Late prenatal immune activation causes hippocampal deficits in the absence of persistent inflammation across aging
Open accessAbstract
BACKGROUND: Prenatal exposure to infection and/or inflammation is increasingly recognized to play an important role in neurodevelopmental brain disorders. It has recently been postulated that prenatal immune activation, especially when occurring during late gestational stages, may also induce pathological brain aging via sustained effects on systemic and central inflammation. Here, we tested this hypothesis using an established mouse model of exposure to viral-like immune activation in late pregnancy. METHODS: Pregnant C57BL6/J mice on gestation day 17 were treated with the viral mimetic polyriboinosinic-polyribocytidilic acid (poly(I:C)) or control vehicle solution. The resulting offspring were first tested using cognitive and behavioral paradigms known to be sensitive to hippocampal damage, after which they were assigned to quantitative analyses of inflammatory cytokines, microglia density and morphology, astrocyte density, presynaptic markers, and neurotrophin expression in the hippocampus throughout aging (1, 5, and 22 months of age). RESULTS: Maternal poly(I:C) treatment led to a robust increase in inflammatory cytokine levels in late gestation but did not cause persistent systemic or hippocampal inflammation in the offspring. The late prenatal manipulation also failed to cause long-term changes in microglia density, morphology, or activation, and did not induce signs of astrogliosis in pubescent, adult, or aged offspring. Despite the lack of persistent inflammatory or glial anomalies, offspring of poly(I:C)-exposed mothers showed marked and partly age-dependent deficits in hippocampus-regulated cognitive functions as well as impaired hippocampal synaptophysin and brain-derived neurotrophic factor (BDNF) expression. CONCLUSIONS: Late prenatal exposure to viral-like immune activation in mice causes hippocampus-related cognitive and synaptic deficits in the absence of chronic inflammation across aging. These findings do not support the hypothesis that this form of prenatal immune activation may induce pathological brain aging via sustained effects on systemic and central inflammation. We further conclude that poly(I:C)-based prenatal immune activation models are reliable in their effectiveness to induce (hippocampal) neuropathology across aging, but they appear unsuited for studying the role of chronic systemic or central inflammation in brain aging.
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Prenatal poly(I:C) exposure impaired spatial recognition memory in the Y maze.
“spatial recognition memory in the Y maze (Giovanoli et al., 2015)”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Giovanoli et al., 2015
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Maternal immune activation: Implications for neuropsychiatric disorders
Estes, M. L., & McAllister, A. K. (2016) · Science · doi:10.1126/science.aag3194 · Cited by 1,206 · see citing works
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Cross talk: the microbiota and neurodevelopmental disorders
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Maternal immune activation in neurodevelopmental disorders
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Richetto, J., Massart, R., Weber-Stadlbauer, U., Szyf, M., Riva, M. A., & Meyer, U. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.08.010 · Cited by 148 · see citing works
Self-citationEnvironment matters: microglia function and dysfunction in a changing world
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Goldstein, J. M., Cohen, J. E., Mareckova, K., Holsen, L., Whitfield-Gabrieli, S., Gilman, S. E., Buka, S. L., & Hornig, M. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2014464118 · Cited by 70 · see citing works
- Authors
- Giovanoli, S., Notter, T., Richetto, J., Labouesse, M. A., Vuillermot, S., Riva, M. A., & Meyer, U.
- Affiliations
- ETH Zurich (CH)
- University of Zurich (CH)
- University of Milan (IT)
- Corresponding author
- Meyer, Urs
- Venue
- Journal of Neuroinflammation
- Published
- 2015-11-25
- Volume
- 12
- Issue
- 1
- Pages
- 221-221
- ISSN
- 1742-2094 (ISSN-L)
- PMC
- PMC4659211
- OpenAlex
- W2174739469
- Cited by
- 124
- References
- 104
- Citations by year
- 2026: 8 · 2025: 7 · 2024: 8 · 2023: 8 · 2022: 12 · 2021: 20 · 2020: 16 · 2019: 11 · 2018: 16 · 2017: 6 · 2016: 12
- FWCI
- 6.05
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Journal of Neuroinflammation (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by)
- ETH Zürich Research Collection (cc-by)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- National Science Foundation (259679)
- European Commission (FP7/2007-2011, FP7/2007, 259679)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (146217, FP7/2007-2011)
- Fondazione Cariplo (2012-0503)
- Ministero dell'Università e della Ricerca
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- prenatal immune activation, late pregnancy, hippocampus, brain aging, poly(I:C), maternal infection, neuroinflammation, microglia, astrocytes, synaptophysin, brain-derived neurotrophic factor, cognitive impairment, synaptic dysfunction, neurodevelopmental disorders, mouse model
- MeSH terms
- Aging, Animals, Female, Hippocampus, Inflammation, Male, Mice, Inbred C57BL, Pregnancy, Prenatal Exposure Delayed Effects, Inflammation Mediators, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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