Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Development and plasticity of cortical areas and networks

Key Points

  • The development of cortical layers, areas and networks is mediated by a combination of factors that are present in the cortex and are influenced by thalamic input. So, the specification of cortical areas requires multiple cues that involve the regional and/or graded expression of molecules along with spatial and temporal signals regulated by thalamic afferents.

  • The influence of thalamic inputs has been studied intensively in the formation of thalamocortical patterns and intracortical connections. Most evidence indicates that the presence of activity might be sufficient for the establishment of early thalamic innervation. By contrast, the spatiotemporal pattern of activity often has an instructive role for the development features that develop later, such as the formation of intracortical networks.

  • Experiments that route projections from the retina to the auditory pathway alter the pattern of activity in auditory thalamocortical afferents at a very early stage and reveal the progressive influence of activity on cortical development. So, cortical features such as layers and thalamocortical innervation are unaffected, whereas features that develop later, such as intracortical connections are affected significantly.

Abstract

The development of cortical layers, areas and networks is mediated by a combination of factors that are present in the cortex and are influenced by thalamic input. Electrical activity of thalamocortical afferents has a progressive role in shaping cortex. For early thalamic innervation and patterning, the presence of activity might be sufficient; for features that develop later, such as intracortical networks that mediate emergent responses of cortex, the spatiotemporal pattern of activity often has an instructive role. Experiments that route projections from the retina to the auditory pathway alter the pattern of activity in auditory thalamocortical afferents at a very early stage and reveal the progressive influence of activity on cortical development. Thus, cortical features such as layers and thalamocortical innervation are unaffected, whereas features that develop later, such as intracortical connections, are affected significantly. Surprisingly, the behavioural role of 'rewired' cortex is also influenced profoundly, indicating the importance of patterned activity for this key aspect of cortical function.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Timeline illustrating many of the main events during the development of the visual cortex and its connections with the thalamus in the ferret.
Figure 2: The development of the ferret's visual cortex and its interconnections with the thalamus.
Figure 3: Terminal patterns of subcortical afferents to the dorsal lateral geniculate nucleus and the medial geniculate nucleus in normal ferrets, and to the medial geniculate nucleus in rewired ferrets.
Figure 4: Cortical maps and thalamocortical projections in normal and rewired ferrets.
Figure 5: Orientation maps and horizontal connections in V1 of normal ferrets and in A1 of rewired ferrets.

Similar content being viewed by others

References

  1. Rakic, P. Specification of cerebral cortical areas. Science 241 , 170–176 (1988).

    Article  CAS  PubMed  Google Scholar 

  2. O'Leary, D. D. Do cortical areas emerge from a protocortex? Trends Neurosci. 12, 400–406 (1989).

    CAS  PubMed  Google Scholar 

  3. Angevine, J. B. & Sidman, R. L. Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse . Nature 192, 766–768 (1961).

    PubMed  Google Scholar 

  4. Rakic, P. Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183, 425–427 (1974).

    CAS  PubMed  Google Scholar 

  5. Luskin, M. B. & Shatz, C. J. Neurogenesis of the cat's primary visual cortex. J. Comp. Neurol. 242, 611 –631 (1985).

    CAS  PubMed  Google Scholar 

  6. Luskin, M. B., Pearlman, A. L. & Sanes, J. R. Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron 1, 635–647 ( 1988).

    CAS  PubMed  Google Scholar 

  7. Price, J. & Thurlow, L. Cell lineage in the rat cerebral cortex: a study using retroviral-mediated gene transfer. Development 104, 473–482 ( 1988).

    CAS  PubMed  Google Scholar 

  8. Reid, C. B., Tavazoie, S. F. & Walsh, C. A. Clonal dispersion and evidence for asymmetric cell division in ferret cortex. Development 124, 2441–2450 (1997).

    CAS  PubMed  Google Scholar 

  9. Desai, A. R. & McConnell, S. K. Progressive restriction in fate potential by neural progenitors during cerebral cortical development . Development 127, 2863– 2872 (2000).Cortical layer IV neurons transplanted into an older host where layer II/III cells were being generated resulted in the transplanted cells adopting a layer II/III fate; however, transplantation of layer IV cells into a younger host where layer VI was being generated did not adopt a layer VI fate. This suggests that layer IV neurons are multipotent with respect to production of more superficial layers but cannot be induced to adopt a layer VI fate.

    CAS  PubMed  Google Scholar 

  10. McConnell, S. K. & Kaznowski, C. E. Cell cycle dependence of laminar determination in developing neocortex. Science 254, 282–285 ( 1991).

    CAS  PubMed  Google Scholar 

  11. Eagleson, K. L., Lillien, L., Chan, A. V. & Levitt, P. Mechanisms specifying area fate in cortex include cell-cycle-dependent decisions and the capacity of progenitors to express phenotype memory. Development 124, 1623–1630 (1997).

    CAS  PubMed  Google Scholar 

  12. Dehay, C., Giroud, P., Berland, M., Smart, I. & Kennedy, H. Modulation of the cell cycle contributes to the parcellation of the primate visual cortex. Nature 366, 464–466 (1993).

    CAS  PubMed  Google Scholar 

  13. Polleux, F., Dehay, C., Moraillon, B. & Kennedy, H. Regulation of neuroblast cell-cycle kinetics plays a crucial role in the generation of unique features of neocortical areas. J. Neurosci. 17, 7763–7783 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Dehay, C., Savatier, P., Cortay, V. & Kennedy, H. Cell-cycle kinetics of neocortical precursors are influenced by embryonic thalamic axons. J. Neurosci. 21, 201–214 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Rubenstein, J. L. et al. Genetic control of cortical regionalization and connectivity . Cereb. Cortex 9, 524– 532 (1999).

    CAS  PubMed  Google Scholar 

  16. Barbe, M. F. & Levitt, P. The early commitment of fetal neurons to the limbic cortex. J. Neurosci. 11, 519 –533 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Cohen-Tannoudji, M., Babinet, C. & Wassef, M. Early determination of a mouse somatosensory cortex marker. Nature 368, 460– 463 (1994).

    CAS  PubMed  Google Scholar 

  18. Levitt, P., Eagleson, K. L., Chan, A. V., Ferri, R. T. & Lillien, L. Signaling pathways that regulate specification of neurons in developing cerebral cortex. Dev. Neurosci. 19, 6–8 (1997 ).

    CAS  PubMed  Google Scholar 

  19. Nothias, F., Fishell, G. & Ruiz i Altaba, A. Cooperation of intrinsic and extrinsic signals in the elaboration of regional identity in the posterior cerebral cortex. Curr. Biol. 8, 459–462 ( 1998).

    CAS  PubMed  Google Scholar 

  20. Gitton, Y., Cohen-Tannoudji, M. & Wassef, M. Specification of somatosensory area identity in cortical explants. J. Neurosci. 19, 4889– 4898 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Gaillard, A. & Roger, M. Early commitment of embryonic neocortical cells to develop area-specific thalamic connections. Cereb. Cortex 10, 443–453 ( 2000).Following transplantation, E16 cortical cells form connections with the thalamic nucleus appropriate for their region of origin: occipital cortex transplanted to the parietal region forms connections with the dorsal lateral geniculate nucleus, whereas parietal cortex transplanted to the occipital region connects with the somatosensory thalamus.

    CAS  PubMed  Google Scholar 

  22. Pinaudeau, C., Gaillard, A. & Roger, M. Stage of specification of the spinal cord and tectal projections from cortical grafts. Eur. J. Neurosci. 12, 2486–2496 (2000).

    CAS  PubMed  Google Scholar 

  23. Arimatsu, Y. et al. Early regional specification for a molecular neuronal phenotype in the rat neocortex. Proc. Natl Acad. Sci. USA 89, 8879–8883 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Bulfone, A. et al. T-brain-1: a homolog of Brachyury whose expression defines molecularly distinct domains within the cerebral cortex. Neuron 15, 63–78 ( 1995).

    CAS  PubMed  Google Scholar 

  25. Nakagawa, Y., Johnson, J. E. & O'Leary, D. D. Graded and areal expression patterns of regulatory genes and cadherins in embryonic neocortex independent of thalamocortical input. J. Neurosci. 19, 10877– 10885 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Liu, Q., Dwyer, N. D. & O'Leary, D. D. Differential expression of COUP-TFI, CHL1, and two novel genes in developing neocortex identified by differential display PCR . J. Neurosci. 20, 7682– 7690 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Miyashita-Lin, E. M., Hevner, R., Wassarman, K. M., Martinez, S. & Rubenstein, J. L. Early neocortical regionalization in the absence of thalamic innervation. Science 285 , 906–909 (1999). In Gbx-2 mutant mice, thalamic differentiation is disrupted and thalamic axons do not innervate the cortex. However, the staining patterns of several region-specific markers in the cortex develop normally in these mice, suggesting that factors intrinsic to the neocortex are responsible for the development of these markers of cortical area.

    CAS  PubMed  Google Scholar 

  28. Walther, C. & Gruss, P. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435–1449 (1991).

    CAS  PubMed  Google Scholar 

  29. Stoykova, A. & Gruss, P. Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J. Neurosci. 14, 1395–1412 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Bishop, K. M., Goudreau, G. & O'Leary, D. D. Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science 288, 344– 349 (2000).

    CAS  PubMed  Google Scholar 

  31. Gulisano, M., Broccoli, V., Pardini, C. & Boncinelli, E. Emx1 and Emx2 show different patterns of expression during proliferation and differentiation of the developing cerebral cortex in the mouse. Eur. J. Neurosci. 8, 1037–1050 (1996).

    CAS  PubMed  Google Scholar 

  32. Mallamaci, A. et al. EMX2 protein in the developing mouse brain and olfactory area . Mech. Dev. 77, 165–172 (1998).

    Article  CAS  PubMed  Google Scholar 

  33. Mallamaci, A., Muzio, L., Chan, C. H., Parnavelas, J. & Boncinelli, E. Area identity shifts in the early cerebral cortex of Emx2−/− mutant mice. Nature Neurosci. 3, 679–686 ( 2000).

    CAS  PubMed  Google Scholar 

  34. Donoghue, M. J. & Rakic, P. Molecular evidence for the early specification of presumptive functional domains in the embryonic primate cerebral cortex. J. Neurosci. 19, 5967–5979 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Mackarehtschian, K., Lau, C. K., Caras, I. & McConnell, S. K. Regional differences in the developing cerebral cortex revealed by ephrin-A5 expression . Cereb. Cortex 9, 601– 610 (1999).

    CAS  PubMed  Google Scholar 

  36. Vanderhaeghen, P. et al. A mapping label required for normal scale of body representation in the cortex. Nature Neurosci. 3, 358– 365 (2000).

    CAS  PubMed  Google Scholar 

  37. Huffman, K. J. et al. Formation of cortical fields on a reduced cortical sheet. J. Neurosci. 19, 9939–9952 (1999).Marsupials provide an excellent model for studying cortical development. These animals are born very early in development, before the differentiation of the cortical plate and thalamic innervation. Early cortical ablation reduced the size of the cortical sheet but still resulted in normal spatial relationships between visual, somatosensory and auditory cortices.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Gitton, Y., Cohen-Tannoudji, M. & Wassef, M. Role of thalamic axons in the expression of H-2Z1, a mouse somatosensory cortex specific marker. Cereb. Cortex 9, 611–620 (1999).

    CAS  PubMed  Google Scholar 

  39. Arimatsu, Y., Ishida, M., Takiguchi-Hayashi, K. & Uratani, Y. Cerebral cortical specification by early potential restriction of progenitor cells and later phenotype control of postmitotic neurons. Development 126, 629–638 ( 1999).

    CAS  PubMed  Google Scholar 

  40. Barbe, M. F. & Levitt, P. Attraction of specific thalamic input by cerebral grafts depends on the molecular identity of the implant. Proc. Natl Acad. Sci. USA 89, 3706– 3710 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Schlaggar, B. L. & O'Leary, D. D. Potential of visual cortex to develop an array of functional units unique to somatosensory cortex. Science 252, 1556– 1560 (1991).

    CAS  PubMed  Google Scholar 

  42. Barbe, M. F. & Levitt, P. Age-dependent specification of the corticocortical connections of cerebral grafts. J. Neurosci. 15, 1819–1834 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Rakic, P., Suner, I. & Williams, R. W. A novel cytoarchitectonic area induced experimentally within the primate visual cortex. Proc. Natl Acad. Sci. USA 88, 2083–2087 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Dehay, C., Giroud, P., Berland, M., Killackey, H. & Kennedy, H. Contribution of thalamic input to the specification of cytoarchitectonic cortical fields in the primate: effects of bilateral enucleation in the fetal monkey on the boundaries, dimensions, and gyrification of striate and extrastriate cortex. J. Comp. Neurol. 367, 70–89 (1996).

    CAS  PubMed  Google Scholar 

  45. Windrem, M. S. & Finlay, B. L. Thalamic ablations and neocortical development: alterations of cortical cytoarchitecture and cell number. Cereb. Cortex 1, 230– 240 (1991).

    CAS  PubMed  Google Scholar 

  46. Clasca, F., Angelucci, A. & Sur, M. Layer-specific programs of development in neocortical projection neurons. Proc. Natl Acad. Sci. USA 92, 11145–11149 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Marotte, L. R., Leamey, C. A. & Waite, P. M. Timecourse of development of the wallaby trigeminal pathway: III. Thalamocortical and corticothalamic projections. J. Comp. Neurol. 387, 194–214 (1997).

    CAS  PubMed  Google Scholar 

  48. Rakic, P. Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature 261, 467– 471 (1976).

    CAS  PubMed  Google Scholar 

  49. Crowley, J. C. & Katz, L. C. Early development of ocular dominance columns. Science 290, 1321–1324 (2000).

    CAS  PubMed  Google Scholar 

  50. Crair, M. C., Horton, J. C., Antonini, A. & Stryker, M. P. Emergence of ocular dominance columns in cat visual cortex by 2 weeks of age . J. Comp. Neurol. 430, 235– 249 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Crowley, J. C. & Katz, L. C. Development of ocular dominance columns in the absence of retinal input. Nature Neurosci. 2, 1125–1130 ( 1999).Patchy arbourizations of thalamic afferents, reminiscent of ocular dominance columns, were found to be present in layer IV of the visual cortex in binocularly enucleated ferrets, suggesting that these might be set up by endogenous mechanisms. The actual nature of the relationship of these arbours to normal adult ocular dominance columns remains to be determined.

    CAS  PubMed  Google Scholar 

  52. Crair, M. C., Gillespie, D. C. & Stryker, M. P. The role of visual experience in the development of columns in cat visual cortex. Science 279, 566–570 (1998).The early development of ocular dominance and orientation maps in the visual cortex of cats was found to be independent of visual experience. However, visual experience during the critical period for cortical plasticity was found to be necessary for their maintenance.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Miller, K. D., Keller, J. B. & Stryker, M. P. Ocular dominance column development: analysis and simulation. Science 245, 605– 615 (1989).

    CAS  PubMed  Google Scholar 

  54. Turing, A. M. The chemical basis of morphogenesis. Phil. Trans. R. Soc. Lond. B 237, 23–72 ( 1952).

    Google Scholar 

  55. Galli, L. & Maffei, L. Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science 242 , 90–91 (1988).

    CAS  PubMed  Google Scholar 

  56. Meister, M., Wong, R. O., Baylor, D. A. & Shatz, C. J. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939– 943 (1991).

    CAS  PubMed  Google Scholar 

  57. Mooney, R., Penn, A. A., Gallego, R. & Shatz, C. J. Thalamic relay of spontaneous retinal activity prior to vision. Neuron 17, 863–874 (1996).

    CAS  PubMed  Google Scholar 

  58. Weliky, M. & Katz, L. C. Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo . Science 285, 599– 604 (1999).

    CAS  PubMed  Google Scholar 

  59. Constantine-Paton, M. & Law, M. I. Eye-specific termination bands in tecta of three-eyed frogs. Science 202, 639–641 (1978).

    CAS  PubMed  Google Scholar 

  60. Cline, H. T., Debski, E. A. & Constantine-Paton, M. N-methyl-d-aspartate receptor antagonist desegregates eye-specific stripes. Proc. Natl Acad. Sci. USA 84, 4342–4345 ( 1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Antonini, A. & Stryker, M. P. Rapid remodeling of axonal arbors in the visual cortex. Science 260, 1819– 1821 (1993).

    CAS  PubMed  Google Scholar 

  62. Reiter, H. O. & Stryker, M. P. Neural plasticity without postsynaptic action potentials: less-active inputs become dominant when kitten visual cortical cells are pharmacologically inhibited. Proc. Natl Acad. Sci. USA 85, 3623–3627 ( 1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Hata, Y. & Stryker, M. P. Control of thalamocortical afferent rearrangement by postsynaptic activity in developing visual cortex. Science 265, 1732–1755 ( 1994).

    CAS  PubMed  Google Scholar 

  64. Hata, Y., Tsumoto, T. & Stryker, M. P. Selective pruning of more active afferents when cat visual cortex is pharmacologically inhibited. Neuron 22, 375–381 (1999).

    CAS  PubMed  Google Scholar 

  65. Kirkwood, A., Lee, H. K. & Bear, M. F. Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience. Nature 375, 328–331 ( 1995).

    CAS  PubMed  Google Scholar 

  66. Kirkwood, A., Rioult, M. C. & Bear, M. F. Experience-dependent modification of synaptic plasticity in visual cortex. Nature 381, 526– 528 (1996).

    CAS  PubMed  Google Scholar 

  67. Kleinschmidt, A., Bear, M. F. & Singer, W. Blockade of 'NMDA' receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238, 355–358 (1987).

    CAS  PubMed  Google Scholar 

  68. Miller, K. D., Chapman, B. & Stryker, M. P. Visual responses in adult cat visual cortex depend on N-methyl-d-aspartate receptors. Proc. Natl Acad. Sci. USA 86, 5183–5187 ( 1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Roberts, E. B., Meredith, M. A. & Ramoa, A. S. Suppression of NMDA receptor function using antisense DNA block ocular dominance plasticity while preserving visual responses. J. Neurophysiol. 80, 1021–1032 (1998).

    CAS  PubMed  Google Scholar 

  70. Rossi, F. M., Bozzi, Y., Pizzorusso, T. & Maffei, L. Monocular deprivation decreases brain-derived neurotrophic factor immunoreactivity in the rat visual cortex. Neuroscience 90, 363–368 (1999).

    CAS  PubMed  Google Scholar 

  71. Lein, E. S. & Shatz, C. J. Rapid regulation of brain-derived neurotrophic factor mRNA within eye-specific circuits during ocular dominance column formation. J. Neurosci. 20, 1470– 1483 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Cabelli, R. J., Shelton, D. L., Segal, R. A. & Shatz, C. J. Blockade of endogenous ligands of trkB inhibits formation of ocular dominance columns. Neuron 19, 63– 76 (1997).

    CAS  PubMed  Google Scholar 

  73. McAllister, A. K., Katz, L. C. & Lo, D. C. Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron 18, 767 –778 (1997).

    CAS  PubMed  Google Scholar 

  74. Galuske, R. A., Kim, D. S., Castren, E. & Singer, W. Differential effects of neurotrophins on ocular dominance plasticity in developing and adult cat visual cortex. Eur. J. Neurosci. 12, 3315 –3330 (2000).

    CAS  PubMed  Google Scholar 

  75. Gao, W. J., Newman, D. E., Wormington, A. B. & Pallas, S. L. Development of inhibitory circuitry in visual and auditory cortex of postnatal ferrets: immunocytochemical localization of GABAergic neurons. J. Comp. Neurol. 409, 261–273 (1999).

    CAS  PubMed  Google Scholar 

  76. Issa, N. P., Trachtenberg, J. T., Chapman, B., Zahs, K. R. & Stryker, M. P. The critical period for ocular dominance plasticity in the ferret's visual cortex. J. Neurosci. 19, 6965–6978 ( 1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Fagiolini, M. & Hensch, T. K. Inhibitory threshold for critical-period activation in primary visual cortex. Nature 404, 183–186 (2000).In transgenic mice lacking an isoform of the synthetic enzyme for the inhibitory neurotransmitter GABA (γ-aminobutyric acid), there is no critical period for sensitivity to monocular deprivation. Using benzodiazepines to enhance inhibition by GABA, this study showed that a threshold level of inhibition is required to trigger a critical period for cortical plasticity.

    CAS  PubMed  Google Scholar 

  78. Benevento, L. A., Bakkum, B. W. & Cohen, R. S. Gamma-aminobutyric acid and somatostatin immunoreactivity in the visual cortex of normal and dark-reared rats. Brain Res. 689, 172–182 ( 1995).

    CAS  PubMed  Google Scholar 

  79. Sala, R. et al. Nerve growth factor and brain-derived neurotrophic factor increase neurotransmitter release in the rat visual cortex. Eur. J. Neurosci. 10, 2185–2191 ( 1998).

    CAS  PubMed  Google Scholar 

  80. Hanover, J. L., Huang, Z. J., Tonegawa, S. & Stryker, M. P. Brain-derived neurotrophic factor overexpression induces precocious critical period in mouse visual cortex. J. Neurosci. 19, RC40 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Huang, Z. J. et al. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98 , 739–755 (1999).

    CAS  PubMed  Google Scholar 

  82. Hensch, T. K. et al. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282, 1504–1508 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Quinlan, E. M., Philpot, B. D., Huganir, R. L. & Bear, M. F. Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nature Neurosci. 2, 352–357 (1999).

    CAS  PubMed  Google Scholar 

  84. Van der Loos, H. & Woolsey, T. A. Somatosensory cortex: structural alterations following early injury to sense organs. Science 179, 395–398 ( 1973).

    CAS  PubMed  Google Scholar 

  85. Crair, M. C. & Malenka, R. C. A critical period for long-term potentiation at thalamocortical synapses. Nature 375 , 325–328 (1995).

    CAS  PubMed  Google Scholar 

  86. Isaac, J. T., Crair, M. C., Nicoll, R. A. & Malenka, R. C. Silent synapses during development of thalamocortical inputs. Neuron 18, 269–280 ( 1997).

    CAS  PubMed  Google Scholar 

  87. Flint, A. C., Maisch, U. S., Weishaupt, J. H., Kriegstein, A. R. & Monyer, H. NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J. Neurosci. 17, 2469–2476 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. 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. 66, 146–152 ( 1992).

    CAS  PubMed  Google Scholar 

  89. 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. 66, 244–250 ( 1992).

    CAS  PubMed  Google Scholar 

  90. Iwasato, T. et al. Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 406, 726– 731 (2000).A cortex-specific deletion of a critical subunit of the NMDA (N-methyl- d -aspartate) receptor has demonstrated that cortical NMDA receptor activity is required for the formation of whisker-related barrels in the somatosensory cortex of mice. Interestingly, presynaptic thalamic axons cluster to form a whisker-related pattern and can undergo structural plasticity in the absence of NMDA receptor activity, although the patterning and boundaries between barrels is not as well defined as in normal animals.

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Fox, K., Sato, H. & Daw, N. The location and function of NMDA receptors in cat and kitten visual cortex . J. Neurosci. 9, 2443– 2454 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Rivadulla, C., Sharma, J. & Sur, M. Specific roles of NMDA and AMPA receptors in direction-selective and spatial phase-selective responses in visual cortex. J. Neurosci. 21, 1710–1719 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Ferster, D. & Miller, K. D. Neural mechanisms of orientation selectivity in the visual cortex. Annu. Rev. Neurosci. 23, 441–471 (2000).

    CAS  PubMed  Google Scholar 

  94. Douglas, R. J. & Martin, K. A. A functional microcircuit for cat visual cortex. J. Physiol. 440 , 735–769 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Somers, D. C., Nelson, S. B. & Sur, M. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 15, 5448–5465 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Wiesel, T. N. & Hubel, D. H. Ordered arrangement of orientation columns in monkeys lacking visual experience. J. Comp. Neurol. 158, 307–318 ( 1974).

    CAS  PubMed  Google Scholar 

  97. Imbert, M. & Buisseret, P. Receptive field characteristics and plastic properties of visual cortical cells in kittens reared with or without visual experience. Exp. Brain Res. 22, 25–36 (1975).

    CAS  PubMed  Google Scholar 

  98. Blakemore, C. & Van Sluyters, R. C. Innate and environmental factors in the development of the kitten's visual cortex. J. Physiol. (Lond.) 248, 663–716 ( 1975).

    CAS  PubMed Central  Google Scholar 

  99. Albus, K. & Wolf, W. Early post-natal development of neuronal function in the kitten's visual cortex: a laminar analysis. J. Physiol. (Lond.) 348, 153–185 (1984).

    CAS  Google Scholar 

  100. Chapman, B. & Stryker, M. P. Development of orientation selectivity in ferret visual cortex and effects of deprivation. J. Neurosci. 13, 5251–5262 ( 1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Pettigrew, J. D. The effect of visual experience on the development of stimulus specificity by kitten cortical neurons. J. Physiol. (Lond.) 237 , 49–74 (1974).

    CAS  Google Scholar 

  102. Sherman, S. M. & Spear, P. D. Organization of visual pathways in normal and visually deprived cats. Physiol. Rev. 62, 738–755 ( 1982).

    CAS  PubMed  Google Scholar 

  103. Fregnac, Y. & Imbert, M. Development of neuronal selectivity in primary visual cortex of cat. Physiol. Rev. 64, 325–434 (1984).

    CAS  PubMed  Google Scholar 

  104. Mower, G. D., Caplan, C. J., Christen, W. G. & Duffy, F. H. Dark rearing prolongs physiological but not anatomical plasticity of the cat visual cortex. J. Comp. Neurol. 235, 448 –466 (1985).

    CAS  PubMed  Google Scholar 

  105. Gilbert, C. D. & Wiesel, T. N. Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex . J. Neurosci. 9, 2432– 2442 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Bonhoeffer, T. & Grinvald, A. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature 353, 429–431 ( 1991).

    CAS  PubMed  Google Scholar 

  107. Coogan, T. A. & Van Essen, D. C. Development of connections within and between areas V1 and V2 of macaque monkeys. J. Comp. Neurol. 372, 327–342 (1996).

    CAS  PubMed  Google Scholar 

  108. Callaway, E. M. & Katz, L. C. Emergence and refinement of clustered horizontal connections in cat striate cortex. J. Neurosci. 10, 1134–1153 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Durack, J. C. & Katz, L. C. Development of horizontal projections in layer 2/3 of ferret visual cortex. Cereb. Cortex 6, 178–183 ( 1996).

    CAS  PubMed  Google Scholar 

  110. Ruthazer, E. S. & Stryker, M. P. The role of activity in the development of long-range horizontal connections in area 17 of the ferret. J. Neurosci. 16, 7253– 7269 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Callaway, E. M. & Katz, L. C. Effects of binocular deprivation on the development of clustered horizontal connections in cat striate cortex. Proc. Natl Acad. Sci. USA 88, 745–749 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Chapman, B., Stryker, M. P. & Bonhoeffer, T. Development of orientation preference maps in ferret primary visual cortex. J. Neurosci. 16, 6443–6453 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Godecke, I., Kim, D. S., Bonhoeffer, T. & Singer, W. Development of orientation preference maps in area 18 of kitten visual cortex . Eur. J. Neurosci. 9, 1754– 1762 (1997).

    CAS  PubMed  Google Scholar 

  114. Kim, D. S. & Bonhoeffer, T. Reverse occlusion leads to a precise restoration of orientation preference maps in visual cortex. Nature 370, 370–372 ( 1994).

    CAS  PubMed  Google Scholar 

  115. Godecke, I. & Bonhoeffer, T. Development of identical orientation maps for two eyes without common visual experience. Nature 379, 251–254 (1996). Normally, the map of orientation-selective cells in V1 is identical for the two eyes. This study used a reverse suture paradigm to show that even when the eyes have never shared visual experience, these maps are identical. This indicates that correlated visual input might not be necessary for the alignment of these maps.

    CAS  PubMed  Google Scholar 

  116. Hubel, D. H. & Wiesel, T. N. Binocular interaction in striate cortex of kittens reared with artificial squint. J. Neurophysiol. 28, 1041–1059 ( 1965).

    CAS  PubMed  Google Scholar 

  117. Crawford, M. L. & von Noorden, G. K. The effects of short-term experimental strabismus on the visual system in Macaca mulatta . Invest. Ophthalmol. Vis. Sci. 18, 496–505 (1979).

    CAS  PubMed  Google Scholar 

  118. Van Sluyters, R. C. & Levitt, F. B. Experimental strabismus in the kitten. J. Neurophysiol. 43, 686–699 (1980).

    CAS  PubMed  Google Scholar 

  119. Shatz, C. J., Lindstrom, S. & Wiesel, T. N. The distribution of afferents representing the right and left eyes in the cat's visual cortex. Brain Res. 131, 103–116 (1977).

    CAS  PubMed  Google Scholar 

  120. Lowel, S. Ocular dominance column development: strabismus changes the spacing of adjacent columns in cat visual cortex. J. Neurosci. 14, 7451–7468 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  121. Lowel, S. & Singer, W. Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science 255, 209–212 ( 1992).

    CAS  PubMed  Google Scholar 

  122. Schmidt, K. E., Kim, D. S., Singer, W., Bonhoeffer, T. & Lowel, S. Functional specificity of long-range intrinsic and interhemispheric connections in the visual cortex of strabismic cats. J. Neurosci. 17, 5480–5492 ( 1997).Rearing kittens with artificial strabismus caused intrinsic horizontal connections in V1, as well as callosal connections, to link neurons with the same eye-dominance and orientation preference. Normally, horizontal connections do not respect eye-dominance columns. So, correlated activity is important for shaping horizontal connections.

    CAS  PubMed  PubMed Central  Google Scholar 

  123. Goodhill, G. J. & Lowel, S. Theory meets experiment: correlated neural activity helps determine ocular dominance column periodicity . Trends Neurosci. 18, 437– 439 (1995).

    CAS  PubMed  Google Scholar 

  124. Stryker, M. P. & Strickland, S. L. Physiological segregation of ocular dominance columns depends on the pattern of afferent electrical activity. Invest. Opthamol. Vis. Sci. 25 , 278 (1984).

    Google Scholar 

  125. Weliky, M. & Katz, L. C. Disruption of orientation tuning in visual cortex by artificially correlated neuronal activity. Nature 386, 680–685 ( 1997).

    CAS  PubMed  Google Scholar 

  126. Goodhill, G. J. Stimulating issues in cortical map development. Trends Neurosci. 20, 375–376 ( 1997).

    CAS  PubMed  Google Scholar 

  127. Blakemore, C. & Cooper, G. F. Development of the brain depends on the visual environment. Nature 228, 477–478 (1970).

    CAS  PubMed  Google Scholar 

  128. Stryker, M. P. & Sherk, H. Modification of cortical orientation selectivity in the cat by restricted visual experience: a reexamination. Science 190, 904– 906 (1975).

    CAS  PubMed  Google Scholar 

  129. Stryker, M. P., Sherk, H., Leventhal, A. G. & Hirsch, H. V. Physiological consequences for the cat's visual cortex of effectively restricting early visual experience with oriented contours. J. Neurophysiol. 41, 896–909 ( 1978).

    CAS  PubMed  Google Scholar 

  130. Sengpiel, F., Stawinski, P. & Bonhoeffer, T. Influence of experience on orientation maps in cat visual cortex. Nature Neurosci. 2, 727– 732 (1999).Optical imaging was used to show that kittens reared in a striped environment consisting of a single orientation had twice as much cortical surface area devoted to the experienced orientation as to the orthogonal one. Thus, visual experience can have an instructive effect on orientation columns.

    CAS  PubMed  Google Scholar 

  131. Linden, D. C., Guillery, R. W. & Cucchiaro, J. The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development. J. Comp. Neurol. 203, 189–211 (1981).

    CAS  PubMed  Google Scholar 

  132. Roe, A. W., Garraghty, P. E. & Sur, M. Terminal arbors of single ON-center and OFF-center X and Y retinal ganglion cell axons within the ferret's lateral geniculate nucleus . J. Comp. Neurol. 288, 208– 242 (1989).

    CAS  PubMed  Google Scholar 

  133. Hahm, J. O., Cramer, K. S. & Sur, M. Pattern formation by retinal afferents in the ferret lateral geniculate nucleus: developmental segregation and the role of N-methyl- d-aspartate receptors. J. Comp. Neurol. 411, 327–345 (1999).

    CAS  PubMed  Google Scholar 

  134. Kudo, M. & Niimi, K. Ascending projections of the inferior colliculus in the cat: an autoradiographic study. J. Comp. Neurol. 191, 545–556 ( 1980).

    CAS  PubMed  Google Scholar 

  135. Winer, J. A. in The Mammalian Auditory Pathway, Neuroanatomy (eds Webster, D. D., Popper, A. N. & Fay, R. R.) 222–409 (Springer, New York, 1982).

    Google Scholar 

  136. Angelucci, A., Clasca, F., Bricolo, E., Cramer, K. S. & Sur, M. Experimentally induced retinal projections to the ferret auditory thalamus: development of clustered eye-specific patterns in a novel target. J. Neurosci. 17, 2040– 2055 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  137. Pallas, S. L. & Sur, M. Morphology of retinal axon arbors induced to arborize in a novel target, the medial geniculate nucleus. II. Comparison with axons from the inferior colliculus. J. Comp. Neurol. 349, 363–376 ( 1994).

    CAS  PubMed  Google Scholar 

  138. Roe, A. W., Hahm, J.-O. & Sur, M. Experimentally induced establishment of visual topography in auditory thalamus. Soc. Neurosci. Abs. 17, 898 (1991).

    Google Scholar 

  139. Roe, A. W., Garraghty, P. E., Esguerra, M. & Sur, M. Experimentally induced visual projections to the auditory thalamus in ferrets: evidence for a W cell pathway. J. Comp. Neurol. 334 , 263–280 (1993).

    CAS  PubMed  Google Scholar 

  140. Roe, A. W., Pallas, S. L., Hahm, J. O. & Sur, M. A map of visual space induced in primary auditory cortex. Science 250, 818–820 (1990).

    CAS  PubMed  Google Scholar 

  141. Andersen, R. A., Knight, P. L. & Merzenich, M. M. The thalamocortical and corticothalamic connections of AI, AII, and the anterior auditory field (AAF) in the cat: evidence for two largely segregated systems of connections. J. Comp. Neurol. 194, 663–701 ( 1980).

    CAS  PubMed  Google Scholar 

  142. McMullen, N. T. & de Venecia, R. K. Thalamocortical patches in auditory neocortex. Brain Res. 620, 317–322 (1993).

    CAS  PubMed  Google Scholar 

  143. Pallas, S. L., Roe, A. W. & Sur, M. Visual projections induced into the auditory pathway of ferrets. I. Novel inputs to primary auditory cortex (AI) from the LP/pulvinar complex and the topography of the MGN-AI projection. J. Comp. Neurol. 298, 50–68 (1990).

    CAS  PubMed  Google Scholar 

  144. Angelucci, A. Experimental Retinal Projections to the Ferret Auditory Thalamus: Morphology, Development and Effects on Cortical Organization Thesis, Massachusetts Institute of Technology (1996).

    Google Scholar 

  145. Roe, A. W., Pallas, S. L., Kwon, Y. H. & Sur, M. Visual projections routed to the auditory pathway in ferrets: receptive fields of visual neurons in primary auditory cortex. J. Neurosci. 12, 3651–3664 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  146. Sharma, J., Angelucci, A. & Sur, M. Induction of visual orientation modules in auditory cortex. Nature 404, 841– 847 (2000).Ferrets in which retinal projections are routed to the auditory pathway develop orientation maps in the 'rewired' primary auditory cortex. Horizontal connections that underlie the map are more patchy and periodic than connections in normal auditory cortex, demonstrating that the pattern of activity in inputs to cortex can shape horizontal connections and the orientation map.

    CAS  PubMed  Google Scholar 

  147. Rao, S. C., Toth, L. J. & Sur, M. Optically imaged maps of orientation preference in primary visual cortex of cats and ferrets. J. Comp. Neurol. 387, 358–370 (1997).

    CAS  PubMed  Google Scholar 

  148. Gao, W. & Pallas, S. L. Cross-modal reorganization of horizontal connectivity in auditory cortex without altering thalamocortical projections. J. Neurosci. 19, 7940– 7950 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  149. von Melchner, L., Pallas, S. L. & Sur, M. Visual behaviour mediated by retinal projections directed to the auditory pathway. Nature 404, 871 –876 (2000).This study shows that the rewired projection from the retina to the auditory pathway can mediate visual behaviour. When light stimuli are presented to the rewired projection, animals respond as if they perceive the stimuli to be visual rather than auditory. Thus, the behavioural role of a cortical area is influenced significantly by the pattern of inputs during development.

    CAS  PubMed  Google Scholar 

  150. Frost, D. O., Boire, D., Gingras, G. & Ptito, M. Surgically created neural pathways mediate visual pattern discrimination. Proc. Natl Acad. Sci. USA 97, 11068–11073 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  151. Swindale, N. V. Brain development: Lightning is always seen, thunder always heard. Curr. Biol. 10, R569–R571 (2000).

    CAS  PubMed  Google Scholar 

  152. Schneider, G. E. Early lesions of superior colliculus: factors affecting the formation of abnormal retinal projections. Brain Behav. Evol. 8, 73–109 (1973).

    CAS  PubMed  Google Scholar 

  153. Devor, M. Neuroplasticity in the sparing or deterioration of function after early olfactory tract lesions. Science 190, 998– 1000 (1975).

    CAS  PubMed  Google Scholar 

  154. Graziadei, P. P., Levine, R. R. & Monti Graziadei, G. A. Plasticity of connections of the olfactory sensory neuron: regeneration into the forebrain following bulbectomy in the neonatal mouse. Neuroscience 4, 713– 727 (1979).

    CAS  PubMed  Google Scholar 

  155. Frost, D. O. Anomalous visual connections to somatosensory and auditory systems following brain lesions in early life. Brain Res. 255, 627–635 (1982).

    CAS  PubMed  Google Scholar 

  156. Frost, D. O. & Metin, C. Induction of functional retinal projections to the somatosensory system. Nature 317, 162–164 (1985).

    CAS  PubMed  Google Scholar 

  157. 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 39, 533–545 (1990).

    CAS  PubMed  Google Scholar 

  158. Sur, M., Garraghty, P. E. & Roe, A. W. Experimentally induced visual projections into auditory thalamus and cortex. Science 242, 1437– 1441 (1988).

    CAS  PubMed  Google Scholar 

  159. Angelucci, A., Clasca, F. & Sur, M. Brainstem inputs to the ferret medial geniculate nucleus and the effect of early deafferentation on novel retinal projections to the auditory thalamus . J. Comp. Neurol. 400, 417– 439 (1998).

    CAS  PubMed  Google Scholar 

  160. Lyckman, A. et al. Do Ephrin-A and EphA serve to compartmentalize visual and auditory structures in the developing thalamus? Soc. Neurosci. Abs. 24, 901 (1999).

    Google Scholar 

  161. Pallas, S. L., Hahm, J. & Sur, M. Morphology of retinal axons induced to arborize in a novel target, the medial geniculate nucleus. I. Comparison with arbors in normal targets. J. Comp. Neurol. 349, 343–362 (1994).

    CAS  PubMed  Google Scholar 

  162. Sur, M., Pallas, S. L. & Roe, A. W. Cross-modal plasticity in cortical development: differentiation and specification of sensory neocortex. Trends Neurosci. 13, 227–233 (1990).

    CAS  PubMed  Google Scholar 

  163. Jackson, C. A., Peduzzi, J. D. & Hickey, T. L. Visual cortex development in the ferret. I. Genesis and migration of visual cortical neurons. J. Neurosci. 9, 1242–1253 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  164. Johnson, J. K. & Casagrande, V. A. Prenatal development of axon outgrowth and connectivity in the ferret visual system . Vis. Neurosci. 10, 117– 130 (1993).

    CAS  PubMed  Google Scholar 

  165. Herrmann, K., Antonini, A. & Shatz, C. J. Ultrastructural evidence for synaptic interactions between thalamocortical axons and subplate neurons. Eur. J. Neurosci. 6, 1729–1742 ( 1994).

    CAS  PubMed  Google Scholar 

  166. Finney, E. M. & Shatz, C. J. Establishment of patterned thalamocortical connections does not require nitric oxide synthase . J. Neurosci. 18, 8826– 8838 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  167. Ruthazer, E. S., Baker, G. E. & Stryker, M. P. Development and organization of ocular dominance bands in primary visual cortex of the sable ferret. J. Comp. Neurol. 407, 151–165 ( 1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  168. Angelucci, A., Sharma, J. & Sur, M. in The Mutable Brain (ed. Kaas, J. H.) 351– 392 (Harwood Academic, Amsterdam, 2000).

    Google Scholar 

Download references

Acknowledgements

We thank Christine Waite for assistance, and Ania Majewska and Atomu Sawatari for their comments on the manuscript. This work was supported by grants from the NIH.

Author information

Authors and Affiliations

Authors

Related links

Related links

DATABASE LINKS

bFGF

Latexin

Tbr-1

Cad6

Cad11

COUP-TF1

CHL1

Gbx2

Mash1

Pax6

Emx2

ephrin-A2

ephrin-A5

BDNF

NR2B

NR2A

ENCYCLOPEDIA OF LIFE SCIENCES

Cerebral cortex development

Cortex plasticity: use-dependent remodelling

Glossary

EPHRINS AND EPH RECEPTORS

Two families of molecules that mediate cell-contact-dependent signalling, and are primarily involved in the generation and maintenance of patterns of cellular organization. They accomplish this goal by the control of repulsion at a boundary or gradient, or by upregulating cell adhesion.

SOMATOSENSORY BARRELS

Discrete functional units present in layer IV of the rat cortex, which process tactile inputs derived from a single whisker.

HEBB'S RULE

“When the axon of cell A excites cell B and repeatedly or persistently takes part in firing it, some growth process or metabolic change takes place in one or both cells so that A's efficiency as one of the cells firing B is increased.”

LONG-TERM POTENTIATION AND DEPRESSION

Long-lasting activity-dependent changes in the efficacy of synaptic transmission.

ORIENTATION SELECTIVITY

Property of visual cortex neurons that allows for the detection of bars and edges within visual images and the encoding of their orientations. As the cortex is organized in columns, neurons that belong to the same column share the same orientation tuning.

RETINAL GANGLION CELLS

The three main classes of retinal ganglion cells in carnivores are: X cells, which have the smallest receptive fields; Y cells, which have larger receptive fields; and W cells, which have heterogeneous properties.

ANISOTROPIC

Medium in which physical properties have different values when measured along axes orientated in different directions.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sur, M., Leamey, C. Development and plasticity of cortical areas and networks. Nat Rev Neurosci 2, 251–262 (2001). https://doi.org/10.1038/35067562

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/35067562

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing