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Abstract

In the brain of adult mice, cells that divide in the subventricular zone of the lateral ventricle migrate up to 5 millimeters to the olfactory bulb where they differentiate into neurons. These migrating cells were found to move as chains through a well-defined pathway, the rostral migratory stream. Electron microscopic analysis of serial sections showed that these chains contained only closely apposed, elongated neuroblasts connected by membrane specializations. A second cell type, which contained glial fibrillary acidic protein, ensheathed the chains of migrating neuroblasts. Thus, during chain migration, neural precursors moved associated with each other and were not guided by radial glial or axonal fibers.

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References

1
ANAT REC 166, 257 (1970).
2
ALTMAN J, AUTORADIOGRAPHIC INVESTIGATION OF CELL PROLIFERATION IN BRAINS OF RATS AND CATS, ANATOMICAL RECORD 145, 573 (1963).
3
ALTMAN J, AUTORADIOGRAPHIC AND HISTOLOGICAL STUDIES OF POSTNATAL NEUROGENESIS .4. CELL PROLIFERATION AND MIGRATION IN ANTERIOR FOREBRAIN, WITH SPECIAL REFERENCE TO PERSISTING NEUROGENESIS IN OLFACTORY BULB, JOURNAL OF COMPARATIVE NEUROLOGY 137, 433 (1969).
4
ALVAREZBUYLLA A, MONOCLONAL-ANTIBODY REVEALS RADIAL GLIA IN ADULT AVIAN BRAIN, JOURNAL OF COMPARATIVE NEUROLOGY 264, 159 (1987).
5
ALVAREZBUYLLA A, MIGRATION OF YOUNG NEURONS IN ADULT AVIAN BRAIN, NATURE 335, 353 (1988).
6
BAYER A. S., NEURONS IN THE RAT DENTATE GYRUS GRANULAR LAYER SUBSTANTIALLY INCREASE DURING JUVENILE AND ADULT LIFE, SCIENCE 216, 890 (1982).
7
BIGNAMI A, LOCALIZATION OF GLIAL FIBRILLARY ACIDIC PROTEIN IN ASTROCYTES BY IMMUNOFLUORESCENCE, BRAIN RESEARCH 43, 429 (1972).
8
BIGNAMI A, ASTROCYTE-SPECIFIC PROTEIN AND NEUROGLIAL DIFFERENTIATION - IMMUNOFLUORESCENCE STUDY WITH ANTIBODIES TO GLIAL FIBRILLARY ACIDIC PROTEIN, JOURNAL OF COMPARATIVE NEUROLOGY 153, 27 (1974).
9
BONFANTI L, EXPRESSION OF POLYSIALYLATED NEURAL CELL-ADHESION MOLECULE BY PROLIFERATING CELLS IN THE SUBEPENDYMAL LAYER OF THE ADULT-RAT, IN ITS ROSTRAL EXTENSION AND IN THE OLFACTORY-BULB, NEUROSCIENCE 62, 291 (1994).
10
BOURRAT F, MIGRATORY PATHWAYS AND SELECTIVE AGGREGATION OF THE LATERAL RETICULAR NEURONS IN THE RAT EMBRYO - A HORSERADISH-PEROXIDASE INVITRO STUDY, WITH SPECIAL REFERENCE TO MIGRATION PATTERNS OF THE PRECEREBELLAR NUCLEI, JOURNAL OF COMPARATIVE NEUROLOGY 294, 1 (1990).
11
COROTTO S. F., NEUROGENESIS PERSISTS IN THE SUBEPENDYMAL LAYER OF THE ADULT-MOUSE BRAIN, NEUROSCIENCE LETTERS 149, 111 (1993).
12
CREMER H, INACTIVATION OF THE N-CAM GENE IN MICE RESULTS IN SIZE-REDUCTION OF THE OLFACTORY-BULB AND DEFICITS IN SPATIAL-LEARNING, NATURE 367, 455 (1994).
13
CULICAN M. S., CORTICAL RADIAL GLIA - IDENTIFICATION IN TISSUE-CULTURE AND EVIDENCE FOR THEIR TRANSFORMATION TO ASTROCYTES, JOURNAL OF NEUROSCIENCE 10, 684 (1990).
14
EDMONDSON C. J., GLIAL-GUIDED GRANULE NEURON MIGRATION INVITRO - A HIGH-RESOLUTION TIME-LAPSE VIDEO MICROSCOPIC STUDY, JOURNAL OF NEUROSCIENCE 7, 1928 (1987).
15
FARQUHAR G. M., JUNCTIONAL COMPLEXES IN VARIOUS EPITHELIA, JOURNAL OF CELL BIOLOGY 17, 375 (1963).
16
FISHELL G, DISPERSION OF NEURAL PROGENITORS WITHIN THE GERMINAL ZONES OF THE FOREBRAIN, NATURE 362, 636 (1993).
17
GADISSEUX F. J., DYNAMIC CHANGES IN THE DENSITY OF RADIAL GLIAL FIBERS OF THE DEVELOPING MURINE CEREBRAL WALL - A QUANTITATIVE IMMUNOHISTOLOGICAL ANALYSIS, JOURNAL OF COMPARATIVE NEUROLOGY 322, 246 (1992).
18
GARCIAVERDUGO M. J., ULTRASTRUCTURE OF PUTATIVE MIGRATING CELLS IN THE CEREBRAL-CORTEX OF LACERTA-GALLOTI, JOURNAL OF MORPHOLOGY 189, 189 (1986).
19
GOLDMAN A. S., NEURONAL PRODUCTION, MIGRATION, AND DIFFERENTIATION IN A VOCAL CONTROL NUCLEUS OF THE ADULT FEMALE CANARY BRAIN, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 80, 2390 (1983).
20
GOODENOUGH A. D., A FINE STRUCTURAL ANALYSIS OF INTERCELLULAR JUNCTIONS IN MOUSE LIVER, JOURNAL OF CELL BIOLOGY 45, 272 (1970).
21
GRAY E. G., RADIAL ARRANGEMENT OF CLONALLY RELATED CELLS IN THE CHICKEN OPTIC TECTUM - LINEAGE ANALYSIS WITH A RECOMBINANT RETROVIRUS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 85, 7356 (1988).
22
HERRUP K, CURR OPIN NEUROBIOL 4, 108 (1994).
23
JACOBSON M, DEV NEUROBIOLOGY (1991).
24
KAPLAN S. M., NEUROGENESIS IN ADULT RAT - ELECTRON-MICROSCOPIC ANALYSIS OF LIGHT AUTORADIOGRAPHS, SCIENCE 197, 1092 (1977).
25
KISHI K, MIGRATION OF BIPOLAR SUBEPENDYMAL CELLS, PRECURSORS OF THE GRANULE CELLS OF THE RAT OLFACTORY-BULB, WITH REFERENCE TO THE ARRANGEMENT OF THE RADIAL GLIAL FIBERS, ARCHIVES OF HISTOLOGY AND CYTOLOGY 53, 219 (1990).
26
KISHI K, GOLGI STUDIES ON THE DEVELOPMENT OF GRANULE CELLS OF THE RAT OLFACTORY-BULB WITH REFERENCE TO MIGRATION IN THE SUBEPENDYMAL LAYER, JOURNAL OF COMPARATIVE NEUROLOGY 258, 112 (1987).
27
LOIS C, LONG-DISTANCE NEURONAL MIGRATION IN THE ADULT MAMMALIAN BRAIN, SCIENCE 264, 1145 (1994).
28
LOPEZGARCIA C, DELAYED POSTNATAL NEUROGENESIS IN THE CEREBRAL-CORTEX OF LIZARDS, DEVELOPMENTAL BRAIN RESEARCH 43, 167 (1988).
29
LUSKIN B. M., RESTRICTED PROLIFERATION AND MIGRATION OF POSTNATALLY GENERATED NEURONS DERIVED FROM THE FOREBRAIN SUBVENTRICULAR ZONE, NEURON 11, 173 (1993).
30
MCCONNELL K. S., DEVELOPMENT AND DECISION-MAKING IN THE MAMMALIAN CEREBRAL-CORTEX, BRAIN RESEARCH REVIEWS 13, 1 (1988).
31
MISSON P. J., IDENTIFICATION OF RADIAL GLIAL-CELLS WITHIN THE DEVELOPING MURINE CENTRAL NERVOUS-SYSTEM - STUDIES BASED UPON A NEW IMMUNOHISTOCHEMICAL MARKER, DEVELOPMENTAL BRAIN RESEARCH 44, 95 (1988).
32
MOODY A. S., DEVELOPMENTAL RELATIONSHIPS BETWEEN TRIGEMINAL GANGLIA AND TRIGEMINAL MOTONEURONS IN CHICK-EMBRYOS .2. GANGLION AXON INGROWTH GUIDES MOTONEURON MIGRATION, JOURNAL OF COMPARATIVE NEUROLOGY 213, 344 (1983).
33
ONO K, MODE OF NEURONAL MIGRATION OF THE PONTINE STREAM IN FETAL MICE, ANATOMY AND EMBRYOLOGY 182, 11 (1990).
34
ONO K, N-CAM MUTATION INHIBITS TANGENTIAL NEURONAL MIGRATION AND IS PHENOCOPIED BY ENZYMATIC REMOVAL OF POLYSIALIC ACID, NEURON 13, 595 (1994).
35
OROURKE A. N., DIVERSE MIGRATORY PATHWAYS IN THE DEVELOPING CEREBRAL-CORTEX, SCIENCE 258, 299 (1992).
36
PIXLEY SKR, TRANSITION BETWEEN IMMATURE RADIAL GLIA AND MATURE ASTROCYTES STUDIED WITH A MONOCLONAL-ANTIBODY TO VIMENTIN, DEVELOPMENTAL BRAIN RESEARCH 15, 201 (1984).
37
PUELLES L, OCULOMOTOR NEUROBLASTS MIGRATE ACROSS MIDLINE IN FETAL RAT-BRAIN, ANATOMY AND EMBRYOLOGY 150, 187 (1977).
38
RAKIC P, PRINCIPLES OF NEURAL CELL-MIGRATION, EXPERIENTIA 46, 882 (1990).
39
RAKIC P, MODE OF CELL MIGRATION TO SUPERFICIAL LAYERS OF FETAL MONKEY NEOCORTEX, JOURNAL OF COMPARATIVE NEUROLOGY 145, 61 (1972).
40
RAKIC P, NEURONAL-GLIAL INTERACTION DURING BRAIN-DEVELOPMENT, TRENDS IN NEUROSCIENCES 4, 184 (1981).
41
RAYMOND A. P., POST-EMBRYONIC GROWTH OF THE OPTIC TECTUM IN GOLDFISH .1. LOCATION OF GERMINAL CELLS AND NUMBERS OF NEURONS PRODUCED, JOURNAL OF NEUROSCIENCE 3, 1077 (1983).
42
ROUSSELOT P, EMBRYONIC (PSA) N-CAM REVEALS CHAINS OF MIGRATING NEUROBLASTS BETWEEN THE LATERAL VENTRICLE AND THE OLFACTORY-BULB OF ADULT MICE, JOURNAL OF COMPARATIVE NEUROLOGY 351, 51 (1995).
43
SCHMECHEL E. D., GOLGI-STUDY OF RADIAL GLIAL-CELLS IN DEVELOPING MONKEY TELENCEPHALON - MORPHOGENESIS AND TRANSFORMATION INTO ASTROCYTES, ANATOMY AND EMBRYOLOGY 156, 115 (1979).
44
STAHELIN A. L., INT REV CYTOL 39, 191 (1974).
45
TOMASIEWICZ H, GENETIC DELETION OF A NEURAL CELL-ADHESION MOLECULE VARIANT (N-CAM-180) PRODUCES DISTINCT DEFECTS IN THE CENTRAL-NERVOUS-SYSTEM, NEURON 11, 1163 (1993).
46
VOIGT T, DEVELOPMENT OF GLIAL-CELLS IN THE CEREBRAL WALL OF FERRETS - DIRECT TRACING OF THEIR TRANSFORMATION FROM RADIAL GLIA INTO ASTROCYTES, JOURNAL OF COMPARATIVE NEUROLOGY 289, 74 (1989).
47
WALSH C, CELL LINEAGE AND CELL-MIGRATION IN THE DEVELOPING CEREBRAL-CORTEX, EXPERIENTIA 46, 940 (1990).
48
WALSH C, CLONALLY RELATED CORTICAL-CELLS SHOW SEVERAL MIGRATION PATTERNS, SCIENCE 241, 1342 (1988).

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Science
Volume 271 | Issue 5251
16 February 1996

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Published in print: 16 February 1996

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Carlos Lois
C. Lois and A. Alvarez-Buylla, Rockefeller University, 1230 York Avenue, New York, NY 10021, USA.
Jose-Manuel García-Verdugo
J.-M. García-Verdugo, Facultad de Biológicas, Universitas Valencia, Burjassot, Valencia 46100, Spain.
Arturo Alvarez-Buylla(1)
C. Lois and A. Alvarez-Buylla, Rockefeller University, 1230 York Avenue, New York, NY 10021, USA.

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(1)
To whom correspondence should be addressed.

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