Investigating neuronal activity with planar microelectrode arrays: Achievements and new perspectives

Journal of Bioscience and Bioengineering

Volumn 100, Issue 2, 2005, Pages 131-143

  Morin, Fabrice O ^a   Takamura, Yuzuru ^a   Tamiya, Eiichi ^a  

^a JAPAN ADVANCED INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

Cultured neural networks; Electrical stimulation; Long term monitoring; Planar microelectrode arrays; Synchronization

Indexed keywords

DYNAMICS; MICROELECTRODES; PHYSIOLOGY;

CULTURED NEURAL NETWORKS; ELECTRICAL STIMULATION; LONG-TERM MONITORING; PLANAR MICROELECTRODE ARRAYS;

NEURAL NETWORKS;

ADAPTATION; BIOTECHNOLOGY; CELL ACTIVITY; CONSCIOUSNESS; DYNAMICS; ELECTROSTIMULATION; INFORMATION PROCESSING; LEARNING; MEMORY CONSOLIDATION; MICROELECTRODE; NERVE CELL; NERVE CELL NETWORK; REVIEW; SIGNAL TRANSDUCTION;

EID: 27644594482     PISSN: 13891723     EISSN: None     Source Type: Journal    
DOI: 10.1263/jbb.100.131     Document Type: Review

References (117)

1. Thomas, C., Springer, P., Loeb, G., Berwald-Netter, Y., and Okun, L.: A miniature microelectrode array to monitor the bioelectric activity of cultured cells. Exp. Cell Res., 74, 61-66 (1972).
2. Potter, S. M.: Distributed processing in cultured neuronal networks. Prog. Brain Res., 130, 49-62 (2001).
3. Pine, J.: Recording action potentials from cultured neurons with extracellular microcircuit electrodes. J. Neurosci. Methods, 2, 19-31 (1980).
4. Israel, D., Barry, W., Edell, D., and Mark, R.: An array of microelectrodes to stimulate and record from cardiac cells in culture. Am. J. Physiol., 247, H669-H674 (1984).
5. Novak, J. and Wheeler, B.: Recording from the aplysia abdominal ganglion with a planar microelectrode array. IEEE Trans. Biomed. Eng., 33, 196-202 (1986).
6. Regehr, W. G., Pine, J., Cohan, C. S., Mischke, M. D., and Tank, D. W.: Sealing cultured invertebrate neurons to embedded dish electrodes facilitates long-term stimulation and recording. J. Neurosci. Methods, 30, 91-106 (1989).
7. Connolly, P., Curtis, A., Dow, J., and Wilkinson, C.: An extracellular microelectrode array for monitoring electrogenic cells in culture. Biosens. Bioelectron., 5, 223-234 (1990).
8. Jimbo, Y. and Kawana, A.: Electrical stimulation and recording from cultured neurons using a planar microelectrode array. Bioelectrochem. Bioenerg., 29, 193-204 (1992).
9. Martinoia, S., Bove, M., Carlini, G., Ciccarelli, C., Grattarola, M., Storment, C., and Kovacs, G.: A general-purpose system for long-term recording from a microelectrode array coupled to excitable cells. J. Neurosci. Methods, 48, 115-121 (1993).
10. Nisch, W., Bock, J., Egert, U., Hammerle, H., and Mohr, A.: A thin film microelectrode array for monitoring extracellular neuronal activity in vitro. Biosens. Bioelectron., 9, 737-741 (1994).
11. Cunningham, W., Mathieson, K., McEwan, F., Blue, A., McGeachy, R., McLeod, J., Morris-Ellis, C., O'Shea, V., Smith, K., Litke, A., and Rahman, M.: Fabrication of microelectrode arrays for neural measurements from retinal tissue. J. Phys. D Appl. Phys., 34, 2804-2809 (2001).
12. Egert, U., Schlosshauer, B., Fennrich, S., Nisch, W., Fejtl, M., Knott, T., Muller, T., and Hammerle, H.: A novel organotypic long-term culture of the rat hippocampus on substrate-integrated multielectrode arrays. Brain Res. Brain Res. Protoc., 2, 229-242 (1998).
13. Honma, S., Shirakawa, T., Katsuno, Y., Namishii, M., and Honma, K.: Circadian periods of single suprachiasmatic neurons in rats. Neurosci. Lett., 250, 157-160 (1998).
14. Egert, U., Heck, D., and Aertsen, A.: Two-dimensional monitoring of spiking networks in acute brain slices. Exp. Brain Res., 142, 268-274 (2002).
15. Wirth, C. and Lücher, H.-R.: Spatiotemporal evolution of excitation and inhibition in the rat barrel cortex investigated with multielectrode array. J. Neurophysiol., 91, 1635-1647 (2004).
16. Hofmann, F., Guenther, E., Hämerle, H., Leibrock, C., Berezin, V., Bock, E., and Volkmer, H.: Functional re-establishment of the perforant pathway in organotypic co-cultures on microelectrode arrays. Brain Res., 1071, 184-196 (2004).
17. Stett, A., Egert, U., Guenther, E., Hofmann, F., Meyer, T., Nisch, W., and Hammerle, H.: Biological applications of microelectrode arrays in drug discovery and basic research. Anal. Bioanal. Chem., 377, 486-495 (2003).
18. Gross, G., Rhoades, B., Reust, D., and Schwalm, F.: Stimulation of mmonolayer networks in culture through thin-film indium-tin oxide recording electrodes. J. Neurosci. Methods, 50, 131-143 (1993).
19. Gholmieh, G., Courellis, S., Fakheri, S., Cheung, E., Marmarelis, V., Baudry, M., and Berger, T.: Detection and classification of neurotoxins using a novel short-term plasticity quantification method. Biosens. Bioelectron., 18, 1467-1478 (2003).
20. Jimbo, Y., Tateno, T., and Robinson, H.: Simultaneous induction of pathway-specific potentiation and depression in networks of cortical neurons. Biophys. J., 76, 670-678 (1999).
21. Shahaf, G. and Marom, S.: Learning in networks of cortical neurons. J. Neurosci., 21, 8782-8788 (2001).
22. Eytan, D., Brenner, N., and Marom, S.: Selective adaptation in networks of cortical neurons. J. Neurosci., 23, 9349-9356 (2003).
23. Prasad, S., Yang, M., Zhang, X., Ozkan, C. S., and Ozkan, M.: Neurons as sensors: individual and cascaded chemical sensing. Biosens. Bioelectron., 19, 1599-1610 (2004).
24. Bucher, V., Graf, M., Stelzle, M., and Nisch, W.: Low impedance thin-film polycrystalline silicon microelectrodes for extracellular stimulation and recording. Biosens. Bioelectron., 14, 639-649 (1999).
25. Ziegler, C.: Cell-based biosensors. Fresenius J. Anal. Chem., 366, 552-559 (2000).
26. Gross, G. W. and Kowalski, J. M.: Origin of activity patterns in self-organizing neuronal networks in vitro. J. Intell. Mater. Syst. Struct., 10, 558-564 (2001).
27. Heuschkel, M., Guérin, L., Buisson, B., Bertrand, D., and Renaud, P.: Buried microchannels in photopolymer for delivering of solutions to neurons in a network. Sens. Actuators B, 48, 356-361 (1998).
28. Chang, J. C., Brewer, G. J., and Wheeler, B. C.: Microelectrode array recordings of patterned hippocampal neurons for four weeks. Biomed. Microdev., 2, 245-253 (2000).
29. James, C., Davis, R., Meyer, M., Turner, A., Turner, S., Withers, G., Kam, L., Banker, G., Craighead, H., Isaacson, M., Turner, J., and Shain, W.: Aligned microcontact printing of micrometer-scale poly-L-lysine for controlled growth of cultured neurons on planar microelectrode arrays. IEEE Trans. Biomed. Eng., 47, 17-21 (2000).
30. Chang, J., Brewer, G., and Wheeler, B.: Modulation of neural network activity by patterning. Biosens. Bioelectron., 16, 527-533 (2001).
31. James, C. D., Spence, A. J. H., Dowell-Mesfin, N. M., Rifat, J. H., Smith, K. L., Craighead, H. G., Isaacson, M. S., Shain, W., and Turner, J. N.: Extracellular recordings from patterned neuronal networks using planar microelectrode arrays. IEEE Trans. Biomed. Eng., 51, 1640-1648 (2004).
32. Nam, Y., Chang, J. C., Wheeler, B. C., and Brewer, G. J.: Gold-coated microelectrode array with thiol linked self-assembled monolayers for engineering neuronal cultures. IEEE Trans. Biomed. Eng., 51, 158-165 (2004).
33. Claverol-Tinture, E. and Pine, J.: Extracellular potentials in low-density dissociated neuronal cultures. J. Neurosci. Methods, 117, 13-21 (2002).
34. Bove, M., Grattarola, M., Tedesco, M., and Verreschi, G.: Characterization of growth and electrical activity of nerve cells cultured on microelectronic substrates: towards hybrid neuro-electronic devices. J. Mater. Sci. Mater. Med., 5, 684-687 (1994).
35. Breckenridge, L., Wilson, R., Connolly, P., Curtis, A., Dow, J., Blackshaw, S., and Wilkinson, C.: Advantages of using microfabricated extracellular electrodes for in vitro neuronal recording. J. Neurosci. Res., 42, 266-276 (1995).
36. Buitenweg, J., Rutten, W., Willems, W., and Nieuwkasteele, J. V.: Measurement of sealing resistance of cell-electrode interfaces in neuronal cultures using impedance spectroscopy. Med. Biol. Eng. Comput., 36, 630-637 (1998).
37. Buitenweg, J. R., Rutten, W. L., and Marani, E.: Modeled channel distributions explain extracellular recordings from cultured neurons sealed to microelectrodes. IEEE Trans. Biomed. Eng., 49, 1580-1590 (2002).
38. Martinoia, S., Massobrio, P., Bove, M., and Massobrio, G.: Cultured neurons coupled to microelectrode arrays: circuit models simulations and experimental data. IEEE Trans. Biomed. Eng., 51, 859-864 (2004).
39. Lind, R., Connolly, P., Wilkinson, C., and Thomson, R.: Finite-element analysis applied to extracellular microelectrode design. Sens. Actuators B, 3, 23-30 (1991).
40. Kovacs, G.: Introduction to the theory, design, and modeling of thin-film microelectrodes for neural interfaces, p. 121-165. In Stenger, D. and McKenna, T. (ed.), Enabling technologies for cultured neural networks. Academic Press, San Diego (1994).
41. Fromherz, P.: Neuroelectronic interfacing: semicondictor chips with ion channels, nerve cells and brain, p. 783-810. In Waser, R. (ed.), Nanoelectronics and information technology. Wiley-VCH, Weinheim (2003).
42. Gross, G. and Kowalski, J.: Experimental and theoretical analysis of random nerve cell networks dynamics, p. 47-110. In Antognetti, P. and Miltunovic, E. (ed.), Neural networks: concepts, applications and implementations. Prentice-Hall, NJ (1991).
43. Kamioka, H., Maeda, E., Jimbo, Y., Robinson, H., and Kawana, A.: Spontaneous periodic synchronized bursting during formation of mature patterns of connections in cortical cultures. Neurosci. Lett., 206, 109-112 (1996).
44. Maeda, E., Robinson, H. P., and Kawana, A.: The mechanisms of generation and propagation of synchronized bursting in developing networks of cortical neurons. J. Neurosci., 15, 6834-6845 (1995).
45. Nakanishi, K. and Kukita, F.: Functional synapses in synchronized bursting of neocortical neurons in culture. Brain Res., 795, 137-146 (1998).
46. Streit, J., Tscherter, A., Heuschkel, M. O., and Renaud, P.: The generation of rhythmic activity in dissociated cultures of rat spinal cord. Eur. J. Neurosci., 14, 191-202 (2001).
47. Robinson, H. P., Kawahara, M., Jimbo, Y., Torimitsu, K., Kuroda, Y., and Kawana, A.: Periodic synchronized bursting and intracellular calcium transients elicited by low magnesium in cultured cortical neurons. J. Neurophysiol., 70, 1606-1616 (1993).
48. van Pelt, J., Vajda, L., Wolters, P. S., Corner, M. A., and Ramakers, G. J.: Dynamics and plasticity in developing neuronal networks in vitro. Prog. Brain Res., 147, 173-188 (2005).
49. Darbon, P., Scicluna, L., Tscherter, A., and Streit, J.: Mechanisms controlling bursting activity induced by disinhibition in spinal cord networks. Eur. J. Neurosci., 15, 671-683 (2002).
50. Keefer, E. W., Gramowski, A., and Gross, G. W.: NMDA receptor-dependent periodic oscillations in cultured spinal cord networks. J. Neurophysiol., 86, 3030-3042 (2001).
51. Legrand, J.-C., Darbon, P., and Streit, J.: Contributions of NMDA receptors to network recruitment and rhythm generation in spinal cord cultures. Eur. J. Neurosci., 19, 521-532 (2004).
52. NaP underlies intrinsic spiking and rhythm generation in networks of cultured rat spinal cord neurons. Eur. J. Neurosci., 20, 976-988 (2004).
53. Ben-Ari, Y.: Developing networks play a similar melody. Trends Neurosci., 24, 353-360 (2001).
54. Canepari, M., Bove, M., Maeda, E., Capello, M., and Kawana, A.: Experimental analysis of neuronal dynamics in cultured cortical networks and transitions between different patterns of activity. Biol. Cybern., 77, 153-162 (1997).
55. Corner, M., van Pelt, J., Wolters, P., Baker, R., and Nuytinck, R.: Physiological effects of sustained blockade of excitatory synaptic transmission on spontaneously active developing neural networks: an inquiry into the reciprocal linkage between intrinsic biorhythms and neuroplasticity in early ontogeny. Neurosci. Biobehav. Rev., 26, 127-185 (2002).
56. Corner, M. A., Baker, R. E., van Pelt, J., and Wolters, P. S.: Compensatory physiological responses to chronic blockade of amino acid receptors during early development in spontaneously active organotypic cerebral cortex explants cultured in vitro. Prog. Brain Res., 147, 231-248 (2005).
57. Latham, P., Richmond, B., Niremberg, S., and Nelson, P.: Intrinsic dynamics in cortical neural networks. II. Experiment. J. Neurophysiol., 83, 828-835 (2000).
58. Wagenaar, D. A., Madhavan, R., Pine, J., and Potter, S. M.: Controlling bursting in cortical cultures with closed-loop multi-electrode stimulation. J. Neurosci., 25, 680-688 (2004).
59. Xia, Y., Gopal, K. V., and Gross, G. W.: Differential accute effects of fluoxetine on frontal and auditory cortex networks in vitro. Brain Res., 973, 151-160 (2003).
60. Martinoia, S., Sanguinetti, V., Cozzi, L., Berdondini, L., van Pelt, J., Tomas, J., Masson, G. L., and Davide, F.: Towards an embodied in vitro electrophysiology: the neurobit project. Neurocomputing, 58-60, 1065-1072 (2004).
61. Chiappalone, M., Novellino, A., Vajda, I., Vato, A., Martinoia, S., and van Pelt, J.: Burst detection algorithms for the analysis of spatio-temporal patterns in cortical networks of neurons. Neurocomputing, 65/66, 653-662 (2005).
62. Tateno, T., Kawana, A., and Jimbo, Y.: Analytical characterization of spontaneous firing in networks of developing rat cultured cortical neurons. Phys. Rev. E Stat. Nonlin. Soft. Mat. Phys., 65, 051924 (2002).
63. Beggs, J. M. and Plenz, D.: Neuronal avalanches in neocortical circuits. J. Neurosci., 23, 11167-11177 (2003).
64. Segev, R., Benveniste, M., Hulata, E., Cohen, N., Pavelski, A., Kapon, E., Shapira, Y., and Ben-Jacob, E.: Long term behavior of lithographically prepared in vitro neuronal networks. Phys. Rev. Lett., 88, 118102 (2002).
65. Segev, R., Baruchi, I., Hulata, E., and Ben-Jacob, E.: Hidden neuronal correlations in cultured networks. Phys. Rev. Lett., 92, 118102 (2004).
66. Selinger, J. V., Pancrazio, J. J., and Gross, G. W.: Measuring synchronization in neuronal networks for biosensor applications. Biosens. Bioelectron., 19, 675-683 (2004).
67. Baruchi, I. and Ben-Jacob, E.: Functional holography of recorded neuronal networks activity. Neuroinformatics, 2, 333-352 (2004).
68. Beggs, J. M. and Plenz, D.: Neuronal avalanches are diverse and precise activity patterns that are stable for many hours in cortical slice cultures. J. Neurosci., 24, 5216-5229 (2004).
69. Fellous, J.-M. and Sejnowski, T. J.: Regulation of persistent activity by background inhibition in an in vitro model of a cortical microcircuit. Cereb. Cortex, 13, 1232-1241 (2003).
70. Shu, Y., Hasentaub, A., and McCormick, D. A.: Turning on and off recurrent balanced cortical activity. Nature, 423, 288-293 (2003).
71. Gross, G., Rhoades, B., Azzazy, H., and Wu, M.-C.: The use of neuronal networks on multielectrode arrays as biosensors. Biosens. Bioelectron., 10, 553-567 (1995).
72. Gross, G., Harsch, A., Rhoades, B., and Göpel, W.: Odor, drug and toxin analysis with neuronal networks in vitro: extracellular array recording of network responses. Biosens. Bioelectron., 12, 373-393 (1997).
73. Morefield, S., Keefer, E., Chapman, K., and Gross, G.: Drug evaluations using neuronal networks cultured on microelectrode arrays. Biosens. Bioelectron., 15, 383-396 (2000).
74. Stenger, D. A., Gross, G. W., Keefer, E. W., Shaffer, K. M., Andreadis, J. D., Ma, W., and Pancrazio, J. J.: Detection of physiologically active compounds using cell-based biosensors. Trends Biotechnol., 19, 304-309 (2001).
75. Chiappalone, M., Vato, A., Tedesco, M. B., Marcoli, M., Davide, F., and Martinoia, S.: Networks of neurons coupled to microelectrode arrays: a neuronal sensory system for pharmacological applications. Biosens. Bioelectron., 18, 627-634 (2003).
76. Pancrazio, J. J., Gray, S. A., Shubin, Y. S., Kulagina, N., Cuttino, D. S., Shaffer, K. M., Eisemann, K., Curran, A., Zim, B., Gross, G. W., and O'Shaughnessy, T. J.: A portable microelectrode array recording system incorporating cultured neuronal networks for neurotoxin detection. Biosens. Bioelectron., 18, 1339-1347 (2003).
77. Prasad, S., Zhang, X., Ozkan, C. S., and Ozkan, M.: Neuron-based microarray sensors for environmental sensing. Electrophoresis, 25, 3746-3760 (2004).
78. Gramowski, A., Jügelt, K., Weiss, D., and Gross, G. W.: Substance identification by quantitative characterization of oscillatory activity in murine spinal cord networks on microelectrode arrays. Eur. J. Neurosci., 19, 2815-2825 (2004).
79. Suyama, K., Daikoku, S., Funabashi, T., and Kimura, F.: Effects of GABA and bicuculline on the electrical activity of rat olfactory placode neurons derived at E13.5 and cultured for one week on multi-electrode dishes. Endocr. J., 51, 171-176 (2004).
80. Harsch, A., Ziegler, C., and Göpel, W.: Strychnine analysis with neuronal networks in vitro: extracellular array recording of network responses. Biosens. Bioelectron., 12, 827-835 (1997).
81. Eytan, D., Minerbi, A., Ziv, N., and Marom, S.: Dopamine-induced depression of correlations between action potentials in networks of cortical neurons. J. Neurophysiol., 92, 1817-1824 (2004).
82. Arnold, F., Hofmann, F., Bengston, P., Wittmann, M., Vanhoutte, P., and Bading, H.: Microelectrode array recordings of cultured hippocampal networks reveal a simple model for transcription and protein synthesis-dependant plasticity. J. Physiol., 564, 3-19 (2004).
83. Keefer, E. W., Norton, S. J., Boyle, N. A., Talesa, V., and Gross, G. W.: Acute toxicity screening of novel AChE inhibitors using neuronal networks on microelectrode arrays. Neurotoxicology, 22, 3-12 (2001).
84. Keefer, E. E., Gramowski, A., Stenger, D. A., Pancrazio, J. J., and Gross, G. W.: Characterization of accute neurotoxic effects of trimethylolpropane phosphate on neuronal networks biosensors. Biosens. Bioelectron., 16, 513-525 (2001).
85. O'Shaughnessy, T., Zim, B., Ma, W., Shaffer, K., Stenger, D., Zamani, K., Gross, G., and Pancrazio, J.: Acute neuropharmacologic action of chloroquine on cortical neurons in vitro. Brain Res., 959, 280-286 (2003).
86. Xia, Y. and Gross, G. W.: Histiotypic electrophysiological responses of cultured neuronal networks to ethanol. Alcohol, 30, 167-174 (2003).
87. Krause, M. and Jia, Y.: Serotonergic modulation of carbachol-induced rhythmic activity in hippocampal slices. Neuropharmacology, 48, 381-390 (2005).
88. Shimono, K., Baudry, M., Panchenko, V., and Taketani, M.: Chronic multichannel recordings from organotypic hippocampal slice cultures: protection from excitotoxic effects of NMDA by non-competitive NMDA antagonists. J. Neurosci. Methods, 120, 193-202 (2002).
89. Gholmieh, G., Soussou, W., Courellis, S., Marmarelis, V., Berger, T., and Baudry, M.: A biosensor for detecting changes in cognitive processing based on nonlinear systems analysis. Biosens. Bioelectron., 16, 491-501 (2001).
90. Potter, S. M., Wagenaar, D. A., and DeMarse, T. B.: Closing the loop: stimulation feedback systems for embodied MEA cultures. In Taketani, M. and Baudry, M. (ed.), Advances in network electrophysiology: using multi-electrode arrays. Springer, Heidelberg (2006). (in press)
91. Wagenaar, D. A. and Potter, S. M.: Real-time multi-channel stimulus artifact suppression by local curve fitting. J. Neurosci. Methods, 120, 113-120 (2002).
92. Jimbo, Y., Kasai, N., Torimitsu, K., Tateno, T., and Robinson, H. P. C.: A system for MEA-based multisite stimulation. IEEE Trans. Biomed. Eng., 50, 241-248 (2003).
93. Wagenaar, D. A., Pine, J., and Potter, S. M.: Effective parameters for stimulation of dissociated cultures using multi-electrode arrays. J. Neurosci. Methods, 138, 27-37 (2004).
94. Jimbo, Y., Kawana, A., Parodi, P., and Torre, V.: The dynamics of a neuronal culture of dissociated cortical neurons of neonatal rats. Biol. Cybern., 83, 1-20 (2000).
95. Maeda, E., Kuroda, Y., Robinson, H. P., and Kawana, A.: The mechanisms of generation and propagation of synchronized bursting in developing networks of cortical neurons. Eur. J. Neurosci., 10, 488-496 (1998).
96. Wagenaar, D. A. and Potter, S. M.: A versatile all-channel stimulator for electrode arrays, with real-time control. J. Neural Eng., 1, 39-45 (2004).
97. Regehr, W., Pine, J., and Rutledge, D.: A long term in vitro silicon-based microelectrode-neuron connection. IEEE Trans. Biomed. Eng., 35, 1023-1032 (1988).
98. Sandison, M., Curtis, A., and Wilkinson, C.: Effective extra-cellular recording from vertebrate neurons in culture using a new type of micro-electrode array. J. Neurosci. Methods, 114, 63-71 (2002).
99. Maher, M. P., Pine, J., Wright, J., and Tai, Y.-C.: The neurochip: a new multielectrode device for stimulating and recording from cultured neurons. J. Neurosci. Methods, 87, 45-56 (1999).
100. Meng, E., Tai, Y.-C., Erickson, J., and Pine, J.: Parylene technology for mechanically robust neuro-cages, p. 1109-1112. In Northrup, M. A., Jensen, K. F., and Harrison, D. J. (ed.), Proceedings of MicroTAS 2003 - 7th international conference on miniaturized chemical and biochemical analysis systems. Transducers Research Foundation, Cleveland, OH (2003).
101. Suzuki, I., Sugio, Y., Moriguchi, H., Hattori, A., Yasuda, K., and Jimbo, Y.: Pattern modification of a neuronal network for individual cell-based electrophysiological measurement using photothermal etching of an agarose architecture with a multielectrode array. IEEE Proc. Nanobiotechnol., 151, 116-121 (2004).
102. Heuschkel, M., Fejtl, M., Raggenbass, M., Bertrand, D., and Renaud, P.: A three-dimensional multi-electrode array for multi-site stimulation and recording in acute brain slices. J. Neurosci. Methods, 114, 135-148 (2002).
103. Thiebaud, P., Lauer, L., Knoll, W., and Offenhäuser, A.: PDMS device for patterned application of microfluids to neuronal cells arranged by microcontact printing. Biosens. Bioelectron., 17, 87-93 (2002).
104. Pearce, T. M., Wilson, J. A., Oakes, S. G., Chiub, S.-Y., and Williams, J. C.: Integrated microelectrode array and microfluidics for temperature clamp of sensory neurons in culture. Lab. Chip, 5, 97-101 (2005).
105. Bucher, V., Brunner, B., Leibrock, C., Schubert, M., and Nisch, W.: Electrical properties of a light-addressable microelectrode chip with high electrode density for extracellular stimulation and recording of excitable cells. Biosens. Bioelectron., 16, 205-210 (2001).
106. Colicos, M., Collins, B., Sailor, M., and Goda, Y.: Remodeling of synaptic actin induced by photoconductive stimulation. Cell, 107, 605-616 (2001).
107. Heer, F., Franks, W., Blau, A., Taschini, S., Ziegler, C., Hierlemann, A., and Baltes, H.: CMOS microelectrode array for the monitoring of electrogenic cells. Biosens. Bioelectron., 20, 358-366 (2004).
108. Campenot, R.: NGF and the local control of nerve terminal growth. J. Neurobiol., 25, 599-611 (1994).
109. Taylor, A. M., Rhee, S. W., Tu, C. H., Cribbs, D. H., Cotman, C. W., and Jeon, N. L.: Microfluidic multicompartment device for neuroscience research. Langmuir, 19, 1551-1556 (2003).
110. Degenaar, P., Pioufle, B. L., Griscom, L., Tixier, A., Akagi, Y., Morita, Y., Murakami, Y., Yokoyama, K., Fujita, H., and Tamiya, E.: A method for micrometer resolution patterning of primary culture neurons for SPM analysis. J. Biochem., 130, 367-376 (2001).
111. Gross, G. and Schwalm, F.: A closed flow chamber for long-term multichannel recording and optical monitoring. J. Neurosci. Methods, 52, 73-85 (1994).
112. Blau, A. W. and Ziegler, C.: Prototype of a novel autonomous perfusion chamber for long-term culturing and in situ investigation of various cell types. J. Biochem. Biophys. Methods, 50, 15-27 (2000).
113. Mukai, Y., Shiina, T., and Jimbo, Y.: Continuous monitoring of developmental activity changes in cultured cortical networks. Elec. Eng. J., 145, 28-37 (2003).
114. van Pelt, J., Wolters, P. S., Corner, M. A., Rutten, W. L., and Ramakers, G. J.: Long-term characterization of firing dynamics of spontaneous bursts in cultured neural networks. IEEE Trans. Biomed. Eng., 51, 2051-2062 (2004).
115. Potter, S. M. and DeMarse, T. B.: A new approach to neural cell culture for long-term studies. J. Neurosci. Methods, 110, 17-24 (2001).
116. Brischwein, M., Motrescu, E., Cabala, E., Otto, A., Grothe, H., and Wolf, B.: Functional cellular assays with multiparametric silicon sensor chips. Lab Chip, 3, 234-240 (2003).
117. van Bergen, A., Papanikolaou, T., Schuker, A., Möller, A., and Schlosshauer, B.: Long-term stimulation of mouse hippocampal slice culture on microelectrode array. Brain Res. Protoc., 11, 123-133 (2003).