Continuous postnatal neurogenesis contributes to formation of the olfactory bulb neural circuits and flexible olfactory associative learning

Journal of Neuroscience

Volumn 34, Issue 17, 2014, Pages 5788-5799

  Sakamoto, Masayuki ^a,b   Ieki, Nao ^c   Miyoshi, Goichi ^d   Mochimaru, Daisuke ^c   Miyachi, Hitoshi ^a   Imura, Tetsuya ^e   Yamaguchi, Masahiro ^c   Fishell, Gord ^d   Mori, Kensaku ^c   Kageyama, Ryoichiro ^a,f,g   Imayoshi, Itaru ^a,f,g  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

^f JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^g KYOTO UNIVERSITY   (Japan)

Author keywords

Dentate gyrus; Hippocampus; Learning; Neural stem cells; Neurogenesis; Olfactory bulb

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CALBINDIN 1; CALRETICULIN; CRE RECOMBINASE; CYAN FLUORESCENT PROTEIN; DEOXYRIBONUCLEASE I; NEURON SPECIFIC ENOLASE; NEURON SPECIFIC NUCLEAR PROTEIN; REELIN; SYNAPTOBREVIN 2; SYNAPTOPHYSIN; TAMOXIFEN; TYPE II SITE SPECIFIC DEOXYRIBONUCLEASE; TYROSINE 3 MONOOXYGENASE; VESICULAR GLUTAMATE TRANSPORTER 1; VIRUS VECTOR;

ADULT; AGE DISTRIBUTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CONFOCAL LASER MICROSCOPY; CONTINUOUS POSTNATAL NEUROGENESIS; CONTROLLED STUDY; DENTATE GYRUS; DNA HYBRIDIZATION; EMBRYO; GENE MAPPING; GENE TARGETING; GENOTYPE; GRANULE CELL; HABITUATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; LEARNING AND MEMORY TEST; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEURULATION; NEWBORN; NONHUMAN; OLFACTORY BULB; OLFACTORY MEMORY; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STATE DEPENDENT LEARNING;

DENTATE GYRUS; HIPPOCAMPUS; LEARNING; NEURAL STEM CELLS; NEUROGENESIS; OLFACTORY BULB;

ANIMALS; ASSOCIATION LEARNING; CEREBRAL VENTRICLES; DENTATE GYRUS; INTERNEURONS; MALE; MICE; MICE, TRANSGENIC; NERVE NET; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; ODORS; OLFACTORY BULB; OLFACTORY PERCEPTION;

EID: 84899472458     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0674-14.2014     Document Type: Article

References (60)

1. Adam Y, Mizrahi A (2011) Long-term imaging reveals dynamic changes in the neuronal composition of the glomerular layer. J Neurosci 31:7967-7973. CrossRef Medline
2. Ahn S, Joyner AL (2005) In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437:894-897. CrossRef Medline
3. Alonso M, Lepousez G, Wagner S, Bardy C, Gabellec MM, Torquet N, Lledo PM (2012) Activation of adult-born neurons facilitates learning and memory. Nat Neurosci 15:899-904. CrossRef Medline
4. Anderson JC, Douglas RJ, Martin KA, Nelson JC (1994) Mapof the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex. J Comp Neurol 341:25-38. CrossRef Medline
5. Bagley J, LaRocca G, Jimenez DA, Urban NN (2007) Adult neurogenesis and specific replacement of interneuron subtypes in the mouse main olfactory bulb. BMC Neurosci 8:92. CrossRef Medline
6. Batista-Brito R, Close J, Machold R, Fishell G (2008) The distinct temporal origins of olfactory bulb interneuron subtypes. J Neurosci 28:3966-3975. CrossRef Medline
7. 3H-Thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp Brain Res 50:329-340. Medline
8. Boyd AM, Sturgill JF, Poo C, Isaacson JS (2012) Cortical feedback control of olfactory bulb circuits. Neuron 76:1161-1174. CrossRef Medline
9. Branda CS, Dymecki SM (2004) Talking about a revolution: the impact of site-specific recombinases on genetic analyses in mice. Dev Cell 6:7-28. CrossRef Medline
10. Breton-Provencher V, Saghatelyan A (2012) Newborn neurons in the adult olfactory bulb: unique properties for specific odor behavior. Behav Brain Res 227:480-489. CrossRef Medline
11. Brill MS, Snapyan M, Wohlfrom H, Ninkovic J, Jawerka M, Mastick GS, Ashery-Padan R, Saghatelyan A, Berninger B, Götz M (2008) A dlx2-and pax6-dependent transcriptional code for periglomerular neuron specification in the adult olfactory bulb. J Neurosci 28:6439-6452. CrossRef Medline
12. Egger V, Urban NN (2006) Dynamic connectivity in the mitral cell-granule cell microcircuit. Semin Cell Dev Biol 17:424-432. CrossRef Medline
13. Eyre MD, Antal M, Nusser Z (2008) Distinct deep short-axon cell subtypes of the main olfactory bulb provide novel intrabulbar and extrabulbar GABAergic connections. J Neurosci 28:8217-8229. CrossRef Medline
14. Eyre MD, Kerti K, Nusser Z (2009) Molecular diversity of deep short-axon cells of the rat main olfactory bulb. Eur J Neurosci 29:1397-1407. CrossRef Medline
15. Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV (2004) GFAPexpressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7:1233-1241. CrossRef Medline
16. Garthe A, Behr J, Kempermann G (2009) Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS One 4:e5464. CrossRef Medline
17. Gould E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8:481-488. CrossRef Medline
18. Huang L, Garcia I, Jen HI, Arenkiel BR (2013) Reciprocal connectivity between mitral cells and external plexiform layer interneurons in the mouse olfactory bulb. Front Neural Circuits 7:32. CrossRef Medline
19. Ihrie RA, Alvarez-Buylla A (2011) Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. Neuron 70:674-686. CrossRef Medline
20. Imamura F, Nagao H, Naritsuka H, Murata Y, Taniguchi H, Mori K (2006) A leucine-rich repeat membrane protein, 5T4, is expressed by a subtype of granule cells with dendritic arbors in specific strata of the mouse olfactory bulb. J Comp Neurol 495:754-768. CrossRef Medline
21. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11:1153-1161. CrossRef Medline
22. Imayoshi I, Sakamoto M, Yamaguchi M, Mori K, Kageyama R (2010) Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci 30:3489-3498. CrossRef Medline
23. Imayoshi I, Sakamoto M, Kageyama R (2011) Genetic methods to identify and manipulate newly born neurons in the adult brain. Front Neurosci 5:64. CrossRef Medline
24. Imayoshi I, Hirano K, Sakamoto M, Miyoshi G, Imura T, Kitano S, Miyachi H, Kageyama R (2012) A multifunctional teal-fluorescent Rosa26 reporter mouse line for Cre-and Flp-mediated recombination. Neurosci Res 73:78-84. CrossRef Medline
25. Isaacson JS, Strowbridge BW (1998) Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20:749-761. CrossRef Medline
26. Kato HK, Gillet SN, Peters AJ, Isaacson JS, Komiyama T (2013) Parvalbumin-expressing interneurons linearly control olfactory bulb output. Neuron 80:1218-1231. CrossRef Medline
27. Kohwi M, Petryniak MA, Long JE, Ekker M, Obata K, Yanagawa Y, Rubenstein JL, Alvarez-Buylla A (2007) A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1-and Dlx5/6-expressing progenitors. J Neurosci 27:6878-6891. CrossRef Medline
28. Kosaka K, Toida K, Aika Y, Kosaka T (1998) How simple is the organization of the olfactory glomerulus? The heterogeneity of so-called periglomerular cells. Neurosci Res 30:101-110. CrossRef Medline
29. Kosaka T, Kosaka K (2011) "Interneurons" in the olfactory bulb revisited. Neurosci Res 69:93-99. CrossRef Medline
30. Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149-184. CrossRef Medline
31. Lagace DC, Whitman MC, Noonan MA, Ables JL, DeCarolis NA, Arguello AA, Donovan MH, Fischer SJ, Farnbauch LA, Beech RD, DiLeone RJ, Greer CA, Mandyam CD, Eisch AJ (2007) Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J Neurosci 27:12623-12629. CrossRef Medline
32. Lazarini F, Lledo PM (2011) Is adult neurogenesis essential for olfaction? Trends Neurosci 34:20-30. CrossRef Medline
33. Lemasson M, Saghatelyan A, Olivo-Marin JC, Lledo PM (2005) Neonatal and adult neurogenesis provide two distinct populations of newborn neurons to the mouse olfactory bulb. J Neurosci 25:6816-6825. CrossRef Medline
34. Lledo PM, Alonso M, Grubb MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179-193. CrossRef Medline
35. Long JE, Garel S, Alvarez-Dolado M, Yoshikawa K, Osumi N, Alvarez-Buylla A, Rubenstein JL (2007) Dlx-dependent and-independent regulation of olfactory bulb interneuron differentiation. J Neurosci 27:3230-3243. CrossRef Medline
36. Manabe H, Kusumoto-Yoshida I, Ota M, Mori K (2011) Olfactory cortex generates synchronized top-down inputs to the olfactory bulb during slow-wave sleep. J Neurosci 31:8123-8133. CrossRef Medline
37. Mao J, Barrow J, McMahon J, Vaughan J, McMahon AP (2005) An ES cell system for rapid, spatial and temporal analysis of gene function in vitro and in vivo. Nucleic Acids Res 33:e155. CrossRef Medline
38. Markopoulos F, Rokni D, Gire DH, Murthy VN (2012) Functional properties of cortical feedback projections to the olfactory bulb. Neuron 76: 1175-1188. CrossRef Medline
39. Ming GL, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687-702. CrossRef Medline
40. Miyamichi K, Shlomai-Fuchs Y, Shu M, Weissbourd BC, Luo L, Mizrahi A (2013) Dissecting local circuits: parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 80:1232-1245. CrossRef Medline
41. Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J, Johnson JE, Machold RP, Fishell G (2010) Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 30:1582-1594. CrossRef Medline
42. Mori K, Kishi K, Ojima H (1983) Distribution of dendrites of mitral, displaced mitral, tufted, and granule cells in the rabbit olfactory bulb. J Comp Neurol 219:339-355. CrossRef Medline
43. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211. Medline
44. Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Rodriguez Barrera V, Chittajallu R, Iwamoto KS, McBain CJ, Fanselow MS, Tonegawa S (2012) Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149:188-201. CrossRef Medline
45. Ninkovic J, Mori T, Götz M (2007) Distinct modes of neuron addition in adult mouse neurogenesis. J Neurosci 27:10906-10911. CrossRef Medline
46. Nissant A, Bardy C, Katagiri H, Murray K, Lledo PM (2009) Adult neurogenesis promotes synaptic plasticity in the olfactory bulb. Nat Neurosci 12:728-730. CrossRef Medline
47. Orona E, Scott JW, Rainer EC (1983) Different granule cell populations innervate superficial and deep regions of the external plexiform layer in rat olfactory bulb. J Comp Neurol 217:227-237. CrossRef Medline
48. Pressler RT, StrowbridgeBW (2006) Blanes cells mediate persistent feedforward inhibition onto granule cells in the olfactory bulb. Neuron 49:889-904. CrossRef Medline
49. Rosselli-Austin L, Altman J (1979) The postnatal development of the main olfactory bulb of the rat. J Dev Physiol 1:295-313. Medline
50. Sakamoto M, Imayoshi I, Ohtsuka T, Yamaguchi M, Mori K, Kageyama R (2011) Continuous neurogenesis in the adult forebrain is required for innate olfactory responses. Proc Natl Acad Sci U S A 108:8479-8484. CrossRef Medline
51. Sawada M, Kaneko N, Inada H, Wake H, Kato Y, Yanagawa Y, Kobayashi K, Nemoto T, Nabekura J, Sawamoto K (2011) Sensory input regulates spatial and subtype-specific patterns of neuronal turnover in the adult olfactory bulb. J Neurosci 31:11587-11596. CrossRef Medline
52. Sequerra EB, Miyakoshi LM, Fró es MM, Menezes JR, Hedin-Pereira C (2010) Generation of glutamatergic neurons from postnatal and adult subventricular zone with pyramidal-like morphology. Cereb Cortex 20: 2583-2591. CrossRef Medline
53. Shepherd GM, Greer CA (2004) Olfactory bulb in the synaptic organization of the brain (Shepherd GM, ed), pp 159-204. New York: Oxford UP.
54. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F (2001) Cre reporer strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4. CrossRef Medline
55. Stenman JM, Rajagopal J, Carroll TJ, Ishibashi M, McMahon J, McMahon AP (2008) Canonical Wnt signaling regulates organ-specific assembly and differentiation of CNS vasculature. Science 322:1247-1250. CrossRef Medline
56. Stenman J, Toresson H, Campbell K (2003) Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J Neurosci 23:167-174. Medline
57. Winpenny E, Lebel-Potter M, Fernandez ME, Brill MS, GötzM, Guillemot F, Raineteau O (2011) Sequential generation of olfactory bulb glutamatergic neurons by Neurog2-expressing precursor cells. Neural Dev 6:12. CrossRef Medline
58. Yamaguchi M, Manabe H, Murata K, MoriK (2013) Reorganization of neuronal circuits of the central olfactory system during postprandial sleep. Front Neural Circuits 7:132. CrossRef Medline
59. Yokoi M, Mori K, Nakanishi S (1995) Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci U S A 92:3371-3375. CrossRef Medline
60. Yoshihara S, Takahashi H, Nishimura N, Naritsuka H, Shirao T, Hirai H, Yoshihara Y, Mori K, Stern PL, Tsuboi A (2012) 5T4 glycoprotein regulates the sensory input-dependent development of a specific subtype of newborn interneurons in the mouse olfactory bulb. J Neurosci 32:2217-2226. CrossRef Medline