Saturated Reconstruction of a Volume of Neocortex

Cell

Volumn 162, Issue 3, 2015, Pages 648-661

  Kasthuri, Narayanan ^a,g   Hayworth, Kenneth Jeffrey ^a,h   Berger, Daniel Raimund ^a,e   Schalek, Richard Lee ^a   Conchello, José Angel ^a   Knowles Barley, Seymour ^a   Lee, Dongil ^a   Vázquez Reina, Amelio ^b   Kaynig, Verena ^b   Jones, Thouis Raymond ^a,b   Roberts, Mike ^b,i   Morgan, Josh Lyskowski ^a   Tapia, Juan Carlos ^a,j   Seung, H Sebastian ^e,k   Roncal, William Gray ^c,l   Vogelstein, Joshua Tzvi ^f,m   Burns, Randal ^c   Sussman, Daniel Lewis ^d   Priebe, Carey Eldin ^c   Pfister, Hanspeter ^b   Lichtman, Jeff William ^a   more..

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c Johns Hopkins University   (United States)

^d HARVARD UNIVERSITY   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h Columbia University ^*  (United States)

ⁱ Stanford University   (United States)

^j Applied Physics Laboratory ^*  (United States)

^k Princeton University   (United States)

^l JOHNS HOPKINS UNIVERSITY APPLIED PHYSICS LABORATORY   (United States)

^m Johns Hopkins University   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOTECHNOLOGY; BRAIN SIZE; BRAIN SLICE; BRAIN TISSUE; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; GLIA; HIPPOCAMPUS; IMAGE RECONSTRUCTION; MITOCHONDRION; MOUSE; NEOCORTEX; NERVE FIBER; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SOMATOSENSORY CORTEX; SYNAPSE VESICLE; YOUNG ADULT; ANIMAL; AUTOMATION; CYTOLOGY; MICROTOMY; NERVE CELL; PROCEDURES; SCANNING ELECTRON MICROSCOPY; SYNAPSE; ULTRASTRUCTURE;

ANIMALS; AUTOMATION; AXONS; DENDRITES; MICE; MICROSCOPY, ELECTRON, SCANNING; MICROTOMY; NEOCORTEX; NEURONS; SYNAPSES; SYNAPTIC VESICLES;

EID: 84938233335     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.06.054     Document Type: Article

References (62)

1. J.R. Anderson, B.W. Jones, C.B. Watt, M.V. Shaw, J.H. Yang, D. Demill, J.S. Lauritzen, Y. Lin, K.D. Rapp, D. Mastronarde, and et al. Exploring the retinal connectome Mol. Vis. 17 2011 355 379
2. R. Araya, J. Jiang, K.B. Eisenthal, and R. Yuste The spine neck filters membrane potentials Proc. Natl. Acad. Sci. USA 103 2006 17961 17966
3. G.A. Ascoli, D.E. Donohue, and M. Halavi NeuroMorpho.Org: a central resource for neuronal morphologies J. Neurosci. 27 2007 9247 9251
4. M. Beierlein, J.R. Gibson, and B.W. Connors Two dynamically distinct inhibitory networks in layer 4 of the neocortex J. Neurophysiol. 90 2003 2987 3000
5. R. Benavides-Piccione, I. Ballesteros-Yáñez, J. DeFelipe, and R. Yuste Cortical area and species differences in dendritic spine morphology J. Neurocytol. 31 2002 337 346
6. T. Binzegger, R.J. Douglas, and K.A. Martin A quantitative map of the circuit of cat primary visual cortex J. Neurosci. 24 2004 8441 8453
7. D.D. Bock, W.C. Lee, A.M. Kerlin, M.L. Andermann, G. Hood, A.W. Wetzel, S. Yurgenson, E.R. Soucy, H.S. Kim, and R.C. Reid Network anatomy and in vivo physiology of visual cortical neurons Nature 471 2011 177 182
8. V. Braitenberg, and A. Schuz Cortex: Statistics and Geometry of Neuronal Connectivity 1998 Springer Berlin
9. K.L. Briggman, M. Helmstaedter, and W. Denk Wiring specificity in the direction-selectivity circuit of the retina Nature 471 2011 183 188
10. Burns, R., Roncal, W.G., Kleissas, D., Lillaney, K., Manavalan, P., Perlman, E., Berger, D.R., Bock, D.D., Chung, K., Grosenick, L., et al. (2013). The open connectome project data cluster: Scalable analysis and vision for high-throughput neuroscience. A. Szalay, T. Budavari, M. Balazinska, A. Meliou, and A. Sacan, eds. Proceedings of the 25th International Conference on Scientific and Statistical Database Management.
11. R.S. Cajal Textura del sistema nervioso del hombre y de los vertebrados 1899 Moya Madrid
12. M.E. Chicurel, and K.M. Harris Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus J. Comp. Neurol. 325 1992 169 182
13. H. Colman, J. Nabekura, and J.W. Lichtman Alterations in synaptic strength preceding axon withdrawal Science 275 1997 356 361
14. N.M. da Costa, and K.A. Martin Sparse reconstruction of brain circuits: or, how to survive without a microscopic connectome Neuroimage 80 2013 27 36
15. J.K. Deans, A.D. Powell, and J.G. Jefferys Sensitivity of coherent oscillations in rat hippocampus to AC electric fields J. Physiol. 583 2007 555 565
16. J. DeFelipe, and I. Fariñas The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs Prog. Neurobiol. 39 1992 563 607
17. S. Druckmann, L. Feng, B. Lee, C. Yook, T. Zhao, J.C. Magee, and J. Kim Structured synaptic connectivity between hippocampal regions Neuron 81 2014 629 640
18. A.L. Eberle, S. Mikula, R. Schalek, J.W. Lichtman, M.L. Tate, and D. Zeidler High-resolution, high-throughput imaging with a multibeam scanning electron microscope J. Microsc. 2015 10.1111/jmi.12224 Published online January 27, 2015
19. P.L. Friedman, and M.H. Ellisman Enhanced visualization of peripheral nerve and sensory receptors in the scanning electron microscope using cryofracture and osmium-thiocarbohydrazide-osmium impregnation J. Neurocytol. 10 1981 111 131
20. A.I. Gulyás, M. Megías, Z. Emri, and T.F. Freund Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus J. Neurosci. 19 1999 10082 10097
21. Haehn, D., Knowles-Barley, S., Roberts, M., Beyer, J., Kasthuri, N., Lichtman, J.W., and Pfister, H. (2014). Design and evaluation of interactive proofreading tools for connectomics. Proceedings of IEEE Transactions on Visualization and Computer Graphics.
22. K. Hashimoto, and M. Kano Postnatal development and synapse elimination of climbing fiber to Purkinje cell projection in the cerebellum Neurosci. Res. 53 2005 221 228
23. K.J. Hayworth, J.L. Morgan, R. Schalek, D.R. Berger, D.G. Hildebrand, and J.W. Lichtman Imaging ATUM ultrathin section libraries with WaferMapper: a multi-scale approach to EM reconstruction of neural circuits Front. Neural Circuits 8 2014 68
24. M. Helmstaedter, K.L. Briggman, and W. Denk High-accuracy neurite reconstruction for high-throughput neuroanatomy Nat. Neurosci. 14 2011 1081 1088
25. M. Helmstaedter, K.L. Briggman, S.C. Turaga, V. Jain, H.S. Seung, and W. Denk Connectomic reconstruction of the inner plexiform layer in the mouse retina Nature 500 2013 168 174
26. S.L. Hill, Y. Wang, I. Riachi, F. Schürmann, and H. Markram Statistical connectivity provides a sufficient foundation for specific functional connectivity in neocortical neural microcircuits Proc. Natl. Acad. Sci. USA 109 2012 E2885 E2894
27. Kaynig, V., Vazquez-Reina, A., Knowles-Barley, S., Roberts, M., Jones, T.R., Kasthuri, N., Miller, E., Lichtman, J.W., and Pfister, H. (2013). Large scale automatic reconstruction of neuronal processes from electron microscopy images. arXiv, arXiv:1303.7186, http://arxiv.org/abs/1303.7186.
28. J.S. Kim, M.J. Greene, A. Zlateski, K. Lee, M. Richardson, S.C. Turaga, M. Purcaro, M. Balkam, A. Robinson, B.F. Behabadi, et al. EyeWirers Space-time wiring specificity supports direction selectivity in the retina Nature 509 2014 331 336
29. P. Krieger, T. Kuner, and B. Sakmann Synaptic connections between layer 5B pyramidal neurons in mouse somatosensory cortex are independent of apical dendrite bundling J. Neurosci. 27 2007 11473 11482
30. Z. Li, K. Okamoto, Y. Hayashi, and M. Sheng The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses Cell 119 2004 873 887
31. J.W. Lichtman, H. Pfister, and N. Shavit The big data challenges of connectomics Nat. Neurosci. 17 2014 1448 1454 10.1038/nn.3837
32. Marblestone, A., Daugharthy, E., Kalhor, R., Peikon, I., Kebschull, J., Shipman, S., Mishchenko, Y., Dalrymple, D., Zamft, B., Kording, K., Boyden, E., Zador, A., and Church, G. (2013). Conneconomics: The economics of large-scale neural connectomics. http://dx.doi.org/10.1101/001214.
33. H. Markram, J. Lubke, M. Frotscher, A. Roth, and B. Sakmann Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex J. Physiol. 500 Pt 2 1997 409 440
34. H. Markram, Y. Wang, and M. Tsodyks Differential signaling via the same axon of neocortical pyramidal neurons Proc. Natl. Acad. Sci. USA 95 1998 5323 5328
35. Markram, H., Ailamaki A., Alvandpour A., Amunts K., Andreoni W., Ashburner J., Axer M., Baaden M., Badia R., Bartolome J., et al. (2012). The human brain project: A report to the European Commission. https://www.humanbrainproject.eu/documents/10180/17648/TheHBPReport-LR.pdf/18e5747e-10af-4bec-9806-d03aead57655.
36. M. Megías, Z. Emri, T.F. Freund, and A.I. Gulyás Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells Neuroscience 102 2001 527 540
37. Y. Mishchenko Automation of 3D reconstruction of neural tissue from large volume of conventional serial section transmission electron micrographs J. Neurosci. Methods 176 2009 276 289
38. Y. Mishchenko, T. Hu, J. Spacek, J. Mendenhall, K.M. Harris, and D.B. Chklovskii Ultrastructural analysis of hippocampal neuropil from the connectomics perspective Neuron 67 2010 1009 1020
39. V.B. Mountcastle The columnar organization of the neocortex Brain 120 1997 701 722
40. J. Nunez-Iglesias, R. Kennedy, S.M. Plaza, A. Chakraborty, and W.T. Katz Graph-based active learning of agglomeration (GALA): a Python library to segment 2D and 3D neuroimages Front. Neuroinform. 8 2014 34
41. A. Peters, K. Josephson, and S.L. Vincent Effects of aging on the neuroglial cells and pericytes within area 17 of the rhesus monkey cerebral cortex Anat. Rec. 229 1991 384 398
42. S.M. Plaza, L.K. Scheffer, and D.B. Chklovskii Toward large-scale connectome reconstructions Curr. Opin. Neurobiol. 25 2014 201 210
43. V.I. Popov, and M.G. Stewart Complexity of contacts between synaptic boutons and dendritic spines in adult rat hippocampus: three-dimensional reconstructions from serial ultrathin sections in vivo Synapse 63 2009 369 377
44. D.P. Purpura Dendritic differentiation in human cerebral cortex: normal and aberrant developmental patterns Adv. Neurol. 12 1975 91 134
45. C. Sherrington The Integrative Action of the Nervous System 1906 Yale University Press Yale
46. Sinha, A., Roncal, W.G., Kasthuri, N., Lichtman, J.W., Burns, R., and Kazhdan, M. (2013). Automatic annotation of axoplasmic reticula in pursuit of connectomes using high resolution neural EM data. 3rd Annual Hopkins Imaging Conference.
47. J.F. Smiley, and P.S. Goldman-Rakic Heterogeneous targets of dopamine synapses in monkey prefrontal cortex demonstrated by serial section electron microscopy: a laminar analysis using the silver-enhanced diaminobenzidine sulfide (SEDS) immunolabeling technique Cereb. Cortex 3 1993 223 238
48. S. Song, P.J. Sjöström, M. Reigl, S. Nelson, and D.B. Chklovskii Highly nonrandom features of synaptic connectivity in local cortical circuits PLoS Biol. 3 2005 e68
49. K.E. Sorra, J.C. Fiala, and K.M. Harris Critical assessment of the involvement of perforations, spinules, and spine branching in hippocampal synapse formation J. Comp. Neurol. 398 1998 225 240
50. A. Stepanyants, and D.B. Chklovskii Neurogeometry and potential synaptic connectivity Trends Neurosci. 28 2005 387 394
51. A. Stepanyants, G. Tamás, and D.B. Chklovskii Class-specific features of neuronal wiring Neuron 43 2004 251 259
52. S.Y. Takemura, A. Bharioke, Z. Lu, A. Nern, S. Vitaladevuni, P.K. Rivlin, W.T. Katz, D.J. Olbris, S.M. Plaza, P. Winston, and et al. A visual motion detection circuit suggested by Drosophila connectomics Nature 500 2013 175 181
53. J.C. Tapia, N. Kasthuri, K.J. Hayworth, R. Schalek, J.W. Lichtman, S.J. Smith, and J. Buchanan High-contrast en bloc staining of neuronal tissue for field emission scanning electron microscopy Nat. Protoc. 7 2012 193 206
54. G.S. Tomassy, D.R. Berger, H.H. Chen, N. Kasthuri, K.J. Hayworth, A. Vercelli, H.S. Seung, J.W. Lichtman, and P. Arlotta Distinct profiles of myelin distribution along single axons of pyramidal neurons in the neocortex Science 344 2014 319 324
55. S.G. Turney, and J.W. Lichtman Reversing the outcome of synapse elimination at developing neuromuscular junctions in vivo: evidence for synaptic competition and its mechanism PLoS Biol. 10 2012 e1001352
56. C. van Vreeswijk, and H. Sompolinsky Chaos in neuronal networks with balanced excitatory and inhibitory activity Science 274 1996 1724 1726
57. A. Vanharreveld, J. Crowell, and S.K. Malhotra A study of extracellular space in central nervous tissue by freeze-substitution J. Cell Biol. 25 1965 117 137
58. Vazquez-Reina, A., Gelbart, M., Huang, D., Lichtman, J., Miller, E.L., Pfister, H. (2011). Segmentation fusion for connectomics. Proceedings of IEEE International Conference on Computer Vision, 177-184.
59. 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
60. M. Wehr, and A.M. Zador Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex Nature 426 2003 442 446
61. J.G. White, E. Southgate, J.N. Thomson, and S. Brenner The structure of the nervous system of the nematode Caenorhabditis elegans Philos. Trans. R. Soc. Lond. B Biol. Sci. 314 1986 1 340
62. M.E. Williams, J. de Wit, and A. Ghosh Molecular mechanisms of synaptic specificity in developing neural circuits Neuron 68 2010 9 18