Seamless reconstruction of intact adult-born neurons by serial end-block imaging reveals complex axonal guidance and development in the adult hippocampus

Journal of Neuroscience

Volumn 33, Issue 28, 2013, Pages 11400-11411

  Sun, Gerald J ^a,b   Sailor, Kurt A ^a,b,c   Mahmood, Qasim A ^a   Chavali, Nikhil ^a   Christian, Kimberly M ^a,b   Song, Hongjun ^a,b,c   Ming, Guo Li ^a,b,c  

^a Institute for Cell Engineering   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Diana Helis Henry Medical Research Foundation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GREEN FLUORESCENT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; FEMALE; GRANULE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LASER MICROSCOPY; MICROTOME; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NERVE FIBER; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL; SERIAL END BLOCK IMAGING; WOODCHUCK HEPATITIS;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; AXONS; FEMALE; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; NEUROGENESIS; NEURONS;

EID: 84880433749     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1374-13.2013     Document Type: Article

References (38)

1. Acsády L, Kamondi A, Sík A, Freund T, Buzsáki G (1998) GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci 18:3386-3403. Medline
2. Aimone JB, Deng W, Gage FH (2011) Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70:589-596. CrossRef Medline
3. Blackstad TW, Brink K, Hem J, Jeune B (1970) Distribution of hippocampal mossy fibers in the rat. An experimental study with silver impregnation methods. J Comp Neurol 138:433-449. CrossRef Medline
4. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185-193. CrossRef Medline
5. Bonaguidi MA, Song J, Ming GL, Song H (2012) A unifying hypothesis on mammalian neural stem cell properties in the adult hippocampus. Curr Opin Neurobiol 22:754-761. CrossRef Medline
6. Chung K, Wallace J, Kim SY, Kalyanasundaram S, Andalman AS, Davidson TJ, Mirzabekov JJ, Zalocusky KA, Mattis J, Denisin AK, Pak S, Bernstein H, Ramakrishnan C, Grosenick L, Gradinaru V, Deisseroth K (2013) Structural and molecular interrogation of intact biological systems. Nature 497:332-337. CrossRef
7. Claiborne BJ, Amaral DG, Cowan WM (1986) A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. J Comp Neurol 246:435-458. CrossRef Medline
8. Duan X, Chang JH, Ge S, Faulkner RL, Kim JY, Kitabatake Y, Liu XB, Yang CH, Jordan JD, Ma DK, Liu CY, Ganesan S, Cheng HJ, Ming GL, Lu B, Song H (2007) Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130:1146-1158. CrossRef Medline
9. Emmenlauer M, Ronneberger O, Ponti A, Schwarb P, Griffa A, Filippi A, Nitschke R, Driever W, Burkhardt H (2009) XuvTools: free, fast and reliable stitching of large 3D datasets. J Microsc 233:42-60. CrossRef Medline
10. Espósito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF (2005) Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25:10074-10086. CrossRef Medline
11. Faulkner RL, Jang MH, Liu XB, Duan X, Sailor KA, Kim JY, Ge S, Jones EG, Ming GL, Song H, Cheng HJ (2008) Development of hippocampal mossy fiber synaptic outputs by new neurons in the adult brain. Proc Natl Acad Sci U S A 105:14157-14162. CrossRef Medline
12. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589-593. CrossRef Medline
13. Ge S, Yang CH, Hsu KS, Ming GL, Song H (2007) A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54:559-566. CrossRef Medline
14. Gu Y, Arruda-Carvalho M, Wang J, Janoschka SR, Josselyn SA, Frankland PW, Ge S (2012) Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci 15:1700-1706. CrossRef Medline
15. Hama H, Kurokawa H, Kawano H, Ando R, Shimogori T, Noda H, Fukami K, Sakaue-Sawano A, Miyawaki A (2011) Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nat Neurosci 14:1481-1488. CrossRef Medline
16. Hastings NB, Gould E (1999) Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 413:146-154. CrossRef Medline
17. Henze DA, Urban NN, Barrionuevo G (2000) The multifarious hippocampal mossy fiber pathway: a review. Neuroscience 98:407-427. CrossRef Medline
18. Kim JY, Liu CY, Zhang F, Duan X, Wen Z, Song J, Feighery E, Lu B, Rujescu D, St Clair D, Christian K, Callicott JH, Weinberger DR, Song H, Ming GL (2012) Interplay between DISC1 and GABA signaling regulates neurogenesis in mice and risk for schizophrenia. Cell 148:1051-1064. CrossRef Medline
19. Kron MM, Zhang H, Parent JM (2010) The developmental stage of dentate granule cells dictates their contribution to seizure-induced plasticity. J Neurosci 30:2051-2059. CrossRef Medline
20. Kuwajima T, Sitko AA, Bhansali P, Jurgens C, Guido W, Mason C (2013) ClearT: a detergentand solvent-free clearing method for neuronal and non-neuronal tissue. Development 140:1364-1368. CrossRef Medline
21. Lorente de Nó R (1934) Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J Psychol Neurol 45:381-438.
22. Luzzati F, Fasolo A, Peretto P (2011) Combining confocal laser scanning microscopy with serial section reconstruction in the study of adult neurogenesis. Front Neurosci 5:70. Medline
23. Marín-Burgin A, Mongiat LA, Pardi MB, Schinder AF (2012) Unique processing during a period of high excitation/inhibition balance in adultborn neurons. Science 335:1238-1242. CrossRef Medline
24. Markakis EA, Gage FH (1999) Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J Comp Neurol 406:449-460. CrossRef Medline
25. McLardy T (1963) Some cells and fiber peculiarities of uncal hippocampus. Progr Brain Res 3:71-88. CrossRef
26. McLardy T, Kilmer WL (1970) Hippocampal circuitry. Am Psychol 25:563-566. CrossRef Medline
27. Ming GL, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687-702. CrossRef Medline
28. Piatti VC, Davies-Sala MG, Espósito MS, Mongiat LA, Trinchero MF, Schinder AF (2011) The timing for neuronal maturation in the adult hippocampus is modulated by local network activity. J Neurosci 31:7715-7728. CrossRef Medline
29. Ragan T, Kadiri LR, Venkataraju KU, Bahlmann K, Sutin J, Taranda J, Arganda-Carreras I, Kim Y, Seung HS, Osten P (2012) Serial twophoton tomography for automated ex vivo mouse brain imaging. Nat Methods.
30. Ramóny Cajal S (1893) Estructura del asta de Ammon fascia dentata. Am Soc Esp Hist Nat 22:53-114.
31. Römer B, Krebs J, Overall RW, Fabel K, Babu H, Overstreet-Wadiche L, Brandt MD, Williams RW, Jessberger S, Kempermann G (2011) Adult hippocampal neurogenesis and plasticity in the infrapyramidal bundle of the mossy fiber projection: I. Co-regulation by activity. Front Neurosci 5:107. Medline
32. Sahay A, Wilson DA, Hen R (2011) Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 70:582-588. CrossRef Medline
33. Swanson LW, Wyss JM, Cowan WM (1978) An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J Comp Neurol 181:681-715. CrossRef Medline
34. Tamamaki N, Nojyo Y (1991) Crossing fiber arrays in the rat hippocampus as demonstrated by three-dimensional reconstruction. J Comp Neurol 303:435-442. CrossRef Medline
35. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123-1133. CrossRef Medline
36. Toni N, Laplagne DA, Zhao C, Lombardi G, Ribak CE, Gage FH, Schinder AF (2008) Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci 11:901-907. CrossRef Medline
37. Zhao C, Teng EM, Summers RG Jr, Ming GL, Gage FH (2006) Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26:3-11. CrossRef Medline
38. Zhou M, Li W, Huang S, Song J, Kim JY, Tian X, Kang E, Sano Y, Liu C, Balaji J, Wu S, Zhou Y, Zhou Y, Parivash SN, Ehninger D, He L, Song H, Ming GL, Silva AJ (2013) mTOR inhibition ameliorates cognitive and affective deficits caused by Disc1 knockdown in adult-born dentate granule neurons. Neuron 77:647-654. CrossRef Medline