DOI: 10.1146/annurev.neuro.21.1.445. REGIONALIZATION OF THE PROSENCEPHALIC NEURAL PLATE

REGIONALIZATION OF THE PROSENCEPHALIC NEURAL PLATE

10.1146/annurev.neuro.21.1.445

Crossref journal-article

Annual Reviews

Annual Review of Neuroscience (22)

Abstract

▪ Abstract Recent embryological studies are beginning to establish that the underlying organization of the forebrain may be reduced to relatively simple elements that are common to all vertebrates. We begin this chapter by reviewing studies that describe the similarities in prospective fate and molecular organization of the developing neural plate in fish, frogs, chickens, and mice. The chapter next addresses mechanisms that regulate regional specification in the anterior central nervous system. There is now evidence that the axial mesendoderm anterior to the notochord (the prechordal plate) has a central role in induction of the floor and basal plate primordia (hypothalamus) of the forebrain. Patterning of the anterolateral neural plate (telencephalon) may be regulated by FGF8 produced in the anterior neural ridge. Thus, the synthesis of information from fate mapping and experimental embryological and genetic studies is illuminating the mechanisms that generate the different components of the forebrain.

Bibliography

Rubenstein, J. L. R., Shimamura, K., Martinez, S., & Puelles, L. (1998). REGIONALIZATION OF THE PROSENCEPHALIC NEURAL PLATE. Annual Review of Neuroscience, 21(1), 445â477.

Authors 4

John L. R. Rubenstein (first)
Kenji Shimamura (additional)
Salvador Martinez (additional)
Luis Puelles (additional)

References 139 Referenced 434

10.1242/dev.121.10.3279 / Development by Acampora D (1996)
10.1016/0012-1606(84)90326-9
10.1002/cne.903550207
10.1002/(SICI)1096-9861(19970310)379:2<171::AID-CNE1>3.3.CO;2-0
10.1016/S0896-6273(00)80345-1
10.1242/dev.120.10.2979 / Development by Ang SL (1994)
10.1242/dev.122.1.243 / Development by Ang S-L (1996)
10.1093/icb/21.2.391
10.1016/0925-4773(94)00301-3
10.1242/dev.121.6.1755 / Development by Barth KA (1995)
10.1016/0092-8674(93)90249-P
10.1242/dev.121.4.993 / Development by Blitz IL (1995)
10.1242/dev.124.2.373 / Development by Blumberg B (1997)
{'key': 'b14', 'author': 'Bortier H', 'year': '1992', 'journal-title': 'Development'} / Development by Bortier H (1992)
10.1038/382595a0
10.1523/JNEUROSCI.13-07-03155.1993
10.1016/0896-6273(95)90065-9
10.1002/neu.480240909
10.1038/383407a0
10.1016/0012-1606(85)90101-0
10.1016/0012-1606(87)90118-7
10.1242/dev.121.12.4349 / Development by Cox WG (1995)
10.1242/dev.121.2.439 / Development by Crossley PH (1995)
10.1038/380066a0
10.1016/0012-1606(83)90065-9
10.1242/dev.121.7.2099 / Development by Dickinson ME (1995)
10.1002/neu.480241003
10.1073/pnas.93.12.6191
{'key': 'b29', 'first-page': '735', 'volume': '40', 'author': 'Eagleson GW', 'year': '1996', 'journal-title': 'Int. J. Dev. Biol.'} / Int. J. Dev. Biol. by Eagleson GW (1996)
10.1002/neu.480280203
10.1002/neu.480210305
10.1016/0092-8674(93)90627-3
10.1016/S0960-9822(95)00185-0
10.1016/S0092-8674(00)81386-0
10.1016/0092-8674(95)90536-7
10.1038/363630a0
10.1159/000147600
10.1046/j.1432-0436.1994.5710031.x
10.1002/jez.1402670409
10.1016/0306-4522(92)90149-V
10.1242/dev.121.5.1433 / Development by Grindley JC (1995)
10.1242/dev.123.1.143 / Development by Hammerschmidt M (1996)
10.1016/S0168-9525(00)89073-3
10.1242/dev.120.10.2879 / Development by Hatada Y (1994)
10.1002/neu.480251010
10.1073/pnas.91.6.2061
10.1242/dev.123.1.191 / Development by Heisenberg CP (1996)
{'key': 'b48', 'volume-title': 'Manipulating the Mouse Embryo.', 'author': 'Hogan B', 'year': '1994'} / Manipulating the Mouse Embryo. by Hogan B (1994)
10.1242/dev.122.1.195 / Development by Hyatt GA (1996)
10.1016/0896-6273(95)90062-4
10.1016/0092-8674(95)90454-9
10.1002/jez.1401540303
10.1093/icb/31.4.628
{'key': 'b54', 'first-page': '1', 'volume': '7', 'author': 'Jacobson CO', 'year': '1959', 'journal-title': 'J. Embryol. Exp. Morph.'} / J. Embryol. Exp. Morph. by Jacobson CO (1959)
10.1146/annurev.ne.08.030185.000443
Jacobson M. 1990. Methods for clonal analysis and tracing cell lineages in the vertebrate CNS. InMethods in Neuroscience, ed. PM Conn. Orlando, FL: Academic (10.1016/B978-0-12-185254-2.50029-2)
10.1016/0168-9525(96)81383-7
10.1242/dev.115.1.1 / Development by Kawamura K (1992)
10.1002/aja.1001930302
10.1002/aja.1001930303
10.1242/dev.108.4.581 / Development by Kimmel CB (1990)
10.1101/gad.10.1.60
10.1016/0092-8674(93)90628-4
10.1242/dev.121.11.3627 / Development by Lamb TM (1995)
Lawson KA, Pedersen RA. 1992. Clonal analysis of cell fate during gastrulation and early neurulation in the mouse. InPostimplantation Development in the Mouse, pp. 3–26. Chichester: Wiley (Ciba Found. Symp. 165) (10.1002/9780470514221.ch2)
10.1016/0014-4827(73)90600-9
10.1007/BF01940787
10.1242/dev.124.3.603 / Development by Li HS (1997)
10.1016/0925-4773(94)90062-0
10.1016/0092-8674(95)90276-7
10.1126/science.274.5290.1109
10.1242/dev.121.10.3267 / Development by Macdonald R (1995)
10.1016/0896-6273(94)90044-2
10.1006/dbio.1994.1120
10.1038/375322a0
10.1016/0925-4773(95)00376-2
10.1016/0896-6273(91)90237-T
10.1101/gad.9.21.2646
10.1002/cne.902130303
10.1242/dev.122.9.2933 / Development by Nicolas JF (1996)
10.1111/j.1440-169X.1990.00023.x
10.1006/dbio.1996.0207
10.1242/dev.121.1.87 / Development by Quinlan GA (1995)
10.1242/dev.121.3.707 / Development by Pannese M (1995)
10.1242/dev.122.12.3893 / Development by Pellegrini M (1996)
10.1016/0959-437X(95)90055-L
10.1242/dev.117.1.205 / Development by Placzek M (1993)
10.1242/dev.122.5.1523 / Development by Psychoyos D (1996)
10.1159/000113282
10.1002/cne.902660210
10.1002/jmor.1051940205
10.1159/000113247
10.1016/0166-2236(93)90080-6
10.1016/0092-8674(94)90514-2
10.1016/0092-8674(95)90397-6
10.1038/ng1196-357
{'key': 'b97', 'volume-title': 'The Avian Embryo. Structural and Functional Development.', 'author': 'Romanoff AI', 'year': '1960'} / The Avian Embryo. Structural and Functional Development. by Romanoff AI (1960)
{'key': 'b98', 'first-page': '73', 'volume': '38', 'author': 'Rosenquist GC', 'year': '1966', 'journal-title': 'Carnegie Contrib. Embryol.'} / Carnegie Contrib. Embryol. by Rosenquist GC (1966)
10.1016/0925-4773(95)00380-J
10.1126/science.7939711
10.1016/S0070-2153(08)60546-3
Rubenstein JLR, Shimamura K. 1997. Regulation of patterning and differentiation in the embryonic vertebrate forebrain. InNeuronal Development, ed. WM Cowan, TM Jessell, SL Zipurski, pp. 356–90. Oxford: Oxford Univ. Press. (10.1093/acprof:oso/9780195111668.003.0010)
10.1016/0166-2236(94)90006-X
10.1016/S0959-437X(05)80176-5
10.1016/0092-8674(94)90068-X
10.1242/dev.118.1.47 / Development by Sasaki H (1993)
10.1242/dev.123.1.165 / Development by Schier AF (1996)
10.1007/BF00334879
10.1002/ar.1092330211
10.1242/dev.112.3.713 / Development by Schoenwolf GC (1991)
10.1002/jez.1402490305
10.1242/dev.105.1.17 / Development by Schoenwolf GC (1989)
10.1038/374425a0
10.1242/dev.121.12.3923 / Development by Shimamura K (1995)
10.1159/000111190
10.1242/dev.124.14.2709 / Development by Shimamura K (1997)
10.1016/S0960-9822(95)00041-8
10.1017/CBO9780511525322
10.1002/jez.1401200105
10.1016/0925-4773(94)00300-C
10.1007/BF00299630
10.1523/JNEUROSCI.14-03-01395.1994
10.1242/dev.122.11.3453 / Development by Stoykova A (1996)
10.1002/aja.1002010309
10.1126/science.274.5290.1115
10.1016/S0960-9822(95)00130-8
10.1242/dev.122.11.3381 / Development by Torres M (1996)
{'key': 'b128', 'first-page': '1', 'volume': '41', 'author': 'Vaage S', 'year': '1969', 'journal-title': 'Ergeb. Anat. Entwicklungsgesch.'} / Ergeb. Anat. Entwicklungsgesch. by Vaage S (1969)
10.1093/icb/33.4.434
10.1242/dev.105.1.9 / Development by Wetts R (1989)
10.1007/BF01381160
10.1016/0168-9525(93)90039-K
10.1242/dev.121.8.2595 / Development by Woo K (1995)
10.1038/381319a0
10.1016/0896-6273(95)90262-7
10.1016/0092-8674(91)90247-V
10.1242/dev.124.1.101 / Development by Yoshida M (1997)
10.1038/382632a0
10.1242/dev.119.1.221 / Development by Zimmerman K (1993)

Dates

Type	When
Created	23 years, 1 month ago (July 27, 2002, 7:45 a.m.)
Deposited	3 years, 10 months ago (Oct. 14, 2021, 12:40 p.m.)
Indexed	2 weeks ago (Aug. 23, 2025, 12:59 a.m.)
Issued	27 years, 6 months ago (March 1, 1998)
Published	27 years, 6 months ago (March 1, 1998)
Published Print	27 years, 6 months ago (March 1, 1998)

Funders 0

None

BibTeX

@article{Rubenstein_1998, title={REGIONALIZATION OF THE PROSENCEPHALIC NEURAL PLATE}, volume={21}, ISSN={1545-4126}, url={http://dx.doi.org/10.1146/annurev.neuro.21.1.445}, DOI={10.1146/annurev.neuro.21.1.445}, number={1}, journal={Annual Review of Neuroscience}, publisher={Annual Reviews}, author={Rubenstein, John L. R. and Shimamura, Kenji and Martinez, Salvador and Puelles, Luis}, year={1998}, month=mar, pages={445–477} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        23
      ]
    ],
    "date-time": "2025-08-23T04:59:12Z",
    "timestamp": 1755925152456
  },
  "reference-count": 139,
  "publisher": "Annual Reviews",
  "issue": "1",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1998,
        3
      ]
    ]
  },
  "abstract": "<jats:p> \u25aa Abstract\u2002 Recent embryological studies are beginning to establish that the underlying organization of the forebrain may be reduced to relatively simple elements that are common to all vertebrates. We begin this chapter by reviewing studies that describe the similarities in prospective fate and molecular organization of the developing neural plate in fish, frogs, chickens, and mice. The chapter next addresses mechanisms that regulate regional specification in the anterior central nervous system. There is now evidence that the axial mesendoderm anterior to the notochord (the prechordal plate) has a central role in induction of the floor and basal plate primordia (hypothalamus) of the forebrain. Patterning of the anterolateral neural plate (telencephalon) may be regulated by FGF8 produced in the anterior neural ridge. Thus, the synthesis of information from fate mapping and experimental embryological and genetic studies is illuminating the mechanisms that generate the different components of the forebrain. </jats:p>",
  "DOI": "10.1146/annurev.neuro.21.1.445",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        27
      ]
    ],
    "date-time": "2002-07-27T11:45:50Z",
    "timestamp": 1027770350000
  },
  "page": "445-477",
  "source": "Crossref",
  "is-referenced-by-count": 434,
  "title": "REGIONALIZATION OF THE PROSENCEPHALIC NEURAL PLATE",
  "prefix": "10.1146",
  "volume": "21",
  "author": [
    {
      "given": "John L. R.",
      "family": "Rubenstein",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Nina Ireland Laboratory of Developmental Neurobiology, Center for Neurobiology and Psychiatry, Department of Psychiatry, University of California, San Francisco, 401 Parnassus Avenue, San Francisco, California 94143-0984"
        }
      ]
    },
    {
      "given": "Kenji",
      "family": "Shimamura",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Nina Ireland Laboratory of Developmental Neurobiology, Center for Neurobiology and Psychiatry, Department of Psychiatry, University of California, San Francisco, 401 Parnassus Avenue, San Francisco, California 94143-0984"
        }
      ]
    },
    {
      "given": "Salvador",
      "family": "Martinez",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Morphology, Faculty of Medicine, University of Murcia, Murcia, 30100, Spain"
        }
      ]
    },
    {
      "given": "Luis",
      "family": "Puelles",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Morphology, Faculty of Medicine, University of Murcia, Murcia, 30100, Spain"
        }
      ]
    }
  ],
  "member": "22",
  "reference": [
    {
      "key": "b1",
      "doi-asserted-by": "crossref",
      "first-page": "3279",
      "DOI": "10.1242/dev.121.10.3279",
      "volume": "121",
      "author": "Acampora D",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "b2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(84)90326-9"
    },
    {
      "key": "b3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.903550207"
    },
    {
      "key": "b4",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1096-9861(19970310)379:2<171::AID-CNE1>3.3.CO;2-0"
    },
    {
      "key": "b5",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0896-6273(00)80345-1"
    },
    {
      "key": "b6",
      "doi-asserted-by": "crossref",
      "first-page": "2979",
      "DOI": "10.1242/dev.120.10.2979",
      "volume": "120",
      "author": "Ang SL",
      "year": "1994",
      "journal-title": "Development"
    },
    {
      "key": "b7",
      "doi-asserted-by": "crossref",
      "first-page": "243",
      "DOI": "10.1242/dev.122.1.243",
      "volume": "122",
      "author": "Ang S-L",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "b8",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/icb/21.2.391"
    },
    {
      "key": "b9",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0925-4773(94)00301-3"
    },
    {
      "key": "b10",
      "doi-asserted-by": "crossref",
      "first-page": "1755",
      "DOI": "10.1242/dev.121.6.1755",
      "volume": "121",
      "author": "Barth KA",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b11",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(93)90249-P"
    },
    {
      "key": "b12",
      "doi-asserted-by": "crossref",
      "first-page": "993",
      "DOI": "10.1242/dev.121.4.993",
      "volume": "121",
      "author": "Blitz IL",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b13",
      "doi-asserted-by": "crossref",
      "first-page": "373",
      "DOI": "10.1242/dev.124.2.373",
      "volume": "124",
      "author": "Blumberg B",
      "year": "1997",
      "journal-title": "Development"
    },
    {
      "key": "b14",
      "author": "Bortier H",
      "year": "1992",
      "journal-title": "Development"
    },
    {
      "key": "b15",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/382595a0"
    },
    {
      "key": "b16",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.13-07-03155.1993"
    },
    {
      "key": "b17",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0896-6273(95)90065-9"
    },
    {
      "key": "b18",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/neu.480240909"
    },
    {
      "key": "b19",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/383407a0"
    },
    {
      "key": "b20",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(85)90101-0"
    },
    {
      "key": "b21",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(87)90118-7"
    },
    {
      "key": "b22",
      "doi-asserted-by": "crossref",
      "first-page": "4349",
      "DOI": "10.1242/dev.121.12.4349",
      "volume": "121",
      "author": "Cox WG",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b23",
      "doi-asserted-by": "crossref",
      "first-page": "439",
      "DOI": "10.1242/dev.121.2.439",
      "volume": "121",
      "author": "Crossley PH",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/380066a0"
    },
    {
      "key": "b25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(83)90065-9"
    },
    {
      "key": "b26",
      "doi-asserted-by": "crossref",
      "first-page": "2099",
      "DOI": "10.1242/dev.121.7.2099",
      "volume": "121",
      "author": "Dickinson ME",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b27",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/neu.480241003"
    },
    {
      "key": "b28",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.93.12.6191"
    },
    {
      "key": "b29",
      "first-page": "735",
      "volume": "40",
      "author": "Eagleson GW",
      "year": "1996",
      "journal-title": "Int. J. Dev. Biol."
    },
    {
      "key": "b30",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/neu.480280203"
    },
    {
      "key": "b31",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/neu.480210305"
    },
    {
      "key": "b32",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(93)90627-3"
    },
    {
      "key": "b33",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0960-9822(95)00185-0"
    },
    {
      "key": "b34",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)81386-0"
    },
    {
      "key": "b35",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(95)90536-7"
    },
    {
      "key": "b36",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/363630a0"
    },
    {
      "key": "b37",
      "doi-asserted-by": "publisher",
      "DOI": "10.1159/000147600"
    },
    {
      "key": "b38",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1432-0436.1994.5710031.x"
    },
    {
      "key": "b39",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jez.1402670409"
    },
    {
      "key": "b40",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0306-4522(92)90149-V"
    },
    {
      "key": "b41",
      "doi-asserted-by": "crossref",
      "first-page": "1433",
      "DOI": "10.1242/dev.121.5.1433",
      "volume": "121",
      "author": "Grindley JC",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b42",
      "doi-asserted-by": "crossref",
      "first-page": "143",
      "DOI": "10.1242/dev.123.1.143",
      "volume": "123",
      "author": "Hammerschmidt M",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "b43",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0168-9525(00)89073-3"
    },
    {
      "key": "b44",
      "doi-asserted-by": "crossref",
      "first-page": "2879",
      "DOI": "10.1242/dev.120.10.2879",
      "volume": "120",
      "author": "Hatada Y",
      "year": "1994",
      "journal-title": "Development"
    },
    {
      "key": "b45",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/neu.480251010"
    },
    {
      "key": "b46",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.91.6.2061"
    },
    {
      "key": "b47",
      "doi-asserted-by": "crossref",
      "first-page": "191",
      "DOI": "10.1242/dev.123.1.191",
      "volume": "123",
      "author": "Heisenberg CP",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "b48",
      "volume-title": "Manipulating the Mouse Embryo.",
      "author": "Hogan B",
      "year": "1994"
    },
    {
      "key": "b49",
      "doi-asserted-by": "crossref",
      "first-page": "195",
      "DOI": "10.1242/dev.122.1.195",
      "volume": "122",
      "author": "Hyatt GA",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "b50",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0896-6273(95)90062-4"
    },
    {
      "key": "b51",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(95)90454-9"
    },
    {
      "key": "b52",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jez.1401540303"
    },
    {
      "key": "b53",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/icb/31.4.628"
    },
    {
      "key": "b54",
      "first-page": "1",
      "volume": "7",
      "author": "Jacobson CO",
      "year": "1959",
      "journal-title": "J. Embryol. Exp. Morph."
    },
    {
      "key": "b55",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.ne.08.030185.000443"
    },
    {
      "key": "b56",
      "doi-asserted-by": "crossref",
      "unstructured": "Jacobson M. 1990. Methods for clonal analysis and tracing cell lineages in the vertebrate CNS. InMethods in Neuroscience, ed. PM Conn. Orlando, FL: Academic",
      "DOI": "10.1016/B978-0-12-185254-2.50029-2"
    },
    {
      "key": "b57",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0168-9525(96)81383-7"
    },
    {
      "key": "b58",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1242/dev.115.1.1",
      "volume": "115",
      "author": "Kawamura K",
      "year": "1992",
      "journal-title": "Development"
    },
    {
      "key": "b59",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/aja.1001930302"
    },
    {
      "key": "b60",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/aja.1001930303"
    },
    {
      "key": "b61",
      "doi-asserted-by": "crossref",
      "first-page": "581",
      "DOI": "10.1242/dev.108.4.581",
      "volume": "108",
      "author": "Kimmel CB",
      "year": "1990",
      "journal-title": "Development"
    },
    {
      "key": "b62",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.10.1.60"
    },
    {
      "key": "b63",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(93)90628-4"
    },
    {
      "key": "b64",
      "doi-asserted-by": "crossref",
      "first-page": "3627",
      "DOI": "10.1242/dev.121.11.3627",
      "volume": "121",
      "author": "Lamb TM",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b65",
      "doi-asserted-by": "crossref",
      "unstructured": "Lawson KA, Pedersen RA. 1992. Clonal analysis of cell fate during gastrulation and early neurulation in the mouse. InPostimplantation Development in the Mouse, pp. 3\u201326. Chichester: Wiley (Ciba Found. Symp. 165)",
      "DOI": "10.1002/9780470514221.ch2"
    },
    {
      "key": "b66",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-4827(73)90600-9"
    },
    {
      "key": "b67",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF01940787"
    },
    {
      "key": "b68",
      "doi-asserted-by": "crossref",
      "first-page": "603",
      "DOI": "10.1242/dev.124.3.603",
      "volume": "124",
      "author": "Li HS",
      "year": "1997",
      "journal-title": "Development"
    },
    {
      "key": "b69",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0925-4773(94)90062-0"
    },
    {
      "key": "b70",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(95)90276-7"
    },
    {
      "key": "b71",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.274.5290.1109"
    },
    {
      "key": "b72",
      "doi-asserted-by": "crossref",
      "first-page": "3267",
      "DOI": "10.1242/dev.121.10.3267",
      "volume": "121",
      "author": "Macdonald R",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b73",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0896-6273(94)90044-2"
    },
    {
      "key": "b74",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1994.1120"
    },
    {
      "key": "b75",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/375322a0"
    },
    {
      "key": "b76",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0925-4773(95)00376-2"
    },
    {
      "key": "b77",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0896-6273(91)90237-T"
    },
    {
      "key": "b78",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.9.21.2646"
    },
    {
      "key": "b79",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.902130303"
    },
    {
      "key": "b80",
      "doi-asserted-by": "crossref",
      "first-page": "2933",
      "DOI": "10.1242/dev.122.9.2933",
      "volume": "122",
      "author": "Nicolas JF",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "b81",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1440-169X.1990.00023.x"
    },
    {
      "key": "b82",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1996.0207"
    },
    {
      "key": "b83",
      "doi-asserted-by": "crossref",
      "first-page": "87",
      "DOI": "10.1242/dev.121.1.87",
      "volume": "121",
      "author": "Quinlan GA",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b84",
      "doi-asserted-by": "crossref",
      "first-page": "707",
      "DOI": "10.1242/dev.121.3.707",
      "volume": "121",
      "author": "Pannese M",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b85",
      "doi-asserted-by": "crossref",
      "first-page": "3893",
      "DOI": "10.1242/dev.122.12.3893",
      "volume": "122",
      "author": "Pellegrini M",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "b86",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0959-437X(95)90055-L"
    },
    {
      "key": "b87",
      "doi-asserted-by": "crossref",
      "first-page": "205",
      "DOI": "10.1242/dev.117.1.205",
      "volume": "117",
      "author": "Placzek M",
      "year": "1993",
      "journal-title": "Development"
    },
    {
      "key": "b88",
      "doi-asserted-by": "crossref",
      "first-page": "1523",
      "DOI": "10.1242/dev.122.5.1523",
      "volume": "122",
      "author": "Psychoyos D",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "b89",
      "doi-asserted-by": "publisher",
      "DOI": "10.1159/000113282"
    },
    {
      "key": "b90",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.902660210"
    },
    {
      "key": "b91",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jmor.1051940205"
    },
    {
      "key": "b92",
      "doi-asserted-by": "publisher",
      "DOI": "10.1159/000113247"
    },
    {
      "key": "b93",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0166-2236(93)90080-6"
    },
    {
      "key": "b94",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(94)90514-2"
    },
    {
      "key": "b95",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(95)90397-6"
    },
    {
      "key": "b96",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ng1196-357"
    },
    {
      "key": "b97",
      "volume-title": "The Avian Embryo. Structural and Functional Development.",
      "author": "Romanoff AI",
      "year": "1960"
    },
    {
      "key": "b98",
      "first-page": "73",
      "volume": "38",
      "author": "Rosenquist GC",
      "year": "1966",
      "journal-title": "Carnegie Contrib. Embryol."
    },
    {
      "key": "b99",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0925-4773(95)00380-J"
    },
    {
      "key": "b100",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.7939711"
    },
    {
      "key": "b101",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0070-2153(08)60546-3"
    },
    {
      "key": "b102",
      "doi-asserted-by": "crossref",
      "unstructured": "Rubenstein JLR, Shimamura K. 1997. Regulation of patterning and differentiation in the embryonic vertebrate forebrain. InNeuronal Development, ed. WM Cowan, TM Jessell, SL Zipurski, pp. 356\u201390. Oxford: Oxford Univ. Press.",
      "DOI": "10.1093/acprof:oso/9780195111668.003.0010"
    },
    {
      "key": "b103",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0166-2236(94)90006-X"
    },
    {
      "key": "b104",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0959-437X(05)80176-5"
    },
    {
      "key": "b105",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(94)90068-X"
    },
    {
      "key": "b106",
      "doi-asserted-by": "crossref",
      "first-page": "47",
      "DOI": "10.1242/dev.118.1.47",
      "volume": "118",
      "author": "Sasaki H",
      "year": "1993",
      "journal-title": "Development"
    },
    {
      "key": "b107",
      "doi-asserted-by": "crossref",
      "first-page": "165",
      "DOI": "10.1242/dev.123.1.165",
      "volume": "123",
      "author": "Schier AF",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "b108",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00334879"
    },
    {
      "key": "b109",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ar.1092330211"
    },
    {
      "key": "b110",
      "doi-asserted-by": "crossref",
      "first-page": "713",
      "DOI": "10.1242/dev.112.3.713",
      "volume": "112",
      "author": "Schoenwolf GC",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "b111",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jez.1402490305"
    },
    {
      "key": "b112",
      "doi-asserted-by": "crossref",
      "first-page": "17",
      "DOI": "10.1242/dev.105.1.17",
      "volume": "105",
      "author": "Schoenwolf GC",
      "year": "1989",
      "journal-title": "Development"
    },
    {
      "key": "b113",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/374425a0"
    },
    {
      "key": "b114",
      "doi-asserted-by": "crossref",
      "first-page": "3923",
      "DOI": "10.1242/dev.121.12.3923",
      "volume": "121",
      "author": "Shimamura K",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b115",
      "doi-asserted-by": "publisher",
      "DOI": "10.1159/000111190"
    },
    {
      "key": "b116",
      "doi-asserted-by": "crossref",
      "first-page": "2709",
      "DOI": "10.1242/dev.124.14.2709",
      "volume": "124",
      "author": "Shimamura K",
      "year": "1997",
      "journal-title": "Development"
    },
    {
      "key": "b117",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0960-9822(95)00041-8"
    },
    {
      "key": "b118",
      "doi-asserted-by": "publisher",
      "DOI": "10.1017/CBO9780511525322"
    },
    {
      "key": "b119",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jez.1401200105"
    },
    {
      "key": "b120",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0925-4773(94)00300-C"
    },
    {
      "key": "b121",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00299630"
    },
    {
      "key": "b122",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.14-03-01395.1994"
    },
    {
      "key": "b123",
      "doi-asserted-by": "crossref",
      "first-page": "3453",
      "DOI": "10.1242/dev.122.11.3453",
      "volume": "122",
      "author": "Stoykova A",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "b124",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/aja.1002010309"
    },
    {
      "key": "b125",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.274.5290.1115"
    },
    {
      "key": "b126",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0960-9822(95)00130-8"
    },
    {
      "key": "b127",
      "doi-asserted-by": "crossref",
      "first-page": "3381",
      "DOI": "10.1242/dev.122.11.3381",
      "volume": "122",
      "author": "Torres M",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "b128",
      "first-page": "1",
      "volume": "41",
      "author": "Vaage S",
      "year": "1969",
      "journal-title": "Ergeb. Anat. Entwicklungsgesch."
    },
    {
      "key": "b129",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/icb/33.4.434"
    },
    {
      "key": "b130",
      "doi-asserted-by": "crossref",
      "first-page": "9",
      "DOI": "10.1242/dev.105.1.9",
      "volume": "108",
      "author": "Wetts R",
      "year": "1989",
      "journal-title": "Development"
    },
    {
      "key": "b131",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF01381160"
    },
    {
      "key": "b132",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0168-9525(93)90039-K"
    },
    {
      "key": "b133",
      "doi-asserted-by": "crossref",
      "first-page": "2595",
      "DOI": "10.1242/dev.121.8.2595",
      "volume": "121",
      "author": "Woo K",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b134",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/381319a0"
    },
    {
      "key": "b135",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0896-6273(95)90262-7"
    },
    {
      "key": "b136",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90247-V"
    },
    {
      "key": "b137",
      "doi-asserted-by": "crossref",
      "first-page": "101",
      "DOI": "10.1242/dev.124.1.101",
      "volume": "124",
      "author": "Yoshida M",
      "year": "1997",
      "journal-title": "Development"
    },
    {
      "key": "b138",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/382632a0"
    },
    {
      "key": "b139",
      "doi-asserted-by": "crossref",
      "first-page": "221",
      "DOI": "10.1242/dev.119.1.221",
      "volume": "119",
      "author": "Zimmerman K",
      "year": "1993",
      "journal-title": "Development"
    }
  ],
  "container-title": "Annual Review of Neuroscience",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.annualreviews.org/doi/pdf/10.1146/annurev.neuro.21.1.445",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2021,
        10,
        14
      ]
    ],
    "date-time": "2021-10-14T16:40:27Z",
    "timestamp": 1634229627000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.annualreviews.org/doi/10.1146/annurev.neuro.21.1.445"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1998,
        3
      ]
    ]
  },
  "references-count": 139,
  "journal-issue": {
    "issue": "1",
    "published-print": {
      "date-parts": [
        [
          1998,
          3
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1146/annurev.neuro.21.1.445"
  ],
  "URL": "http://dx.doi.org/10.1146/annurev.neuro.21.1.445",
  "relation": {},
  "ISSN": [
    "0147-006X",
    "1545-4126"
  ],
  "subject": [],
  "container-title-short": "Annu. Rev. Neurosci.",
  "published": {
    "date-parts": [
      [
        1998,
        3
      ]
    ]
  }
}