensional space. II. Coding of the direction of movement by a neuronal population. J Neurosci. 1988;8(8):2928-2937.
128. Lempka SF, Johnson MD, Barnett DW, Moffitt MA, Otto KJ, Kipke DR, McIntyre CC. Optimization of microelectrode design for cortical recording based on thermal noise considerations. Conf Proc IEEE Eng Med Biol Soc. 2006;1:3361-3364.
129. Moffitt MA, McIntyre CC. Model-based analysis of cortical recording with silicon microelectrodes. Clin Neurophysiol. 2005;116(9):2240-2250.
130. Lempka SF, Johnson MD, Moffitt MA, Otto KJ, Kipke DR, McIntyre CC. Theoretical analysis of intracortical microelectrode recordings. J Neural Eng. 2011;8(4):045006.
131. Ajiboye AB, Simeral JD, Donoghue JP, Hochberg LR, Kirsch RF. Prediction of imagined single-joint movements in a person with high-level tetraplegia. IEEE Trans Biomed Eng. 2012;59(10):2755-2765.
132. Katzner S, Nauhaus I, Benucci A, Bonin V, Ringach DL, Carandini M. Local origin of field potentials in visual cortex. Neuron. 2009;61(1):35-41.
133. Henze DA, Borhegyi Z, Csicsvari J, Mamiya A, Harris KD, Buzsaki G. Intracellular features predicted by extracellular recordings in the hippocampus in vivo. J Neurophysiol. 2000;84(1):390-400.
134. Tao J, Rolls MM. Dendrites have a rapid program of injury-induced degeneration that is molecularly distinct from developmental pruning. J Neurosci. 2011;31(14):5398-5405.
135. Rennaker RL, Street S, Ruyle AM, Sloan AM. A comparison of chronic multi-channel cortical implantation techniques: manual versus mechanical insertion. J Neurosci Methods. 2005;142(2):169-176.
136. Rennaker RL, Ruyle AM, Street SE, Sloan AM. An economical multi-channel cortical electrode array for extended periods of recording during behavior. J Neurosci Methods. 2005;142(1):97-105.
137. Tresco PA, Winslow BD. The challenge of integrating devices into the central nervous system. Crit Rev Biomed Eng. 2011;39(1):29-44.
138. Kim SP, Simeral JD, Hochberg LR, Donoghue JP, Friehs GM, Black MJ. Point-and-click cursor control with an intracortical neural interface system in humans with tetraplegia. IEEE Trans Neural Syst Rehabil Eng. 2011;19(2):193-203.
139. Kim SP, Simeral JD, Hochberg LR, Donoghue JP, Black MJ. Neural control of computer cursor velocity by decoding motor cortical spiking activity in humans with tetraplegia. J Neural Eng. 2008;5(4):455-476.
140. Leach J, Achyuta AKH, Murthy SK. Bridging the divide between neuroprosthetic design, tissue engineering and neurobiology. Front Neuroeng. 2010;2:18.
141. Grill WM, Norman SE, Bellamkonda RV. Implanted neural interfaces: biochallenges and engineered solutions. Annu Rev Biomed Eng. 2009;11:1-24.
142. Williams JC, Hippensteel JA, Dilgen J, Shain W, Kipke DR. Complex impedance spectroscopy for monitoring tissue responses to inserted neural implants. J Neural Eng. 2007;4(4):410-423.
143. Mercanzini A, Colin P, Bensadoun JC, Bertsch A, Renaud P. In vivo electrical impedance spectroscopy of tissue reaction to microelectrode arrays. IEEE Trans Biomed Eng. 2009;56(7):1909-1918.
144. Otto KJ, Johnson MD, Kipke DR. Voltage pulses change neural interface properties and improve unit recordings with chronically implanted microelectrodes. IEEE Trans Biomed Eng. 2006;53(2):333-340.
145. Suner S, Fellows MR, Vargas-Irwin C, Nakata GKANGK, Donoghue JPADJP. Reliability of signals from a chronically implanted, silicon-based electrode array in non-human primate primary motor cortex. IEE Trans Neural Syst Rehabil Eng. 2005;13(4):524-541.
146. Wadhwa R, Lagenaur CF, Cui XT. Electrochemically controlled release of dexamethasone from conducting polymer polypyrrole coated electrode. J Control Release. 2006;110(3):531-541.
147. Kim DH, Martin DC. Sustained release of dexamethasone from hydrophilic matrices using PLGA nanoparticles for neural drug delivery. Biomaterials. 2006;27(15):3031-3037.
148. Spataro L, Dilgen J, Retterer S, Spence AJ, Isaacson M, Turner JN, Shain W. Dexamethasone treatment reduces astroglia responses to inserted neuroprosthetic devices in rat neocortex. Exp Neurol. 2005;194(2):289-300.
149. Harris JP. The glia-neuronal response to cortical electrodes: interactions with substrate stiffness and electrophysiology [dissertation]. Cleveland (OH): Case Western Reserve University; 2011.