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Glutamate induces the rapid formation of spine head protrusions in hippocampal slice cultures

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Richards, David A., Mateos, José Maria, Hugel, Sylvain, de Paola, Vincenzo, Caroni, Pico, Gähwiler, Beat H., McKinney, R. Anne·2005·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.0501881102PMC PMC556130
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Abstract

Synaptic plasticity at neuronal connections has been well characterized functionally by using electrophysiological approaches, but the structural basis for this phenomenon remains controversial. We have studied the dynamic interactions between presynaptic and postsynaptic structures labeled with FM 4-64 and a membrane-targeted GFP, respectively, in hippocampal slices. Under conditions of reduced neuronal activity (1 μM tetrodotoxin), we observed extension of glutamate receptor-dependent processes from dendritic spines of CA1 pyramidal cells to presynaptic boutons. The formation of these spine head protrusions is blocked by α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA) receptor antagonists and by agents that reduce the release of glutamate from presynaptic terminals. Moreover, spine head protrusions form in response to exogenously applied glutamate, with clear directionality toward the glutamate electrode. Our results suggest that spontaneously released glutamate is sufficient to activate nearby spines, which can then lead to the growth of new postsynaptic processes connecting to a presynaptic site. Spines thus can compare their recent history with that of neighboring synapses and modify local connectivity accordingly.

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  • These observations confirm that spine head filopodia induction might trigger spine switching and potentially the replacement of inefficient with more efficient synapses.

    “These observations confirm that spine head filopodia induction might trigger spine switching and potentially the replacement of inefficient with more efficient synapses41,42,53.”

    From Microglia remodel synapses by presynaptic trogocytosis and spine head filopodia induction (2018) · cites this paper as [41]

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Authors
Richards, D. A., Mateos, J. M., Hugel, S., de Paola, V., Caroni, P., Gähwiler, B. H., & McKinney, R. A.
Affiliations
  • University of Zurich (CH)
  • Brain Research Institute, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland; and Friedrich Miescher Institute, Novartis Research Foundation, Maulbeerstrasse 66, CH-4058 Basel, Switzerland
  • University of Bern (CH)
Corresponding author
Gähwiler, Beat H.
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2005-04-14
Volume
102
Issue
17
Pages
6166-6171
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.0501881102
PMC
PMC556130
OpenAlex
W2122092731
Cited by
161
References
29
Citations by year
2026: 3 · 2025: 4 · 2024: 7 · 2023: 6 · 2022: 4 · 2021: 11 · 2020: 5 · 2019: 5 · 2018: 6 · 2017: 8 · 2016: 5 · 2015: 4 · 2014: 15 · 2013: 12 · 2012: 6
FWCI
3.51
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
Funders
  • National Science Foundation
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (61518)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Keywords
dendritic spines, glutamate, synaptic plasticity, hippocampus, CA1 pyramidal neurons, presynaptic terminals, glutamate receptors, AMPA receptor antagonists, tetrodotoxin, glutamate release, spine morphogenesis, synaptic connectivity
MeSH terms
Animals, Dendrites, Hippocampus, Image Processing, Computer-Assisted, Kinetics, Organ Culture Techniques, Quinoxalines, Tetrodotoxin, N-Methylaspartate, Pyramidal Cells, Glutamic Acid, Mice

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