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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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E. Korkotian and M. Segal
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N. Toni, P.-A. Buchs, I. Nikonenko, P. Povilaitite, L. Parisi, and D. Muller
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E. A. Nimchinsky, A. M. Oberlander, and K. Svoboda
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W. Zhang and D. L. Benson
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E. Hanse and B. Gustafsson
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J. Physiol., March 1, 2001; 531(2): 467 - 480.
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E. Hanse and B. Gustafsson
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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): 186 - 193.
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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
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Actin-Based Plasticity in Dendritic Spines
Science, October 27, 2000; 290(5492): 754 - 758.
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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): 946 - 951.
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A. K. McAllister
Cellular and Molecular Mechanisms of Dendrite Growth
Cereb Cortex, October 1, 2000; 10(10): 963 - 973.
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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
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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; 20(13): 5024 - 5036.
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NeuroscientistHome page
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.
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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
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Developmental regulation of spine motility in the mammalian central nervous system
PNAS, November 9, 1999; 96(23): 13438 - 13443.
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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): 12893 - 12900.
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P.C. Bridgman
Myosin VA Movements in Normal and Dilute-Lethal Axons Provide Support for a Dual Filament Motor Complex
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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
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M. Maletic-Savatic, R. Malinow, and K. Svoboda
Rapid Dendritic Morphogenesis in CA1 Hippocampal Dendrites Induced by Synaptic Activity
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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
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