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Cited by 51Neuroscience and Neuropharmacology ResearchNicotinic Acetylcholine Receptors StudySmoking Behavior and Cessation

Nicotine exposure during adolescence leads to short-and long-term changes in spike timing-dependent plasticity in rat prefrontal cortex

Open access
Goriounova, N. A., Mansvelder, H. D.·2012·Journal of Neuroscience
DOI 10.1523/jneurosci.5502-11.2012PMC PMC3552309
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Abstract

Adolescence is a critical period of brain development during which maturation of areas involved in cognitive functioning, such as the medial prefrontal cortex (mPFC), is still ongoing. Tobacco smoking during this age can compromise the normal course of prefrontal development and lead to cognitive impairments in later life. Recently, we reported that nicotine exposure during adolescence results in a short-term increase and lasting reduction in synaptic mGluR2 levels in the rat mPFC, causing attention deficits during adulthood. It is unknown how changed synaptic mGluR2 levels after adolescent nicotine exposure affect the ability of mPFC synapses to undergo long-term synaptic plasticity. Here, we addressed this question. To model nicotine exposure, adolescent (P34-P43) or adult (P60-P69) rats were treated with nicotine injections three times per day for 10 d. We found that, both during acute activation of nicotinic receptors in the adolescent mPFC as well as immediately following nicotine treatment during adolescence, long-term plasticity in response to timed presynaptic and postsynaptic activity (tLTP) was strongly reduced. In contrast, in the mPFC of adult rats 5 weeks after they received nicotine treatment during adolescence, but not during adulthood, tLTP was increased. Short- and long-term adaptation of mPFC synaptic plasticity after adolescent nicotine exposure could be explained by changed mGluR2 signaling. Blocking mGluR2s augmented tLTP, whereas activating mGluR2s reduced tLTP. Our findings suggest neuronal mechanisms by which exposure to nicotine during adolescence alters the rules for spike timing-dependent plasticity in prefrontal networks that may explain the observed deficits in cognitive performance in later life.

AI snapshot

Written from the paper’s full text.

TL;DR

Adolescent nicotine exposure in rats acutely and shortly after treatment reduces spike timing-dependent long-term potentiation (tLTP) in medial prefrontal cortex, but 5 weeks later it increases tLTP. These bidirectional changes are linked to altered mGluR2 signaling, and adult nicotine exposure does not produce the lasting STDP change.

Key findings

  • Acute nicotine (10 μM) abolished tLTP in adolescent mPFC: control cells showed 130 ± 15% EPSP slope change, while nicotine-treated cells showed no significant tLTP (t(11)=2.51, p=0.028); 3 of 6 cells instead showed tLTD.
  • One to four days after adolescent nicotine treatment, the stronger five-action-potential burst protocol produced tLTD in 10 of 13 cells, whereas saline-treated rats showed tLTP (t(23)=2.49, p=0.02).
  • Five weeks after adolescent nicotine exposure, adult rats showed increased tLTP: single-action-potential pairing gave 163 ± 10% in nicotine-treated vs 121 ± 9% in saline-treated rats (t(44)=2.94, p=0.005), and five-action-potential bursts gave 150 ± 12% vs 104 ± 7% (t(19)=3.35, p=0.003). Nicotine exposure during adulthood did not alter tLTP.
  • mGluR2 manipulation bidirectionally affected tLTP: in nicotine-treated rats shortly after adolescent exposure, MPPG increased the proportion of cells showing tLTP to all cells vs 2 of 13 without MPPG (χ²₂=9.22, p=0.01); in adult saline-treated rats, MPPG increased tLTP to levels comparable with adolescent-nicotine-treated adults (t(34)=2.072, p=0.046); in adult nicotine-treated rats, LY379268 abolished tLTP (t(29)=4.19, p=0.0002).

Methods

  • Male Wistar rats were injected subcutaneously with nicotine (0.4 mg/kg) or saline three times daily for 10 days during adolescence (P34–P43) or adulthood (P60–P69); electrophysiology was performed 1–4 days or 5 weeks after treatment.
  • Whole-cell patch-clamp recordings were made from layer V pyramidal cells in prelimbic mPFC; EPSPs were evoked by extracellular stimulation and paired with single postsynaptic action potentials or bursts of five action potentials at 100 Hz, 50 times at 0.1 Hz, with a 5 ms pre-before-post interval.
  • Synaptic gain was measured as percentage change in initial EPSP slope 35–45 min after pairing; pharmacology included nicotine, LY379268, MPPG, and gabazine for EPSC experiments; statistics used t tests and χ² tests. In total, 47 saline-treated, 40 nicotine-treated, and 7 untreated control rats were killed.

Limitations

  • The paper does not include a dedicated limitations section. Evident limitations include use of only male Wistar rats and in vitro mPFC slices, which may not fully capture in vivo network conditions.
  • STDP recordings were performed without blockers of GABAergic synaptic transmission, so inhibitory network contributions cannot be excluded from the plasticity effects.
  • The mGluR2 mechanism is inferred from pharmacology and prior work; direct mGluR2 levels were not measured in these STDP experiments, and the average slope change with MPPG shortly after adolescent nicotine was not significantly different from no MPPG (t(16)=1.65, p=0.12) despite a higher proportion of cells showing tLTP.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1523/jneurosci.5502-11.2012

Cites

53 of 53 references verified0 citation errors · 0 not checkable

Statistics

5 tests recomputed · 0 with the reported and recomputed p on opposite sides of .05

Claims the paper makes

0 of 35 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    In adult rats 5 weeks after nicotine treatment during adolescence, tLTP is increased in mPFC.

    “in the mPFC of adult rats 5 weeks after they received nicotine treatment during adolescence, but not during adulthood, tLTP was increased.”
    • Also stated in: § STDP is enhanced in adult rats exposed to nicotine during adolescence · plain
      “Also here tLTP was increased in adult rats treated with nicotine during adolescence with respect to saline-treated rats (Fig. 3f,g; nicotine, 150 ± 12%; saline, 104 ± 7%; t(19)=3.35, p=0.003).”
    Quote in the paperSubstantial claim
  • Findingown data

    Acute activation of nicotinic receptors in the adolescent mPFC reduces tLTP.

    “both during acute activation of nicotinic receptors in the adolescent mPFC as well as immediately following nicotine treatment during adolescence, long-term plasticity in response to timed presynaptic and postsynaptic activity (tLTP) was strongly reduced.”
    • Also stated in: § Acute nicotine reduces tLTP in adolescent PFC · plain
      “Thus, consistent with the results in juvenile mice (Couey et al., 2007), acute nicotine in adolescent mPFC reduces the ability of excitatory synapses to undergo tLTP.”
    Quote in the paperSubstantial claim
  • Findingown data

    In adult rats treated with nicotine during adolescence, single AP pairing led to higher potentiation than in saline-treated controls (nicotine 163 ± 10% vs saline 121 ± 9%).

    “Surprisingly, in nicotine-treated rats the same pairing protocol led to substantially higher potentiation compared with saline-treated controls (increase in EPSP slope in nicotine, 163 ± 10%; saline, 121 ± 9%, t(44)=2.94, p=0.005; Fig. 3c,d).”
    Quote in the paperSubstantial claim
  • Findingown data

    mGluR2 agonist LY379268 decreases EPSC amplitude in mPFC glutamatergic synapses.

    “When mGluR2 receptors were activated by bath application of mGluR2 agonist LY379268, EPSC amplitude significantly decreased.”
    Quote in the paperSubstantial claim
  • Findingown data

    In adult rats treated with nicotine during adolescence, the stronger five-AP burst protocol also increased tLTP compared with saline-treated rats (nicotine 150 ± 12% vs saline 104 ± 7%).

    “Also here tLTP was increased in adult rats treated with nicotine during adolescence with respect to saline-treated rats (Fig. 3f,g; nicotine, 150 ± 12%; saline, 104 ± 7%; t(19)=3.35, p=0.003).”
    Quote in the paperSubstantial claim
  • May combine two claims. 15
  • Classified as probably not a substantial claim. 7

  • May combine two claims.

    Findingown data

    In the nicotine-treated control group without MPPG, only 2 of 13 cells showed tLTP, 10 of 13 cells showed tLTD, and 1 cell showed no change.

    “in which only 2 of 13 cells showed tLTP; 10 of 13 cells showed tLTD, and 1 cell showed no change”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Nicotine exposure during adolescence results in a short-term increase and lasting reduction in synaptic mGluR2 levels in the rat mPFC.

    “Recently, we reported that nicotine exposure during adolescence results in a short-term increase and lasting reduction in synaptic mGluR2 levels in the rat mPFC, causing attention deficits during adulthood.”
    • Also stated in: § Introduction · plain
      “These molecular adaptations involve a short-term upregulation, followed by a long-term downregulation of the inhibitory metabotropic glutamate receptor 2 (mGluR2) (Counotte et al., 2011).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Counotte et al., 2011

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Tobacco smoking during adolescence can compromise normal prefrontal development and lead to cognitive impairments in later life.

    “Tobacco smoking during this age can compromise the normal course of prefrontal development and lead to cognitive impairments in later life.”
    • Also stated in: § Introduction · plain
      “This early exposure of prefrontal brain areas to nicotine can compromise normal development and have long-lasting consequences for cognitive performance.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Jacobsen et al., 2005, 2007

      Not checked in the free run.

    • cites Musso et al., 2007

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In juvenile mouse PFC, acute nicotine application increases the threshold for synaptic spike timing-dependent potentiation due to increased inhibitory transmission to pyramidal neurons.

    “In the juvenile mouse PFC, acute nicotine application increases the threshold for synaptic spike timing-dependent potentiation due to increased inhibitory transmission to pyramidal neurons (Couey et al., 2007).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Couey et al., 2007

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    STDP is thought to play an important role in cortical development and underlie some forms of learning.

    “The ability of synapses to change their strength in response to timed presynaptic and postsynaptic activity called spike timing-dependent plasticity (STDP) is thought to play an important role in cortical development and underlie some forms of learning (Feldman et al., 1999; Feldman and Brecht, 2005; Letzkus et al., 2007).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Feldman et al., 1999

      Not checked in the free run.

    • cites Feldman and Brecht, 2005

      Not checked in the free run.

    • cites Letzkus et al., 2007

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Nicotine treatment during adolescence has lasting effects on the mechanisms of STDP and leads to augmented tLTP in adult rats.

    “Thus, nicotine treatment during adolescence has lasting effects on the mechanisms of STDP and leads to augmented tLTP in adult rats.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    Nicotine exposure during adolescence alters the rules for spike timing-dependent plasticity in prefrontal networks, which may explain observed deficits in cognitive performance in later life.

    “Our findings suggest neuronal mechanisms by which exposure to nicotine during adolescence alters the rules for spike timing-dependent plasticity in prefrontal networks that may explain the observed deficits in cognitive performance in later life.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The rat model of adolescent nicotine exposure (P34–P43, 0.4 mg/kg three times daily for 10 d) adequately models human adolescent tobacco smoking.
    • Rests on an assumption: The effects of nicotine on STDP in rat mPFC are relevant to human cognitive performance in later life.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The acute effects of nicotine on cognition may be explained by the action of nicotine on excitatory synapses in the PFC.

    “The acute effects of nicotine on cognition may be explained by the action of nicotine on excitatory synapses in the PFC (Counotte et al., 2011).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Counotte et al., 2011

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    A lasting reduction in mGluR2 signaling after nicotine exposure can result in increased LTP and potentially to a less efficient ability to filter information, thereby hampering cognitive performance.

    “A lasting reduction in mGluR2 signaling after nicotine exposure can result in increased LTP and therefore potentially to a less efficient ability to filter information, thereby hampering cognitive performance.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The STDP observed in mPFC slices reflects synaptic plasticity as it occurs in the intact PFC in vivo.

  • May combine two claims.

    Premisecitation

    Adolescence is a period when PFC networks are still actively developing, which may underlie the fact that nicotine exposure at this age results in lasting changes at the cellular and behavioral level.

    “Adolescence is a period when PFC networks are still actively developing, which may underlie the fact that nicotine exposure at this age results in lasting changes at the cellular as well as at the behavioral level (Counotte et al., 2011).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Counotte et al., 2011

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In adolescents, chronic smoking is associated with disturbances in working memory and attention as well as reduced PFC activation.

    “In adolescents, chronic smoking is associated with disturbances in working memory and attention as well as reduced PFC activation (Jacobsen et al., 2005, 2007; Musso et al., 2007).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Jacobsen et al., 2005, 2007

      Not checked in the free run.

    • cites Musso et al., 2007

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Both increased long-term potentiation and reduced short-term plasticity contribute to reduced signal-to-noise ratio.

    “Therefore, both increased long-term potentiation and reduced short-term plasticity contribute to reduced signal-to-noise ratio.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The STDP observed in mPFC slices reflects synaptic plasticity as it occurs in the intact PFC in vivo.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    mGluR2 receptors modulate excitatory transmission by inhibiting glutamate release and are implicated in plasticity.

    “Metabotropic GluR2 receptors modulate excitatory transmission by inhibiting glutamate release and were also implicated in plasticity (Yokoi et al., 1996; Nicholls et al., 2006; Bellone et al., 2008).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Yokoi et al., 1996

      Not checked in the free run.

    • cites Nicholls et al., 2006

      Not checked in the free run.

    • cites Bellone et al., 2008

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    In juvenile mice, acute nicotine application can change the rules for plasticity at excitatory synapses and thereby affect prefrontal network development and function.

    “In juvenile mice, acute nicotine application can change the rules for plasticity at excitatory synapses (Mansvelder and McGehee, 2000; Couey et al., 2007) and thereby affect prefrontal network development and function.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Mansvelder and McGehee, 2000

      Not checked in the free run.

    • cites Couey et al., 2007

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Presynaptic terminals of mPFC glutamatergic synapses are rich in mGluR2 receptors, which are activated by glutamate spillover and inhibit further glutamate release.

    “Presynaptic terminals of mPFC glutamatergic synapses are rich in mGluR2 receptors, which are activated by glutamate spillover and inhibit further glutamate release (Mateo and Porter, 2007).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Mateo and Porter, 2007

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    mGluR2 signaling can bidirectionally influence tLTP: reducing mGluR2-dependent inhibition leads to increased tLTP, while enhancing mGluR2 activation blocks LTP.

    “These findings show that mGluR2 signaling can bidirectionally influence tLTP: reducing mGluR2-dependent inhibition leads to increased tLTP, while enhancing mGluR2 activation blocked LTP.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: LY379268 and MPPG act specifically on mGluR2 receptors without off-target effects.

  • May combine two claims.

    Premisecitation

    Nicotine exposure during adolescence leads to an initial increase in mGluR2 protein levels in mPFC synaptic membranes on the first day of withdrawal and a lasting decrease in mGluR2 levels in adult rats 5 weeks after exposure.

    “Nicotine exposure during adolescence leads to an initial increase in protein levels of this receptor in mPFC synaptic membranes on the first day of withdrawal and is followed by a lasting decrease in mGluR2 levels in adult rats 5 weeks after nicotine exposure during adolescence (Counotte et al., 2011).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Counotte et al., 2011

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Restoring mGluR2 activity in vivo by intra-PFC infusion of mGluR2 agonist in adult rats that received nicotine as adolescents rescues attention disturbances.

    “Restoring mGluR2 activity in vivo by intra-PFC infusion of mGluR2 agonist in adult rats that received nicotine as adolescents rescues attention disturbances (Counotte et al., 2011).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Counotte et al., 2011

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    70% of adolescents report experimenting with smoking cigarettes.

    “Indeed, 70% of adolescents report experimenting with smoking cigarettes (Escobedo et al., 1993; Currie et al., 2008).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Escobedo et al., 1993

      Not checked in the free run.

    • cites Currie et al., 2008

      Not checked in the free run.

19 of 19

  • The paper relies on this without support.

    The rat model of adolescent nicotine exposure (P34–P43, 0.4 mg/kg three times daily for 10 d) adequately models human adolescent tobacco smoking.

    “To model nicotine exposure, adolescent (P34–P43) or adult (P60–P69) rats were treated with nicotine injections three times per day for 10 d.”

  • The paper relies on this without support.

    It is unknown how changed synaptic mGluR2 levels after adolescent nicotine exposure affect the ability of mPFC synapses to undergo long-term synaptic plasticity.

    “It is unknown how changed synaptic mGluR2 levels after adolescent nicotine exposure affect the ability of mPFC synapses to undergo long-term synaptic plasticity.”

  • The paper relies on this without support.

    The effects of nicotine on STDP in rat mPFC are relevant to human cognitive performance in later life.

    “Our findings suggest neuronal mechanisms by which exposure to nicotine during adolescence alters the rules for spike timing-dependent plasticity in prefrontal networks that may explain the observed deficits in cognitive performance in later life.”

  • The paper relies on this without support.

    The STDP observed in mPFC slices reflects synaptic plasticity as it occurs in the intact PFC in vivo.

    “Thus, repeated exposure to nicotine during adolescence may thereby affect the way the prefrontal circuitry matures and lead to changes in the prefrontal network that may last for a lifetime.”

  • The paper relies on this without support.

    LY379268 and MPPG act specifically on mGluR2 receptors without off-target effects.

    “Enhancing mGluR2 activity with LY379268 abolished tLTP in saline-treated rats”
    “Blocking mGluR2 receptors with MPPG resulted in increased tLTP comparable with levels observed in adult rats treated with nicotine during adolescence”
5 of 5

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Changes in mGluR2 expression are thought to mediate changes in pre and postsynaptic activity in mPFC.

    “These changes in mGluR2 expression are also thought to mediate changes in pre and postsynaptic activity in the mPFC [206].”

    From Consequences of adolescent drug use (2023) · cites this paper as [206]

    The Results section (‘Reduced mGluR2 signaling underlies short- and long-term changes in STDP’; page unavailable) links altered mGluR2 levels in rat mPFC to changes in synaptic plasticity. It also describes presynaptic inhibition of glutamate release, but does not show that mGluR2 expression changes postsynaptic activity specifically; the study pairs presynaptic stimulation with postsynaptic action potentials to measure plasticity. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

  • Mid-adolescent nicotine exposure (PND 34-43) enduringly alters PFC long-term potentiation into adulthood, marked by an increased ability of prefrontal synapses to undergo spike-timing-dependent LTP.

    “This exposure pattern also enduringly altered PFC long term potentiation (LTP) into adulthood, marked by an increased ability of prefrontal synapses to undergo spike-timing-dependent LTP [147].”

    From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [147]

  • The electrophysiological and behavioral alterations from mid-adolescent nicotine exposure are associated with transient changes in nAChR expression and enduring changes in mGluR2 signaling.

    “These electrophysiological and behavioral alterations were associated with transient changes in nAChR expression [57], and enduring changes in mGluR2 signaling [147, 148].”

    From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [147]

  • These cognitive disturbances are associated with reduced presynaptic mGluR2 protein and function on excitatory synapses in the prefrontal cortex.

    “These cognitive disturbances are associated with reduced presynaptic mGluR2 protein and function on excitatory synapses in the prefrontal cortex, which alters the rules for spike timing-dependent plasticity in prefrontal networks (Counotte et al. 2011; Goriounova & Mansvelder, 2012).”

    From <scp>N</scp> icotine and the adolescent brain (2015) · cites this paper as Goriounova & Mansvelder, 2012

  • Reduced presynaptic mGluR2 protein and function alters the rules for spike timing-dependent plasticity in prefrontal networks.

    “These cognitive disturbances are associated with reduced presynaptic mGluR2 protein and function on excitatory synapses in the prefrontal cortex, which alters the rules for spike timing-dependent plasticity in prefrontal networks (Counotte et al. 2011; Goriounova & Mansvelder, 2012).”

    From <scp>N</scp> icotine and the adolescent brain (2015) · cites this paper as Goriounova & Mansvelder, 2012

Statistics that don’t add up

Each reported p-value recomputed from its test statistic and degrees of freedom.

  • Inconsistent p-value: t(11)=2.51, p = .028

    Minor

    The paper reports p = .028 here; recomputing from the test statistic and its degrees of freedom gives p = .029 (two-tailed). The check cannot tell whether the statistic or the p-value is the misprint.

    Reported p = .028 · recomputed p = .029

1 of 1

Statistics recomputed

Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.

  • Doesn’t add upt(11) = 2.51reported p = .028 · recomputed p = .029

    “t(11)=2.51, p = .028”

  • Consistentt(23) = 2.49reported p = .02 · recomputed p = .020

    “t(23)=2.49, p = .02”

  • Consistentt(44) = 2.94reported p = .005 · recomputed p = .005

    “t(44)=2.94, p = .005”

  • Consistentt(19) = 2.27reported p = .03 · recomputed p = .035

    “t(19)=2.27, p = .03”

  • Consistentt(19) = 3.35reported p = .003 · recomputed p = .003

    “t(19)=3.35, p = .003”

5 of 5

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Adult plasticity described as both decreased and increased

    Minor

    The paper reports increased tLTP in adult rats exposed to nicotine during adolescence, but later refers to decreased plasticity in those rats.

1 of 1

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Related

Authors
Goriounova, N. A., & Mansvelder, H. D.
Affiliations
Amsterdam Neuroscience (NL)
ORCID
Venue
Journal of Neuroscience
Publisher
Society for Neuroscience
Published
2012-08-01
Volume
32
Issue
31
Pages
10484-10493
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
DOI
10.1523/jneurosci.5502-11.2012
PMC
PMC3552309
OpenAlex
W2090285951
Cited by
51
References
54
Citations by year
2026: 1 · 2025: 5 · 2024: 2 · 2023: 3 · 2022: 1 · 2021: 2 · 2020: 1 · 2019: 1 · 2018: 6 · 2017: 5 · 2016: 5 · 2015: 6 · 2014: 3 · 2013: 7 · 2012: 3
FWCI
2.50
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • VU Research Portal (publishedVersion, other-oa)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders
  • European Commission (242167)
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek (917.76.360)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
  • Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
Keywords
adolescent nicotine exposure, spike-timing-dependent plasticity, medial prefrontal cortex, mGluR2, long-term synaptic plasticity, nicotinic acetylcholine receptors, synaptic plasticity, cognitive impairment, smoking, brain development
MeSH terms
Action Potentials, Age Factors, Aging, Alanine, Amino Acids, Animals, Animals, Newborn, Electric Stimulation, Female, Male, Neurons, Nicotine, Pregnancy, Time Factors, Rats, Wistar, Prefrontal Cortex, Long-Term Potentiation, Excitatory Amino Acid Agonists, Excitatory Amino Acid Antagonists, Nicotinic Agonists, Bridged Bicyclo Compounds, Heterocyclic, Excitatory Postsynaptic Potentials, Rats, In Vitro Techniques

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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.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

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