A resource from 3D electron microscopy of hippocampal neuropil for user training and tool development

Scientific Data

Volumn 2, Issue , 2015, Pages

  Harris, Kristen M ^a   Spacek, Josef ^b   Bell, Maria Elizabeth ^a   Parker, Patrick H ^a   Lindsey, Laurence F ^a,e   Baden, Alexander D ^c   Vogelstein, Joshua T ^d   Burns, Randal ^c  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b CHARLES UNIVERSITY   (Czech Republic)

^c Johns Hopkins University   (United States)

^d Johns Hopkins University   (United States)

^e GOOGLE INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANATOMY AND HISTOLOGY; ANIMAL; COMPUTER PROGRAM; ELECTRON MICROSCOPY; HIPPOCAMPUS; IMAGE PROCESSING; NEUROPIL; RAT;

ANIMALS; HIPPOCAMPUS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, ELECTRON; NEUROPIL; RATS; SOFTWARE;

EID: 84955239846     PISSN: None     EISSN: 20524463     Source Type: Journal    
DOI: 10.1038/sdata.2015.46     Document Type: Article

References (71)

1. Chiang, R. G., & Govind, C. K. Reorganization of synaptic ultrastructure at facilitated lobster neuromuscular terminals. J. Neurocytol. 15, 63-74 (1986).
2. Jarrell, T. A., et al. The connectome of a decision-making neural network. Science 337, 437-444 (2012).
3. Bundgaard, M. The three-Dimensional organization of tight junctions in a capillary endothelium revealed by serial-section electron microscopy. J Ultrastruct. Res. 88, 1-17 (1984).
4. Keddie, F. M., & Barajas, L. Three-Dimensional reconstruction of Pityrosporum yeast cells based on serial section electron microscopy. J. Ultrastruct. Res. 29, 260-275 (1969).
5. Novikoff, P. M., Novikoff, A. B., Quintana, N., & Hauw, J. J. Golgi apparatus, GERL, and lysosomes of neurons in rat dorsal root ganglia, studied by thick section and thin section cytochemistry. J. Cell Biol. 50, 859-886 (1971).
6. Osafune, T., & Schwartzbach, S. D. Serial section immunoelectron microscopy of algal cells. Methods Mol. Biol. 657, 259-274 (2010).
7. Spacek, J., & Lieberman, A. R. Spine-like astrocytic protrusions into large axon terminals. Z. Zellforsch. Mikrosk. Anat. 115, 494-500 (1971).
8. Spacek, J., & Lieberman, A. R. Ultrastructure and three-Dimensional organization of synaptic glomeruli in rat somatosensory thalamus. J. Anat. 117, 487-516 (1974).
9. Starborg, T., Lu, Y., Huffman, A., Holmes, D. F., & Kadler, K. E. Electron microscope 3D reconstruction of branched collagen fibrils in vivo. Scand. J Med. Sci. Sports 19, 547-552 (2009).
10. Thaemert, J. C. Ultrastructural interrelationships of nerve processes and smooth muscle cells in three dimensions. J. Cell Biol. 28, 37-49 (1966).
11. Mishchenko, Y., et al. Ultrastructural analysis of hippocampal neuropil from the connectomics perspective. Neuron 67, 1009-1020 (2010).
12. Marc, R. E., Jones, B. W., Lauritzen, J. S., Watt, C. B., & Anderson, J. R. Building retinal connectomes. Curr. Opin. Neurobiol. 22, 568-574 (2012).
13. Bock, D. D., et al. Network anatomy and in vivo physiology of visual cortical neurons. Nature 471, 177-182 (2011).
14. Briggman, K. L., Helmstaedter, M., & Denk, W. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471, 183-188 (2011).
15. Helmstaedter, M., Briggman, K. L., & Denk, W. 3D structural imaging of the brain with photons and electrons. Curr. Opin. Neurobiol. 18, 633-641 (2008).
16. Ostroff, L. E., Fiala, J. C., Allwardt, B., & Harris, K. M. Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35, 535-545 (2002).
17. Knott, G. W., Quairiaux, C., Genoud, C., & Welker, E. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 34, 265-273 (2002).
18. Bourne, J. N., & Harris, K. M. Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus 21, 354-373 (2011).
19. Ostroff, L. E., Cain, C. K., Bedont, J., Monfils, M. H., & Ledoux, J. E. Fear and safety learning differentially affect synapse size and dendritic translation in the lateral amygdala. Proc. Natl. Acad. Sci. USA 107, 9418-9423 (2010).
20. Ostroff, L. E., Cain, C. K., Jindal, N., Dar, N., & Ledoux, J. E. Stability of presynaptic vesicle pools and changes in synapse morphology in the amygdala following fear learning in adult rats. J. Comp Neurol. 520, 295-314 (2012).
21. Spacek, J. Ultrastructural pathology of dendritic spines in epitumorous human cerebral cortex. Acta Neuropathol. 73, 77-85 (1987).
22. Witcher, M. R., et al. Three-Dimensional relationships between perisynaptic astroglia and human hippocampal synapses. Glia 58, 572-587 (2010).
23. Kuwajima, M., Spacek, J., & Harris, K. M. Beyond counts and shapes: Studying pathology of dendritic spines in the context of the surrounding neuropil through serial section electron microscopy. Neurosci 251, 75-89 (2013).
24. Fiala, J. C., Feinberg, M., Peters, A., & Barbas, H. Mitochondrial degeneration in dystrophic neurites of senile plaques may lead to extracellular deposition of fine filaments. Brain Struct. Funct. 212, 195-207 (2007).
25. Nuntagij, P., et al. Amyloid deposits show complexity and intimate spatial relationship with dendrosomatic plasma membranes: an electron microscopic 3D reconstruction analysis in 3xTg-AD mice and aged canines. J Alzheimers. Dis. 16, 315-323 (2009).
26. Hara, Y., et al. Synaptic characteristics of dentate gyrus axonal boutons and their relationships with aging, menopause, and memory in female rhesus monkeys. J Neurosci. 31, 7737-7744 (2011).
27. Popov, V. I., Kleschevnikov, A. M., Klimenko, O. A., Stewart, M. G., & Belichenko, P. V. Three-Dimensional synaptic ultrastructure in the dentate gyrus and hippocampal area CA3 in the Ts65Dn mouse model of Down syndrome. J Comp Neurol. 519, 1338-1354 (2011).
28. Villalba, R. M., & Smith, Y. Neuroglial plasticity at striatal glutamatergic synapses in Parkinson's disease. Front Syst. Neurosci 5, 68 (2011).
29. Burns, R., et al. The Open Connectome Project Data Cluster: Scalable Analysis and Vision for High-Throughput Neuroscience. Sci. Stat. Database. Manag. (2013).
30. Briggman, K. L., & Bock, D. D. Volume electron microscopy for neuronal circuit reconstruction. Curr. Opin. Neurobiol. 22, 154-161 (2012).
31. Tomassy, G. S., et al. Distinct profiles of myelin distribution along single axons of pyramidal neurons in the neocortex. Science 344, 319-324 (2014).
32. Lichtman, J. W., Pfister, H., & Shavit, N. The big data challenges of connectomics. Nat. Neurosci. 17, 1448-1454 (2014).
33. Helmstaedter, M. Cellular-resolution connectomics: challenges of dense neural circuit reconstruction. Nat. Methods 10, 501-507 (2013).
34. Burns, R., Vogelstein, J. T., & Szalay, A. S. From cosmos to connectomes: the evolution of data-intensive science. Neuron 83, 1249-1252 (2014).
35. Fiala, J. C., & Harris, K. M. Computer-Based Alignment and Reconstruction of Serial Sections. Microscopy and Analysis 87, 5-8 (2002).
36. Fiala, J. C., & Harris, K. M. Extending unbiased stereology of brain ultrastructure to three-Dimensional volumes. J. Am. Med. Inform. Assoc 8, 1-16 (2001).
37. Harris, K. M., & Stevens, J. K. Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9, 2982-2997 (1989).
38. Sorra, K. E., & Harris, K. M. Occurrence and three-Dimensional structure of multiple synapses between individual radiatum axons and their target pyramidal cells in hippocampal area CA1. J. Neurosci. 13, 3736-3748 (1993).
39. Shepherd, G. M., & Harris, K. M. Three-Dimensional structure and composition of CA3->CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J. Neurosci. 18, 8300-8310 (1998).
40. Lisman, J., & Harris, K. M. Quantal analysis and synaptic anatomy-integrating two views of hippocampal plasticity. Trends Neurosci. 16, 141-147 (1993).
41. Bourne, J. N., Chirillo, M. A., & Harris, K. M. Presynaptic ultrastructural plasticity along CA3->CA1 axons during long-Term potentiation in mature hippocampus. J Comp Neurol. 521, 3898-3912 (2013).
42. Harris, K. M., & Stevens, J. K. Dendritic spines of rat cerebellar Purkinje cells: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 8, 4455-4469 (1988).
43. Spacek, J., & Harris, K. M. Three-Dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J. Neurosci. 17, 190-203 (1997).
44. Cooney, J. R., Hurlburt, J. L., Selig, D. K., Harris, K. M., & Fiala, J. C. Endosomal compartments serve multiple hippocampal dendritic spines from a widespread rather than a local store of recycling membrane. J. Neurosci. 22, 2215-2224 (2002).
45. Park, M., et al. Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52, 817-830 (2006).
46. Cui-Wang, T., et al. Local zones of endoplasmic reticulum complexity confine cargo in neuronal dendrites. Cell 148, 309-321 (2012).
47. Bourne, J. N., Sorra, K. E., Hurlburt, J., & Harris, K. M. Polyribosomes are increased in spines of CA1 dendrites 2 h after the induction of LTP in mature rat hippocampal slices. Hippocampus 17, 1-4 (2007).
48. Spacek, J., & Harris, K. M. Three-Dimensional organization of cell adhesion junctions at synapses and dendritic spines in area CA1 of the rat hippocampus. J. Comp Neurol. 393, 58-68 (1998).
49. Franks, K. M., Stevens, C. F., & Sejnowski, T. J. Independent sources of quantal variability at single glutamatergic synapses. J. Neurosci. 23, 3186-3195 (2003).
50. Franks, K. M., Bartol, T. M. Jr., & Sejnowski, T. J. A Monte Carlo model reveals independent signaling at central glutamatergic synapses. Biophys. J. 83, 2333-2348 (2002).
51. Bell, M. E., et al. Dynamics of nascent and active zone ultrastructure as synapses enlarge during long-Term potentiation in mature hippocampus. J. Comp Neurol. 522, 3861-3884 (2014).
52. Kinney, J. P., et al. Extracellular sheets and tunnels modulate glutamate diffusion in hippocampal neuropil. J. Comp Neurol. 521, 448-464 (2013).
53. Ventura, R., & Harris, K. M. Three-Dimensional relationships between hippocampal synapses and astrocytes. J. Neurosci 19, 6897-6906 (1999).
54. Witcher, M. R., Kirov, S. A., & Harris, K. M. Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus. Glia 55, 13-23 (2007).
55. Cardona, A. Towards semi-Automatic reconstruction of neural circuits. Neuroinformatics 11, 31-33 (2013).
56. Saalfeld, S., Fetter, R., Cardona, A., & Tomancak, P. Elastic volume reconstruction from series of ultra-Thin microscopy sections. Nat. Methods 9, 717-720 (2012).
57. Harris, K. M., et al. Uniform serial sectioning for transmission electron microscopy. J. Neurosci. 26, 12101-12103 (2006).
58. Kuwajima, M., Mendenhall, J. M., Lindsey, L. F., & Harris, K. M. Automated transmission-mode scanning electron microscopy (tSEM) for large volume analysis at nanoscale resolution. PLoS. ONE. 8, e59573 (2013).
59. Fiala, J. C. Reconstruct: a free editor for serial section microscopy. J. Microsc. 218, 52-61 (2005).
60. Cardona, A., et al. TrakEM2 software for neural circuit reconstruction. PLoS. ONE 7, e38011 (2012).
61. Schindelin, J., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).
62. Fiala, J. C., & Harris, K. M. Cylindrical diameters method for calibrating section thickness in serial electron microscopy. J. Microsc. 202, 468-472 (2001).
63. Saalfeld, S., Cardona, A., Hartenstein, V., & Tomancak, P. CATMAID: collaborative annotation toolkit for massive amounts of image data. Bioinformatics 25, 1984-1986 (2009).
64. Bushong, E. A., Martone, M. E., & Ellisman, M. H. Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. International Journal of Developmental Neuroscience 22, 73-86 (2004).
65. Bushong, E. A., Martone, M. E., Jones, Y. Z., & Ellisman, M. H. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22, 183-192 (2002).
66. Boissonnat, J. D. Shape reconstruction from planar cross sections. Computer Vision, Graphics, and Image Processing 44, 1-29 (1988).
67. Fiala, J. C., et al. Timing of neuronal and glial ultrastructure disruption during brain slice preparation and recovery in vitro. J Comp Neurol 465, 90-103 (2003).
68. von Bartheld, C. S., & Altick, A. L. Multivesicular bodies in neurons: distribution, protein content, and trafficking functions. Prog. Neurobiol. 93, 313-340 (2011).
69. Peters, A., Palay, S. L., & Webster, H. d. The fine structure of the nervous system: The neurons and supporting cells (W.B.Saunders, Co., 1991).
70. Edwards, J., et al. VolRoverN: enhancing surface and volumetric reconstruction for realistic dynamical simulation of cellular and subcellular function. Neuroinformatics 12, 277-289 (2014).
71. Thorne, R. G., & Nicholson, C. In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space. Proc. Natl. Acad. Sci. USA 103, 5567-5572 (2006).