Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Mar 14;92(6):1797–1799. doi: 10.1073/pnas.92.6.1797

Use, disuse, and growth of the brain.

R O Wong 1
PMCID: PMC42368  PMID: 7892179

Abstract

It is well known that across species, the relative size of the cortical area representing a particular sensory surface is proportional to how important that sense is for the animal. Furthermore, we are commonly aware of the observation that the loss of one sense, such as sight, appears to lead to an increase in sensitivity of the remaining senses, although the physiological basis for this is not entirely clear. Now, several studies, including that of Zheng and Purves (11), have suggested that the cortical area devoted to a particular sensory system can be modulated by neuronal activity during development. The fact that use, or disuse, of a sensory organ can lead to significant changes in its area of representation in the developing cortex is intriguing and calls for further investigations aimed at understanding the functional significance and the mechanisms underlying these changes. What remains to be determined is whether enhanced "growth" also means enhanced performance by that sensory system and, if so, whether this is the result of selective changes in neuronal connectivity and/or synaptic efficacy. It is too early to tell, but, whatever the outcome, it is refreshing to consider neuronal growth in the light of enhanced neural activity, in parallel to the results of activity deprivation, to which we are more accustomed.

Full text

PDF
1797

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. Development of individual geniculocortical arbors in cat striate cortex and effects of binocular impulse blockade. J Neurosci. 1993 Aug;13(8):3549–3573. doi: 10.1523/JNEUROSCI.13-08-03549.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Asanuma C., Stanfield B. B. Induction of somatic sensory inputs to the lateral geniculate nucleus in congenitally blind mice and in phenotypically normal mice. Neuroscience. 1990;39(3):533–545. doi: 10.1016/0306-4522(90)90241-u. [DOI] [PubMed] [Google Scholar]
  3. Bronchti G., Schönenberger N., Welker E., Van der Loos H. Barrelfield expansion after neonatal eye removal in mice. Neuroreport. 1992 Jun;3(6):489–492. doi: 10.1097/00001756-199206000-00008. [DOI] [PubMed] [Google Scholar]
  4. COOK W. H., WALKER J. H., BARR M. L. A cytological study of transneuronal atrophy in the cat and rabbit. J Comp Neurol. 1951 Apr;94(2):267–291. doi: 10.1002/cne.900940207. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Constantine-Paton M., Cline H. T., Debski E. Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annu Rev Neurosci. 1990;13:129–154. doi: 10.1146/annurev.ne.13.030190.001021. [DOI] [PubMed] [Google Scholar]
  7. Cox S. B., Woolsey T. A., Rovainen C. M. Localized dynamic changes in cortical blood flow with whisker stimulation corresponds to matched vascular and neuronal architecture of rat barrels. J Cereb Blood Flow Metab. 1993 Nov;13(6):899–913. doi: 10.1038/jcbfm.1993.113. [DOI] [PubMed] [Google Scholar]
  8. Dubin M. W., Stark L. A., Archer S. M. A role for action-potential activity in the development of neuronal connections in the kitten retinogeniculate pathway. J Neurosci. 1986 Apr;6(4):1021–1036. doi: 10.1523/JNEUROSCI.06-04-01021.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eysel U. T., Wolfhard U. The effects of partial retinal lesions on activity and size of cells in the dorsal lateral geniculate nucleus. J Comp Neurol. 1984 Oct 20;229(2):301–309. doi: 10.1002/cne.902290214. [DOI] [PubMed] [Google Scholar]
  10. Frostig R. D., Lieke E. E., Ts'o D. Y., Grinvald A. Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6082–6086. doi: 10.1073/pnas.87.16.6082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Goodman C. S., Shatz C. J. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell. 1993 Jan;72 (Suppl):77–98. doi: 10.1016/s0092-8674(05)80030-3. [DOI] [PubMed] [Google Scholar]
  12. Greenough W. T., Chang F. L. Dendritic pattern formation involves both oriented regression and oriented growth in the barrels of mouse somatosensory cortex. Brain Res. 1988 Sep 1;471(1):148–152. doi: 10.1016/0165-3806(88)90160-5. [DOI] [PubMed] [Google Scholar]
  13. Guillery R. W. Quantitative studies of transneuronal atrophy in the dorsal lateral geniculate nucleus of cats and kittens. J Comp Neurol. 1973 Jun 15;149(4):423–438. doi: 10.1002/cne.901490403. [DOI] [PubMed] [Google Scholar]
  14. Guillery R. W., Stelzner D. J. The differential effects of unilateral lid closure upon the monocular and binocular segments of the dorsal lateral geniculate nucleus in the cat. J Comp Neurol. 1970 Aug;139(4):413–421. doi: 10.1002/cne.901390403. [DOI] [PubMed] [Google Scholar]
  15. Harris R. M., Woolsey T. A. Dendritic plasticity in mouse barrel cortex following postnatal vibrissa follicle damage. J Comp Neurol. 1981 Mar 1;196(3):357–376. doi: 10.1002/cne.901960302. [DOI] [PubMed] [Google Scholar]
  16. Hubel D. H., Wiesel T. N. Binocular interaction in striate cortex of kittens reared with artificial squint. J Neurophysiol. 1965 Nov;28(6):1041–1059. doi: 10.1152/jn.1965.28.6.1041. [DOI] [PubMed] [Google Scholar]
  17. Hubel D. H., Wiesel T. N., LeVay S. Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond B Biol Sci. 1977 Apr 26;278(961):377–409. doi: 10.1098/rstb.1977.0050. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Katz L. C. Coordinate activity in retinal and cortical development. Curr Opin Neurobiol. 1993 Feb;3(1):93–99. doi: 10.1016/0959-4388(93)90041-v. [DOI] [PubMed] [Google Scholar]
  20. Keller A., Arissian K., Asanuma H. Synaptic proliferation in the motor cortex of adult cats after long-term thalamic stimulation. J Neurophysiol. 1992 Jul;68(1):295–308. doi: 10.1152/jn.1992.68.1.295. [DOI] [PubMed] [Google Scholar]
  21. Killackey H. P., Belford G. R. The formation of afferent patterns in the somatosensory cortex of the neonatal rat. J Comp Neurol. 1979 Jan 15;183(2):285–303. doi: 10.1002/cne.901830206. [DOI] [PubMed] [Google Scholar]
  22. Kuppermann B. D., Kasamatsu T. Changes in geniculate cell size following brief monocular blockade of retinal activity in kittens. Nature. 1983 Dec 1;306(5942):465–468. doi: 10.1038/306465a0. [DOI] [PubMed] [Google Scholar]
  23. LEVI-MONTALCINI R. The development to the acoustico-vestibular centers in the chick embryo in the absence of the afferent root fibers and of descending fiber tracts. J Comp Neurol. 1949 Oct;91(2):209-41, illust, incl 3 pl. doi: 10.1002/cne.900910204. [DOI] [PubMed] [Google Scholar]
  24. Lachica E. A., Crooks M. W., Casagrande V. A. Effects of monocular deprivation on the morphology of retinogeniculate axon arbors in a primate. J Comp Neurol. 1990 Jun 8;296(2):303–323. doi: 10.1002/cne.902960210. [DOI] [PubMed] [Google Scholar]
  25. Lau K. C., So K. F., Tay D. Effects of visual or light deprivation on the morphology, and the elimination of the transient features during development, of type I retinal ganglion cells in hamsters. J Comp Neurol. 1990 Oct 22;300(4):583–592. doi: 10.1002/cne.903000411. [DOI] [PubMed] [Google Scholar]
  26. Leventhal A. G., Hirsch H. V. Effects of visual deprivation upon the morphology of retinal ganglion cells projecting to the dorsal lateral geniculate nucleus of the cat. J Neurosci. 1983 Feb;3(2):332–344. doi: 10.1523/JNEUROSCI.03-02-00332.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Matthews M. R., Cowan W. M., Powell T. P. Transneuronal cell degeneration in the lateral geniculate nucleus of the macaque monkey. J Anat. 1960 Apr;94(Pt 2):145–169. [PMC free article] [PubMed] [Google Scholar]
  28. Mattson M. P., Dou P., Kater S. B. Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons. J Neurosci. 1988 Jun;8(6):2087–2100. doi: 10.1523/JNEUROSCI.08-06-02087.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mattson M. P. Neurotransmitters in the regulation of neuronal cytoarchitecture. Brain Res. 1988 Apr-Jun;472(2):179–212. doi: 10.1016/0165-0173(88)90020-3. [DOI] [PubMed] [Google Scholar]
  30. McMullen N. T., Goldberger B., Suter C. M., Glaser E. M. Neonatal deafening alters nonpyramidal dendrite orientation in auditory cortex: a computer microscope study in the rabbit. J Comp Neurol. 1988 Jan 1;267(1):92–106. doi: 10.1002/cne.902670107. [DOI] [PubMed] [Google Scholar]
  31. Parks T. N., Jackson H. A developmental gradient of dendritic loss in the avian cochlear nucleus occurring independently of primary afferents. J Comp Neurol. 1984 Aug 10;227(3):459–466. doi: 10.1002/cne.902270315. [DOI] [PubMed] [Google Scholar]
  32. Rauschecker J. P., Tian B., Korte M., Egert U. Crossmodal changes in the somatosensory vibrissa/barrel system of visually deprived animals. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):5063–5067. doi: 10.1073/pnas.89.11.5063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rice F. L., Van der Loos H. Development of the barrels and barrel field in the somatosensory cortex of the mouse. J Comp Neurol. 1977 Feb 15;171(4):545–560. doi: 10.1002/cne.901710408. [DOI] [PubMed] [Google Scholar]
  34. Riddle D. R., Gutierrez G., Zheng D., White L. E., Richards A., Purves D. Differential metabolic and electrical activity in the somatic sensory cortex of juvenile and adult rats. J Neurosci. 1993 Oct;13(10):4193–4213. doi: 10.1523/JNEUROSCI.13-10-04193.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Riddle D., Richards A., Zsuppan F., Purves D. Growth of the rat somatic sensory cortex and its constituent parts during postnatal development. J Neurosci. 1992 Sep;12(9):3509–3524. doi: 10.1523/JNEUROSCI.12-09-03509.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Shatz C. J., Stryker M. P. Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science. 1988 Oct 7;242(4875):87–89. doi: 10.1126/science.3175636. [DOI] [PubMed] [Google Scholar]
  38. Sokoloff L. Relation between physiological function and energy metabolism in the central nervous system. J Neurochem. 1977 Jul;29(1):13–26. doi: 10.1111/j.1471-4159.1977.tb03919.x. [DOI] [PubMed] [Google Scholar]
  39. Sretavan D. W., Shatz C. J., Stryker M. P. Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature. 1988 Dec 1;336(6198):468–471. doi: 10.1038/336468a0. [DOI] [PubMed] [Google Scholar]
  40. Tucci D. L., Rubel E. W. Afferent influences on brain stem auditory nuclei of the chicken: effects of conductive and sensorineural hearing loss on n. magnocellularis. J Comp Neurol. 1985 Aug 22;238(4):371–381. doi: 10.1002/cne.902380402. [DOI] [PubMed] [Google Scholar]
  41. Wong R. O., Herrmann K., Shatz C. J. Remodeling of retinal ganglion cell dendrites in the absence of action potential activity. J Neurobiol. 1991 Oct;22(7):685–697. doi: 10.1002/neu.480220704. [DOI] [PubMed] [Google Scholar]
  42. Wong R. O. The role of spatio-temporal firing patterns in neuronal development of sensory systems. Curr Opin Neurobiol. 1993 Aug;3(4):595–601. doi: 10.1016/0959-4388(93)90061-3. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Zheng D., Purves D. Effects of increased neural activity on brain growth. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):1802–1806. doi: 10.1073/pnas.92.6.1802. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES