Nature Publishing Group, publisher of Nature, and other science journals and reference works
Nature
my account e-alerts subscribe register
   
Wednesday 24 May 2017
Journal Home
Current Issue
AOP
Archive
Download PDF
References
Export citation
Export references
Send to a friend
More articles like this

WARNING: This article category has no been recognised
Nature 385, 313 - 318 (23 January 1997); doi:10.1038/385313a0

A tension-based theory of morphogenesis and compact wiring in the central nervous system

David C. Van Essen

Department of Anatomy and Neurobiology, Washington University School of Medicine, 660 South Euclid Avenue, St Louis, Missouri 63110, USA

Many structural features of the mammalian central nervous system can be explained by a morphogenetic mechanism that involves mechanical tension along axons, dendrites and glial processes. In the cerebral cortex, for example, tension along axons in the white matter can explain how and why the cortex folds in a characteristic species-specific pattern. In the cerebellum, tension along parallel fibres can explain why the cortex is highly elongated but folded like an accordion. By keeping the aggregate length of axonal and dendritic wiring low, tension should contribute to the compactness of neural circuitry throughout the adult brain.

  1. Drury, H. A. & Van Essen, D. C. J. Neurosci (Submitted).
  2. Jouandet, M. et al. J. Cogn. Neurosci. 1, 88−117 (1989).
  3. Welker, W. in Cerebral Cortex (eds Jones, E. G. & Peters, A.) 3−136 (Plenum, 1990).
  4. Ono, M., Kubik, K. S. & Abernathey, C. D. Atlas of the Cerebral Sulci (Thieme, Stuttgart, 1990).
  5. Harrison, R. G. Proc. R. Soc. Lond. B 118, 155−196 (1935).
  6. Bray, D. J. Cell Sci. 37, 391−410 (1979). | PubMed | ChemPort |
  7. Odell, G. M., Oster, G., Alberch, P. & Burnside, B. Dev. Biol. 85, 446−462 (1981). | Article | PubMed | ISI | ChemPort |
  8. Stopak, D. & Harris, A. K. Dev. Biol. 90, 383−398 (1982). | Article | PubMed | ChemPort |
  9. Ingber, D. E. & Folkman, J. in Cell Shape Determinants (ed. Stein, W. D.) 3−31 (Academic, New York, 1989).
  10. Mead, C. & Conway, L. (eds) Introduction to VLSI Systems (Addison-Wesley, Reading, MA, 1978).
  11. Allman, J. & Kaas, J. Brain Res. 76, 247−265 (1974). | Article | PubMed | ChemPort |
  12. Barlow, H. Vision Res. 26, 81−90 (1986). | Article | PubMed | ChemPort |
  13. Cherniak, C. Biol. Cybern. 66, 503−510 (1992). | PubMed | ChemPort |
  14. Cherniak, C. Trends Neurosci. 18, 522−527 (1995). | Article | PubMed | ChemPort |
  15. Cowey A. Q. J. Exp. Psychol. 31, 1−17 (1979). | PubMed | ChemPort |
  16. Mitchison, G. Proc. R. Soc. Lond. B 245, 151−158 (1991). | PubMed | ISI | ChemPort |
  17. Felleman, D. J. & Van Essen, D. C. Cereb. Cortex 1, 1−47 (1991). | PubMed | ChemPort |
  18. Scannell, J., Blakemore, C. & Young, M. J. Neurosci. 15, 1463−1483 (1995). | PubMed | ISI | ChemPort |
  19. Young, M. Nature 358, 152−155 (1992). | Article | PubMed | ISI | ChemPort |
  20. Dehay, C., Giroud, P., Berland, M., Killackey, H. & Kennedy, H. J. Comp. Neurol. 367, 70−89 (1996). | Article | PubMed | ISI | ChemPort |
  21. Toga, A. W., Thompson, P. & Payne, B. A. in Developmental Neuroimaging (ed. Thatcher, R. W.) 15−27 (Academic, San Diego, 1996).
  22. Thompson, D. On Growth and Form (Cambridge Univ. Press, 1917).
  23. Wainwright, S. A. Axis and Circumference. The Cylindrical Shape of Plants and Animals (Harvard Univ. Press, Cambridge, MA, 1988).
  24. Lamoureux, P., Buxbaum, R. E. & Heidemann, S. R. Nature 340, 159−162 (1989). | Article | PubMed | ChemPort |
  25. Dennerll, T., Joshi, H. C., Steel, V. L., Buxbaum, R. E. & Heidemann, S. R. J. Cell Biol. 107, 665−674 (1988). | Article | PubMed | ChemPort |
  26. Lamoureux, P., Zheng, J., Buxbaum, R. E. & Heidemann, S. R. J. Cell Biol. 118, 655−661 (1992). | Article | PubMed | ChemPort |
  27. Burke, R. E. in Handbook of Physiology—The Nervous System (ed. Brooks, V. B.) 345−422 (Am. Phys. Soc., Bethesda, MD, 1981).
  28. Dennerll, T. J., Lamoureuux, P., Buxbaum, R. E. & Heidemann, S. R. J. Cell Biol. 109, 3073−3083 (1989). | Article | PubMed | ChemPort |
  29. Cajal, S. R. Studies on Vertebrate Neurogenesis (Thomas, Springfield, 1960).
  30. Coogan, T. A. & Van Essen, D. C. J. Comp. Neurol. 372, 327−342 (1996). | Article | PubMed | ISI | ChemPort |
  31. Steineke, T. C. S. & Kirby, M. A. Dev. Brain Res. 74, 151−162 (1993). | Article | ChemPort |
  32. Whittaker, V. in Handbook of Neurochemistry Vol 7 (ed. Lajtha, A.) 1−40 (Plenum, New York, 1984). | ChemPort |
  33. Buckminster Fuller, R. Synergetics (MacMillan, New York, 1975).
  34. Morest, D. K. Z. Anat. Entwickl.-Gesch. 128, 290−317 (1969). | ChemPort |
  35. Cajal, S. Histologie du Systeme Nerveux de l'Homme et des Vertebres (Maloine, Paris, 1911).
  36. Sauer, F. C. J. Comp. Neurol. 62, 377−405 (1935). | Article |
  37. Miller, J. D., Peller, D. F., Pattisapu, J. & Parent, A. D. Neurol Res. 9, 193−197 (1987). | PubMed | ChemPort |
  38. Pöll, W., Brock, M., Markakis, E., Winkelmuller, W. & Dietz, H. (eds Brock, M. & Dietz, H.) 188−194 (Springer, Berlin, 1972).
  39. Desmond, M. E. & Jacobson, A. G. Dev. Biol 57, 188−198 (1977). | Article | PubMed | ISI | ChemPort |
  40. Coulombre, A. J. J. Exp. Zool. 133, 211−225 (1956). | Article |
  41. Enlow, D. Facial Growth (Saunders, Philadelphia, 1990).
  42. Hofman, M. A. Prog. Neurobiol. 32, 137−158 (1989). | Article | PubMed | ISI | ChemPort |
  43. Frahm, H., Stephan, H. & Stephan, M. J. Hirnforsch. 23, 375−389 (1982). | PubMed | ISI | ChemPort |
  44. Caviness, V. S. Jr, Takahashi, T. & Nowakowski, R. S. Trends Neurosci. 9, 379−383 (1995).
  45. Finlay, B. L. & Darlington, R. B. Science 268, 1578−1584 (1995). | PubMed | ISI | ChemPort |
  46. Rakic, P. Trends Neurosci. 18, 383−388 (1995). | Article | PubMed | ISI | ChemPort |
  47. LeGrosClark, W. E. in Essays on Growth and Form (eds LeGrosClark, W. E. & Medawar, P. B.) 1−22 (Oxford University Press, London, 1945).
  48. Barron, D. H. J. Exp. Zool. 113, 553−573 (1950). | Article | ISI |
  49. Richman, D. P., Stewart, R. M., Hutchinson, J. W. & Caviness, J. V. S. Science 188, 18−21 (1975).
  50. Goldman-Rakic, P. S. Prog. Brain Res. 53, 3−19 (1980).
  51. Rakic, P. Science 241, 170−176 (1988). | PubMed | ISI | ChemPort |
  52. DeCarlos, J. & O'Leary, D. J. Neurosci. 12, 1194−1211 (1992). | PubMed | ChemPort |
  53. Schwartz, M. L., Rakic, P. & Goldman-Rakic, P. S. Proc. Natl Acad. Sci. USA 88, 1354−1358 (1991). | PubMed | ChemPort |
  54. Auladell, C., Martinez, A., Alcantara, S., Super, H. & Soriano, E. Neuroscience 64, 1091−1103 (1995). | Article | PubMed | ChemPort |
  55. Bok, S. T. Histonomy of the Cerebral Cortex (Elsevier, Amsterdam, 1959).
  56. Drury, H. A. et al. J. Cogn. Neurosci. 8, 1−28 (1996). | PubMed | ISI | ChemPort |
  57. Van Essen, D. C., Newsome, W., Maunsell, J. & Bixby, J. J. Comp. Neurol. 244, 451−480 (1986). | Article | PubMed | ChemPort |
  58. Sereno, A. M. et al. Science 268, 889−893 (1995). | PubMed |
  59. Sousa, A. P. B., Carmen, M., Pinon, G. P., Gattass, R. & Rosa, M. G. P. J. Comp. Neurol. 308, 665−682 (1991). | Article | PubMed | ChemPort |
  60. Tusa, R. J., Rosenquist, A. C. & Palmer, L. A. J. Comp. Neurol. 185, 657−678 (1979). | Article | PubMed | ISI | ChemPort |
  61. Van Essen, D. C., Newsome, W. T. & Maunsell, J. H. R. Vision Res. 24, 429−448 (1984). | Article | PubMed | ChemPort |
  62. Hopfield, J. J. & Tank, D. W. Biol. Cybern. 52, 141−152 (1985). | PubMed | ISI | ChemPort |
  63. Welker, W. I. Arch. Ital. Biol. 128, 87−109 (1990). | PubMed | ChemPort |
  64. Sultan, F. & Braitenberg, V. J. Hirnforsch. 34, 79−92 (1993). | PubMed | ChemPort |
  65. Polyak, S. The Vertebrate System (Univ. Chicago Press, 1957).
  66. Hendrickson, A. E. & Yuodelis, C. Ophthalmology 91, 603−612 (1984). | PubMed | ChemPort |
  67. Kirby, M. A. & Steineke, T. C. Vis. Neurosci. 9, 603−616 (1992). | PubMed | ChemPort |
  68. Stewart, R., Richman, D. & Caviness, J. Acta Neuropth. 31, 1−12 (1975). | ChemPort |
  69. Takada, K., Becker, L. & Chan, F. Clin. Neuropathol. 7, 111−119 (1988). | PubMed | ISI | ChemPort |
  70. Kuida, K. et al. Nature 384, 368−372 (1996). | Article | PubMed | ISI | ChemPort |
  71. Jones, E. G., Coulter, J. D. & Hendry, S. H. C. J. Comp. Neurol. 181, 291−348 (1978). | Article | PubMed | ISI | ChemPort |
  72. Pons, T. P. & Kaas, J. H. J. Comp. Neurol. 248, 313−335 (1986). | Article | PubMed | ChemPort |
  73. Friedman, D. P., Jones, E. G. & Burton, H. J. Comp. Neurol. 192, 21−41 (1980). | Article | PubMed | ChemPort |
  74. Barbas, H. & Pandya, D. N. J. Comp. Neurol. 256, 211−228 (1987). | Article | PubMed | ISI | ChemPort |
  75. Barbas, H. J. Comp. Neurol. 276, 353−375 (1988).
  76. Barbas, H. & Pandya, D. N. J. Comp. Neurol. 286, 353−375 (1989). | Article | PubMed | ISI | ChemPort |
  77. Seltzer, B. & Pandya, D. N. Brain Res. 192, 339−351 (1980). | Article | PubMed | ChemPort |
  78. Galaburda, A. M. & Pandya, D. N. J. Comp. Neurol. 221, 169−184 (1983). | Article | PubMed | ISI | ChemPort |



© 1997 Nature Publishing Group
Privacy Policy