Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors

Bashir, Zafar I.; Bortolotto, Zuner A.; Davies, Ceri H.; Berretta, Nicola; Irving, Andrew J.; Seal, Andrew; Henley, Jeremy M.; Jane, David E.; Watkins, Johnathan; Collingridge, Graham L.

doi:10.1038/363347a0

Cited by 703 publications

(297 citation statements)

References 33 publications

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“…Thus, there is a clear-cut difference between interneuron subtypes that exhibit rhythmic firing (I and II) versus those that do not (III and IV), with frequent mGluR1 expression in the former and rare expression in the latter two classes. This observation is of particular interest in view of previous data indicating that the contribution of mGluRs to excitatory responses is significant only after activation by highfrequency stimuli (Bashir et al, 1993;Miles and Poncer, 1993). The evidence for the preferential extrasynaptic localization of mGluRs (Baude et al, 1993) is also indicative for a functional role of these glutamate receptors under conditions of highfrequency stimulation.…”

Section: Discussionmentioning

confidence: 63%

Differential Expression of Group I Metabotropic Glutamate Receptors in Functionally Distinct Hippocampal Interneurons

et al. 2000

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Metabotropic glutamate receptors (mGluRs) have been proposed to be involved in oscillatory rhythmic activity in the hippocampus. However, the subtypes of mGluRs involved and their precise distribution in different populations of interneurons is unclear. In this study, we combined functional analysis of mGluR-mediated inward currents in CA1 oriens-alveus interneurons with anatomical and immunocytochemical identification of these interneurons and expression analysis of group I mGluR using single-cell reverse transcription-PCR (RT-PCR). Four major interneuron subtypes could be distinguished based on the mGluR-mediated inward current induced by the application of 100 M trans-(1S,3R)-1-aminocyclopentane-1,3-dicarboxylic acid (ACPD) under voltage-clamp conditions and the action potential firing pattern under current-clamp conditions. Type I interneurons responded with a large inward current of ϳ224 pA, were positive for somatostatin, and the majority expressed both mGluR1 and mGluR5. Type II interneurons responded with an inward current of ϳ80 pA, contained calbindin, and expressed mainly mGluR1. Type III interneurons responded with an inward current of ϳ60 pA. These interneurons were fast-spiking, contained parvalbumin, and expressed mainly mGluR5. Type IV interneurons did not respond with an inward current upon application of ACPD, yet they expressed group I mGluRs. Activation of group I mGluRs under currentclamp conditions increased spike frequency and resulted in rhythmic firing activity in type I and II, but not in type III and IV, interneurons. RT-PCR results suggest that activation of mGluR1 in the subsets of GABAergic interneurons, classified here as type I and II, may play an important role in mediating synchronous activity.

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Section: Discussionmentioning

confidence: 63%

Differential Expression of Group I Metabotropic Glutamate Receptors in Functionally Distinct Hippocampal Interneurons

et al. 2000

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“…This has previously been reported by some groups (Bashir et al, 1993;Bortolotto et al, 1995;Richter-Levin et al, 1994;Riedel et al, 1995), and not by others (Chinestra et al, 1993;Manzoni et al, 1994;Selig et al, 1995). Also work from mGluR5 knockout mice have shown that NMDA-receptor mediated LTP is impaired in these animals (Jia et al, 1998;Lu et al, 1997).…”

Section: Discussionmentioning

confidence: 80%

“…The involvement of the mGluRs in hippocampal LTD has been well established (Bolshakov and Siegelbaum, 1994;Fitzjohn et al, 1999;O'Mara et al, 1995;Snyder et al, 2001), however their contribution to LTP has been a subject of unresolved debate (Bashir et al, 1993;Bortolotto et al, 1995;Chinestra et al, 1993;Manzoni et al, 1994;Richter-Levin et al, 1994;Riedel et al, 1995;Selig et al, 1995). To date, eight mGluR subtypes, designated mGluR1 to mGluR8, have been cloned from the mammalian brain.…”

Section: Introductionmentioning

confidence: 99%

Evidence for a role for the group I metabotropic glutamate receptor in the inhibitory effect of tumor necrosis factor-α on long-term potentiation

Cumiskey¹,

Butler²,

Moynagh³

et al. 2007

Brain Research

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Pro-inflammatory cytokines are known to be elevated in several neuropathological states that are associated with learning and memory. We have previously demonstrated in our laboratory that the inhibition of long-term potentiation (LTP) in the dentate gyrus region of the rat hippocampus, by tumor necrosis factor (TNF)-α, represents a biphasic response, an early phase dependent on p38 mitogen activated protein kinase (MAPK) activation and a later phase, possible dependent on protein synthesis. Many of the factors involved in the early modulation of LTP by TNF-α have yet to be elucidated. This study investigated if metabotropic glutamate receptors (mGluRs) are functionally linked to the inhibitory effect of TNF-α on LTP in the rat dentate gyrus in vitro. We report that the impairment of early-LTP by TNF-α is significantly attenuated by prior application of the group I/II mGluR antagonist MCPG and more specifically the mGluR5 antagonist MPEP. Since TNF-α is now known to cause transient increases in intracellular Ca 2+ levels from ryanodine-sensitive stores, we explored the possibility that disruption of intracellular Ca 2+ homeostasis could be involved.Ryanodine was found to significantly reverse the inhibition of LTP by TNF-α. From these studies we propose that the TNF-α inhibition of LTP is dependent upon the activation of TNFR1 and mGlu5-receptors. Importantly this study provides the first proof of the involvement of ryanodine-sensitive intracellular Ca 2+ stores in TNF-α mediated inhibition of LTP. IntroductionThe pro-inflammatory cytokine tumor-necrosis factor (TNF)-α is elevated in the brain in a number of neuropathological states including trauma, ischemia, Parkinson's disease, multiple sclerosis and HIV-associated dementia (Iida et al., 2000;Kassiotis and Kollias, 2001;Sriram et al., 2002). The signaling mechanism underlying the ability of TNF-α to cause the cognitive dysfunction associated with many of these conditions has been probed, but to date no clear mechanistic understanding has been reached. TNF-α and IL-1β at pathophysiological levels have been shown by many authors to inhibit long-term potentiation (LTP) in the CA1 and the dentate gyrus regions of the rat hippocampus (Cunningham et al., 1996;Murray and Lynch, 1998;Tancredi et al., 1992) but not by others (Stellwagen and Malenka, 2006). IL-1β has been shown to depress NMDAreceptor mediated field potentials in the dentate gyrus (Coogan B R A I N R E S E A R C H 1 1 3 6 ( 2 0 0 7 ) 1 3 -1 9 ⁎ Corresponding author.

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“…The study of hippocampal LTP has been a preferred experimental model due to the planar arrangement of the Schaffer collateral pathways leading to the CA1 region of the hippocampus. The induction of LTP in the CAI region of the hippocampus typically involves the activation of NMDA and metabotropic glutamate receptors, which increase intracellular calcium concentration [3][4][5][6]. Stimulation of these glutamate receptors promotes the activation of phospholipase A2 leading to the release of arachidonic acid [7,8] and the initiation of PAF synthesis.…”

Section: Introductionmentioning

confidence: 99%

Long‐term potentiation requires activation of calcium‐independent phospholipase A₂

et al. 1995

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The predominant phospholipase activity present in rat hippocampus is a calcium-independent phospholipase A 2 (302.9 + 19.8 pmol/mg.min for calcium-independent phospholipase A2 activity vs. 14.6 _+ 1.0 pmol/mg" rain for calcium-dependent phospholipase A2 activity). This calcium-independent phospholipase A 2 is exquisitely sensitive to inhibition by the mechanismbased inhibitor, (E)-6-(bromomethylene)-tetrahydro-3-(1-naphthalenyl)-2H-pyran -2-one (BEL). Moreover, treatment of hippocampal slices with BEL prior to tetanic stimulation prevents the induction of LTP (40.8 _+ 5.6% increase in excitatory postsynaptic potential (EPSP) slope for control slices (n = 6) vs. 5.8 + 8.5% increase in EPSP slope for BEL-treated slices (n = 8)). Importantly, LTP can be induced following mechanismbased inhibition of phospholipase A 2 by providing the end product of the phospholipase A 2 reaction, arachidonic acid, during the application of tetanic stimulation. Furthermore, the induction of LTP after treatment with BEL is dependent on the stereoelectronic configuration of the fatty acid provided since eicosa-5,8,1 ltrienoic acid, but not eicosa-8,11,14-trienoic acid, rescues LTP after BEL treatment (37.6 + 16.1% increase in EPSP slope for eicosa-5,8,11-trienoic acid vs. -3.7 + 5.2% increase in EPSP slope for eicosa-8,11,14-trienoic acid).Collectively, these results provide the first demonstration of the essential role of calciumindependent phospholipase A 2 in synaptic plasticity.

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Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors

Cited by 703 publications

References 33 publications

Differential Expression of Group I Metabotropic Glutamate Receptors in Functionally Distinct Hippocampal Interneurons

Differential Expression of Group I Metabotropic Glutamate Receptors in Functionally Distinct Hippocampal Interneurons

Evidence for a role for the group I metabotropic glutamate receptor in the inhibitory effect of tumor necrosis factor-α on long-term potentiation

Long‐term potentiation requires activation of calcium‐independent phospholipase A₂

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Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors

Cited by 703 publications

References 33 publications

Differential Expression of Group I Metabotropic Glutamate Receptors in Functionally Distinct Hippocampal Interneurons

Differential Expression of Group I Metabotropic Glutamate Receptors in Functionally Distinct Hippocampal Interneurons

Evidence for a role for the group I metabotropic glutamate receptor in the inhibitory effect of tumor necrosis factor-α on long-term potentiation

Long‐term potentiation requires activation of calcium‐independent phospholipase A2

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Long‐term potentiation requires activation of calcium‐independent phospholipase A₂