Mechanical forces in cerebral cortical folding: A review of measurements and models

Journal of the Mechanical Behavior of Biomedical Materials

Volumn 29, Issue , 2014, Pages 568-581

  Bayly, P V ^a   Taber, L A ^a   Kroenke, C D ^b  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICAL DATA; CORTICAL FOLDING; CORTICAL SURFACES; INTERNAL TENSION; MECHANICAL BEHAVIOR; MECHANICAL FORCE; MOLECULAR PROCESS; PLAUSIBLE ASSUMPTIONS;

MECHANICAL ENGINEERING; MODELS; NEURONS;

BRAIN;

ARTICLE; AXONAL TENSION; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN GROWTH; CELL MIGRATION; CEREBRAL CORTICAL FOLDING; CORTICAL THICKNESS (BRAIN); DIFFUSION TENSOR IMAGING; FRACTIONAL ANISOTROPY; GLIA CELL; GRAY MATTER; HUMAN; MATHEMATICAL MODEL; MECHANICAL STRESS; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NERVE FIBER; NEUROANATOMY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; TENSION; VISCOELASTICITY; WHITE MATTER;

CEREBRAL CORTEX; HUMANS; MECHANICAL PROCESSES; MODELS, BIOLOGICAL; NEUROBIOLOGY;

EID: 84888135161     PISSN: 17516161     EISSN: 18780180     Source Type: Journal    
DOI: 10.1016/j.jmbbm.2013.02.018     Document Type: Article

References (76)

1. Alford P.W., Taber L.A. Computational study of growth and remodelling in the aortic arch. Computer Methods in Biomechanics and Biomedical Engineering 2008, 11:525-538.
2. Barnette A.R., Neil J.J., Kroenke C.D., Griffith J.L., Epstein A.A., Bayly P.V., Knutsen A.K., Inder T.E. Characterization of brain development in the ferret via MRI. Pediatric Research 2009, 66:80-84.
3. Barron D.H. An experimental analysis of some factors involved in the development of the fissure pattern of the cerebral cortex. Journal of Experimental Zoology 1950, 113:553-581.
4. Basser P.J., Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. Journal of Magnetic Resonance, Series B 1996, 111:209-219.
5. Bayly P.V., Okamoto R.J., Xu G., Shi Y., Taber L.A. A cortical folding model incorporating stress-dependent growth explains gyral wavelengths and stress patterns in the developing brain. Physical Biology 2013, 10(1):016005.
6. Ben Amar M., Goriely A. Growth and instability in elastic tissues. Journal of the Mechanics and Physics of Solids 2005, 53:2284-2319.
7. Biot M.A. Folding instability of a layered viscoelastic medium under compression. Proceedings of the Royal Society of London-Series A: Mathematical, Physical and Engineering Sciences 1957, 242:444-454.
8. Biot M.A. Mechanics of Incremental Deformations; Theory of Elasticity and Viscoelasticity of Initially Stressed Solids and Fluids, Including Thermodynamic Foundations and Applications to Finite Strain 1965, Wiley, New York.
9. Bystron I., Blakemore C., Rakic P. Development of the human cerebral cortex: Boulder Committee revisited. Nature Reviews Neuroscience 2008, 9:110-122.
10. Chada S., Lamoureux P., Buxbaum R.E., Heidemann S.R. Cytomechanics of neurite outgrowth from chick brain neurons. Journal of Cell Science 1997, 110(Pt 10):1179-1186.
11. Chatelin S., Constantinesco A., Willinger R. Fifty years of brain tissue mechanical testing: from in vitro to in vivo investigations. Biorheology 2010, 47:255-276.
12. Chenn A., Walsh C.A. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 2002, 297:365-369.
13. Chklovskii D.B., Schikorski T., Stevens C.F. Wiring optimization in cortical circuits. Neuron 2002, 34:341-347.
14. Csernansky J.G., Gillespie S.K., Dierker D.L., Anticevic A., Wang L., Barch D.M., Van Essen D.C. Symmetric abnormalities in sulcal patterning in schizophrenia. NeuroImage 2008, 43:440-446.
15. Csernansky J.G., Gillespie S.K., Dierker D.L., Anticevic A., Wang L., Barch D.M., Van Essen D.C. Symmetric abnormalities in sulcal patterning in schizophrenia. NeuroImage 2008, 43:440-446.
16. Dennerll T.J., Lamoureux P., Buxbaum R.E., Heidemann S.R. The cytomechanics of axonal elongation and retraction. Journal of Cell Biology 1989, 109:3073-3083.
17. Dervaux J., Ben Amar M. Morphogenesis of growing soft tissues. Physical Review Letters 2008, 101.
18. Dervaux J., Ben Amar M. Buckling condensation in constrained growth. Journal of the Mechanics and Physics of Solids 2011, 59:538-560.
19. Dervaux J., Couder Y., Guedeau-Boudeville M.A., Ben Amar M. Shape transition in artificial tumors: from smooth buckles to singular creases. Physical Review Letters 2011, 107.
20. Dubois J., Benders M., Borradori-Tolsa C., Cachia A., Lazeyras F., Ha-Vinh Leuchter R., Sizonenko S.V., Warfield S.K., Mangin J.F., Huppi P.S. Primary cortical folding in the human newborn: an early marker of later functional development. Brain 2008, 131:2028-2041.
21. Filas B.A., Knutsen A.K., Bayly P.V., Taber L.A. A new method for measuring deformation of folding surfaces during morphogenesis. Journal of Biomechanical Engineering 2008, 130:061010.
22. Filas B.A., Xu G., Taber L.A. Mechanisms of brain morphogenesis. Computer Models in Biomechanics 2013, 337-349. Springer, New York. G.A. Holzapfel, E. Kuhl (Eds.).
23. Goktepe S., Abilez O.J., Parker K.K., Kuhl E. A multiscale model for eccentric and concentric cardiac growth through sarcomerogenesis. Journal of Theoretical Biology 2010, 265:433-442.
24. Goldman P.S., Galkin T.W. Prenatal removal of frontal association cortex in the fetal rhesus monkey: anatomical and functional consequences in postnatal life. Brain Research 1978, 152:451-485.
25. Goriely A., Ben Amar M. Differential growth and instability in elastic shells. Physical Review Letters 2005, 94.
26. Hardan A.Y., Jou R.J., Keshavan M.S., Varma R., Minshew N.J. Increased frontal cortical folding in autism: a preliminary MRI study. Psychiatric Research 2004, 131:263-268.
27. Harris J.M., Whalley H., Yates S., Miller P., Johnstone E.C., Lawrie S.M. Abnormal cortical folding in high-risk individuals: a predictor of the development of schizophrenia?. Biological Psychiatry 2004, 56:182-189.
28. Heidemann S.R., Buxbaum R.E. Tension as a regulator and integrator of axonal growth. Cell Motility and the Cytoskeleton 1990, 17:6-10.
29. Heidemann S.R., Buxbaum R.E. Mechanical tension as a regulator of axonal development. Neurotoxicology 1994, 15:95-107.
30. Herculano-Houzel S., Mota B., Wong P., Kaas J.H. Connectivity-driven white matter scaling and folding in primate cerebral cortex. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:19008-19013.
31. Hofman M.A. On the evolution and geometry of the brain in mammals. Progress in Neurobiology 1989, 32:137-158.
32. Hohlfeld E., Mahadevan L. Unfolding the sulcus. Physical Review Letters 2011, 106.
33. Jespersen S.N., Leigland L.A., Cornea A., Kroenke C.D. Determination of axonal and dendritic orientation distributions within the developing cerebral cortex by diffusion tensor imaging. IEEE Transactions of Medical Imaging 2012, 31:16-32.
34. Jin L., Cai S., Suo Z. Creases in soft tissue generated by growth. EPL (Europhysics Letters) 2011, 95:64002.
35. Joshi H.C., Chu D., Buxbaum R.E., Heidemann S.R. Tension and compression in the cytoskeleton of PC 12 neurites. Journal of Cell Biology 1985, 101:697-705.
36. Knutsen A.K., Kroenke C.D., Chang Y.V., Taber L.A., Bayly P.V. Spatial and temporal variations of cortical growth during gyrogenesis in the developing ferret brain. Cerebral Cortex 2012.
37. Kroenke C.D., Taber E.N., Leigland L.A., Knutsen A.K., Bayly P.V. Regional patterns of cerebral cortical differentiation determined by diffusion tensor MRI. Cerebral Cortex 2009, 19:2916-2929.
38. Kucken M., Newell A.C. Fingerprint formation. Journal of Theoretical Biology 2005, 235:71-83.
39. Le Gros Clark W.E. Deformation patterns in the cerebral cortex. Essays on Growth and Form 1945, 1-22. Oxford University Press, London. W.E. Le Gros Clark, P.B. Medawar (Eds.).
40. Leigland L.A., Kroenke C.D. A comparative analysis of cellular morphological differentiation within the cerebral cortex using diffusion tensor imaging. Neuromethods 2011, 50:329-351.
41. Lin I.E., Taber L.A. A model for stress-induced growth in the developing heart. Journal of Biomechanical Engineering 1995, 117:343-349.
42. Manzini M.C., Walsh C.A. What disorders of cortical development tell us about the cortex: one plus one does not always make two. Current Opinion in Genetics and Development 2011, 21:333-339.
43. Mota B., Herculano-Houzel S. How the cortex gets its folds: an inside-out, connectivity-driven model for the scaling of mammalian cortical folding. Frontiers in. Neuroanatomy 2012, 6:3.
44. Neal J., Takahashi M., Silva M., Tiao G., Walsh C.A., Sheen V.L. Insights into the gyrification of developing ferret brain by magnetic resonance imaging. Journal of Anatomy 2007, 210:66-77.
45. Nie J., Guo L., Li G., Faraco C., Stephen Miller L., Liu T. A computational model of cerebral cortex folding. Journal of Theoretical Biology i 2010, 264:467-478.
46. Nordahl C.W., Dierker D., Mostafavi I., Schumann C.M., Rivera S.M., Amaral D.G., Van Essen D.C. Cortical folding abnormalities in autism revealed by surface-based morphometry. Journal of Neuroscience 2007, 27:11725-11735.
47. Pang T., Atefy R., Sheen V. Malformations of cortical development. Neurologist 2008, 14:181-191.
48. Pavone L., Rizzo R., Dobyns W.B. Clinical manifestations and evaluation of isolated lissencephaly. Child's Nervous System 1993, 9:387-390.
49. Prange M.T., Margulies S.S. Regional, directional, and age-dependent properties of the brain undergoing large deformation. Journal of Biomechanical Engineering 2002, 124:244-252.
50. Prothero J.W., Sundsten J.W. Folding of the cerebral-ortex cortex in mammals-a scaling model. Brain Behavior and Evolution. 1984, 24:152-167.
51. Raghavan R., Lawton W., Ranjan S.R., Viswanathan R.R. A continuum mechanics-based model for cortical growth. Journal of Theoretical Biology 1997, 187:285-296.
52. Rakic P. Specification of cerebral cortical areas. Science 1988, 241:170-176.
53. Rakic P. A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends in Neurosciences 1995, 18:383-388.
54. Ramasubramanian A., Latacha K.S., Benjamin J.M., Voronov D.A., Ravi A., Taber L.A. Computational model for early cardiac looping. Annales of Biomedical Engineering 2006, 34:1655-1669.
55. Reillo I., De Juan Romero C., Garcia-Cabezas M.A., Borrell V. A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cerebral Cortex 2011, 21:1674-1694.
56. Richman D.P., Stewart R.M., Caviness V.S. Microgyria, lissencephaly, and neuron migration to cerebral-cortex - architectonic approach. Neurology 1973, 23:413. -&.
57. Richman D.P., Stewart R.M., Hutchinson J.W., Caviness V.S. Mechanical model of brain convolutional development. Science 1975, 189:18-21.
58. Rodriguez E.K., Hoger A., McCulloch A.D. Stress-dependent finite growth in soft elastic tissues. Journal of Biomechanics 1994, 27:455-467.
59. Sallet P.C., Elkis H., Alves T.M., Oliveira J.R., Sassi E., Campi De Castro C., Busatto G.F., Gattaz W.F. Reduced cortical folding in schizophrenia: an MRI morphometric study. American Journal of Psychiatry 2003, 160:1606-1613.
60. Smart I.H., McSherry G.M. Gyrus formation in the cerebral cortex in the ferret. I. Description of the external changes. Journal of Anatomy 1986, 146:141-152.
61. Smart I.H., McSherry G.M. Gyrus formation in the cerebral cortex of the ferret. II. Description of the internal histological changes. Journal of Anatomy 1986, 147:27-43.
62. Stewart R.M., Caviness V.S., Richman D.P. Lissencephaly and pachygyria-architectonic and topographical analysis. Acta Neuropathologica 1975, 31:1-12.
63. Taber L.A., Chabert S. Theoretical and experimental study of growth and remodeling in the developing heart. Biomechanics and Modeling in Mechanobiology 2002, 1:29-43.
64. Todd P.H. A geometric model for the cortical folding pattern of simple folded brains. Journal of Theoretical Biology 1982, 97:529-538.
65. van Dommelen J.A., van der Sande T.P., Hrapko M., Peters G.W. Mechanical properties of brain tissue by indentation: interregional variation. Journal of the Mechanical Behavior of Biomedical Materials 2010, 3:158-166.
66. Van Essen D.C. A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 1997, 385:313-318.
67. Van Essen D.C., Dierker D., Snyder A.Z., Raichle M.E., Reiss A.L., Korenberg J. Symmetry of cortical folding abnormalities in Williams syndrome revealed by surface-based analyses. Journal of Neuroscience 2006, 26:5470-5483.
68. Van Essen D.C., Dierker D.L., Snyder A.Z., Raichle M.E., Reiss A.L., Korenberg J. Symmetry of cortical folding abnormalities in Williams syndrome revealed by surface-based analyses. Journal of Neuroscience 2006, 26:5470-5483.
69. Varner V.D., Voronov D.A., Taber L.A. Mechanics of head fold formation: investigating tissue-level forces during early development, Development 2010, 37:3801-3811.
70. Welker W. Why does the cortex fissure and fold: a review of determinants of gyri and sulci. Cerebral Cortex: Comparative Structure and Evolution of Cerebral Cortex 1990, 3-136. Plenum Press, New York. E.G. Jones, A. Peters (Eds.).
71. Xu G., Bayly P.V., Taber L.A. Residual stress in the adult mouse brain. Biomechanics and Modeling in Mechanobiology 2009, 8:253-262.
72. Xu G., Knutsen A.K., Dikranian K., Kroenke C.D., Bayly P.V., Taber L.A. Axons pull on the brain, but tension does not drive cortical folding. Journal of Biomechanical Engineering 2010, 132:071013.
73. Yin J., Cao Z., Li C., Sheinman I., Chen X. Stress-driven buckling patterns in spheroidal core/shell structures. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:19132-19135.
74. Zervas M., Walkley S.U. Ferret pyramidal cell dendritogenesis: changes in morphology and ganglioside expression during cortical development. Journal of Comparative Neurology 1999, 413:429-448.
75. Zollner A.M., Buganza Tepole A., Gosain A.K., Kuhl E. Growing skin: tissue expansion in pediatric forehead reconstruction. Biomechanics and Modeling in Mechanobiology 2012, 11:855-867.
76. Zollner A.M., Buganza Tepole A., Kuhl E. On the biomechanics and mechanobiology of growing skin. Journal of Theoretical Biology 2012, 297:166-175.