The zebrafish is an excellent vertebrate model for the study of the cellular interactions underlying the patterning and the morphogenesis of the nervous system. Here, we report regional fate maps of the zebrafish anterior nervous system at two key stages of neural development: the beginning (6 hours) and the end (10 hours) of gastrulation. Early in gastrulation, we find that the presumptive neurectoderm displays a predictable organization that reflects the future anteroposterior and dorsoventral order of the central nervous system. The precursors of the major brain subdivisions (forebrain, midbrain, hindbrain, neural retina) occupy discernible, though overlapping, domains within the dorsal blastoderm at 6 hours. As gastrulation proceeds, these domains are rearranged such that the basic order of the neural tube is evident at 10 hours. Furthermore, the anteroposterior and dorsoventral order of the progenitors is refined and becomes aligned with the primary axes of the embryo. Time-lapse video microscopy shows that the rearrangement of blastoderm cells during gastrulation is highly ordered. Cells near the dorsal midline at 6 hours, primarily forebrain progenitors, display anterior-directed migration. Cells more laterally positioned, corresponding to midbrain and hindbrain progenitors, converge at the midline prior to anteriorward migration. These results demonstrate a predictable order in the presumptive neurectoderm, suggesting that patterning interactions may be well underway by early gastrulation. The fate maps provide the basis for further analyses of the specification, induction and patterning of the anterior nervous system, as well as for the interpretation of mutant phenotypes and gene-expression patterns.

Reference

Ballard
W.
(
1973
)
A new fate map for Salmo gairdneri.
J. Exp. Zool
184
,
49
73
Cho
K. W. Y.
,
Blumberg
B.
,
Steinbeisser
H.
,
De Robertis
E. M.
(
1991
)
Molecular nature of Spemman's organizer: the role of Xenopus homeobox gene goosecoid.
Cell
67
,
1111
1120
Couly
G.
,
Le Douarin
N. M.
(
1988
)
The fate map of the cephalic neural convergence and extension of the neural plate by the organizer of Xenopus.
Dev. Dyn
193
,
218
234
Donaich
T.
(
1993
)
Planar and vertical induction of anteroposterior pattern during the development of the amphibian central nervous system.
J. Neurobiol
24
,
1256
1275
Driever
W.
,
Stemple
D.
,
Schier
A.
,
Solnica-Krezel
L.
(
1994
)
Zebrafish: genetic tools for studying vertebrate development.
Trends Genet
10
,
152
159
Hatta
K.
,
Bremiller
R.
,
Westerfield
M.
,
Kimmel
C. B.
(
1991
)
Diversity of expression of engrailed -like antigens in zebrafish.
Development
112
,
821
832
Hatta
D.
,
Kimmel
C. B.
,
Ho
R. K.
,
Walker
C.
(
1991
)
The cyclops mutation blocks specification of the floor plate of the zebrafish central nervous system.
Nature
350
,
339
341
Hatta
K.
,
Puschel
A. W.
,
Kimmel
C. B.
(
1994
)
Midline signaling in the primordium of the zebrafish anterior central nervous system.
Proc. Natl. Acad. Sci. USA
91
,
2061
2065
Helde
K. A.
,
Wilson
E. T.
,
Cretekos
C. J.
,
Grunwald
D. J.
(
1994
)
Contribution of early cells to the fate map of the zebrafish gastrula.
Science
265
,
517
520
Jacobson
M.
,
Hirose
G.
(
1978
)
Origin of the retina from both sides of the embryonic brain: A contribution to the problem of crossing at the optic chiasma.
Science
202
,
637
639
Keller
R. E.
(
1975
)
Vital dye mapping of the gastrula and neurula of Xenopus laevis. I. Prospective areas and morphogenetic movements of the superficial layer.
Dev. Biol
42
,
222
241
Keller
R. E.
(
1976
)
Vital dye mapping of the gastrula and neurula of Xenopus laevis. II. Prospective areas and morphogenetic movements of the deep layer.
Dev. Biol
51
,
118
137
Keller
R. E.
,
Shih
J.
,
Sater
A.
(
1992
)
The cellular basis of the convergence and extension of the Xenopus neural plate.
Dev. Dyn
193
,
199
217
Kessler
D. S.
,
Melton
D. A.
(
1994
)
Vertebrate embryonic induction: mesodermal and neural patterning.
Science
266
,
596
604
Keynes
R.
,
Lumsden
A.
(
1990
)
Segmentation and origin of regional diversity in the vertebrate central nervous system.
Neuron
2
,
1
9
Kimmel
C. B.
,
Law
R. D.
(
1985
)
Cell lineage of zebrafish blastomeres. III. Clonal analysis of the blastula and gastrula stages.
Dev. Biol
108
,
94
101
Kimmel
C. B.
,
Warga
R. M.
,
Kane
D. A.
(
1994
)
Cell cycles and clonal strings during formation of the zebrafish central nervous system.
Development
120
,
265
276
Kimmel
C. B.
,
Warga
R. M.
,
Schilling
T. F.
(
1990
)
Origin and organization of the zebrafish fate map.
Development
108
,
581
594
Krauss
S.
,
Concordet
J.-P.
,
Ingham
P. W.
(
1993
)
A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos.
Cell
75
,
1431
1444
Krauss
S.
,
Johansen
T.
,
Korzh
V.
,
Fjose
A.
(
1991
)
Expression of the zebrafish paired box gene pax [zf-b] during early neurogenesis.
Development
113
,
1193
1206
Lawson
K. A.
,
Meneses
J. J.
,
Pedersen
R. A.
(
1991
)
Clonal analysis of epiblast fate during germ layer formation in the mouse embryo.
Development
113
,
891
911
Moon
R. T.
,
Christian
J. L.
(
1992
)
Competence modifiers synergize with growth factors during mesoderm induction and patterning in Xenopus.
Cell
71
,
709
712
Mullins
M. C.
,
Hammerschmidt
M.
,
Haffter
P.
,
Nusslein-Volhard
C.
(
1994
)
Large-scale mutagenesis in the zebrafish: in search of genes controlling development in a vertebrate.
Current Biol
4
,
189
202
Oppenheimer
J. M.
(
1936
)
Transplantation experiments on developing teleosts (Fundulus and Perca).
J. Exp. Zool
72
,
409
437
Oxtoby
E.
,
Jowett
T.
(
1993
)
Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development.
Nucl. Acids Res
21
,
1087
1095
Puschel
A. W.
,
Gruss
P.
,
Westerfield
M.
(
1992
)
Sequnce and expression pattern of pax-6 are highly conserved between zebrafish and mice.
Development
114
,
643
651
Ruiz i Altaba
A.
,
Jessel
T. M.
(
1993
)
Midline cells and the organization of the vertebrate neuraxis.
Curr. Op. Genet. Dev
3
,
633
640
Ruiz i Altaba
A.
(
1993
)
Induction and axial patterning of the neural plate: planar and vertical signals.
J. Neurobiol
24
,
1276
1304
Schmitt
E. A.
,
Dowling
J. E.
(
1994
)
Early eye morphogenesis in the zebrafish, Brachydanio rerio.
J. Comp. Neurol
344
,
532
542
Schulte-Merker
S.
,
Hammerschmidt
M.
,
Beuchle
D.
,
Cho
K. W.
,
De Robertis
E. M.
,
Nusslein-Volhard
C.
(
1994
)
Expression of zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos.
Development
120
,
843
852
Selleck
M. A.
,
Stern
C. D.
(
1991
)
Fate mapping and cell lineage analysis of Hensen's node in the chick embryo.
Development
112
,
615
626
Slack
J. M. W.
,
Tannahill
D.
(
1992
)
Mechanism of anteroposterior axis specification in vertebrates. Lessons from the amphibians.
Development
114
,
285
30
Stachel
S. E.
,
Grunwald
D. J.
,
Myers
P. Z.
(
1993
)
Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish.
Development
117
,
1261
1274
Strahle
U.
,
Blader
P.
,
Henrique
D.
,
Ingham
P. W.
(
1993
)
Axial, a zebrafish gene expressed along the developing body axis, shows altered expression in cyclops mutant embryos.
Gene Dev
7
,
1436
1446
Warga
R. M.
,
Kimmel
C. B.
(
1990
)
Cell movements during epiboly and gastrulation in zebrafish.
Development
108
,
569
590
Wetts
R.
,
Fraser
S. E.
(
1988
)
Multipotent precursors can give rise to all major cell types of the frog retina.
Science
39
,
1142
1145
Wetts
R.
,
Fraser
S. E.
(
1989
)
Slow intermixing of cells during Xenopus embryogenesis contributes to the consistency of the blastomere fate map.
Development
108
,
9
15
Wilson
E. T.
,
Helde
K. A.
,
Grunwald
D. J.
(
1993
)
Something's fishy here- rethinking cell movements and cell fate in the zebrafish embryo.
Trends. Neurosci
9
,
348
352
Xu
Q.
,
Holder
N.
,
Patient
R.
,
Wilson
S. W.
(
1994
)
Spatially regulated expression of three receptor tyrosine kinase genes during gastrulation in the zebrafish.
Development
120
,
2287
299
This content is only available via PDF.