 |
 Previous Article | Next Article 
Journal of Neuroscience, Vol 14, 6695-6706, Copyright © 1994 by Society for Neuroscience
Synaptogenesis in hippocampal cultures: evidence indicating that axons and dendrites become competent to form synapses at different stages of neuronal development
TL Fletcher, P De Camilli and G Banker
Department of Psychiatry, Albany Medical College, New York 12208.
Hippocampal neurons in culture develop extensive axonal and dendritic
arbors and form numerous synapses. Presynaptic specializations occur at
sites of contact between axons and somata or dendrites but they do not
appear until day 3 in culture, even though numerous contacts between cells
develop within the first 24 hr (Fletcher et al., 1991). To determine
whether this delay in the appearance of presynaptic specializations could
be related to maturational events in the presynaptic axon or in the
postsynaptic target, "heterochronic" cocultures were prepared by adding
newly dissociated neurons to cultures containing mature neurons. The
competence of axons to form presynaptic vesicle clusters in response to
contact with the somata or dendrites of mature or immature neurons was
determined by immunofluorescent staining for synapsin I or synaptophysin.
After only 1 d of coculture, there was a fivefold increase in the number of
synapses along the somata and dendrites of the mature neurons, compared to
mature neurons cultured alone. If newly dissociated neurons were labeled
with a fluorescent dye before coculture, dye-labeled axons frequently were
colocalized with presynaptic specializations on mature cells. In contrast,
when the axons of mature neurons contacted immature neurons, synapses were
first observed only after coculture for 3 d. These results suggest that the
axons of hippocampal neurons have the capacity to form presynaptic
specializations soon after they emerge, provided they encounter appropriate
targets, but that the cell bodies and dendrites of hippocampal neurons are
not capable of inducing the formation of presynaptic specializations until
they reach a critical stage of maturation.
This article has been cited by other articles:
|
|
|
|
 
A. J. Barker, S. M. Koch, J. Reed, B. A. Barres, and E. M. Ullian
Developmental Control of Synaptic Receptivity
J. Neurosci.,
August 13, 2008;
28(33):
8150 - 8160.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Chen and J. L. Napoli
All-trans-retinoic acid stimulates translation and induces spine formation in hippocampal neurons through a membrane-associated RAR{alpha}
FASEB J,
January 1, 2008;
22(1):
236 - 245.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. I. Fogel, M. R. Akins, A. J. Krupp, M. Stagi, V. Stein, and T. Biederer
SynCAMs Organize Synapses through Heterophilic Adhesion
J. Neurosci.,
November 14, 2007;
27(46):
12516 - 12530.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Deng, J. Yao, C. Fang, N. Dong, B. Luscher, and G. Chen
Sequential Postsynaptic Maturation Governs the Temporal Order of GABAergic and Glutamatergic Synaptogenesis in Rat Embryonic Cultures
J. Neurosci.,
October 3, 2007;
27(40):
10860 - 10869.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Ben-Ari, J.-L. Gaiarsa, R. Tyzio, and R. Khazipov
GABA: A Pioneer Transmitter That Excites Immature Neurons and Generates Primitive Oscillations
Physiol Rev,
October 1, 2007;
87(4):
1215 - 1284.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. M. Valor, P. Charlesworth, L. Humphreys, C. N. G. Anderson, and S. G. N. Grant
Network activity-independent coordinated gene expression program for synapse assembly
PNAS,
March 13, 2007;
104(11):
4658 - 4663.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. A. Smith, H. Roy, P. De Koninck, P. Grutter, and Y. De Koninck
Dendritic Spine Viscoelasticity and Soft-Glassy Nature: Balancing Dynamic Remodeling with Structural Stability
Biophys. J.,
February 15, 2007;
92(4):
1419 - 1430.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Leterrier, J. Laine, M. Darmon, H. Boudin, J. Rossier, and Z. Lenkei
Constitutive activation drives compartment-selective endocytosis and axonal targeting of type 1 cannabinoid receptors.
J. Neurosci.,
March 22, 2006;
26(12):
3141 - 3153.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Monea, B. A. Jordan, S. Srivastava, S. DeSouza, and E. B. Ziff
Membrane localization of membrane type 5 matrix metalloproteinase by AMPA receptor binding protein and cleavage of cadherins.
J. Neurosci.,
February 22, 2006;
26(8):
2300 - 2312.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Cove, P. Blinder, E. Abi-Jaoude, M. Lafreniere-Roula, L. Devroye, and D. Baranes
Growth of Neurites toward Neurite- Neurite Contact Sites Increases Synaptic Clustering and Secretion and Is Regulated by Synaptic Activity
Cereb Cortex,
January 1, 2006;
16(1):
83 - 92.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Biederer
Progress from the Postsynaptic Side: Signaling in Synaptic Differentiation
Sci. Signal.,
March 8, 2005;
2005(274):
pe9 - pe9.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I.-J. Kim, K. M. Drahushuk, W.-Y. Kim, E. A. Gonsiorek, P. Lein, D. A. Andres, and D. Higgins
Extracellular Signal-Regulated Kinases Regulate Dendritic Growth in Rat Sympathetic Neurons
J. Neurosci.,
March 31, 2004;
24(13):
3304 - 3312.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Kim, A. Krichevsky, Y. Grad, G. D. Hayes, K. S. Kosik, G. M. Church, and G. Ruvkun
Identification of many microRNAs that copurify with polyribosomes in mammalian neurons
PNAS,
January 6, 2004;
101(1):
360 - 365.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Q. Sang and S.-S. Tan
Contact-associated Neurite Outgrowth and Branching of Immature Cortical Interneurons
Cereb Cortex,
June 1, 2003;
13(6):
677 - 683.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Gozlan and Y. Ben-Ari
Interneurons are the Source and the Targets of the First Synapses Formed in the Rat Developing Hippocampal Circuit
Cereb Cortex,
June 1, 2003;
13(6):
684 - 692.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Wang, A. Iacoangeli, S. Popp, I. A. Muslimov, H. Imataka, N. Sonenberg, I. B. Lomakin, and H. Tiedge
Dendritic BC1 RNA: Functional Role in Regulation of Translation Initiation
J. Neurosci.,
December 1, 2002;
22(23):
10232 - 10241.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I.-J. Kim, H. N. Beck, P. J. Lein, and D. Higgins
Interferon gamma Induces Retrograde Dendritic Retraction and Inhibits Synapse Formation
J. Neurosci.,
June 1, 2002;
22(11):
4530 - 4539.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. K. Mistry, E. W. Keefer, B. A. Cunningham, G. M. Edelman, and K. L. Crossin
Cultured rat hippocampal neural progenitors generate spontaneously active neural networks
PNAS,
January 24, 2002;
(2002)
22646599.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. G. Wells, X. Dong, E. M. Quinlan, Y.-S. Huang, M. F. Bear, J. D. Richter, and J. R. Fallon
A Role for the Cytoplasmic Polyadenylation Element in NMDA Receptor-Regulated mRNA Translation in Neurons
J. Neurosci.,
December 15, 2001;
21(24):
9541 - 9548.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. L. Scotti and H. Reuter
Synaptic and extrasynaptic gamma -aminobutyric acid type A receptor clusters in rat hippocampal cultures during development
PNAS,
March 1, 2001;
(2001)
61028798.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
C. M. Bose, D. Qiu, A. Bergamaschi, B. Gravante, M. Bossi, A. Villa, F. Rupp, and A. Malgaroli
Agrin Controls Synaptic Differentiation in Hippocampal Neurons
J. Neurosci.,
December 15, 2000;
20(24):
9086 - 9095.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. R. Cottrell, G. R. Dube, C. Egles, and G. Liu
Distribution, Density, and Clustering of Functional Glutamate Receptors Before and After Synaptogenesis in Hippocampal Neurons
J Neurophysiol,
September 1, 2000;
84(3):
1573 - 1587.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Grosse, A. Draguhn, L. Hohne, R. Tapp, R. W. Veh, and G. Ahnert-Hilger
Expression of Kv1 Potassium Channels in Mouse Hippocampal Primary Cultures: Development and Activity-Dependent Regulation
J. Neurosci.,
March 1, 2000;
20(5):
1869 - 1882.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Mohrmann, M. Werner, H. Hatt, and K. Gottmann
Target-Specific Factors Regulate the Formation of Glutamatergic Transmitter Release Sites in Cultured Neocortical Neurons
J. Neurosci.,
November 15, 1999;
19(22):
10004 - 10013.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Sestan, S. Artavanis-Tsakonas, and P. Rakic
Contact-Dependent Inhibition of Cortical Neurite Growth Mediated by Notch Signaling
Science,
October 22, 1999;
286(5440):
741 - 746.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
C. Verderio, S. Coco, A. Bacci, O. Rossetto, P. De Camilli, C. Montecucco, and M. Matteoli
Tetanus Toxin Blocks the Exocytosis of Synaptic Vesicles Clustered at Synapses But Not of Synaptic Vesicles in Isolated Axons
J. Neurosci.,
August 15, 1999;
19(16):
6723 - 6732.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Becher, A. Drenckhahn, I. Pahner, M. Margittai, R. Jahn, and G. Ahnert-Hilger
The Synaptophysin-Synaptobrevin Complex: a Hallmark of Synaptic Vesicle Maturation
J. Neurosci.,
March 15, 1999;
19(6):
1922 - 1931.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. D. Hazuka, D. L. Foletti, S.-C. Hsu, Y. Kee, F. W. Hopf, and R. H. Scheller
The sec6/8 Complex Is Located at Neurite Outgrowth and Axonal Synapse-Assembly Domains
J. Neurosci.,
February 15, 1999;
19(4):
1324 - 1334.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Shimada, C. A. Mason, and M. E. Morrison
TrkB Signaling Modulates Spine Density and Morphology Independent of Dendrite Structure in Cultured Neonatal Purkinje Cells
J. Neurosci.,
November 1, 1998;
18(21):
8559 - 8570.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Vicario-Abejon, C. Collin, R. D. G. McKay, and M. Segal
Neurotrophins Induce Formation of Functional Excitatory and Inhibitory Synapses between Cultured Hippocampal Neurons
J. Neurosci.,
September 15, 1998;
18(18):
7256 - 7271.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. L. Benson and H. Tanaka
N-Cadherin Redistribution during Synaptogenesis in Hippocampal Neurons
J. Neurosci.,
September 1, 1998;
18(17):
6892 - 6904.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S.-Y. Lin and M. Constantine-Paton
Suppression of Sprouting: An Early Function of NMDA Receptors in the Absence of AMPA/Kainate Receptor Activity
J. Neurosci.,
May 15, 1998;
18(10):
3725 - 3737.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. K. Hennig and D. A. Cotanche
Regeneration of Cochlear Efferent Nerve Terminals after Gentamycin Damage
J. Neurosci.,
May 1, 1998;
18(9):
3282 - 3296.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B Wolf, M. Seeger, and A Chiba
Commissureless endocytosis is correlated with initiation of neuromuscular synaptogenesis
Development,
January 10, 1998;
125(19):
3853 - 3863.
[Abstract]
[PDF]
|
|
|
|
|
|
|
R. M. FITZSIMONDS and M.-M. POO
Retrograde Signaling in the Development and Modification of Synapses
Physiol Rev,
January 1, 1998;
78(1):
143 - 170.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. E. West, R. L. Neve, and K. M. Buckley
Targeting of the Synaptic Vesicle Protein Synaptobrevin in the Axon of Cultured Hippocampal Neurons: Evidence for Two Distinct Sorting Steps
J. Cell Biol.,
November 17, 1997;
139(4):
917 - 927.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. M. Porter, O. Thibault, V. Thibault, K.-C. Chen, and P. W. Landfield
Calcium Channel Density and Hippocampal Cell Death with Age in Long-Term Culture
J. Neurosci.,
July 15, 1997;
17(14):
5629 - 5639.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Daly and E. B. Ziff
Post-Transcriptional Regulation of Synaptic Vesicle Protein Expression and the Developmental Control of Synaptic Vesicle Formation
J. Neurosci.,
April 1, 1997;
17(7):
2365 - 2375.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Tiedge and J. Brosius
Translational Machinery in Dendrites of Hippocampal Neurons in Culture
J. Neurosci.,
November 15, 1996;
16(22):
7171 - 7181.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. M. Craig, G. Banker, W. Chang, M. E. McGrath, and A. S. Serpinskaya
Clustering of Gephyrin at GABAergic but Not Glutamatergic Synapses in Cultured Rat Hippocampal Neurons
J. Neurosci.,
May 15, 1996;
16(10):
3166 - 3177.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Overly, H. Rieff, and P. Hollenbeck
Organelle motility and metabolism in axons vs dendrites of cultured hippocampal neurons
J. Cell Sci.,
January 5, 1996;
109(5):
971 - 980.
[Abstract]
[PDF]
|
|
|
|
|
|
|
S. K. Mistry, E. W. Keefer, B. A. Cunningham, G. M. Edelman, and K. L. Crossin
Cultured rat hippocampal neural progenitors generate spontaneously active neural networks
PNAS,
February 5, 2002;
99(3):
1621 - 1626.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. L. Scotti and H. Reuter
Synaptic and extrasynaptic gamma -aminobutyric acid type A receptor clusters in rat hippocampal cultures during development
PNAS,
March 13, 2001;
98(6):
3489 - 3494.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
