Erratum to FIB/SEM technology and high-throughput 3D reconstruction of dendritic spines and synapses in GFP-labeled adult-generated neurons (Front. Neuroanat., (2015) 9, (60), 10.3389/fnana.2015.00060);FIB/SEM technology and high-throughput 3D reconstruction of dendritic spines and synapses in GFP-labeled adult-generated neurons

Frontiers in Neuroanatomy

Volumn 9, Issue MAY, 2015, Pages

  Bosch, Carles ^a,b,c   Martínez, Albert ^a   Masachs, Nuria ^a,b   Teixeira, Cátia M ^a,b   Fernaud, Isabel ^b,d,e   Ulloa, Fausto ^a,b   Pérez Martínez, Esther ^a,b   Lois, Carlos ^f   Comella, Joan X ^b,c,g   De Felipe, Javier ^b,d,e   Soriano, Eduardo ^a,a,b,c,i  

^a UNIVERSITY OF BARCELONA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^d UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

^e INSTITUTO CAJAL   (Spain)

^f UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^g INSTITUT DE NEUROCIÈNCIES   (Spain)

^h UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

ⁱ INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

3D reconstruction; Adult neurogenesis; Dendritic spines; Electron microscopy; FIB SEM; Synapses

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COMPARATIVE STUDY; DENDRITIC SPINE; EXPERIMENTAL MODEL; FOCUSED ION BEAM; GRANULE CELL; ISOTOPE LABELING; LIGHT RELATED PHENOMENA; MORPHOMETRICS; MOUSE; NEUROLOGIC EXAMINATION; NONHUMAN; QUALITY CONTROL; RETROVIRIDAE; SCANNING ELECTRON MICROSCOPY; SYNAPSE; SYNAPTIC POTENTIAL; SYNAPTOGENESIS; THREE DIMENSIONAL IMAGING; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84930653359     PISSN: None     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2016.00100     Document Type: Erratum

References (77)

1. Aimone, J. B., Deng, W., and Gage, F. H. (2011). Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70, 589-596. doi: 10. 1016/j. neuron. 2011. 05. 010.
2. Allegra Mascaro, A. L., Cesare, P., Sacconi, L., Grasselli, G., Mandolesi, G., Maco, B., et al. (2013). In vivo single branch axotomy induces GAP-43-dependent sprouting and synaptic remodeling in cerebellar cortex. Proc. Natl. Acad. Sci. U. S. A. 110, 10824-10829. doi: 10. 1073/pnas. 1219256110.
3. Arellano, J. I., Benavides-Piccione, R., Defelipe, J., and Yuste, R. (2007). Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front. Neurosci. 1, 131-143. doi: 10. 3389/neuro. 01. 1. 1. 010. 2007.
4. Blazquez-Llorca, L., Merchán-Pérez, A., Rodríguez, J.-R., Gascón, J., and Defelipe, J. (2013). FIB/SEM Technology and Alzheimer's disease: three-dimensional analysis of human cortical synapses. J. Alzheimers Dis. 34, 995-1013. doi: 10. 3233/JAD-122038.
5. Bock, D. D., Lee, W. C., Kerlin, A. M., Andermann, M. L., Hood, G., Wetzel, A. W., et al. (2011). Network anatomy and in vivo physiology of visual cortical neurons. Nature471, 177-182. doi: 10. 1038/nature09802.
6. Bourne, J. N., and Harris, K. M. (2008). Balancing structure and function at hippocampal dendritic spines. Annu. Rev. Neurosci. 31, 47-67. doi: 10. 1146/annurev. neuro. 31. 060407. 125646.
7. Briggman, K. L., and Bock, D. D. (2012). Volume electron microscopy for neuronal circuit reconstruction. Curr. Opin. Neurobiol. 22, 154-161. doi: 10. 1016/j. conb. 2011. 10. 022.
8. Briggman, K. L., and Denk, W. (2006). Towards neural circuit reconstruction with volume electron microscopy techniques. Curr. Opin. Neurobiol. 16, 562-570. doi: 10. 1016/j. conb. 2006. 08. 010.
9. Bushby, A. J., Ping, K., M., Young, R. D., Pinali, C., Knupp, C., and Quantock, A. J. (2011). Imaging three-dimensional tissue architectures by focused ion beam scanning electron microscopy. Nat. Protoc. 6, 845-858. doi: 10. 1038/nprot. 2011. 332.
10. Buzsaki, G., and Moser, E. I. (2013). Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16, 130-138. doi: 10. 1038/nn. 3304.
11. Cane, M., Maco, B., Knott, G., and Holtmaat, A. (2014). The relationship between PSD-95 clustering and spine stability in vivo. J. Neurosci. 34: 2075-2086. doi: 10. 1523/JNEUROSCI. 3353-13. 2014.
12. Deng, W., Aimone, J. B., and Gage, F. H. (2010). New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci. 11, 339-350. doi: 10. 1038/nrn2822.
13. Denk, W., and Horstmann, H. (2004). Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol. 2: e329. doi: 10. 1371/journal. pbio. 0020329.
14. Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A., et al. (1998). Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317. doi: 10. 1038/3305.
15. Fairen, A., Peters, A., and Saldanha, J. (1977). A new procedure for examining Golgi impregnated neurons by light and electron microscopy. J. Neurocytol. 6, 311-337. doi: 10. 1007/BF01175194.
16. Fairen, A. (2005). Pioneering a golden age of cerebral microcircuits: the births of the combined Golgi-electron microscope methods. Neuroscience 136, 607-614. doi: 10. 1016/j. neuroscience. 2005. 08. 011.
17. Fiala, J. C. (2005). Reconstruct: a free editor for serial section microscopy. J. Microsc. 218, 52-61. doi: 10. 1111/j. 1365-2818. 2005. 01466. x.
18. Frotscher, M., and Leranth, C. (1986). The cholinergic innervation of the rat fascia dentata: identification of target structures on granule cells by combining choline acetyltransferase immunocytochemistry and Golgi impregnation. J. Comp. Neurol. 243, 58-70. doi: 10. 1002/cne. 902430106.
19. Gage, F. H. (2000). Mammalian neural stem cells. Science 287, 1433-1438. doi: 10. 1126/science. 287. 5457. 1433.
20. Garthe, A., Behr, J., and Kempermann, G. (2009). Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS ONE4: e5464. doi: 10. 1371/journal. pone. 0005464.
21. Ge, S., Goh, E. L., Sailor, K. A., Kitabatake, Y., Ming, G. L., and Song, H. (2006). GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature439, 589-593. doi: 10. 1038/nature04404.
22. Ge, S., Sailor, K. A., Ming, G. L., and Song, H. (2008). Synaptic integration and plasticity of new neurons in the adult hippocampus. J. Physiol. 586, 3759-3765. doi: 10. 1113/jphysiol. 2008. 155655.
23. Ge, S., Yang, C. H., Hsu, K. S., Ming, G. L., and Song, H. (2007). A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron54, 559-566. doi: 10. 1016/j. neuron. 2007. 05. 002.
24. Geinisman, Y., Berry, R. W., Disterhoft, J. F., Power, J. M., and Van Der Zee, E. A. (2001). Associative learning elicits the formation of multiple-synapse boutons. J. Neurosci. 21, 5568-5573.
25. Geinisman, Y., Morrell, F., and Detoledo-Morrell, L. (1989). Perforated synapses on double-headed dendritic spines: a possible structural substrate of synaptic plasticity. Brain Res. 480, 326-329. doi: 10. 1016/0006-8993(89)90201-1.
26. Gu, Y., Arruda-Carvalho, M., Wang, J., Janoschka, S. R., Josselyn, S. A., Frankland, P. W., et al. (2012). Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat. Neurosci. 15, 1700-1706. doi: 10. 1038/nn. 3260.
27. Harris, K. M., Jensen, F. E., and Tsao, B. (1992). Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J. Neurosci. 12, 2685-2705.
28. Harris, K. M., Perry, E., Bourne, J., Feinberg, M., Ostroff, L., and Hurlburt, J. (2006). Uniform serial sectioning for transmission electron microscopy. J. Neurosci. 26, 12101-12103. doi: 10. 1523/JNEUROSCI. 3994-06. 2006.
29. Harris, K. M., and Weinberg, R. J. (2012). Ultrastructure of synapses in the mammalian brain. Cold Spring Harb. Perspect. Biol. 4: a005587. doi: 10. 1101/cshperspect. a005587.
30. Helmstaedter, M. (2013). Cellular-resolution connectomics: challenges of dense neural circuit reconstruction. Nat. Methods 10, 501-507. doi: 10. 1038/nmeth. 2476.
31. Hoffpauir, B. K., Pope, B. A., and Spirou, G. A. (2007). Serial sectioning and electron microscopy of large tissue volumes for 3D analysis and reconstruction: a case study of the calyx of Held. Nat. Protoc. 2, 9-22. doi: 10. 1038/nprot. 2007. 9.
32. Honkura, N., Matsuzaki, M., Noguchi, J., Ellis-Davies, G. C., and Kasai, H. (2008). The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron 57, 719-729. doi: 10. 1016/j. neuron. 2008. 01. 013.
33. Jain, V., Seung, H. S., and Turaga, S. C. (2010). Machines that learn to segment images: a crucial technology for connectomics. Curr. Opin. Neurobiol. 20, 653-666. doi: 10. 1016/j. conb. 2010. 07. 004.
34. Kee, N., Teixeira, C. M., Wang, A. H., and Frankland, P. W. (2007). Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci. 10, 355-362. doi: 10. 1038/nn1847.
35. Kelsch, W., Lin, C. W., and Lois, C. (2008). Sequential development of synapses in dendritic domains during adult neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 105, 16803-16808. doi: 10. 1073/pnas. 0807970105.
36. Knoth, R., Singec, I., Ditter, M., Pantazis, G., Capetian, P., Meyer, R. P., et al. (2010). Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS ONE 5: e8809. doi: 10. 1371/journal. pone. 0008809.
37. Knott, G., Marchman, H., Wall, D., and Lich, B. (2008). Serial section scanning electron microscopy of adult brain tissue using focused ion beam milling. J. Neurosci. 28, 2959-2964. doi: 10. 1523/JNEUROSCI. 3189-07. 2008.
38. Knott, G. W., Holtmaat, A., Wilbrecht, L., Welker, E., and Svoboda, K. (2006). Spine growth precedes synapse formation in the adult neocortex in vivo. Nat. Neurosci. 9, 1117-1124. doi: 10. 1038/nn1747.
39. Konur, S., and Yuste, R. (2004). Imaging the motility of dendritic protrusions and axon terminals: roles in axon sampling and synaptic competition. Mol. Cell Neurosci. 27, 427-440. doi: 10. 1016/j. mcn. 2004. 07. 005.
40. Lois, C., and Alvarez-Buylla, A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145-1148. doi: 10. 1126/science. 8178174.
41. Maco, B., Cantoni, M., Holtmaat, A., Kreshuk, A., Hamprecht, F. A., and Knott, G. W. (2014). Semiautomated correlative 3D electron microscopy of in vivo-imaged axons and dendrites. Nat. Protoc. 9: 1354-1366. doi: 10. 1038/nprot. 2014. 101.
42. Maco, B., Holtmaat, A., Cantoni, M., Kreshuk, A., Straehle, C. N., Hamprecht, F. A., et al. (2013). Correlative in vivo 2 photon and focused ion beam scanning electron microscopy of cortical neurons. PLoS ONE 8: e57405. doi: 10. 1371/journal. pone. 0057405.
43. Merchan-Perez, A., Rodriguez, J. R., Alonso-Nanclares, L., Schertel, A., and Defelipe, J. (2009). Counting synapses using FIB/SEM microscopy: a true revolution for ultrastructural volume reconstruction. Front. Neuroanat. 3: 18. doi: 10. 3389/neuro. 05. 018. 2009.
44. Merchan-Perez, A., Rodriguez, J. R., Gonzalez, S., Robles, V., Defelipe, J., Larranaga, P., et al. (2014). Three-dimensional spatial distribution of synapses in the neocortex: a dual-beam electron microscopy study. Cereb. Cortex 24, 1579-1588. doi: 10. 1093/cercor/bht018.
45. Mishchenko, Y., Hu, T., Spacek, J., Mendenhall, J., Harris, K. M., and Chklovskii, D. B. (2010). Ultrastructural analysis of hippocampal neuropil from the connectomics perspective. Neuron 67, 1009-1020. doi: 10. 1016/j. neuron. 2010. 08. 014.
46. Morales, J., Alonso-Nanclares, L., Rodriguez, J. R., Defelipe, J., Rodriguez, A., and Merchan-Perez, A. (2011). Espina: a tool for the automated segmentation and counting of synapses in large stacks of electron microscopy images. Front. Neuroanat. 5: 18. doi: 10. 3389/fnana. 2011. 00018.
47. Peddie, C. J., and Collinson, L. M. (2014). Exploring the third dimension: volume electron microscopy comes of age. Micron 61, 9-19. doi: 10. 1016/j. micron. 2014. 01. 009.
48. Peters, A., and Kaiserman-Abramof, I. R. (1970). The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. Am. J. Anat. 127, 321-355. doi: 10. 1002/aja. 1001270402.
49. Peters, A., and Palay, S. L. (1996). The morphology of synapses. J. Neurocytol. 25, 687-700. doi: 10. 1007/BF02284835.
50. Peters, A., Palay, S. L., and Webster, H. (1991). The Fine Structure of the Nervous System. Neurons and their Supporting Cells, 3rd Edn. New York, NY: Oxford University Press.
51. Popov, V. I., and Stewart, M. G. (2009). Complexity of contacts between synaptic boutons and dendritic spines in adult rat hippocampus: three-dimensional reconstructions from serial ultrathin sections in vivo. Synapse 63, 369-377. doi: 10. 1002/syn. 20613.
52. Racz, B., and Weinberg, R. J. (2013). Microdomains in forebrain spines: an ultrastructural perspective. Mol. Neurobiol. 47, 77-89. doi: 10. 1007/s12035-012-8345-y.
53. Rochefort, N. L., and Konnerth, A. (2012). Dendritic spines: from structure to in vivofunction. EMBO Rep. 13, 699-708. doi: 10. 1038/embor. 2012. 102.
54. Rusakov, D. A., Stewart, M. G., and Korogod, S. M. (1996). Branching of active dendritic spines as a mechanism for controlling synaptic efficacy. Neuroscience 75, 315-323. doi: 10. 1016/0306-4522(96)00253-9.
55. Sanai, N., Nguyen, T., Ihrie, R. A., Mirzadeh, Z., Tsai, H. H., Wong, M., et al. (2011). Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478, 382-386. doi: 10. 1038/nature10487.
56. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682. doi: 10. 1038/nmeth. 2019.
57. Somogyi, P., and Hodgson, A. J. (1985). Antisera to gamma-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex. J. Histochem. Cytochem. 33, 249-257. doi: 10. 1177/33. 3. 2579124.
58. Sonomura, T., Furuta, T., Nakatani, I., Yamamoto, Y., Unzai, T., Matsuda, W., et al. (2013). Correlative analysis of immunoreactivity in confocal laser-scanning microscopy and scanning electron microscopy with focused ion beam milling. Front. Neural Circuits 7: 26. doi: 10. 3389/fncir. 2013. 00026.
59. Southwell, D. G., Nicholas, C. R., Basbaum, A. I., Stryker, M. P., Kriegstein, A. R., Rubenstein, J. L., et al. (2014). Interneurons from embryonic development to cell-based therapy. Science 344: 1240622. doi: 10. 1126/science. 1240622.
60. Spalding, K. L., Bergmann, O., Alkass, K., Bernard, S., Salehpour, M., Huttner, H. B., et al. (2013). Dynamics of hippocampal neurogenesis in adult humans. Cell 153, 1219-1227. doi: 10. 1016/j. cell. 2013. 05. 002.
61. Stevens, J. K., Davis, T. L., Friedman, N., and Sterling, P. (1980). A systematic approach to reconstructing microcircuitry by electron microscopy of serial sections. Brain Res. 2, 265-293. doi: 10. 1016/0165-0173(80)90010-7.
62. Sun, G. J., Sailor, K. A., Mahmood, Q. A., Chavali, N., Christian, K. M., Song, H., et al. (2013). Seamless reconstruction of intact adult-born neurons by serial end-block imaging reveals complex axonal guidance and development in the adult hippocampus. J. Neurosci. 33, 11400-11411. doi: 10. 1523/JNEUROSCI. 1374-13. 2013.
63. Teixeira, C. M., Kron, M. M., Masachs, N., Zhang, H., Lagace, D. C., Martinez, A., et al. (2012). Cell-autonomous inactivation of the reelin pathway impairs adult neurogenesis in the hippocampus. J. Neurosci. 32, 12051-12065. doi: 10. 1523/JNEUROSCI. 1857-12. 2012.
64. Toni, N., Buchs, P. A., Nikonenko, I., Bron, C. R., and Muller, D. (1999). LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402, 421-425. doi: 10. 1038/46574.
65. Toni, N., Laplagne, D. A., Zhao, C., Lombardi, G., Ribak, C. E., Gage, F. H., et al. (2008). Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat. Neurosci. 11, 901-907. doi: 10. 1038/nn. 2156.
66. Toni, N., and Sultan, S. (2011). Synapse formation on adult-born hippocampal neurons. Eur. J. Neurosci. 33, 1062-1068. doi: 10. 1111/j. 1460-9568. 2011. 07604. x.
67. Toni, N., Teng, E. M., Bushong, E. A., Aimone, J. B., Zhao, C., Consiglio, A., et al. (2007). Synapse formation on neurons born in the adult hippocampus. Nat. Neurosci. 10, 727-734. doi: 10. 1038/nn1908.
68. Trommald, M., and Hulleberg, G. (1997). Dimensions and density of dendritic spines from rat dentate granule cells based on reconstructions from serial electron micrographs. J. Comp. Neurol. 377, 15-28.
69. Trommald, M., Hulleberg, G., and Andersen, P. (1996). Long-term potentiation is associated with new excitatory spine synapses on rat dentate granule cells. Learn. Mem. 3, 218-228. doi: 10. 1101/lm. 3. 2-3. 218.
70. Van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., and Gage, F. H. (2002). Functional neurogenesis in the adult hippocampus. Nature 415, 1030-1034. doi: 10. 1038/4151030a.
71. Wadell, H. (1935). Volume, shape, and roundness of quartz particles. J. Geol. 43, 250-280. doi: 10. 1086/624298.
72. Yasumatsu, N., Matsuzaki, M., Miyazaki, T., Noguchi, J., and Kasai, H. (2008). Principles of long-term dynamics of dendritic spines. J. Neurosci. 28, 13592-13608. doi: 10. 1523/JNEUROSCI. 0603-08. 2008.
73. Yuste, R., and Majewska, A. (2001). On the function of dendritic spines. Neuroscientist 7, 387-395. doi: 10. 1177/107385840100700508.
74. Zhao, C., Deng, W., and Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660. doi: 10. 1016/j. cell. 2008. 01. 033.
75. Zhao, C., Jou, J., Wolff, L. J., Sun, H., and Gage, F. H. (2014). Spine morphogenesis in newborn granule cells is differentially regulated in the outer and middle molecular layers. J. Comp. Neurol. 522, 2756-2766. doi: 10. 1002/cne. 23581.
76. Zhao, C., Teng, E. M., Summers, R. G. Jr., Ming, G. L., and Gage, F. H. (2006). Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J. Neurosci. 26, 3-11. doi: 10. 1523/JNEUROSCI. 3648-05. 2006.
77. Ziv, N. E., and Smith, S. J. (1996). Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17, 91-102. doi: 10. 1016/S0896-6273(00)80283-4.