Axons and synaptic boutons are highly dynamic in adult visual cortex

Neuron

Volumn 49, Issue 6, 2006, Pages 877-887

  Stettler, Dan D ^a,c   Yamahachi, Homare ^a   Li, Wu ^a   Denk, Winfried ^b   Gilbert, Charles D ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^c College of Physicians and Surgeons ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN;

ADENO ASSOCIATED VIRUS; ARTICLE; BRAIN CELL; BRAIN CORTEX; CELL LABELING; CONTROLLED STUDY; MACACA; MOUSE; NERVE FIBER; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; SYNAPTOGENESIS; VISUAL CORTEX;

ANIMALS; AXONS; DEPENDOVIRUS; GREEN FLUORESCENT PROTEINS; MACACA FASCICULARIS; MICE; NEURONS; NONLINEAR DYNAMICS; PHOTONS; PRESYNAPTIC TERMINALS; TIME FACTORS; VISUAL CORTEX;

EID: 33644864762     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.02.018     Document Type: Article

References (98)

1. B. Ahmed, J.C. Anderson, K.A.C. Martin, and J.C. Nelson Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat J. Comp. Neurol. 380 1997 230 242
2. B. Alsina, T. Vu, and S. Cohen-Cory Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF Nat. Neurosci. 4 2001 1093 1101
3. Y. Amir, M. Harel, and R. Malach Cortical hierarchy reflected in the organization of intrinsic connections in Macaque monkey visual cortex J. Comp. Neurol. 334 1993 19 46
4. J.C. Anderson, and K.A.C. Martin Does bouton morphology optimize axon length? Nat. Neurosci. 4 2001 1166 1167
5. J.C. Anderson, and K.A.C. Martin Connection from cortical area V2 to V3A in macaque monkey J. Comp. Neurol. 488 2005 320 330
6. J.C. Anderson, T. Binzegger, K.A.C. Martin, and K.S. Rockland The connection from cortical area V1 to V5: a light and electron microscopic study J. Neurosci. 18 1998 10525 10540
7. J.C. Anderson, T. Binzegger, R.J. Douglas, and K.A.C. Martin Chance or design? Some specific considerations concerning synaptic boutons in cat visual cortex J. Neurocytol. 31 2003 211 229
8. A. Antonini, and M.P. Stryker Development of individual geniculocortical arbors in cat striate cortex and effects of binocular impulse blockade J. Neurosci. 13 1993 3549 3573
9. L. Arckens, G. Schweigart, Y. Qu, G. Wouters, D.V. Pow, F. Vandesande, U.T. Eysel, and G.A. Orban Cooperative changes in GABA, glutamate and activity levels: the missing link in cortical plasticity Eur. J. Neurosci. 12 2000 4222 4232
10. R.J. Balice-Gordon, and J.W. Lichtman In vivo visualization of the growth of pre- and postsynaptic elements of neuromuscular junctions in the mouse J. Neurosci. 10 1990 894 908
11. J. Bennett, A.M. Maguire, A.V. Cideciyan, M. Schnell, E. Glover, V. Anand, T.S. Aleman, N. Chirmule, A.R. Gupta, and Y. Huang Stable transgene expression in rod photoreceptors after recombinant adeno-associated virus-mediated gene transfer to monkey retina Proc. Natl. Acad. Sci. USA 96 1999 9920 9925
12. D.H. Bhatt, S.J. Otto, B. Depoister, and J.R. Fetcho Cyclic AMP-induced repair of zebrafish spinal circuits Science 305 2004 254 258
13. D.L. Bishop, T. Misgeld, M.K. Walsh, W.-B. Gan, and J.W. Lichtman Axon branch removal at developing synapses by axosome shedding Neuron 44 2004 651 661
14. G.G. Blasdel, J.S. Lund, and D. Fitzpatrick Intrinsic connections of macaque striate cortex: axonal projection of cells outside lamina 4C J. Neurosci. 5 1985 3350 3369
15. V. Braitenberg, and A. Schüz Cortex: Statistics and Geometry of Neuronal Connectivity 1998 Springer Berlin
16. M. Buffelli, R.W. Burgess, G. Feng, C.G. Lobe, J.W. Lichtman, and J.R. Sanes Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition Nature 424 2003 430 434
17. M.B. Calford, and R. Tweedale Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation Nature 332 1988 446 448
18. M.B. Calford, C. Wang, V. Taglianetti, W.J. Waleszczyk, W. Burke, and B. Dreher Plasticity in adult cat visual cortex (area 17) following circumscribed monocular lesions of all retinal layers J. Physiol. 524 2000 587 602
19. M.B. Calford, L.L. Wright, A.B. Metha, and V. Taglianetti Topographic plasticity in primary visual cortex is mediated by local corticortical connections J. Neurosci. 23 2003 6434 6442
20. E.M. Callaway, and L.C. Katz Emergence and refinement of clustered horizontal connections in cat striate cortex J. Neurosci. 10 1990 1134 1153
21. N.L. Chamberlin, B. Du, S. de Lacalle, and C.B. Saper Recombinant adeno-associated virus vector: use for transgene expression and anterograde tract tracing in the CNS Brain Res. 793 1998 169 175
22. Y.M. Chino, E.L. Smith III, H. Wada, W.L. Ridder III, A.L. Langston, and G.A. Lesher Disruption of binocularly correlated input leads to deficits in spatial properties of striate cortical neurons in cats J. Neurophysiol. 65 1991 841 859
23. Y.M. Chino, J.H. Kaas, E.L. Smith, A.L. Langston, and H. Cheng Rapid reorganization of cortical maps in adult cats following restricted deafferentation in retina Vision Res. 32 1992 789 796
24. D.B. Chklovskii, B.W. Mel, and K. Svoboda Cortical rewiring and information storage Nature 431 2004 782 788
25. S. Cohen-Cory, and S.E. Fraser Effects of brain-derived neurotrophic factor on optic axon branching and remodeling in vivo Nature 378 1995 192 196
26. M. Colman, J. Nabekura, and J.W. Lichtman Alterations in synaptic strength preceding axon withdrawal Science 275 1997 356 361
27. R.E. Crist, W. Li, and C.D. Gilbert Learning to see: experience and attention in primary visual cortex Nat. Neurosci. 4 2001 519 525
28. C. Darian-Smith, and C.D. Gilbert Axonal sprouting accompanies functional reorganization in adult cat striate cortex Nature 368 1994 737 740
29. A. Das, and C.D. Gilbert Long-range horizontal connections and their role in cortical reorganization revealed by optical-recording of cat primary visual cortex Nature 375 1995 780 784
30. W. Denk, and K. Svoboda Photon upmanship: why multiphoton imaging is more than a gimmick Neuron 18 1997 351 357
31. W. Denk, J.H. Strickler, and W.W. Webb Two-photon laser scanning microscopy Science 248 1990 73 76
32. V. De Paola, S. Arber, and P. Caroni AMPA receptors regulate dynamic equilibrium of presynaptic terminals in mature hippocampal networks Nat. Neurosci. 6 2003 491 500
33. V. De Paola, A. Holtmaat, G. Knott, S. Song, L. Wilbrecht, P. Caroni, and K. Svoboda Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex Neuron 49 2006 861 875 this issue
34. T. Dittgen, A. Nimmerjahn, S. Komai, P. Licznerski, J. Waters, T.W. Margrie, F. Helmchen, W. Denk, W. Brecht, and P. Osten Lenti-virus-based genetic manipulations of cortical neurons and their optical and electrophysiological monitoring in vivo Proc. Natl. Acad. Sci. USA 101 2004 18206 18211
35. H. Flanagan-Street, M.A. Fox, D. Meyer, and J.R. Sanes Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations Development 132 2005 4471 4481
36. S.L. Florence, H.B. Taub, and J.H. Kaas Large-scale sprouting of cortical connections after peripheral injury in adult Macaque monkeys Science 282 1998 1117 1121
37. L. Foa, I. Rajan, K. Haas, G.-Y. Wu, P. Brakeman, P. Worley, and H. Cline The scaffold protein, Homer1b/c, regulates axon pathfinding in the central nervous system in vivo Nat. Neurosci. 4 2001 499 506
38. M.J. Friedlander, K.A.C. Martin, and D. Wassenhove-McCarthy Effects of monocular visual deprivation on geniculocortical innervation of area 18 in cat J. Neurosci. 11 1991 3268 3288
39. W.B. Gan, and J.W. Lichtman Synaptic segregation at the developing neuromuscular junction Science 282 1998 1508 1511
40. W.-B. Gan, E. Kwon, G. Feng, J.R. Sanes, and J.W. Lichtman Synaptic dynamism measured over minutes to months: age-dependent decline in an autonomic ganglion Nat. Neurosci. 6 2003 956 960
41. C.D. Gilbert, and T.N. Wiesel Morphology and intracortical projections of functionally chacterized neurons in the cat visual cortex Nature 280 1979 120 125
42. C.D. Gilbert, and T.N. Wiesel Clustered intrinsic connections in cat visual cortex J. Neurosci. 3 1983 1116 1133
43. C.D. Gilbert, and T.N. Wiesel Receptive field dynamics in adult primary visual cortex Nature 356 1992 150 152
44. C.D. Gilbert, J.A. Hirsch, and T.N. Wiesel Lateral interactions in visual cortex Cold Spring Harb. Symp. Quant. Biol. 55 1990 663 677
45. J. Grutzendler, N. Kasthuri, and W.B. Gan Long-term dendritic spine stability in the adult cortex Nature 420 2002 812 816
46. K.M. Harris, and P. Sultan Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the nonuniform probability of release at hippocampal CA1 synapses Neuropharmacology 34 1995 1387 1395
47. S.J. Heinen, and A.A. Skavenski Recovery of visual responses in foveal V1 neurons following bilateral foveal lesions in adult monkey Exp. Brain Res. 83 1991 670 674
48. H. Hering, and M. Sheng Dendritic spines: structure, dynamics and regulation Nat. Rev. Neurosci. 2 2001 880 888
49. A.J. Holtmaat, J.T. Trachtenberg, L. Wilbrecht, G.M. Shepherd, X. Zhang, G.W. Knott, and K. Svoboda Transient and persistent dendritic spines in the neocortex in vivo Neuron 45 2005 279 291
50. B. Hu, A.M. Nikolakopoulou, and S. Cohen-Cory BDNF stabilizes synapses and maintains the structural complexity of optic axons in vivo Development 132 2005 4285 4298
51. J.Y. Hua, M.C. Smear, H. Baler, and S.J. Smith Regulation of axon growth in vivo by activity-based competition Nature 434 2005 1022 1026
52. D.H. Hubel, T.N. Wiesel, and S. LeVay Plasticity of ocular dominance columns in monkey striate cortex Philos. Trans. R. Soc. Lond. B Biol. Sci. 278 1977 377 409
53. A. Javaherian, and H.T. Cline Coordinated motor neuron axon growth and neuromuscular synaptogenesis are promoted by CPG15 in vivo Neuron 45 2005 505 512
54. F.A. Johnson, A.J. Dawson, and R.L. Meyer Activity-dependent refinement in the goldfish retinotectal system is mediated by the dynamic regulation of processes withdrawal: an in vivo imaging study J. Comp. Neurol. 406 1999 548 562
55. J.D. Jontes, J. Buchanan, and S.J. Smith Growth cone and dendrite dynamics in zebrafish embryos: early events in synaptogenesis images in vivo Nat. Neurosci. 3 2000 231 237
56. J.H. Kaas, L.A. Krubitzer, Y.M. Chino, A.L. Langston, E.H. Polley, and N. Blair Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina Science 248 1990 229 231
57. N. Kasthuri, and J.W. Lichtman The role of neuronal identity in synaptic competition Nature 424 2003 426 430
58. M. Kerschensteiner, M.E. Schwab, J.W. Lichtman, and T. Misgeld In vivo imaging of axonal degeneration and regeneration in the injured spinal cord Nat. Med. 11 2005 572 577
59. A.E. Kincaid, T. Zheng, and C.J. Wilson Connectivity and convergence of single corticostriatal axons J. Neurosci. 18 1998 4722 4731
60. Z.F. Kisvarday, K.A.C. Martin, T.F. Freund, Z.S. Magloczky, D. Whitteridge, and P. Somogyi Synaptic targets of HRP-filled layer III pyramidal cells in the cat striate cortex Exp. Brain Res. 64 1986 541 552
61. W. Li, V. Piech, and C.D. Gilbert Perceptual learning and top-down influences in primary visual cortex Nat. Neurosci. 7 2004 651 657
62. J.W. Lichtman, L. Magrassi, and D. Purves Visualization of neuromuscular junctions over periods of several months in living mice J. Neurosci. 7 1987 1215 1222
63. Y. Liu, and M.C. Halloran Central and peripheral axon branches from one neuron are guided differentially by semaphorin3D and transient axonal glycoprotein-1 J. Neurosci. 25 2005 10556 10563
64. J. Lubke, A. Roth, D. Feldmeyer, and B. Sakmann Morphometric analysis of the columnar innervation domain of neurons connecting layer 4 and layer 2/3 of juvenile rat barrel cortex Cereb. Cortex 13 2003 1051 1063
65. A. Majewska, and M. Sur Motility of dendritic spines in visual cortex in vivo: changes during the critical period and effects of visual deprivation Proc. Natl. Acad. Sci. USA 100 2003 16024 16029
66. B.A. McGuire, C.D. Gilbert, P.K. Rivlin, and T.N. Wiesel Targets of horizontal connections in Macaque primary visual cortex J. Comp. Neurol. 305 1991 370 392
67. M.M. Merzenich, J.H. Kaas, J. Wall, R.J. Nelson, M. Sur, and D. Felleman Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentiation Neuroscience 8 1983 33 55
68. A. Mizrahi, and L.C. Katz Dendritic stability in the adult olfactory bulb Nat. Neurosci. 6 2003 1201 1207
69. Q.T. Nguyen, J.R. Sanes, and J.W. Lichtman Pre-existing pathways promote precise projection patterns Nat. Neurosci. 5 2002 861 867
70. Y.A. Pan, T. Misgeld, J.W. Lichtman, and J.R. Sanes Effects of neurotoxic and neuroprotective agents on peripheral nerve regeneration assayed by time-lapse imaging in vivo J. Neurosci. 23 2003 11479 11488
71. A. Peters, and C.C. Proskauer Synaptic relationships between a multipolar stellate cell and a pyramidal neuron in the rat visual cortex. A combined Golgi-electron microscope study J. Neurocytol. 9 1980 163 183
72. A. Peters, S.L. Palay, and H. Webster The Fine Structure of the Nervous System: Neurons and Their Supporting Cells 1991 Oxford New York
73. J.P. Pierce, and G.R. Lewin An ultrastructural size principal Neuroscience 58 1994 441 446
74. T. Pons, P.E. Garraghty, A.K. Ommaya, J.H. Kaas, E. Taub, and M. Mishkin Massive cortical reorganization after sensory deafferentiation in adult Macaques Science 252 1991 1857 1860
75. C. Portera-Cailliau, R.M. Weimer, V. De Paola, P. Caroni, and K. Svoboda Diverse modes of axon elaboration in the developing neocortex PLoS Biol. 3 2005 e727 10.1371/journal.pbio.0030272
76. K. Rockland, and J.S. Lund Widespread periodic intrinsic connections in the tree shrew visual cortex Science 215 1982 1532 1534
77. E.S. Ruthazer, C.J. Akerman, and H.T. Cline Control of axon branch dynamics by correlated activity in vivo Science 301 2003 66 70
78. A.M. Schaefer, J.R. Sanes, and J.W. Lichtman A compensatory subpopulation of motor neurons in a mouse model of amyotrophic lateral sclerosis J. Comp. Neurol. 490 2005 209 219
79. T. Schikorski, and C.F. Stevens Quantitative ultrastructural analysis of hippocampal excitatory synapses J. Neurosci. 17 1997 5858 5867
80. T. Schikorski, and C.F. Stevens Quantitative fine-structural analysis of olfactory cortical synapses Proc. Natl. Acad. Sci. USA 96 1999 4107 4112
81. L.M. Schmid, M.G. Rosa, M.B. Calford, and J.S. Ambler Visuotopic reorganization in the primary visual cortex Cereb. Cortex 6 1996 388 405
82. J.T. Schmidt, M. Buzzard, R. Borress, and S. Dhilon MK801 increases retinotectal arbor size in developing zebrafish without affecting kinetics of branch elimination and addition J. Neurobiol. 42 2000 303 314
83. J.T. Schmidt, M.R. Fleming, and B. Leu Presynaptic protein kinase C controls maturation and branch dynamics of developing retinotectal arbors: possible role in activity-driven sharpening J. Neurobiol. 58 2004 328 340
84. A. Schoups, R. Vogels, N. Qian, and G. Orban Practising orientation identification improves orientation coding in V1 neurons Nature 412 2001 549 553
85. A. Schuz, and A. Munster Synaptic density on the axonal tree of a pyramidal cell in the cortex of the mouse Neuroscience 15 1985 33 39
86. R.A. Silver, J. Lubke, B. Sakmann, and D. Feldmeyer High-probability uniquantal transmission at excitatory synapses in barrel cortex Science 302 2003 1981 1984
87. S.M. Smirnakis, A.A. Brewer, M.C. Schmid, A.S. Tolias, A. Schuz, M. Augath, W. Inhoffen, B.A. Wandell, and N.K. Logothetis Lack of long-term cortical reorganization after Macaque retinal lesions Nature 435 2005 300 307
88. P. Somogyi The study of Golgi stained cells and of experimental degeneration under the electron microscope: a direct method for the identification in the visual cortex of three successive links in a neuron chain Neuroscience 3 1978 167 180
89. P. Somogyi, T.F. Freund, and A. Cowey The axon-axonic interneuron in the cerebral cortex of the rat, cat and monkey Neuroscience 7 1982 2577 2607
90. D.D. Stettler, A. Das, J. Bennett, and C.D. Gilbert Lateral connectivity and contextual interactions in Macaque primary visual cortex Neuron 36 2002 739 750
91. E.M. Surace, A. Auricchio, S.J. Reich, T. Rex, E. Glover, S. Pineles, W. Tang, E. O'Connor, A. Lyubarsky, and A. Savchenko Delivery of adeno-associated virus vectors to the fetal retina: impact of viral capsid proteins on retinal neuronal progenitor transduction J. Virol. 77 2003 7957 7963
92. K. Svoboda, W. Denk, D. Kleinfeld, and D.W. Tank In vivo dendritic calcium dynamics in neocortical pyramidal neurons Nature 385 1997 161 165
93. J.T. Trachtenberg, B.E. Chen, G.W. Knott, G. Feng, J.R. Sanes, E. Welker, and K. Svoboda Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex Nature 420 2002 788 794
94. M.K. Walsh, and J.W. Lichtman In vivo time-lapse imaging of synaptic takeover associated with naturally occurring synapse elimination Neuron 37 2003 67 73
95. D.A. Winfield, N.L. Brooke, J.J. Sloper, and T.P.S. Powell A combined Golgi-electron microscopic study of the synapses made by the proximal axon and recurrent collaterals of a pyramidal cell in the somatic sensory cortex of the monkey Neuroscience 6 1981 1217 1230
96. W. Xiao, N. Chirmule, S.C. Berta, B. McCullough, G. Gao, and J.M. Wilson Gene therapy vectors based on adeno-associated virus type 1 J. Virol. 73 1999 3994 4003
97. R. Yuste, and T. Bonhoeffer Genesis of dendritic spines: insights from ultrastructural and imaging studies Nat. Rev. Neurosci. 5 2004 24 34
98. Y. Zuo, A. Lin, P. Chang, and W.B. Gan Development of long-term dendritic spine stability in diverse regions of cerebral cortex Neuron 46 2005 181 189