Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus
Open accessAbstract
The adult dentate gyrus produces new neurons that morphologically and functionally integrate into the hippocampal network. In the adult brain, most excitatory synapses are ensheathed by astrocytic perisynaptic processes that regulate synaptic structure and function. However, these processes are formed during embryonic or early postnatal development and it is unknown whether astrocytes can also ensheathe synapses of neurons born during adulthood and, if so, whether they play a role in their synaptic transmission. Here, we used a combination of serial-section immuno-electron microscopy, confocal microscopy, and electrophysiology to examine the formation of perisynaptic processes on adult-born neurons. We found that the afferent and efferent synapses of newborn neurons are ensheathed by astrocytic processes, irrespective of the age of the neurons or the size of their synapses. The quantification of gliogenesis and the distribution of astrocytic processes on synapses formed by adult-born neurons suggest that the majority of these processes are recruited from pre-existing astrocytes. Furthermore, the inhibition of astrocytic glutamate re-uptake significantly reduced postsynaptic currents and increased paired-pulse facilitation in adult-born neurons, suggesting that perisynaptic processes modulate synaptic transmission on these cells. Finally, some processes were found intercalated between newly formed dendritic spines and potential presynaptic partners, suggesting that they may also play a structural role in the connectivity of new spines. Together, these results indicate that pre-existing astrocytes remodel their processes to ensheathe synapses of adult-born neurons and participate to the functional and structural integration of these cells into the hippocampal network.
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Astrocytic processes ensheath synapses from adult-born neurons.
“Examination of afferent and efferent synapses of adult-born neurons has shown that astrocytic processes ensheath synapses from adult-born neurons (Krzisch et al., 2015)”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Krzisch et al., 2015
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- Authors
- Krzisch, M., Temprana, S. G., Mongiat, L. A., Armida, J., Schmutz, V., Virtanen, M. A., Kocher-Braissant, J., Kraftsik, R., Vutskits, L., Conzelmann, K.-K., Bergami, M., Gage, F. H., Schinder, A. F., & Toni, N.
- Affiliations
- University of Lausanne (CH)
- Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
- University of Geneva (CH)
- Max-von-Pettenkofer-Institut für Hygiene und Medizinische Mikrobiologie (DE)
- Cologne Excellence Cluster on Cellular Stress Responses in Aging Associated Diseases (DE)
- Salk Institute for Biological Studies (US)
- Corresponding author
- Toni, Nicolas
- ORCID
- Venue
- Brain Structure and Function
- Published
- 2014-04-19
- Volume
- 220
- Issue
- 4
- Pages
- 2027-2042
- ISSN
- 1863-2653 (ISSN-L)
- 1863-2661
- PMC
- PMC4481333
- OpenAlex
- W2010598641
- Cited by
- 57
- References
- 68
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 3 · 2023: 4 · 2022: 3 · 2021: 5 · 2020: 4 · 2019: 6 · 2018: 9 · 2017: 8 · 2016: 4 · 2015: 5 · 2014: 1
- FWCI
- 2.74
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Brain Structure and Function (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
- SERVAL (Université de Lausanne) (publishedVersion, other-oa)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion)
- reroDoc Digital Library (submittedVersion)
- IRIS (submittedVersion, other-oa)
- Americanae (AECID Library) (submittedVersion, cc-by-nc-sa)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Greater South Information System
- Funders
- National Science Foundation
- Howard Hughes Medical Institute
- James S. McDonnell Foundation
- Deutsche Forschungsgemeinschaft (SFB 870)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Consejo Nacional de Investigaciones Científicas y Técnicas
- Université de Lausanne
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (R01NS050217, NS050217)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- astrocytes, adult neurogenesis, dentate gyrus, hippocampus, gliogenesis, glutamate uptake, synaptic transmission, paired-pulse facilitation, dendritic spines, synaptic remodeling
- MeSH terms
- Aldehyde Dehydrogenase 1 Family, Animals, Astrocytes, Bromodeoxyuridine, Gene Expression Regulation, Glial Fibrillary Acidic Protein, Hippocampus, Isoenzymes, Kainic Acid, Mice, Inbred C57BL, Mice, Transgenic, Synaptic Transmission, Neurons, Phosphopyruvate Hydratase, Synapses, Microscopy, Immunoelectron, Patch-Clamp Techniques, Microscopy, Confocal, Excitatory Postsynaptic Potentials, Dendritic Spines, Green Fluorescent Proteins, Retinal Dehydrogenase, Mice, Neurogenesis, S100 Calcium Binding Protein beta Subunit
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