Dual modulation of synaptic inhibition by distinct metabotropic glutamate receptors in the rat hippocampus.

Poncer, Jean-Christophe; Shinozaki, Haruhiko; Miles, Richard

doi:10.1113/jphysiol.1995.sp020717

Cited by 134 publications

(90 citation statements)

References 42 publications

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“…In the presynaptic active zone of glutamatergic boutons, mGluR8 is probably an autoreceptor regulating glutamate release (Baskys and Malenka, 1991;Desai et al, 1994;Gereau and Conn, 1995;Scanziani et al, 1998), whereas in GABAergic terminals, it may regulate heterosynaptically GABA release (Gereau and Conn, 1995;Poncer et al, 1995;Morishita et al, 1998;Semyanov and Kullmann, 2000;Kogo et al, 2004). We have shown recently that at 50 M L-AP-4 depressed IPSCs in oriens/ alveus interneurons, including identified O-LM cells (Kogo et al, 2004), consistent with the activation of mGluR8 (Wu et al, 1998;Schoepp et al, 1999;Rosemond et al, 2002).…”

Section: The Role Of Group III Mglurssupporting

confidence: 60%

Metabotropic Glutamate Receptor 8-Expressing Nerve Terminals Target Subsets of GABAergic Neurons in the Hippocampus

Ferraguti¹,

Klausberger²,

Cobden³

et al. 2005

J. Neurosci.

123

138

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Presynaptic metabotropic glutamate receptors (mGluRs) show a highly selective expression and subcellular location in nerve terminals modulating neurotransmitter release. We have demonstrated that alternatively spliced variants of mGluR8, mGluR8a and mGluR8b, have an overlapping distribution in the hippocampus, and besides perforant path terminals, they are expressed in the presynaptic active zone of boutons making synapses selectively with several types of GABAergic interneurons, primarily in the stratum oriens. Boutons labeled for mGluR8 formed either type I or type II synapses, and the latter were GABAergic. Some mGluR8-positive boutons also expressed mGluR7 or vasoactive intestinal polypeptide. Interneurons strongly immunopositive for the muscarinic M2 or the mGlu1 receptors were the primary targets of mGluR8-containing terminals in the stratum oriens, but only neurochemically distinct subsets were innervated by mGluR8-enriched terminals. The majority of M2-positive neurons were mGluR8 innervated, but a minority, which expresses somatostatin, was not. Rare neurons coexpressing calretinin and M2 were consistently targeted by mGluR8-positive boutons. In vivo recording and labeling of an mGluR8-decorated and strongly M2-positive interneuron revealed a trilaminar cell with complex spike bursts during theta oscillations and strong discharge during sharp wave/ripple events. The trilaminar cell had a large projection from the CA1 area to the subiculum and a preferential innervation of interneurons in the CA1 area in addition to pyramidal cell somata and dendrites. The postsynaptic interneuron type-specific expression of the high-efficacy presynaptic mGluR8 in both putative glutamatergic and in identified GABAergic terminals predicts a role in adjusting the activity of interneurons depending on the level of network activity.

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Section: The Role Of Group III Mglurssupporting

confidence: 60%

Metabotropic Glutamate Receptor 8-Expressing Nerve Terminals Target Subsets of GABAergic Neurons in the Hippocampus

Ferraguti¹,

Klausberger²,

Cobden³

et al. 2005

J. Neurosci.

123

138

View full text Add to dashboard Cite

show abstract

“…(Staub, Vranesic & Knopfel, 1992;McBain, DiChiara & Kauer, 1994;Shirasaki, Harata & Akaike, 1994;Poncer, Shinozaki & Miles, 1995). A number of other responses induced by stimulation of mGluRs, such as the reduction in a leak K+ conductance, did not fade with prolonged agonist application (Fig.…”

Section: Hippocampal Slice Culturesmentioning

confidence: 89%

G‐protein‐mediated desensitization of metabotropic glutamatergic and muscarinic responses in CA3 cells in rat hippocampus.

Guérineau

Bossu

Gähwiler

et al. 1997

The Journal of Physiology

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1. Desensitization of a metabotropic response was investigated in CA3 pyramidal neurons in hippocampal slice cultures using the patch‐clamp technique. 2. 1S,3R‐1‐aminocyclopentane‐1,3‐dicarboxylate (1S,3R‐ACPD), an agonist at metabotropic glutamate receptors (mGluRs), and metacholine (MCh), an agonist at muscarinic receptors, induced a cationic current that appears to be activated through a G‐protein‐independent transduction process, as previously shown. Prolonged or repetitive bath application of agonists led to rapid desensitization of the cationic current with a time constant of approximately 20 s. 3. Complete recovery from desensitization was observed within 6 min. 4. These responses mediated by mGluRs and muscarinic receptors cross‐desensitized. 5. Preventing the activation of G‐proteins by loading cells with GDP beta S strongly reduced or suppressed desensitization, and resulted in a sustained inward cationic current. When cells were filled with GTP gamma S to irreversibly activate G‐proteins, the desensitization process was enhanced such that a first application of agonist caused a markedly reduced response. 6. These results show that a cationic current induced by metabotropic agonists in hippocampal pyramidal cells undergoes apparent desensitization and suggests that this process occurs through a G‐protein‐mediated inhibition of the underlying membrane conductance.

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“…Immunohistochemical studies have found mGluR1 to be highly enriched on the soma and dendrites of somatostatin-containing inhibitory interneurons in hippocampus (Baude et al 1993;Ferraguti et al 2004;Hampson et al 1994) as well as on other interneuron subtypes (Ferraguti et al 2004). Activation of group I mGluRs increases the excitability of GABAergic interneurons, both in hippocampus (Mannaioni et al 2001;Mori and Gerber 2002;Poncer et al 1995;Yanovsky et al 1997) and in other brain regions (Chu and Hablitz 1998;Zheng and Johnson 2003). This can cause an increase in the release of GABA (Chu and Hablitz 1998;Mannaioni et al 2001;Mori and Gerber 2002), thus increasing inhibition of pyramidal cells.…”

Section: Location Of Mglur1 Receptors That Reduce Short-term Facilitamentioning

confidence: 99%

Developmental Decrease in Short-Term Facilitation at Schaffer Collateral Synapses in Hippocampus Is mGluR1 Sensitive

Speed

Dobrunz

2008

Journal of Neurophysiology

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Speed HE, Dobrunz LE. Developmental decrease in short-term facilitation at Schaffer collateral synapses in hippocampus is mGluR1 sensitive. J Neurophysiol 99: 799 -813, 2008. First published November 21, 2007 doi:10.1152/jn.00625.2007. Developmental changes can occur in the dynamic properties of synapses, known as short-term plasticity. Using rat acute hippocampal slices at room temperature, we have previously shown a decrease in short-term facilitation at Schaffer collateral synapses from young adults compared with juveniles in response to temporally complex natural stimulus patterns such as synapses receive in vivo. Here we show that this developmental decrease in facilitation is also seen at 32°C and investigate the underlying mechanism. Addition of the mGluR1 antagonist LY367385 increases short-term facilitation in response to the natural stimulus pattern, showing that mGluR1 is activated by synaptically released glutamate. Although synaptic activation of mGluR1 occurs at both ages, the effect is larger in young adults. Furthermore, blocking mGluR1 eliminates most of the developmental decrease in short-term facilitation during the natural stimulus pattern. We investigated possible retrograde/downstream messengers involved after synaptic activation of mGluR1. Blocking cannabinoid receptors has no effect on the response during the natural stimulus pattern, indicating that the reduction in facilitation during synaptic activation of mGluR1 does not occur through release of endocannabinoids. We find that blocking GABA B receptors increases facilitation during the natural stimulus pattern and occludes the effect of the mGluR1 antagonist, indicating a role for the modulation of GABA release from inhibitory interneurons by mGluR1 activation. These data suggest a model where synaptic activation of mGluR1 on inhibitory interneurons causes an increase in GABA release by inhibitory interneurons, which activates GABA B receptors on Schaffer collateral synapses and inhibits shortterm facilitation during the natural stimulus pattern.

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Dual modulation of synaptic inhibition by distinct metabotropic glutamate receptors in the rat hippocampus.

Cited by 134 publications

References 42 publications

Metabotropic Glutamate Receptor 8-Expressing Nerve Terminals Target Subsets of GABAergic Neurons in the Hippocampus

Metabotropic Glutamate Receptor 8-Expressing Nerve Terminals Target Subsets of GABAergic Neurons in the Hippocampus

G‐protein‐mediated desensitization of metabotropic glutamatergic and muscarinic responses in CA3 cells in rat hippocampus.

Developmental Decrease in Short-Term Facilitation at Schaffer Collateral Synapses in Hippocampus Is mGluR1 Sensitive

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