Patterns of hypothalamic regionalization in amphibians and reptiles: Common traits revealed by a genoarchitectonic approach

Frontiers in Neuroanatomy

Volumn 9, Issue FEB, 2015, Pages

  Domínguez, Laura ^a   González, Agustín ^a   Moreno, Nerea ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Development; Evolution; Forebrain patterning; Hypothalamus; Prosencephalon

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX2.1; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR OTP; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SIM1; UNCLASSIFIED DRUG;

AMNIOTE; AMPHIBIA; ANTERIOR HYPOTHALAMUS; BRAIN REGION; CATECHOLAMINE NERVE CELL; CHICK; DIENCEPHALON; EVOLUTION; EVOLUTIONARY HOMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENOARCHITECTONIC APPROACH; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS; LAMPREY; LUNGFISH; MAMMILLARY BODY; NONHUMAN; POSTERIOR HYPOTHALAMUS; PREOPTIC AREA; PROTEIN EXPRESSION; REVIEW; SUPRACHIASMATIC NUCLEUS; SUPRAOPTOPARAVENTRICULAR REGION; TELENCEPHALON; TRACHEMYS SCRIPTA; XENOPUS LAEVIS;

EID: 84922269896     PISSN: None     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2015.00003     Document Type: Review

References (124)

1. Abellan, A., and Medina, L. (2009). Subdivisions and derivatives of the chicken subpallium based on expression ofLIM and other regulatorygenes and markers of neuron subpopulations during development. J. Comp. Neurol. 515, 465-501. doi: 10.1002/cne.22083
2. Abellan, A., Vernier, B., Rétaux, S., and Medina, L. (2010). 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. doi: 10.1002/cne.22410
3. Acampora, D., Postiglione, M. P., Avantaggiato, V., Di Bonito, M., Vaccarino, F. M., Michaud, J., et al. (1999). Progressive impairment of developing neuroendocrine cell lineages in the hypothalamus of mice lacking the Orthopedia gene. Genes Dev. 13, 2787-2800. doi: 10.1101/gad.13.21.2787
4. Alunni, A., Blin, M., Deschet, K., Bourrat, F., Vernier, P., and Rétaux, S. (2004). Cloning and developmental expression patterns of Dlx2, Lhx7 and Lhx9 in the medaka fish (Oryzias latipes). Mech. Dev. 121, 977-983. doi: 10.1016/j.mod.2004.03.023
5. Bachy, I., Berthon, J., and Rétaux, S. (2002). Defining pallial and subpallial divisions in the developing Xenopus forebrain. Mech. Dev. 117, 163-172. doi: 10.1016/s0925-4773(02)00199-5
6. Bandin, S., Morona, R., Moreno, N., and Gonzalez, A. (2013). Regional expression ofPax7 in the brain of Xenopus laevis during embryonic and larval development. Front. Neuroanat. 7:48. doi: 10.3389/fnana.2013.00048
7. Bardet, S. M., Cobos, I., Puelles, E., Martinez-De-La-Torre, M., and Puelles, L. (2006). Chicken lateral septal organ and other circumventricular organs form in a striatal subdomain abutting the molecular striatopallidal border. J. Comp. Neurol. 499, 745-767. doi: 10.1002/cne.21121
8. Bardet, S. M., Ferran, J. L., Sanchez-Arrones, L., and Puelles, L. (2010). Ontogenetic expression of sonic hedgehog in the chicken subpallium. Front. Neuroanat. 4:28. doi: 10.3389/fnana.2010.00028
9. Bardet, S. M., Martinez-de-la-Torre, M., Northcutt, R. G., Rubenstein, J. L., and Puelles, L. (2008). Conserved pattern of OTP-positive cells in the paraventricular nucleus and other hypothalamic sites of tetrapods. Brain Res. Bull. 75, 231-235. doi: 10.1016/j.brainresbull.2007.10.037
10. Blechman, J., Borodovsky, N., Eisenberg, M., Nabel-Rosen, H., Grimm, J., and Levkowitz, G. (2007). Specification ofhypothalamic neurons by dual regulation ofthe homeodomain protein Orthopedia. Development 134, 4417-4426. doi: 10.1242/dev.011262
11. Bourguignon, C., Li, J., and Papalopulu, N. (1998). XBF-1, a winged helix transcription factor with dual activity, has a role in positioning neurogenesis in Xenopus competent ectoderm. Development 125, 4889-4900.
12. Briscoe, J., and Ericson, J. (1999). The specification of neuronal identity by graded Sonic Hedgehog signalling. Semin. Cell Dev. Biol. 10, 353-362. doi: 10.1006/scdb.1999.0295
13. Brox, A., Puelles, L., Ferreiro, B., and Medina, L. (2003). Expression of the genes GAD67 and Distal-less-4 in the forebrain of Xenopus laevis confirms a common pattern in tetrapods. J. Comp. Neurol. 461, 370-393. doi: 10.1002/cne.10688
14. Bruce, L. (2008). “Evolution of the hypothalamus in amniotes. Evolution and Embryological development of forebrain,” in Encyclopedia of Neuroscience, eds M. D. Binder, N. Hirokawa and U. Windhorst (Berlin Heidelberg: Springer Verlag), 1363-1367.
15. Bruce, L. L., and Neary, T. J. (1995). The limbic system oftetrapods: a comparative analysis of cortical and amygdalar populations. Brain Behav. Evol. 46, 224-234. doi: 10.1159/000113276
16. Bulfone, A., Puelles, L., Porteus, M. H., Frohman, M. A., Martin, G. R., and Rubenstein, J. L. (1993). Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2 and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J. Neurosci. 13, 3155-3172.
17. Bupesh, M., Abellan, A., and Medina, L. (2011b). Genetic and experimental evidence supports the continuum of the central extended amygdala and a mutiple embryonic origin of its principal neurons. J. Comp. Neurol. 519, 3507-3531. doi: 10.1002/cne.22719
18. Bupesh, M., Legaz, I., Abellan, A., and Medina, L. (2011a). Multiple telencephalic and extratelencephalic embryonic domains contribute neurons to the medial extended amygdala. J. Comp. Neurol. 519, 1505-1525. doi: 10.1002/cne.22581
19. Butler, A., and Hodos, W. (2005). “The visceral brain: the hypothalamus and autonomic nervous system,” in Comparative Vertebrate Neuroanatomy: Evolution and Adaptation, ed J. W. Sons (New Jersey: Wiley), 445-467.
20. Caqueret, A., Coumailleau, P., and Michaud, J. L. (2006). Regionalization of the anterior hypothalamus in the chick embryo. Dev. Dyn. 233, 652-658. doi: 10.1002/dvdy.20372
21. Crossley, P. H., Martinez, S., Ohkubo, Y., and Rubenstein, J. L. (2001). Coordinate expression of Fgf8, Otx2, Bmp4 and Shh in the rostral prosencephalon during development of the telencephalic and optic vesicles. Neuroscience 108, 183-206. doi: 10.1016/s0306-4522(01)00411-0
22. D’Aniello, B., Pinelli, C., Jadhao, A. G., Rastogi, R. K., and Meyer, D. L. (1999). Comparative analysis of FMRFamide-like immunoreactivity in caiman (Caiman crocodilus) and turtle (Trachemys scripta elegans) brains. Cell Tissue Res. 298, 549-559. doi: 10.1007/s004410050077
23. Davis, A. M., Seney, M. L., Stallings, N. R., Zhao, L., Parker, K. L., and Tobet, S. A. (2004). Loss of steroidogenic factor 1 alters cellular topography in the mouse ventromedial nucleus of the hypothalamus. J. Neurobiol. 60, 424-436. doi: 10.1002/neu.20030
24. Del Giacco, L., Pistocchi, A., Cotelli, F., Fortunato, A. E., and Sordino, P. (2008). A peek inside the neurosecretory brain through Orthopedia lenses. Dev. Dyn. 237, 2295-2303. doi: 10.1002/dvdy.21668
25. Del Giacco, L., Sordino, P., Pistocchi, A., Andreakis, N., Tarallo, R., Di Benedetto, B., et al. (2006). Differential regulation of the zebrafish orthopedia 1 gene during fate determination of diencephalic neurons. BMC Dev. Biol. 6:50. doi: 10.1186/1471-213X-6-50
26. Diez-Roux, G., Banfi, S., Sultan, M., Geffers, L., Anand, S., Rozado, D., etal. (2011). A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoSBiol. 9:e1000582. doi: 10.1371/journal.pbio.1000582
27. Dominguez, L., Gonzalez, A., and Moreno, N. (2010). Sonic hedgehog expression during Xenopus laevisforebrain development. Brain Res. 1347, 19-32. doi: 10.1016/j.brainres.2010.06.007
28. Dominguez, L., Gonzalez, A., and Moreno, N. (2011). Ontogenetic distribution of the transcription factor nkx2.2 in the developing forebrain of Xenopus laevis. Front. Neuroanat. 5:11. doi: 10.3389/fnana.2011.00011
29. Dominguez, L., Gonzalez, A., and Moreno, N. (2014). Characterization of the hypothalamus of Xenopus laevis during development. II. The basal regions. J. Comp. Neurol. 522, 1102-1131. doi: 10.1002/cne.23471
30. Dominguez, L., Lopez, J. M., and Gonzalez, A. (2008). Distribution of thyrotropin-releasing hormone (TRH) immunoreactivity in the brain of urodele amphibians. Brain Behav. Evol. 71, 231-246. doi: 10.1159/000122835
31. Dominguez, L., Morona, R., Gonzalez, A., and Moreno, N. (2013). Characterization of the hypothalamus of Xenopus laevis during development. I. The alar regions. J. Comp. Neurol. 521, 725-759. doi: 10.1002/cne.23222
32. Eaton, J. L., and Glasgow, E. (2007). Zebrafish orthopedia (otp) is required for isotocin cell development. Dev. Genes Evol. 217, 149-158. doi: 10.1007/s00427-006-0123-2
33. Eaton, J. L., Holmqvist, B., and Glasgow, E. (2008). Ontogeny of vasotocin- expressing cells in zebrafish: selective requirement for the transcriptional regulators orthopedia and single-minded 1 in the preoptic area. Dev. Dyn. 237, 995-1005. doi: 10.1002/dvdy.21503
34. Figdor, M. C., and Stern, C. D. (1993). Segmental organization of embryonic diencephalon. Nature 363, 630-634. doi: 10.1038/363630a0
35. Flames, N., Pla, R., Gelman, D. M., Rubenstein, J. L., Puelles, L., and Marin, O. (2007). Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J. Neurosci. 27, 9682-9695. doi: 10.1523/jneurosci.2750-07.2007
36. Garcia-Calero, E., Fernândez-Garre, P., Martinez, S., and Puelles, L. (2008). Early mammillary pouch specification in the course of prechordal ventralization of the forebrain tegmentum. Dev. Biol. 320, 366-377. doi: 10.1016/j.ydbio.2008.05.545
37. Garcia-Lopez, R., Pombero, A., and Martinez, S. (2009). Fate map of the chick embryo neural tube. Dev. Growth Differ. 51, 145-165. doi: 10.1111/j.1440-169x.2009.01096.x
38. Garcia-Lopez, R., Vieira, C., Echevarria, D., and Martinez, S. (2004). Fate map of the diencephalon and the zona limitans at the 10-somites stage in chick embryos. Dev. Biol. 268, 514-530. doi: 10.1016/j.ydbio.2003.12.038
39. Garcia-Moreno, F., Pedraza, M., Di Giovannantonio, L. G., Di Salvio, M., Lopez- Mascaraque, L., Simeone, A., et al. (2010). A neuronal migratory pathway crossing from diencephalon to telencephalon populates amygdala nuclei. Nat. Neurosci. 13, 680-689. doi: 10.1038/nn.2556
40. Gonzâlez, A., and Northcutt, R. G. (2009). An immunohistochemical approach to lungfish telencephalic organization. Brain Behav. Evol. 74, 43-55. doi: 10.1159/000229012
41. Gonzâlez, A., and Smeets, W. J. (1991). Comparative analysis of dopamine and tyrosine hydroxylase immunoreactivities in the brain of two amphibians, the anuran Rana ridibunda and the urodele Pleurodeles waltlii. J. Comp. Neurol. 303, 457-477. doi: 10.1002/cne.903030311
42. Gonzâlez, A., Tuinhof, R., and Smeets, W. J. (1993). Distribution of tyrosine hydroxylase and dopamine immunoreactivities in the brain of the South African clawedfrog Xenopus laevis. Anat. Embryol. (Berl) 187, 193-201. doi: 10.1007/bf00171750
43. Goshu, E., Jin, H., Lovejoy, J., Marion, J. F., Michaud, J. L., and Fan, C. M. (2004). Sim2 contributes to neuroendocrine hormone gene expression in the anterior hypothalamus. Mol. Endocrinol. 18, 1251-1262. doi: 10.1210/me.2003-0372
44. Herget, U., Wolf, A., Wullimann, M. F., and Ryu, S. (2014). Molecular neuroanatomy and chemoarchitecture of the neurosecretory preoptic- hypothalamic area in zebrafishlarvae. J. Comp. Neurol. 522, 1542-1564. doi: 10.1002/cne.23480
45. Herrick, C. (1910). The morphology of the forebrain in Amphibian and Reptilia. J. Comp. Neurol. 20, 413-547. doi: 10.1002/cne.920200502
46. Herrick, C. (1948). The Brain of the Tiger Salamander, Ambystina Tigrinum. Chicago: The University of Chigaco Press.
47. His, W. (1893a). Über das frontale Ende des Gehirnrohrs. Arch Anat Entwickelungsges. Anatomische Abteilung des Arch f.Anat u. Physiol 3, 157-171.
48. His, W. (1893b). Vorschläge zur Eintheilung des Gehirns. Arch Anat Entwickelungsges. Anatomische Abteilung des Arch f.Anat u.
49. Hodos, W. (2008). “Evolution of the hypothalamus in amniotes,” in Encyclopedia of Neuroscience, eds M. D. Binder, N. Hirokawa and U. Windhorst (Berlin Heidelberg: Springer-Verlag), 1361-1363.
50. Hökfelt, T., Fuxe, K., Johansson, O., Jeffcoate, S., and White, N. (1975). Distribution of thyrotropin-releasing hormone (TRH) in the central nervous system as revealed with immunohistochemistry. Eur. J. Pharmacol. 34, 389-392. doi: 10.1016/0014-2999(75)90269-1
51. Hökfelt, T., Martensson, R., Björklund, A., Kleinau, S., and Goldstein, M. (1984). “Distributional maps of tirosine hydroxilase immunoreactive neurons in the rat brain," in Classical Transmitters in the CNS. I. Handbook of Chemical Neuroanatomy, eds A. Björklund and T. Hökfelt (Amsterdam: Elsevier), 277-386.
52. Horjales-Araujo, E., Hellysaz, A., and Broberger, C. (2014). Lateral hypothalamic thyrotropin-releasing hormone neurons: distribution and relationship to histochemically defined cell populations in the rat. Neuroscience 277, 87-102. doi: 10.1016/j.neuroscience.2014.06.043
53. Kano, S., Xiao, J. H., Osorio, J., Ekker, M., Hadzhiev, Y., Müller, F., et al. (2010). Two lamprey Hedgehog genes share non-coding regulatory sequences and expression patterns with gnathostome Hedgehogs. PLoS One 5:e13332. doi: 10.1371/journal.pone.0013332
54. Kawano, H., Horie, M., Honma, S., Kawamura, K., Takeuchi, K., and Kimura, S. (2003). Aberrant trajectory of ascending dopaminergic pathway in mice lacking Nkx2.1. Exp. Neurol. 182, 103-112. doi: 10.1016/s0014-4886(03)00030-x
55. Kimura, S., Hara, Y., Pineau, T., Fernandez-Salguero, P., Fox, C. H., Ward, J. M., et al. (1996). The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain and pituitary. Genes Dev. 10, 60-69. doi: 10.1101/gad.10.1.60
56. Kuhlenbeck, H. (1973). The Central Nervous System of Vertebrates (Overall Morphologic Pattern, Vol. 3, PartII). Basel: Karger.
57. Kurrasch, D. M., Cheung, C. C., Lee, F. Y., Tran, P. V., Hata, K., and Ingraham, H. A. (2007). The neonatal ventromedial hypothalamus transcriptome reveals novel markers with spatially distinct patterning. J. Neurosci. 27, 13624-13634. doi: 10.1523/jneurosci.2858-07.2007
58. Lechan, R. M., Wu, P., and Jackson, I. M. (1986). Immunolocalization of the thyrotropin-releasing hormone prohormone in the rat central nervous system. Endocrinology 119, 1210-1216. doi: 10.1210/endo-119-3-1210
59. Löhr, H., Ryu, S., and Driever, W. (2009). Zebrafish diencephalic A11- related dopaminergic neurons share a conserved transcriptional network with neuroendocrine cell lineages. Development 136, 1007-1017. doi: 10.1242/dev.033878
60. Lopez, J. M., Dominguez, L., and Gonzâlez, A. (2008). Immunohistochemical localization of thyrotropin-releasing hormone in the brain of reptiles. J. Chem. Neuroanat. 36, 251-263. doi: 10.1016/j.jchemneu.2008.06.006
61. Machluf, Y., Gutnick, A., and Levkowitz, G. (2011). Development of the zebrafish hypothalamus. Ann. NY Acad. Sci. 1220, 93-105. doi: 10.1111/j.1749-6632.2010.05945.x.
62. Manning, L., Ohyama, K., Saeger, B., Hatano, O., Wilson, S. A., Logan, M., et al. (2006). Regional morphogenesis in the hypothalamus: a BMP-Tbx2 pathway coordinates fate and proliferation through Shh downregulation. Dev. Cell 11, 873-885. doi: 10.1016/j.devcel.2006.09.021
63. Marin, O., and Rubenstein, J. L. (2001). A long, remarkable journey: tangential migration in the telencephalon. Nat. Rev. Neurosci. 2, 780-790. doi: 10.1038/35097509
64. Markakis, E. A. (2002). Development of the neuroendocrine hypothalamus. Front. Neuroendocrinol. 23, 257-291. doi: 10.1016/s0091-3022(02)00003-1
65. Marti, E., Takada, R., Bumcrot, D. A., Sasaki, H., and McMahon, A. P. (1995). Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo. Development 121, 2537-2547.
66. Martinez-de-la-Torre, M., Pombal, M. A., and Puelles, L. (2011). Distal-less-like protein distribution in the larval lamprey forebrain. Neuroscience 178, 270-284. doi: 10.1016/j.neuroscience.2010.12.030
67. Medina, L. (2008). “Evolution and embryological development of forebrain,” in Encyclopedia of Neuroscience, eds M. D. Binder, N. Hirokawa and U. Windhorst (Berlin Heidelberg: Springer-Verlag), 1172-1192.
68. Medina, L., Bupesh, M., and Abellân, A. (2011). Contribution of genoarchitecture to understanding forebrain evolution and development, with particular emphasis on the amygdala. Brain Behav. Evol. 78, 216-236. doi: 10.1159/000330056
69. Menuet, A., Alunni, A., Joly, J. S., Jeffery, W. R., and Rétaux, S. (2007). Expanded expression of Sonic Hedgehog in Astyanax cavefish: multiple consequences on forebrain development and evolution. Development 134, 845-855. doi: 10.1242/dev.02780
70. Merchenthaler, I., Csernus, V., Csontos, C., Petrusz, P., and Mess, B. (1988). New data on the immunocytochemical localization of thyrotropin-releasing hormone in the rat central nervous system. Am. J. Anat. 181, 359-376. doi: 10.1002/aja.1001810404
71. Michaud, J. L., DeRossi, C., May, N. R., Holdener, B. C., and Fan, C. M. (2000). ARNT2 acts as the dimerization partner of SIM1 for the development of the hypothalamus. Mech. Dev. 90, 253-261. doi: 10.1016/s0925-4773(99)00328-7
72. Michaud, J. L., Rosenquist, T., May, N. R., and Fan, C. M. (1998). Development of neuroendocrine lineages requires the bHLH-PAS transcription factor SIM1. Genes Dev. 12, 3264-3275. doi: 10.1101/gad.12.20.3264
73. Morales-Delgado, N., Castro-Robles, B., Ferrân, J. L., Martinez-de-la-Torre, M., Puelles, L., and Diaz, C. (2014). Regionalized differentiation of CRH, TRH and GHRH peptidergic neurons in the mouse hypothalamus. Brain Struct. Funct. 219, 1083-1111. doi: 10.1007/s00429-013-0554-2
74. Morales-Delgado, N., Merchân, P., Bardet, S. M., Ferrân, J. L., Puelles, L., and Diaz, C. (2011). Topography of Somatostatin gene expression relative to molecular progenitor domains during ontogeny of the mouse hypothalamus. Front. Neuroanat. 5:10. doi: 10.3389/fnana.2011.00010
75. Moreno, N., Bachy, I., Rétaux, S., and Gonzâlez, A. (2004). LIM-homeodomain genes as developmental and adult genetic markers of Xenopus forebrain functional subdivisions. J. Comp. Neurol. 472, 52-72. doi: 10.1002/cne.20046
76. Moreno, N., Dominguez, L., Morona, R., and Gonzalez, A. (2012). Subdivisions of the turtle Pseudemys scripta hypothalamus based on the expression of regulatory genes and neuronal markers. J. Comp. Neurol. 520, 453-478. doi: 10.1002/cne.22762
77. Moreno, N., Dominguez, L., Rétaux, S., and Gonzalez, A. (2008b). Islet1 as a marker of subdivisions and cell types in the developing forebrain of Xenopus. Neuroscience 154, 1423-1439. doi: 10.1016/j.neuroscience.2008.04.029
78. Moreno, N., and Gonzalez, A. (2011). The non-evaginated secondary prosencephalon of vertebrates. Front. Neuroanat. 5:12. doi: 10.3389/fnana.2011.00012
79. Moreno, N., Morona, R., Lopez, J. M., and Gonzalez, A. (2010). Subdivisions of the turtle Pseudemys scripta subpallium based on the expression of regulatory genes and neuronal markers. J. Comp. Neurol. 518, 4877-4902. doi: 10.1002/cne.22493
80. Moreno, N., Rétaux, S., and Gonzalez, A. (2008a). Spatio-temporal expression of Pax6inXenopus forebrain. BrainRes. 1239,92-99. doi: 10.1016/j.brainres.2008.08.052
81. Morona, R., and Gonzalez, A. (2008). Calbindin-D28k and calretinin expression in the forebrain of anuran and urodele amphibians: further support for newly identified subdivisions. J. Comp. Neurol. 511, 187-220. doi: 10.1002/cne.21832
82. Murakami, Y., Ogasawara, M., Sugahara, F., Hirano, S., Satoh, N., and Kuratani, S. (2001). Identification and expression of the lamprey Pax6 gene: evolutionary origin of the segmented brain of vertebrates. Development 128, 3521-3531.
83. Murphy, D. B., Wiese, S., Burfeind, P., Schmundt, D., Mattei, M. G., Schulz- Schaeffer, W., et al. (1994). Human brain factor 1, a new member of the fork head gene family. Genomics 21, 551-557. doi: 10.1006/geno.1994.1313
84. Nieuwenhuys, R., Voogd, J., and van Huijzen, C. (2008). The Human Central Nervous System. Germany: Springer.
85. Northcutt, R. G. (1970). The Telencephalon of the Western Painted Turtle (Chrysemys Picta Bellis). Chicago: University of Illinois Press.
86. Ohyama, K., Ellis, P., Kimura, S., and Placzek, M. (2005). Directed differentiation of neural cells to hypothalamic dopaminergic neurons. Development 132, 5185-5197. doi: 10.1242/dev.02094
87. Osorio, J., Mazan, S., and Rétaux, S. (2005). Organisation of the lamprey (Lampetra fluviatilis) embryonic brain: insights from LIM-homeodomain, Pax and hedgehog genes. Dev. Biol. 288, 100-112. doi: 10.1016/j.ydbio.2005.08.042
88. Patten, I., Kulesa, P., Shen, M. M., Fraser, S., and Placzek, M. (2003). Distinct modes of floor plate induction in the chick embryo. Development 130, 4809-4821. doi: 10.1242/dev.00694
89. Price, M., Lemaistre, M., Pischetola, M., Di Lauro, R., and Duboule, D. (1991). A mouse gene related to Distal-less shows a restricted expression in the developing forebrain. Nature 351, 748-751. doi: 10.1038/351748a0
90. Propper, C. R., Jones, R. E., and Lopez, K. H. (1992). Distribution of arginine vasotocin in the brain of the lizard Anolis carolinensis. Cell Tissue Res. 267, 391-398. doi: 10.1007/bf00302978
91. Puelles, L. (1995). A segmental morphological paradigm for understanding vertebrate forebrains. Brain Behav. Evol. 46, 319-337. doi: 10.1159/000316271
92. Puelles, L. (2001). Brain segmentation and forebrain development in amniotes. Brain Res. Bull. 55, 695-710. doi: 10.1016/s0361-9230(01)00588-3
93. Puelles, L., Kuwana, E., Puelles, E., Bulfone, A., Shimamura, K., Keleher, J., et al. (2000). Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6 and Tbr-1. J. Comp. Neurol. 424, 409-438. doi: 10.1002/1096-9861(20000828)424:3<409::aid-cne3>3.0.co;2-7
94. Puelles, L., Martinez, S., Martinez-de-la-Torre, M., and Rubenstein, J. L. (2004). “Gene maps and related histogenetic domains in the forebrain and midbrain,” in The Rat Nervous System, ed G. Paxinos 3rd Edn. (San Diego: Elsevier), 3-125.
95. Puelles, L., Martinez de la Torre, M., Bardet, S., and Rubenstein, J. L. (2012a). “Hypothalamus,” in The Mouse Nervous System, eds C. Watson, G. Paxinos and L. Puelles (London: Academic press. Elsevier), 221-313.
96. Puelles, L., Martinez de la Torre, M., Ferran, J. L., and Watson, C. (2012b). “Diencephalon,” in The Mouse Nervous System, eds C. Watson, G. Paxinos and L. Puelles (London: Academic press. Elsevier), 313-337.
97. Puelles, L., and Rubenstein, J. L. (1993). Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci. 16, 472-479. doi: 10.1016/0166-2236(93)90080-6
98. Puelles, L., and Rubenstein, J. L. (2003). Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci. 26, 469-476. doi: 10.1016/s0166-2236(03)00234-0
99. Rohr, K. B., Barth, K. A., Varga, Z. M., and Wilson, S. W. (2001). The nodal pathway acts upstream of hedgehog signaling to specify ventral telencephalic identity. Neuron 29, 341-351. doi: 10.1016/s0896-6273(01)00210-0
100. Roth, M., Bonev, B., Lindsay, J., Lea, R., Panagiotaki, N., Houart, C., et al. (2010). FoxG1 and TLE2 act cooperatively to regulate ventral telencephalon formation. Development 137, 1553-1562. doi: 10.1242/dev.044909
101. Rubenstein, J. L., Martinez, S., Shimamura, K., and Puelles, L. (1994). The embryonic vertebrate forebrain: the prosomeric model. Science 266, 578-580. doi: 10.1126/science.7939711
102. Ryu, S., Mahler, J., Acampora, D., Holzschuh, J., Erhardt, S., Omodei, D., et al. (2007). Orthopedia homeodomain protein is essential for diencephalic dopaminergic neuron development. Curr. Biol. 17, 873-880. doi: 10.1016/j.cub.2007.04.003
103. Sanchez-Arrones, L., Ferran, J. L., Rodriguez-Gallardo, L., and Puelles, L. (2009). Incipient forebrain boundaries traced by differential gene expression and fate mapping in the chick neural plate. Dev. Biol. 335, 43-65. doi: 10.1016/j.ydbio.2009.08.012
104. Sander, M., Paydar, S., Ericson, J., Briscoe, J., Berber, E., German, M., et al. (2000). Ventral neural patterning by Nkx homeobox genes: Nkx6.1 controls somatic motor neuron and ventral interneuron fates. Genes Dev. 14, 2134-2139. doi: 10.1101/gad.820400
105. Shimamura, K., Hartigan, D. J., Martinez, S., Puelles, L., and Rubenstein, J. L. (1995). Longitudinal organization of the anterior neural plate and neural tube. Development 121, 3923-3933.
106. Shimogori, T., Lee, D. A., Miranda-Angulo, A., Yang, Y., Wang, H., Jiang, L., et al. (2010). A genomic atlas of mouse hypothalamic development. Nat. Neurosci. 13, 767-775. doi: 10.1038/nn.2545
107. Smeets, W. J., and Gonzalez, A. (2000). Catecholamine systems in the brain of vertebrates: new perspectives through a comparative approach. Brain Res. Brain Res. Rev. 33, 308-379. doi: 10.1016/s0165-0173(00)00034-5
108. Smeets, W. J., Jonker, A. J., and Hoogland, P. V. (1987). Distribution of dopamine in the forebrain and midbrain of the red-eared turtle, Pseudemys scripta elegans, reinvestigated using antibodies against dopamine. Brain Behav. Evol. 30, 121-142. doi: 10.1159/000118642
109. Smeets, W. J., Sevensma, J. J., and Jonker, A. J. (1990). Comparative analysis of vasotocin-like immunoreactivity in the brain of the turtle Pseudemys scripta elegans and the snake Python regius. Brain Behav. Evol. 35, 65-84. doi: 10.1159/000115857
110. Stoykova, A., and Gruss, P. (1994). Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J. Neurosci. 14, 1395-1412.
111. Striedter, G. F. (1997). The telencephalon of tetrapods in evolution. Brain Behav. Evol. 49, 179-213. doi: 10.1159/000105936
112. Tao, W., and Lai, E. (1992). Telencephalon-restricted expression of BF-1, a new member of the HNF-3/fork head gene family, in the developing rat brain. Neuron 8, 957-966. doi: 10.1016/0896-6273(92)90210-5
113. Ten Donkelaar, H. J. (1998a). “Anurans,” in The Central Nervous System of Vertebrates, eds R. Nieuwenhuys, H. J. ten Donkelaar and C. Nicholson (London: Springer), 1151-1314.
114. Ten Donkelaar, H. J. (1998b). “Reptiles,” in The Central Nervous System of Vertebrates, ed R. Nieuwenhuys (London: Springer), 1315-1524.
115. Tessmar-Raible, K., Raible, F., Christodoulou, F., Guy, K., Rembold, M., Hausen, H., et al. (2007). Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution. Cell 129, 1389-1400. doi: 10.1016/j.cell.2007.04.041
116. Toresson, H., Potter, S. S., and Campbell, K. (2000). Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development 127, 4361-4371.
117. Tsuruo, Y., Hökfelt, T., and Visser, T. (1987). Thyrotropin releasing hormone (TRH)-immunoreactive cell groups in the rat central nervous system. Exp. Brain Res. 68,213-217. doi: 10.1007/bf00255248
118. van den Akker, W. M., Brox, A., Puelles, L., Durston, A. J., and Medina, L. (2008). Comparative functional analysis provides evidence for a crucial role for the homeoboxgene Nkx2.1/Titf-1 in forebrain evolution. J. Comp. Neurol. 506,211-223. doi: 10.1002/cne.21542
119. Wang, W., and Lufkin, T. (2000). The murine Otp homeobox gene plays an essential role in the specification of neuronal cell lineages in the developing hypothalamus. Dev. Biol. 227, 432-449. doi: 10.1006/dbio.2000.9902
120. Wolf, A., and Ryu, S. (2013). Specification of posterior hypothalamic neurons requires coordinated activities of Fezf2, Otp, Sim1a and Foxb1.2. Development 140, 1762-1773. doi: 10.1242/dev.085357
121. Yee, C. L., Wang, Y., Anderson, S., Ekker, M., and Rubenstein, J. L. (2009). Arcuate nucleus expression of NKX2.1 and DLX and lineages expressing these transcription factors in neuropeptide Y(+), proopiomelanocortin(+) and tyrosine hydroxylase(+) neurons in neonatal and adult mice. J. Comp. Neurol. 517, 37-50. doi: 10.1002/cne.22132
122. Zardoya, R., and Meyer, A. (2001a). The evolutionary position of turtles revised. Naturwissenschaften 88, 193-200. doi: 10.1007/s001140100228
123. Zardoya, R., and Meyer, A. (2001b). On the origin of and phylogenetic relationships among living amphibians. Proc. Natl. Acad. Sci. U S A98, 7380-7383. doi: 10.1073/pnas.111455498
124. Zhao, X. F., Suh, C. S., Prat, C. R., Ellingsen, S., and Fjose, A. (2009). Distinct expression of two foxg1 paralogues in zebrafish. Gene Expr. Patterns 9, 266-272. doi: 10.1016/j.gep.2009.04.001