Development of cortical circuits: Lessons from ocular dominance columns

Nature Reviews Neuroscience

Volumn 3, Issue 1, 2002, Pages 34-42

  Katz, Lawrence C ^a   Crowley, Justin C ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; EYE DOMINANCE; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; RETINA; REVIEW; THALAMUS; VISION; VISUAL CORTEX; VISUAL SYSTEM;

ANIMALS; DOMINANCE, OCULAR; MODELS, BIOLOGICAL; RETINA; THALAMUS; VISUAL CORTEX; VISUAL PATHWAYS; VISUAL PERCEPTION;

FELIS CATUS; MUSTELA;

EID: 0036371004     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn703     Document Type: Article

References (107)

1. Cowan, W. M. in International Review of Physiology, Neurophysiology III (ed. Porter, R.) 149–191 (Univ. Park Press, Baltimore, 1978).
2. Katz, L. C. & Shatz, C. J. Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996).
3. Swindale, N. V. The development of topography in the visual cortex — a review of models. Netw. Comput. Neural Syst. 7, 161–247 (1996).
4. Stryker, M. P. & Harris, W. A. Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. J. Neurosci. 6, 2117–2133 (1986).
5. Erwin, E. & Miller, K. D. Correlation-based development of ocularly matched orientation and ocular dominance maps: determination of required input activities. J. Neurosci. 18, 9870–9895 (1998).
6. Sur, M. & Leamey, C. A. Development and plasticity of cortical areas and networks. Nature Rev. Neurosci. 2, 251–262 (2001).
7. Weliky, M. Correlated neuronal activity and visual cortical development. Neuron 27, 427–430 (2000).
8. Miller, K. D. in Self-Organizing Brain: from Growth Cones to Functional Networks (eds Vanpelt, J. et al.) 303–318 (Elsevier Science, Amsterdam, The Netherlands, 1994).
9. Miller, K. D., Keller, J. B. & Stryker, M. P. Ocular dominance column development: analysis and simulation. Science 245, 605–615 (1989).
10. Constantine-Paton, M., Cline, H. T. & Debski, E. Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annu. Rev. Neurosci. 13, 129–154 (1990).
11. Wong, R. O. The role of spatio-temporal firing patterns in neuronal development of sensory systems. Curr. Opin. Neurobiol. 3, 595–601 (1993).
12. Wiesel, T. N. & Hubel, D. H. Single cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, 1003–1017 (1963).
13. Wiesel, T. N. & Hubel, D. H. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. Neurophysiol. 28, 1029–1040 (1965).
14. Hubel, D. H. & Wiesel, T. N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. (Lond.) 206, 419–436 (1970).
15. Hubel, D. H. & Wiesel, T. N. Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J. Physiol. (Lond.) 160, 106–154 (1962).
16. Hubel, D. H. & Wiesel, T. N. Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J. Neurophysiol. 26, 994–1002 (1963).
17. Wiesel, T. N. & Hubel, D. H. Ordered arrangement of orientation columns in monkeys lacking visual experience. J. Comp. Neurol. 158, 307–318 (1974).
18. Wiesel, T. N. & Hubel, D. H. Extent of recovery from the effects of visual deprivation in kittens. J. Neurophysiol. 28, 1060–1072 (1965).
19. Wiesel, T. N., Hubel, D. H. & Lam, D. M. K. Autoradiographic demonstration of ocular-dominance columns in the monkey striate cortex by means of transneuronal transport. Brain Res. 79, 273–279 (1974).
20. LeVay, S., Hubel, D. H. & Wiesel, T. N. The pattern of ocular dominance columns in macaque visual cortex revealed by a reduced silver stain. J. Comp. Neurol. 159, 559–576 (1975).
21. Hubel, D. H. & Wiesel, T. N. Ferrier lecture. Functional architecture of the macaque monkey visual cortex. Proc. R. Soc. Lond. B 198, 1–59 (1977).
22. LeVay, S., Wiesel, T. N. & Hubel, D. The development of ocular dominance columns in normal and visually deprived monkeys. J. Comp. Neurol. 191, 1–51 (1980).
23. 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. 179, 223–244 (1978).
24. Hubel, D. H., Wiesel, T. N. & LeVay, S. Plasticity of ocular dominance columns in monkey striate cortex. Phil. Trans. R. Soc. Lond. B 278, 377–409 (1977).
25. Wiesel, T. N. & Hubel, D. H. Single cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, 1003–1017 (1963).
26. Von der Malsberg, C. & Willshaw, D. J. A mechanism for producing continuous neural mappings: ocularity dominance stripes and ordered retino-tectal projections. Exp. Brain Res. (Suppl. 1), 463–469 (1976).
27. Swindale, N. V. A model for the formation of ocular dominance stripes. Proc. R. Soc. Lond. B 208, 243–264 (1980).
28. Jones, D. G., Van Sluyters, R. C. & Murphy, K. M. A computational model for the overall pattern of ocular dominance. J. Neurosci. 11, 3794–3808 (1991).
29. Rakic, P. Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature 261, 467–471 (1976).
30. Des Rosiers, M. H. et al. Functional plasticity in the immature striate cortex of the monkey shown by the [14C]deoxyglucose method. Science 200, 447–449 (1978).
31. Horton, J. C. & Hocking, D. R. An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience. J. Neurosci. 16, 1791–1807 (1996).
32. Mastronarde, D. N. Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells. J. Neurophysiol. 49, 303–324 (1983).
33. Maffei, L. & Galli-Resta, L. Correlation in the discharges of neighboring rat retinal ganglion cells during prenatal life. Proc. Natl Acad. Sci. USA 87, 2861–2864 (1990).
34. Galli, L. & Maffei, L. Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science 242, 90–91 (1988).
35. 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
36. Wong, R. O., Meister, M. & Shatz, C. J. Transient period of correlated bursting activity during development of the mammalian retina. Neuron 11, 923–938 (1993).
37. Wong, R. O. L., Chernjavsky, A., Smith, S. J. & Shatz, C. J. Early functional neural networks in the developing retina. Nature 374, 716–718 (1995).
38. Wong, R. O. L. & Oakley, D. M. Changing patterns of spontaneous bursting activity of on and off retinal ganglion cells during development. Neuron 16, 1087–1095 (1996).
39. Penn, A. A., Riquelme, P. A., Feller, M. B. & Shatz, C. J. Competition in retinogeniculate patterning driven by spontaneous activity. Science 279, 2108–2112 (1998).
40. Mooney, R., Penn, A. A., Gallego, R. & Shatz, C. J. Thalamic relay of spontaneous retinal activity prior to vision. Neuron 17, 863–874 (1996).
41. Mooney, R., Madison, D. V. & Shatz, C. J. Enhancement of transmission at the developing retinogeniculate synapse. Neuron 10, 815–825 (1993).
42. Weliky, M. & Katz, L. C. Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo. Science 285, 599–604 (1999).
43. 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).
44. Crowley, J. C. & Katz, L. C. Development of ocular dominance columns in the absence of retinal input. Nature Neurosci. 2, 1125–1130 (1999).
45. Sretavan, D. W. & Shatz, C. J. Prenatal development of retinal ganglion cell axons: segregation into eye-specific layers within the cat’s lateral geniculate nucleus. J. Neurosci. 6, 234–251 (1986).
46. Garraghty, P. E., Shatz, C. J., Sretavan, D. W. & Sur, M. Axon arbors of X and Y retinal ganglion cells are differentially affected by prenatal disruption of binocular inputs. Proc. Natl Acad. Sci. USA 85, 7361–7365 (1988).
47. Garraghty, P. E., Shatz, C. J. & Sur, M. Prenatal disruption of binocular interactions creates novel lamination in the cat’s lateral geniculate nucleus. Vis. Neurosci. 1, 93–102 (1988).
48. 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).
49. Sretavan, D. W., Shatz, C. J. & Stryker, M. P. Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336, 468–471 (1988).
50. Antonini, A. & Stryker, M. P. Development of individual geniculocortical arbors in cat striate cortex and effects of binocular impulse blockade. J. Neurosci. 13, 3549–3573 (1993).
51. Reh, T. A. & Constantine-Paton, M. Eye-specific segregation requires neural activity in three-eyed Rana pipiens. J. Neurosci. 5, 1132–1143 (1985).
52. Frank, E. The influence of neuronal activity on patterns of synaptic connections. Trends Neurosci. 10, 188–190 (1989).
53. Chapman, B. Necessity for afferent activity to maintain eyespecific segregation in ferret lateral geniculate nucleus. Science 287, 2479–2482 (2000).
54. Berardi, N., Pizzorusso, T. & Maffei, L. Critical periods during sensory development. Curr. Opin. Neurobiol. 10, 138–145 (2000).
55. Finney, E. M. & Shatz, C. J. Establishment of patterned thalamocortical connections does not require nitric oxide synthase. J. Neurosci. 18, 8826–8838 (1998).
56. 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).
57. Issa, N. P., Trachtenberg, J. T., Chapman, B., Zahs, K. R. & Stryker, M. P. The critical period for ocular dominance plasticity in ferret visual cortex. J. Neurosci. 19, 6965–6978 (1999).
58. Crowley, J. C. & Katz, L. C. Early development of ocular dominance columns. Science 290, 1321–1324 (2000).
59. Chiu, C. & Weliky, M. Spontaneous activity in developing ferret visual cortex in vivo. J. Neurosci. 21, 8906–8914 (2001).
60. 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).
61. Bear, M. F. & Rittenhouse, C. D. Molecular basis for induction of ocular dominance plasticity. J. Neurobiol. 41, 83–91 (1999).
62. Wiesel, T. N. Postnatal development of the visual cortex and the influence of environment. Nature 299, 583–591 (1982).
63. Purves, D. & LaMantia, A. S. Construction of modular circuits in the mammalian brain. Cold Spring Harb. Symp. Quant. Biol. 55, 445–452 (1990).
64. Purves, D., Riddle, D. R. & LaMantia, A. S. Iterated patterns of brain circuitry (or how the cortex gets its spots). Trends Neurosci. 15, 362–368 (1992).
65. Purves, D., White, L. E. & Riddle, D. R. Is neural development Darwinian? Trends Neurosci. 19, 460–464 (1996).
66. Fregnac, Y. & Imbert, M. Early development of visual cortical cells in normal and dark-reared kittens: relationship between orientation selectivity and ocular dominance. J. Physiol. (Lond.) 278, 27–44 (1978).
67. Fagiolini, M. & Hensch, T. K. Inhibitory threshold for criticalperiod activation in primary visual cortex. Nature 404, 183–186 (2000).
68. Trachtenberg, J. T., Trepel, C. & Stryker, M. P. Rapid extragranular plasticity in the absence of thalamocortical plasticity in the developing primary visual cortex. Science 287, 2029–2032 (2000).
69. Johnson, J. K. & Casagrande, V. A. Prenatal development of axon outgrowth and connectivity in the ferret visual system. Vis. Neurosci. 10, 117–130 (1993).
70. 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).
71. Wong, R. O. L. Retinal waves and visual system development. Annu. Rev. Neurosci. 22, 29–47 (1999).
72. Ghosh, A. Subplate neurons and the patterning of thalamocortial connections. Ciba Found. Symp. 193, 150–172 (1995).
73. Ghosh, A. & Shatz, C. J. Involvement of subplate neurons in the formation of ocular dominance columns. Science 255, 1441–1443 (1992).
74. Katz, L. C., Weliky, M. & Crowley, J. C. in The New Cognitive Neurosciences (ed. Gazzaniga, M. S.) 199–212 (MIT Press, Cambridge, Massachusetts, 1999).
75. Mason, C. A. & Sretavan, D. W. Glia, neurons, and axon pathfinding during optic chiasm development. Curr. Opin. Neurobiol. 7, 647–653 (1997).
76. Meissirel, C., Wikler, K. C., Chalupa, L. M. & Rakic, P. Early divergence of magnocellular and parvocellular functional subsystems in the embryonic primate visual system. Proc. Natl Acad. Sci. USA 94, 5900–5905 (1997).
77. Chalupa, L. M., Meissirel, C. & Lia, B. Specificity of retinal ganglion cell projections in the embryonic rhesus monkey. Perspect. Dev. Neurobiol. 3, 223–231 (1996).
78. Casagrande, V. A. & Condo, G. J. Is binocular competition essential for layer formation in the lateral geniculate nucleus? Brain Behav. Evol. 31, 198–208 (1988).
79. Williams, R. W., Hogan, D. & Garraghty, P. E. Target recognition and visual maps in the thalamus of achiasmatic dogs. Nature 367, 637–639 (1994).
80. Donoghue, M. J. & Rakic, P. Molecular gradients and compartments in the embryonic primate cerebral cortex. Cereb. Cortex 9, 586–600 (1999).
81. Dyck, R. H. & Cynader, M. S. An interdigitated columnar mosaic of cytochrome oxidase, zinc, and neurotransmitterrelated molecules in cat and monkey visual cortex. Proc. Natl Acad. Sci. USA 90, 9066–9069 (1993).
82. Trepel, C., Duffy, K. R., Pegado, V. D. & Murphy, K. M. Patchy distribution of NMDAR1 subunit immunoreactivity in developing visual cortex. J. Neurosci. 18, 3404–3415 (1998).
83. Gordon, J. A. & Stryker, M. P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J. Neurosci. 16, 3274–3286 (1996).
84. Weliky, M. & Katz, L. C. Disruption of orientation tuning in visual cortex by artificially correlated neuronal activity. Nature 386, 680–685 (1997).
85. Constantine-Paton, M. & Law, M. I. Eye-specific termination bands in tecta of three-eyed frogs. Science 202, 639–641 (1978).
86. Constantine-Paton, M. in The Organization of the Cerebral Cortex: Proceedings of a Neurosciences Research Program Colloquium (eds Schmitt, F. O., Worden, F. G., Adelman, G. & Dennis, S. G.) 47–67 (MIT Press, Cambridge, Massachusetts, 1981).
87. Boss, V. C. & Schmidt, J. T. Activity and the formation of ocular dominance patches in dually innervated tectum of goldfish. J. Neurosci. 4, 2891–2905 (1984).
88. 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).
89. Cline, H. T. & Constantine-Paton, M. NMDA receptor antagonists disrupt the retinotectal topographic map. Neuron 3, 413–426 (1989).
90. Law, M. I. & Constantine-Paton, M. Anatomy and physiology of experimentally produced striped tecta. J. Neurosci. 1, 741–759 (1981).
91. Shatz, C. J. Emergence of order in visual system development. Proc. Natl Acad. Sci. USA 93, 602–608 (1996).
92. Catalano, S. M., Robertson, R. T. & Killackey, H. P. Rapid alteration of thalamocortical axon morphology follows peripheral damage in the neonatal rat. Proc. Natl Acad. Sci. USA 92, 2549–2552 (1995).
93. Catalano, S. M., Robertson, R. T. & Killackey, H. P. Individual axon morphology and thalamocortical topography in developing rat somatosensory cortex. J. Comp. Neurol. 367, 36–53 (1996).
94. Agmon, A., Yang, L. T., O’Dowd, D. K. & Jones, E. G. Organized growth of thalamocortical axons from the deep tier of terminations into layer IV of developing mouse barrel cortex. J. Neurosci. 13, 5365–5382 (1993).
95. Senft, S. L. & Woolsey, T. A. Growth of thalamic afferents into mouse barrel cortex. Cereb. Cortex 1, 308–335 (1991).
96. O’Leary, D. M., Borngasser, D. J., Fox, K. & Schlagger, B. L. in Symposium on the Development of the Cerebral Cortex No. 193 (eds Bock, G. R. & Cardew, G.) 214–222 (John Wiley & Sons, Inc., New York, 1995).
97. Chiaia, N. L. et al. Postnatal blockade of cortical activity by tetrodotoxin does not disrupt the formation of vibrissarelated patterns in the rat’s somatosensory cortex. Brain Res. Dev. Brain Res. 66, 244–250 (1992).
98. Chiaia, N. L. et al. Effects of postnatal blockade of cortical activity with tetrodotoxin upon the development and plasticity of vibrissa-related patterns in the somatosensory cortex of hamsters. Somatosens. Mot. Res. 11, 219–228 (1994).
99. Iwasato, T. et al. Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 406, 726–731 (2000).
100. Vassar, R. et al. Topographic organization of sensory projections to the olfactory bulb. Cell 79, 981–991 (1994).
101. Mombaerts, P. et al. Visualizing an olfactory sensory map. Cell 87, 675–686 (1996).
102. Ressler, K. J., Sullivan, S. L. & Buck, L. B. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79, 1245–1255 (1994).
103. Belluscio, L., Gold, G. H., Nemes, A. & Axel, R. Mice deficient in Golf are anosmic. Neuron 20, 69–81 (1998).
104. Lin, D. M. et al. Formation of precise connections in the olfactory bulb occurs in the absence of odorant-evoked neuronal activity. Neuron 26, 69–80 (2000).
105. Bulfone, A. et al. An olfactory sensory map develops in the absence of normal projection neurons or GABAergic interneurons. Neuron 21, 1273–1282 (1998).
106. Zheng, C. et al. Peripheral olfactory projections are differentially affected in mice deficient in a cyclic nucleotidegated channel subunit. Neuron 26, 81–91 (2000).
107. Zhao, H. & Reed, R. R. X inactivation of the OCNC1 channel gene reveals a role for activity-dependent competition in the olfactory system. Cell 104, 651–660 (2001).