Perinatal Caffeine, Acting on Maternal Adenosine A1 Receptors, Causes Long-Lasting Behavioral Changes in Mouse Offspring
Open accessAbstract
BACKGROUND: There are lingering concerns about caffeine consumption during pregnancy or the early postnatal period, partly because there may be long-lasting behavioral changes after caffeine exposure early in life. METHODOLOGY/PRINCIPAL FINDINGS: We show that pregnant wild type (WT) mice given modest doses of caffeine (0.3 g/l in drinking water) gave birth to offspring that as adults exhibited increased locomotor activity in an open field. The offspring also responded to cocaine challenge with greater locomotor activity than mice not perinatally exposed to caffeine. We performed the same behavioral experiments on mice heterozygous for adenosine A(1) receptor gene (A(1)RHz). In these mice signaling via adenosine A(1) receptors is reduced to about the same degree as after modest consumption of caffeine. A(1)RHz mice had a behavioral profile similar to WT mice perinatally exposed to caffeine. Furthermore, it appeared that the mother's genotype, not offspring's, was critical for behavioral changes in adult offspring. Thus, if the mother partially lacked A(1) receptors the offspring displayed more hyperactivity and responded more strongly to cocaine stimulation as adults than did mice of a WT mother, regardless of their genotype. This indicates that long-term behavioral alterations in the offspring result from the maternal effect of caffeine, and not a direct effect on fetus. WT offspring from WT mother but having a A(1)R Hz grandmother preserved higher locomotor response to cocaine. CONCLUSIONS/SIGNIFICANCE: We suggest that perinatal caffeine, by acting on adenosine A(1) receptors in the mother, causes long-lasting behavioral changes in the offspring that even manifest themselves in the second generation.
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Caffeine consumption by the dam (the human equivalent of two to three cups of coffee per day) was associated with caffeine concentrations in the offspring brain that were similar to those in the umbilical cords of women drinking two to three cups of coffee per day.
“Caffeine consumption by the dam (the human equivalent of two to three cups of coffee per day) was associated with caffeine concentrations in the offspring brain that were similar to those in the umbilical cords of women drinking two to three cups of coffee per day (138).”
From The Safety of Ingested Caffeine: A Comprehensive Review (2017) · cites this paper as [138]
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- Authors
- Björklund, O., Kahlström, J., Salmi, P., & Fredholm, B. B.
- Affiliations
- Karolinska Institutet (SE)
- Corresponding author
- Björklund, Olga
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2008-12-18
- Volume
- 3
- Issue
- 12
- Pages
- e3977
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2597749
- OpenAlex
- W1999541069
- Cited by
- 37
- References
- 49
- Citations by year
- 2025: 1 · 2024: 3 · 2023: 4 · 2022: 2 · 2021: 1 · 2020: 2 · 2019: 1 · 2017: 4 · 2016: 2 · 2015: 1 · 2014: 3 · 2013: 1
- FWCI
- 3.61
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- European Commission
- Karolinska Institutet
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (R01NS048995)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Health Sciences › Medicine › Pharmacology › Coffee research and impacts
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Adenosine and Purinergic Signaling
- Keywords
- adenosine A1 receptor, maternal caffeine consumption, cocaine sensitivity, locomotor activity, maternal effects, prenatal drug exposure
- MeSH terms
- Algorithms, Animals, Animals, Newborn, Behavior, Animal, Caffeine, Cocaine, Female, Genotype, Heterozygote, Male, Mice, Inbred C57BL, Mothers, Pregnancy, Prenatal Exposure Delayed Effects, Mice, Knockout, Gene Expression Regulation, Developmental, Receptor, Adenosine A1, Receptor, Adenosine A2A, 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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