Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission

McBain, Chris J.; DiChiara, Timothy J.; Kauer, Julie A.

doi:10.1523/jneurosci.14-07-04433.1994

Cited by 282 publications

(308 citation statements)

References 41 publications

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“…The presence of the ion current was related to the presence of the agonist; upon removal of the agonist, the ion current returned to baseline. It has previously been reported that bath perfusion of ACPD results in an oscillatory inward current with long latency (ϳ1 min) and slow time course in a subset of interneurons (McBain et al, 1994). Similar ion currents could be evoked using bath application of 100 M ACPD under the conditions used in our experiments (Fig.…”

Section: Oriens-alveus Interneurons Respond Differentially To Mglur Asupporting

confidence: 86%

“…The ACPD-induced inward current is mediated by group I mGluRs ACPD-induced inward currents in oriens-alveus interneurons do not depend on fast synaptic transmission (McBain et al, 1994). In concordance with this finding, Figure 4 A shows that the ACPDinduced inward current is resistant to 1 M TTX.…”

Section: Oriens-alveus Interneurons Respond Differentially To Mglur Asupporting

confidence: 78%

“…It has been shown before that bath application of ACPD evokes large, oscillatory inward currents in a subset of oriensalveus interneurons, which innervate stratum lacunosummoleculare (McBain et al, 1994;Woodhall et al, 1999). In addition, another subset of interneurons, which innervate somata and proximal dendrites of CA1 pyramidal neurons, respond with a small, non-oscillatory inward current upon bath application of ACPD (McBain et al, 1994).…”

Section: Discussionmentioning

confidence: 96%

“…In addition, another subset of interneurons, which innervate somata and proximal dendrites of CA1 pyramidal neurons, respond with a small, non-oscillatory inward current upon bath application of ACPD (McBain et al, 1994). These two subsets of interneurons appear identical to type I and type III interneurons.…”

Section: Discussionmentioning

confidence: 97%

“…Group I mGluRs are G-protein-coupled receptors, and activation results in release of Ca 2ϩ from intracellular stores via an inositol triphosphate/Ca 2ϩ signal transduction mechanism (Carment et al, 1997;Nakanishi et al, 1998). It has been suggested that the molecular basis of the inward currents evoked by activation of mGluRs is an electrogenic Na ϩ -Ca 2ϩ exchanger that is activated upon release from intracellular Ca 2ϩ (Staub et al, 1992;McBain et al, 1994;Lee and Boden, 1997). Hence, one possible explanation for the nonresponsiveness of type IV interneurons upon mGluR activation could reside in the absence or the later maturation of the effector molecule (e.g., Na ϩ -Ca 2ϩ exchanger) in these interneurons.…”

Section: Discussionmentioning

confidence: 99%

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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: Oriens-alveus Interneurons Respond Differentially To Mglur Asupporting

confidence: 86%

Section: Oriens-alveus Interneurons Respond Differentially To Mglur Asupporting

confidence: 78%

Section: Discussionmentioning

confidence: 96%

Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

See 3 more Smart Citations

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

et al. 2000

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Immunostaining for substance P receptor labels GABAergic cells with distinct termination patterns in the hippocampus

et al. 1997

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A specific antiserum against substance P receptor (SPR) labels nonprincipal neurons in the cerebral cortex of the rat (T. Kaneko et al. [1994], Neuroscience 60:199-211; Y. Nakaya et al. [1994], J. Comp. Neurol. 347:249-274). In the present study, we aimed to identify the types of SPR-immunoreactive neurons in the hippocampus according to their content of neurochemical markers, which label interneuron populations with distinct termination patterns. Markers for perisomatic inhibitory cells, parvalbumin and cholecystokinin (CCK), colocalized with SPR in pyramidallike basket cells in the dentate gyrus and in large multipolar or bitufted cells within all hippocampal subfields respectively. A dense meshwork of SPR-immunoreactive spiny dendrites in the hilus and stratum lucidum of the CA3 region belonged largely to inhibitory cells terminating in the distal dendritic region of granule cells, as indicated by the somatostatin and neuropeptide Y (NPY) content. In addition, SPR and NPY were colocalized in numerous multipolar interneurons with dendrites branching close to the soma. Twenty-five percent of the SPR-immunoreactive cells overlapped with calretinin-positive neurons in all hippocampal subfields, showing that interneurons specialized to contact other gamma-aminobutyric acid-ergic cells may also contain SPR. On the basis of the known termination pattern of the colocalized markers, we conclude that SPR-positive interneurons are functionally heterogeneous and participate in different inhibitory processes: (1) perisomatic inhibition of principal cells (CCK-containing cells, and parvalbumin-positive cells in the dentate gyrus), (2) feedback dendritic inhibition in the entorhinal termination zone (somatostatin and NPY-containing cells), and (3) innervation of other interneurons (calretinin-containing cells).

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Light and electron microscopic demonstration of mGluR5 metabotropic glutamate receptor immunoreactive neuronal elements in the rat cerebellar cortex

et al. 1997

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The cellular and subcellular localization of the mGluR5 metabotropic glutamate receptor subtype was studied in the rat cerebellar cortex, by using the preembedding immunoperoxidase and immunogold techniques. Light microscopic observations revealed an abundant, intense labeling of neurons in the granular layer as well as in the molecular layer. Lugaro and Golgi cells exhibited an intense mGluR5 immunoreactivity, while only a fraction of the neurons in the molecular layer were found to be mGluR5 immunopositive. In addition to a dense plexus of immunoreactive dendrites in the molecular layer of the cerebellar cortex, the mGluR5 immunopositive Golgi cell dendrites resembling axons at the light microscopic level were also labeled in the granular layer. At the ultrastructural level, mGluR5 immunoreactivity was present in neuronal elements postsynaptic to axon terminals of different morphology. By using a pre-embedding immunogold method, it was found that mGluR5 immunoreactivity is accumulated at the plasma membranes extrasynaptically as well as at the periphery of the postsynaptic specializations, mainly of the parallel fiber synaptic contacts. These findings provide morphological evidence that mGluR5 is expressed by a population of neurons in the cerebellar cortex and can synaptically be activated via the parallel fiber system.

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Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission

Cited by 282 publications

References 41 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

Immunostaining for substance P receptor labels GABAergic cells with distinct termination patterns in the hippocampus

Light and electron microscopic demonstration of mGluR5 metabotropic glutamate receptor immunoreactive neuronal elements in the rat cerebellar cortex

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