Role of central amygdala neuronal ensembles in incubation of nicotine craving
Open accessAbstract
UNLABELLED: The craving response to smoking-associated cues in humans or to intravenous nicotine-associated cues in adult rats progressively increases or incubates after withdrawal. Here, we further characterized incubation of nicotine craving in the rat model by determining whether this incubation is observed after adolescent-onset nicotine self-administration. We also used the neuronal activity marker Fos and the Daun02 chemogenetic inactivation procedure to identify cue-activated neuronal ensembles that mediate incubation of nicotine craving. We trained adolescent and adult male rats to self-administer nicotine (2 h/d for 12 d) and assessed cue-induced nicotine seeking in extinction tests (1 h) after 1, 7, 14, or 28 withdrawal days. In both adult and adolescent rats, nicotine seeking in the relapse tests followed an inverted U-shaped curve, with maximal responding on withdrawal day 14. Independent of the withdrawal day, nicotine seeking in the relapse tests was higher in adult than in adolescent rats. Analysis of Fos expression in different brain areas of adolescent and adult rats on withdrawal days 1 and 14 showed time-dependent increases in the number of Fos-positive neurons in central and basolateral amygdala, orbitofrontal cortex, ventral and dorsal medial prefrontal cortex, and nucleus accumbens core and shell. In adult Fos-lacZ transgenic rats, selective inactivation of nicotine-cue-activated Fos neurons in central amygdala, but not orbitofrontal cortex, decreased "incubated" nicotine seeking on withdrawal day 14. Our results demonstrate that incubation of nicotine craving occurs after adolescent-onset nicotine self-administration and that neuronal ensembles in central amygdala play a critical role in this incubation. SIGNIFICANCE STATEMENT: The craving response to smoking-associated cues in humans or to intravenous nicotine-associated cues in adult rats progressively increases or incubates after withdrawal. It is currently unknown whether incubation of craving also occurs after adolescent-onset nicotine self-administration. The brain areas that mediate such incubation are also unknown. Here, we used a rat model of incubation of drug craving, the neuronal activity marker Fos, and the Daun02 chemogenetic inactivation method to demonstrate that incubation of nicotine craving is also observed after adolescent-onset nicotine self-administration and that neuronal ensembles in the central nucleus of the amygdala play a critical role in this incubation in adult rats.
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In Funk et al. (2016), FosB expression in the dorsal mPFC on day 1 and 14 after nicotine was increased in adults versus adolescents and age-matched controls.
“FosB in the dorsal mPFC- Day 1 and 14 after nicotine: Adults ↑ vs adolescents and age-matched controls.”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al. (2016)
The Fos expression section (page unavailable) reports somewhat higher dorsal mPFC Fos expression in adult than adolescent rats on withdrawal days 1 and 14 after nicotine self-administration. It measures Fos, not FosB, and does not establish the claimed increase over age-matched controls; its separate basal-Fos groups showed no age difference and were not directly compared with the extinction-test groups. (LLM, conf=0.90)
Experimental — accuracy not yet measuredIn Funk et al. (2016), active lever presses were increased in adults versus adolescents and age-matched controls.
“Active lever presses: Adults ↑ vs adolescents and age-matched controls.”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al. (2016)
The ‘Incubation of nicotine craving’ section reports more active-lever presses by adult than adolescent rats during extinction tests. It does not report a comparison with age-matched controls; the ‘Nicotine self-administration training’ section also reports no age difference during training. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn Funk et al. (2016), FosB expression in ventral mPFC, OFC, NAc core and shell, CeA and BLA showed no age differences and no effect of nicotine.
“FosB in ventral mPFC, OFC, NAc core and shell, CeA and BLA: No age differences. No effect of nicotine.”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al. (2016)
The Fos expression section reports no age effect in the listed regions for rats tested after nicotine withdrawal; the reported age effect was confined to dorsal mPFC. But the paper measured Fos, not FosB, and its comparison of withdrawal days does not establish that nicotine had no effect. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIn rats, cue-induced drug-seeking behaviour increased with longer withdrawal duration in both adolescent- and adult-exposed groups.
“Both age groups showed cue-induced drug- seeking behaviour that increased with longer withdrawal duration.”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al., 2016
The “Incubation of nicotine craving” results report time-dependent cue-induced responding in both adolescent and adult rats, peaking on withdrawal day 14. The claim omits the subsequent decline: responding followed an inverted U-shaped curve, rather than increasing throughout the longer withdrawal periods. Page numbers are not provided in our copy. (LLM, conf=0.87)
Experimental — accuracy not yet measuredWithdrawal-induced craving is higher when nicotine exposure occurs during adulthood than during adolescence.
“This suggests withdrawal-induced craving is higher when exposed to nicotine during adulthood.”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al., 2016
The ‘Incubation of nicotine craving’ results report more active-lever presses after withdrawal in adult than adolescent rats, regardless of withdrawal day. The claim omits that this was cue-induced nicotine seeking measured in rats; the study also found no age-by-withdrawal-day interaction, so it does not establish a greater increase in craving over withdrawal in adults. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Age-related differences were present in the dorsal mPFC with adult-exposed rats showing elevated fosB expression, compared to adolescent-exposed rats and relative to age-matched controls.
“Age-related differences were present in the dorsal mPFC with adult-exposed rats showing elevated fosB expression, compared to adolescent-exposed rats and relative to age-matched con trols (Funk et al., 2016).”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al., 2016
The Fos expression section reports somewhat higher Fos expression in the dorsal mPFC of adult than adolescent rats after extinction tests. It measures Fos, not fosB, and says the no-test groups were not directly compared with the extinction-test groups; it therefore does not establish elevated expression relative to age-matched controls. No page number is provided in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measuredElevated deltafos-B expression in the NAc is associated with incubated nicotine seeking in both adolescent and adult exposed rats.
“Elevated deltafos-B expression in the NAc has also been associated with incubated nicotine seeking in both adolescent and adult exposed rats (Funk et al., 2016)”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al., 2016
The Fos expression section (page unavailable) reports higher Fos expression in the NAc core and shell on withdrawal day 14 than day 1, without an age-by-withdrawal-day interaction. The experiment section identifies day 14 as the period of maximal incubated nicotine seeking in both adolescent and adult rats. The paper measures Fos, not deltaFosB, so it does not support the claim about that specific marker. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe increase in cue-induced drug-seeking behaviour with longer withdrawal was more pronounced in adult-exposed rats than in adolescent-exposed rats.
“This effect was more pronounced in adult-exposed rats compared to adolescent-exposed rats.”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al., 2016
The central nucleus of the amygdala has a causal role in the incubation of nicotine craving in adult rats.
“This suggests a causal role of the central nucleus of the amygdala in the incubation of nicotine craving in adult rats.”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al., 2016
Experimental — accuracy not yet measuredOn withdrawal day 14, incubated nicotine seeking was associated with increased neuronal activity in the amygdala, NAc, mPFC and OFC across both age groups.
“Interestingly, within the same study, incubated nicotine seeking on withdrawal day 14 was associated with increased neuronal activity in the amygdala, NAc, mPFC and OFC across both age groups.”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al., 2016
Inactivation of nicotine-cue-activated Fos-expressing neurons in the central nucleus of the amygdala decreased incubation of nicotine seeking in adult-exposed rats.
“Moreover, inactivation of nicotine-cue-activated Fos-expressing neurons in the central nucleus of the amygdala resulted in decreased incubation of nicotine seeking in adult-exposed rats.”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al., 2016
Twelve days of self-administration did not result in age-related differences in the NAc core or shell, and no differences were found in the ventral mPFC, OFC, and central and basolateral amygdala of male rats when tested both one and 14 days after the last day of access to nicotine.
“In contrast, 12 days of self-administration did not result in age-related differences in the NAc core or shell, and no differences were found in the ventral mPFC, OFC, and central and basolateral amygdala of male rats when tested both one and 14 days after the last day of access to nicotine (Funk et al., 2016).”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al., 2016
In the one study to investigate craving in rats, withdrawal-induced craving was higher in adults.
“In addition, in the one study to investigate craving in rats, withdrawal-induced craving was higher in adults (Funk et al., 2016).”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al., 2016
Nicotine exposure increased c-fos expression in the amygdala in both age groups, whilst no effects of nicotine were found on fosB expression in both age groups.
“Nicotine exposure increased c-fos expression in the amyg dala in both age groups (Dao et al., 2011; Cao et al., 2007), whilst no effects of nicotine were found on fosB expression in both age groups (Funk et al., 2016).”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Funk et al., 2016
The cited Funk et al. citation is attached to the claim that nicotine had no effect on FosB expression in either age group. The Fos expression and Experiment 1 sections examine Fos in adolescent and adult rats, but the passages found when searching for FosB and ΔFosB do not address FosB expression or a nicotine effect on it. The reported absence of changes in basal Fos after withdrawal does not establish the claimed result for FosB. (LLM, conf=0.76)
Experimental — accuracy not yet measured
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Research works printed but not linked: 1
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- Authors
- Funk, D., Coen, K., Tamadon, S., Hope, B. T., Shaham, Y., & Lê, A. D.
- Affiliations
- Centre for Addiction and Mental Health (CA)
- National Institutes of Health (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2016-08-17
- Volume
- 36
- Issue
- 33
- Pages
- 8612-8623
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4987435
- OpenAlex
- W2510803292
- Semantic Scholar
- a5a425fc437aff4735f7167456368dc59e28605e
- Cited by
- 87
- References
- 78
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 6 · 2023: 12 · 2022: 8 · 2021: 5 · 2020: 8 · 2019: 7 · 2018: 14 · 2017: 15 · 2016: 3
- FWCI
- 10.47
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute on Drug Abuse (R21DA034394)
- 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
- nicotine craving, incubation of craving, central amygdala, neuronal ensembles, nicotine self-administration, adolescent nicotine exposure, nicotine withdrawal, Fos expression, chemogenetic inactivation, nicotine seeking, relapse
- MeSH terms
- Age Factors, Animals, Animals, Newborn, beta-Galactosidase, Daunorubicin, Extinction, Psychological, Female, Neurons, Nicotine, Phosphopyruvate Hydratase, Self Administration, Substance Withdrawal Syndrome, Sucrose, Time Factors, Oncogene Proteins v-fos, Rats, Sprague-Dawley, Nicotinic Agonists, Rats, Rats, Transgenic, Craving, Central Amygdaloid Nucleus
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.
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