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University of Texas at San Antonio, Department of Biology, San Antonio, Texas
Submitted 30 August 2004; accepted in final form 12 November 2004
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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; Pin and Duvoisin 1995; Skeberdis et al. 2001), all of which underlie learning and memory-related mechanisms. To date, eight subtypes of the mGluRs have been identified and placed into three distinct classes (mGluR1–8). Class I includes mGluR1 and mGluR5, both of which are coupled to phospholipase C (PLC). Classes II (mGluR2 and mGluR3) and III (mGluR4,6–8) are negatively coupled to adenylyl cyclase (Pin and Duvoisin 1995). Because of the role mGluRs play in the modulation of such significant neuronal channels, multiple studies have addressed the role of the various mGluR subclasses on learning and memory.
Intra-peritoneal (ip) injections of the class I selective mGluR antagonist -aminoindan-1, 5-dicarboxylic acid (AIDA) improves short-term memory and impairs long-term memory in a spatial memory task in rodents (Christofferson et al. 1999). Four-CPG, another class I antagonist, blocked retention of shock-reinforced spatial alternation in the Y-maze (Balschun and Wetzel 1998; Balschun et al. 1999). Administration of nonselective mGluR agonists, such as ACPD (1-aminocyclopentane-1, 3-dicarboxylic acid), and (2S,3S)-carboxycyclopropylglycin (L-CCG-1), results in poor performance on the Morris water maze and the shock-reinforced Y maze (Riedel et al. 1995). AIDA (ip) limits kainate-induced hippocampal dysfunction, as indexed by water maze training and in vitro LTP (Reinaud et al. 2002), thus indicating behavioral and electrophysiological changes induced by central administration of AIDA. The class I and II antagonist (R,S)-
-methyl-4-carboxyphenylglycine (MCPG) also impairs water maze performance (Bordi 1996). Although this evidence clearly implicates that mGluRs play a role in various types of learning paradigms, the underlying mechanism by which this occurs is not yet understood.
Some of the existing electrophysiological work focuses on elucidating the role of mGluRs on long-term potentiation (LTP) at multiple hippocampal synapses. The results of mGluRs activation/inhibition on hippocampal LTP have been quite contradictory. For example, the mGluR antagonist MCPG blocked mossy fiber LTP in vitro (Bashir et al. 1993) in one preparation but not in another (Manzoni et al. 1994). Yeckel et al. (1999) reported that in vitro mossy fiber (MF) LTP induction was dependent on the activation of mGluRs, whereas Mellor and Nicoll (2001) found that mGluRs antagonist had no effect on MF LTP in vitro. Additional work using mGluR1-knockout mice and mGluR antagonists did not identify a role for mGluRs in MF LTP (Hsia et al. 1995), whereas a different study using mGluR1-knockout mice reported impaired MF LTP (Conquet et al. 1994). More recently, kainate 1 (KA1) and kainate 2 (KA2) receptors were found both pre- and postsynaptically at the MF synapses and are thought to coassemble with mGluR6 subunits to modulate MF activity (Darstein et al. 2003).
The mechanisms underlying MF-CA3 LTP are particularly important because of the pathway's involvement in spatial learning. This pathway projects from granule cells in the dentate gyrus to the stratum lucidum layer of area CA3 of the hippocampus, displays an NMDA-independent form of LTP, and is dependent on the activation of opioid receptors. This activation is thought to be facilitated by opioid peptides contained in and released by the MFs and has been confirmed both in vivo and in vitro (Derrick et al. 1991, 1992; Derrick and Martinez 1994; Jin and Chavkin 1999). Further evidence suggests that Ca2+ entry is necessary for MF-LTP induction (Bashir et al. 1993; Ito and Sugiyama 1991; Williams and Johnston 1996; Yeckel et al. 1999). However, little is known regarding the specific receptor systems that interact with opioid receptors to result in LTP induction at the MF pathway.
In this study, we examined the role of the mGluR1 antagonist AIDA on LTP induction at the MF-CA3 pathway in vivo using Sprague Dawley (Mata et al. 2000) and F344 rats. Although there is evidence against the role of mGluR in MF LTP (Hsia et al. 1995), all of these previous studies were conducted in vitro, and there is extensive evidence documenting differences in LTP induction and maintenance at the MF pathway in vivo and in vitro (Barea-Rodriguez et al. 2000; Derrick and Martinez 1996; Nicoll et al. 1994). We report that AIDA significantly impairs induction of MF LTP in both of the strains tested.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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All experimental procedures were approved in advance by the Institutional Animal Care and Use Committee at the University of Texas at San Antonio and are in accordance with National Institutes of Health guidelines. Adult male Sprague Dawley and F344 rats (300–450 g; Charles River Laboratories, Indianapolis, IN) were anesthetized with pentobarbital sodium (Nembutal solution; 50 mg/kg ip, Henry Schein Veterinary Supply) and placed on a stereotaxic frame. Electrodes were placed in the MF pathway at coordinates corresponding to the s. lucidum. The first electrode was initially placed in the granule cell layer of the dentate gyrus with the aid of stereotaxic coordinates and audio monitoring of CA1 pyramidal and granule cell unit discharges due to injury. The second electrode was placed above the CA3 pyramidal layer of the dorsal hippocampus (AP: –2.9 mm; ML: 2.2 mm; DV: 3.1–3.3 below dura). Dorsoventral (DV) coordinates were determined using previously described criteria (Derrick and Martinez 1994, 1996). We delivered stimulation at 0.05 Hz until antidromic spikes (2–3 ms to peak) were observed in the granule cells. We then evoked orthodromic responses by delivering stimulation through the dentate electrode and recording from the electrode placed in CA3 (See Fig. 1). We adjusted the stimulating electrode until a characteristic MF excitatory postsynaptic potential (EPSP) was observed (
0.5 mV negative potential) and easily elicited with low (10–50 µA) current intensity and an onset at 2.5 ms and a peak at 8–10 ms.
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20 min at 0.05 Hz, animals received either ((±))-3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid (CPP; NMDA-R antagonist, 10 mg/kg ip; Sigma RBI, St. Louis, MO), naloxone hydrochloride (opioid receptor antagonist, 10 mg/kg ip; Sigma RBI) or AIDA (mGluR1 antagonist, 1 mg/kg ip, Sigma). CPP was delivered to ensure that the recordings were from MF-evoked responses, and was given at a dose previously found to be effective at blocking NMDA-dependent LTP in vivo (Hernandez et al. 1994). One hour or 30 min (respectively) after drug administration, LTP was induced by two 100-Hz, 1-s trains delivered at the same intensity sufficient to evoke 50% of the maximal MF response. Evoked MF responses were collected for an additional 60 min in all groups (n = 3, F344; n = 7, Sprague Dawley). In control animals, low-frequency MF responses were collected at 0.05 Hz for 1 h, but 100-Hz trains were not delivered. Electroencephalogram (EEG) recordings were monitored for 1 min after high-frequency train and no seizures or after discharge activity was noted in the animals. MF LTP was measured at 1 h by obtaining the percent change in the field EPSP slope as calculated using a 20% trimmed mean from the last 5 min of baseline and the last 5 min of the 1-h collection period. All animals were killed using Nembutal solution (100 mg/kg ip) 1 h after delivery of the high-frequency train. Intrahippocampal injections
A 33-gauge stainless steel cannula-recording electrode was placed above the CA3 pyramidal cell layer of the dorsal hippocampus using the coordinates listed in the preceding text. The combination of cannula-recording electrode was constructed by insulating (Epoxylite, Irvine, CA) the outside of the cannula, except for the tip and a 3-cm portion at the top. A stainless steel wire (A-M Systems) was wrapped around the cannula at the noninsulated top, and connected to an amplifier using an amphenol connector. Plastic tubing (PE 20) was attached to the top opening of the cannula to allow for drug delivery into the area in which evoked responses were collected. Responses were evoked via direct stimulation of the MFs using a stainless steel bipolar electrode. Evoked responses were collected using the protocol mentioned previously. After a 20-min baseline period, AIDA (25, 37.5, or 50 nmol; 1 µl total volume; Sigma, n = 3) or saline (1 µl total, n = 3) were delivered unilaterally into the s. lucidum of hippocampal area CA3 via pressure injection using a syringe pump (Harvard Apparatus, Indianapolis, IN). The drugs were delivered over a 5-min period of time. The drug infusion period was followed by a 30-min post infusion period, followed by delivery of high-frequency stimulation of two 100-Hz trains, with an intertrain interval of 20 s (200 total pulses). Evoked responses were collected for 1 h post high-frequency stimulation.
Verification of electrode placement
Verifications were performed using electrophysiological criteria for all animals. Electrophysiological criteria involved audio localization of CA1, CA3, and granule cells in the dentate, localization of antidromic response in the dentate gyrus, and the presence of MF evoked responses preceded by a presynaptic volley with an onset of 2.5 ms (orthodromic response). Histological verification of electrode placement was performed on 10% of subjects and correct electrode placement was observed in all of these brains.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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) and F344 rats. MF-CA3 LTP was also blocked after intrahippocampal infusion of AIDA in Sprague Dawley rats.
In the MF synaptic pathway, class I mGluRs have been localized to CA3 dendritic spines in s. radiatum (Lujan et al. 1996). Activation of these mGluR1s evoke Ca2+ release in CA3 neurons (Kapur et al. 2001), supporting the idea that mGluRs are activated by MF bursts, and initiate Ca2+ release in CA3 pyramidal cells (Kapur et al. 2001). Our findings reiterate the importance of postsynaptic Ca2+ in LTP induction at the MF synapse. Various studies show that any experimental procedure that impedes an increase in postsynaptic Ca2+ consequently disrupts LTP at this synapse (Kapur et al. 2001; Yeckel et al. 1999). Our work in vivo with AIDA shows an mGluR-mediated blockade of LTP induction at the MF synapse that is potentially due to an mGluR effect on Ca2+ -mediated transmission at the MF-CA3 synapse.
The MFs contain and release prodynorphin and proenkephalin-derived opioid peptides (Chavkin et al. 1993a, b; Gall et al. 1981; McGinty and Bloom 1983; McGinty et al. 1983), and the release of endogenous opioid peptides by MF synapses requires high-frequency synaptic activity (Derrick and Martinez 1996). In our in vivo preparation, MF-CA3 LTP is blocked by the opioid antagonist naloxone. Our findings agree with previous literature showing that activation of endogenous opioid peptides is essential for LTP induction at the MF-CA3 pathway (Derrick and Martinez 1994a, b, 1996; Derrick et al. 1992). Blockade of NMDA-R by CPP and the presence of LTP in the MFs observed in these experiments also rules out the possibility of this receptor type being involved in this form of synaptic plasticity.
In our preparation, no strain differences were seen, as the AIDA-induced blockade of LTP induction was observed in both Sprague Dawley and F344 rats. The lack of between strain differences in our experiment is noteworthy because strain differences in spatial learning among Long Evans, F344, Dark-Agouti, Wistar, and Sprague Dawley rats have been documented (Troy Harker and Whishaw 2002). These studies indicate more dramatic differences on spatial learning acquisition but also occur in matching to place performance (Troy Harker and Whishaw 2002). In general, both spatial and nonspatial deficits can be associated with inbreeding. Despite these known behavioral differences in learning-related mechanisms between F344 and Sprague Dawley rats, the processes for LTP induction at the MF pathway appear to be quite similar. Both strains show an NMDA receptor-independent form of LTP that is blocked by the opioid-receptor antagonist naloxone as well as by the mGluR antagonist AIDA. Even with the mounting evidence supporting NMDA receptor-independent LTP in the MF-CA3 pathway, the specific mechanisms by which opioid peptides, and more recently, mGluRs, mediate LTP in this region are not completely understood.
Interestingly, the concentration of AIDA used for intrahippocampal injections in this study (37.5 nmol) is relatively low when compared with the values typically used in in vitro preparations (Brandrowski et al. 2003; Yeckel et al. 1999). This is not surprising as a complete understanding of the relationship between in vitro and in vivo drug metabolism/drug-drug interaction is still emerging. In fact, some literature suggests that using in vitro-in vivo correlation models (IVIVC) to predict in vivo concentration profiles given the in vitro release characteristics of a drug is not always accurate (Pitsiu et al. 2001). Multiple systematic differences must be considered, such as temporal variations between in vitro and in vivo release, the mechanics involved in slice preparation, and overall drug pharmacokinetics differences due to exposure in a controlled bath versus the intact animal. We are confident that the concentration of AIDA used in this study corresponds with typical doses used for in vivo intracranial administration of the drug. In fact, concentrations as low as 0.4 nmol successfully reduce acute neuronal degeneration and behavioral deficits after traumatic brain injury in rats (Lyeth et al. 2001). Similarly low concentrations of intrahippocampal AIDA (50 nmol) significantly alter fear conditioning (Maciejak et al. 2003). We found that other concentrations of AIDA (25 and 50 nmol, data not shown) did not result in significant changes in LTP induction. The dramatic differences that exist between in vitro and in vivo preparations further reiterate the importance of validating results using both in vitro and in vivo models.
Earlier reports indicate that rodent long-term retention is impaired by AIDA (Christoffersen et al. 1999; Nielsen et al. 1997) and that this impairment is not due to drug-induced behavioral effects (Nielsen et al. 1997). LTP, as the widely accepted model for hippocampally dependent reference memory, has also been inhibited by the class I/II mGluR antagonist MCPG (Riedel et al. 1996a, b). In this experiment, we find that in addition to opioid peptides, mGluRs are also involved in the induction of MF-LTP in vivo. As mentioned earlier, there is extensive work documenting differences in LTP induction and maintenance at the MF pathway in vivo and in vitro (Barea-Rodriguez et al. 2000; Derrick and Martinez 1994a, b 1996; Derrick et al. 1992; Nicoll et al. 1994; Zalutsky et al. 1992). Despite some evidence against the role of mGluRs in MF LTP in vitro (Hsia et al. 1995; Mellor and Nicoll 2001), our results indicate a blockade of in vivo MF LTP induction in the presence of AIDA, thus supporting the literature linking mGluRs to hippocampally dependent memory mechanisms (Conquet et al. 1994; Kapur et al. 2001).
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GRANTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: K. Thompson, University of Texas at San Antonio, Dept. of Biology, 6900 N. Loop 1604 West, San Antonio, TX 78249 (E-mail: kthompson{at}utsa.edu)
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Balschun D, Manahan-Vaughan D, Wagner T, Behnisch T, Reymann KG, and Wetzel W. A specific role for group I mGluRs in hippocampal LTP and hippocampus-dependent spatial learning. Learn Mem 6: 138–152, 1999.
Barea-Rodriguez EJ, Rivera DT, Jaffe DB, and Martinez JL Jr. Protein synthesis inhibition blocks the induction of mossy fiber long-term potentiation in vivo. J Neurosci 20: 8528–8523, 2000.
Bashir ZI, Bortolotto ZA, Davies CH, Berretta N, Irving AJ, Seal AJ, Henley JM, Jane DE, Watkins JC, and Collingridge GL. Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature 363: 347–350, 1993.[CrossRef][Medline]
Blasco-Ibanez JM and Freund TF. Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CA1 subfield: structural basis of feed-back activation. Eur J Neurosci 7: 2170–2180, 1995.[CrossRef][ISI][Medline]
Bliss TV and Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31–39, 1993.[CrossRef][Medline]
Bordi F. Reduced long-term potentiation in the dentate gyrus of mGlu1 receptor-mutant mice in vivo. Eur J Pharmacol 301: R15–16, 1996.[CrossRef][ISI][Medline]
Brandowski AE, Huguenard JR, and Prince DA. Baseline glutamate levels affect group I and II mGluRs in layer pyramidal neurons of rat sensorimotor cortex. J Neurophysiol 89: 1308–1316, 2003.
Chavkin C, Bakhit C, and Bloom FE. Evidence for dynorphin-A as a neurotransmitter in rat hippocampus. Life Sci 33, Suppl 1: 13–16, 1983a.
Chavkin C, Bakhit C, Weber E, and Bloom FE. Relative contents and concomitant release of prodynorphin/neoendorphin-derived peptides in rat hippocampus. Proc Natl Acad Sci USA 80: 7669–7673, 1983b.
Christoffersen GR, Christensen LH, Hammer P, and Vang M. The class I metabotropic glutamate receptor antagonist, AIDA, improves short-term and impairs long-term memory in a spatial task for rats. Neuropharmacology 38: 817–823, 1999.[CrossRef][ISI][Medline]
Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, and Conde F. Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372: 237–243, 1994.[CrossRef][Medline]
Darstein M, Petralia RS, Swanson GT, Wenthold RJ, and Heinemann SF. Distribution of kainate receptor subunits at hippocampal mossy fiber synapses. J Neurosci 23: 8013–8019, 2003.
Derrick BE and Martinez JL Jr. Frequency-dependent associative long-term potentiation at the hippocampal mossy fiber-CA3 synapse. Proc Natl Acad Sci USA 91: 10290–10294, 1994a.
Derrick BE and Martinez JL Jr. Opioid receptor activation is one factor underlying thefrequency dependence of mossy fiber LTP induction. J Neurosci 14: 4359–4367, 1994b.[Abstract]
Derrick BE and Martinez JL Jr. Associative, bidirectional modifications at the hippocampal mossy fibre-CA3 synapse. Nature 381: 429–434, 1996.[CrossRef][Medline]
Derrick BE, Rodriguez SB, Lieberman DN, and Martinez JL Jr. Mu opioid receptors are associated with the induction of hippocampal mossy fiber long-term potentiation. J Pharmacol Exp Ther 263: 725–733, 1992.
Derrick BE, Weinberger SB, and Martinez JL Jr. Opioid receptors are involved in an NMDA receptor-independent mechanism of LTP induction at hippocampal mossy fiber-CA3 synapses. Brain Res Bull 27: 219–223, 1991.[CrossRef][ISI][Medline]
Gall C, Brecha N, Karten HJ, and Chang KJ. Localization of enkephalin-like immunoreactivity to identified axonal and neuronal populations of the rat hippocampus. J Comp Neurol 198: 335–350, 1981.[CrossRef][ISI][Medline]
Hernandez RV, Derrick BE, Rodriguez WA, and Martinez JL, Jr. (+/–) CPP, and NMDA receptor antagonist, blocks the induction of commissural-CA3 LTP in the anesthetized rat. Brain Res 656: 215–219,1994.[CrossRef][ISI][Medline]
Hsia AY, Salin PA, Castillo PE, Aiba A, Abeliovich A, Tonegawa S, and Nicoll RA. Evidence against a role for metabotropic glutamate receptors in mossy fiber LTP: the use of mutant mice and pharmacological antagonists. Neuropharmacol 34: 1567–1572, 1995.[CrossRef][ISI][Medline]
Ito I and Sugiyama H. Roles of glutamate receptors in long-term potentiation at hippocampal mossy fiber synapses. Neuroreport 2: 333–336, 1991.[ISI][Medline]
Jin W and Chavkin C. Mu opioids enhance mossy fiber synaptic transmission indirectly by reducing GABAB receptor activation. Brain Res 821: 286–293, 1999.[CrossRef][ISI][Medline]
Kapur A, Yeckel M, and Johnston D. Hippocampal mossy fiber activity evokes Ca2+ release in CA3 pyramidal neurons via a metabotropic glutamate receptor pathway. Neuroscience 107: 59–69, 2001.[CrossRef][ISI][Medline]
Lyeth BG, Ging QZ, Shields S, Muizelaar JP, and Berman RF. Group 1 metabotropic glutamate antagonist reduces acute neuronal degeneration and behavioral deficits after traumatic brain injury in rats. Exp Neurol 169: 191–199, 2001.[CrossRef][ISI][Medline]
Lujan R, Nusser Z, Roberts JD, Shigemoto R, and Somogyi P. Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 8: 1488–1500, 1996.[CrossRef][ISI][Medline]
Maciejak P, Taracha E, Lehner M, Szyndler J, Bidzinski A, Skorzewska A, Wislowska A, Zienowicz M, and Plaznik A. Hippocampal mGluR1 and consolidation of contextual fear conditioning. Brain Res Bull 62: 39–45, 2003.[CrossRef][ISI][Medline]
Manzoni OJ, Weisskopf MG, and Nicoll RA. MCPG antagonizes metabotropic glutamate receptors but not long-term potentiation in the hippocampus. Eur J Neurosci 6: 1050–1054, 1994.[CrossRef][ISI][Medline]
Mata ML, Barea-Rodriguez, EJ, and Martinez JL Jr. The involvement of mGluR1 in two forms of mossy fiber long term potentiation in vivo. Soc Neurosci Abstr 26: 362, 2000.
McGinty JF and Bloom FE. Double immunostaining reveals distinctions among opioid peptidergic neurons in the medial basal hypothalamus. Brain Res 278: 145–153, 1983.[CrossRef][ISI][Medline]
McGinty JF, Henriksen SJ, Goldstein A, Terenius L, and Bloom FE. Dynorphin is contained within hippocampal mossy fibers: immunochemical alterations after kainic acid administration and colchicine-induced neurotoxicity. Proc Natl Acad Sci USA 80: 589–593, 1983.
Mellor J and Nicoll RA. Hippocampal mossy fiber LTP is independent of postsynaptic calcium. Nat Neurosci 4: 125–126, 2001.[CrossRef][ISI][Medline]
Nicoll RA, Castillo PE, and Weisskopf MG. The role of Ca2+ in transmitter release and long-term potentiation at hippocampal mossy fiber synapses. Adv Second Messenger Phosphoprotein Res 29: 497–505, 1994.[ISI][Medline]
Nicoletti F, Bruno V, Catania MV, Battaglia G, Copani A, Barbagallo G, Cena V, Sanchez-Prieto J, Spano PF, and Pizzi M. Group-I metabotropic glutamate receptors: hypotheses to explain their dual role in neurotoxicity and neuroprotection. Neuropharmacology 38: 477–484, 1999.[CrossRef][ISI][Medline]
Nielsen KS, Macphail EM, and Riedel G. Class I mGlu receptor antagonist 1-aminoindan-1,5-dicarboxylic acid blocks contextual but not cue conditioning in rats. Eur J Pharmacol 326:105–108, 1997.[CrossRef][ISI][Medline]
Pin JP and Duvoisin R. The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34: 1–26, 1995.[CrossRef][ISI][Medline]
Pitsiu M, Sathyan G, Gupta S, and Verotta D. A semiparametric deconvolution model to establish in vivo-in vitro correlation applied to OROS oxybutynin. J Pharmacol Sci 90: 702–712, 2001.[CrossRef][ISI][Medline]
Renaud J, Emond M, Meilleur S, Psarropoulou C, and Carmant L. AIDA, a class I metabotropic glutamate-receptor antagonist limits kainate-induced hippocampal dysfunction. Epilepsia 43: 1306–1317, 2002.[CrossRef][ISI][Medline]
Riedel G. Function of metabotropic glutamate receptors in learning and memory. Trends Neurosci 19: 219–224, 1996.[CrossRef][ISI][Medline]
Riedel G, Opitz T, and Reymann KG. Blockade of metabotropic glutamate receptors protects hippocampal neurons from hypoxia-induced cell death in rat in vivo. Prog Neuropsychopharmacol Biol Psychiatry 20: 1253–1263, 1996a.[CrossRef][Medline]
Riedel GT, Wetzel W, and Reymann KG. Metabotropic glutamate receptors in spatial and nonspatial learning in rats studied by means of agonist and antagonist application. Learn Mem 2: 243–265, 1995.
Riedel GT, Wetzel W, and Reymann KG. Comparing the role of metabotropic glutamate receptors in long-term potentiation and in learning and memory. Prog Neuropsychopharmacol Biol Psychiatry 20: 761–789, 1996b.[CrossRef][Medline]
Shigemoto R, Kulik A, Roberts JD, Ohishi H, Nusser Z, Kaneko T, and Somogyi P. Target-cell-specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature 381: 523–525, 1996.[CrossRef][Medline]
Skeberdis VA, Lan J, Opitz T, Zheng X, Bennett MV, and Zukin RS. mGluR1-Mediated potentiation of NMDA receptors involves a rise in intracellular calcium and activation of protein kinase C. Neuropharmacology 40: 856–865, 2001.[CrossRef][ISI][Medline]
Troy Harker K and Whishaw IQ. Place and matching-to-place spatial learning affected by rat inbreeding (Dark-Agouti, Fischer 344) and albinism (Wistar, Sprague-Dawley) but not domestication (wild rat vs. Long-Evans, Fischer-Norway). Behav Brain Res 21; 134: 467–477, 2002.
Williams SH and Johnston D. Actions of endogenous opioids on NMDA receptor-independent long-term potentiation in area CA3 of the hippocampus. J Neurosci 16: 3652–3660, 1996.
Yeckel MF, Kapur A, and Johnston D. Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism. Nat Neurosci 2: 625–633, 1999.[CrossRef][ISI][Medline]
Zalutsky RA and Nicoll RA. Mossy fiber long-term potentiation shows specificity but no apparent cooperativity. Neurosci Lett 138: 193–197, 1992.[CrossRef][ISI][Medline]
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