Intracellular mechanisms underlying the nicotinic enhancement of LTP in the rat dentate gyrus

Welsby, Philip J.; Rowan, Michael J.; Anwyl, Roger

doi:10.1111/j.1460-9568.2008.06562.x

Cited by 57 publications

(49 citation statements)

References 83 publications

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“…The deficits in basal synaptic transmission and LTP could be associated with alterations in nAChR subtypes that lend a modulatory role synaptic transmission and plasticity [75,76]. This notion is supported by a recent finding that mRNA levels of a7-nAChRs were reduced in the hippocampus of rats exposed to nicotine prenatally [20].…”

Section: Discussionsupporting

confidence: 69%

Developmental nicotine exposure induced alterations in behavior and glutamate receptor function in hippocampus

Parameshwaran

Buabeid

Karuppagounder

et al. 2011

Cell. Mol. Life Sci.

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In the developing brain, nicotinic acetylcholine receptors (nAChRs) are involved in cell survival, targeting, formation of neural and sensory circuits, and development and maturation of other neurotransmitter systems. This regulatory role is disrupted when the developing brain is exposed to nicotine, which occurs with tobacco use during pregnancy. Prenatal nicotine exposure has been shown to be a strong risk factor for memory deficits and other behavioral aberrations in the offspring. The molecular mechanisms underlying these neurobehavioral outcomes are not clearly elucidated. We used a rodent model to assess behavioral, neurophysiological, and neurochemical consequences of prenatal nicotine exposure in rat offspring with specific emphasis on the hippocampal glutamatergic system. Pregnant dams were infused with nicotine (6 mg/kg/day) subcutaneously from the third day of pregnancy until birth. Results indicate that prenatal nicotine exposure leads to increased anxiety and depressive-like effects and impaired spatial memory. Synaptic plasticity in the form of long-term potentiation (LTP), basal synaptic transmission, and AMPA receptor-mediated synaptic currents were reduced. The deficit in synaptic plasticity was paralleled by declines in protein levels of vesicular glutamate transporter 1 (VGLUT1), synaptophysin, AMPA receptor subunit GluR1, phospho(Ser845) GluR1, and postsynaptic density 95 (PSD-95). These results suggest that prenatal nicotine exposure by maternal smoking could result in alterations in the glutamatergic system in the hippocampus contributing to the abnormal neurobehavioral outcomes.

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Section: Discussionsupporting

confidence: 69%

Developmental nicotine exposure induced alterations in behavior and glutamate receptor function in hippocampus

Parameshwaran

Buabeid

Karuppagounder

et al. 2011

Cell. Mol. Life Sci.

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“…Pretreatment with anticholinesterase drugs has been found to prevent the inhibition of LTP by Ab both in vitro and in vivo [32,41] but the underlying mechanisms are uncertain. Given the ability of anticholinesterases to enhance control LTP, as outlined above, it might be expected that post-Ab treatment should be as effective as pretreatment in ameliorating synaptic plasticity deficits.…”

Section: Endogenous Acetylcholine-dependent Mechanismsmentioning

confidence: 99%

Neurotransmitter receptor and time dependence of the synaptic plasticity disrupting actions of Alzheimer's disease Aβ in vivo

Klyubin

Ondrejčák²,

Hayes³

et al. 2014

Phil. Trans. R. Soc. B

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Many endogenous factors influence the time course and extent of the detrimental effects of amyloid β-protein (Aβ) on synaptic function. Here, we assessed the impact of varying endogenous glutamatergic and cholinergic transmission by pharmacological means on the disruption of plasticity at hippocampal CA3-to-CA1 synapses in the anaesthetized rat. NMDA receptors (NMDARs) are considered critical in mediating Aβ-induced inhibition of long-term potentiation (LTP). However, intracerebroventricular injection of Aβ 1–42 inhibited not only NMDAR-dependent LTP but also voltage-activated Ca 2+ -dependent LTP induced by strong conditioning stimulation during NMDAR blockade. On the other hand, another form of NMDAR-independent synaptic plasticity, endogenous acetylcholine-induced muscarinic receptor-dependent long-term enhancement, was not hindered by Aβ 1–42 . Interestingly, augmenting endogenous acetylcholine activation of nicotinic receptors prior to the injection of Aβ 1–42 prevented the inhibition of NMDAR-dependent LTP, whereas the same intervention when introduced after the infusion of Aβ was ineffective. We also examined the duration of action of Aβ, including water soluble Aβ from Alzheimer's disease (AD) brain. Remarkably, the inhibition of LTP induction caused by a single injection of sodium dodecyl sulfate-stable Aβ dimer-containing AD brain extract persisted for at least a week. These findings highlight the need to increase our understanding of non-NMDAR mechanisms and of developing novel means of overcoming, rather than just preventing, the deleterious synaptic actions of Aβ.

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“…Finally, the DG is a brain region that is highly sensitive to nicotine and significantly affects synaptic plasticity. Either application of nicotine in brain slices or subcutaneous injection of nicotine, in vivo, enhances LTP in dentate gyrus (Sawada et al 1994;Curran and Connor 2003;Welsby et al 2006Welsby et al , 2009. Acute nicotine treatment prevents sleep deprivation-induced impairment of LTP in the DG (Aleisa et al 2011) and administration of a highdose of nicotine causes synaptic potentiation in the DG, without pairing of tetanic stimulation (Matsuyama et al 2000;Tang and Dani 2009).…”

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confidence: 99%

D1/D5 receptors and histone deacetylation mediate the Gateway Effect of LTP in hippocampal dentate gyrus

et al. 2014

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The dentate gyrus (DG) of the hippocampus is critical for spatial memory and is also thought to be involved in the formation of drug-related associative memory. Here, we attempt to test an aspect of the Gateway Hypothesis, by studying the effect of consecutive exposure to nicotine and cocaine on long-term synaptic potentiation (LTP) in the DG. We find that a single injection of cocaine does not alter LTP. However, pretreatment with nicotine followed by a single injection of cocaine causes a substantial enhancement of LTP. This priming effect of nicotine is unidirectional: There is no enhancement of LTP if cocaine is administrated prior to nicotine. The facilitation induced by nicotine and cocaine can be blocked by oral administration of the dopamine D1/D5 receptor antagonist (SKF 83566) and enhanced by the D1/D5 agonist (SKF 38393). Application of the histone deacetylation inhibitor suberoylanilide hydroxamic acid (SAHA) simulates the priming effect of nicotine on cocaine. By contrast, the priming effect of nicotine on cocaine is blocked in genetically modified mice that are haploinsufficient for the CREB-binding protein (CBP) and possess only one functional CBP allele and therefore exhibit a reduction in histone acetylation. These results demonstrate that the DG of the hippocampus is an important brain region contributing to the priming effect of nicotine on cocaine. Moreover, both activation of dopamine-D1 receptor/ PKA signaling pathway and histone deacetylation/CBP mediated transcription are required for the nicotine priming effect in the DG.

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Intracellular mechanisms underlying the nicotinic enhancement of LTP in the rat dentate gyrus

Cited by 57 publications

References 83 publications

Developmental nicotine exposure induced alterations in behavior and glutamate receptor function in hippocampus

Developmental nicotine exposure induced alterations in behavior and glutamate receptor function in hippocampus

Neurotransmitter receptor and time dependence of the synaptic plasticity disrupting actions of Alzheimer's disease Aβ in vivo

D1/D5 receptors and histone deacetylation mediate the Gateway Effect of LTP in hippocampal dentate gyrus

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