Neuronal network morphology and electrophysiologyof hippocampal neurons cultured on surface-treated multielectrode arrays

IEEE Transactions on Biomedical Engineering

Volumn 54, Issue 7, 2007, Pages 1309-1320

  Soussou, Walid V ^a   Yoon, Geoffrey J ^b   Brinton, Roberta Diaz ^a   Berger, Theodore W ^c  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b NONE   (United States)

^c NONE   (United States)

Author keywords

Basement membrane; Multielectrode array; Neuronal network morphology; Spontaneous electrophysiological activity

Indexed keywords

BIOCHEMISTRY; BIOCOMPATIBILITY; ELECTROPHYSIOLOGY; IMAGE ANALYSIS; MEMBRANES; NEURONS; SURFACE MORPHOLOGY;

BASEMENT MEMBRANE; ELECTRODE ARRAYS; MULTIELECTRODE ARRAY; SPONTANEOUS ELECTROPHYSIOLOGICAL ACTIVITY;

NEURAL NETWORKS;

POLY DEXTRO LYSINE; POLYETHYLENEIMINE; POLYORNITHINE;

ARTICLE; BASEMENT MEMBRANE; CLUSTER ANALYSIS; CORRELATION ANALYSIS; DENDRITE; ELECTRODE; ELECTROPHYSIOLOGY; HIPPOCAMPUS; HUMAN; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; NERVE CELL; NERVE CELL CULTURE; NERVE CELL NETWORK; NERVE FIBER;

ACTION POTENTIALS; ANIMALS; CELL ADHESION; CELL CULTURE TECHNIQUES; CELLS, CULTURED; ELECTROPHYSIOLOGY; EQUIPMENT DESIGN; EQUIPMENT FAILURE ANALYSIS; FEMALE; HIPPOCAMPUS; MICROELECTRODES; NERVE NET; NEURONS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 34250716330     PISSN: 00189294     EISSN: None     Source Type: Journal    
DOI: 10.1109/TBME.2006.889195     Document Type: Article

References (55)

1. W. L. Rutten, J. P. Smit, T. A. Frieswijk, J. A. Bielen, A. L. Brouwer, J. R. Buitenweg, and C. Heida, "Neuro-electronic interfacing with multielectrode arrays," IEEE Eng. Med. Biol. Mag., vol. 18, no. 3, pp. 47-55, May-Jun. 1999.
2. T. W. Berger, M. Baudry, R. D. Brinton, J. S. Liaw, V. Z. Marmarelis, A. Y. Park, B. J. Sheu, and A. R. J. Tanguay, "Brain-Implantable biomimetic electronics as the next era in neural prosthetics," Proc IEEE, vol. 89, pp. 993-1012, 2001.
3. G. W. Gross, B. K. Rhoades, H. M. Azzazy, and M. C. Wu, "The use of neuronal networks on multielectrode arrays as biosensors," Biosens. Bioelectron., vol. 10, pp. 553-567, 1995.
4. D. A. Stenger, J. J. Hickman, K. E. Bateman, M. S. Ravenscroft, W. Ma, J. J. Pancrazio, K. Shaffer, A. E. Schaffner, D. H. Cribbs, and C. W. Cotman, "Microlithographic determination of axonal/dendritic polarity in cultured hippocampal neurons," J. Neurosci. Meth., vol. 82, pp. 167-173, 1998.
5. M. P. Maher, J. Pine, J. Wright, and Y. C. Tai, "The neurochip: A new multielectrode device for stimulating and recording from cultured neurons," J. Neurosci. Meth., vol. 87, pp. 45-56, 1999.
6. S. A. Deadwyler, T. Bunn, and R. E. Hampson, "Hippocampal ensemble activity during spatial delayed-nonmatch-to-sample performance in rats," J. Neurosci., vol. 16, pp. 354-372, 1996.
7. J. C. Williams, R. L. Rennaker, and D. R. Kipke, "Long-term neural recording characteristics of wire microelectrode arrays implanted in cerebral cortex," Brain Res. Brain Res. Protoc., vol. 4, pp. 303-313, 1999.
8. J. F. Hetke, J. L. Lund, K. Najafi, K. D.Wise, and D. J. Anderson, "Silicon ribbon cables for chronically implantable microelectrode arrays," IEEE Trans. Biomed. Eng., vol. 41, no. 4, pp. 314-321, Apr. 1994.
9. C. T. Nordhausen, P. J. Rousche, and R. A. Normann, "Optimizing recording capabilities of the utah intracortical electrode array," Brain Res., vol. 637, pp. 27-36, 1994.
10. A. Bragin, J. Hetke, C. L. Wilson, D. J. Anderson, J. Engel, Jr, and G. Buzsaki, "Multiple site silicon-based probes for chronic recordings in freely moving rats: Implantation, recording and histological verification," J. Neurosci. Meth., vol. 98, pp. 77-82, 2000.
11. J. J. Burmeister, K. Moxon, and G. A. Gerhardt, "Ceramic-based multisite microelectrodes for electrochemical recordings," Analytical Chem., vol. 72, pp. 187-192, 2000.
12. J. Pine, "Recording action potentials from cultured neurons with extracellular microcircuit electrodes," J. Neurosci. Meth., vol. 2, pp. 19-31, 1980.
13. G. W. Gross, A. N. Williams, and J. H. Lucas, "Recording of spontaneous activity with photoetched microelectrode surfaces from mouse spinal neurons in culture," J. Neurosci. Meth., vol. 5, pp. 13-22, 1982.
14. U. Egert, B. Schlosshauer, S. Fennrich, W. Nisch, M. Fejtl, T. Knott, T. Müller, and H. Hämmerle, "A novel organotypic long-term culture of the rat hippocampus on substrate-integrated multielectrode arrays," Brain Res. Brain Res. Protoc., vol. 2, pp. 229-242, 1998.
15. H. Oka, K. Shimono, R. Ogawa, H. Sugihara, and M. Taketani, "A new planar multielectrode array for extracellular recording: Application to hippocampal acute slice," J. Neurosci. Meth., vol. 93, pp. 61-67, 1999.
16. J. C. Chang, G. J. Brewer, and B. C. Wheeler, "Modulation of neural network activity by patterning," Biosens. Bioelectron., vol. 16, pp. 527-33, 2001.
17. Y. Jimbo, N. Kasai, K. Torimitsu, T. Tateno, and H. P. Robinson, "A system for MEA-based multisite stimulation," IEEE Trans. Biomed. Eng., vol. 50, no. 2, pp. 241-248, Feb. 2003.
18. F. O. Morin, Y. Takamura, and E. Tamiya, "Investigating neuronal activity with planar microelectrode arrays: Achievements and new perspectives," J. Biosci. Bioeng., vol. 100, pp. 131-143, 2005.
19. L. Kam, W. Shain, J. N. Turner, and R. Bizios, "Correlation of astroglial cell function on micro-patterned surfaces with specific geometric parameters," Biomaterials, vol. 20, pp. 2343-2350, 1999.
20. L. Kam, W. Shain, J. N. Turner, and R. Bizios, "Selective adhesion of astrocytes to surfaces modified with immobilized peptides," Biomaterials, vol. 23, pp. 511-315, 2002.
21. W. Shain, L. Spataro, J. Dilgen, K. Haverstick, S. Retterer, M. Isaacson, M. Saltzman, and J. N. Turner, "Controlling cellular reactive responses around neural prosthetic devices using peripheral and local intervention strategies," IEEE Trans. Neural Syst. Rehabil. Eng., vol. 11, no. 2, pp. 186-188, Jun. 2003.
22. D. Kleinfeld, K. H. Kahler, and P. E. Hockberger, "Controlled outgrowth of dissociated neurons on patterned substrates," J. Neurosci., vol. 8, pp. 4098-4120, 1988.
23. C. D. James, R. Davis, M. Meyer, A. Turner, S. Turner, G. Withers, L. Kam, G. Banker, H. Craighead, M. Isaacson, J. Turner, and W. Shain, "Aligned microcontact printing of micrometer-scale poly-L-lysine structures for controlled growth of cultured neurons on planar microelectrode arrays," IEEE Trans. Biomed. Eng., vol. 47, no. 1, pp. 17-21, Jan. 2000.
24. E. Yavin and Z. Yavin, "Attachment and culture of dissociated cells from rat embryo cerebral hemispheres on polylysine-coated surface," J. Cell. Biol., vol. 62, pp. 540-546, 1974.
25. P. C. Letourneau, "Possible roles for cell-to-substratum adhesion in neuronal morphogenesis," Dev. Biol., vol. 44, pp. 77-91, 1975.
26. W. L. McKeehan and R. G. Ham, "Stimulation of clonal growth of normal fibroblasts with substrata coated with basic polymers," J. Cell. Biol., vol. 71, pp. 727-734, 1976.
27. H. K. Kleinman, M. L. McGarvey, J. R. Hassell, V. L. Star, F. B. Cannon, G. W. Laurie, and G. R. Martin, "Basement membrane complexes with biological activity," Biochemistry, vol. 25, pp. 312-8, 1986.
28. J. R. Sanes, "Extracellular matrix molecules that influence neural development," Annu. Rev. Neurosci., vol. 12, pp. 491-516, 1989.
29. I. H. Lelong, V. Petegnief, and G. Rebel, "Neuronal cells mature faster on polyethyleneimine coated plates than on polylysine coated plates," J. Neurosci. Res., vol. 32, pp. 562-8, 1992.
30. M. Matsuzawa, F. F. Weight, R. S. Potember, and P. Liesi, "Directional neurite outgrowth and axonal differentiation of embryonic hippocampal neurons are promoted by a neurite outgrowth domain of the B2-chain of laminin," Int. J. Dev. Neurosci., vol. 14, pp. 283-295, 1996.
31. A. Goldberger, P. Flaherty, R. Villalba, L. A. Riblet, and A. Cornell-Bell, Extracellular matrix proteins influence cell morphology and function in rat neural cultures, Becton Dickinson Labware, Tech. Bull. 1997.
32. M. J. Ignatius, N. Sawhney, A. Gupta, B. M. Thibadeau, O. R. Monteiro, and I. G. Brown, "Bioactive surface coatings for nanoscale instruments: Effects on cns neurons," J. Biomed. Mater. Res., vol. 40, pp. 264-274, 1998.
33. T. Esch, V. Lemmon, and G. Banker, "Local presentation of substrate molecules directs axon specification by cultured hippocampal neurons," J. Neurosci., vol. 19, pp. 6417-6426, 1999.
34. A. Dityatev and M. Schachner, "Extracellular matrix molecules and synaptic plasticity," Nat. Rev. Neurosci., vol. 4, pp. 456-468, 2003.
35. Y. Jimbo, H. P. Robinson, and A. Kawana, "Simultaneous measurement of intracellular calcium and electrical activity from patterned neural networks in culture," IEEE Trans. Biomed. Eng., vol. 40, no. 8, pp. 804-810, Aug. 1993.
36. R. O.Wong, "Calcium imaging and multielectrode recordings of global patterns of activity in the developing nervous system," Histochem. J., vol. 30, pp. 217-229, 1998.
37. T. Tateno, Y. Jimbo, and H. P. Robinson, "Spatio-temporal cholinergic modulation in cultured networks of rat cortical neurons: Spontaneous activity," Neuroscience, vol. 134, pp. 425-437, 2005.
38. M. H. Droge, G. W. Gross, M. H. Hightower, and L. E. Czisny, "Multielectrode analysis of coordinated, multisite, rhythmic bursting in cultured cns monolayer networks," J. Neurosci., vol. 6, pp. 1583-1592, 1986.
39. H. Kamioka, E. Maeda, Y. Jimbo, H. P. Robinson, and A. Kawana, "Spontaneous periodic synchronized bursting during formation of mature patterns of connections in cortical cultures," Neurosci. Lett., vol. 206, pp. 109-112, 1996.
40. R. M. Fitzsimonds, H. J. Song, and M. M. Poo, "Propagation of activity-dependent synaptic depression in simple neural networks," Nature, vol. 388, pp. 439-448, 1997.
41. G. Banker and K. Goslin, Culturing Nerve Cells, 2nd ed. Cambridge, MA: MIT Press, 1999.
42. C. R. Legendy and M. Salcman, "Bursts and recurrences of bursts in the spike trains of spontaneously active striate cortex neurons," J. Neurophysiol., vol. 53, pp. 926-939, 1985.
43. G. Gholmieh, W. Soussou, S. Courellis, V. Z. Marmarelis, T. W. Berger, and M. Baudry, "A biosensor for detecting changes in cognitive processing based on nonlinear systems analysis," Biosens. Bioelectron., vol. 16, pp. 491-501, 2001.
44. P. S. Motta and J. W. Judy, "Multielectrode microprobes for deep-brain stimulation fabricated with a customizable 3-D electroplating process," IEEE Trans. Biomed. Eng., vol. 52, no. 5, pp. 923-933, May 2005.
45. R. D. Brinton, W. Soussou, M. Baudry, M. Thompson, and T. W. Berger, "The biotic/abiotic interface: Achievements and foreseeable challenges," in Towards Replacement Parts for the Brain: Implantable Biomimetic Electronics as Neural Prostheses, T. W. Berger and D. L. Glanzman, Eds. Cambridge, MA: MIT Press, 2005.
46. D. W. Branch, B. C. Wheeler, G. J. Brewer, and D. E. Leckband, "Long-term maintenance of patterns of hippocampal pyramidal cells on substrates of polyethylene glycol and microstamped polylysine," IEEE Trans. Biomed. Eng., vol. 47, no. 3, pp. 290-300, Mar. 2000.
47. R. Milner and I. L. Campbell, "The integrin family of cell adhesion molecules has multiple functions within the cns," Neurosci. Res., vol. 69, pp. 286-291, 2002.
48. P. E. Latham, B. J. Richmond, P. G. Nelson, and S. Nirenberg, "Intrinsic dynamics in neuronal networks. I. Theory," J. Neurophysiol., vol. 83, pp. 808-827, 2000.
49. P. E. Latham, B. J. Richmond, S. Nirenberg, and P. G. Nelson, "Intrinsic dynamics in neuronal networks. II. Experiment," J. Neurophysiol., vol. 83, pp. 828-835, 2000.
50. E. Claverol-Tinture and J. Pine, "Extracellular potentials in low-density dissociated neuronal cultures," J. Neurosci. Meth., vol. 117, pp. 13-21, 2002.
51. Q. Liu, M. Coulombe, J. Dumm, K. M. Shaffer, A. E. Schaffner, J. L. Barker, J. J. Pancrazio, D. A. Stenger, and W. Ma, "Synaptic connectivity in hippocampal neuronal networks cultured on micropatterned surfaces," Brain Res. Dev. Brain Res., vol. 120, pp. 223-231, 2000.
52. W. Ma, Q. Y. Liu, D. Jung, P. Manos, J. J. Pancrazio, A. E. Schaffner, J. L. Barker, and D. A. Stenger, "Central neuronal synapse formation on micropatterned surfaces," Brain. Res. Dev. Brain Res., vol. 111, pp. 231-243, 1998.
53. M. Canepari, M. Bove, E. Maeda, M. Cappello, and A. Kawana, "Experimental analysis of neuronal dynamics in cultured cortical networks and transitions between different patterns of activity," Biol. Cybern., vol. 77, pp. 153-162, 1997.
54. M. Matsuzawa, T. Tabata, W. Knoll, and M. Kano, "Formation of hippocampal synapses on patterned substrates of a laminin- derived synthetic peptide," Eur. J. Neurosci., vol. 12, pp. 903-910, 2000.
55. P. R. Kennedy and R. A. Bakay, "Restoration of neural output from a paralyzed patient by a direct brain connection," Neuroreport, vol. 9, pp. 1707-1711, 1998.