A critical period for nicotine-induced disruption of synaptic development in rat auditory cortex
Open accessAbstract
Cholinergic markers in the middle layers of rat auditory cortex are transiently upregulated during the second postnatal week, at which time alpha 7 nicotinic acetylcholine receptors (nAChRs) selectively regulate NMDA receptor (NMDAR)-mediated EPSPs. To investigate the developmental role of this regulation, we determined whether manipulating nAChR function at specific times during the first 4 weeks after birth could alter subsequent neuronal function. Rat pups were injected twice daily with nicotine (1 or 2 mg/kg) or saline during approximately the first, second, or fourth postnatal week (i. e., before, during, or after the peak upregulation of nAChRs). Glutamate EPSPs and intrinsic membrane properties were measured during whole-cell recordings from visually identified pyramidal neurons in layers II-IV of brain slices prepared at least 15 hr after the last injection. Chronic nicotine exposure (CNE) had little effect on intrinsic membrane properties and during week 1 or 4 did not affect synaptic function. However, CNE during week 2 resulted in EPSPs with long durations, multiple peaks, and enhanced NMDAR components. These changes remained significant even 10 d after CNE. Rapid application of nicotine, which in control neurons selectively enhances NMDAR EPSPs during week 2, produced only weak effects after CNE. Receptor binding studies showed that CNE-induced EPSP alterations occurred in the absence of altered alpha 7 nAChR numbers or agonist binding affinity. Thus, altered stimulation of nAChRs by CNE during week 2, but not before or after, disrupts the development of glutamate synapses in rat auditory cortex.
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Manipulation of these nAChRs with chronic nicotine exposure during the second, but not the first or fourth, postnatal weeks disrupts synaptic development in the auditory cortex by altering NMDA receptor-mediated synaptic signaling.
“Manipulation of these nAChRs with chronic nicotine exposure during the second, but not the first or fourth, postnatal weeks disrupts synaptic development in the auditory cortex by altering NMDA receptor-mediated synaptic signaling [96].”
From Nicotine on the developing brain. (2023) · cites this paper as [96]
Nicotine exposure in rats during the second postnatal week disrupted auditory cortex glutamate synapses, linked to long-term auditory processing and learning deficits.
“Exposure of rats to nicotine in the second postnatal week, corresponding to the third trimester of human fetal brain development,(147) disrupted the development of glutamate synapses in the auditory cortex, which has been associated with long-term deficits in auditory processing and learning.”
From Developmental toxicity of nicotine: A transdisciplinary synthesis and implications for emerging tobacco products (2017) · cites this paper as [71]
Animal research supports that nicotine harms auditory processing.
“Animal research supports that nicotine adversely affects auditory processing.”
From Developmental toxicity of nicotine: A transdisciplinary synthesis and implications for emerging tobacco products (2017) · cites this paper as [71]
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- Authors
- Aramakis, V. B., Hsieh, C. Y., Leslie, F. M., & Metherate, R.
- Affiliations
- University of California, Irvine (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2000-08-15
- Volume
- 20
- Issue
- 16
- Pages
- 6106-6116
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6772566
- OpenAlex
- W1785827736
- Cited by
- 120
- References
- 70
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 1 · 2023: 3 · 2022: 4 · 2020: 4 · 2019: 4 · 2017: 2 · 2016: 3 · 2015: 4 · 2014: 3 · 2013: 5 · 2012: 5
- FWCI
- 2.77
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Tobacco-Related Disease Research Program
- University of California, Irvine
- National Institute on Deafness and Other Communication Disorders (R29DC002967, DC 02967, R01DC002967)
- 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
- nicotine, alpha7 nicotinic acetylcholine receptor, auditory cortex, synaptic development, NMDA receptor, cholinergic markers, postnatal development, pyramidal neurons, intrinsic membrane properties, chronic nicotine exposure, receptor binding affinity
- MeSH terms
- Age Factors, Animals, Animals, Newborn, Auditory Cortex, Drug Administration Schedule, Female, Membrane Potentials, Microinjections, Synaptic Transmission, Neurons, Nicotine, Pregnancy, Prenatal Exposure Delayed Effects, Receptors, Nicotinic, Synapses, Receptors, N-Methyl-D-Aspartate, Rats, Sprague-Dawley, Excitatory Postsynaptic Potentials, Rats, alpha7 Nicotinic Acetylcholine Receptor
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