Prenatal immune activation leads to multiple changes in basal neurotransmitter levels in the adult brain: implications for brain disorders of neurodevelopmental origin such as schizophrenia
Open accessAbstract
Maternal infection during pregnancy enhances the offspring's risk for severe neuropsychiatric disorders in later life, including schizophrenia. Recent attempts to model this association in animals provided further experimental evidence for a causal relationship between in-utero immune challenge and the postnatal emergence of a wide spectrum of behavioural, pharmacological and neuroanatomical dysfunctions implicated in schizophrenia. However, it still remains unknown whether the prenatal infection-induced changes in brain and behavioural functions may be associated with multiple changes at the neurochemical level. Here, we tested this hypothesis in a recently established mouse model of viral-like infection. Pregnant dams on gestation day 9 were exposed to viral mimetic polyriboinosinic-polyribocytidilic acid (PolyI:C, 5 mg/kg i.v.) or vehicle treatment, and basal neurotransmitter levels were then compared in the adult brains of animals born to PolyI:C- or vehicle-treated mothers by high-performance liquid chromatography on post-mortem tissue. We found that prenatal immune activation significantly increased the levels of dopamine and its major metabolites in the lateral globus pallidus and prefrontal cortex, whilst at the same time it decreased serotonin and its metabolite in the hippocampus, nucleus accumbens and lateral globus pallidus. In addition, a specific reduction of the inhibitory amino acid taurine in the hippocampus was noted in prenatally PolyI:C-exposed offspring relative to controls, whereas central glutamate and gamma-aminobutyric acid (GABA) content was largely unaffected by prenatal immune activation. Our results thus confirm that maternal immunological stimulation during early/middle pregnancy is sufficient to induce long-term changes in multiple neurotransmitter levels in the brains of adult offspring. This further supports the possibility that infection-mediated interference with early fetal brain development may predispose the developing organism to the emergence of neurochemical imbalances in adulthood, which may be critically involved in the precipitation of adult behavioural and pharmacological abnormalities after prenatal immune challenge.
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In murine models, LPS and poly(I:C) exposure decreased 5-HT levels in hippocampus.
“In murine models, exposure to LPS (Depino, 2015) and poly(I:C) (Winter et al., 2009) decreased 5-HT levels in the hippocampus.”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Winter et al., 2009
Prenatal poly(I:C) exposure reduced 5-HT and 5-HIAA levels in nucleus accumbens and lateral globus pallidus.
“The levels of 5-HT and its metabolite 5-hydroxyindoleacetic acid (5-HIAA) were reduced in the nucleus accumbens and lateral globus pallidus by prenatal poly(I:C) exposure (Winter et al., 2009)”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Winter et al., 2009
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- Authors
- Winter, C., Djodari-Irani, A., Sohr, R., Morgenstern, R., Feldon, J., Juckel, G., & Meyer, U.
- Affiliations
- ETH Zurich (CH)
- Ruhr University Bochum (DE)
- Corresponding author
- Juckel, Georg
- Venue
- The International Journal of Neuropsychopharmacology
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-08-28
- Volume
- 12
- Issue
- 04
- Pages
- 513
- ISSN
- 1461-1457 (ISSN-L)
- 1469-5111
- OpenAlex
- W1984715501
- Cited by
- 242
- References
- 76
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 11 · 2023: 13 · 2022: 16 · 2021: 13 · 2020: 14 · 2019: 13 · 2018: 9 · 2017: 5 · 2016: 23 · 2015: 18 · 2014: 19 · 2013: 16 · 2012: 23
- FWCI
- 4.23
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The International Journal of Neuropsychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Eidgenössische Technische Hochschule Zürich
- Topics
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- prenatal immune activation, maternal infection, schizophrenia, neurodevelopmental disorders, neurotransmitter levels, dopamine, serotonin, taurine, glutamate, GABA, poly(I:C), globus pallidus, prefrontal cortex, hippocampus, nucleus accumbens
- MeSH terms
- Animals, Brain Chemistry, Brain Diseases, Chromatography, High Pressure Liquid, Dopamine, Female, gamma-Aminobutyric Acid, Homovanillic Acid, Hydroxyindoleacetic Acid, Immunity, Interferon Inducers, Male, Mice, Inbred C57BL, Poly I-C, Pregnancy, Prenatal Exposure Delayed Effects, Schizophrenia, Serotonin, Taurine, 3,4-Dihydroxyphenylacetic Acid, Neurotransmitter Agents, Glutamic Acid, 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.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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