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

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1

    Drury, H. A. & Van Essen, D. C. J. Neurosci (Submitted).

  2. 2

    Jouandet, M. et al. J. Cogn. Neurosci. 1, 88–117 (1989).

    CAS  Article  Google Scholar 

  3. 3

    Welker, W. in Cerebral Cortex (eds Jones, E. G. & Peters, A.) 3–136 (Plenum, 1990).

    Google Scholar 

  4. 4

    Ono, M., Kubik, K. S. & Abernathey, C. D. Atlas of the Cerebral Sulci (Thieme, Stuttgart, 1990).

    Google Scholar 

  5. 5

    Harrison, R. G. Proc. R. Soc. Lond. B 118, 155–196 (1935).

    ADS  Article  Google Scholar 

  6. 6

    Bray, D. J. Cell Sci. 37, 391–410 (1979).

    CAS  Google Scholar 

  7. 7

    Odell, G. M., Oster, G., Alberch, P. & Burnside, B. Dev. Biol. 85, 446–462 (1981).

    CAS  Article  Google Scholar 

  8. 8

    Stopak, D. & Harris, A. K. Dev. Biol. 90, 383–398 (1982).

    CAS  Article  Google Scholar 

  9. 9

    Ingber, D. E. & Folkman, J. in Cell Shape Determinants (ed. Stein, W. D.) 3–31 (Academic, New York, 1989).

    Google Scholar 

  10. 10

    Mead, C. & Conway, L. (eds) Introduction to VLSI Systems (Addison-Wesley, Reading, MA, 1978).

  11. 11

    Allman, J. & Kaas, J. Brain Res. 76, 247–265 (1974).

    CAS  Article  Google Scholar 

  12. 12

    Barlow, H. Vision Res. 26, 81–90 (1986).

    CAS  Article  Google Scholar 

  13. 13

    Cherniak, C. Biol. Cybern. 66, 503–510 (1992).

    CAS  Article  Google Scholar 

  14. 14

    Cherniak, C. Trends Neurosci. 18, 522–527 (1995).

    CAS  Article  Google Scholar 

  15. 15

    Cowey A. Q. J. Exp. Psychol. 31, 1–17 (1979).

    CAS  Article  Google Scholar 

  16. 16

    Mitchison, G. Proc. R. Soc. Lond. B 245, 151–158 (1991).

    ADS  CAS  Article  Google Scholar 

  17. 17

    Felleman, D. J. & Van Essen, D. C. Cereb. Cortex 1, 1–47 (1991).

    CAS  Article  Google Scholar 

  18. 18

    Scannell, J., Blakemore, C. & Young, M. J. Neurosci. 15, 1463–1483 (1995).

    CAS  Article  Google Scholar 

  19. 19

    Young, M. Nature 358, 152–155 (1992).

    ADS  CAS  Article  Google Scholar 

  20. 20

    Dehay, C., Giroud, P., Berland, M., Killackey, H. & Kennedy, H. J. Comp. Neurol. 367, 70–89 (1996).

    CAS  Article  Google Scholar 

  21. 21

    Toga, A. W., Thompson, P. & Payne, B. A. in Developmental Neuroimaging (ed. Thatcher, R. W.) 15–27 (Academic, San Diego, 1996).

    Google Scholar 

  22. 22

    Thompson, D. On Growth and Form (Cambridge Univ. Press, 1917).

    Google Scholar 

  23. 23

    Wainwright, S. A. Axis and Circumference. The Cylindrical Shape of Plants and Animals (Harvard Univ. Press, Cambridge, MA, 1988).

    Google Scholar 

  24. 24

    Lamoureux, P., Buxbaum, R. E. & Heidemann, S. R. Nature 340, 159–162 (1989).

    ADS  CAS  Article  Google Scholar 

  25. 25

    Dennerll, T., Joshi, H. C., Steel, V. L., Buxbaum, R. E. & Heidemann, S. R. J. Cell Biol. 107, 665–674 (1988).

    CAS  Article  Google Scholar 

  26. 26

    Lamoureux, P., Zheng, J., Buxbaum, R. E. & Heidemann, S. R. J. Cell Biol. 118, 655–661 (1992).

    CAS  Article  Google Scholar 

  27. 27

    Burke, R. E. in Handbook of Physiology—The Nervous System (ed. Brooks, V. B.) 345–422 (Am. Phys. Soc., Bethesda, MD, 1981).

    Google Scholar 

  28. 28

    Dennerll, T. J., Lamoureuux, P., Buxbaum, R. E. & Heidemann, S. R. J. Cell Biol. 109, 3073–3083 (1989).

    CAS  Article  Google Scholar 

  29. 29

    Cajal, S. R. Studies on Vertebrate Neurogenesis (Thomas, Springfield, 1960).

    Google Scholar 

  30. 30

    Coogan, T. A. & Van Essen, D. C. J. Comp. Neurol. 372, 327–342 (1996).

    CAS  Article  Google Scholar 

  31. 31

    Steineke, T. C. S. & Kirby, M. A. Dev. Brain Res. 74, 151–162 (1993).

    CAS  Article  Google Scholar 

  32. 32

    Whittaker, V. in Handbook of Neurochemistry Vol 7 (ed. Lajtha, A.) 1–40 (Plenum, New York, 1984).

    Google Scholar 

  33. 33

    Buckminster Fuller, R. Synergetics (MacMillan, New York, 1975).

    Google Scholar 

  34. 34

    Morest, D. K. Z. Anat. Entwickl.-Gesch. 128, 290–317 (1969).

    CAS  Article  Google Scholar 

  35. 35

    Cajal, S. Histologie du Systeme Nerveux de l'Homme et des Vertebres (Maloine, Paris, 1911).

    Google Scholar 

  36. 36

    Sauer, F. C. J. Comp. Neurol. 62, 377–405 (1935).

    Article  Google Scholar 

  37. 37

    Miller, J. D., Peller, D. F., Pattisapu, J. & Parent, A. D. Neurol Res. 9, 193–197 (1987).

    CAS  Article  Google Scholar 

  38. 38

    Pöll, W., Brock, M., Markakis, E., Winkelmuller, W. & Dietz, H. (eds Brock, M. & Dietz, H.) 188–194 (Springer, Berlin, 1972).

  39. 39

    Desmond, M. E. & Jacobson, A. G. Dev. Biol 57, 188–198 (1977).

    CAS  Article  Google Scholar 

  40. 40

    Coulombre, A. J. J. Exp. Zool. 133, 211–225 (1956).

    Article  Google Scholar 

  41. 41

    Enlow, D. Facial Growth (Saunders, Philadelphia, 1990).

    Google Scholar 

  42. 42

    Hofman, M. A. Prog. Neurobiol. 32, 137–158 (1989).

    CAS  Article  Google Scholar 

  43. 43

    Frahm, H., Stephan, H. & Stephan, M. J. Hirnforsch. 23, 375–389 (1982).

    CAS  PubMed  Google Scholar 

  44. 44

    Caviness, V. S. Jr, Takahashi, T. & Nowakowski, R. S. Trends Neurosci. 9, 379–383 (1995).

    Article  Google Scholar 

  45. 45

    Finlay, B. L. & Darlington, R. B. Science 268, 1578–1584 (1995).

    ADS  CAS  Article  Google Scholar 

  46. 46

    Rakic, P. Trends Neurosci. 18, 383–388 (1995).

    CAS  Article  Google Scholar 

  47. 47

    LeGrosClark, W. E. in Essays on Growth and Form (eds LeGrosClark, W. E. & Medawar, P. B.) 1–22 (Oxford University Press, London, 1945).

    Google Scholar 

  48. 48

    Barron, D. H. J. Exp. Zool. 113, 553–573 (1950).

    Article  Google Scholar 

  49. 49

    Richman, D. P., Stewart, R. M., Hutchinson, J. W. & Caviness, J. V. S. Science 188, 18–21 (1975).

    ADS  Google Scholar 

  50. 50

    Goldman-Rakic, P. S. Prog. Brain Res. 53, 3–19 (1980).

    Article  Google Scholar 

  51. 51

    Rakic, P. Science 241, 170–176 (1988).

    ADS  CAS  Article  Google Scholar 

  52. 52

    DeCarlos, J. & O'Leary, D. J. Neurosci. 12, 1194–1211 (1992).

    CAS  Article  Google Scholar 

  53. 53

    Schwartz, M. L., Rakic, P. & Goldman-Rakic, P. S. Proc. Natl Acad. Sci. USA 88, 1354–1358 (1991).

    ADS  CAS  Article  Google Scholar 

  54. 54

    Auladell, C., Martinez, A., Alcantara, S., Super, H. & Soriano, E. Neuroscience 64, 1091–1103 (1995).

    CAS  Article  Google Scholar 

  55. 55

    Bok, S. T. Histonomy of the Cerebral Cortex (Elsevier, Amsterdam, 1959).

    Google Scholar 

  56. 56

    Drury, H. A. et al. J. Cogn. Neurosci. 8, 1–28 (1996).

    CAS  Article  Google Scholar 

  57. 57

    Van Essen, D. C., Newsome, W., Maunsell, J. & Bixby, J. J. Comp. Neurol. 244, 451–480 (1986).

    CAS  Article  Google Scholar 

  58. 58

    Sereno, A. M. et al. Science 268, 889–893 (1995).

    ADS  CAS  Article  Google Scholar 

  59. 59

    Sousa, A. P. B., Carmen, M., Pinon, G. P., Gattass, R. & Rosa, M. G. P. J. Comp. Neurol. 308, 665–682 (1991).

    CAS  Article  Google Scholar 

  60. 60

    Tusa, R. J., Rosenquist, A. C. & Palmer, L. A. J. Comp. Neurol. 185, 657–678 (1979).

    CAS  Article  Google Scholar 

  61. 61

    Van Essen, D. C., Newsome, W. T. & Maunsell, J. H. R. Vision Res. 24, 429–448 (1984).

    CAS  Article  Google Scholar 

  62. 62

    Hopfield, J. J. & Tank, D. W. Biol. Cybern. 52, 141–152 (1985).

    CAS  PubMed  Google Scholar 

  63. 63

    Welker, W. I. Arch. Ital. Biol. 128, 87–109 (1990).

    CAS  PubMed  Google Scholar 

  64. 64

    Sultan, F. & Braitenberg, V. J. Hirnforsch. 34, 79–92 (1993).

    CAS  PubMed  Google Scholar 

  65. 65

    Polyak, S. The Vertebrate System (Univ. Chicago Press, 1957).

    Google Scholar 

  66. 66

    Hendrickson, A. E. & Yuodelis, C. Ophthalmology 91, 603–612 (1984).

    CAS  Article  Google Scholar 

  67. 67

    Kirby, M. A. & Steineke, T. C. Vis. Neurosci. 9, 603–616 (1992).

    CAS  Article  Google Scholar 

  68. 68

    Stewart, R., Richman, D. & Caviness, J. Acta Neuropth. 31, 1–12 (1975).

    CAS  Article  Google Scholar 

  69. 69

    Takada, K., Becker, L. & Chan, F. Clin. Neuropathol. 7, 111–119 (1988).

    PubMed  Google Scholar 

  70. 70

    Kuida, K. et al. Nature 384, 368–372 (1996).

    ADS  CAS  Article  Google Scholar 

  71. 71

    Jones, E. G., Coulter, J. D. & Hendry, S. H. C. J. Comp. Neurol. 181, 291–348 (1978).

    CAS  Article  Google Scholar 

  72. 72

    Pons, T. P. & Kaas, J. H. J. Comp. Neurol. 248, 313–335 (1986).

    CAS  Article  Google Scholar 

  73. 73

    Friedman, D. P., Jones, E. G. & Burton, H. J. Comp. Neurol. 192, 21–41 (1980).

    CAS  Article  Google Scholar 

  74. 74

    Barbas, H. & Pandya, D. N. J. Comp. Neurol. 256, 211–228 (1987).

    CAS  Article  Google Scholar 

  75. 75

    Barbas, H. J. Comp. Neurol. 276, 353–375 (1988).

    Article  Google Scholar 

  76. 76

    Barbas, H. & Pandya, D. N. J. Comp. Neurol. 286, 353–375 (1989).

    CAS  Article  Google Scholar 

  77. 77

    Seltzer, B. & Pandya, D. N. Brain Res. 192, 339–351 (1980).

    CAS  Article  Google Scholar 

  78. 78

    Galaburda, A. M. & Pandya, D. N. J. Comp. Neurol. 221, 169–184 (1983).

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Essen, D. A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385, 313–318 (1997). https://doi.org/10.1038/385313a0

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.