In Vitro Models for Biomechanical Studies of Neural Tissues

Studies in Mechanobiology, Tissue Engineering and Biomaterials

Volumn 3, Issue , 2011, Pages 247-285

  Morrison, Barclay ^a   Cullen, D Kacy ^b   LaPlaca, Michelle ^c  

^a Department of Earth and Environmental Sciences   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

3D; Mechanical properties; Mechanotransduction; Neural cell culture; Neural injury; Neural mechanical tolerance; Organotypic culture

Indexed keywords

EID: 84889673213     PISSN: 18682006     EISSN: 18682014     Source Type: Book Series    
DOI: 10.1007/8415_2011_79     Document Type: Chapter

References (173)

1. Kindle, E., Schwartz, J., Jessell, T.: Principles of Neural Science. McGraw-Hill, New York (2000)
2. Sycoma, E., Nicholson, C.: Diffusion in brain extracellular space. Physiol. Rev. 88, 1277–1340 (2008)
3. Sycoma, E.: Extra synaptic volume transmission and diffusion parameters of the extracellular space. Neuroscience 129, 861–876 (2004)
4. Sycoma, E.: Diffusion properties of the brain in health and disease. Neurochem. Int. 45, 453–466 (2004)
5. Fedoroff, S., Richardson, A.: Protocols for Neural Cell Culture, 3rd edn. Humana Press, Totowa (2001)
6. Hayflick, L., Moorhead, P.: The serial cultivation of human diploid cell strains. Exp. Cell Res. 25, 585–621 (1961)
7. Jacobson, M.: Clonal analysis and cell lineages of the vertebrate central nervous system. Annu. Rev. Neurosci. 8, 71–102 (1985)
8. Potter, S.M., DeMarse, T.B.: A new approach to neural cell culture for long-term studies. J. Neurosci. Methods 110, 17–24 (2001)
9. Dichter, M.A.: Rat cortical neurons in cell culture: culture methods, cell morphology, electrophysiology, and synapse formation. Brain. Res. 149, 279–293 (1978)
10. Corey, J.M., Wheeler, B.C., Brewer, G.J.: Compliance of hippocampal neurons to patterned substrate networks. J. Neurosci. Res. 30, 300–307 (1991)
11. Choi, H.K., Won, L., Heller, A.: Dopaminergic neurons grown in three-dimensional reaggregate culture for periods of up to one year. J. Neurosci. Methods 46, 233–244 (1993)
12. Hsiang, J., Heller, A., Hoffmann, P.C., Mobley, W.C., Wainer, B.H.: The effects of nerve growth factor on the development of septal cholinergic neurons in reaggregate cell cultures. Neuroscience 29, 209–223 (1989)
13. O’Connor, S.M., Andreadis, J.D., Shaffer, K.M., Ma, W., Pancrazio, J.J., Stenger, D.A.: Immobilization of neural cells in three-dimensional matrices for biosensor applications. Biosens. Bioelectron. 14, 871–881 (2000)
14. Cullen, D.K., Simon, C.M., LaPlaca, M.C.: Strain rate-dependent induction of reactive astrogliosis and cell death in three-dimensional neuronal-astrocytic co-cultures. Brain Res. 1158, 103–115 (2007)
15. O’Connor, S.M., Stenger, D.A., Shaffer, K.M., Ma, W.: Survival and neurite outgrowth of rat cortical neurons in three-dimensional agarose and collagen gel matrices. Neurosci. Lett. 304, 189–193 (2001)
16. Woerly, S., Plant, G.W., Harvey, A.R.: Cultured rat neuronal and glial cells entrapped within hydrogel polymer matrices: a potential tool for neural tissue replacement. Neurosci. Lett. 205, 197–201 (1996)
17. LaPlaca, M.C., Cullen, D.K., McLoughlin, J.J., Cargill 2nd, R.S.: High rate shear strain of three-dimensional neural cell cultures: a new in vitro traumatic brain injury model. J. Biomech. 38, 1093–1105 (2005)
18. Edelman, D.B., Keefer, E.W.: A cultural renaissance: in vitro cell biology embraces three-dimensional context. Exp. Neurol. 192, 1–6 (2005)
19. Cukierman, E., Pankov, R., Stevens, D.R., Yamada, K.M.: Taking cell-matrix adhesions to the third dimension. Science 294, 1708–1712 (2001)
20. Cukierman, E., Pankov, R., Yamada, K.M.: Cell interactions with three-dimensional matrices. Curr. Opin. Cell. Biol. 14, 633–639 (2002)
21. Schmeichel, K.L., Bissell, M.J.: Modeling tissue-specific signaling and organ function in three dimensions. J. Cell Sci. 116, 2377–2388 (2003)
22. Yamada, K.M., Pankov, R., Cukierman, E.: Dimensions and dynamics in integrin function. Braz. J. Med. Biol. Res. 36, 959–966 (2003)
23. Miller, B.E., Miller, F.R., Heppner, G.H.: Factors affecting growth and drug sensitivity of mouse mammary tumor lines in collagen gel cultures. Cancer Res. 45, 4200–4205 (1985)
24. Grinnell, F.: Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol. 13, 264–269 (2003)
25. Balgude, A.P., Yu, X., Szymanski, A., Bellamkonda, R.V.: Agarose gel stiffness determines rate of DRAG neurite extension in 3M cultures. Biomaterials 22, 1077–1084 (2001)
26. Coates, P.W., Fermini, B., Strahlendorf, J.C., Strahlendorf, H.K.: Utilization of three-dimensional culture for early morphometric and electrophysiological analyses of solitary cerebellar neurons. Dev. Neurosci. 14, 35–43 (1992)
27. Coates, P.W., Nathan, R.D.: Feasibility of electrical recordings from unconnected vertebrate CNS neurons cultured in a three-dimensional extracellular matrix. J. Neurosci. Methods 20, 203–210 (1987)
28. O’Shaughnessy, T.J., Lin, H.J., Ma, W.: Functional synapse formation among rat cortical neurons grown on three-dimensional collagen gels. Neurosci. Lett. 340, 169–172 (2003)
29. Spector, D.H., Boss, B.D., Strecker, R.E.: A model three-dimensional culture system for mammalian dopaminergic precursor cells: application for functional intracerebral transplantation. Exp. Neurol. 124, 253–264 (1993)
30. Bellamkonda, R., Ranieri, J.P., Aebischer, P.: Laminin oligopeptide derivatized agarose gels allow three-dimensional neurite extension in vitro. J. Neurosci. Res. 41, 501–509 (1995)
31. Cullen, D.K., LaPlaca, M.C.: Neuronal response to high rate shear deformation depends on heterogeneity of the local strain field. J. Neurotrauma 23, 1304–1319 (2006)
32. Cullen, D.K., Lessing, M.C., LaPlaca, M.C.: Collagen-dependent neurite outgrowth and response to dynamic deformation in three-dimensional neuronal cultures. Ann Biomed. Eng. 35, 835–846 (2007)
33. Vukasinovic, J., Cullen, D.K., LaPlaca, M.C., Glezer, A.: A microperfused incubator for tissue mimetic 3D cultures. Biomed. Microdevices 11, 1155–1165 (2009)
34. Dillon, G.P., Yu, X., Sridharan, A., Ranieri, J.P., Bellamkonda, R.V.: The influence of physical structure and charge on neurite extension in a 3D hydrogel scaffold. J. Biomater. Sci. Polym. Ed. 9, 1049–1069 (1998)
35. Willits, R.K., Skornia, S.L.: Effect of collagen gel stiffness on neurite extension. J. Biomater. Sci. Polym. Ed. 15, 1521–1531 (2004)
36. Schense, J.C., Hubbell, J.A.: Three-dimensional migration of neurites is mediated by adhesion site density and affinity. J. Biol. Chem. 275, 6813–6818 (2000)
37. Yu, T.T., Shoichet, M.S.: Guided cell adhesion and outgrowth in peptide-modified channels for neural tissue engineering. Biomaterials 26, 1507–1514 (2005)
38. Yu, X., Bellamkonda, R.V.: Dorsal root ganglia neurite extension is inhibited by mechanical and chondroitin sulfate-rich interfaces. J. Neurosci. Res. 66, 303–310 (2001)
39. Borkenhagen, M., Clemence, J.F., Sigrist, H., Aebischer, P.: Three-dimensional extracellular matrix engineering in the nervous system. J. Biomed. Mater. Res. 40, 392–400 (1998)
40. Tsacopoulos, M.: Metabolic signaling between neurons and glial cells: a short review. J. Physiol. Paris 96, 283–288 (2002)
41. Tsacopoulos, M., Magistretti, P.J.: Metabolic coupling between glia and neurons. J. Neurosci. 16, 877–885 (1996)
42. Aschner, M.: Neuron-astrocyte interactions: implications for cellular energetics and antioxidant levels. Neurotoxicology 21, 1101–1107 (2000)
43. Pardo, B., Honegger, P.: Differentiation of rat striatal embryonic stem cells in vitro: monolayer culture vs three-dimensional coculture with differentiated brain cells. J. Neurosci. Res. 59, 504–512 (2000)
44. Pulliam, L., Stubblebine, M., Hyun, W.: Quantification of neurotoxicity and identification of cellular subsets in a three-dimensional brain model. Cytometry 32, 66–69 (1998)
45. Irons, H.R., Cullen, D.K., Shapiro, N.P., Lambert, N.A., Lee, R.H., LaPlaca, M.C.: Three-dimensional neural constructs: a novel platform for neurophysiological investigation. J. Neural. Eng. 5, 333–341 (2008)
46. Ahmed, S.M., Rzigalinski, B.A., Willoughby, K.A., Sitterding, H.A., Ellis, E.F.: Stretch-induced injury alters mitochondrial membrane potential and cellular ATP in cultured astrocytes and neurons. J. Neurochem. 74, 1951–1960 (2000)
47. Steinschneider, R., Delmas, P., Nedelec, J., Gola, M., Bernard, D., Boucraut, J.: Appearance of neurofilament subunit epitopes correlates with electrophysiological maturation in cortical embryonic neurons cocultured with mature astrocytes. Brain. Res. Dev. Brain. Res. 95, 15–27 (1996)
48. Nakanishi, K., Nakanishi, M., Kukita, F.: Dual intracellular recording of neocortical neurons in a neuron-glia co-culture system. Brain Res. Brain. Res. Protoc. 4, 105–114 (1999)
49. LaPlaca, M.C., Vernekar, V.N., Shoemaker, J.T., Cullen, D.K.: Three-dimensional neuronal cultures. In: Berthiaume, F., Morgan, J. (eds.) Methods in Bioengineering: 3D Tissue Engineering. Artech House Publishers, London (2010)
50. Nicholson, C., Sykova, E.: Extracellular space structure revealed by diffusion analysis. Trends Neurosci. 21, 207–215 (1998)
51. Cullen, D.K., Vukasinovic, J., Glezer, A., Laplaca, M.C.: Microfluidic engineered high cell density three-dimensional neural cultures. J. Neural Eng. 4, 159–172 (2007)
52. Braitenberg, V.: Brain size and number of neurons: an exercise in synthetic neuroanatomy. J. Comput. Neurosci. 10, 71–77 (2001)
53. Gabbott, P.L., Stewart, M.G.: Distribution of neurons and glia in the visual cortex (area 17) of the adult albino rat: a quantitative description. Neuroscience 21, 833–845 (1987)
54. Alves, P., Moreira, J., Rodrigues, J., Aunins, J., Carrondo, M.: Two-dimensional versus three-dimensional culture systems: effects on growth and productivity of BHK cells. Biotechnol. Bioeng. 52, 429–432 (1996)
55. Kleinman, H.K., McGarvey, M.L., Hassell, J.R., Star, V.L., Cannon, F.B., et al.: Basement membrane complexes with biological activity. Biochemistry 25, 312–318 (1986)
56. Vukicevic, S., Kleinman, H.K., Luyten, F.P., Roberts, A.B., Roche, N.S., Reddi, A.H.: Identification of multiple active growth factors in basement membrane Matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components. Exp. Cell Res. 202, 1–8 (1992)
57. Morrison III, B., Cater, H.L., Benham, C.D., Sundstrom, L.E.: An in vitro model of traumatic brain injury utilising two-dimensional stretch of organotypic hippocampal slice cultures. J. Neurosci. Meth. 150, 192–201 (2006)
58. Stoppini, L., Buchs, P.A., Muller, D.: Lesion-induced neurite sprouting and synapse formation in hippocampal organotypic cultures. Neuroscience 57, 985–994 (1993)
59. Gahwiler, B.H.: Organotypic monolayer cultures of nervous tissue. J. Neurosci. Meth. 4, 329–342 (1981)
60. Elkin, B.S., Morrison III, B.: Region-specific tolerance criteria for the living brain. Stapp Car Crash J. 51, 127–138 (2007)
61. Sieg, F., Wahle, P., Pape, H.C.: Cellular reactivity to mechanical axonal injury in an organotypic in vitro model of neurotrauma. J. Neurotrauma 16, 1197–1213 (1999)
62. Morrison III, B., Eberwine, J.H., Meaney, D.F., McIntosh, T.K.: Traumatic injury induces differential expression of cell death genes in organotypic brain slice cultures determined by complementary DNA array hybridization. Neuroscience 96, 131–139 (2000)
63. Krassioukov, A.V., Ackery, A., Schwartz, G., Adamchik, Y., Liu, Y., Fehlings, M.G.: An in vitro model of neurotrauma in organotypic spinal cord cultures from adult mice. Brain Res. Brain Res. Protoc. 10, 60–68 (2002)
64. Stavridis, S.I., Dehghani, F., Korf, H.W., Hailer, N.P.: Characterisation of transverse slice culture preparations of postnatal rat spinal cord: preservation of defined neuronal populations. Histochem. Cell Biol. 123, 377–392 (2005)
65. Gahwiler, B.H.: Development of the hippocampus in vitro: cell types, synapses, and receptors. Neuroscience 11, 751–760 (1984)
66. Del. Rio., J.A., Heimrich, B., Soriano, E., Schwegler, H., Frotscher, M.: Proliferation and differentiation of glial fibrillary acidic protein immunoreactive glial cells in organotypic slice cultures of rat hippocampus. Neuroscience 43, 335–347 (1991)
67. Caeser, M., Aertsen, A.: Morphological organization of rat hippocampal slice cultures. J. Comp. Neurol. 307, 87–106 (1991)
68. Stoppini, L., Buchs, P.A., Muller, D.: A simple method for organotypic cultutres of nervous tissue. J. Neurosci. Meth. 37, 173–182 (1991)
69. Buchs, P.A., Stoppini, L., Muller, D.: Structural modifications associated with synaptic development in area CA1 of rat hippocampal organotypic cultures. Brain Res. Dev. Brain Res. 71, 81–91 (1993)
70. Mielke, J.G., Comas, T., Woulfe, J., Monette, R., Chakravarthy, B., Mealing, G.A.: Cytoskeletal, synaptic, and nuclear protein changes associated with rat interface organotypic hippocampal slice culture development. Brain Res. Dev. Brain Res. 160, 275–286 (2005)
71. De Simoni, A., Griesinger, C.B., Edwards, F.A.: Development of rat CA1 neurones in acute versus organotypic slices: role of experience in synaptic morphology and activity. J. Physiol. 550, 135–147 (2003)
72. Collin, C., Miyaguchi, K., Segal, M.: Dendritic spine density and LTP induction in cultured hippocampal slices. J. Neurophysiol. 77, 1614–1623 (1997)
73. Gahwiler, B.H.: Slice cultures of cerebellar, hippocampal, and hypothalamic tissue. Experientia 40, 235–243 (1984)
74. Robain, O., Barbin, G., de Billette, V., Jardin, L., Jahchan, T., Ben-Ari, Y.: Development of mossy fiber synapses in hippocampal slice culture. Brain Res. Dev. Brain Res. 80, 244–250 (1994)
75. Hartel, R., Matus, A.: Cytoskeletal maturation in cultured hippocampal slices. Neuroscience 78, 1–5 (1997)
76. Bahr, B.A., Kessler, M., Rivera, S., Vanderklish, P.W., Hall, R.A., et al.: Stable maintenance of glutamate receptors and other synaptic components in long-term hippocampal slices. Hippocampus 5, 425–439 (1995)
77. Martens, U., Wree, A.: Distribution of [3H]MK-801, [3H]AMPA and [3H]kainate binding sites in rat hippocampal long-term slice cultures isolated from external afferents. Anat. Embryol. (Berl) 203, 491–500 (2001)
78. Morrison III, B., Pringle, A.K., McManus, T., Ellard, J., Bradley, M., et al.: L-Arginyl-3, 4-Spermidine is neuroprotective in several in vitro models of neurodegeneration and in vivo ischaemia without suppressing synaptic transmission. Brit. J. Pharm. 137, 1255–1268 (2002)
79. Vornov, J.J., Tasker, R.C., Lost, D.: Direct observation of the agonist-specific regional vulnerability to glutamate, NMDA, and kainate neurotoxicity in organotypic hippocampal cultures. Exp. Neurol. 114, 11–22 (1991)
80. Gutierrez, R., Heinemann, U.: Synaptic reorganization in explanted cultures of rat hippocampus. Brain Res. 815, 304–316 (1999)
81. Parent, J.M., Yu, T.W., Leibowitz, R.T., Geschwind, D.H., Sloviter, R.S., Lowenstein, D.H.: Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosc. Off. J. Soc. Neurosci. 17, 3727–3738 (1997)
82. Muller, D., Buchs, P.A., Stoppini, L.: Time course of synaptic development in hippocampal organotypic cultures. Brain Res. Mol. Brain Res. 71, 93–100 (1993)
83. McBain, C.J., Boden, P., Hill, R.G.: Rat hippocampal slices ‘in vitro’ display spontaneous epileptiform activity following long-term organotypic culture. J. Neurosci. Meth. 27, 35–49 (1989)
84. Fowler, J., Bornstein, M.B., Crain, S.M.: Sustained hyperexcitability elicited by repetitive electric stimulation of organotypic hippocampal explants. Brain Res. 378, 398–404 (1986)
85. Xiang, Z., Hrabetova, S., Moskowitz, S.I., Casaccia-Bonnefil, P., Young, S.R., et al.: Long-term maintenance of mature hippocampal slices in vitro. J. Neurosci. Meth. 98, 145–154 (2000)
86. Finley, M., Fairman, D., Liu, D., Li, P., Wood, A., Cho, S.: Functional validation of adult hippocampal organotypic cultures as an in vitro model of brain injury. Brain Res. 1001, 125–132 (2004)
87. Wilhelmi, E., Schoder, U.H., Benabdallah, A., Sieg, F., Breder, J., Reymann, K.G.: Organotypic brain-slice cultures from adult rats: approaches for a prolonged culture time. Altern. Lab Anim. 30, 275–283 (2002)
88. Takhounts, E.G., Eppinger, R.H., Campbell, J.Q., Tannous, R.E., Power, E.D.: On the development of the SIMon finite element head model. Stapp Car Crash J. 47, 107–133 (2003)
89. Cheng, S., Clarke, E.C., Bilston, L.E.: Rheological properties of the tissues of the central nervous system: a review. Med. Eng. Phys. 30, 1318–1337 (2008)
90. Hrapko, M., van Dommelen, J.A., Peters, G.W., Wismans, J.S.: The influence of test conditions on characterization of the mechanical properties of brain tissue. J. Biomech. Eng. 130, 031003 (2008)
91. Fallenstein, G.T., Hulce, V.D.: Dynamic mechanical properties of human brain tissue. J. Biomech. 2, 217–226 (1969)
92. Arbogast, K.B., Margulies, S.S.: Material characterization of the brainstem from oscillatory shear tests. J. Biomech. 31, 801–807 (1998)
93. Nicolle, S., Lounis, M., Willinger, R., Palierne, J.F.: Shear linear behavior of brain tissue over a large frequency range. Biorheology 42, 209–223 (2005)
94. Bilston, L.E., Liu, Z., Phan-Thien, N.: Large strain behaviour of brain tissue in shear: some experimental data and differential constitutive model. Biorheology 38, 335–345 (2001)
95. Takhounts E., Crandall, J.R., Darvish, K.K.: On the importance of nonlinearity of brain tissue under large deformations. Stapp Car Crash J. 47, 79–92 (2003)
96. Tamura, A., Hayashi, S., Watanabe, I., Nagayama, K., Matsumoto, T.: Mechanical characterization of brain tissue in high-rate compression. J. Biomech. Sci. Eng. 2, 115–126 (2007)
97. Cheng, S., Bilston, L.E.: Unconfined compression of white matter. J. Biomech. 40, 117–124 (2007)
98. Miller, K., Chinzei, K.: Mechanical properties of brain tissue in tension. J. Biomech. 35, 483–490 (2002)
99. Franceschini, G., Bigoni, D., Regitnig, P., Holzapfel, G.A.: Brain tissue deforms similarly to filled elastomers and follows consolidation theory. J. Mech. Phys. Solids 54, 2592–2620 (2006)
100. Mao, H., Jin, X., Zhang, L., Yang, K.H., Igarashi, T., et al.: Finite element analysis of controlled cortical impact-induced cell loss. J. Neurotrauma 27, 877–888 (2010)
101. Hicks, R., Soares, H., Smith, D., McIntosh, T.: Temporal and spatial characterization of neuronal injury following lateral fluid-percussion brain injury in the rat. Acta Neuropathol. 91, 236–246 (1996)
102. van Dommelen, J.A., van der Sande, T.P., Hrapko, M., Peters, G.W.: Mechanical properties of brain tissue by indentation: interregional variation. J. Mech. Behav. Biomed. Mater. 3, 158–166 (2010)
103. Gefen, A., Margulies, S.S.: Are in vivo and in situ brain tissues mechanically similar? J. Biomech. 37, 1339–1352 (2004)
104. Elkin, B.S., Azeloglu, E.U., Costa, K.D., Morrison III, B.: Mechanical heterogeneity of the rat hippocampus measured by AFM indentation. J. Neurotrauma 24, 812–822 (2007)
105. Elkin, B.S., Ilankovan, A., Morrison, III B.: Age-dependent regional mechanical properties of the rat hippocampus and cortex. J. Biomech. Eng. 132, 011010 (2010)
106. Elkin, B.S., Ilankovan, A., Morrison, III B.: A detailed viscoelastic characterization of the P17 and adult rat brain. J. Neurotrauma (2011, in press)
107. Tripathy, S., Berger, E.J.: Measuring viscoelasticity of soft samples using atomic force microscopy. J. Biomech. Eng. 131, 094507 (2009)
108. Neubert, H.K.P.: A simple model representing internal damping in solid materials. Aeronaut. Quart. 14, 187–210 (1963)
109. Schiessel, H., Metzler, R., Blumen, A., Nonnenmacher, T.F.: Generalized viscoelastic models: their fractional equations with solutions. J. Phys. A Math. Gen. 28, 6567–6584 (1995)
110. Harding, J.W., Sneddon, I.N.: The elastic stresses produced by the indentation of the plane surface of a semi-infinite elastic solid by a rigid punch. Proc. Camb. Philol. Soc. 41, 16–26 (1945)
111. Cheng, L., Xia, X., Yu, W., Scriven, L.E., Gerberich, W.W.: Flat-punch indentaiton of viscoelastic material. J. Polym. Sci. B 38, 10–22 (2000)
112. Hayes, W.C., Keer, L.M., Herrmann, G., Mockros, L.F.: A mathematical analysis for indentation tests of articular cartilage. J. Biomech. 5, 541–551 (1972)
113. Lu, Y.B., Franze, K., Seifert, G., Steinhauser, C., Kirchhoff, F., et al.: Viscoelastic properties of individual glial cells and neurons in the CNS. Proc. Natl. Acad. Sci. U.S.A 103, 17759–17764 (2006)
114. Darvish, K.K., Crandall, J.R.: Nonlinear viscoelastic effects in oscillatory shear deformation of brain tissue. Med. Eng. Phys. 23, 633–645 (2001)
115. Donnelly, B.R., Medige, J.: Shear properties of human brain tissue. J. Biomech. Eng. 119, 423–432 (1997)
116. Rivlin, R.S.: Large elastic deformations of isotropic material I fundamental concepts. Philol. Trans. R. Soc. Lond. A 240, 459–490 (1948)
117. Mooney, M.: A theory of large elastic deformation. J. Appl. Phys. 11, 582–592 (1940)
118. Adkins, J.E., Rivlin, R.S.: Large elastic deformations of isotropic materials IX. The deformation of thin shells. Philol. Trans. R. Soc. Lond. A 244, 505–531 (1952)
119. Ogden, R.W.: Large deformation isotropic elasticity—correlation of theory and experiment for compressible rubberlike solids. Proc. R. Soc. Lond. A 328, 567–583 (1972)
120. Gefen, A., Gefen, N., Zhu, Q., Raghupathi, R., Margulies, S.S.: Age-dependent changes in material properties of the brain and braincase of the rat. J. Neurotrauma 20, 1163–1177 (2003)
121. Prange, M.T., Margulies, S.S.: Regional, directional, and age-dependent properties of the brain undergoing large deformation. J. Biomech. Eng. 124, 244–252 (2002)
122. Ting, T.C.T.: Contact stresses between a rigid indenter and a viscoelastic half-space. J. Appl. Mech. 33, 845–854 (1966)
123. Segedin, C.M.: The relationship between load and penetration for a spherical punch. Mathematika 4, 156–161 (1957)
124. Sneddon, I.N.: The relation between load and penetration in the axisymmetric Boussinesq problem for a punch of arbitrary profile. Int. J. Eng. Sci. 3, 47–57 (1965)
125. Mahaffy, R.E., Park, S., Gerde, E., Kas, J., Shih, C.K.: Quantitative analysis of the viscoelastic properties of thin regions of fibroblasts using atomic force microscopy. Biophys. J. 86, 1777–1793 (2004)
126. Mahaffy, R.E., Shih, C.K., MacKintosh, F.C., Kas, J.: Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells. Phys. Rev. Lett. 85, 880–883 (2000)
127. Alcaraz, J., Buscemi, L., Puig-de-Morales, M., Colchero, J., Baro, A., Navajas, D.: Correction of microrheological measurements of soft samples with atomic force microscopy for the hydrodynamic drag on the cantilever. Langmuir 18, 716–721 (2002)
128. Lodge AS. 1964. Elastic Liquids. London: Academic Press
129. Wilhelm, M.: Fourier-transform rheology. Macromol. Mater. Eng. 287, 83–105 (2002)
130. Cho, K.S., Hyun, K., Ahn, K.H., Lee, S.J.: A geometrical interpretation of large amplitude oscillatory shear response. J. Rheol. 49, 747–758 (2005)
131. Ewoldt, R.H., Hosoi, A.E., McKinley, G.H.: New measures for characterizing nonlinear viscoelasticity in large amplitude oscillatory shear. J. Rheol. 52, 1427–1458 (2008)
132. Coats, B., Margulies, S.S.: Material properties of porcine parietal cortex. J. Biomech. 39, 2521–2525 (2006)
133. Thibault, K.L., Margulies, S.S.: Age-dependent material properties of the porcine cerebrum: effect on pediatric inertial head injury criteria. J. Biomech. 31, 1119–1126 (1998)
134. Gillespie, P.G., Muller, U.: Mechanotransduction by hair cells: models, molecules, and mechanisms. Cell 139, 33–44 (2009)
135. Lin, Y.W., Cheng, C.M., Leduc, P.R., Chen, C.C.: Understanding sensory nerve mechanotransduction through localized elastomeric matrix control. PLoS One 4, e4293 (2009)
136. Stabenfeldt, S.E., Garcia, A.J., LaPlaca, M.C.: Thermoreversible laminin-functionalized hydrogel for neural tissue engineering. J. Biomed. Mater. Res. A 77A, 718–725 (2006)
137. Dai, W.G., Belt, J., Saltzman, W.M.: Cell-binding peptides conjugated to poly(ethylene glycol) promote neural cell-aggregation. Bio-Technology 12, 797–801 (1994)
138. Hern, D.L., Hubbell, J.A.: Incorporation of adhesion peptides into nonadhesive hydrogels useful for tissue resurfacing. J. Biomed. Mater. Res. 39, 266–276 (1998)
139. Mahoney, M.J., Anseth, K.S.: Three-dimensional growth and function of neural tissue in degradable polyethylene glycol hydrogels. Biomaterials 27, 2265–2274 (2006)
140. Georges, P.C., Miller, W.J., Meaney, D.F., Sawyer, E.S., Janmey, P.A.: Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys. J. 90, 3012–3018 (2006)
141. Flanagan, L.A., Ju, Y.E., Marg, B., Osterfield, M., Janmey, P.A.: Neurite branching on deformable substrates. Neuroreport 13, 2411–2415 (2002)
142. Guo, W.H., Frey, M.T., Burnham, N.A., Wang, Y.L.: Substrate rigidity regulates the formation and maintenance of tissues. Biophys. J. 90, 2213–2220 (2006)
143. Pelham Jr., R.J., Wang, Y.: Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. U.S.A. 94, 13661–13665 (1997)
144. Engler, A.J., Griffin, M.A., Sen, S., Bonnemann, C.G., Sweeney, H.L., Discher, D.E.: Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell. Biol. 166, 877–887 (2004)
145. Georges, P.C., Janmey, P.A.: Cell type-specific response to growth on soft materials. J. Appl. Physiol. 98, 1547–1553 (2005)
146. Slemmer, J.E., Matser, E.J., de Zeeuw, C.I., Weber, J.T.: Repeated mild injury causes cumulative damage to hippocampal cells. Brain 125, 2699–2709 (2002)
147. Balentine, J.D., Greene, W.B., Bornstein, M.: In vitro spinal cord trauma. Lab. Invest. 58, 93–99 (1988)
148. Regan, R.F., Choi, D.W.: The effect of NMDA, AMPA/kainate, and calcium channel antagonists on traumatic cortical neuronal injury in culture. Brain Res. 633, 236–242 (1994)
149. Cargill, R.S., Thibault, L.E.: Acute alterations in [Ca2 +]i in NG108–15 cells subjected to high strain rate deformation and chemical hypoxia: An in vitro model for neural trauma. J. Neurotrauma 13, 395–407 (1996)
150. Ellis, E.F., McKinney, J.S., Willoughby, K.A., Liang, S., Povlishock, J.T.: A new model for rapid stretch-induced injury of cells in culture: Characterization of the model using astrocytes. J. Neurotrauma 12, 325–339 (1995)
151. LaPlaca, M.C., Thibault, L.E.: An in vitro traumatic injury model to examine the response of neurons to a hydrodynamicaly induced deformation. Ann. Biomed. Eng. 25, 665–677 (1997)
152. Morrison III, B., Meaney, D.F., McIntosh, T.K.: Mechanical characterization of an in vitro device designed to quantitatively injure living brain tissue. Ann. Biomed. Eng. 26, 381–390 (1998)
153. Smith, D.H., Wolf, J.A., Lusardi, T.A., Lee, V.M., Meaney, D.F.: High tolerance and delayed elastic response of cultured axons to dynamic stretch injury. J. Neurosci. 19, 4263– 4269 (1999)
154. Morrison III, B., Cater, H.L., Wang, C.C., Thomas, F.C., Hung, C.T., et al.: A tissue level tolerance criterion for living brain developed with an in vitro model of traumatic mechanical loading. Stapp Car Crash J. 47, 93–105 (2003)
155. Elkin, B.S., Morrison, B.: Region-specific tolerance criteria for the living brain. Stapp Car Crash J. 51, 127–138 (2007)
156. LaPlaca, M.C., Lee, V.M., Thibault, L.E.: An in vitro model of traumatic neuronal injury: loading rate-dependent changes in acute cytosolic calcium and lactate dehydrogenase release. J. Neurotrauma 14, 355–368 (1997)
157. Geddes, D.M., Cargill 2nd, R.S., LaPlaca, M.C.: Mechanical stretch to neurons results in a strain rate and magnitude-dependent increase in plasma membrane permeability. J. Neurotrauma 20, 1039–1049 (2003)
158. Pfister, B.J., Weihs, T.P., Betenbaugh, M., Bao, G.: An in vitro uniaxial stretch model for axonal injury. Ann. Biomed. Eng. 31, 589–598 (2003)
159. Lusardi, T.A., Rangan, J., Sun, D., Smith, D.H., Meaney, D.F.: A device to study the initiation and propagation of calcium transients in cultured neurons after mechanical stretch. Ann. Biomed. Eng. 32, 1546–1558 (2004)
160. Cater, H.L., Sundstrom, L.E., Morrison III, B.: Temporal development of hippocampal cell death is dependent on tissue strain but not strain rate. J. Biomech. 39, 2810–2818 (2006)
161. Bain, A.C., Meaney, D.F.: Tissue-level thresholds for axonal damage in an experimental model of central nervous system white matter injury. J. Biomech. Eng. 122, 615–622 (2000)
162. Galle, B., Ouyang, H., Shi, R., Nauman, E.: Correlations between tissue-level stresses and strains and cellular damage within the guinea pig spinal cord white matter. J. Biomech. 40, 3029–3033 (2007)
163. Barbee, K.A.: Mechanical cell injury. Ann. N. Y. Acad. Sci. 1066, 67–84 (2005)
164. Kumaria, A., Tolias, C.M.: In vitro models of neurotrauma. Br. J. Neurosurg 22, 200–206 (2008)
165. LaPlaca, M.C., Simon, C.M., Prado, G.R., Cullen, D.K.: CNS injury biomechanics and experimental models. Prog. Brain Res. 161, 13–26 (2007)
166. Morrison III, B., Saatman, K.E., Meaney, D.F., McIntosh, T.K.: In vitro central nervous system models of mechanically induced trauma: a review. J. Neurotrauma 15, 911–928 (1998)
167. Geddes, D.M., LaPlaca, M.C., Cargill, R.S.: Susceptibility of hippocampal neurons to mechanically induced injury. Exp. Neurol. 184, 420–427 (2003)
168. Lusardi, T.A., Wolf, J.A., Putt, M.E., Smith, D.H., Meaney, D.F.: Effect of acute calcium influx after mechanical stretch injury in vitro on the viability of hippocampal neurons. J. Neurotrauma 21, 61–72 (2004)
169. Lusardi, T.A., Smith, D.H., Wolf, J.A., Meaney, D.F.: The separate roles of calcium and mechanical forces in mediating cell death in mechanically injured neurons. Biorheology 40, 401–409 (2003)
170. DeRidder, M.N., Simon, M.J., Siman, R., Auberson, Y.P., Raghupathi, R., Meaney, D.F.: Traumatic mechanical injury to the hippocampus in vitro causes regional caspase-3 and calpain activation that is influenced by NMDA receptor subunit composition. Neurobiol. Dis. 22, 165–176 (2006)
171. Geddes-Klein, D.M., Schiffman, K.B., Meaney, D.F.: Mechanisms and consequences of neuronal stretch injury in vitro differ with the model of trauma. J. Neurotrauma 23, 193–204 (2006)
172. Yu, Z., Morrison III, B.: Experimental mild traumatic brain injury induces functional alteration of the developing hippocampus. J. Neurophysiol. 103, 499–510 (2010)
173. Prado, G.R., Ross, J.D., Deweerth, S.P., LaPlaca, M.C.: Mechanical trauma induces immediate changes in neuronal network activity. J. Neural. Eng. 2, 148–158 (2005)