Distinct NMDA Receptors Provide Differential Modes of Transmission at Mossy Fiber-Interneuron Synapses

Lei, Saobo; McBain, Chris J.

doi:10.1016/s0896-6273(02)00608-6

Cited by 139 publications

(187 citation statements)

References 55 publications

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“…A second important feature that differentiates activity through CP-versus CI-AMPAR synapses is the magnitude of temporal summation observed at either synapse when measured under current clamp conditions (Lei et al, 2002). At CI-AMPAR containing synapses the presence of NR2B-lacking NMDARs endows synapses with a distinct temporal feature when compared with CP-AMPAR containing synapses (which contain NR2B-containing NMDARs).…”

Section: Two Types Of Ampa/nmdar Populate Mossy Fiber-interneuron Synmentioning

confidence: 99%

“…: +1 301 4024778; Fax: +1 301 4024777; E-mail: E-mail: mcbainc@mail.nih.gov. Uncited references: Castillo et al (1994), Chicurel and Harris (1992), Henze et al (2000), Lei and McBain (2002), Urban et al (2001), Zucker and Regehr (2002). diameter and about 18 μm along its long axis.…”

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confidence: 99%

“…The ratios of these two synapse types show some developmental regulation, with CP-AMPA receptor containing synapses modestly predominating (62% of measured synapses) early in development. However, it is important to appreciate that there is not a complete conversion of one synapse type to another on developmental maturation, at least at time points up to postnatal day 40 (Lei et al, 2002). At postnatal day 40, approximately 45% of mossy fiber-interneuron synapses are comprised of CI-AMPARs, whereas only 37% are comprised CP-AMPARs.…”

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confidence: 99%

“…Indeed short trains (five events) of synaptically evoked currents were observed to induced facilitation when measured at −20 mV but not at resting potential. This facilitation is absent when polyamines are omitted from the intracellular recording solution or when endogenous polyamines are chelated with ATP.A second important feature that differentiates activity through CP-versus CI-AMPAR synapses is the magnitude of temporal summation observed at either synapse when measured under current clamp conditions (Lei et al, 2002). At CI-AMPAR containing synapses the presence of NR2B-lacking NMDARs endows synapses with a distinct temporal feature when compared with CP-AMPAR containing synapses (which contain NR2B-containing NMDARs).…”

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confidence: 99%

“…In contrast, temporal summation at CP-AMPAR/NR2B-containing NMDARs is modest. Synaptic events triggered by NR2B-containing NMDARs possess a slower time course, but their small amplitude renders them unable to significantly influence transmission at these synapses at resting membrane potentials (Bischofberger et al, 2002;Lei et al, 2002). Consequently, repetitive activation of CP-AMPAR synapses results in rapid and brief synaptic potentials (Lei et al, 2002;Walker et al, 2002) that trigger single action potentials at their peak with little jitter.…”

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Chapter 13 Differential mechanisms of transmission and plasticity at mossy fiber synapses

McBain

2008

Progress in Brain Research

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The last few decades have seen the hippocampal formation at front and center in the field of synaptic transmission. However, much of what we know about hippocampal short-and long-term plasticity has been obtained from research at one particular synapse; the Schaffer collateral input onto principal cells of the CA1 subfield. A number of recent studies, however, have demonstrated that there is much to be learned about target-specific mechanisms of synaptic transmission by study of the lesser known synapse made between the granule cells of the dentate gyrus; the so-called mossy fiber synapse, and its targets both within the hilar region and the CA3 hippocampus proper. Indeed investigation of this synapse has provided an embarrassment of riches concerning mechanisms of transmission associated with feedforward excitatory and inhibitory control of the CA3 hippocampus. Importantly, work from a number of labs has revealed that mossy fiber synapses possess unique properties at both the level of their anatomy and physiology, and serve as an outstanding example of a synapse designed for target-specific compartmentalization of synaptic transmission. The purpose of the present review is to highlight several aspects of this synapse as they pertain to a novel mechanism of bidirectional control of synaptic plasticity at mossy fiber synapses made onto hippocampal stratum lucidum interneurons. It is not my intention to pour over all that is known regarding the mossy fiber synapse since many have explored this topic exhaustively in the past and interested readers are directed to other fine reviews (Henze et al., 2000;Urban et al., 2001;Lawrence et al., 2003;Bischofberger et al., 2006;Nicoll and Schmitz, 2005). Keywordshippocampus; local circuit inhibitory interneuron; long-term depression; glutamate receptors; plasticity; mossy fiber; mGluR7 Anatomy of the granule cell mossy fiber axonBefore discussing the physiological properties of the mossy fiber synapse, a short description of the granule cell anatomy and in particular the mossy fiber axon is warranted. The granule cell is the principal cell of the dentate gyrus and releases the neurotransmitter glutamate (Spruston and McBain, 2006). Granule cells typically possess small, ovoid cell bodies with a single apical, and conical dendritic tree, which extends into the molecular layer and terminates close to the hippocampal fissure. Compared to other principal cells of the hippocampal formation the granule cell is relatively small, possessing a somata approximately 10 μm in *Corresponding author. Tel.: +1 301 4024778; Fax: +1 301 4024777; E-mail: E-mail: mcbainc@mail.nih.gov. Uncited references: Castillo et al. (1994), Chicurel and Harris (1992), Henze et al. (2000), Lei and McBain (2002), Urban et al. (2001), Zucker and Regehr (2002). diameter and about 18 μm along its long axis. The number of dendritic branches is highly variable but the total dendritic length is significantly shorter than their CA1 and CA3 pyramidal neuron counterparts. The axon of the granule cell emerges ...

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Section: Two Types Of Ampa/nmdar Populate Mossy Fiber-interneuron Synmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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confidence: 99%

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confidence: 99%

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Chapter 13 Differential mechanisms of transmission and plasticity at mossy fiber synapses

McBain

2008

Progress in Brain Research

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Neurogranin is expressed by principal cells but not interneurons in the rodent and monkey neocortex and hippocampus

Singeç

Knoth

Ditter

et al. 2004

J of Comparative Neurology

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As a substrate of protein kinase C (PKC), neurogranin (NG) is involved in the regulation of calcium signaling and activity-dependent plasticity. Recently, we have shown that, in the rodent cerebellum, NG is exclusively expressed by gamma-aminobutyric acidergic Golgi cells, whereas, in the monkey cerebellum, brush cells were the only neuronal population expressing NG (Singec et al. [2003] J. Comp. Neurol. 459:278-289). In the present study, we analyzed the neocortical and hippocampal expression patterns of NG in adult mouse (C57Bl/6), rat (Wistar), and monkey (Cercopithecus aetiops). By using immunocytochemistry and nonradioactive in situ hybridization, we demonstrate strong NG expression by principal cells in different neocortical layers and in the hippocampus by granule cells of the dentate gyrus and pyramidal neurons of CA1-CA3. In contrast, double-labeling experiments in rodents revealed that neocortical and hippocampal interneurons expressing glutamate decarboxylase 67 (GAD67) were consistently devoid of NG. In addition, by using antibodies against parvalbumin, calbindin, and calretinin, we could demonstrate the absence of NG in interneurons of monkey frontal cortex and hippocampus. Together these findings corroborate the idea of different calcium signaling pathways in excitatory and inhibitory cells that may contribute to different modes of synaptic plasticity in these neurons.

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Development of NMDA NR2 subunits and their roles in critical period maturation of neocortical GABAergic interneurons

Zhi

Sun

2011

Developmental Neurobiology

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The goals of this research are to 1) determine the changes in the composition of NMDA receptor (NMDAR) subunits in GABAergic interneurons during critical period (CP); and 2) test the effect of chronic blockage of specific NR2 subunits on the maturation of specific GABAergic interneurons. Our data demonstrate that: 1) The amplitude of NMDAR mediated EPSCs (EPSCsNMDAR) was significantly larger in the postCP group. 2) The coefficient of variation (CV), τdecay and half-width of EPSCsNMDAR were significantly larger in the preCP group. 3) A leftward shift in the half-activation voltages in the postCP vs. preCP group. 4) Using subunit-specific antagonists, we found a postnatal shift in NR2 composition towards more NR2A mediated EPSCsNMDAR. These changes occurred within a 2-day narrow window of CP and were similar between fast-spiking (FS) and regular spiking (RSNP) interneurons. 5) Chronic blockage of NR2A, but not NR2B, decreased the expression of parvalbumin (PV), but not other calcium binding proteins in layer 2/3 and 4 of barrel cortex. 6) Chronic blockage of NR2A selectively affected the maturation of IPSCs mediated by FS cells. In summary, we have reported, for the first time, developmental changes in the molecular composition of NMDA NR2 subunits in interneurons during CP, and the effects of chronic blockage of NR2A but not NR2B on PV expression and inhibitory synaptic transmission from FS cells. These results support an important role of NR2A subunits in developmental plasticity of fast-spiking GABAergic circuits during CP.

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Distinct NMDA Receptors Provide Differential Modes of Transmission at Mossy Fiber-Interneuron Synapses

Cited by 139 publications

References 55 publications

Chapter 13 Differential mechanisms of transmission and plasticity at mossy fiber synapses

Chapter 13 Differential mechanisms of transmission and plasticity at mossy fiber synapses

Neurogranin is expressed by principal cells but not interneurons in the rodent and monkey neocortex and hippocampus

Development of NMDA NR2 subunits and their roles in critical period maturation of neocortical GABAergic interneurons

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