Prenatal nicotine is associated with reduced AMPA and NMDA receptor-mediated rises in calcium within the laterodorsal tegmentum: a pontine nucleus involved in addiction processes

McNair, L. F.; Kohlmeier, K. A.

doi:10.1017/s2040174414000439

Cited by 22Neuroscience and Neuropharmacology ResearchPrenatal Substance Exposure EffectsNicotinic Acetylcholine Receptors Study

Prenatal nicotine is associated with reduced AMPA and NMDA receptor-mediated rises in calcium within the laterodorsal tegmentum: a pontine nucleus involved in addiction processes

McNair, L. F., Kohlmeier, K. A.·2015·Journal of Developmental Origins of Health and Disease

DOI 10.1017/s2040174414000439

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Abstract

Despite huge efforts from public sectors to educate society as to the deleterious physiological consequences of smoking while pregnant, 12-25% of all babies worldwide are born to mothers who smoked during their pregnancies. Chief among the negative legacies bestowed to the exposed individual is an enhanced proclivity postnatally to addict to drugs of abuse, which suggests that the drug exposure during gestation changed the developing brain in such a way that biased it towards addiction. Glutamate signalling has been shown to be altered by prenatal nicotine exposure (PNE) and glutamate is the major excitatory neurotransmitter within the laterodorsal tegmental nucleus (LDT), which is a brainstem region importantly involved in responding to motivational stimuli and critical in development of drug addiction-associated behaviours, however, it is unknown whether PNE alters glutamate signalling within this nucleus. Accordingly, we used calcium imaging, to evaluate AMPA and NMDA receptor-mediated calcium responses in LDT brain slices from control and PNE mice. We also investigated whether the positive AMPA receptor modulator cyclothiazide (CYZ) had differential actions on calcium in the LDT following PNE. Our data indicated that PNE significantly decreased AMPA receptor-mediated calcium responses, and altered the neuronal calcium response to consecutive NMDA applications within the LDT. Furthermore, CYZ strongly potentiated AMPA-induced responses, however, this action was significantly reduced in the LDT of PNE mice when compared with enhancements in responses in control LDT cells. Immunohistochemical processing confirmed that calcium imaging recordings were obtained from the LDT nucleus as determined by presence of cholinergic neurons. Our results contribute to the body of evidence suggesting that neurobiological changes are induced if gestation is accompanied by nicotine exposure. We conclude that in light of the role played by the LDT in motivated behaviour, the cellular changes in the LDT induced by exposures to nicotine prenatally, when combined with alterations in other reward-related regions, could contribute to the increased susceptibility to smoking observed in the offspring.

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Electrophysiological analysis of in vitro brain slices has shown that oral nicotine (300 μg/ml) exposure throughout gestation reduces nicotine-induced intracellular calcium and AMPA-mediated glutamate responses in LDTg neurons.
“Electrophysiological analysis of in vitro brain slices has shown that oral nicotine (300 μg/ml) exposure throughout gestation reduces nicotine-induced intracellular calcium and AMPA-mediated glutamate responses in LDTg neurons [44,45].”
From Nicotine on the developing brain. (2023) · cites this paper as [45]

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Nicotine on the developing brain.
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“, DR2, DAT, and DR1) signaling plasticity in the hippocampus [44, 45], the laterodorsal tegmental nucleus [46], and theNAc [47–49].”
Background
Teratogenic effects of maternal drug abuse on developing brain and underlying neurotransmitter mechanisms
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“This investigation was conducted because the larger postsynaptic responses of the AMPARs in the PNE were inconsistent with our earlier speculation that smaller amplitude calcium rises elicited by AMPA seen in the PNE were due to functional changes of the postsynaptic AMPARs leading to reduced membrane responses (McNai…”
Influential
Alterations in NMDAR-mediated signaling within the laterodorsal tegmental nucleus are associated with prenatal nicotine exposure
Polli, F. S., & Kohlmeier, K. A. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107744 · Cited by 15 · see citing works
Calcium rises induced by AMPA and nicotine receptors in the ventral tegmental area show differences in mouse brain slices prenatally exposed to nicotine
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Sex‐specific alterations in GABA receptor‐mediated responses in laterodorsal tegmentum are associated with prenatal exposure to nicotine
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Neuropeptide S (NPS) is a neuropeptide with cellular actions in arousal and anxiety-related nuclei: Functional implications for effects of NPS on wakefulness and mood
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“The loading time was increased by 1 min for every day of age greater than postnatal day 10, that we and others (MacLean and Yuste, 2009; McNair and Kohlmeier, 2015) have shown enhances loading quality, which generally reduces as the postnatal age of the tissue increases.”
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“Indeed, we have previously shown that the outcome of glutamate excitation is altered in an animal model of prenatal drug exposure (McNair and Kohlmeier 2015).”
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“In a research report in this issue, one possible neural mechanism that may alter reward assignment in the brain of an individual prenatally exposed to nicotine is examined.(6) In this study, reductions in the responsitivity of glutamate receptors in a motivationregulating brain nucleus were detected in mice exposed to…”
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Prenatal Nicotine Exposure and Impact on the Behaviors of Offspring
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Alterations in NMDAR-mediated signaling within the laterodorsal tegmental nucleus are associated with prenatal nicotine exposure
Polli, F. S., & Kohlmeier, K. A. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107744 · Cited by 15 · see citing works
Prenatal nicotine exposure alters postsynaptic AMPA receptors and glutamate neurotransmission within the laterodorsal tegmentum (LDT) of juvenile mice
Polli, F. S., & Kohlmeier, K. A. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.04.024 · Cited by 16 · see citing works
Electrophysiological changes in laterodorsal tegmental neurons associated with prenatal nicotine exposure: Implications for heightened susceptibility to addict to drugs of abuse
Christensen, M. H., Nielsen, M. L., & Kohlmeier, K. A. (2015) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s204017441400049x · Cited by 17 · see citing works
Sex‐specific alterations in GABA receptor‐mediated responses in laterodorsal tegmentum are associated with prenatal exposure to nicotine
Eliasen, J. N., Krall, J., Frølund, B., & Kohlmeier, K. A. (2020) · Developmental Neurobiology · doi:10.1002/dneu.22772 · Cited by 9 · see citing works
Prenatal exposure to nicotine in mice is associated with alterations in development and cellular and synaptic effects of alcohol in a brainstem arousal nucleus
Nunes‐Freitas, A. L., Soni, N., Polli, F. S., & Kohlmeier, K. A. (2021) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2021.106980 · Cited by 1 · see citing works

Authors: McNair, L. F., & Kohlmeier, K. A.
Affiliations: University of Copenhagen (DK)
Corresponding author: Kohlmeier, K. A.
ORCID: McNair, L. F.
Kohlmeier, K. A.
Venue: Journal of Developmental Origins of Health and Disease
Publisher: Cambridge University Press (CUP)
Published: 2014-11-03
Volume: 6
Issue: 3
Pages: 225-241
ISSN: 2040-1744 (ISSN-L)
2040-1752
DOI: 10.1017/s2040174414000439
OpenAlex: W2326541765
Cited by: 22
References: 100
Citations by year: 2026: 2 · 2024: 1 · 2023: 2 · 2022: 2 · 2021: 4 · 2020: 2 · 2019: 3 · 2018: 3 · 2017: 1 · 2016: 1 · 2015: 1
FWCI: 0.46
Type: journal article
Language: en
Open access: closed
Licence: www.cambridge.org/core/terms (unspecified)
Locations: Journal of Developmental Origins of Health and Disease (publishedVersion)
PubMed (publishedVersion)
Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
Keywords: prenatal nicotine exposure, laterodorsal tegmental nucleus, AMPA receptors, NMDA receptor, glutamate signalling, calcium imaging, cyclothiazide, cholinergic neurons, maternal smoking, brain development, motivated behavior
MeSH terms: Animals, Calcium, Female, Humans, Motivation, Nicotine, Pregnancy, Prenatal Exposure Delayed Effects, Tegmentum Mesencephali, Signal Transduction, Receptors, N-Methyl-D-Aspartate, N-Methylaspartate, Receptors, AMPA, alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid, Glutamic Acid, Substance-Related Disorders, Mice

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Prenatal nicotine is associated with reduced AMPA and NMDA receptor-mediated rises in calcium within the laterodorsal tegmentum: a pontine nucleus involved in addiction processes

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