Segregated labeling of olfactory bulb projection neurons based on their birthdates

European Journal of Neuroscience

Volumn 41, Issue 2, 2015, Pages 147-156

  Imamura, Fumiaki ^a,b   Greer, Charles A ^b  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Development; in utero electroporation; Neuronal circuit; Olfactory bulb; Projection neuron

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; DENDRITE; ELECTROPORATION; EMBRYO; GENE; GENE EXPRESSION; GFP GENE; IMMUNOHISTOCHEMISTRY; MITRAL CELL; MOUSE; NERVE FIBER TRANSPORT; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; OLFACTORY BULB PROJECTION NEURON; PLASMID; ANIMAL; CYTOLOGY; EMBRYOLOGY; GENE VECTOR; GENETICS; METABOLISM; NERVE CELL; NERVE TRACT; PROCEDURES;

BROXURIDINE; GREEN FLUORESCENT PROTEIN;

ANIMALS; BROMODEOXYURIDINE; ELECTROPORATION; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; MICE; NEURAL PATHWAYS; NEUROGENESIS; NEURONS; OLFACTORY BULB; PLASMIDS;

EID: 84921032412     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12784     Document Type: Article

References (52)

1. Angelo, K., Rancz, E.A., Pimentel, D., Hundahl, C., Hannibal, J., Fleischmann, A., Pichler, B. & Margrie, T.W. (2012) A biophysical signature of network affiliation and sensory processing in mitral cells. Nature, 488, 375-378.
2. Blanchart, A., De Carlos, J.A. & López-Mascaraque, L. (2006) Time frame of mitral cell development in the mice olfactory bulb. J. Comp. Neurol., 496, 529-543.
3. von Campenhausen, H. & Mori, K. (2000) Convergence of segregated pheromonal pathways from the accessory olfactory bulb to the cortex in the mouse. Eur. J. Neurosci., 12, 33-46.
4. Cho, J.H., Prince, J.E., Cutforth, T. & Cloutier, J.F. (2011) The pattern of glomerular map formation defines responsiveness to aversive odorants in mice. J. Neurosci., 31, 7920-7926.
5. Deguchi, Y., Donato, F., Galimberti, I., Cabuy, E. & Caroni, P. (2011) Temporally matched subpopulations of selectively interconnected principal neurons in the hippocampus. Nat. Neurosci., 14, 495-504.
6. Dewan, A., Pacifico, R., Zhan, R., Rinberg, D. & Bozza, T. (2013) Non-redundant coding of aversive odours in the main olfactory pathway. Nature, 497, 486-489.
7. Ezeh, P.I., Wellis, D.P. & Scott, J.W. (1993) Organization of inhibition in the rat olfactory bulb external plexiform layer. J. Neurophysiol., 70, 263-274.
8. Faedo, A., Ficara, F., Ghiani, M., Aiuti, A., Rubenstein, J.L. & Bulfone, A. (2002) Developmental expression of the T-box transcription factor T-bet/Tbx21 during mouse embryogenesis. Mech. Develop., 116, 157-160.
9. Feng, W., Simoes-de-Souza, F., Finger, T.E., Restrepo, D. & Williams, T. (2009) Disorganized olfactory bulb lamination in mice deficient for transcription factor AP-2epsilon. Mol. Cell. Neurosci., 42, 161-171.
10. Fukunaga, I., Berning, M., Kollo, M., Schmaltz, A. & Schaefer, A.T. (2012) Two distinct channels of olfactory bulb output. Neuron, 75, 320-329.
11. Gheusi, G. & Lledo, P.M. (2014) Adult neurogenesis in the olfactory system shapes odor memory and perception. Prog. Brain Res., 208, 157-175.
12. Ghosh, S., Larson, S.D., Hefzi, H., Marnoy, Z., Cutforth, T., Dokka, K. & Baldwin, K.K. (2011) Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature, 472, 217-220.
13. Giacobini, P., Parkash, J., Campagne, C., Messina, A., Casoni, F., Vanacker, C., Langlet, F., Hobo, B., Cagnoni, G., Gallet, S., Hanchate, N.K., Mazur, D., Taniguchi, M., Mazzone, M., Verhaagen, J., Ciofi, P., Bouret, S.G., Tamagnone, L. & Prevot, V. (2014) Brain endothelial cells control fertility through ovarian-steroid-dependent release of semaphorin 3A. PLoS Biol., 12, e1001808.
14. Haberly, L.B. & Price, J.L. (1977) The axonal projection patterns of the mitral and tufted cells of the olfactory bulb in the rat. Brain Res., 129, 152-157.
15. Haddad, R., Lanjuin, A., Madisen, L., Zeng, H., Murthy, V.N. & Uchida, N. (2013) Olfactory cortical neurons read out a relative time code in the olfactory bulb. Nat. Neurosci., 16, 949-957.
16. Hinds, J.W. (1972) Early neuron differentiation in the mouse of olfactory bulb I. Light microscopy. J. Comp. Neurol., 146, 233-252.
17. Igarashi, K.M., Ieki, N., An, M., Yamaguchi, Y., Nagayama, S., Kobayakawa, K., Kobayakawa, R., Tanifuji, M., Sakano, H., Chen, W.R. & Mori, K. (2012) Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J. Neurosci., 32, 7970-7985.
18. Imamura, F. & Greer, C.A. (2013) Pax6 regulates Tbr1 and Tbr2 expressions in olfactory bulb mitral cells. Mol. Cell. Neurosci., 54, 58-70.
19. Imamura, F. & Greer, C.A. (2014) Electroporation in the developing mouse olfactory bulb. In Saito, T. (Ed.) Electroporation Methods and Neuroscience, Neuromethods. Springer Science+Business Media, LLC, New York, NY.
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.
21. Imamura, F., Ayoub, A.E., Rakic, P. & Greer, C.A. (2011) Timing of neurogenesis is a determinant of olfactory circuitry. Nat. Neurosci., 14, 331-337.
22. Inaki, K., Nishimura, S., Nakashiba, T., Itohara, S. & Yoshihara, Y. (2004) Laminar organization of the developing lateral olfactory tract revealed by differential expression of cell recognition molecules. J. Comp. Neurol., 479, 243-256.
23. Kang, N., Baum, M.J. & Cherry, J.A. (2009) A direct main olfactory bulb projection to the 'vomeronasal' amygdala in female mice selectively responds to volatile pheromones from males. Eur. J. Neurosci., 29, 624-634.
24. Kikuta, S., Fletcher, M.L., Homma, R., Yamasoba, T. & Nagayama, S. (2013) Odorant response properties of individual neurons in an olfactory glomerular module. Neuron, 77, 1122-1135.
25. Kitamura, H., Okumura, M., Sato, F., Kimoto, K., Kohama, M., Hashimoto, Y., Tagami, M. & Iwanaga, T. (2001) Increased concentrations of protein gene product 9.5 in the synovial fluid from horses with osteoarthritis. Jpn. J. Vet. Res., 49, 115-123.
26. Kobayakawa, K., Kobayakawa, R., Matsumoto, H., Oka, Y., Imai, T., Ikawa, M., Okabe, M., Ikeda, T., Itohara, S., Kikusui, T., Mori, K. & Sakano, H. (2007) Innate versus learned odour processing in the mouse olfactory bulb. Nature, 450, 503-508.
27. Mandairon, N., Sacquet, J., Jourdan, F. & Didier, A. (2006) Long-term fate and distribution of newborn cells in the adult mouse olfactory bulb: influences of olfactory deprivation. Neuroscience, 141, 443-451.
28. Matsuda, T. & Cepko, C.L. (2004) Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc. Natl. Acad. Sci. USA, 101, 16-22.
29. Mitsui, S., Igarashi, K.M., Mori, K. & Yoshihara, Y. (2011) Genetic visualization of the secondary olfactory pathway in Tbx21 transgenic mice. Neural Syst. Circuits, 1, 5.
30. Miyamichi, K., Amat, F., Moussavi, F., Wang, C., Wickersham, I., Wall, N.R., Taniguchi, H., Tasic, B., Huang, Z.J., He, Z., Callaway, E.M., Horowitz, M.A. & Luo, L. (2010) Cortical representations of olfactory input by trans-synaptic tracing. Nature, 472, 191-196.
31. Mizuguchi, R., Naritsuka, H., Mori, K. & Yoshihara, Y. (2012) Tbr2 deficiency in mitral and tufted cells disrupts excitatory-inhibitory balance of neural circuitry in the mouse olfactory bulb. J. Neurosci., 32, 8831-8844.
32. Molyneaux, B.J., Arlotta, P., Menezes, J.R. & Macklis, J.D. (2007) Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci., 8, 427-437.
33. Mori, K. (1987) Membrane and synaptic properties of identified neurons in the olfactory bulb. Prog. Neurobiol., 29, 275-320.
34. 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.
35. Mouradian, L.E. & Scott, J.W. (1988) Cytochrome oxidase staining marks dendritic zones of the rat olfactory bulb external plexiform layer. J. Comp. Neurol., 271, 507-518.
36. Nagai, Y., Sano, H. & Yokoi, M. (2005) Transgenic expression of Cre recombinase in mitral/tufted cells of the olfactory bulb. Genesis, 43, 12-16.
37. Nagayama, S., Takahashi, Y.K., Yoshihara, Y. & Mori, K. (2004) Mitral and tufted cells differ in the decoding manner of odor maps in the rat olfactory bulb. J. Neurophysiol., 91, 2532-2540.
38. Nagayama, S., Enerva, A., Fletcher, M.L., Masurkar, A.V., Igarashi, K.M., Mori, K. & Chen, W.R. (2010) Differential axonal projection of mitral and tufted cells in the mouse main olfactory system. Front. Neural Circuits, 4, 120.
39. Orona, E., Rainer, E.C. & Scott, J.W. (1984) Dendritic and axonal organization of mitral and tufted cells in the rat olfactory bulb. J. Comp. Neurol., 226, 346-356.
40. Padmanabhan, K. & Urban, N.N. (2010) Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content. Nat. Neurosci., 13, 1276-1282.
41. Payton, C.A., Wilson, D.A. & Wesson, D.W. (2012) Parallel odor processing by two anatomically distinct olfactory bulb target structures. PLoS One, 7, e34926.
42. Rakic, P., Ayoub, A.E., Breunig, J.J. & Dominguez, M.H. (2009) Decision by division: making cortical maps. Trends Neurosci., 32, 291-301.
43. Scott, J.W. (1981) Electrophysiological identification of mitral and tufted cells and distributions of their axons in olfactory system of the rat. J. Neurophysiol., 46, 918-931.
44. Shepherd, G.M., Chen, W.R. & Greer, C.A. (2004) Olfactory bulb. In Shepherd, G.M. (Ed.), The Synaptic Organization of the Brain. Oxford UP, New York, pp. 165-216.
45. Sosulski, D.L., Lissitsyna Bloom, M., Cutforth, T., Axel, R. & Datta, S.R. (2011) Distinct representations of olfactory information in different cortical centres. Nature, 472, 213-216.
46. Stancik, E.K., Navarro-Quiroga, I., Sellke, R. & Haydar, T.F. (2010) Heterogeneity in ventricular zone neural precursors contributes to neuronal fate diversity in the postnatal neocortex. J. Neurosci., 30, 7028-7036.
47. Taniguchi, K., Saito, H., Okamura, M. & Ogawa, K. (1993) Immunohistochemical demonstration of protein gene product 9.5 (PGP 9.5) in the primary olfactory system of the rat. Neurosci. Lett., 156, 24-26.
48. Tripodi, M., Stepien, A.E. & Arber, S. (2011) Motor antagonism exposed by spatial segregation and timing of neurogenesis. Nature, 479, 61-66.
49. Whitman, M.C. & Greer, C.A. (2007) Synaptic integration of adult-generated olfactory bulb granule cells: basal axodendritic centrifugal input precedes apical dendrodendritic local circuits. J. Neurosci., 27, 9951-9961.
50. Whitman, M.C. & Greer, C.A. (2009) Adult neurogenesis and the olfactory system. Prog. Neurobiol., 89, 162-175.
51. Yan, Z., Tan, J., Qin, C., Lu, Y., Ding, C. & Luo, M. (2008) Precise circuitry links bilaterally symmetric olfactory maps. Neuron, 58, 613-624.
52. Yoshihara, S., Omichi, K., Yanazawa, M., Kitamura, K. & Yoshihara, Y. (2005) Arx homeobox gene is essential for development of mouse olfactory system. Development, 132, 751-762.