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Canadian Association of Neurosciences Review: Postnatal Development of the Mammalian Neocortex: Role of Activity Revisited

Published online by Cambridge University Press:  02 December 2014

Zhong-wei Zhang
Zhong-wei Zhang*
Affiliation:
Centre de recherche Université Laval Robert-Giffard, Department of Psychiatry, Laval University School of Medicine, Québec, QC
*
Centre de recherche Université Laval Robert-Giffard, 2601, de la canardière, F-6500, Quebec, QC G1J 2G3, Canada.
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Abstract:

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The mammalian neocortex is the largest structure in the brain, and plays a key role in brain function. A critical period for the development of the neocortex is the early postnatal life, when the majority of synapses are formed and when much of synaptic remodeling takes place. Early studies suggest that initial synaptic connections lack precision, and this rudimentary wiring pattern is refined by experience-related activity through selective elimination and consolidation. This view has been challenged by recent studies revealing the presence of a relatively precise pattern of connections before the onset of sensory experience. The recent data support a model in which specificity of neuronal connections is largely determined by genetic factors. Spontaneous activity is required for the formation of neural circuits, but whether it plays an instructive role is still controversial. Neurotransmitters including acetylcholine, serotonin, and γ-Aminobutyric acid (GABA) may have key roles in the regulation of spontaneous activity, and in the maturation of synapses in the developing brain.

Résumé:

RÉSUMÉ:

Le néocortex des mammifères est la plus grosse structure du cerveau et il joue un rôle stratégique dans la function cérébrale. La période postnatale est critique pour son développement. La majorité des synapses se forment à ce moment-là ainsi qu’une grande partie du remodelage synaptique. Plusieurs études ont suggéré que les connections synaptiques initiales manquent de précision et que ce « câblage » rudimentaire du cerveau est raffiné par l’activité reliée à l’expérience, par élimination et consolidation sélective. Cette notion a été remise en question parce que des études récentes ont démontré la présence de motifs relativement précis de connections avant le début de l’expérience sensorielle. Les données récentes sont en faveur d’un modèle où la spécificité des connections neuronales est déterminée en grande partie par des facteurs génétiques. L’activité spontanée est requise pour la formation de circuits neuraux, mais son rôle informatif demeure controversé. Des neurotransmetteurs comme l’acétylcholine, la sérotonine et l’acide g-aminobutyrique (GABA) pourraient jouer un rôle important dans la régulation de l’activité spontanée et dans la maturation des synapses du cerveau en développement.

Type
Review Article
Information
Canadian Journal of Neurological Sciences , Volume 33 , Issue 2 , May 2006 , pp. 158 - 169
Copyright
Copyright © The Canadian Journal of Neurological 2006

References

1. Wong, RO, Meister, M, Shatz, CJ. Transient period of correlated bursting activity during development of the mammalian retina. Neuron. 1993;11:923–38.Google Scholar
2. Penn, AA, Riquelme, PA, Feller, MB, Shatz, CJ. Competition in retinogeniculate patterning driven by spontaneous activity. Science. 1998;279:2108–12.CrossRefGoogle ScholarPubMed
3. Wong, RO, Chernjavsky, A, Smith, SJ, Shatz, CJ. Early functional neural networks in the developing retina. Nature. 1995;374:716–8.Google Scholar
4. Douglas, RJ, Martin, KA. Neuronal circuits of the neocortex. Annu Rev Neurosci. 2004;27:419–51.Google Scholar
5. Katz, LC, Shatz, CJ. Synaptic activity and the construction of cortical circuits. Science. 1996;274:1133–8.Google Scholar
6. Hubel, DH, Wiesel, TN. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol. (Lond) 1970;206:419–36.Google Scholar
7. Wiesel, TN, Hubel, DH. Extent of recovery from the effects of visual deprivation in kittens. J Neurophysiol. 1965;28:1060–72.Google Scholar
8. Wiesel, TN. Postnatal development of the visual cortex and the influence of environment. Nature. 1982;299:583–91.Google Scholar
9. Webb, SJ, Monk, CS, Nelson, CA. Mechanisms of postnatal neurobiological development: implications for human development. Dev Neuropsychol. 2001;19:147–71.Google Scholar
10. Levitt, P. Structural and functional maturation of the developing primate brain. J Pediatr. 2003;143:S35–45.CrossRefGoogle ScholarPubMed
11. Thomson, AM, Bannister, AP. Interlaminar connections in the neocortex. Cereb Cortex. 2003;13:5–14.Google Scholar
12. Zhu, JJ. Maturation of layer 5 neocortical pyramidal neurons: amplifying salient layer 1 and layer 4 inputs by Ca2+ action potentials in adult rat tuft dendrites. J Physiol. 2000;526(Pt 3): 571–87.CrossRefGoogle ScholarPubMed
13. Zhang, ZW. Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. J Neurophysiol. 2004;91:1171–82.Google Scholar
14. Franceschetti, S, Sancini, G, Panzica, F, Radici, C, Avanzini, G. Postnatal differentiation of firing properties and morphological characteristics in layer V pyramidal neurons of the sensorimotor cortex. Neuroscience. 1998;83:1013–24.Google Scholar
15. Van Eden, CG, Uylings, HB. Postnatal volumetric development of the prefrontal cortex in the rat. J Comp Neurol. 1985;241:268–74.Google Scholar
16. Kim, HG, Fox, K, Connors, BW. Properties of excitatory synaptic events in neurons of primary somatosensory cortex of neonatal rats. Cereb Cortex. 1995;5:148–57.Google Scholar
17. Micheva, KD, Beaulieu, C. Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry. J Comp Neurol. 1996;373:340–54.Google Scholar
18. LeVay, S, Stryker, MP, Shatz, CJ. Ocular dominance columns and their development in layer IV of the cat’s visual cortex: a quantitative study. J Comp Neurol. 1978;179:223–44.Google Scholar
19. LeVay, S, Wiesel, TN, Hubel, DH. The development of ocular dominance columns in normal and visually deprived monkeys. J Comp Neurol. 1980;191:1–51.Google Scholar
20. Shatz, CJ, Stryker, MP. Ocular dominance in layer IV of the cat’s visual cortex and the effects of monocular deprivation. J Physiol. 1978;281:267–83.Google Scholar
21. Rakic, P. Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature. 1976;261:467–71.Google Scholar
22. Horton, JC, Hocking, DR. An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience. J Neurosci. 1996;16:1791–807.CrossRefGoogle ScholarPubMed
23. Des Rosiers, MH, Sakurada, O, Jehle, J, Shinohara, M, Kennedy, C, Sokoloff, L. Functional plasticity in the immature striate cortex of the monkey shown by the [14C]deoxyglucose method. Science. 1978;200:447–9.Google Scholar
24. Crowley, JC, Katz, LC. Early development of ocular dominance columns [In Process Citation]. Science. 2000;290:1321–4.Google Scholar
25. Crair, MC, Gillespie, DC, Stryker, MP. The role of visual experience in the development of columns in cat visual cortex. Science. 1998;279:566–70.Google Scholar
26. Crair, MC, Horton, JC, Antonini, A, Stryker, MP. Emergence of ocular dominance columns in cat visual cortex by 2 weeks of age. J Comp Neurol. 2001;430:235–49.Google Scholar
27. Katz, LC, Crowley, JC. Development of cortical circuits: lessons from ocular dominance columns. Nat Rev Neurosci. 2002;3:34–42.Google Scholar
28. Crowley, JC, Katz, LC. Ocular dominance development revisited. Curr Opin Neurobiol. 2002;12:104–9.Google Scholar
29. Shatz, CJ. The prenatal development of the cat’s retinogeniculate pathway. J Neurosci. 1983;3:482–99.Google Scholar
30. Rakic, P. Development of visual centers in the primate brain depends on binocular competition before birth. Science. 1981;214:928–31.Google Scholar
31. Shatz, CJ, Stryker, MP. Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science. 1988;242:87–9.Google Scholar
32. Wong, RO. Retinal waves and visual system development. Annu Rev Neurosci. 1999;22:29–47.Google Scholar
33. Meister, M, Wong, RO, Baylor, DA, Shatz, CJ. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science. 1991;252:939–43.Google Scholar
34. McLaughlin, T, Torborg, CL, Feller, MB, O’Leary, DD. Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron. 2003;40:1147–60.Google Scholar
35. Stellwagen, D, Shatz, CJ. An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron. 2002;33:357–67.Google Scholar
36. Huberman, AD, Wang, GY, Liets, LC, Collins, OA, Chapman, B, Chalupa, LM. Eye-specific retinogeniculate segregation independent of normal neuronal activity. Science. 2003;300:994–8.Google Scholar
37. Borodinsky, LN, Root, CM, Cronin, JA, Sann, SB, Gu, X, Spitzer, NC. Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature. 2004;429:523–30.Google Scholar
38. Spitzer, NC, Root, CM, Borodinsky, LN. Orchestrating neuronal differentiation: patterns of Ca2+ spikes specify transmitter choice. Trends Neurosci. 2004;27:415–21.Google Scholar
39. Hanson, MG, Landmesser, LT. Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules. Neuron. 2004;43, 687–701.Google Scholar
40. Yuste, R, Nelson, DA, Rubin, WW, Katz, LC. Neuronal domains in developing neocortex: mechanisms of coactivation. Neuron. 1995;14:7–17.Google Scholar
41. Yuste, R, Peinado, A, Katz, LC. Neuronal domains in developing neocortex. Science. 1992;257:665–9.CrossRefGoogle ScholarPubMed
42. Feller, MB, Wellis, DP, Stellwagen, D, Werblin, FS, Shatz, CJ. Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science. 1996;272:1182–7.Google Scholar
43. Stellwagen, D, Shatz, C J, Feller, MB. Dynamics of retinal waves are controlled by cyclic AMP. Neuron. 1999;24:673–85.Google Scholar
44. Mesulam, MM, Mufson, EJ, Wainer, BH, Levey, AI. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience. 1983;10:1185–201.Google Scholar
45. Mesulam, MM, Mufson, EJ, Levey, AI, Wainer, BH. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol. 1983;214:170–97.Google Scholar
46. Mechawar, N, Descarries, L. The cholinergic innervation develops early and rapidly in the rat cerebral cortex: a quantitative immunocytochemical study. Neuroscience. 2001;108:555–67.Google Scholar
47. Hohmann, CF, Potter, ED, Levey, AI. Development of muscarinic receptor subtypes in the forebrain of the mouse. J Comp Neurol. 1995;358:88–101.Google Scholar
48. Zoli, M, Le Novere, N, Hill, JA Jr., Changeux, JP. Developmental regulation of nicotinic ACh receptor subunit mRNAs in the rat central and peripheral nervous systems. J Neurosci. 1995;15:1912–39.Google Scholar
49. Peinado, A. Traveling slow waves of neural activity: a novel form of network activity in developing neocortex. J Neurosci. 2000;20:RC54.Google Scholar
50. Aghajanian, GK, Sanders-Bush, E. In: Neupsychopharmacology The Fifth Generation of Progess. KL Davis, DC, JT Cole, C Nemeroff Editors. Philadelphia: Lippincott Williams and Wilkins; 2002. p. 15–34.Google Scholar
51. Lauder, JM, Bloom, FE. Ontogeny of monoamine neurons in the locus coeruleus, Raphe nuclei and substantia nigra of the rat. I. Cell differentiation. J Comp Neurol. 1974;155:469–81.Google Scholar
52. Lauder, JM, Bloom, FE. Ontogeny of monoamine neurons in the locus coeruleus, raphe nuclei and substantia nigra of the rat. II. Synaptogenesis. J Comp Neurol. 1975;163:251–64.Google Scholar
53. Dori, I, Dinopoulos, A, Blue, ME, Parnavelas, JG. Regional differences in the ontogeny of the serotonergic projection to the cerebral cortex. Exp Neurol. 1996;138:1–14.Google Scholar
54. Hohmann, CF, Hamon, R, Batshaw, ML, Coyle, JT. Transient postnatal elevation of serotonin levels in mouse neocortex. Brain Res. 1988;471:163–6.Google Scholar
55. Hedner, J, Lundell, KH, Breese, GR, Mueller, RA, Hedner, T. Developmental variations in CSF monoamine metabolites during childhood. Biol Neonate. 1986;49:190–7.Google Scholar
56. Toth, G, Fekete, M. 5-Hydroxyindole acetic excretion in newborns, infants and children. Acta Paediatr Hung. 1986;27:221–6.Google Scholar
57. Mansour-Robaey, S, Mechawar, N, Radja, F, Beaulieu, C, Descarries, L. Quantified distribution of serotonin transporter and receptors during the postnatal development of the rat barrel field cortex. Brain Res Dev Brain Res. 1998;107:159–63.Google Scholar
58. Roth, BL, Hamblin, MW, Ciaranello, RD. Developmental regulation of 5-HT2 and 5-HT1c mRNA and receptor levels. Brain Res Dev Brain Res. 1991;58:51–8.Google Scholar
59. Claustre, Y, Rouquier, L, Scatton, B. Pharmacological characterization of serotonin-stimulated phosphoinositide turnover in brain regions of the immature rat. J Pharmacol Exp Ther. 1988;244:1051–6.Google Scholar
60. Azmitia, EC. Modern views on an ancient chemical: serotonin effects on cell proliferation, maturation, and apoptosis. Brain Res Bull. 2001;56:413–24.CrossRefGoogle Scholar
61. Sodhi, MS, Sanders-Bush, E. Serotonin and brain development. Int Rev Neurobiol. 2004;59:111–74.Google Scholar
62. Lauder, JM. Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci. 1993;16:233–40.Google Scholar
63. Cases, O, Seif, I, Grimsby, J, Gaspar, P, Chen, K, Pournin, S, et al. Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science. 1995;268:1763–6.Google Scholar
64. Cases, O, Vitalis, T, Seif, I, De Maeyer, E, Sotelo, C, Gaspar, P. Lack of barrels in the somatosensory cortex of monoamine oxidase A-deficient mice: role of a serotonin excess during the critical period. Neuron. 1996;16:297–307.Google Scholar
65. Brunner, HG, Nelen, M, Breakefield, XO, Ropers, HH, van Oost, BA. Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science. 1993; 262:578–80.Google Scholar
66. Heisler, LK, Chu, HM, Brennan, TJ, Danao, JA, Bajwa, P, Parsons, LH, et al. Elevated anxiety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice. Proc Natl Acad Sci USA. 1998;95:15049–54.Google Scholar
67. Parks, CL, Robinson, PS, Sibille, E, Shenk, T, Toth, M. Increased anxiety of mice lacking the serotonin1A receptor. Proc Natl Acad Sci USA. 1998;95:10734–9.Google Scholar
68. Ramboz, S, Oosting, R, Amara, DA, Kung, HF, Blier, P, Mendelsohn, M, et al. Serotonin receptor 1A knockout: an animal model of anxiety-related disorder. Proc Natl Acad Sci USA. 1998;95:14476–81.Google Scholar
69. Gross, C, Zhuang, X, Stark, K, Ramboz, S, Oosting, R, Kirby, L, et al. Serotonin1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature. 2002; 416:396–400.Google Scholar
70. Ansorge, MS, Zhou, M, Lira, A, Hen, R, Gingrich, JA. Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science. 2004;306:879–81.Google Scholar
71. Kojic, L, Dyck, RH, Gu, Q, Douglas, RM, Matsubara, J, Cynader, MS. Columnar distribution of serotonin-dependent plasticity within kitten striate cortex. Proc Natl Acad Sci USA. 2000;97:1841–4.Google Scholar
72. Kojic, L, Gu, Q, Douglas, RM, Cynader, MS. Serotonin facilitates synaptic plasticity in kitten visual cortex: an in vitro study. Brain Res Dev Brain Res. 1997;101:299–304.Google Scholar
73. Edagawa, Y, Saito, H, Abe, K. Endogenous serotonin contributes to a developmental decrease in long-term potentiation in the rat visual cortex. J Neurosci. 2001;21:1532–7.Google Scholar
74. Bennett-Clarke, CA, Leslie, M J, Chiaia, NL, Rhoades, RW. Serotonin 1B receptors in the developing somatosensory and visual cortices are located on thalamocortical axons. Proc Natl Acad Sci USA. 1993;90:153–7.Google Scholar
75. Salichon, N, Gaspar, P, Upton, AL, Picaud, S, Hanoun, N, Hamon, M, et al. Excessive activation of serotonin (5-HT) 1B receptors disrupts the formation of sensory maps in monoamine oxidase a and 5-ht transporter knock-out mice. J Neurosci. 2001;21:884–96.Google Scholar
76. Zhang, ZW. Serotonin induces tonic firing in layer V pyramidal neurons of rat prefrontal cortex during postnatal development. J Neurosci. 2003;23:3373–84.CrossRefGoogle Scholar
77. Beique, JC, Campbell, B, Perring, P, Hamblin, MW, Walker, P, Mladenovic, L, et al. Serotonergic regulation of membrane potential in developing rat prefrontal cortex: coordinated expression of 5-hydroxytryptamine (5-HT)1A, 5-HT2A, and 5-HT7 receptors. J Neurosci. 2004;24:4807–17.Google Scholar
78. Fuster, JM. The prefrontal cortex and its relation to behavior. Prog Brain Res. 1991;87:201–11.Google Scholar
79. Goldman-Rakic, PS. Cellular and circuit basis of working memory in prefrontal cortex of nonhuman primates. Prog Brain Res. 1990;85:325–35. discussion 335-6.Google Scholar
80. Goldman-Rakic, PS. Working memory dysfunction in schizophrenia. J Neuropsychiatry Clin Neurosci. 1994;6:348–57.Google Scholar
81. Lewis, DA, Levitt, P. Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci. 2002;25:409–32.Google Scholar
82. Jones, EG. Cortical development and thalamic pathology in schizophrenia. Schizophr Bull. 1997;23:483–501.CrossRefGoogle ScholarPubMed
83. Egan, MF, Weinberger, DR. Neurobiology of schizophrenia. Curr Opin Neurobiol. 1997;7:701–7.Google Scholar
84. Cherubini, E, Gaiarsa, JL, Ben-Ari, Y. GABA: an excitatory transmitter in early postnatal life. Trends Neurosci. 1991;14:515–9.Google Scholar
85. Ben-Ari, Y. Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci. 2002;3:728–39.Google Scholar
86. Ben-Ari, Y, Cherubini, E, Corradetti, R, Gaiarsa, JL. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol. 1989;416:303–25.Google Scholar
87. Kandler, K, Friauf, E. Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. J Neurosci. 1995;15:6890–904.Google Scholar
88. Rohrbough, J, Spitzer, NC. Regulation of intracellular Cl- levels by Na(+)-dependent Cl- cotransport distinguishes depolarizing from hyperpolarizing GABAA receptor-mediated responses in spinal neurons. J Neurosci. 1996;16:82–91.Google Scholar
89. Rivera, C, Voipio, J, Payne, J A, Ruusuvuori, E, Lahtinen, H, Lamsa, K, et al. The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature. 1999; 397:251–5.Google Scholar
90. Hennou, S, Khalilov, I, Diabira, D, Ben-Ari, Y, Gozlan, H. Early sequential formation of functional GABA(A) and glutamatergic synapses on CA1 interneurons of the rat foetal hippocampus. Eur J Neurosci. 2002;16:197–208.CrossRefGoogle ScholarPubMed
91. Ganguly, K, Schinder, AF, Wong, ST, Poo, M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell. 2001;105:521–32.Google Scholar
92. Turgeon, SM, Albin, RL. Postnatal ontogeny of GABAB binding in rat brain. Neuroscience. 1994;62:601–13.Google Scholar
93. Lopez-Bendito, G, Shigemoto, R, Kulik, A, Vida, I, Fairen, A, Lujan, R. Distribution of metabotropic GABA GABAB1a/b and GABAB2 in the rat hippocampus during prenatal and postnatal development. Hippocampus. 2004; 14:836–48.Google Scholar
94. Gaiarsa, JL, Tseeb, V, Ben-Ari, Y. Postnatal development of pre- and postsynaptic GABAB-mediated inhibitions in the CA3 hippocampal region of the rat. J Neurophysiol. 1995;73:246–55.Google Scholar
95. Catsicas, M, Mobbs, P. GABAb receptors regulate chick retinal calcium waves. J Neurosci. 2001;21:897–910.Google Scholar
96. Syed, MM, Lee, S, Zheng, J, Zhou, ZJ. Stage-dependent dynamics and modulation of spontaneous waves in the developing rabbit retina. J Physiol. 2004;560:533–49.Google Scholar
97. Blue, ME, Parnavelas, JG. The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis. J Neurocytol. 1983;12:697–712.Google Scholar
98. Sanes, JR, Lichtman, JW. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci. 1999;22:389–442.Google Scholar
99. Li, Z, Sheng, M. Some assembly required: the development of neuronal synapses. Nat Rev Mol Cell Biol. 2003;4:833–41.Google Scholar
100. Devon, RM, Jones, DG. Synaptic parameters in developing rat cerebral cortex: comparison of anaesthetized and unanaesthetized states. Dev Neurosci. 1981;4:351–62.Google Scholar
101. Liao, D, Hessler, NA, Malinow, R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature. 1995;375:400–4.Google Scholar
102. Isaac, JT, Nicoll, RA, Malenka, RC. Evidence for silent synapses: implications for the expression of LTP. Neuron. 1995;15:427–34.Google Scholar
103. Wu, G, Malinow, R, Cline, HT. Maturation of a central glutamatergic synapse. Science. 1996;274:972–6.Google Scholar
104. Isaac, JT, Crair, MC, Nicoll, RA, Malenka, RC. Silent synapses during development of thalamocortical inputs. Neuron. 1997;18:269–80.Google Scholar
105. Malinow, R, Malenka, RC. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci. 2002;25:103–26.Google Scholar
106. Shi, S, Hayashi, Y, Esteban, JA, Malinow, R. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell. 2001;105:331–43.Google Scholar
107. Shi, SH, Hayashi, Y, Petralia, RS, Zaman, SH, Wenthold, RJ, Svoboda, K, et al. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science. 1999;284:1811–6.Google Scholar
108. Hayashi, Y, Shi, SH, Esteban, JA, Piccini, A, Poncer, JC, Malinow, R. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science. 2000;287:2262–7.Google Scholar
109. Zhu, JJ, Esteban, JA, Hayashi, Y, Malinow, R. Postnatal synaptic potentiation: delivery of GluR4-containing AMPA receptors by spontaneous activity. Nat Neurosci. 2000;3:1098–106.Google Scholar
110. Carmignoto, G, Vicini, S. Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science. 1992;258:1007–11.Google Scholar
111. Crair, MC, Malenka, RC. A critical period for long-term potentiation at thalamocortical synapses [see comments]. Nature. 1995; 375:325–8.Google Scholar
112. Crair, MC. Neuronal activity during development: permissive or instructive? Curr Opin Neurobiol. 1999;9:88–93.Google Scholar
113. Ramoa, AS, Prusky, G. Retinal activity regulates developmental switches in functional properties and ifenprodil sensitivity of NMDA receptors in the lateral geniculate nucleus. Brain Res Dev Brain Res. 1997;101:165–75.Google Scholar
114. Quinlan, EM, Philpot, BD, Huganir, RL, Bear, MF. Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat Neurosci. 1999;2:352–7.CrossRefGoogle ScholarPubMed
115. Philpot, BD, Sekhar, AK, Shouval, HZ, Bear, MF. Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex. Neuron. 2001; 29:157–69.Google Scholar
116. Roberts, EB, Ramoa, AS. Enhanced NR2A subunit expression and decreased NMDA receptor decay time at the onset of ocular dominance plasticity in the ferret. J Neurophysiol. 1999; 81:2587–91.Google Scholar
117. Lu, HC, Gonzalez, E, Crair, MC. Barrel cortex critical period plasticity is independent of changes in NMDA receptor subunit composition. Neuron. 2001;32:619–34.Google Scholar
118. Rakic, P, Bourgeois, JP, Eckenhoff, MF, Zecevic, N, Goldman-Rakic, PS. Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science. 1986;232:232–5.Google Scholar
119. Bourgeois, JP, Rakic, P. Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. J Neurosci. 1993;13:2801–20.Google Scholar
120. Huttenlocher, PR, de Courten, C. The development of synapses in striate cortex of man. Hum Neurobiol. 1987;6:1–9.Google Scholar
121. Lichtman, JW, Colman, H. Synapse elimination and indelible memory. Neuron. 2000;25:269–78.Google Scholar
122. Lo, YJ, Poo, MM. Activity-dependent synaptic competition in vitro: heterosynaptic suppression of developing synapses. Science. 1991;254:1019–22.Google Scholar
123. Buffelli, M, Burgess, RW, Feng, G, Lobe, CG, Lichtman, JW, Sanes, JR. Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature. 2003;424:430–4.Google Scholar
124. Crepel, F, Mariani, J, Delhaye-Bouchaud, N. Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. J Neurobiol. 1976;7:567–78.Google Scholar
125. Mariani, J, Changeux, JP. Ontogenesis of olivocerebellar relationships. I. Studies by intracellular recordings of the multiple innervation of Purkinje cells by climbing fibers in the developing rat cerebellum. J Neurosci. 1981;1:696–702.Google Scholar
126. Kakizawa, S, Yamasaki, M, Watanabe, M, Kano, M. Critical period for activity-dependent synapse elimination in developing cerebellum. J Neurosci. 2000;20:4954–61.Google Scholar
127. Zuo, Y, Yang, G, Kwon, E, Gan, WB. Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature. 2005;436:261–5.Google Scholar
128. Wong, WT, Sanes, JR, Wong, RO. Developmentally regulated spontaneous activity in the embryonic chick retina. J Neurosci. 1998;18:8839–52.Google Scholar
129. Clancy, B, Darlington, RB, Finlay, BL. Translating developmental time across mammalian species. Neuroscience. 2001;105:7–17.Google Scholar
130. Rakic, P. Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science. 1974;183:425–7.Google Scholar
131. Luskin, MB, Shatz, CJ. Neurogenesis of the cat’s primary visual cortex. J Comp Neurol. 1985;242:611–31.Google Scholar
132. Van Eden, CG, Uylings, HB. Cytoarchitectonic development of the prefrontal cortex in the rat. J Comp Neurol. 1985;241:253–67.Google Scholar
133. Killackey, HP, Belford, GR. The formation of afferent patterns in the somatosensory cortex of the neonatal rat. J Comp Neurol. 1979; 183:285–303.Google Scholar