Adolescent nicotine exposure induces long-term, sex-specific disturbances in mood and anxiety-related behavioral, neuronal and molecular phenotypes in the mesocorticolimbic system
Open accessAbstract
The majority of lifetime smokers begin using nicotine during adolescence, a critical period of brain development wherein neural circuits critical for mood, affect and cognition are vulnerable to drug-related insults. Specifically, brain regions such as the medial prefrontal cortex (mPFC), the ventral tegmental area (VTA), nucleus accumbens (NAc) and hippocampus, are implicated in both nicotine dependence and pathological phenotypes linked to mood and anxiety disorders. Clinical studies report that females experience higher rates of mood/anxiety disorders and are more resistant to smoking cessation therapies, suggesting potential sex-specific responses to nicotine exposure and later-life neuropsychiatric risk. However, the potential neural and molecular mechanisms underlying such sex differences are not clear. In the present study, we compared the impacts of adolescent nicotine exposure in male vs. female rat cohorts. We performed a combination of behavioral, electrophysiological and targeted protein expression analyses along with matrix assisted laser deionization imaging (MALDI) immediately post-adolescent exposure and later in early adulthood. We report that adolescent nicotine exposure induced long-lasting anxiety/depressive-like behaviors, disrupted neuronal activity patterns in the mPFC-VTA network and molecular alterations in various neural regions linked to affect, anxiety and cognition. Remarkably, these phenotypes were only observed in males and/or were expressed in the opposite direction in females. These findings identify a series of novel, sex-selective biomarkers for adolescent nicotine-induced neuropsychiatric risk, persisting into adulthood.
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DA D1 receptors in the NAc shell are enduringly upregulated in female rats exposed to nicotine in adolescence.
“while, in contrast, D1Rs in the NAc shell were enduringly unregulated in female rats exposed to nicotine in adolescence [97, 98].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [98]
The sex-specific outcomes section reports significantly increased NAc D1R expression in females after adolescent nicotine exposure, and Fig. 4 describes this as a long-term effect. The paper identifies the measured region as the NAc, not specifically its shell; the shell-specific part of the claim is therefore unsupported. (LLM, conf=0.88)
Experimental — accuracy not yet measuredMid-adolescent nicotine exposure (PND 35-44) has sex-dependent effects on PFC function, increasing firing frequency of PFC pyramidal neurons and decreasing PFC D1R protein expression only in male rats.
“Nicotine exposure in mid-adolescence (PND 35–44) has been shown to have sex-dependent effects on PFC function, as it increased the firing frequency of PFC pyramidal neurons and decreased PFC D1R protein expression in only in male rats [96, 98].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [98]
The Adolescent nicotine exposure protocol section specifies PND 35–44, and the neuronal-activity results report increased mPFC pyramidal-neuron firing in nicotine-treated males, with no significant change in females. However, the Sex-specific alterations section locates the decreased D1R expression in the nucleus accumbens (striatum), not the PFC; it also reports increased nucleus accumbens D1R expression in females. Page numbers are unavailable in our copy. (LLM, conf=0.90)
Experimental — accuracy not yet measuredMid-adolescent nicotine exposure (PND 35-44) increases D2R expression in the PFC of male rats while decreasing D2R expression in the PFC of female rats.
“In contrast, this treatment increased D2R expression in the PFC of male rats, while decreasing D2R expression in the PFC of female rats [97, 98].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [98]
The adolescent nicotine exposure protocol identifies PND 35–44 as mid-adolescence. Figure 4 and the discussion of sex-specific molecular outcomes report increased D2R expression in males and decreased D2R expression in females, but locate those changes in the nucleus accumbens (NAc), not the PFC. Page numbers were not available in our copy. (LLM, conf=0.90)
Experimental — accuracy not yet measuredDA D1 receptors are downregulated in the NAc shell of adult male rats exposed to nicotine in mid-adolescence (PND 35-44).
“In the NAc, DA D1 receptors (D1Rs) were downregulated in the shell subregion of adult male rats that were exposed to nicotine in mid-adolescence (PND 35–44)”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [98]
The adolescent nicotine exposure protocol specifies PND 35–44 and testing after a washout until PND 75. Figure 4 and the discussion report reduced NAc D1R expression in nicotine-exposed males, but do not establish that the reduction occurred specifically in the shell subregion; the shell-specific measurements described elsewhere concern GABA, not D1R. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe consequences of adolescent exposure to this nicotine regimen were sex-specific, with nicotine-induced vulnerability to anxiety- or depression-like behavior specific to male rats.
“Notably, the consequences of adolescent exposure to this nicotine regimen were sex-specific, with nicotine-induced vulnerability to anxiety- or depression-like behavior specific to male rats [98].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [98]
Mid-adolescent nicotine treatment (PND 35-44) has sex-specific long-term effects on nAChR protein levels in the PFC: α7 and β2 protein are reduced in adult males (>P75) exposed to nicotine in adolescence, with no change in female rats exposed at the same age.
“Nicotine treatment in mid-adolescence (PND 35–44) had sex-specific long-term effects on nAChR protein levels in the PFC, with α7 and β2 protein reduced in adult males (>P75) exposed to nicotine in adolescence and no change the expression of these subunits in female rats exposed at the same age [98].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [98]
Basal DA neuron firing is increased in adult male rats following mid-adolescent nicotine exposure (PND 35-44).
“At the level of the VTA, basal DA neuron firing was increased in adult, male rats following exposure to nicotine in mid-adolescence (PND 35–44) [96, 98]”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [98]
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- Authors
- Ng, T. H. J., Sarikahya, M. H., Hudson, R., Szkudlarek, H. J., Pérez-Valenzuela, E., Uzuneser, T. C., Proud, E., Gummerson, D., Youssef, M., Machado, M., Zhaksylyk, K., DeVuono, M. V., Chen, C., Yeung, K. K.-C., Rushlow, W. J., & Laviolette, S. R.
- Affiliations
- Western University (CA)
- Corresponding author
- Laviolette, Steven R.
- ORCID
- Venue
- Neuropsychopharmacology
- Published
- 2024-03-23
- Volume
- 49
- Issue
- 7
- Pages
- 1171-1182
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC11109238
- OpenAlex
- W4393119619
- Cited by
- 23
- References
- 87
- Citations by year
- 2026: 12 · 2025: 8 · 2024: 3
- FWCI
- 6.55
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Gouvernement du Canada | Canadian Institutes of Health Research (PJT-189943)
- Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada
- Topics
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- adolescent nicotine exposure, sex differences, anxiety-like behavior, depression-like behavior, mesocorticolimbic system, medial prefrontal cortex, ventral tegmental area, nucleus accumbens, hippocampus, nicotine dependence, mood disorders, MALDI mass spectrometry imaging, neural activity patterns
- MeSH terms
- Animals, Anxiety, Female, Male, Neurons, Nicotine, Phenotype, Sex Characteristics, Rats, Sprague-Dawley, Prefrontal Cortex, Nicotinic Agonists, Rats
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