Abstract
Fabrication of in vitro culture microenvironments that replicate the structure and functionality of the in vivo nervous system has been a long-standing scientific goal. Investigators need tools that allow them explicit control over a variety of neuronal culture parameters as they seek a fuller understanding of basic neuroscience principles, make advances in tissue engineering and medical devices, and improve high throughput screening platforms. This chapter reviews techniques that have been implemented to influence the soma placement, axonal elongation, and network formation of neuronal cultures in vitro. Methods such as topography, printing procedures, photolithography, microfluidics, subtractive fabrication, optical cues, and magnetic and electric fields are discussed. A comparison of manipulatable variables across methods is included, highlighting the benefits and limitations of each approach and lending guidance on technique selection for future experiments.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adams, D.N., E.Y. Kao, C.L. Hypolite, M.D. Distefano, W.S. Hu, and P.C. Letourneau. 2005. Growth Cones Turn and Migrate up an Immobilized Gradient of the Laminin IKVAV peptide. Journal of Neurobiology 62: 134–147.
Alexander, J.K., B. Fuss, and R.J. Colello. 2006. Electric Field-Induced Astrocyte Alignment Directs Neurite Outgrowth. Neuron Glia Biology 2: 93–103.
Astashkina, A., and D.W. Grainger. 2014. Critical Analysis of 3-D Organoid In Vitro Cell Culture Models for High-Throughput Drug Candidate Toxicity Assessments. Advanced Drug Delivery Reviews 69–70: 1–18.
Belisle, J.M., J.P. Correia, P.W. Wiseman, T.E. Kennedy, and S. Costantino. 2008. Patterning Protein Concentration Using Laser-Assisted Adsorption by Photobleaching, LAPAP. Lab on a Chip 8: 2164–2167.
Belisle, J.M., D. Kunik, and S. Costantino. 2009. Rapid Multicomponent Optical Protein Patterning. Lab on a Chip 9: 3580–3585.
Belisle, J.M., L.A. Levin, and S. Costantino. 2012. High-Content Neurite Development Study Using Optically Patterned Substrates. PLoS One 7: e35911.
Belisle, J.M., J. Mazzaferri, and S. Costantino. 2014. Laser-Assisted Adsorption by Photobleaching. Methods in Cell Biology 119: 125–140.
Belkaid, W., P. Thostrup, P.T. Yam, C.A. Juzwik, E.S. Ruthazer, A.S. Dhaunchak, and D.R. Colman. 2013. Cellular Response to Micropatterned Growth Promoting and Inhibitory Substrates. BMC Biotechnology 13: 86.
Berkovitch, Y., D. Yelin, and D. Seliktar. 2015. Photo-Patterning PEG-Based Hydrogels for Neuronal Engineering. European Polymer Journal 72: 473–483.
Bhattacharjee, N., N. Li, T.M. Keenan, and A. Folch. 2010. A Neuron-Benign Microfluidic Gradient Generator for Studying the Response of Mammalian Neurons Towards Axon Guidance Factors. Integrative Biology (Cambridge) 2: 669–679.
Black, B., A. Mondal, Y. Kim, and S.K. Mohanty. 2013. Neuronal Beacon. Optics Letters 38: 2174–2176.
Black, B.J., L. Gu, and S.K. Mohanty. 2014. Highly Effective Photonic Cue for Repulsive Axonal Guidance. PLoS One 9: e86292.
Bohanon, T., G. Elender, W. Knoll, P. Koberle, J.S. Lee, A. Offenhausser, H. Ringsdorf, E. Sackmann, J. Simon, G. Tovar, and F.M. Winnik. 1996. Neural Cell Pattern Formation on Glass and Oxidized Silicon Surfaces Modified with Poly(N-Isopropylacrylamide). Journal of Biomaterials Science Polymer Edition 8: 19–39.
Branch, D.W., J.M. Corey, J.A. Weyhenmeyer, G.J. Brewer, and B.C. Wheeler. 1998. Microstamp Patterns of Biomolecules for High-Resolution Neuronal Networks. Medical and Biological Engineering and Computing 36: 135–141.
Branch, D.W., B.C. Wheeler, G.J. Brewer, and D.E. Leckband. 2000. Long-Term Maintenance of Patterns of Hippocampal Pyramidal Cells on Substrates of Polyethylene Glycol and Microstamped Polylysine. IEEE Transactions on Biomedical Engineering 47: 290–300.
Britland, S., and C. Mccaig. 1996. Embryonic Xenopus Neurites Integrate and Respond to Simultaneous Electrical and Adhesive Guidance Cues. Experimental Cell Research 226: 31–38.
Britland, S., C. Perridge, M. Denyer, H. Morgan, A. Curtis, and C. Wilkinson. 1996. Morphogenetic Guidance Cues Can Interact Synergistically and Hierarchically in Steering Nerve Cell Growth. Experimental Biology Online 1: 1–15.
Bruder, J.M., A.P. Lee, and D. Hoffman-Kim. 2007. Biomimetic Materials Replicating Schwann Cell Topography Enhance Neuronal Adhesion and Neurite Alignment In Vitro. Journal of Biomaterials Science Polymer Edition 18: 967–982.
Carnegie, D.J., T. Cizmar, J. Baumgartl, F.J. Gunn-Moore, and K. Dholakia. 2009. Automated Laser Guidance of Neuronal Growth Cones Using a Spatial Light Modulator. Journal of Biophotonics 2: 682–692.
Catig, G.C., S. Figueroa, and M.J. Moore. 2015. Experimental and Computational Models of Neurite Extension at a Choice Point in Response to Controlled Diffusive Gradients. Journal of Neural Engineering 12: 046012.
Chang, J.C., G.J. Brewer, and B.C. Wheeler. 2003. A Modified Microstamping Technique Enhances Polylysine Transfer and Neuronal Cell Patterning. Biomaterials 24: 2863–2870.
Cheng, J., G. Zhu, L. Wu, X. Du, H. Zhang, B. Wolfrum, Q. Jin, J. Zhao, A. Offenhausser, and Y. Xu. 2013. Photopatterning of Self-Assembled Poly(Ethylene) Glycol Monolayer for Neuronal Network Fabrication. Journal of Neuroscience Methods 213: 196–203.
Chien, H.W., and W.B. Tsai. 2012. Fabrication of Tunable Micropatterned Substrates for Cell Patterning Via Microcontact Printing of Polydopamine with Poly(Ethylene Imine)-Grafted Copolymers. Acta Biomaterialia 8: 3678–3686.
Choi, J.H., H. Lee, H.K. Jin, J.S. Bae, and G.M. Kim. 2013. Fabrication of Microengineered Templates and Their Applications into Micropatterned Cell Culture. Journal of Biomedical Nanotechnology 9: 377–381.
Clark, P., P. Connolly, A.S. Curtis, J.A. Dow, and C.D. Wilkinson. 1990. Topographical Control of Cell Behaviour: II. Multiple Grooved Substrata. Development 108: 635–644.
Corey, J.M., B.C. Wheeler, and G.J. Brewer. 1991. Compliance of Hippocampal Neurons to Patterned Substrate Networks. Journal of Neuroscience Research 30: 300–307.
Corey, J.M., B.C. Wheeler, and G.J. Brewer. 1996. Micrometer Resolution Silane-Based Patterning of Hippocampal Neurons: Critical Variables in Photoresist and Laser Ablation Processes for Substrate Fabrication. IEEE Transactions on Biomedical Engineering 43: 944–955.
Cormie, P., and K.R. Robinson. 2007. Embryonic Zebrafish Neuronal Growth Is Not Affected by an Applied Electric Field In Vitro. Neuroscience Letters 411: 128–132.
Curley, J.L., and M.J. Moore. 2011. Facile Micropatterning of Dual Hydrogel Systems for 3D Models of Neurite Outgrowth. Journal of Biomedical Materials Research. Part A 99: 532–543.
Curley, J.L., S.R. Jennings, and M.J. Moore. 2011. Fabrication of Micropatterned Hydrogels for Neural Culture Systems Using Dynamic Mask Projection Photolithography. Journal of Visualized Experiments 48: 2636.
Curley, J.L., G.C. Catig, E.L. Horn-Ranney, and M.J. Moore. 2014. Sensory Axon Guidance with Semaphorin 6a and Nerve Growth Factor in a Biomimetic Choice Point Model. Biofabrication 6: 035026.
Curley, J.L., S.C. Sklare, D.A. Bowser, J. Saksena, M.J. Moore, and D.B. Chrisey. 2016. Isolated node engineering of neuronal systems using laser direct write. Biofabrication, 8: 015013.
Degenaar, P., B.L. Pioufle, L. Griscom, A. Tixier, Y. Akagi, Y. Morita, Y. Murakami, K. Yokoyama, H. Fujita, and E. Tamiya. 2001. A Method for Micrometer Resolution Patterning of Primary Culture Neurons for SPM Analysis. Journal of Biochemistry 130: 367–376.
Dent, E.W., S.L. Gupton, and F.B. Gertler. 2011. The Growth Cone Cytoskeleton in Axon Outgrowth and Guidance. Cold Spring Harbor Perspectives in Biology 3.
Dertinger, S.K., X. Jiang, Z. Li, V.N. Murthy, and G.M. Whitesides. 2002. Gradients of Substrate-Bound Laminin Orient Axonal Specification of Neurons. Proceedings of the National Academy of Sciences of the United States of America 99: 12542–12547.
Doraiswamy, A., R.J. Narayan, T. Lippert, L. Urech, A. Wokaun, M. Nagel, B. Hopp, M. Dinescu, R. Modi, R.C.Y. Auyeung, and D.B. Chrisey. 2006. Excimer Laser Forward Transfer of Mammalian Cells Using a Novel Triazene Absorbing Layer. Applied Surface Science 252: 4743–4747.
Dowell-Mesfin, N.M., M.A. Abdul-Karim, A.M. Turner, S. Schanz, H.G. Craighead, B. Roysam, J.N. Turner, and W. Shain. 2004. Topographically Modified Surfaces Affect Orientation and Growth of Hippocampal Neurons. Journal of Neural Engineering 1: 78–90.
Dubey, N., P.C. Letourneau, and R.T. Tranquillo. 1999. Guided Neurite Elongation and Schwann Cell Invasion into Magnetically Aligned Collagen in Simulated Peripheral Nerve Regeneration. Experimental Neurology 158: 338–350.
Dubey, N., P.C. Letourneau, and R.T. Tranquillo. 2001. Neuronal Contact Guidance in Magnetically Aligned Fibrin Gels: Effect of Variation in Gel Mechano-Structural Properties. Biomaterials 22: 1065–1075.
Ehrlicher, A., T. Betz, B. Stuhrmann, D. Koch, V. Milner, M.G. Raizen, and J. Kas. 2002. Guiding Neuronal Growth with Light. Proceedings of the National Academy of Sciences of the United States of America 99: 16024–16028.
Ehrlicher, A., T. Betz, B. Stuhrmann, M. Gogler, D. Koch, K. Franze, Y. Lu, and J. Kas. 2007. Optical Neuronal Guidance. Methods in Cell Biology 83: 495–520.
Erskine, L., and C.D. Mccaig. 1997. Integrated Interactions Between Chondroitin Sulphate Proteoglycans and Weak DC Electric Fields Regulate Nerve Growth Cone Guidance In Vitro. Journal of Cell Science 110(Pt 16): 1957–1965.
Esch, T., V. Lemmon, and G. Banker. 1999. Local Presentation of Substrate Molecules Directs Axon Specification by Cultured Hippocampal Neurons. Journal of Neuroscience 19: 6417–6426.
Fan, Y.W., F.Z. Cui, L.N. Chen, Y. Zhai, Q.Y. Xu, and I.S. Lee. 2002a. Adhesion of Neural Cells on Silicon Wafer with Nano-Topographic Surface. Applied Surface Science 187: 313–318.
Fan, Y.W., F.Z. Cui, S.P. Hou, Q.Y. Xu, L.N. Chen, and I.S. Lee. 2002b. Culture of Neural Cells on Silicon Wafers with Nano-Scale Surface Topograph. Journal of Neuroscience Methods 120: 17–23.
Fan, Y., F. Xu, G. Huang, T.J. Lu, and W. Xing. 2012. Single Neuron Capture and Axonal Development in Three-Dimensional Microscale Hydrogels. Lab on a Chip 12: 4724–4731.
Fereol, S., R. Fodil, M. Barnat, V. Georget, U. Milbreta, and F. Nothias. 2011. Micropatterned ECM Substrates Reveal Complementary Contribution of Low and High Affinity Ligands to Neurite Outgrowth. Cytoskeleton (Hoboken, NJ) 68: 373–388.
Francisco, H., B.B. Yellen, D.S. Halverson, G. Friedman, and G. Gallo. 2007. Regulation of Axon Guidance and Extension by Three-Dimensional Constraints. Biomaterials 28: 3398–3407.
Fricke, R., P.D. Zentis, L.T. Rajappa, B. Hofmann, M. Banzet, A. Offenhausser, and S.H. Meffert. 2011. Axon Guidance of Rat Cortical Neurons by Microcontact Printed Gradients. Biomaterials 32: 2070–2076.
Fritz, M., and M. Bastmeyer. 2013. Microcontact Printing of Substrate-Bound Protein Patterns for Cell and Tissue Culture. Methods in Molecular Biology 1018: 247–259.
Gill, A.A., I. Ortega, S. Kelly, and F. Claeyssens. 2015. Towards the Fabrication of Artificial 3d Microdevices for Neural Cell Networks. Biomedical Microdevices 17: 27.
Goldner, J.S., J.M. Bruder, G. Li, D. Gazzola, and D. Hoffman-Kim. 2006. Neurite Bridging Across Micropatterned Grooves. Biomaterials 27: 460–472.
Gomez, N., J.Y. Lee, J.D. Nickels, and C.E. Schmidt. 2007a. Micropatterned Polypyrrole: A Combination of Electrical and Topographical Characteristics for the Stimulation of Cells. Advanced Functional Materials 17: 1645–1653.
Gomez, N., Y. Lu, S. Chen, and C.E. Schmidt. 2007b. Immobilized Nerve Growth Factor and Microtopography Have Distinct Effects on Polarization Versus Axon Elongation in Hippocampal Cells in Culture. Biomaterials 28: 271–284.
Graves, C.E., R.G. Mcallister, W.J. Rosoff, and J.S. Urbach. 2009. Optical Neuronal Guidance in Three-Dimensional Matrices. Journal of Neuroscience Methods 179: 278–283.
Graves, M.S., T. Hassell, B.L. Beier, G.O. Albors, and P.P. Irazoqui. 2011. Electrically Mediated Neuronal Guidance with Applied Alternating Current Electric Fields. Annals of Biomedical Engineering 39: 1759–1767.
Gu, L., B. Black, S. Ordonez, A. Mondal, A. Jain, and S. Mohanty. 2014. Microfluidic Control of Axonal Guidance. Scientific Reports 4: 6457.
Gurkan, U.A., Y. Fan, F. Xu, B. Erkmen, E.S. Urkac, G. Parlakgul, J. Bernstein, W. Xing, E.S. Boyden, and U. Demirci. 2013. Simple Precision Creation of Digitally Specified, Spatially Heterogeneous, Engineered Tissue Architectures. Advanced Materials 25: 1192–1198.
Hammarback, J.A., S.L. Palm, L.T. Furcht, and P.C. Letourneau. 1985. Guidance of Neurite Outgrowth by Pathways of Substratum-Adsorbed Laminin. Journal of Neuroscience Research 13: 213–220.
Hammarback, J.A., J.B. Mccarthy, S.L. Palm, L.T. Furcht, and P.C. Letourneau. 1988. Growth Cone Guidance by Substrate-Bound Laminin Pathways Is Correlated with Neuron-to-Pathway Adhesivity. Developmental Biology 126: 29–39.
Hattori, A., H. Moriguchi, S.I. Ishiwata, and K. Yasuda. 2004. A 1480/1064 nm Dual Wavelength Photo-Thermal Etching System for Non-Contact Three-Dimensional Microstructure Generation into Agar Microculture Chip. Sensors and Actuators B: Chemical 100: 455–462.
Heller, D.A., V. Garga, K.J. Kelleher, T.C. Lee, S. Mahbubani, L.A. Sigworth, T.R. Lee, and M.A. Rea. 2005. Patterned Networks of Mouse Hippocampal Neurons on Peptide-Coated Gold Surfaces. Biomaterials 26: 883–889.
Hinkle, L., C.D. Mccaig, and K.R. Robinson. 1981. The Direction of Growth of Differentiating Neurones and Myoblasts from Frog Embryos in an Applied Electric Field. Journal of Physiology 314: 121–135.
Horn-Ranney, E.L., J.L. Curley, G.C. Catig, R.M. Huval, and M.J. Moore. 2013. Structural and Molecular Micropatterning of Dual Hydrogel Constructs for Neural Growth Models Using Photochemical Strategies. Biomedical Microdevices 15: 49–61.
Horn-Ranney, E.L., P. Khoshakhlagh, J.W. Kaiga, and M.J. Moore. 2014. Light-Reactive Dextran Gels with Immobilized Guidance Cues for Directed Neurite Growth in 3D Models. Biomaterials Science 2: 1450–1459.
Huval, R.M., O.H. Miller, J.L. Curley, Y. Fan, B.J. Hall, and M.J. Moore. 2015. Microengineered Peripheral Nerve-on-a-Chip for Preclinical Physiological Testing. Lab on a Chip 15(10): 2221–2232.
Hynd, M.R., J.P. Frampton, N. Dowell-Mesfin, J.N. Turner, and W. Shain. 2007. Directed Cell Growth on Protein-Functionalized Hydrogel Surfaces. Journal of Neuroscience Methods 162: 255–263.
Jaffe, L.F., and M.M. Poo. 1979. Neurites Grow Faster Towards the Cathode than the Anode in a Steady Field. Journal of Experimental Zoology 209: 115–128.
James, C.D., R. Davis, M. Meyer, A. Turner, S. Turner, G. Withers, L. Kam, G. Banker, H. Craighead, M. Isaacson, J. Turner, and W. Shain. 2000. Aligned Microcontact Printing of Micrometer-Scale Poly-l-Lysine Structures for Controlled Growth of Cultured Neurons on Planar Microelectrode Arrays. IEEE Transactions on Biomedical Engineering 47: 17–21.
Jeong, S.H., S.B. Jun, J.K. Song, and S.J. Kim. 2009. Activity-Dependent Neuronal Cell Migration Induced by Electrical Stimulation. Medical and Biological Engineering and Computing 47: 93–99.
Joanne Wang, C., X. Li, B. Lin, S. Shim, G.L. Ming, and A. Levchenko. 2008. A Microfluidics-Based Turning Assay Reveals Complex Growth Cone Responses to Integrated Gradients of Substrate-Bound ECM Molecules and Diffusible Guidance Cues. Lab on a Chip 8: 227–237.
Johansson, F., P. Carlberg, N. Danielsen, L. Montelius, and M. Kanje. 2006. Axonal Outgrowth on Nano-Imprinted Patterns. Biomaterials 27: 1251–1258.
Johansson, F., M. Jonsson, K. Alm, and M. Kanje. 2010. Cell Guidance by Magnetic Nanowires. Experimental Cell Research 316: 688–694.
Jun, S.B., M.R. Hynd, N. Dowell-Mesfin, K.L. Smith, J.N. Turner, W. Shain, and S.J. Kim. 2007a. Low-Density Neuronal Networks Cultured Using Patterned Poly-l-Lysine on Microelectrode Arrays. Journal of Neuroscience Methods 160: 317–326.
Jun, S.B., M.R. Hynd, K.L. Smith, J.K. Song, J.N. Turner, W. Shain, and S.J. Kim. 2007b. Electrical Stimulation-Induced Cell Clustering in Cultured Neural Networks. Medical and Biological Engineering and Computing 45: 1015–1021.
Jungblut, M., W. Knoll, C. Thielemann, and M. Pottek. 2009. Triangular Neuronal Networks on Microelectrode Arrays: An Approach to Improve the Properties of Low-Density Networks for Extracellular Recording. Biomedical Microdevices 11: 1269–1278.
Kam, L., W. Shain, J.N. Turner, and R. Bizios. 2001. Axonal Outgrowth of Hippocampal Neurons on Micro-Scale Networks of Polylysine-Conjugated Laminin. Biomaterials 22: 1049–1054.
Khan, S., and G. Newaz. 2010. A Comprehensive Review of Surface Modification for Neural Cell Adhesion and Patterning. Journal of Biomedical Materials Research. Part A 93: 1209–1224.
Khoshakhlagh, P., and M.J. Moore. 2015. Photoreactive Interpenetrating Network of Hyaluronic Acid and Puramatrix as a Selectively Tunable Scaffold for Neurite Growth. Acta Biomaterialia 16: 23–34.
Kim, S., W.S. Im, L. Kang, S.T. Lee, K. Chu, and B.I. Kim. 2008. The Application of Magnets Directs the Orientation of Neurite Outgrowth in Cultured Human Neuronal Cells. Journal of Neuroscience Methods 174: 91–96.
Klein, C.L., M. Scholl, and A. Maelicke. 1999. Neuronal Networks In Vitro: Formation and Organization on Biofunctionalized Surfaces. Journal of Materials Science: Materials in Medicine 10: 721–727.
Kleinfeld, D., K.H. Kahler, and P.E. Hockberger. 1988. Controlled Outgrowth of Dissociated Neurons on Patterned Substrates. Journal of Neuroscience 8: 4098–4120.
Koch, D., T. Betz, A. Ehrlicher, M. Gogler, B. Stuhrmann, and J. Kas. 2004. Optical Control of Neuronal Growth. Proceedings of SPIE 5514: 428–436.
Kolodkin, A.L., and M. Tessier-Lavigne. 2011. Mechanisms and Molecules of Neuronal Wiring: A Primer. Cold Spring Harbor Perspectives in Biology 3(6): 1–14
Koppes, A.N., A.M. Seggio, and D.M. Thompson. 2011. Neurite Outgrowth Is Significantly Increased by the Simultaneous Presentation of Schwann Cells and Moderate Exogenous Electric Fields. Journal of Neural Engineering 8: 046023.
Koppes, A.N., N.W. Zaccor, C.J. Rivet, L.A. Williams, J.M. Piselli, R.J. Gilbert, and D.M. Thompson. 2014. Neurite Outgrowth on Electrospun Plla Fibers Is Enhanced by Exogenous Electrical Stimulation. Journal of Neural Engineering 11: 046002.
Koroleva, A., A.A. Gill, I. Ortega, J.W. Haycock, S. Schlie, S.D. Gittard, B.N. Chichkov, and F. Claeyssens. 2012. Two-Photon Polymerization-Generated aNd Micromolding-Replicated 3D Scaffolds for Peripheral Neural Tissue Engineering Applications. Biofabrication 4: 025005.
Lauer, L., C. Klein, and A. Offenhausser. 2001. Spot Compliant Neuronal Networks by Structure Optimized Micro-contact Printing. Biomaterials 22: 1925–1932.
Lauer, L., A. Vogt, C.K. Yeung, W. Knoll, and A. Offenhäusser. 2002. Electrophysiological Recordings of Patterned Rat Brain Stem Slice Neurons. Biomaterials 23: 3123–3130.
Lee, W., J. Pinckney, V. Lee, J.H. Lee, K. Fischer, S. Polio, J.K. Park, and S.S. Yoo. 2009. Three-Dimensional Bioprinting of Rat Embryonic Neural Cells. Neuroreport 20: 798–803.
Leng, T., P. Wu, N.Z. Mehenti, S.F. Bent, M.F. Marmor, M.S. Blumenkranz, and H.A. Fishman. 2004. Directed Retinal Nerve Cell Growth for Use in a Retinal Prosthesis Interface. Investigative Ophthalmology and Visual Science 45: 4132–4137.
Li, B., Y. Ma, S. Wang, and P.M. Moran. 2005. Influence of Carboxyl Group Density on Neuron Cell Attachment and Differentiation Behavior: Gradient-Guided Neurite Outgrowth. Biomaterials 26: 4956–4963.
Li, G.N., J. Liu, and D. Hoffman-Kim. 2008. Multi-molecular Gradients of Permissive and Inhibitory Cues Direct Neurite Outgrowth. Annals of Biomedical Engineering 36: 889–904.
Liazoghli, D., A.D. Roth, P. Thostrup, and D.R. Colman. 2012. Substrate Micropatterning as a New in Vitro Cell Culture System to Study Myelination. ACS Chemical Neuroscience 3: 90–95.
Lorber, B., W.K. Hsiao, I.M. Hutchings, and K.R. Martin. 2014. Adult Rat Retinal Ganglion Cells and Glia Can Be Printed By Piezoelectric Inkjet Printing. Biofabrication 6: 015001.
Lowery, L.A., and D. Van Vactor. 2009. The Trip of the Tip: Understanding the Growth Cone Machinery. Nature Reviews. Molecular Cell Biology 10: 332–343.
Luo, Y., and M.S. Shoichet. 2004a. A Photolabile Hydrogel for Guided Three-Dimensional Cell Growth and Migration. Nature Materials 3: 249–253.
Luo, Y., and M.S. Shoichet. 2004b. Light-Activated Immobilization of Biomolecules to Agarose Hydrogels for Controlled Cellular Response. Biomacromolecules 5: 2315–2323.
Macias, M.Y., J.H. Battocletti, C.H. Sutton, F.A. Pintar, and D.J. Maiman. 2000. Directed and Enhanced Neurite Growth with Pulsed Magnetic Field Stimulation. Bioelectromagnetics 21: 272–286.
Mai, J., L. Fok, H. Gao, X. Zhang, and M.M. Poo. 2009. Axon Initiation and Growth Cone Turning on Bound Protein Gradients. Journal of Neuroscience 29: 7450–7458.
Martinoia, S., M. Bove, M. Tedesco, B. Margesin, and M. Grattarola. 1999. A Simple Microfluidic System for Patterning Populations of Neurons on Silicon Micromachined Substrates. Journal of Neuroscience Methods 87: 35–44.
Mathew, M., I. Amat-Roldan, R. Andres, S.I. Santos, D. Artigas, E. Soriano, and P. Loza-Alvarez. 2010. Signalling Effect of Nir Pulsed Lasers on Axonal Growth. Journal of Neuroscience Methods 186: 196–201.
Matsuda, T., T. Sugawara, and K. Inoue. 1992. Two-Dimensional Cell Manipulation Technology. An Artificial Neural Circuit Based on Surface Microphotoprocessing. ASAIO Journal 38: M243–M247.
Mccaig, C.D. 1986. Electric Fields, Contact Guidance and the Direction of Nerve Growth. Journal of Embryology and Experimental Morphology 94: 245–255.
Mccaig, C.D. 1989. Nerve Growth in the Absence of Growth Cone Filopodia and the Effects of a Small Applied Electric Field. Journal of Cell Science 93(Pt 4): 715–721.
Mccaig, C.D., L. Sangster, and R. Stewart. 2000. Neurotrophins Enhance Electric Field-Directed Growth Cone Guidance and Directed Nerve Branching. Developmental Dynamics 217: 299–308.
Mccormick, A.M., A. Wijekoon, and N.D. Leipzig. 2013. Specific Immobilization of Biotinylated Fusion Proteins NGF and Sema3A Utilizing a Photo-Cross-Linkable Diazirine Compound for Controlling Neurite Extension. Bioconjugate Chemistry 24: 1515–1526.
Mccormick, A.M., M.V. Maddipatla, S. Shi, E.A. Chamsaz, H. Yokoyama, A. Joy, and N.D. Leipzig. 2014. Micropatterned Coumarin Polyester Thin Films Direct Neurite Orientation. ACS Applied Materials & Interfaces 6: 19655–19667.
Mccormick, A.M., N.A. Jarmusik, and N.D. Leipzig. 2015. Co-immobilization of semaphorin3A and Nerve Growth Factor to Guide and Pattern Axons. Acta Biomaterialia 28: 33–44.
Mckinnon, D.D., T.E. Brown, K.A. Kyburz, E. Kiyotake, and K.S. Anseth. 2014. Design and Characterization of a Synthetically Accessible, Photodegradable Hydrogel for User-Directed Formation of Neural Networks. Biomacromolecules 15: 2808–2816.
Mehenti, N.Z., G.S. Tsien, T. Leng, H.A. Fishman, and S.F. Bent. 2006. A Model Retinal Interface Based on Directed Neuronal Growth for Single Cell Stimulation. Biomedical Microdevices 8: 141–150.
Melissinaki, V., A.A. Gill, I. Ortega, M. Vamvakaki, A. Ranella, J.W. Haycock, C. Fotakis, M. Farsari, and F. Claeyssens. 2011. Direct Laser Writing of 3D Scaffolds for Neural Tissue Engineering Applications. Biofabrication 3: 045005.
Millet, L.J., M.E. Stewart, R.G. Nuzzo, and M.U. Gillette. 2010. Guiding Neuron Development with Planar Surface Gradients of Substrate Cues Deposited Using Microfluidic Devices. Lab on a Chip 10: 1525–1535.
Mondal, A., B. Black, Y.T. Kim, and S. Mohanty. 2014. Loop Formation and Self-Fasciculation of Cortical Axon Using Photonic Guidance at Long Working Distance. Scientific Reports 4: 6902.
Moriguchi, H., Y. Wakamoto, Y. Sugio, K. Takahashi, I. Inoue, and K. Yasuda. 2002. An Agar-Microchamber Cell-Cultivation System: Flexible Change of Microchamber Shapes During Cultivation by Photo-Thermal Etching. Lab on a Chip 2: 125–132.
Moriguchi, H., K. Takahashi, Y. Sugio, Y. Wakamoto, I. Inoue, Y. Jimbo, and K. Yasuda. 2004. On‐Chip Neural Cell Cultivation using Agarose‐Microchamber Array Constructed by a Photothermal Etching Method. Electrical Engineering in Japan 146: 37–42.
Musoke-Zawedde, P., and M.S. Shoichet. 2006. Anisotropic Three-Dimensional Peptide Channels Guide Neurite Outgrowth Within a Biodegradable Hydrogel Matrix. Biomedical Materials 1: 162–169.
Nam, Y., D.W. Branch, and B.C. Wheeler. 2006. Epoxy-Silane Linking of Biomolecules Is Simple and Effective for Patterning Neuronal Cultures. Biosensors and Bioelectronics 22: 589–597.
Odawara, A., M. Gotoh, and I. Suzuki. 2013. Control of Neural Network Patterning Using Collagen Gel Photothermal Etching. Lab on a Chip 13: 2040–2046.
Pan, L., and R.B. Borgens. 2010. Perpendicular Organization of Sympathetic Neurons Within a Required Physiological Voltage. Experimental Neurology 222: 161–164.
Pan, L., and R.B. Borgens. 2012. Strict Perpendicular Orientation of Neural Crest-Derived Neurons In Vitro Is Dependent on an Extracellular Gradient of Voltage. Journal of Neuroscience Research 90: 1335–1346.
Pan, L., J. Cirillo, and R.B. Borgens. 2012. Neuronal Responses to an Asymmetrical Alternating Current Field Can Mimic Those Produced by an Imposed Direct Current Field In Vitro. Journal of Neuroscience Research 90: 1522–1532.
Patel, N., and M.M. Poo. 1982. Orientation of Neurite Growth by Extracellular Electric Fields. Journal of Neuroscience 2: 483–496.
Patel, N.B., and M.M. Poo. 1984. Perturbation of the Direction of Neurite Growth by Pulsed and Focal Electric Fields. Journal of Neuroscience 4: 2939–2947.
Patz, T.M., A. Doraiswamy, R.J. Narayan, W. He, Y. Zhong, R. Bellamkonda, R. Modi, and D.B. Chrisey. 2006. Three-Dimensional Direct Writing of B35 Neuronal Cells. Journal of Biomedical Materials Research Part B: Applied Biomaterials 78: 124–130.
Phamduy, T., D. Corr, and D. Chrisey. 2010. Bioprinting. In Encyclopedia of Industrial Biotechnology: Bioprocess, Bioseparation, and Cell Technology, ed. M. Flickinger. New York: Wiley.
Pine, J., and G. Chow. 2009. Moving Live Dissociated Neurons with an Optical Tweezer. IEEE Transactions on Biomedical Engineering 56: 1184–1188.
Pirlo, R.K., D.M. Dean, D.R. Knapp, and B.Z. Gao. 2006. Cell Deposition System Based on Laser Guidance. Biotechnology Journal 1: 1007–1013.
Pita-Thomas, W., M.B. Steketee, S.N. Moysidis, K. Thakor, B. Hampton, and J.L. Goldberg. 2015. Promoting Filopodial Elongation in Neurons by Membrane-Bound Magnetic Nanoparticles. Nanomedicine 11: 559–567.
Rahjouei, A., S. Kiani, A. Zahabi, N.Z. Mehrjardi, M. Hashemi, and H. Baharvand. 2011. Interactions of Human Embryonic Stem Cell-Derived Neural Progenitors with an Electrospun Nanofibrillar Surface In Vitro. International Journal of Artificial Organs 34: 559–570.
Rajnicek, A.M., N.A. Gow, and C.D. Mccaig. 1992. Electric Field-Induced Orientation of Rat Hippocampal Neurones In Vitro. Experimental Physiology 77: 229–232.
Rajnicek, A., S. Britland, and C. Mccaig. 1997. Contact Guidance of Cns Neurites on Grooved Quartz: Influence of Groove Dimensions, Neuronal Age and Cell Type. Journal of Cell Science 110(Pt 23): 2905–2913.
Rajnicek, A.M., K.R. Robinson, and C.D. Mccaig. 1998. The Direction of Neurite Growth in a Weak DC Electric Field Depends on the Substratum: Contributions of Adhesivity and Net Surface Charge. Developmental Biology 203: 412–423.
Reyes, D.R., E.M. Perruccio, S.P. Becerra, L.E. Locascio, and M. Gaitan. 2004. Micropatterning Neuronal Cells on Polyelectrolyte Multilayers. Langmuir 20: 8805–8811.
Richardson, J.A., C.W. Rementer, J.M. Bruder, and D. Hoffman-Kim. 2011. Guidance of Dorsal Root Ganglion Neurites and Schwann Cells by Isolated Schwann Cell Topography on Poly(Dimethyl Siloxane) Conduits and Films. Journal of Neural Engineering 8: 046015.
Ricoult, S.G., J.S. Goldman, D. Stellwagen, D. Juncker, and T.E. Kennedy. 2012. Generation of Microisland Cultures Using Microcontact Printing to Pattern Protein Substrates. Journal of Neuroscience Methods 208: 10–17.
Riggio, C., M.P. Calatayud, C. Hoskins, J. Pinkernelle, B. Sanz, T.E. Torres, M.R. Ibarra, L. Wang, G. Keilhoff, G.F. Goya, V. Raffa, and A. Cuschieri. 2012. Poly-l-Lysine-Coated Magnetic Nanoparticles as Intracellular Actuators for Neural Guidance. International Journal of Nanomedicine 7: 3155–3166.
Riggio, C., M.P. Calatayud, M. Giannaccini, B. Sanz, T.E. Torres, R. Fernandez-Pacheco, A. Ripoli, M.R. Ibarra, L. Dente, A. Cuschieri, G.F. Goya, and V. Raffa. 2014. The Orientation of the neuronal Growth Process Can Be Directed Via Magnetic Nanoparticles Under an Applied Magnetic Field. Nanomedicine 10: 1549–1558.
Ringeisen, B.R., C.M. Othon, J.A. Barron, D. Young, and B.J. Spargo. 2006. Jet-Based Methods to Print Living Cells. Biotechnology Journal 1: 930–948.
Romanova, E.V., K.A. Fosser, S.S. Rubakhin, R.G. Nuzzo, and J.V. Sweedler. 2004. Engineering the Morphology and Electrophysiological Parameters of Cultured Neurons by Microfluidic Surface Patterning. Faseb Journal 18: 1267–1269.
Rosenbalm, T.N., S. Owens, D. Bakken, and B.Z. Gao. 2006. Cell Viability Test After Laser Guidance. Proceedings of SPIE 6084: 608418–608418-8.
Roth, E.A., T. Xu, M. Das, C. Gregory, J.J. Hickman, and T. Boland. 2004. Inkjet Printing for High-Throughput Cell Patterning. Biomaterials 25: 3707–3715.
Ryan, A.F., J. Wittig, A. Evans, S. Dazert, and L. Mullen. 2006. Environmental Micro-Patterning for the Study of Spiral Ganglion Neurite Guidance. Audiology and Neuro-Otology 11: 134–143.
Sanjana, N.E., and S.B. Fuller. 2004. A Fast Flexible Ink-Jet Printing Method for Patterning Dissociated Neurons in Culture. Journal of Neuroscience Methods 136: 151–163.
Sarig-Nadir, O., N. Livnat, R. Zajdman, S. Shoham, and D. Seliktar. 2009. Laser Photoablation of Guidance Microchannels into Hydrogels Directs Cell Growth in Three Dimensions. Biophysical Journal 96: 4743–4752.
Schiele, N.R., R.A. Koppes, D.T. Corr, K.S. Ellison, D.M. Thompson, L.A. Ligon, T.K.M. Lippert, and D.B. Chrisey. 2009. Laser Direct Writing of Combinatorial Libraries of Idealized Cellular Constructs: Biomedical Applications. Applied Surface Science 255: 5444–5447.
Schiele, N.R., D.T. Corr, Y. Huang, N.A. Raof, Y. Xie, and D.B. Chrisey. 2010. Laser-Based Direct-Write Techniques for Cell Printing. Biofabrication 2(3): 032001.
Schmalenberg, K.E., H.M. Buettner, and K.E. Uhrich. 2004. Microcontact Printing of Proteins on Oxygen Plasma-Activated Poly(Methyl Methacrylate). Biomaterials 25: 1851–1857.
Schmidt, C.E., and J.B. Leach. 2003. Neural Tissue Engineering: Strategies for Repair and Regeneration. Annual Review of Biomedical Engineering 5: 293–347.
Scholl, M., C. Sprossler, M. Denyer, M. Krause, K. Nakajima, A. Maelicke, W. Knoll, and A. Offenhausser. 2000. Ordered Networks of Rat Hippocampal Neurons Attached to Silicon Oxide Surfaces. Journal of Neuroscience Methods 104: 65–75.
Scott, M.A., Z.D. Wissner-Gross, and M.F. Yanik. 2012. Ultra-Rapid Laser Protein Micropatterning: Screening for Directed Polarization of Single Neurons. Lab on a Chip 12: 2265–2276.
Seidlits, S.K., C.E. Schmidt, and J.B. Shear. 2009. High‐Resolution Patterning of Hydrogels in Three Dimensions Using Direct‐Write Photofabrication for Cell Guidance. Advanced Functional Materials 19: 3543–3551.
Shi, P., K. Shen, and L.C. Kam. 2007. Local Presentation of L1 and N-cadherin in Multicomponent, Microscale Patterns Differentially Direct Neuron Function In Vitro. Developmental Neurobiology 67: 1765–1776.
Sorkin, R., T. Gabay, P. Blinder, D. Baranes, E. Ben-Jacob, and Y. Hanein. 2006. Compact Self-Wiring in Cultured Neural Networks. Journal of Neural Engineering 3: 95–101.
Staii, C., C. Viesselmann, J. Ballweg, L. Shi, G.-Y. Liu, J.C. Williams, E.W. Dent, S.N. Coppersmith, and M.A. Eriksson. 2009. Positioning and Guidance of Neurons on Gold Surfaces by Directed Assembly of Proteins Using Atomic Force Microscopy. Biomaterials 30: 3397–3404.
Staii, C., C. Viesselmann, J. Ballweg, J.C. Williams, E.W. Dent, S.N. Coppersmith, and M.A. Eriksson. 2011. Distance Dependence of Neuronal Growth on Nanopatterned Gold Surfaces. Langmuir 27: 233–239.
Stevenson, D.J., T.K. Lake, B. Agate, V. Garces-Chavez, K. Dholakia, and F. Gunn-Moore. 2006. Optically Guided Neuronal Growth at Near Infrared Wavelengths. Optics Express 14: 9786–9793.
Stuhrmann, B., M. Gögler, T. Betz, A. Ehrlicher, D. Koch, and J. Käs. 2005. Automated Tracking and Laser Micromanipulation of Motile Cells. Review of Scientific Instruments 76: 035105.
Sugio, Y., K. Kojima, H. Moriguchi, K. Takahashi, T. Kaneko, and K. Yasuda. 2004. An Agar-Based On-Chip Neural-Cell-Cultivation System for Stepwise Control of Network Pattern Generation During Cultivation. Sensors and Actuators B: Chemical 99: 156–162.
Suzuki, Ikurou, and Y. Kenji. 2007. Constructive Formation and Connection of Aligned Micropatterned Neural Networks by Stepwise Photothermal Etching During Cultivation. Japanese Journal of Applied Physics 46: 6398.
Suzuki, Ikurou, Yoshihiro Sugio, Yasuhiko Jimbo, and Y. Kenji. 2004a. Individual-Cell-Based Electrophysiological Measurement of a Topographically Controlled Neuronal Network Pattern Using Agarose Architecture with a Multi-electrode Array. Japanese Journal of Applied Physics 43: L403.
Suzuki, I., Y. Sugio, H. Moriguchi, A. Hattori, K. Yasuda, and Y. Jimbo. 2004b. Pattern Modification of a Neuronal Network for Individual-Cell-Based Electrophysiological Measurement Using Photothermal Etching of an Agarose Architecture with a Multielectrode Array. IEE Proceedings: Nanobiotechnology 151: 116–121.
Suzuki, I., Y. Sugio, H. Moriguchi, Y. Jimbo, and K. Yasuda. 2004c. Modification of a Neuronal Network Direction Using Stepwise Photo-Thermal Etching of an Agarose Architecture. Journal of Nanobiotechnology 2: 7.
Suzuki, I., Y. Sugio, Y. Jimbo, and K. Yasuda. 2005. Stepwise Pattern Modification of Neuronal Network in Photo-Thermally-Etched Agarose Architecture on Multi-Electrode Array Chip for Individual-Cell-Based Electrophysiological Measurement. Lab on a Chip 5: 241–247.
Swarup, V.P., T.W. Hsiao, J. Zhang, G.D. Prestwich, B. Kuberan, and V. Hlady. 2013. Exploiting Differential Surface Display of Chondroitin Sulfate Variants for Directing Neuronal Outgrowth. Journal of the American Chemical Society 135: 13488–13494.
Tankus, A., I. Fried, and S. Shoham. 2014. Cognitive-Motor Brain–Machine Interfaces. Journal of Physiology, Paris 108: 38–44.
Townes-Anderson, E., R.S. St Jules, D.M. Sherry, J. Lichtenberger, and M. Hassanain. 1998. Micromanipulation of Retinal Neurons by Optical Tweezers. Molecular Vision 4: 12.
Tsuruma, A., M. Tanaka, S. Yamamoto, N. Fukushima, H. Yabu, and M. Shimomura. 2006. Topographical Control of Neurite Extension on Stripe-Patterned Polymer Films. Colloids and Surfaces, A: Physicochemical and Engineering Aspects 284–285: 470–474.
Turcu, F., K. Tratsk-Nitz, S. Thanos, W. Schuhmann, and P. Heiduschka. 2003. Ink-Jet Printing for Micropattern Generation of Laminin for Neuronal Adhesion. Journal of Neuroscience Methods 131: 141–148.
Turner, S., L. Kam, M. Isaacson, H.G. Craighead, W. Shain, and J. Turner. 1997. Cell Attachment on Silicon Nanostructures. Journal of Vacuum Science and Technology B 15: 2848–2854.
Turner, A.M., N. Dowell, S.W. Turner, L. Kam, M. Isaacson, J.N. Turner, H.G. Craighead, and W. Shain. 2000. Attachment of Astroglial Cells to Microfabricated Pillar Arrays of Different Geometries. Journal of Biomedical Materials Research 51: 430–441.
Vogt, A.K., G.J. Brewer, T. Decker, S. Bocker-Meffert, V. Jacobsen, M. Kreiter, W. Knoll, and A. Offenhausser. 2005a. Independence of Synaptic Specificity from Neuritic Guidance. Neuroscience 134: 783–790.
Vogt, A.K., G.J. Brewer, and A. Offenhausser. 2005b. Connectivity Patterns in Neuronal Networks of Experimentally Defined Geometry. Tissue Engineering 11: 1757–1767.
Vogt, A.K., G. Wrobel, W. Meyer, W. Knoll, and A. Offenhausser. 2005c. Synaptic Plasticity in Micropatterned Neuronal Networks. Biomaterials 26: 2549–2557.
Von Philipsborn, A.C., S. Lang, J. Loeschinger, A. Bernard, C. David, D. Lehnert, F. Bonhoeffer, and M. Bastmeyer. 2006. Growth Cone Navigation in Substrate-Bound Ephrin Gradients. Development 133: 2487–2495.
Wang, S., C. WongPoFoo, A. Warrier, M.M. Poo, S.C. Heilshorn, and X. Zhang. 2009. Gradient Lithography of Engineered Proteins to Fabricate 2D and 3D Cell Culture Microenvironments. Biomedical Microdevices 11: 1127–1134.
Wu, T., T.A. Nieminen, S. Mohanty, J. Miotke, R.L. Meyer, H. Rubinsztein-Dunlop, and M.W. Berns. 2012. A Photon-Driven Micromotor Can Direct Nerve Fibre Growth. Nature Photonics 6: 62–67.
Wyart, C., C. Ybert, L. Bourdieu, C. Herr, C. Prinz, and D. Chatenay. 2002. Constrained Synaptic Connectivity in Functional Mammalian Neuronal Networks Grown on Patterned Surfaces. Journal of Neuroscience Methods 117: 123–131.
Xu, T., J. Jin, C. Gregory, J.J. Hickman, and T. Boland. 2005. Inkjet Printing of Viable Mammalian Cells. Biomaterials 26: 93–99.
Xu, T., C.A. Gregory, P. Molnar, X. Cui, S. Jalota, S.B. Bhaduri, and T. Boland. 2006. Viability and Electrophysiology of Neural Cell Structures Generated by the Inkjet Printing Method. Biomaterials 27: 3580–3588.
Xu, X., N.J. Wittenberg, L.R. Jordan, S. Kumar, J.O. Watzlawik, A.E. Warrington, S.H. Oh, and M. Rodriguez. 2013. A Patterned Recombinant Human IgM Guides Neurite Outgrowth of CNS NEurons. Scientific Reports 3: 2267.
Yao, L., L. Shanley, C. Mccaig, and M. Zhao. 2008. Small Applied Electric Fields Guide Migration of Hippocampal Neurons. Journal of Cellular Physiology 216: 527–535.
Yao, L., S. Wang, W. Cui, R. Sherlock, C. O’Connell, G. Damodaran, A. Gorman, A. Windebank, and A. Pandit. 2009. Effect of Functionalized Micropatterned PLGA on Guided Neurite Growth. Acta Biomaterialia 5: 580–588.
Zhang, B.G., A.F. Quigley, D.E. Myers, G.G. Wallace, R.M. Kapsa, and P.F. Choong. 2014a. Recent Advances in Nerve Tissue Engineering. International Journal of Artificial Organs 37: 277–291.
Zhang, K., C.K. Chou, X. Xia, M.C. Hung, and L. Qin. 2014b. Block-Cell-Printing for Live Single-Cell Printing. Proceedings of the National Academy of Sciences of the United States of America 111: 2948–2953.
Zhu, B., Q. Zhang, Q. Lu, Y. Xu, J. Yin, J. Hu, and Z. Wang. 2004. Nanotopographical Guidance of C6 Glioma Cell Alignment and Oriented Growth. Biomaterials 25: 4215–4223.
Zorlutuna, P., J.H. Jeong, H. Kong, and R. Bashir. 2011. Stereolithography-Based Hydrogel Microenvironments to Examine Cellular Interactions. Advanced Functional Materials 21: 3642–3651.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Bowser, D.A., Moore, M.J. (2016). Engineering Neuronal Patterning and Defined Axonal Elongation In Vitro. In: Zhang, L., Kaplan, D. (eds) Neural Engineering. Springer, Cham. https://doi.org/10.1007/978-3-319-31433-4_3
Download citation
DOI: https://doi.org/10.1007/978-3-319-31433-4_3
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-31431-0
Online ISBN: 978-3-319-31433-4
eBook Packages: EngineeringEngineering (R0)