Stress suppresses and learning induces plasticity in CA3 of rat hippocampus: A three-dimensional ultrastructural study of thorny excrescences and their postsynaptic densities
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Chronic stress and spatial training have been proposed to affect hippocampal structure and function in opposite ways. Previous morphological studies that addressed structural changes after chronic restraint stress and spatial training were based on two-dimensional morphometry which does not allow a complete morphometric characterisation of synaptic features. Here, for the first time in such studies, we examined these issues by using three-dimensional (3-D) reconstructions of electron microscope images taken from thorny excrescences of hippocampal CA3 pyramidal cells. Ultrastructural alterations in postsynaptic densities (PSDs) of thorny excrescences receiving input from mossy fibre boutons were also determined, as were changes in numbers of multivesicular bodies (endosome-like structures) within thorny excrescences and dendrites. Quantitative 3-D data demonstrated retraction of thorny excrescences after chronic restraint stress which was reversed after water maze training, whilst water maze training alone increased thorny excrescence volume and number of thorns per thorny excrescence. PSD surface area was unaffected by restraint stress but water maze training increased both number and area of PSDs per thorny excrescence. In restrained rats that were water maze trained PSD volume and surface area increased significantly. The proportion of perforated PSDs almost doubled after water maze training and restraint stress. Numbers of endosome-like structures in thorny excrescences decreased after restraint stress and increased after water maze training. These findings demonstrate that circuits involving contacts between mossy fibre terminals and CA3 pyramidal cells at stratum lucidum level are affected conversely by water maze training and chronic stress, confirming the remarkable plasticity of CA3 dendrites. They provide a clear illustration of the structural modifications that occur after life experiences noted for their different impact on hippocampal function.
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PSD-95 is a reliable marker for mature synapses.
“The postsynaptic density 95 protein (PSD-95), which is localized primarily to dendritic spine heads, was used as a reliable marker for mature synapses.28, 29, 30”
From Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress (2014) · cites this paper as [30]
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Toscano-Silva, M., da Silva, S. G., Scorza, F. A., Bonvent, J. J., Cavalheiro, E. A., & Arida, R. M. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.05.012 · Cited by 27 · see citing works
Vulnerability of conditional NCAM-deficient mice to develop stress-induced behavioral alterations
Bisaz, R., & Sandi, C. (2012) · Stress · doi:10.3109/10253890.2011.608226 · Cited by 28 · see citing works
Self-citation
- Authors
- Stewart, M. G., Davies, H. A., Sandi, C., Kraev, I. V., Rogachevsky, V. V., Peddie, C. J., Rodriguez, J. J., Cordero, M. I., Donohue, H. S., Gabbott, P. L. A., & Popov, V. I.
- Affiliations
- The Open University (GB)
- École Polytechnique Fédérale de Lausanne (CH)
- Russian Academy of Sciences (RU)
- Corresponding author
- Stewart, M.G.
- ORCID
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2005
- Volume
- 131
- Issue
- 1
- Pages
- 43-54
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2129742671
- Cited by
- 197
- References
- 86
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 2 · 2022: 7 · 2021: 5 · 2020: 8 · 2019: 9 · 2018: 7 · 2017: 8 · 2016: 12 · 2015: 11 · 2014: 11 · 2013: 15 · 2012: 12
- FWCI
- 5.54
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Open Research Online - ORO (The Open University) (acceptedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Research Explorer (The University of Manchester) (submittedVersion)
- Funders
- Leverhulme Trust
- Russian Foundation for Basic Research
- Ministerio de Economía y Competitividad
- Biotechnology and Biological Sciences Research Council (NEU15416)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- chronic restraint stress, spatial learning, hippocampal CA3, postsynaptic density, mossy fiber synapses, dendritic plasticity, multivesicular bodies, three-dimensional ultrastructure, stratum lucidum
- MeSH terms
- Animals, Dendrites, Disease Models, Animal, Hippocampus, Reference Values, Restraint, Physical, Stress, Psychological, Synapses, Pyramidal Cells, Maze Learning, Rats
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