Zebrafish and medaka: Model organisms for a comparative developmental approach of brain asymmetry

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1519, 2009, Pages 991-1003

  Signore, Iskra A ^a   Guerrero, Néstor ^a   Loosli, Felix ^b   Colombo, Alicia ^a   Villalón, Aldo ^a   Wittbrodt, Joachim ^c   Concha, Miguel L ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Brain asymmetry; Development; Epithalamus; Heterochrony; Laterality; Teleosts

Indexed keywords

BRAIN; CANALIZATION (BIOLOGY); EMBRYONIC DEVELOPMENT; EVOLUTIONARY BIOLOGY; FISH; NEUROLOGY; ONTOGENY; SPATIOTEMPORAL ANALYSIS; TELEOST;

DANIO RERIO; ORYZIAS; ORYZIAS LATIPES; ORYZIINAE; TELEOSTEI; VERTEBRATA;

TUBULIN;

AGING; ANIMAL; ANIMAL MODEL; ARTICLE; BRAIN; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEMISPHERIC DOMINANCE; HISTOLOGY; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; ORYZIAS; PHYSIOLOGY; REPORTER GENE; VISCERA; ZEBRA FISH;

AGING; ANIMALS; BRAIN; FUNCTIONAL LATERALITY; GENES, REPORTER; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MODELS, ANIMAL; ORYZIAS; TUBULIN; VISCERA; ZEBRAFISH;

EID: 65649135829     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2008.0260     Document Type: Article

References (80)

1. Aizawa, H., Bianco, I. H., Hamaoka, T., Miyashita, T., Uemura, O., Concha, M. L., Russell, C., Wilson, S. W. & Okamoto, H. 2005 Laterotopic representation of left-right information onto the dorso-ventral axis of a zebrafish midbrain target nucleus. Curr. Biol. 15, 238-243. (doi:10. 1016/j.cub.2005.01.014)
2. Aizawa, H., Goto, M., Sato, T. & Okamoto, H. 2007 Temporally regulated asymmetric neurogenesis causes left-right difference in the zebrafish habenular structures. Dev. Cell 12, 87-98. (doi:10.1016/j.devcel. 2006.10.004)
3. Barth, K. A., Miklosi, A., Watkins, J., Bianco, I. H., Wilson, S. W & Andrew, R. J. 2005 fsi zebrafish show concordant reversal of laterality of viscera, neuroanatomy, and a subset of behavioral responses. Curr. Biol. 15, 844-850. (doi:10. 1016/j.cub.2005.03.047)
4. Bianco, I. H. & Wilson, S. W 2009 The habenular nuclei: a conserved asymmetric relay station in the vertebrate brain. Phil. Trans. R. Soc. B 364, 1005-1020. (doi:10.1098/rstb. 2008.0213)
5. Bianco, I. H., Carl, M., Russell, C., Clarke, J. D. & Wilson, S. W 2008 Brain asymmetry is encoded at the level of axon terminal morphology. Neural Dev. 3, 9.
6. Bisgrove, B. W., Essner, J. J. & Yost, H. J. 1999 Regulation of midline development by antagonism of lefty and nodal signaling. Development (Camb. Engl.) 126, 3253-3262.
7. Bisgrove, B. W., Essner, J. J. & Yost, H. J. 2000 Multiple pathways in the midline regulate concordant brain, heart and gut left-right asymmetry. Development (Camb. Engl.) 127, 3567-3579.
8. Borg, B., Ekström, P. & Van Veen, T. 1983 The parapineal organ of teleosts. Acta Zool. (Stockholm) 64, 211-218.
9. Carl, M., Bianco, I. H., Bajoghli, B., Aghaallaei, N., Czerny, T. & Wilson, S. W 2007 Wnt/Axinl/beta-catenin signaling regulates asymmetric nodal activation, elaboration, and concordance of CNS asymmetries. Neuron 55, 393-405. (doi:10.1016/j.neuron.2007.07.007)
10. Chipman, A. D., Haas, A., Tchernov, E. & Khaner, O. 2000 Variation in anuran embryogenesis: differences in sequence and timing of early developmental events. J. Exp. Zool. 288, 352-365. (doi:10.1002/1097-010X (20001215)288:4<352::AID-JEZ8>3.0.CO;2-2)
11. Clancy, B., Darlington, R. B. & Finlay, B. L. 2001 Translating developmental time across mammalian species. Neuroscience 105, 7-17. (doi:10.1016/S0306-4522(01)00171-3)
12. Concha, M. L. 2004 The dorsal diencephalic conduction system of zebrafish as a model of vertebrate brain lateralisation. Neuroreport 15, 1843-1846. (doi:10.1097/00001756-200408260-00001)
13. Concha, M. L. & Wilson, S. W 2001 Asymmetry in the epithalamus of vertebrates. J. Anat. 199, 63-84. (doi:10. 1017/S0021878201008329)
14. Concha, M. L., Burdine, R. D., Russell, C., Schier, A. F. & Wilson, S. W 2000 A nodal signaling pathway regulates the laterality of neuroanatomical asymmetries in the zebrafish forebrain. Neuron 28, 399-409. (doi:10.1016/S0896-6273(00)00120-3)
15. Concha, M. L. et al. 2003 Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality. Neuron 39, 423-438. (doi:10.1016/S0896-6273 (03)00437-9)
16. Dettlaff, T. A. & Dettlaff, A. A. 1961 On relative dimensionless characteristics of the development duration in embryology. Arch. Biol. 72, 1-16.
17. Ekstrom, P., Borg, B. & Van Veen, T. 1983 Ontogenetic development of the pineal organ, parapineal organ, and retina of the three-spined stickleback, Gasterosteus aculeatus L. (Teleostei). Development of photoreceptors. Cell Tiss. Res. 233, 593-609. (doi:10.1007/BF00212227)
18. Ellison, G. 1994 Stimulant-induced psychosis, the dopamine theory of schizophrenia, and the habenula. Brain Res. Rev. 19, 223-239. (doi:10.1016/0165-0173(94)90012-4)
19. Escalante-Mead, P. R., Minshew, N. J. & Sweeney, J. A. 2003 Abnormal brain lateralization in high-functioning autism. J. Autism Dev. Disord. 33, 539-543. (doi:10.1023/A: 10258 87713788)
20. Essner, J. J., Branford, W W., Zhang, J. & Yost, H. J. 2000 Mesendoderm and left-right brain, heart and gut development are differentially regulated by pitx2 isoforms. Development (Camb. Engl.) 127, 1081-1093.
21. Essner, J. J., Amack, J. D., Nyholm, M. K., Harris, E. B. & Yost, H. J. 2005 Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development (Camb. Engl.) 132, 1247-1260. (doi:10.1242/dev.01663)
22. Freitas, C., Rodrigues, S., Saude, L. & Palmeirim, I. 2005 Running after the clock. Int. J. Dev. Biol. 49, 317-324. (doi:10.1387/ijdb.041955cf)
23. Furutani-Seiki, M. & Wittbrodt, J. 2004 Medaka and zebrafish, an evolutionary twin study. Mech. Dev. 121, 629-637. (doi:10.1016/j.mod.2004.05.010)
24. Gajewski, M., Elmasri, H., Girschick, M., Sieger, D. & Winkler, C. 2006 Comparative analysis of her genes during fish somitogenesis suggests a mouse/chick-like mode of oscillation in medaka. Dev. Genes Evol. 216, 315-332. (doi:10.1007/s00427-006-0059-6)
25. Gamse, J. T., Thisse, C., Thisse, B. & Halpern, M. E. 2003 The parapineal mediates left-right asymmetry in the zebrafish diencephalon. Development (Camb. Engl.) 130, 1059-1068. (doi:10.1242/dev.00270)
26. Gamse, J. T., Kuan, Y S., Macurak, M., Brosamle, C., Thisse, B., Thisse, C. & Halpern, M. E. 2005 Directional asymmetry of the zebrafish epithalamus guides dorsoven-tral innervation of the midbrain target. Development (Camb. Engl.) 132, 4869-4881. (doi:10.1242/dev.02046)
27. Gilmour, D. T., Maischein, H. M. & Nusslein-Volhard, C. 2002 Migration and function of a glial subtype in the vertebrate peripheral nervous system. Neuron 34, 577-588. (doi:10. 1016/S0896-6273(02)00683-9)
28. Giudicelli, F. & Lewis, J. 2004 The vertebrate segmentation clock. Curr. Opin. Genet. Dev. 14, 407-414. (doi:10.1016/j.gde.2004.06. 014)
29. Gould, S. J. 1977 Ontogeny and phylogeny. Cambridge, MA: Harvard University Press.
30. Guglielmotti, V. & Cristino, L. 2006 The interplay between the pineal complex and the habenular nuclei in lower vertebrates in the context of the evolution of cerebral asymmetry. Brain Res. Bull. 69, 475-488. (doi:10.1016/j.brainresbull.2006.03.010)
31. Güntürkün, O., Diekamp, B., Manns, M., Nottelmann, F., Prior, H., Schwarz, A. & Skiba, M. 2000 Asymmetry pays: visual lateralization improves discrimination success in pigeons. Curr. Biol. 10, 1079-1081. (doi:10.1016/S0960-9822(00)00671-0)
32. Hallgrimsson, B. 2003 Variation. In Keywords and concepts in evolutionary developmental biology (eds B. K. Hall & W. M. Olson), pp. 368-377. London, UK: Harvard University Press.
33. Halpern, M. E., Liang, J. O. & Gamse, J. T. 2003 Leaning to the left: laterality in the zebrafish forebrain. Trends Neurosci. 26, 308-313. (doi:10.1016/s0166-2236(03) 00129-2)
34. Hart, N. H. & Donovan, M. 2005 Fine structure of the chorion and site of sperm entry in the egg of Brachydanio. J. Exp. Zool. 227, 277-296. (doi:10.1002/jez.1402270212)
35. Hart, N. H., Pietri, R. & Donovan, M. 1984 The structure of the chorion and associated surface filaments in Oryzias: evidence for the presence of extracellular tubules. J. Exp. Zool. 230, 273-296. (doi:10.1002/jez. 1402300213)
36. Hirokawa, N., Tanaka, Y., Okada, Y. & Takeda, S. 2006 Nodal flow and the generation of left-right asymmetry. Cell 125, 33-45. (doi:10.1016/j.cell.2006.03.002)
37. Hutsler, J. & Galuske, R. A. 2003 Hemispheric asymmetries in cerebral cortical networks. Trends Neurosci. 26, 429-435. (doi:10.1016/S0166-2236(03)00198-X)
38. Inohaya, K., Yasumasu, S., Ishimaru, M., Ohyama, A., Iuchi, I. & Yamagami, K. 1995 Temporal and spatial patterns of gene expression for the hatching enzyme in the teleost embryo, Oryzias latipes. Dev. Biol. 171, 374-385. (doi:10. 1006/dbio.1995.1289)
39. Inohaya, K., Yasumasu, S., Araki, K., Naruse, K., Yamazaki, K., Yasumasu, I., Iuchi, I. & Yamagami, K. 1997 Species-dependent migration of fish hatching gland cells that express astacin-like proteases in common [corrected]. Dev. Growth Differ. 39, 191-197. (doi:10.1046/j.1440-169X.1997. t01-l-00007.x)
40. Iwamatsu, T. 2004 Stages of normal development in the medaka Oryzias latipes. Mech. Dev. 121, 605-618. (doi:10. 1016/j.mod.2004.03.012)
41. Jaszczyszyn, Y., Haeussler, M., Heuze, A., Debiais-Thibaud, M., Casane, D., Bourrat, F. & Joly, J. S. 2007 Comparison of the expression of medaka (Oryzias latipes) pitx genes with other vertebrates shows high conservation and a case of functional shuffling in the pituitary. Gene 406, 42-50. (doi:10.1016/j.gene.2007. 05.024)
42. Kennedy, D. N., O'Craven, K. M., Ticho, B. S., Goldstein, A. M., Makris, N. & Henson, J. W. 1999 Structural and functional brain asymmetries in human situs inversus totalis. Neurology 53, 1260-1265.
43. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. & Schilling, T. F. 1995 Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310. (doi:10.1002/aja. 1002030302)
44. Klemm, W. R. 2004 Habenular and interpeduncularis nuclei: shared components in multiple-function networks. Med. Sci. Monit. 10, RA261-RA273.
45. Kramer-Zucker, A. G., Olale, F., Haycraft, C. J., Yoder, B. K., Schier, A. F. & Drummond, I. A. 2005 Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development (Camb. Engl.) 132, 1907-1921. (doi:10.1242/dev.01772)
46. Kuan, Y S., Gamse, J. T., Schreiber, A. M. & Halpern, M. E. 2007 Selective asymmetry in a conserved forebrain to midbrain projection. J. Exp. Zool. Part B 308, 669-678. (doi:10.1002/jez.b.21184)
47. Levin, M. 2005 Left-right asymmetry in embryonic development: a comprehensive review. Mech. Dev. 122, 3-25. (doi:10.1016/j.mod. 2004.08.006)
48. Li, X., Branch, C. A., Ardekani, B. A., Bertisch, H., Hicks, C. & DeLisi, L. E. 2007 fMRI study of language activation in schizophrenia, schizoaffective disorder and in individuals genetically at high risk. Schizophr. Res. 96, 14-24. (doi:10. 1016/j.schres.2007.07.013)
49. Liang, J. O., Etheridge, A., Hantsoo, L., Rubinstein, A. L., Nowak, S. J., Izpisua Belmonte, J. C. & Halpern, M. E. 2000 Asymmetric nodal signaling in the zebrafish diencephalon positions the pineal organ. Development (Camb. Engl.) 127, 5101-5112.
50. Long, S., Ahmad, N. & Rebagliati, M. 2003 The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry. Development (Camb. Engl.) 130, 2303-2316. (doi:10.1242/dev.00436)
51. Loosli, F., Koster, R. W., Carl, M., Krone, A. & Wittbrodt, J. 1998 Six3, a medaka homologue of the Drosophila homeobox gene sine oculis is expressed in the anterior embryonic shield and the developing eye. Mech. Dev. 74, 159-164. (doi:10.1016/S0925-4773(98) 00055-0)
52. Lynn Lamoreux, M., Kelsh, R. N., Wakamatsu, Y & Ozato, K. 2005 Pigment pattern formation in the medaka embryo. Pigment Cell Res. 18, 64-73. (doi:10.1111/j.1600-0749.2005.00216.x)
53. MacArthur, R. H. & Wilson, E. O. 1967 The theory of island biogeography. Princeton, NJ: Princeton University Press.
54. Okada, Y., Takeda, S., Tanaka, Y., Belmonte, J. C. & Hirokawa, N. 2005 Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination. Cell 121, 633-644. (doi:10.1016/j.cell.2005. 04.008)
55. Oteiza, P., Koppen, M., Concha, M. L. & Heisenberg, C. P. 2008 Origin and shaping of the laterality organ in zebrafish. Development (Camb. Engl.) 135, 2807-2813.
56. Palmer, A. R. 2004 Symmetry breaking and the evolution of development. Science (New York, NY) 306, 828-833. (doi: 10.1126/science. 1103707)
57. Pascual, A., Huang, K. L., Neveu, J. & Preat, T. 2004 Neuroanatomy: brain asymmetry and long-term memory. Nature 427, 605-606. (doi:10.1038/427605a)
58. Rebagliati, M. R., Toyama, R., Haffter, P. & Dawid, I. B. 1998 cyclops encodes a nodal-related factor involved in midline signaling. Proc. Natl Acad. Sci. USA 95, 9932-9937. (doi:10.1073/pnas.95.17. 9932)
59. Reiss, J. O. 1989 The meaning of developmental time: a metric for comparative embryology. Am. Nat. 134, 170-189. (doi: 10.1086/284974)
60. Reiss, J. O. 2003 Time. In Keywords and concepts in evolutionary developmental biology (eds B. K. Hall & W. M. Olson), pp. 358-368. London, UK: Harvard University Press.
61. Rogers, L. J. 2000 Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang. 73, 236-253. (doi:10.1006/brln. 2000.2305)
62. Rogers, L. J. & Andrew, R. J. 2002 Comparative vertebrate lateralization. Cambridge, UK: Cambridge University Press.
63. Rogers, L. J. & Vallortigara, G. 2008 From antenna to antenna: lateral shift of olfactory memory recall by honeybees. PLoS ONE 3, e2340. (doi:10.137 I/journal, pone.0002340)
64. Rudeberg, C. 1969 Structure of the parapineal organ of the adult rainbow trout, Salmo gairdneri Richardson. Zeitschrift fur Zellforschung 93, 282-304. (doi:10.1007/BF00336695)
65. Saga, Y. & Takeda, H. 2001 The making of the somite: molecular events in vertebrate segmentation. Nat. Rev. 2, 835-845.
66. Sandyk, R. 1991 Relevance of the habenular complex to neuropsychiatry: a review and hypothesis. Int. J. Neurosci. 61, 189-219.
67. Sherman, G. F., Galaburda, A. M. & Geschwind, N. 1982 Neuroanatomical asymmetries in non-human species. Trends Neurosci. 5, 429-431. (doi:10.1016/0166-2236 (82)90233-8)
68. Soroldoni, D., Bajoghli, B., Aghaallaei, N. & Czerny, T. 2007 Dynamic expression pattern of nodal-related genes during left-right development in medaka. Gene Exp. Patt. 7, 93-101. (doi:10.1016/j.modgep.2006.05. 013)
69. Sutherland, R. J. 1982 The dorsal diencephalic conduction system: a review of the anotomy and functions of the habenular complex. Neurosci. Biobehav. Rev. 6, 1-13. (doi:10.1016/0149-7634(82)90003-3)
70. Tanaka, S., Kanzaki, R., Yoshibayashi, M., Kamiya, T. & Sugishita, M. 1999 Dichotic listening in patients with situs inversus: brain asymmetry and situs asymmetry. Neurop-sychologia 37, 869-874. (doi:10.1016/S0028-3932(98) 00144-4)
71. Thisse, C. & Thisse, B. 1999 Antivin, a novel and divergent member of the TGFbeta superfamily, negatively regulates mesoderm induction. Development (Camb. Engl.) 126, 229-240.
72. Toga, A. W. & Thompson, P. M. 2003 Mapping brain asymmetry. Nat. Rev. Neurosci. 4, 37-48. (doi:10.1038/nrnl009)
73. Torgersen, J. 1950 Situs inversus, asymmetry, and twinning. Am. J. Hum. Genet. 2, 361-370.
74. Toth, C., Rajput, M. & Rajput, A. H. 2004 Anomalies of asymmetry of clinical signs in Parkinsonism. Mov. Disord. 19, 151-157. (doi:10.1002/mds.10685)
75. Vallortigara, G. & Rogers, L. J. 2005 Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav. Brain Sci. 28, 575-589, discussion 589-633. (doi:10.1017/s0140525x05000105)
76. Van Valen, L. 1962 A study of fluctuating asymmetry. Evolution 16, 125-142. (doi:10.2307/2406192)
77. Van Veen, T. 1982 The parapineal and pineal organs of the elver (glass eel), Anguilla anguilla L. Cell Tiss. Res. 222, 433-444. (doi:10.1007/BF00213223)
78. Westerfield, M. 1996 The zebrafish book. Oregon, OR: University of Oregon Press.
79. Wittbrodt, J., Shima, A. & Schartl, M. 2002 Medaka: a model organism from the Far East. Nat. Rev. 3, 53-64. (doi:10.1038/nrg704)
80. Zelditch, M. 2003 Space, time and repatterning. In Keywords and concepts in evolutionary developmental biology (eds B. K. Hall & W. M. Olson), pp. 341-349. London, UK: Harvard University Press.