Action Potential-Independent Release of Glutamate by Ca<sup>2+</sup>Entry through Presynaptic P2X Receptors Elicits Postsynaptic Firing in the Brainstem Autonomic Network

Shigetomi, Eiji; Kato, Fusao

doi:10.1523/jneurosci.0090-04.2004

Cited by 108 publications

(79 citation statements)

References 51 publications

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“…In this case, the general P2 receptor agonist ATP and the P2X1,3 selective agonist α,β-meATP had comparable activities, indicating the involvement of pain-relevant, presynaptic P2X3 receptors [24]. Later on, an ATP-induced facilitation of the sEPSC frequency was demonstrated also for glutamatergically innervated autonomic nuclei in the medulla oblongata [25][26][27]. In these experiments, the omission of Ca 2+ from the bath solution blocked the action of ATP, whereas the pharmacological inhibition of voltage-gated Ca 2+ channels (VGCCs) was ineffective.…”

Section: Discussionmentioning

confidence: 96%

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Potentiation of the glutamatergic synaptic input to rat locus coeruleus neurons by P2X7 receptors

Khakpay

Polster

Köles

et al. 2010

Purinergic Signalling

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Locus coeruleus (LC) neurons in a rat brain slice preparation were superfused with a Mg 2+ -free and bicuculline-containing external medium. Under these conditions, glutamatergic spontaneous excitatory postsynaptic currents (sEPSCs) were recorded by means of the whole-cell patch-clamp method. ATP, as well as its structural analogue 2-methylthio ATP (2-MeSATP), both caused transient inward currents, which were outlasted by an increase in the frequency but not the amplitude of the sEPSCs. PPADS, but not suramin or reactive blue 2 counteracted both effects of 2-MeSATP. By contrast, α,β-methylene ATP (α,β-meATP), UTP and BzATP did not cause an inward current response. Of these latter agonists, only BzATP slightly facilitated the sEPSC amplitude and strongly potentiated its frequency. PPADS and Brilliant Blue G, as well as fluorocitric acid and aminoadipic acid prevented the activity of BzATP. Furthermore, BzATP caused a similar facilitation of the miniature (m)EPSC (recorded in the presence of tetrodotoxin) and sEPSC frequencies (recorded in its absence). Eventually, capsaicin augmented the frequency of the sEPSCs in a capsazepine-, but not PPADS-antagonizable, manner. In conclusion, the stimulation of astrocytic P2X7 receptors appears to lead to the outflow of a signalling molecule, which presynaptically increases the spontaneous release of glutamate onto LC neurons from their afferent fibre tracts. It is suggested, that the two algogenic compounds ATP and capsaicin utilise separate receptor systems to potentiate the release of glutamate and in consequence to increase the excitability of LC neurons.

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Section: Discussionmentioning

confidence: 96%

“…Moreover, the role of P2Y receptors, whose effect is known to be independent of extracellular Ca 2+ was excluded by these experiments. In some, but not all cases, P2X3 receptors appeared to mediate the ATP effect, since α,β-meATP mimicked and preferential P2X3 receptor antagonists such as TNP-ATP [26] or A-317491 [27] antagonised it.…”

Section: Discussionmentioning

confidence: 99%

Potentiation of the glutamatergic synaptic input to rat locus coeruleus neurons by P2X7 receptors

Khakpay

Polster

Köles

et al. 2010

Purinergic Signalling

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“…However, it seems that the ATP released in the NTS following HDA stimulation additionally acts on local P2 receptors, either inducing a release of glutamate by acting on receptors in the presynaptic terminals [22,23] or being co-released with glutamate in the presynaptic membrane [31][32][33][34]. Interestingly, both antagonists suramin and kynurenate injected in to the NTS did not reduce the responses in AP and HR evoked by Fig.…”

Section: Hindlimb Vasodilation In Alerting-defense Responses Is Mediamentioning

confidence: 92%

“…In the NTS, ATP apparently acts as a neuromodulator interacts with terminals promoting glutamate release [21], thus altering sympathetic nerve discharge. In fact, in vitro activation of purinergic P2 receptors located in the presynaptic membrane produces release of glutamate in the neuron terminal observed [22,23].…”

Section: Introductionmentioning

confidence: 99%

Interaction of medullary P2 and glutamate receptors mediates the vasodilation in the hindlimb of rat

Korim

Ferreira-Neto

Pedrino

et al. 2012

Purinergic Signalling

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In the nucleus tractus solitarii (NTS) of rats, blockade of extracellular ATP breakdown to adenosine reduces arterial blood pressure (AP) increases that follow stimulation of the hypothalamic defense area (HDA). The effects of ATP on NTS P2 receptors, during stimulation of the HDA, are still unclear. The aim of this study was to determine whether activation of P2 receptors in the NTS mediates cardiovascular responses to HDA stimulation. Further investigation was taken to establish if changes in hindlimb vascular conductance (HVC) elicited by electrical stimulation of the HDA, or activation of P2 receptors in the NTS, are relayed in the rostral ventrolateral medulla (RVLM); and if those responses depend on glutamate release by ATP acting on presynaptic terminals. In anesthetized and paralyzed rats, electrical stimulation of the HDA increased AP and HVC. Blockade of P2 or glutamate receptors in the NTS, with bilateral microinjections of suramin (10 mM) or kynurenate (50 mM) reduced only the evoked increase in HVC by 75 % or more. Similar results were obtained with the blockade combining both antagonists. Blockade of P2 and glutamate receptors in the RVLM also reduced the increases in HVC to stimulation of the HDA by up to 75 %. Bilateral microinjections of kynurenate in the RVLM abolished changes in AP and HVC to injections of the P2 receptor agonist α,β-methylene ATP (20 mM) into the NTS. The findings suggest that HDA-NTS-RVLM pathways in control of HVC are mediated by activation of P2 and glutamate receptors in the brainstem in alerting-defense reactions.

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“…Transverse brainstem slices from Wistar rats (2-5 weeks) were prepared according to a method described previously [48,49]. Briefly, following the decapitation under sufficient anesthesia with overdose ketamine (100-150 mg kg -1 , i.p.…”

Section: Methodsmentioning

confidence: 99%

Distinct target cell-dependent forms of short-term plasticity of the central visceral afferent synapses of the rat

et al. 2010

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Background The visceral afferents from various cervico-abdominal sensory receptors project to the dorsal vagal complex (DVC), which is composed of the nucleus of the solitary tract (NTS), the area postrema and the dorsal motor nucleus of the vagus nerve (DMX), via the vagus and glossopharyngeal nerves and then the solitary tract (TS) in the brainstem. While the excitatory transmission at the TS-NTS synapses shows strong frequency-dependent suppression in response to repeated stimulation of the afferents, the frequency dependence and short-term plasticity at the TS-DMX synapses, which also transmit monosynaptic information from the visceral afferents to the DVC neurons, remain largely unknown. Results Recording of the EPSCs activated by paired or repeated TS stimulation in the brainstem slices of rats revealed that, unlike NTS neurons whose paired-pulse ratio (PPR) is consistently below 0.6, the distribution of the PPR of DMX neurons shows bimodal peaks that are composed of type I (PPR, 0.6-1.5; 53% of 120 neurons recorded) and type II (PPR, < 0.6; 47%) neurons. Some of the type I DMX neurons showed paired-pulse potentiation. The distinction of these two types depended on the presynaptic release probability and the projection target of the postsynaptic cells; the distinction was not dependent on the location or soma size of the cell, intensity or site of the stimulation, the latency, standard deviation of latency or the quantal size. Repeated stimulation at 20 Hz resulted in gradual and potent decreases in EPSC amplitude in the NTS and type II DMX neurons, whereas type I DMX neurons displayed only slight decreases, which indicates that the DMX neurons of this type could be continuously activated by repeated firing of primary afferent fibers at a high (~10 Hz) frequency. Conclusions These two general types of short-term plasticity might contribute to the differential activation of distinct vago-vagal reflex circuits, depending on the firing frequency and type of visceral afferents.

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Action Potential-Independent Release of Glutamate by Ca²⁺Entry through Presynaptic P2X Receptors Elicits Postsynaptic Firing in the Brainstem Autonomic Network

Cited by 108 publications

References 51 publications

Potentiation of the glutamatergic synaptic input to rat locus coeruleus neurons by P2X7 receptors

Potentiation of the glutamatergic synaptic input to rat locus coeruleus neurons by P2X7 receptors

Interaction of medullary P2 and glutamate receptors mediates the vasodilation in the hindlimb of rat

Distinct target cell-dependent forms of short-term plasticity of the central visceral afferent synapses of the rat

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Action Potential-Independent Release of Glutamate by Ca2+Entry through Presynaptic P2X Receptors Elicits Postsynaptic Firing in the Brainstem Autonomic Network

Cited by 108 publications

References 51 publications

Potentiation of the glutamatergic synaptic input to rat locus coeruleus neurons by P2X7 receptors

Potentiation of the glutamatergic synaptic input to rat locus coeruleus neurons by P2X7 receptors

Interaction of medullary P2 and glutamate receptors mediates the vasodilation in the hindlimb of rat

Distinct target cell-dependent forms of short-term plasticity of the central visceral afferent synapses of the rat

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Action Potential-Independent Release of Glutamate by Ca²⁺Entry through Presynaptic P2X Receptors Elicits Postsynaptic Firing in the Brainstem Autonomic Network