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The Journal of Neuroscience, November 1, 1998, 18(21):8900-8911
Synaptogenesis Via Dendritic Filopodia in Developing Hippocampal
Area CA1
John C.
Fiala1,
Marcia
Feinberg1,
Viktor
Popov2, and
Kristen M.
Harris1
1 Division of Neuroscience in the Department of
Neurology, Children's Hospital, Boston Massachusetts, and
2 Institute of Cell Biophysics, Russian Academy of
Sciences, Pushchino, Moscow Region, 142292, Russia
To determine the role of dendritic filopodia in the genesis of
excitatory synaptic contacts and dendritic spines in hippocampal area
CA1, serial section electron microscopy and three-dimensional analysis
of 16 volumes of neuropil from nine male rat pups, aged postnatal day 1 (P1) through P12, were performed. The analysis revealed that
numerous dendritic filopodia formed asymmetric synaptic contacts with
axons and with filopodia extending from axons, especially during the
first postnatal week. At P1, 22 ± 5.5% of synapses occurred on
dendritic filopodia, with 19 ± 5.9% on filopodia at P4, 20 ± 8.0% at P6, decreasing to 7.2 ± 4.7% at P12
(p < 0.02). Synapses were found at the base
and along the entire length of filopodia, with many filopodia
exhibiting multiple synaptic contacts. In all, 162 completely traceable
dendritic filopodia received 255 asymmetric synaptic contacts. These
synapses were found at all parts of filopodia with equal frequency,
usually occurring on fusiform swellings of the diameter. Most synaptic
contacts (53 ± 11%) occurred directly on dendritic shafts during
the first postnatal week. A smaller but still substantial portion
(32 ± 12%) of synapses were on shafts at P12
(p < 0.036). There was a highly significant
(p < 0.0002) increase in the proportion of dendritic spine synapses with age, rising from just 4.9 ± 4.3% at P1 to 37 ± 14% at P12. The concurrence of primarily shaft and filopodial synapses in the first postnatal week suggests that filopodia
recruit shaft synapses that later give rise to spines through a process
of outgrowth.
Key words:
serial electron microscopy; postsynaptic density; synapse; rat; pyramidal cell; dendrites; spines; three-dimensional
reconstructions
Copyright © 1998 Society for Neuroscience 0270-6474/98/18218900-12$05.00/0
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L. Groc, B. Gustafsson, and E. Hanse
Spontaneous Unitary Synaptic Activity in CA1 Pyramidal Neurons during Early Postnatal Development: Constant Contribution of AMPA and NMDA Receptors
J. Neurosci.,
July 1, 2002;
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[Abstract]
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P. Jourdain, I. Nikonenko, S. Alberi, and D. Muller
Remodeling of Hippocampal Synaptic Networks by a Brief Anoxia-Hypoglycemia
J. Neurosci.,
April 15, 2002;
22(8):
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[Abstract]
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Y. Sara, M. G. Mozhayeva, X. Liu, and E. T. Kavalali
Fast Vesicle Recycling Supports Neurotransmission during Sustained Stimulation at Hippocampal Synapses
J. Neurosci.,
March 1, 2002;
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[Abstract]
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C.-S. Uhm, B. Neuhuber, B. Lowe, V. Crocker, and M. P. Daniels
Synapse-Forming Axons and Recombinant Agrin Induce Microprocess Formation on Myotubes
J. Neurosci.,
December 15, 2001;
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[Abstract]
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R. Khazipov, M. Esclapez, O. Caillard, C. Bernard, I. Khalilov, R. Tyzio, J. Hirsch, V. Dzhala, B. Berger, and Y. Ben-Ari
Early Development of Neuronal Activity in the Primate Hippocampus In Utero
J. Neurosci.,
December 15, 2001;
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[Abstract]
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O. Prange and T. H. Murphy
Modular Transport of Postsynaptic Density-95 Clusters and Association with Stable Spine Precursors during Early Development of Cortical Neurons
J. Neurosci.,
December 1, 2001;
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[Abstract]
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S. Okabe, A. Miwa, and H. Okado
Spine Formation and Correlated Assembly of Presynaptic and Postsynaptic Molecules
J. Neurosci.,
August 15, 2001;
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[Abstract]
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E. Korkotian and M. Segal
Regulation of Dendritic Spine Motility in Cultured Hippocampal Neurons
J. Neurosci.,
August 15, 2001;
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[Abstract]
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N. Toni, P.-A. Buchs, I. Nikonenko, P. Povilaitite, L. Parisi, and D. Muller
Remodeling of Synaptic Membranes after Induction of Long-Term Potentiation
J. Neurosci.,
August 15, 2001;
21(16):
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[Abstract]
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E. A. Nimchinsky, A. M. Oberlander, and K. Svoboda
Abnormal Development of Dendritic Spines in FMR1 Knock-Out Mice
J. Neurosci.,
July 15, 2001;
21(14):
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W. Zhang and D. L. Benson
Stages of Synapse Development Defined by Dependence on F-Actin
J. Neurosci.,
July 15, 2001;
21(14):
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S. Kaech, H. Parmar, M. Roelandse, C. Bornmann, and A. Matus
Cytoskeletal microdifferentiation: A mechanism for organizing morphological plasticity in dendrites
PNAS,
June 19, 2001;
98(13):
7086 - 7092.
[Abstract]
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E. Hanse and B. Gustafsson
Quantal variability at glutamatergic synapses in area CA1 of the rat neonatal hippocampus
J. Physiol.,
March 1, 2001;
531(2):
467 - 480.
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E. Hanse and B. Gustafsson
Vesicle release probability and pre-primed pool at glutamatergic synapses in area CA1 of the rat neonatal hippocampus
J. Physiol.,
March 1, 2001;
531(2):
481 - 493.
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M. Goldin, M. Segal, and E. Avignone
Functional Plasticity Triggers Formation and Pruning of Dendritic Spines in Cultured Hippocampal Networks
J. Neurosci.,
January 1, 2001;
21(1):
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[Abstract]
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B. E. Chen, B. Lendvai, E. A. Nimchinsky, B. Burbach, K. Fox, and K. Svoboda
Imaging High-Resolution Structure of GFP-Expressing Neurons in Neocortex In Vivo
Learn. Mem.,
November 1, 2000;
7(6):
433 - 441.
[Abstract]
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A. Matus
Actin-Based Plasticity in Dendritic Spines
Science,
October 27, 2000;
290(5492):
754 - 758.
[Abstract]
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M. Frotscher, A. Drakew, and B. Heimrich
Role of Afferent Innervation and Neuronal Activity in Dendritic Development and Spine Maturation of Fascia Dentata Granule Cells
Cereb Cortex,
October 1, 2000;
10(10):
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[Abstract]
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A. K. McAllister
Cellular and Molecular Mechanisms of Dendrite Growth
Cereb Cortex,
October 1, 2000;
10(10):
963 - 973.
[Abstract]
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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;
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[Abstract]
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W. T. Wong, B. E. Faulkner-Jones, J. R. Sanes, and R. O. L. Wong
Rapid Dendritic Remodeling in the Developing Retina: Dependence on Neurotransmission and Reciprocal Regulation by Rac and Rho
J. Neurosci.,
July 1, 2000;
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[Abstract]
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M. J. Hasbani, S. M. Underhill, G. De Erausquin, and M. P. Goldberg
Synapse Loss and Regeneration: A Mechanism for Functional Decline and Recovery after Cerebral Ischemia?
Neuroscientist,
April 1, 2000;
6(2):
110 - 119.
[Abstract]
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N. Sans, R. S. Petralia, Y.-X. Wang, J. Blahos II, J. W. Hell, and R. J. Wenthold
A Developmental Change in NMDA Receptor-Associated Proteins at Hippocampal Synapses
J. Neurosci.,
February 1, 2000;
20(3):
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A. Dunaevsky, A. Tashiro, A. Majewska, C. Mason, and R. Yuste
Developmental regulation of spine motility in the mammalian central nervous system
PNAS,
November 9, 1999;
96(23):
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[Abstract]
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E. T. Kavalali, J. Klingauf, and R. W. Tsien
Activity-dependent regulation of synaptic clustering in a hippocampal culture system
PNAS,
October 26, 1999;
96(22):
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P.C. Bridgman
Myosin VA Movements in Normal and Dilute-Lethal Axons Provide Support for a Dual Filament Motor Complex
J. Cell Biol.,
September 6, 1999;
146(5):
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[Abstract]
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S. A. Kirov, K. E. Sorra, and K. M. Harris
Slices Have More Synapses than Perfusion-Fixed Hippocampus from both Young and Mature Rats
J. Neurosci.,
April 15, 1999;
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M. Maletic-Savatic, R. Malinow, and K. Svoboda
Rapid Dendritic Morphogenesis in CA1 Hippocampal Dendrites Induced by Synaptic Activity
Science,
March 19, 1999;
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[Abstract]
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T. Krucker, G. R. Siggins, and S. Halpain
Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus
PNAS,
June 6, 2000;
97(12):
6856 - 6861.
[Abstract]
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