Early postnatal nicotine exposure causes hippocampus-dependent memory impairments in adolescent mice: association with altered nicotinic cholinergic modulation of LTP, but not impaired LTP
Open accessAbstract
Fetal nicotine exposure from smoking during pregnancy causes long-lasting cognitive impairments in offspring, yet little is known about the mechanisms that underlie this effect. Here we demonstrate that early postnatal exposure of mouse pups to nicotine via maternal milk impairs long-term, but not short-term, hippocampus-dependent memory during adolescence. At the Schaffer collateral (SC) pathway, the most widely studied synapses for a cellular correlate of hippocampus-dependent memory, the induction of N-methyl-D-aspartate receptor-dependent transient long-term potentiation (LTP) and protein synthesis-dependent long-lasting LTP are not diminished by nicotine exposure, but rather unexpectedly the threshold for LTP induction becomes lower after nicotine treatment. Using voltage sensitive dye to visualize hippocampal activity, we found that early postnatal nicotine exposure also results in enhanced CA1 depolarization and hyperpolarization after SC stimulation. Furthermore, we show that postnatal nicotine exposure induces pervasive changes to the nicotinic modulation of CA1 activity: activation of nicotinic receptors no longer increases CA1 network depolarization, acute nicotine inhibits rather than facilitates the induction of LTP at the SC pathway by recruiting an additional nicotinic receptor subtype, and acute nicotine no longer blocks LTP induction at the temporoammonic pathway. These findings reflect the pervasive impact of nicotine exposure during hippocampal development, and demonstrate an association of hippocampal memory impairments with altered nicotinic cholinergic modulation of LTP, but not impaired LTP. The implication of our results is that nicotinic cholinergic-dependent plasticity is required for long-term memory formation and that postnatal nicotine exposure disrupts this form of plasticity.
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Mouse pups exposed to nicotine during the first two postnatal weeks also show substantial impairment of long-term hippocampal dependent spatial memory during adolescence.
“Mouse pups exposed to nicotine during the first two postnatal weeks also show substantial impairment of long-term hippocampal dependent spatial memory during adolescence [85].”
From Nicotine on the developing brain. (2023) · cites this paper as [85]
Cognitive deficits from prenatal nicotine exposure reflect effects on nAChR modulation of long-term potentiation in the hippocampus.
“Research suggests that these deficits reflect effects on nAChR modulation of long-term potentiation in the hippocampus.”
From Developmental toxicity of nicotine: A transdisciplinary synthesis and implications for emerging tobacco products (2017) · cites this paper as [187]
Animal studies of prenatal nicotine exposure and cognitive development are more consistent, suggesting global learning and memory impairments.
“there is greater consistency among animal studies examining the effects of prenatal nicotine exposure on cognitive development, suggestive of global impairments in learning and memory.”
From Developmental toxicity of nicotine: A transdisciplinary synthesis and implications for emerging tobacco products (2017) · cites this paper as [187]
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Nicotine Exposure During Gestation: From Placental Dysfunction to Long‐Term Neurobehavioral Outcomes
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- Authors
- Nakauchi, S., Malvaez, M., Su, H., Kleeman, E., Dang, R., Wood, M. A., & Sumikawa, K.
- Affiliations
- University of California, Irvine (US)
- Venue
- Neurobiology of Learning and Memory
- Publisher
- Elsevier BV
- Published
- 2015-02
- Volume
- 118
- Pages
- 178-188
- ISSN
- 1074-7427 (ISSN-L)
- PMC
- PMC4331249
- OpenAlex
- W2020826705
- Cited by
- 27
- References
- 64
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 3 · 2023: 2 · 2022: 1 · 2021: 2 · 2020: 1 · 2019: 2 · 2018: 2 · 2017: 4 · 2016: 6 · 2015: 1
- FWCI
- 1.50
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Neurobiology of Learning and Memory (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- NIDA (DA025269, DA025676, and DA026458)
- NIMH and NIDA (MH101491, DA036984, and DA031989)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Keywords
- prenatal nicotine exposure, maternal smoking, hippocampal-dependent memory, long-term potentiation, nicotinic acetylcholine receptors, cholinergic modulation, Schaffer collateral pathway, temporoammonic pathway, adolescent mice, hippocampal development, memory impairment
- MeSH terms
- Age Factors, Animals, Anxiety, Female, Hippocampus, Male, Memory Disorders, Mice, Inbred C57BL, Neurons, Nicotine, Long-Term Potentiation, Nicotinic Agonists, Nicotinic Antagonists, Recognition, Psychology, Mice, Spatial Memory
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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