Calcium release via activation of presynaptic IP3 receptors contributes to kainate-induced IPSC facilitation in rat neocortex

Mathew, Seena S.; Hablitz, John J.

doi:10.1016/j.neuropharm.2008.05.005

Cited by 31 publications

(26 citation statements)

References 71 publications

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“…A similar mechanism thus appears to be triggered in VP neurons when postsynaptic Ca 2ϩ -permeable Gluk1-containing KARs are activated, leading to the Ca 2ϩ -dependent release of a retrograde signal. Our data, however, do not allow us to assess whether the entry of Ca 2ϩ through GluK1-containing KARs is sufficient by itself to induce the release of dynorphin or whether other mechanisms, such as Ca 2ϩ release from intracellular stores, also contribute to this process (Lauri et al, 2003;Mathew and Hablitz, 2008;Scott et al, 2008).…”

Section: Indirect Inhibitory Action Of Kars On Glutamatergic Inputs Tmentioning

confidence: 75%

“…4C,D). We next assessed whether the GluK1 receptors located on VP neurons were permeable to Ca 2ϩ (Lauri et al, 2003;Pinheiro et al, 2007;Mathew and Hablitz., 2008;Sun et al, 2009). In agreement with this hypothesis, we observed that a blocker of Ca 2ϩ -permeable AMPA/KAR, PhTx (3 M) (Fletcher and Lodge, 1996), inhibited glutamate-evoked response obtained in the presence of D-AP-5 (50 M) and NBQX (1 M) to the same extent as UBP302 (43.1 Ϯ 5.4%; n ϭ 7; p Ͻ 0.05), whereas it has no effect in OT neurons (98.1 Ϯ 3.1%; n ϭ 11; p Ͼ 0.05) (Fig.…”

Section: Postsynaptic Kars In Ot and Vp Neuronsmentioning

confidence: 99%

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Kainate Receptor-Induced Retrograde Inhibition of Glutamatergic Transmission in Vasopressin Neurons

Bonfardin

Theodosis²,

Konnerth³

et al. 2012

J. Neurosci.

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Presynaptic kainate receptors (KARs) exert a modulatory action on transmitter release. We here report that applications of agonists of GluK1-containing KARs in the rat supraoptic nucleus has an opposite action on glutamatergic transmission according to the phenotype of the postsynaptic neuron. Whereas glutamate release was facilitated in oxytocin (OT) neurons, it was inhibited in vasopressin (VP) cells. Interestingly, an antagonist of GluK1-containing KARs caused an inhibition of glutamate release in both OT and VP neurons, revealing the existence of tonically activated presynaptic KARs that are positively coupled to transmitter release. We thus postulated that the inhibition of glutamate release observed with exogenous applications of GluK1 agonists on VP neurons could be indirect. In agreement with this hypothesis, we first showed that functional GluK1-containing KARs were present postsynaptically on VP neurons but not on OT cells. We next showed that the inhibitory effect induced by exogenous GluK1 receptor agonist was compromised when BAPTA was added in the recording pipette to buffer intracellular Ca 2ϩ and block the release of a putative retrograde messenger. Under these conditions, GluK1-containing KAR agonist facilitates glutamatergic transmission in VP neurons in a manner similar to that observed for OT neurons and that resulted from the activation of presynaptic GluK1 receptors. GluK1-mediated inhibition of glutamate release in VP neurons was also blocked by a -opioid receptor antagonist. These findings suggest that activation of postsynaptic GluK1-containing KARs on VP neurons leads to the release of dynorphin, which in turn acts on presynaptic -opioid receptors to inhibit glutamate release.

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Section: Indirect Inhibitory Action Of Kars On Glutamatergic Inputs Tmentioning

confidence: 75%

Section: Postsynaptic Kars In Ot and Vp Neuronsmentioning

confidence: 99%

Kainate Receptor-Induced Retrograde Inhibition of Glutamatergic Transmission in Vasopressin Neurons

Bonfardin

Theodosis²,

Konnerth³

et al. 2012

J. Neurosci.

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“…Furthermore, Ϸ40% of GAD65/67-positive terminals also expressed the glutamate receptor subunit GluR5, a component of non-NMDA receptors, in mechanically dissociated preparations (4). Indeed, the activation of GABAergic terminals by glutamate could be a widespread mechanism, as a similar facilitatory effect on the release of GABA mediated by kainate receptors has also been described in the prefontal cortex (26,27). We must also consider the possibility that the diffusing glutamate (and other compounds) may reach the inhibitory PSD, and not just the cell membrane of the terminal, evoking the release of GABA.…”

Section: Discussionmentioning

confidence: 95%

Proximity of excitatory and inhibitory axon terminals adjacent to pyramidal cell bodies provides a putative basis for nonsynaptic interactions

Merchán-Pérez

Toledo-Rodriguez

Ribak

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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Although pyramidal cells are the main excitatory neurons in the cerebral cortex, it has recently been reported that they can evoke inhibitory postsynaptic currents in neighboring pyramidal neurons. These inhibitory effects were proposed to be mediated by putative axo-axonic excitatory synapses between the axon terminals of pyramidal cells and perisomatic inhibitory axon terminals [Ren M, Yoshimura Y, Takada N, Horibe S, Komatsu Y (2007) Science 316:758 -761]. However, the existence of this type of axo-axonic synapse was not found using serial section electron microscopy. Instead, we observed that inhibitory axon terminals synapsing on pyramidal cell bodies were frequently apposed by terminals that established excitatory synapses with neighbouring dendrites. We propose that a spillover of glutamate from these excitatory synapses can activate the adjacent inhibitory axo-somatic terminals.axo-axonic synapses ͉ glutamate spillover ͉ interpyramidal inhibition ͉ perisomatic innervation ͉ serial electron microscopy P yramidal cells are the most abundant cortical neurons and although they are projection neurons, their axons give rise to axonal collaterals before leaving the cortex, producing a rich local intracortical plexus (1). In general, the pyramidal cell's soma and axon initial segment receive only symmetric (inhibitory) synapses from axon terminals of GABAergic interneurons, whereas its dendrites receive synaptic inputs from axon terminals forming both symmetric and asymmetric (excitatory) synapses. The latter type of synapse is mainly located on dendritic spines and such synapses arise from multiple intrinsic and extrinsic sources (2). Many studies have shown that pyramidal neurons are glutamatergic and that they exert a fundamental excitatory function in cortical circuits (3). Indeed, these neurons represent the primary source of cortical excitatory synapses, and in turn, dendritic spines of pyramidal cells are the target of most excitatory synapses (2).This traditional view has recently been challenged by the discovery that pyramidal neurons in layer II/III of the mouse visual cortex exert an inhibitory influence on neighboring pyramidal cells through the direct activation of inhibitory GABAergic axon terminals forming axo-somatic synapses (4) (referred to here as ''axo-somatic terminals''). Thus, singleaction potentials generated in a pyramidal neuron can produce inhibitory postsynaptic currents (IPSCs) in nearby pyramidal cells with short latencies, which are in many cases comparable to monosynaptic connections. These responses are abolished by both non-NMDA and GABA A receptor antagonists, suggesting that they are disynaptic. Other electrophysiological and pharmacological evidence makes it unlikely that these IPSCs are mediated by the conventional activation of inhibitory interneurons, generating somatic action potentials that subsequently spread through the axonal tree. Instead, they seem to take place in the immediate vicinity of the pyramidal cell body.Because these data imply a very close relationship b...

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“…This finding demonstrates that under certain circumstances, activation of presynaptic GluK1-containing KARs stimulates a metabotropic pathway leading to a decrease in GABA release probability. That facilitation and inhibition of GABA transmission involve an ionotropic and a metabotropic mechanism, respectively, has been already demonstrated in other structures (Rodríguez-Moreno and Lerma, 1998;Jin and Smith, 2007;Mathew and Hablitz, 2008). However, these observations were made separately from each other.…”

Section: Coexistence Of Ionotropic and Metabotropic Kar Modes Of Actionmentioning

confidence: 88%

Glia-Dependent Switch of Kainate Receptor Presynaptic Action

Bonfardin

Fossat²,

Theodosis³

et al. 2010

J. Neurosci.

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Presynaptic kainate receptors (KARs) exert a modulatory action on transmitter release. This effect can be switched from facilitation to inhibition by an increased concentration of KAR agonists. We here report that activation of presynaptic GluK1-containing KARs facilitates GABA release on oxytocin and vasopressin neurons in the supraoptic nucleus of the hypothalamus. Increase in ambient levels of glutamate associated with the physiological reduction of astrocytic coverage of oxytocin neurons in lactating rats switches this KARmediated facilitation to inhibition of GABAergic transmission. This effect was reproduced in both oxytocin and vasopressin neurons of virgin rats when glutamate transporters were blocked pharmacologically, thereby establishing that enhanced levels of extracellular glutamate induce the switch in KAR-mediated action. The facilitation of GABA release was inhibited with philanthotoxin, a Ca 2ϩ -permeable KAR antagonist, suggesting that this effect was associated with an ionotropic mode of action. Conversely, KAR-mediated inhibition was compromised in the presence of U73122, a phospholipase C inhibitor, in agreement with the involvement of a metabotropic pathway. We thus reveal that physiological astrocytic plasticity modifies the mode of action of presynaptic KARs, thereby inversing their coupling with GABA release.

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Calcium release via activation of presynaptic IP3 receptors contributes to kainate-induced IPSC facilitation in rat neocortex

Cited by 31 publications

References 71 publications

Kainate Receptor-Induced Retrograde Inhibition of Glutamatergic Transmission in Vasopressin Neurons

Kainate Receptor-Induced Retrograde Inhibition of Glutamatergic Transmission in Vasopressin Neurons

Proximity of excitatory and inhibitory axon terminals adjacent to pyramidal cell bodies provides a putative basis for nonsynaptic interactions

Glia-Dependent Switch of Kainate Receptor Presynaptic Action

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