Dual origins of the mammalian accessory olfactory bulb revealed by an evolutionarily conserved migratory stream

Nature Neuroscience

Volumn 16, Issue 2, 2013, Pages 157-165

  Huilgol, Dhananjay ^a   Udin, Susan ^b   Shimogori, Tomomi ^c   Saha, Bhaskar ^a   Roy, Achira ^a   Aizawa, Shinichi ^d   Hevner, Robert F ^e   Meyer, Gundela ^f   Ohshima, Toshio ^g   Pleasure, Samuel J ^h   Zhao, Yangu ⁱ   Tole, Shubha ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b UNIVERSITY AT BUFFALO   (United States)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^d RIKEN   (Japan)

^e UNIVERSITY OF WASHINGTON   (United States)

^f UNIVERSIDAD DE LA LAGUNA   (Spain)

^g WASEDA UNIVERSITY   (Japan)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCESSORY OLFACTORY BULB; ANIMAL CELL; ARTICLE; CELL MIGRATION; DIENCEPHALON; GENE EXPRESSION; MOUSE; NERVE CELL; NERVE FIBER; NEUROEPITHELIUM; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; TELENCEPHALON; XENOPUS;

AFFERENT PATHWAYS; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL EVOLUTION; BROMODEOXYURIDINE; CELL MOVEMENT; CYCLIN-DEPENDENT KINASE 5; DIENCEPHALON; DNA-BINDING PROTEINS; ELECTROPORATION; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LUMINESCENT PROTEINS; MALE; MICE; MICE, TRANSGENIC; MICROINJECTIONS; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; OLFACTORY BULB; OOCYTES; ORGAN CULTURE TECHNIQUES; PREGNANCY; TELENCEPHALON; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; VOMERONASAL ORGAN; XENOPUS;

EID: 84873096281     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3297     Document Type: Article

References (60)

1. Kumar, A., Dudley, C.A. & Moss, R.L. Functional dichotomy within the vomeronasal system: distinct zones of neuronal activity in the accessory olfactory bulb correlate with sex-specifc behaviors. J. Neurosci. 19, RC32 (1999).
2. McGregor, I.S., Hargreaves, G.A., Apfelbach, R. & Hunt, G.E. Neural correlates of cat odor-induced anxiety in rats: region-specifc effects of the benzodiazepine midazolam. J. Neurosci. 24, 4134-4144 (2004). (Pubitemid 38620788)
3. Wagner, S., Gresser, A.L., Torello, A.T. & Dulac, C. A multireceptor genetic approach uncovers an ordered integration of VNO sensory inputs in the accessory olfactory bulb. Neuron 50, 697-709 (2006). (Pubitemid 43775740)
4. Del Punta, K., Puche, A., Adams, N.C., Rodriguez, I. & Mombaerts, P. A divergent pattern of sensory axonal projections is rendered convergent by second-order neurons in the accessory olfactory bulb. Neuron 35, 1057-1066 (2002). (Pubitemid 35279534)
5. Choi, G.B. et al. Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 46, 647-660 (2005). (Pubitemid 40797388)
6. Mohedano-Moriano, A. et al. Segregated pathways to the vomeronasal amygdala: differential projections from the anterior and posterior divisions of the accessory olfactory bulb. Eur. J. Neurosci. 25, 2065-2080 (2007). (Pubitemid 46581744)
7. Takami, S., Graziadei, P.P. & Ichikawa, M. The differential staining patterns of two lectins in the accessory olfactory bulb of the rat. Brain Res. 598, 337-342 (1992). (Pubitemid 23013081)
8. Halpern, M. & Martinez-Marcos, A. Structure and function of the vomeronasal system: an update. Prog. Neurobiol. 70, 245-318 (2003). (Pubitemid 37287601)
9. Halpern, M., Shapiro, L.S. & Jia, C. Heterogeneity in the accessory olfactory system. Chem. Senses 23, 477-481 (1998). (Pubitemid 28389147)
10. Jia, C. & Halpern, M. Subclasses of vomeronasal receptor neurons: differential expression of G proteins (Gi alpha 2 and G(o alpha)) and segregated projections to the accessory olfactory bulb. Brain Res. 719, 117-128 (1996).
11. Faedo, A. et al. Developmental expression of the T-box transcription factor Tbet/Tbx21 during mouse embryogenesis. Mech. Dev. 116, 157-160 (2002). (Pubitemid 34786417)
12. Abellán, A., Vernier, B., Retaux, S. & Medina, L. Similarities and differences in the forebrain expression of Lhx1 and Lhx5 between chicken and mouse: insights for understanding telencephalic development and evolution. J. Comp. Neurol. 518, 3512-3528 (2010).
13. Rakic, P. Principles of neural cell migration. Experientia 46, 882-891 (1990). (Pubitemid 20331700)
14. Lavdas, A.A., Grigoriou, M., Pachnis, V. & Parnavelas, J.G. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 19, 7881-7888 (1999). (Pubitemid 30225786)
15. Miyoshi, G. & Fishell, G. GABAergic interneuron lineages selectively sort into specifc cortical layers during early postnatal development. Cereb. Cortex 21, 845-852 (2011).
16. Inaki, K., Nishimura, S., Nakashiba, T., Itohara, S. & Yoshihara, Y. Laminar organization of the developing lateral olfactory tract revealed by differential expression of cell recognition molecules. J. Comp. Neurol. 479, 243-256 (2004). (Pubitemid 39426061)
17. Saha, B., Hari, P., Huilgol, D. & Tole, S. Dual role for LIM-homeodomain gene Lhx2 in the formation of the lateral olfactory tract. J. Neurosci. 27, 2290-2297 (2007). (Pubitemid 46340956)
18. Takiguchi-Hayashi, K. et al. Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles. J. Neurosci. 24, 2286-2295 (2004). (Pubitemid 38314560)
19. Imayoshi, I., Shimogori, T., Ohtsuka, T. & Kageyama, R. Hes genes and neurogenin regulate non-neural versus neural fate specifcation in the dorsal telencephalic midline. Development 135, 2531-2541 (2008).
20. Miquelajáuregui, A. et al. LIM-homeobox gene Lhx5 is required for normal development of Cajal-Retzius cells. J. Neurosci. 30, 10551-10562 (2010).
21. Sato, Y. et al. Stable integration and conditional expression of electroporated transgenes in chicken embryos. Dev. Biol. 305, 616-624 (2007). (Pubitemid 46686603)
22. Bulfone, A. et al. An olfactory sensory map develops in the absence of normal projection neurons or GABAergic interneurons. Neuron 21, 1273-1282 (1998). (Pubitemid 29022530)
23. Tsai, L.H., Takahashi, T., Caviness, V.S. Jr. & Harlow, E. Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system. Development 119, 1029-1040 (1993). (Pubitemid 23358574)
24. Gilmore, E.C., Ohshima, T., Goffnet, A.M., Kulkarni, A.B. & Herrup, K. Cyclin-dependent kinase 5-defcient mice demonstrate novel developmental arrest in cerebral cortex. J. Neurosci. 18, 6370-6377 (1998). (Pubitemid 28373242)
25. Remedios, R. et al. A stream of cells migrating from the caudal telencephalon reveals a link between the amygdala and neocortex. Nat. Neurosci. 10, 1141-1150 (2007). (Pubitemid 47339953)
26. Ohshima, T. et al. Cdk5 is required for multipolar-to-bipolar transition during radial neuronal migration and proper dendrite development of pyramidal neurons in the cerebral cortex. Development 134, 2273-2282 (2007). (Pubitemid 47010016)
27. Hirasawa, M. et al. Perinatal abrogation of Cdk5 expression in brain results in neuronal migration defects. Proc. Natl. Acad. Sci. USA 101, 6249-6254 (2004). (Pubitemid 38520560)
28. Shinozaki, K. et al. Absence of Cajal-Retzius cells and subplate neurons associated with defects of tangential cell migration from ganglionic eminence in Emx1/2 double mutant cerebral cortex. Development 129, 3479-3492 (2002).
29. Meyer, G. et al. Developmental roles of p73 in Cajal-Retzius cells and cortical patterning. J. Neurosci. 24, 9878-9887 (2004). (Pubitemid 39463568)
30. Paredes, M.F., Li, G., Berger, O., Baraban, S.C. & Pleasure, S.J. Stromalderived factor-1 (CXCL12) regulates laminar position of Cajal-Retzius cells in normal and dysplastic brains. J. Neurosci. 26, 9404-9412 (2006). (Pubitemid 44396853)
31. Nguyen-Ba-Charvet, K.T., Plump, A.S., Tessier-Lavigne, M. & Chedotal, A. Slit1 and slit2 proteins control the development of the lateral olfactory tract. J. Neurosci. 22, 5473-5480 (2002). (Pubitemid 35386469)
32. Kawasaki, T., Ito, K. & Hirata, T. Netrin 1 regulates ventral tangential migration of guidepost neurons in the lateral olfactory tract. Development 133, 845-853 (2006).
33. Nguyen-Ba-Charvet, K.T. et al. Multiple roles for slits in the control of cell migration in the rostral migratory stream. J. Neurosci. 24, 1497-1506 (2004). (Pubitemid 38223002)
34. Angot, E. et al. Chemoattractive activity of sonic hedgehog in the adult subventricular zone modulates the number of neural precursors reaching the olfactory bulb. Stem Cells 26, 2311-2320 (2008).
35. Balordi, F. & Fishell, G. Hedgehog signaling in the subventricular zone is required for both the maintenance of stem cells and the migration of newborn neurons. J. Neurosci. 27, 5936-5947 (2007). (Pubitemid 46849750)
36. Holmgren, N. Points of view concerning forebrain morphology in lower vertebrates. J. Comp. Neurol. 34, 391-459 (1922).
37. Krug, L., Wicht, H. & Northcutt, R.G. Afferent and efferent connections of the thalamic eminence in the axolotl, Ambystoma mexicanum. Neurosci. Lett. 149, 145-148 (1993). (Pubitemid 23036901)
38. Moreno, N. et al. Anuran olfactory bulb organization: embryology, neurochemistry and hodology. Brain Res. Bull. 75, 241-245 (2008). (Pubitemid 351335174)
39. Anderson, S.A., Marin, O., Horn, C., Jennings, K. & Rubenstein, J.L. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128, 353-363 (2001). (Pubitemid 32184376)
40. Corbin, J.G., Nery, S. & Fishell, G. Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain. Nat. Neurosci. 4, 1177-1182 (2001). (Pubitemid 33733106)
41. Meyer, G., Perez-Garcia, C.G., Abraham, H. & Caput, D. Expression of p73 and Reelin in the developing human cortex. J. Neurosci. 22, 4973-4986 (2002). (Pubitemid 37465612)
42. Schiffmann, S.N., Bernier, B. & Goffnet, A.M. Reelin mRNA expression during mouse brain development. Eur. J. Neurosci. 9, 1055-1071 (1997). (Pubitemid 27226469)
43. Hevner, R.F., Neogi, T., Englund, C., Daza, R.A. & Fink, A. Cajal-Retzius cells in the mouse: transcription factors, neurotransmitters and birthdays suggest a pallial origin. Brain Res. Dev. Brain Res. 141, 39-53 (2003). (Pubitemid 36315691)
44. Halpern, M. The organization and function of the vomeronasal system. Annu. Rev. Neurosci. 10, 325-362 (1987). (Pubitemid 17022777)
45. Soma, M. et al. Development of the mouse amygdala as revealed by enhanced green fuorescent protein gene transfer by means of in utero electroporation. J. Comp. Neurol. 513, 113-128 (2009).
46. García-Moreno, F. et al. A neuronal migratory pathway crossing from diencephalon to telencephalon populates amygdala nuclei. Nat. Neurosci. 13, 680-689 (2010).
47. Tissir, F. et al. DeltaNp73 regulates neuronal survival in vivo. Proc. Natl. Acad. Sci. USA 106, 16871-16876 (2009).
48. Rakić, S. et al. Cortical interneurons require p35/Cdk5 for their migration and laminar organization. Cereb. Cortex 19, 1857-1869 (2009).
49. Taniguchi, K., Saito, S. & Oikawa, T. Phylogenic aspects of the amphibian dual olfactory system. J. Vet. Med. Sci. 70, 1-9 (2008). (Pubitemid 351214390)
50. Hagino-Yamagishi, K. et al. Expression of vomeronasal receptor genes in Xenopus laevis. J. Comp. Neurol. 472, 246-256 (2004). (Pubitemid 38429024)
51. Ohshima, T. et al. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl. Acad. Sci. USA 93, 11173-11178 (1996). (Pubitemid 26333137)
52. Zhao, Y. et al. Control of hippocampal morphogenesis and neuronal differentiation by the LIM homeobox gene Lhx5. Science 284, 1155-1158 (1999). (Pubitemid 29288402)
53. Hevner, R.F. et al. Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29, 353-366 (2001). (Pubitemid 32206476)
54. Bagri, A. et al. The chemokine SDF1 regulates migration of dentate granule cells. Development 129, 4249-4260 (2002).
55. Barallobre, M.J. et al. Aberrant development of hippocampal circuits and altered neural activity in netrin 1-defcient mice. Development 127, 4797-4810 (2000).
56. Plump, A.S. et al. Slit1 and Slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron 33, 219-232 (2002). (Pubitemid 34127755)
57. Matsui, A., Yoshida, A.C., Kubota, M., Ogawa, M. & Shimogori, T. Mouse in utero electroporation: controlled spatiotemporal gene transfection. J. Vis. Exp. published online, doi:10.3791/3024 (15 August 2011).
58. Nieuwkoop, P.D. & Faber, J. Normal Table of Xenopus Laevis (Daudin), 2nd edn. (North-Holland Publishing Co., Amsterdam, 1967).
59. Katz, L.C. & Iarovici, D.M. Green fuorescent latex microspheres: a new retrograde tracer. Neuroscience 34, 511-520 (1990). (Pubitemid 20110155)
60. Yun, K., Potter, S. & Rubenstein, J.L. Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128, 193-205 (2001). (Pubitemid 32124145)