In vitro microelectrode array technology and neural recordings

Critical Reviews in Biomedical Engineering

Volumn 39, Issue 1, 2011, Pages 45-61

  Nam, Yoonkey ^a   Wheeler, Bruce C ^b  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b J Crayton Pruitt Family Department of Biomedical Engineering   (United States)

Author keywords

Cell electrode coupling; MEA technology; Microelectrode array; Neural interface; Neural recording

Indexed keywords

BRAIN COMPUTER INTERFACE; MICROELECTRODES; NEURAL NETWORKS; NEURONS; SURFACE CHEMISTRY;

BIOLOGICAL ENVIRONMENTS; CELL ELECTRODES; CELL-ELECTRODE INTERFACES; CULTURED NEURAL NETWORKS; ELECTRODE CONFIGURATIONS; MICROELECTRODE ARRAY; NEURAL INTERFACES; NEURAL RECORDINGS;

MORE ELECTRIC AIRCRAFT;

CARBON NANOTUBE; NANOMATERIAL; SELF ASSEMBLED MONOLAYER;

ARTICLE; BIOTECHNOLOGY; BRAIN NERVE CELL; CELL SIZE; ELECTRODE; FIELD EFFECT TRANSISTOR; IN VITRO STUDY; MEMBRANE POTENTIAL; MICROELECTRODE; NERVE CELL NETWORK; NERVE POTENTIAL; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL NOISE RATIO; SIGNAL PROCESSING;

EID: 79960043082     PISSN: 0278940X     EISSN: None     Source Type: Journal    
DOI: 10.1615/critrevbiomedeng.v39.i1.40     Document Type: Article

References (96)

1. Valor LM, Charlesworth P, Humphreys L, Anderson CN, Grant SG. Network activity-independent coordinated gene expression program for synapse assembly. Proc Natl Acad Sci U S A. 2007;104(11):4658-63.
2. Dotti CG, Sullivan CA, Banker GA. The establishment of polarity by hippocampal neurons in culture. J Neurosci. 1988;8(4):1454-68.
3. Taylor AM, Blurton-Jones M, Rhee SW, Cribbs DH, Cotman CW, Jeon NL. A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat Methods. 2005;2(8):599-605.
4. Bi GQ, Poo MM. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci. 1998;18(24):10464-72.
5. Bi G, Poo M. Distributed synaptic modification in neural networks induced by patterned stimulation. Nature. 1999;401(6755):792-6.
6. Campenot RB, Lund K, Mok SA. Production of compartmented cultures of rat sympathetic neurons. Nat Protoc. 2009;4(12):1869-87.
7. Segal MM, Furshpan EJ. Epileptiform activity in microcultures containing small numbers of hippocampal neurons. J Neurophysiol. 1990;64(5):1390-9.
8. Kleinfeld D, Kahler KH, Hockberger PE. Controlled outgrowth of dissociated neurons on patterned substrates. J Neurosci. 1988;8(11):4098-120.
9. Gahwiler BH, Capogna M, Debanne D, McKinney RA, Thompson SM. Organotypic slice cultures: a technique has come of age. Trends Neurosci. 1997;20(10):471-7.
10. Gross GW, Williams AN, Lucas JH. Recording of spontaneous activity with photoetched microelectrode surfaces from mouse spinal neurons in culture. J Neurosci Methods. 1982;5:13-22.
11. Thomas CAJ, Springer PA, Loeb GE, Berwald-Netter Y, Okun LM. A miniature microelectrode array to monitor the bioelectric activity of cultured cells. Exp Cell Res. 1972;74:61-6.
12. Pine J. Recording action potentials from cultured neurons with extracellular microcircuit electrodes. J Neurosci Methods. 1980;2(1):19-31.
13. Jimbo Y, Kawana A, Parodi P, Torre V. The dynamics of a neuronal culture of dissociated cortical neurons of neonatal rats. Biol Cybern. 2000;83:1-20.
14. Eytan D, Marom S. Dynamics and effective topology underlying synchronization in networks of cortical neurons. J Neurosci. 2006;26(33):8465-76.
15. Baruchi I, Volman V, Raichman N, Shein M, Ben-Jacob E. The emergence and properties of mutual synchronization in in vitro coupled cortical networks. Eur J Neurosci. 2008;28(9):1825-35.
16. Wagenaar DA, Madhavan R, Pine J, Potter SM. Controlling bursting in cortical cultures with closed-loop multi-electrode stimulation. J Neurosci. 2005;25(3):680-8.
17. Mathieson K, Cunningham W, Marchal J, Melone J, Horn M, O'Shea V, Smith KM, Litke A, Chichilnisky EJ, Rahman M. Fabricating highdensity microarrays for retinal recording. Microelectronic Engineering. 2003;67-68:520-7.
18. Bucher V, Brunner B, Leibrock C, Schubert M, Nisch W. Electrical properties of a light-addressable microelectrode chip with high electrode density for extracellular stimulation and recording of excitable cells. Biosens Bioelectron. 2001 2001;16(3):205-10.
19. Frey U, Egert U, Heer F, Hafizovic S, Hierlemann A. Microelectronic system for high-resolution mapping of extracellular electric fields applied to brain slices. Biosens Bioelectron. 2009;24(7):2191-8.
20. Berdondini L, Imfeld K, Maccione A, Tedesco M, Neukom S, Koudelka-Hep M, Martinoia S. Active pixel sensor array for high spatio-temporal resolution electrophysiological recordings from single cell to large scale neuronal networks. Lab Chip. 2009;9(18):2644-51.
21. Eversmann B, Jenkner M, Hofmann F, Paulus C, Brederlow R, Holzapfl B, Fromherz P, Merz M, Brenner M, Schreiter M, Gabl R, Plehnert K, Steinhauser M, Eckstein G, Schmitt-Landsiedel D, Thewes R. A 128 × 128 CMOS Biosensor Array for Extracellular Recording of Neural Activity. IEEE J Solid-State Circuits. 2003;38(12):2306-17.
22. Jun SB, Hynd MR, Dowell-Mesfin N, Smith KL, Turner JN, Shain W, Kim S J. Low-density neuronal networks cultured using patterned poly-l-lysine on microelectrode arrays. J Neurosci Methods. 2007;160(2):317-26.
23. Nam Y, Wheeler BC, Heuschkel MO. Neural recording and stimulation of dissociated hippocampal cultures using microfabricated threedimensional tip electrode array. J Neurosci Methods. 2006;155(2):296-9.
24. Chang JC, Brewer GJ, Wheeler BC. Modulation of neural network activity by patterning. Biosens Bioelectron. 2001;16:527-33.
25. Suzuki I, Sugio Y, Jimbo Y, Yasuda K. Stepwise pattern modification of neuronal network in photo-thermally-etched agarose architecture on multi-electrode array chip for individual-cellbased electrophysiological measurement. Lab Chip. 2005;5(3):241-7.
26. Sokal DM, Mason R, Parker TL. Multi-neuronal recordings reveal a differential effect of thapsigargin on bicuculline-or gabazine-induced epileptiform excitability in rat hippocampal neuronal networks. Neuropharmacology. 2000;39(12):2408-17.
27. Golan H, Mikenberg K, Greenberger V, Segal M. GABA withdrawal modifies network activity in cultured hippocampal neurons. Neural Plasticity. 2000;7(1-2):31-42.
28. Selinger JV, Pancrazio JJ, Gross GW. Measuring synchronization in neuronal networks for biosensor applications. Biosens Bioelectron. 2004;19(7):675-83.
29. Morefield SI, Keefer EW, Chapman KD, Gross GW. Drug evaluations using neuronal networks cultured on microelectrode arrays. Biosens Bioelectron. 2000;15(7-8):383-96.
30. Wagenaar DA, Pine J, Potter SM. Searching for plasticity in dissociated cortical cultures on multi-electrode arrays. J Negat Results Biomed. 2006;5:16.
31. Bakkum DJ, Chao ZC, Potter SM. Spatio-temporal electrical stimuli shape behavior of an embodied cortical network in a goal-directed learning task. J Neural Eng. 2008;5(3):310-23.
32. van Pelt J, Wolters PS, Corner MA, Rutten WL, Ramakers GJ. Long-term characterization of firing dynamics of spontaneous bursts in cultured neural networks. IEEE Trans Biomed Eng. 2004;51(11):2051-62.
33. Eytan D, Brenner N, Marom S. Selective adaptation in networks of cortical neurons. J Neurosci. 2003;23(28):9349-56.
34. Eytan D, Minerbi A, Ziv N, Marom S. Dopamineinduced dispersion of correlations between action potentials in networks of cortical neurons. J Neurophysiol. 2004;92(3):1817-24.
35. Shahaf G, Marom S. Learning in networks of cortical neurons. J Neurosci. 2001;21(22):8782-8.
36. Segev R, Shapira Y, Benveniste M, Ben-Jacob E. Observation and modeling of synchronized bursting in two-dimensional neural network. Phys Rev E. 2001;64(011920).
37. Ruaro ME, Bonifazi P, Torre V. Toward the neurocomputer: image processing and pattern recognition with neuronal cultures. IEEE Trans Biomed Eng. 2005;52(3):371-83.
38. Illes S, Theiss S, Hartung HP, Siebler M, Dihne M. Niche-dependent development of functional neuronal networks from embryonic stem cell-derived neural populations. BMC Neurosci. 2009;10:93.
39. Illes S, Fleischer W, Siebler M, Hartung HP, Dihne M. Development and pharmacological modulation of embryonic stem cell-derived neuronal network activity. Exp Neurol. 2007;207(1):171-6.
40. James CD, Spence AJ, Dowell-Mesfin NM, Hussain RJ, Smith KL, Craighead HG, Isaacson MS, Shain W, Turner JN. Extracellular recordings from patterned neuronal networks using planar microelectrode arrays. IEEE Trans Biomed Eng. 2004;51(9):1640-8.
41. Nam Y, Branch DW, Wheeler BC. Epoxy-silane linking of biomolecules is simple and effective for patterning neuronal cultures. Biosens Bioelectron. 2006;22(5):589-97.
42. Potter SM, DeMarse TB. A new approach to neural cell culture for long-term studies. J Neurosci Methods. 2001;110(1-2):17-24.
43. Corey JM, Wheeler BC, Brewer GJ. Compliance of hippocampal neurons to patterned substrate networks. J Neurosci Res. 1991;30:300-7.
44. Nam Y, Wheeler BC, editors. Imaging locations of neurons vs. glia in low density culture. IEEE EMBS Conference on Neural Engineering; 2005; Arlington, VA, USA.
45. Branch DW, Wheeler BC, Brewer GJ, Leckband DE. Long-term stability of grafted polyethylene glycol surfaces for use with microstamped substrates in neuronal cell culture. Biomaterials. 2001;22(10):1035-47.
46. Boulton AA, Baker GB, Vanderwolf CH, Humphrey DR, Schmidt EM. Extracellular singleunit recording methods. Neurophysiological techniques: Humana Press; 1991. p. 1-64.
47. Moffitt MA, McIntyre CC. Model-based analysis of cortical recording with silicon microelectrodes. Clin Neurophysiol. 2005;116(9):2240-50.
48. Rall W. Electrophysiology of a dendritic neuron model. Biophys J. 1962;2(2)Pt 2:145-67.
49. Plonsey R. The active fiber in a volume conductor. IEEE Trans Biomed Eng. 1974;21(5):371-81.
50. Drake KL, Wise KD, Farraye J, Anderson DJ, Be-Ment SL. Performance of planar multisite microprobes in recording extracellular single-unit intracortical activity. IEEE Trans Biomed Eng. 1988;35(9):719-32.
51. Claverol-Tinture E, Pine J. Extracellular potentials in low-density dissociated neuronal cultures. J Neurosci Methods. 2002;117(1):13-21.
52. Regehr WG, Pine J, Cohan CS, Mischke MD, Tank DW. Sealing cultured invertebrate neurons to embedded dish electrodes facilitates long-term stimulation and recording. J Neurosci Methods. 1989;30:91-106.
53. Fromherz P, Offenhausser A, Vetter T, Weis J. A neuron-silicon junction: a Retzius cell of the leech on an insulated-gate field-effect transistor. Science. 1991;252(5010):1290-3.
54. Fromherz P, Muller CO, Weis R. Neuron transistor: Electrical transfer function measured by the patch-clamp technique. Phys Rev Lett. 1993;71(24):4079-82.
55. Jenkner M, Muller B, Fromherz P. Interfacing a silicon chip to pairs of snail neurons connected by electrical synapses. Biol Cybern. 2001;84(4):239-49.
56. Schatzthauer R, Fromherz P. Neuron-silicon junction with voltage-gated ionic currents. Eur J Neurosci. 1998;10(6):1956-62.
57. Vassanelli S, Fromherz P. Transistor records of excitable neurons from rat brain. Appl Phys A. 1998;66:459-63.
58. Buitenweg JR, Rutten WL, Marani E. Modeled channel distributions explain extracellular recordings from cultured neurons sealed to microelectrodes. IEEE Trans Biomed Eng. 2002c;49(12 Pt 2):1580-90.
59. Dworak BJ, Wheeler BC. Novel MEA platform with PDMS microtunnels enables the detection of action potential propagation from isolated axons in culture. Lab Chip. 2009;9(3):404-10.
60. Nam Y. Engineering Principles to design and analyze patterned neuronal cultures using multielectrode arrays. Urbana: University of Illinois; 2005.
61. Costa PF. The kinetic parameters of sodium currents in maturing acutely isolated rat hippocampal CA1 neurones. Dev Brain Res. 1996;91(1):29-40.
62. Picken Bahrey HL, Moody WJ. Early development of voltage-gated ion currents and firing properties in neurons of the mouse cerebral cortex. J Neurophysiol. 2003;89(4):1761-73.
63. Nam Y, Chang J, Khatami D, Brewer GJ, Wheeler BC. Patterning to enhance activity of cultured neuronal networks. IEE Proc Nanobiotechnol. 2004;151(3):109-15.
64. Brewer GJ, Boehler MD, Pearson RA, DeMaris AA, Ide AN, Wheeler BC. Neuron network activity scales exponentially with synapse density. J Neural Eng. 2009;6(1):014001.
65. Ichikawa M, Muramoto K, Kobayashi K, Kawahara M, Kuroda Y. Formation and maturation of synapses in primary cultures of rat cerebral cortical cells: an electron microscopic study. Neurosci Res. 1993;16(2):95-103.
66. Muramoto K, Ichikawa M, Kawahara M, Kobayashi K, Kuroda Y. Frequency of synchronous oscillations of neuronal activity increases during development and is correlated to the number of synapses in cultured cortical neuron networks. Neurosci Lett. 1993;163(2):163-5.
67. Chang JC, Brewer GJ, Wheeler BC. Neuronal network structuring induces greater neuronal activity through enhanced astroglial development. J Neural Eng. 2006;3(3):217-26.
68. Nam Y, Brewer GJ, Wheeler BC. Development of astroglial cells in patterned neuronal cultures. J Biomater Sci Polym Ed. 2007;18(8):1091-100.
69. Polikov VS, Tresco PA, Reichert WM. Response of brain tissue to chronically implanted neural electrodes. J Neurosci Methods. 2005;148(1):1-18.
70. Boehler MD, Wheeler BC, Brewer GJ. Added astroglia promote greater synapse density and higher activity in neuronal networks. Neuron Glia Biol. 2007;3:127-40.
71. Jimbo Y, Robinson HPC, Kawana A. Simultaneous measurement of intracellular calcium and electrical activity from patterned neural networks in culture. IEEE Trans Biomed Eng. 1993;40(8):804-10.
72. Novak JL, Wheeler BC. Recording from the Aplysia abdominal ganglion with a planar microelectrode array. IEEE Trans Biomed Eng. 1986;33(2):196-202.
73. Borkholder DA, Bao J, Maluf NI, Perl ER, Kovacs GT. Microelectrode arrays for stimulation of neural slice preparations. J Neurosci Methods. 1997;77(1):61-6.
74. Oka H, Shimono K, Ogawa R, Sugihara H, Taketani M. A new planar multielectrode array for extracellular recording: application to hippocampal acute slice. J Neurosci Methods. 1999;93(1):61-7.
75. Gross GW, Wen WY, Lin JW. Transparent indium-tin oxide electrode patterns for extracellular, multisite recording in neuronal cultures. J Neurosci Methods. 1985;15(3):243-52.
76. Heuschkel MO, Fejtl M, Raggenbass M, Bertrand D, Renaud P. A three-dimensional multi-electrode array for multi-site stimulation and recording in acute brain slices. J Neurosci Methods. 2002;114(2):135-48.
77. Egert U, Schlosshauer B, Fennrich S, Nisch W, Fejtl M, Knott T, Haemmerle H. A novel organotypic long-term culture of the rat hippocampus on substrate-integrated multielectrode array. Brain Res Brain Res Protoc. 1998;2:229-42.
78. Kim JH, Kang G, Nam Y, Choi YK. Surfacemodified microelectrode array with flake nanostructure for neural recording and stimulation. Nanotechnology. 2010;21(8):85303.
79. Park S, Song YJ, Boo H, Chung TD. Nanoporous Pt microelectrode for neural stimulation and recording: in vitro characterization. J Phys Chem C. 2010;114(19):8721-6.
80. Gabay T, Ben-David M, Kalifa I, Sorkin R, Abrams ZR, Ben-Jacob E, Hanein Y. Electrochemical and biological properties of carbon nanotube based multi-electrode arrays. Nanotechnology. 2007;18(3):035201.
81. Keefer EW, Botterman BR, Romero MI, Rossi AF, Gross GW. Carbon nanotube coating improves neuronal recordings. Nat Nanotechnol. 2008;3(7):434-9.
82. Chang JC, Brewer GJ, Wheeler BC. Microelectrode array recordings of patterned hippocampal neurons for four weeks. Biomed Microdevices. 2000;2(4):245-53.
83. Segev R, Benveniste M, Hulata E, Cohen N, Palevski A, Kapon E, Shapira Y, Ben Jacob E. Long term behavior of lithographically prepared in vitro neuronal networks. Phys Rev Lett. 2002;88(11):118102.
84. Nam Y, Chang JC, Wheeler BC, Brewer GJ. Gold-coated microelectrode array with thiol linked self-assembled monolayers for engineering neuronal cultures. IEEE Trans Biomed Eng. 2004;51(1):158-65.
85. Jungblut M, Knoll W, Thielemann C, Pottek M. Triangular neuronal networks on microelectrode arrays: an approach to improve the properties of low-density networks for extracellular recording. Biomed Microdevices. 2009;11(6):1269-78.
86. Merz M, Fromherz P. Polyester microstructures for topographical control of outgrowth and synapse formation of snail neurons. Adv Mater. 2002;14(2):141-4.
87. Kang G, Lee JH, Lee CS, Nam Y. Agarose microwell based neuronal micro-circuit arrays on microelectrode arrays for high throughput drug testing. Lab Chip. 2009;9(22):3236-42.
88. Morin F, Nishimura N, Griscom L, Lepioufle B, Fujita H, Takamura Y, Tamiya E. Constraining the connectivity of neuronal networks cultured on microelectrode arrays with microfluidic techniques: a step towards neuron-based functional chips. Biosens Bioelectron. 2006;21(7):1093-100.
89. Claverol-Tinture E, Cabestany J, Rosell X. Multisite recording of extracellular potentials produced by microchannel-confined neurons in-vitro. IEEE Trans Biomed Eng. 2007;54(2):331-5.
90. Zeck G, Fromherz P. Noninvasive neuroelectronic interfacing with synaptically connected snail neurons immobilized on a semiconductor chip. Proc Natl Acad Sci U S A. 2001;98(18):10457-62.
91. Griscom L, Degenaar P, LePioufle B, Tamiya E, Fujita H. Techniques for patterning and guidance of primary culture neurons on microelectrode arrays. Sensors Actuators B-Chem. 2002;83(1-3):15-21.
92. Claverol-Tinture E, Ghirardi M, Fiumara F, Rosell X, Cabestany J. Multielectrode arrays with elastomeric microstructured overlays for extracellular recordings from patterned neurons. J Neural Eng. 2005;2(2):L1-7.
93. Ravula SK, McClain MA, Wang MS, Glass JD, Frazier AB. A multielectrode microcom partment culture platform for studying signal transduction in the nervous system. Lab Chip. 2006;6(12):1530-6.
94. Grattarola M, Martinoia S. Modeling the neuron-microtransducer junction: from extracellular to patch recording. IEEE Trans Biomed Eng. 1993;40(1):35-41.
95. Jenkner M, Fromherz P. Bistability of membrane conductance in cell adhesion observed in a neuron transistor. Phys Rev Lett. 1997;79:4705-8.
96. Hai A, Shappir J, Spira ME. In-cell recordings by extracellular microelectrodes. Nat Methods. 2010;7(3):200-2.