1932

Abstract

During development, the environment exerts a profound influence on the wiring of brain circuits. Due to the limited resolution of studies in fixed tissue, this experience-dependent structural plasticity was once thought to be restricted to a specific developmental time window. The recent introduction of two-photon microscopy for in vivo imaging has opened the door to repeated monitoring of individual neurons and the study of structural plasticity mechanisms at a very fine scale. In this review, we focus on recent work showing that synaptic structural rearrangements are a key mechanism mediating neural circuit adaptation and behavioral plasticity in the adult brain. We examine this work in the context of classic studies in the visual systems of model organisms, which have laid much of the groundwork for our understanding of activity-dependent synaptic remodeling and its role in brain plasticity.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-111815-114638
2016-10-14
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/vision/2/1/annurev-vision-111815-114638.html?itemId=/content/journals/10.1146/annurev-vision-111815-114638&mimeType=html&fmt=ahah

Literature Cited

  1. Ackman JB, Burbridge TJ, Crair MC. 2012. Retinal waves coordinate patterned activity throughout the developing visual system. Nature 490:219–25 [Google Scholar]
  2. Antonini A, Fagiolini M, Stryker MP. 1999. Anatomical correlates of functional plasticity in mouse visual cortex. J. Neurosci. 19:4388–406 [Google Scholar]
  3. Antonini A, Gillespie DC, Crair MC, Stryker MP. 1998. Morphology of single geniculocortical afferents and functional recovery after reverse monocular deprivation in kitten. J. Neurosci. 18:9896–909 [Google Scholar]
  4. Antonini A, Stryker MP. 1993a. Development of individual geniculocortical arbors in cat striate cortex and effects of binocular impulse blockade. J. Neurosci. 13:3549–73 [Google Scholar]
  5. Antonini A, Stryker MP. 1993b. Rapid remodeling of axonal arbors in the visual cortex. Science 260:1819–21 [Google Scholar]
  6. Antonini A, Stryker MP. 1996. Plasticity of geniculocortical afferents following brief or prolonged monocular occlusion in the cat. J. Comp. Neurol. 369:64–82 [Google Scholar]
  7. Baker FH, Grigg P, Von Noorden GK. 1974. Effects of visual deprivation and strabismus on the response of neurons in visual cortex of monkey, including studies on the striate and prestriate cortex in normal animal. Brain Res. 66:185–208 [Google Scholar]
  8. Beaulieu C, Colonnier M. 1985. A laminar analysis of the number of round-asymmetrical and flat-symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat. J. Comp. Neurol. 231:180–89 [Google Scholar]
  9. Blue ME, Parnavelas JG. 1983a. The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis. J. Neurocytol. 12:599–616 [Google Scholar]
  10. Blue ME, Parnavelas JG. 1983b. The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis. J. Neurocytol. 12:697–712 [Google Scholar]
  11. Burbridge TJ, Xu HP, Ackman JB, Ge X, Zhang Y. et al. 2014. Visual circuit development requires patterned activity mediated by retinal acetylcholine receptors. Neuron 84:1049–64 [Google Scholar]
  12. Callaway EM. 1998. Prenatal development of layer-specific local circuits in primary visual cortex of the macaque monkey. J. Neurosci. 18:1505–27 [Google Scholar]
  13. Callaway EM, Katz LC. 1990. Emergence and refinement of clustered horizontal connections in cat striate cortex. J. Neurosci. 10:1134–53 [Google Scholar]
  14. Callaway EM, Katz LC. 1991. Effects of binocular deprivation on the development of clustered horizontal connections in cat striate cortex. PNAS 88:745–49 [Google Scholar]
  15. Callaway EM, Katz LC. 1992. Development of axonal arbors of layer 4 spiny neurons in cat striate cortex. J. Neurosci. 12:570–82 [Google Scholar]
  16. Cane M, Maco B, Knott G, Holtmaat A. 2014. The relationship between PSD-95 clustering and spine stability in vivo. J. Neurosci. 34:2075–86 [Google Scholar]
  17. Cantallops I, Haas K, Cline HT. 2000. Postsynaptic CPG15 promotes synaptic maturation and presynaptic axon arbor elaboration in vivo. Nat. Neurosci. 3:1004–11 [Google Scholar]
  18. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. 1994. Green fluorescent protein as a marker for gene expression. Science 263:802–5 [Google Scholar]
  19. Chen BE, Lendvai B, Nimchinsky EA, Burbach B, Fox K, Svoboda K. 2000. Imaging high-resolution structure of GFP-expressing neurons in neocortex in vivo. Learn. Mem. 7:433–41 [Google Scholar]
  20. Chen JL, Flanders GH, Lee WC, Lin WC, Nedivi E. 2011a. Inhibitory dendrite dynamics as a general feature of the adult cortical microcircuit. J. Neurosci. 31:12437–43 [Google Scholar]
  21. Chen JL, Lin WC, Cha JW, So PT, Kubota Y, Nedivi E. 2011b. Structural basis for the role of inhibition in facilitating adult brain plasticity. Nat. Neurosci. 14:587–94 [Google Scholar]
  22. Chen JL, Nedivi E. 2010. Neuronal structural remodeling: Is it all about access?. Curr. Opin. Neurobiol. 20:1–6 [Google Scholar]
  23. Chen JL, Nedivi E. 2013. Highly specific structural plasticity of inhibitory circuits in the adult neocortex. Neuroscientist 19:384–93 [Google Scholar]
  24. Chen JL, Villa KL, Cha JW, So PT, Kubota Y, Nedivi E. 2012. Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. Neuron 74:361–73 [Google Scholar]
  25. Chklovskii DB, Mel BW, Svoboda K. 2004. Cortical rewiring and information storage. Nature 431:782–88 [Google Scholar]
  26. Clark SA, Allard T, Jenkins WM, Merzenich MM. 1988. Receptive fields in the body-surface map in adult cortex defined by temporally correlated inputs. Nature 332:444–45 [Google Scholar]
  27. Cline HT, Debski EA, Constantine-Paton M. 1987. N-methyl-d-aspartate receptor antagonist desegregates eye-specific stripes. PNAS 84:4342–45 [Google Scholar]
  28. Constantine-Paton M, Cline HT, Debski E. 1990. Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annu. Rev. Neurosci. 13:129–54 [Google Scholar]
  29. Constantine-Paton M, Law MI. 1978. Eye-specific termination bands in tecta of three-eyed frogs. Science 202:639–41 [Google Scholar]
  30. Darian-Smith C, Gilbert CD. 1994. Axonal sprouting accompanies functional reorganization in adult cat striate cortex. Nature 368:737–40 [Google Scholar]
  31. Darian-Smith C, Gilbert CD. 1995. Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated. J. Neurosci. 15:1631–47 [Google Scholar]
  32. Daw NW, Fox K, Sato H, Czepita D. 1992. Critical period for monocular deprivation in the cat visual cortex. J. Neurophysiol. 67:197–202 [Google Scholar]
  33. De Paola V, Holtmaat A, Knott G, Song S, Wilbrecht L. et al. 2006. Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron 49:861–75 [Google Scholar]
  34. DeFelipe J, Alonso-Nanclares L, Arellano J. 2002. Microstructure of the neocortex: comparative aspects. J. Neurocytol. 31:3299–316 [Google Scholar]
  35. Denk W, Strickler JH, Webb WW. 1990. Two-photon laser scanning fluorescence microscopy. Science 248:73–76 [Google Scholar]
  36. Denk W, Svoboda K. 1997. Photo upmanship: Why multiphoton imaging is more than a gimmick. Neuron 18:351–57 [Google Scholar]
  37. Diamond ME, Armstrong-James M, Ebner FF. 1993. Experience-dependent plasticity in adult rat barrel cortex. PNAS 90:2082–86 [Google Scholar]
  38. Diamond ME, Huang W, Ebner FF. 1994. Laminar comparison of somatosensory cortical plasticity. Science 265:1885–88 [Google Scholar]
  39. Feller MB. 2009. Retinal waves are likely to instruct the formation of eye-specific retinogeniculate projections. Neural Dev. 4:24 [Google Scholar]
  40. Florence SL, Taub HB, Kaas JH. 1998. Large-scale sprouting of cortical connections after peripheral injury in adult macaque monkeys. Science 282:1117–20 [Google Scholar]
  41. Gilbert CD, Wiesel TN. 1979. Morphology and intracortical projections of functionally characterized neurons in the cat visual cortex. Nature 280:120–25 [Google Scholar]
  42. Gilbert CD, Wiesel TN. 1992. Receptive field dynamics in adult primary visual cortex. Nature 356:150–52 [Google Scholar]
  43. Greenough WT, Hwang H-MF, Gorman C. 1985. Evidence for active synapse formation or altered postsynaptic metabolism in visual cortex of rats reared in complex environments. PNAS 82:4549–52 [Google Scholar]
  44. Greenough WT, Juraska JM, Volkmar FR. 1979. Maze training effects on dendritic branching in occipital cortex of adult rats. Behav. Neural Biol. 26:287–97 [Google Scholar]
  45. Greenough WT, Volkmar FR. 1973. Pattern of dendritic branching in occipital cortex of rats reared in complex environments. Exp. Neurol. 40:491–504 [Google Scholar]
  46. Grutzendler J, Kasthuri N, Gan W-B. 2002. Long-term dendritic spine stability in the adult cortex. Nature 420:812–16 [Google Scholar]
  47. Harris KM, Jensen FE, Tsao BH. 1989. Ultrastructure, development and plasticity of dendritic spine synapses in area CA1 of the rat hippocampus: extending our vision with serial electron microscopy and three-dimensional analyses. The Hippocampus: New Vistas V Chan-Palay, C Kohler 33–52 New York: Liss [Google Scholar]
  48. Hebb DO. 1949. The Organization of Behavior: A Neuropsychological Theory New York: Wiley
  49. Helmchen F, Svoboda K, Denk W, Tank DW. 1999. In vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons. Nat. Neurosci. 2:989–95 [Google Scholar]
  50. Hensch TK. 2004. Critical period regulation. Annu. Rev. Neurosci. 27:549–79 [Google Scholar]
  51. Hickmott PW, Steen PA. 2005. Large-scale changes in dendritic structure during reorganization of adult somatosensory cortex. Nat. Neurosci. 2:140–42 [Google Scholar]
  52. Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hubener M. 2009. Experience leaves a lasting structural trace in cortical circuits. Nature 457:313–17 [Google Scholar]
  53. Holtmaat A, Bonhoeffer T, Chow DK, Chuckowree J, De Paola V. et al. 2009. Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat. Protoc. 4:1128–44 [Google Scholar]
  54. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X. et al. 2005. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45:279–91 [Google Scholar]
  55. Hubel DH. 1982. Exploration of the primary visual cortex, 1955–78. Nature 299:515–24 [Google Scholar]
  56. Hubel DH, Wiesel TN. 1970. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. 206:419–36 [Google Scholar]
  57. Hubel DH, Wiesel TN, LeVay S. 1977. Plasticity of ocular dominance columns in monkey striate cortex. Philos. Trans. R. Soc. B 278:377–409 [Google Scholar]
  58. Javaherian A, Cline HT. 2005. Coordinated motor neuron axon growth and neuromuscular synaptogenesis are promoted by CPG15 in vivo. Neuron 45:505–12 [Google Scholar]
  59. Jones EG, Powell TPS. 1969. Morphological variations in the dendritic spines of the neocortex. J. Cell Sci. 5:509–29 [Google Scholar]
  60. Kaas JH, Krubitzer LA, Chino YM, Langston AL, Polley EH, Blair N. 1990. Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science 248:229–31 [Google Scholar]
  61. Kawaguchi Y, Karube F, Kubota Y. 2006. Dendritic branch typing and spine expression patterns in cortical nonpyramidal cells. Cereb. Cortex 16:696–711 [Google Scholar]
  62. Keck T, Mrsic-Flogel TD, Vaz Afonso M, Eysel UT, Bonhoeffer T, Hübener M. 2008. Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex. Nat. Neurosci. 11:1162–67 [Google Scholar]
  63. Keck T, Scheuss V, Jacobsen RI, Wierenga CJ, Eysel UT. et al. 2011. Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron 71:869–82 [Google Scholar]
  64. Knott GW, Holtmaat A, Wilbrecht L, Welker E, Svoboda K. 2006. Spine growth precedes synapse formation in the adult neocortex in vivo. Nat. Neurosci. 9:1117–24 [Google Scholar]
  65. Knott GW, Quairiaux C, Genoud C, Welker E. 2002. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 34:265–73 [Google Scholar]
  66. Kubota Y, Hatada S, Kondo S, Karube F, Kawaguchi Y. 2007. Neocortical inhibitory terminals innervate dendritic spines targeted by thalamocortical afferents. J. Neurosci. 27:1139–50 [Google Scholar]
  67. Law MI, Zahs KR, Stryker MP. 1988. Organization of primary visual cortex (area 17) in the ferret. J. Comp. Neurol. 278:157–80 [Google Scholar]
  68. Lee WC, Chen JL, Huang H, Leslie JH, Amitai Y. et al. 2008. A dynamic zone defines interneuron remodeling in the adult neocortex. PNAS 105:19968–73 [Google Scholar]
  69. Lee WC, Huang H, Feng G, Sanes JR, Brown EN. et al. 2006. Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLOS Biol. 4:e29 [Google Scholar]
  70. Lendvai B, Stern EA, Chen B, Svoboda K. 2000. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404:876–81 [Google Scholar]
  71. LeVay S, Stryker MP, Shatz CJ. 1978. Ocular dominance columns and their development in layer IV of the cat's visual cortex. J. Comp. Neurol. 179:223–44 [Google Scholar]
  72. LeVay S, Wiesel TN, Hubel DH. 1980. The development of ocular dominance columns in normal and visually deprived monkeys. J. Comp. Neurol. 191:1–51 [Google Scholar]
  73. Li Z, Van Aelst L, Cline HT. 2000. Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo. Nat. Neurosci. 3:217–25 [Google Scholar]
  74. Majewska A, Sur M. 2003. Motility of dendritic spines in visual cortex in vivo: changes during the critical period and effects of visual deprivation. PNAS 100:16024–29 [Google Scholar]
  75. Majewska AK, Newton JR, Sur M. 2006. Remodeling of synaptic structure in sensory cortical areas in vivo. J. Neurosci. 26:3021–29 [Google Scholar]
  76. Malach R, Amir Y, Harel M, Grinvald A. 1993. Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. PNAS 90:10469–73 [Google Scholar]
  77. Malenka RC, Bear MF. 2004. LTP and LTD: an embarrassment of riches. Neuron 44:5–21 [Google Scholar]
  78. Maletic-Savatic M, Malinow R, Svoboda K. 1999. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283:1923–27 [Google Scholar]
  79. Marik SA, Yamahachi H, McManus JNJ, Szabo G, Gilbert CD. 2010. Axonal dynamics of excitatory and inhibitory neurons in somatosensory cortex. PLOS Biol. 8:e1000395 [Google Scholar]
  80. Marik SA, Yamahachi H, Meyer zum Alten Borgloh S, Gilbert CD. 2014. Large-scale axonal reorganization of inhibitory neurons following retinal lesions. J. Neurosci. 34:1625–32 [Google Scholar]
  81. Mataga N, Mizuguchi Y, Hensch TK. 2004. Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron 44:1031–41 [Google Scholar]
  82. McGuire BA, Gilbert CD, Rivlin PK, Wiesel TN. 1991. Targets of horizontal connections in macaque primary visual cortex. J. Comp. Neurol. 305:370–92 [Google Scholar]
  83. McGuire BA, Hornung J-P, Gilbert CD, Weisel TN. 1984. Patterns of synaptic input to layer 4 of cat striate cortex. J. Neurosci. 4:3021–33 [Google Scholar]
  84. Merzenich MM, Nelson RJ, Stryker MP, Cynader MS, Schoppmann A, Zook JM. 1984. Somatosensory cortical map changes following digit amputation in adult monkeys. J. Comp. Neurol. 224:591–605 [Google Scholar]
  85. Mizrahi A, Katz LC. 2003. Dendritic stability in the adult olfactory bulb. Nat. Neurosci. 6:1201–7 [Google Scholar]
  86. Moriyoshi K, Richards LJ, Akazawa C, O'Leary DD, Nakanishi S. 1996. Labeling neural cells using adenoviral gene transfer of membrane-targeted GFP. Neuron 16:255–60 [Google Scholar]
  87. Nedivi E, Wu GY, Cline HT. 1998. Promotion of dendritic growth by CPG15, an activity-induced signaling molecule. Science 281:1863–66 [Google Scholar]
  88. Oberlaender M, Ramirez A, Bruno RM. 2012. Sensory experience restructures thalamocortical axons during adulthood. Neuron 74:648–55 [Google Scholar]
  89. Oray S, Majewska A, Sur M. 2004. Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron 44:1021–30 [Google Scholar]
  90. Penn AA, Riquelme PA, Feller MB, Shatz CJ. 1998. Competition in retinogeniculate patterning driven by spontaneous activity. Science 279:2108–12 [Google Scholar]
  91. Pons TP, Garraghty PE, Ommaya AK, Kaas JH, Taub E, Mishkin M. 1991. Massive cortical reorganization after sensory deafferentation in adult macaques. Science 252:1857–60 [Google Scholar]
  92. Rajan I, Cline HT. 1998. Glutamate receptor activity is required for normal development of tectal cell dendrites in vivo. J. Neurosci. 18:7836–46 [Google Scholar]
  93. Rajan I, Witte S, Cline HT. 1999. NMDA receptor activity stabilizes presynaptic retinotectal axons and postsynaptic optic tectal cell dendrites in vivo. J. Neurobiol. 38:357–68 [Google Scholar]
  94. Rakic P. 1976. Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature 261:467–71 [Google Scholar]
  95. Ramachandran VS, Rogers-Ramachandran D, Stewart M. 1992. Perceptual correlates of massive cortical reorganization. Science 258:1159–60 [Google Scholar]
  96. Reh T, Constantine-Paton M. 1985. Eye-specific segregation requires neural activity in three-eyed Rana pipiens. J. Neurosci. 5:1132–43 [Google Scholar]
  97. Robertson D, Irvine DR. 1989. Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness. J. Comp. Neurol. 282:456–71 [Google Scholar]
  98. Rochefort NL, Konnerth A. 2012. Dendritic spines: from structure to in vivo function. EMBO Rep. 13:699–708 [Google Scholar]
  99. Ruthazer ES, Baker GE, Stryker MP. 1999. Development and organization of ocular dominance bands in primary visual cortex of the sable ferret. J. Comp. Neurol. 407:151–65 [Google Scholar]
  100. Sanes JR, Lichtman JW. 1999. Development of the vertebrate neuromuscular junction. Annu. Rev. Neurosci. 22:389–442 [Google Scholar]
  101. Shatz CJ. 1983. The prenatal development of the cat's retinogeniculate pathway. J. Neurosci. 3:482–99 [Google Scholar]
  102. Shatz CJ. 1990. Impulse activity and the patterning of connections during CNS development. Neuron 5:745–56 [Google Scholar]
  103. Shatz CJ, Stryker MP. 1978. Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. J. Physiol. 281:267–83 [Google Scholar]
  104. Shatz CJ, Stryker MP. 1988. Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242:87–89 [Google Scholar]
  105. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ. et al. 1999. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284:1811–16 [Google Scholar]
  106. Sin WC, Haas K, Ruthazer ES, Cline HT. 2002. Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. Nature 419:475–80 [Google Scholar]
  107. Sirevaag AM, Greenough WT. 1987. Differential rearing effects on rat visual cortex synapses. III. Neuronal and glial nuclei, boutons, dendrites, and capillaries. Brain Res. 424:320–32 [Google Scholar]
  108. Sretavan D, Shatz CJ. 1984. Prenatal development of individual retinogeniculate axons during the period of segregation. Nature 308:845–48 [Google Scholar]
  109. Sretavan DW, Shatz CJ. 1986a. Prenatal development of cat retinogeniculate axon arbors in the absence of binocular interactions. J. Neurosci. 6:990–1003 [Google Scholar]
  110. Sretavan DW, Shatz CJ. 1986b. Prenatal development of retinal ganglion cell axons: segregation into eye-specific layers. J. Neurosci. 6:234–51 [Google Scholar]
  111. Sretavan DW, Shatz CJ, Stryker MP. 1988. Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336:468–71 [Google Scholar]
  112. Stepanyants A, Hof PR, Chklovskii DB. 2002. Geometry and structural plasticity of synaptic connectivity. Neuron 34:275–88 [Google Scholar]
  113. Stettler DD, Yamahachi H, Li W, Denk W, Gilbert CD. 2006. Axons and synaptic boutons are highly dynamic in the adult visual cortex. Neuron 49:877–87 [Google Scholar]
  114. Stryker MP, Strickland SL. 1984. Physiological segregation of ocular dominance columns depends on the pattern of afferent electrical activity. Investig. Ophthalmol. Vis. Sci. 25:278 [Google Scholar]
  115. Svoboda K, Denk W, Kleinfeld D, Tank DW. 1997. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385:161–65 [Google Scholar]
  116. Svoboda K, Helmchen F, Denk W, Tank DW. 1999. Spread of dendritic excitation in layer 2/3 pyramidal neurons in rat barrel cortex in vivo. Nat. Neurosci. 2:65–73 [Google Scholar]
  117. Svoboda K, Tank DW, Denk W. 1996. Direct measurement of coupling between dendritic spines and shafts. Science 272:716–19 [Google Scholar]
  118. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR. et al. 2002. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420:788–94 [Google Scholar]
  119. van Versendaal D, Rajendran R, Saiepour MH, Klooster J, Smit-Rigter L. et al. 2012. Elimination of inhibitory synapses is a major component of adult ocular dominance plasticity. Neuron 74:374–83 [Google Scholar]
  120. Villa KL, Berry KP, Subramanian J, Cha JW, Oh WC. et al. 2016. Inhibitory synapses are repeatedly assembled and removed at persistent sites in vivo. Neuron 89:756–69 [Google Scholar]
  121. Volkmar FR, Greenough WT. 1972. Rearing complexity affects branching of dendrites in the visual cortex of the rat. Science 176:1445–47 [Google Scholar]
  122. Wiesel TN. 1982. Postnatal development of the visual cortex and the influence of environment. Nature 299:583–91 [Google Scholar]
  123. Wiesel TN, Hubel DH. 1963. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26:1003–17 [Google Scholar]
  124. Wiesel TN, Hubel DH. 1965. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. Neurophysiol. 28:1029–40 [Google Scholar]
  125. Wiesel TN, Hubel DH, Lam DMK. 1974. Autoradiographic demonstration of ocular-dominance columns in monkey striate cortex by means of transneuronal transport. Brain Res. 79:273–79 [Google Scholar]
  126. Witte S, Stier H, Cline HT. 1996. In vivo observations of timecourse and distribution of morphological dynamics in Xenopus retinotectal axon arbors. J. Neurobiol. 31:219–34 [Google Scholar]
  127. Wong ROL, Chernjavsky A, Smith SJ, Shatz CJ. 1995. Early functional neural networks in the developing retina. Nature 374:716–18 [Google Scholar]
  128. Wu GY, Cline HT. 1998. Stabilization of dendritic arbor structure in vivo by CaMKII. Science 279:222–26 [Google Scholar]
  129. Wu GY, Zou DJ, Rajan I, Cline H. 1999. Dendritic dynamics in vivo change during neuronal maturation. J. Neurosci. 19:4472–83 [Google Scholar]
  130. Yabuta NH, Callaway EM. 1998. Cytochrome-oxidase blobs and intrinsic horizontal connections of layer 2/3 pyramidal neurons in primate V1. Vis. Neurosci. 15:1007–27 [Google Scholar]
  131. Yamahachi H, Marik SA, McManus JNJ, Denk W, Gilbert CD. 2009. Rapid axonal sprouting and pruning accompany functional reorganization in primary visual cortex. Neuron 64:719–29 [Google Scholar]
  132. Zhang J, Ackman JB, Xu HP, Crair MC. 2012. Visual map development depends on the temporal pattern of binocular activity in mice. Nat. Neurosci. 15:298–307 [Google Scholar]
  133. Zou DJ, Cline HT. 1999. Postsynaptic calcium/calmodulin-dependent protein kinase II is required to limit elaboration of presynaptic and postsynaptic neuronal arbors. J. Neurosci. 19:8909–18 [Google Scholar]
  134. Zuo Y, Yang G, Kwon E, Gan WB. 2005. Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 436:261–65 [Google Scholar]
/content/journals/10.1146/annurev-vision-111815-114638
Loading
/content/journals/10.1146/annurev-vision-111815-114638
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error