Skip to main content
PMC home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1997 Dec 29;352(1364):1975–1983. doi: 10.1098/rstb.1997.0183

Axonal processes and neural plasticity. III. Competition for dendrites.

T Elliott 1, C I Howarth 1, N R Shadbolt 1
PMCID: PMC1692164  PMID: 9451744

Abstract

In previous work we have developed a computational framework for topographic map formation and plasticity based on axonal process sprouting and retraction, in which sprouting and retraction are governed by competition for neurotrophic support. Here we show that such an approach can account for certain aspects of the dendritic morphology of cortical maps. In particular, we model the development of ocular dominance columns in the primary visual cortex and show that cortical cells near to column boundaries prefer to elaborate dendritic fields which avoid crossing the boundaries. This emerges as different functional inputs are spatially separated. We predict that afferent segregation occurs before or simultaneously with, but not after, the emergence of dendritic bias. We predict that animals reared with complete but asynchronous stimulation of the optic nerves do not develop a dendritic bias. We suggest that the emergence of a dendritic bias might provide a partial account for the critical period for a response to monocular deprivation. In particular, we predict that animals reared with asynchronous optic nerve stimulation might exhibit an extended critical period. Our results also indicate that the number of synapses supported by cortical cells depends on the intra-ocular image correlations used in our simulations. This suggests that inter-ocular image correlations, and thus strabismic rearing of kittens, may also affect the innervation density.

Full Text

The Full Text of this article is available as a PDF (313.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Antonini A., Stryker M. P. Plasticity of geniculocortical afferents following brief or prolonged monocular occlusion in the cat. J Comp Neurol. 1996 May 20;369(1):64–82. doi: 10.1002/(SICI)1096-9861(19960520)369:1<64::AID-CNE5>3.0.CO;2-I. [DOI] [PubMed] [Google Scholar]
  2. Bear M. F., Colman H. Binocular competition in the control of geniculate cell size depends upon visual cortical N-methyl-D-aspartate receptor activation. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9246–9249. doi: 10.1073/pnas.87.23.9246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bear M. F., Kleinschmidt A., Gu Q. A., Singer W. Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist. J Neurosci. 1990 Mar;10(3):909–925. doi: 10.1523/JNEUROSCI.10-03-00909.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bienenstock E. L., Cooper L. N., Munro P. W. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci. 1982 Jan;2(1):32–48. doi: 10.1523/JNEUROSCI.02-01-00032.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blöchl A., Thoenen H. Characterization of nerve growth factor (NGF) release from hippocampal neurons: evidence for a constitutive and an unconventional sodium-dependent regulated pathway. Eur J Neurosci. 1995 Jun 1;7(6):1220–1228. doi: 10.1111/j.1460-9568.1995.tb01112.x. [DOI] [PubMed] [Google Scholar]
  6. Bozzi Y., Pizzorusso T., Cremisi F., Rossi F. M., Barsacchi G., Maffei L. Monocular deprivation decreases the expression of messenger RNA for brain-derived neurotrophic factor in the rat visual cortex. Neuroscience. 1995 Dec;69(4):1133–1144. doi: 10.1016/0306-4522(95)00321-9. [DOI] [PubMed] [Google Scholar]
  7. Cabelli R. J., Hohn A., Shatz C. J. Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science. 1995 Mar 17;267(5204):1662–1666. doi: 10.1126/science.7886458. [DOI] [PubMed] [Google Scholar]
  8. Campenot R. B. Development of sympathetic neurons in compartmentalized cultures. II. Local control of neurite survival by nerve growth factor. Dev Biol. 1982 Sep;93(1):13–21. doi: 10.1016/0012-1606(82)90233-0. [DOI] [PubMed] [Google Scholar]
  9. Campenot R. B. Development of sympathetic neurons in compartmentalized cultures. Il Local control of neurite growth by nerve growth factor. Dev Biol. 1982 Sep;93(1):1–12. doi: 10.1016/0012-1606(82)90232-9. [DOI] [PubMed] [Google Scholar]
  10. Carmignoto G., Canella R., Candeo P., Comelli M. C., Maffei L. Effects of nerve growth factor on neuronal plasticity of the kitten visual cortex. J Physiol. 1993 May;464:343–360. doi: 10.1113/jphysiol.1993.sp019638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Castrén E., Zafra F., Thoenen H., Lindholm D. Light regulates expression of brain-derived neurotrophic factor mRNA in rat visual cortex. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9444–9448. doi: 10.1073/pnas.89.20.9444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Changeux J. P., Danchin A. Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature. 1976 Dec 23;264(5588):705–712. doi: 10.1038/264705a0. [DOI] [PubMed] [Google Scholar]
  13. Chiaia N. L., Fish S. E., Bauer W. R., Bennett-Clarke C. A., Rhoades R. W. Postnatal blockade of cortical activity by tetrodotoxin does not disrupt the formation of vibrissa-related patterns in the rat's somatosensory cortex. Brain Res Dev Brain Res. 1992 Apr 24;66(2):244–250. doi: 10.1016/0165-3806(92)90086-c. [DOI] [PubMed] [Google Scholar]
  14. Clothiaux E. E., Bear M. F., Cooper L. N. Synaptic plasticity in visual cortex: comparison of theory with experiment. J Neurophysiol. 1991 Nov;66(5):1785–1804. doi: 10.1152/jn.1991.66.5.1785. [DOI] [PubMed] [Google Scholar]
  15. Cohen-Cory S., Fraser S. E. Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature. 1995 Nov 9;378(6553):192–196. doi: 10.1038/378192a0. [DOI] [PubMed] [Google Scholar]
  16. Elliott T., Howarth C. I., Shadbolt N. R. Axonal processes and neural plasticity. II: Adult somatosensory maps. Cereb Cortex. 1996 Nov-Dec;6(6):789–793. doi: 10.1093/cercor/6.6.789. [DOI] [PubMed] [Google Scholar]
  17. Elliott T., Howarth C. I., Shadbolt N. R. Axonal processes and neural plasticity.I: Ocular dominance columns. Cereb Cortex. 1996 Nov-Dec;6(6):781–788. doi: 10.1093/cercor/6.6.781. [DOI] [PubMed] [Google Scholar]
  18. Elliott T., Howarth C. I., Shadbolt N. R. Neural competition and statistical mechanics. Proc Biol Sci. 1996 May 22;263(1370):601–606. doi: 10.1098/rspb.1996.0090. [DOI] [PubMed] [Google Scholar]
  19. Fraser S. E., Perkel D. H. Competitive and positional cues in the patterning of nerve connections. J Neurobiol. 1990 Jan;21(1):51–72. doi: 10.1002/neu.480210105. [DOI] [PubMed] [Google Scholar]
  20. Friedlander M. J., Martin K. A., Wassenhove-McCarthy D. Effects of monocular visual deprivation on geniculocortical innervation of area 18 in cat. J Neurosci. 1991 Oct;11(10):3268–3288. doi: 10.1523/JNEUROSCI.11-10-03268.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Goodhill G. J., Löwel S. Theory meets experiment: correlated neural activity helps determine ocular dominance column periodicity. Trends Neurosci. 1995 Oct;18(10):437–439. doi: 10.1016/0166-2236(95)94490-v. [DOI] [PubMed] [Google Scholar]
  22. Goodhill G. J. Topography and ocular dominance: a model exploring positive correlations. Biol Cybern. 1993;69(2):109–118. doi: 10.1007/BF00226194. [DOI] [PubMed] [Google Scholar]
  23. Gwag B. J., Springer J. E. Activation of NMDA receptors increases brain-derived neurotrophic factor (BDNF) mRNA expression in the hippocampal formation. Neuroreport. 1993 Nov 18;5(2):125–128. doi: 10.1097/00001756-199311180-00007. [DOI] [PubMed] [Google Scholar]
  24. HUBEL D. H., WIESEL T. N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol. 1962 Jan;160:106–154. doi: 10.1113/jphysiol.1962.sp006837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Harris R. M., Woolsey T. A. Morphology of golgi-impregnated neurons in mouse cortical barrels following vibrissae damage at different post-natal ages. Brain Res. 1979 Jan 26;161(1):143–149. doi: 10.1016/0006-8993(79)90201-4. [DOI] [PubMed] [Google Scholar]
  26. Hata Y., Stryker M. P. Control of thalamocortical afferent rearrangement by postsynaptic activity in developing visual cortex. Science. 1994 Sep 16;265(5179):1732–1735. doi: 10.1126/science.8085163. [DOI] [PubMed] [Google Scholar]
  27. Henderson T. A., Woolsey T. A., Jacquin M. F. Infraorbital nerve blockade from birth does not disrupt central trigeminal pattern formation in the rat. Brain Res Dev Brain Res. 1992 Mar 20;66(1):146–152. doi: 10.1016/0165-3806(92)90152-m. [DOI] [PubMed] [Google Scholar]
  28. Hopfield J. J. Neural networks and physical systems with emergent collective computational abilities. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2554–2558. doi: 10.1073/pnas.79.8.2554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hubel D. H., Wiesel T. N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol. 1970 Feb;206(2):419–436. doi: 10.1113/jphysiol.1970.sp009022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Katz L. C., Constantine-Paton M. Relationships between segregated afferents and postsynaptic neurones in the optic tectum of three-eyed frogs. J Neurosci. 1988 Sep;8(9):3160–3180. doi: 10.1523/JNEUROSCI.08-09-03160.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Katz L. C., Gilbert C. D., Wiesel T. N. Local circuits and ocular dominance columns in monkey striate cortex. J Neurosci. 1989 Apr;9(4):1389–1399. doi: 10.1523/JNEUROSCI.09-04-01389.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kleinschmidt A., Bear M. F., Singer W. Blockade of "NMDA" receptors disrupts experience-dependent plasticity of kitten striate cortex. Science. 1987 Oct 16;238(4825):355–358. doi: 10.1126/science.2443978. [DOI] [PubMed] [Google Scholar]
  33. Kossel A., Löwel S., Bolz J. Relationships between dendritic fields and functional architecture in striate cortex of normal and visually deprived cats. J Neurosci. 1995 May;15(5 Pt 2):3913–3926. doi: 10.1523/JNEUROSCI.15-05-03913.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. LeVay S., Stryker M. P., Shatz C. J. Ocular dominance columns and their development in layer IV of the cat's visual cortex: a quantitative study. J Comp Neurol. 1978 May 1;179(1):223–244. doi: 10.1002/cne.901790113. [DOI] [PubMed] [Google Scholar]
  35. LeVay S., Wiesel T. N., Hubel D. H. The development of ocular dominance columns in normal and visually deprived monkeys. J Comp Neurol. 1980 May 1;191(1):1–51. doi: 10.1002/cne.901910102. [DOI] [PubMed] [Google Scholar]
  36. Löwel S. Ocular dominance column development: strabismus changes the spacing of adjacent columns in cat visual cortex. J Neurosci. 1994 Dec;14(12):7451–7468. doi: 10.1523/JNEUROSCI.14-12-07451.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. McAllister A. K., Katz L. C., Lo D. C. Neurotrophin regulation of cortical dendritic growth requires activity. Neuron. 1996 Dec;17(6):1057–1064. doi: 10.1016/s0896-6273(00)80239-1. [DOI] [PubMed] [Google Scholar]
  38. McAllister A. K., Lo D. C., Katz L. C. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron. 1995 Oct;15(4):791–803. doi: 10.1016/0896-6273(95)90171-x. [DOI] [PubMed] [Google Scholar]
  39. Meyer-Franke A., Kaplan M. R., Pfrieger F. W., Barres B. A. Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron. 1995 Oct;15(4):805–819. doi: 10.1016/0896-6273(95)90172-8. [DOI] [PubMed] [Google Scholar]
  40. Montague P. R., Gally J. A., Edelman G. M. Spatial signaling in the development and function of neural connections. Cereb Cortex. 1991 May-Jun;1(3):199–220. doi: 10.1093/cercor/1.3.199. [DOI] [PubMed] [Google Scholar]
  41. Mustari M., Cynader M. Prior strabismus protects kitten cortical neurons from the effects of monocular deprivation. Brain Res. 1981 Apr 27;211(1):165–170. doi: 10.1016/0006-8993(81)90077-9. [DOI] [PubMed] [Google Scholar]
  42. Riddle D. R., Lo D. C., Katz L. C. NT-4-mediated rescue of lateral geniculate neurons from effects of monocular deprivation. Nature. 1995 Nov 9;378(6553):189–191. doi: 10.1038/378189a0. [DOI] [PubMed] [Google Scholar]
  43. Schlaggar B. L., Fox K., O'Leary D. D. Postsynaptic control of plasticity in developing somatosensory cortex. Nature. 1993 Aug 12;364(6438):623–626. doi: 10.1038/364623a0. [DOI] [PubMed] [Google Scholar]
  44. Schoups A. A., Elliott R. C., Friedman W. J., Black I. B. NGF and BDNF are differentially modulated by visual experience in the developing geniculocortical pathway. Brain Res Dev Brain Res. 1995 May 26;86(1-2):326–334. doi: 10.1016/0165-3806(95)00043-d. [DOI] [PubMed] [Google Scholar]
  45. Snider W. D. Nerve growth factor enhances dendritic arborization of sympathetic ganglion cells in developing mammals. J Neurosci. 1988 Jul;8(7):2628–2634. doi: 10.1523/JNEUROSCI.08-07-02628.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Steffen H., Van der Loos H. Early lesions of mouse vibrissal follicles:: their influence on dendrite orientation in the cortical barrelfield. Exp Brain Res. 1980;40(4):419–431. doi: 10.1007/BF00236150. [DOI] [PubMed] [Google Scholar]
  47. Tanaka S. Theory of ocular dominance column formation. Mathematical basis and computer simulation. Biol Cybern. 1991;64(4):263–272. doi: 10.1007/BF00199589. [DOI] [PubMed] [Google Scholar]
  48. Weliky M., Katz L. C. Disruption of orientation tuning in visual cortex by artificially correlated neuronal activity. Nature. 1997 Apr 17;386(6626):680–685. doi: 10.1038/386680a0. [DOI] [PubMed] [Google Scholar]
  49. Welker C. Receptive fields of barrels in the somatosensory neocortex of the rat. J Comp Neurol. 1976 Mar 15;166(2):173–189. doi: 10.1002/cne.901660205. [DOI] [PubMed] [Google Scholar]
  50. Woolsey T. A., Van der Loos H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 1970 Jan 20;17(2):205–242. doi: 10.1016/0006-8993(70)90079-x. [DOI] [PubMed] [Google Scholar]
  51. von der Malsburg C. Development of ocularity domains and growth behaviour of axon terminals. Biol Cybern. 1979 Feb 2;32(1):49–62. doi: 10.1007/BF00337452. [DOI] [PubMed] [Google Scholar]
  52. von der Malsburg C. Self-organization of orientation sensitive cells in the striate cortex. Kybernetik. 1973 Dec 31;14(2):85–100. doi: 10.1007/BF00288907. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES