The Role of AMPA Receptor Gating in the Development of High-Fidelity Neurotransmission at the Calyx of Held Synapse

Joshi, Indu; Shokralla, Shahira; Titis, Paul; Wang, Lu-Yang

doi:10.1523/jneurosci.1074-03.2004

Cited by 85 publications

(122 citation statements)

References 69 publications

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“…The calyx of Held synapse, at maturity, is capable of phaselocking postsynaptic firing to presynaptic input at high rates, as a result of multiple adaptations (Wang and Kaczmarek, 1998;Trussell 1999;Joshi and Wang, 2002;von Gersdorff and Borst, 2002;Joshi et al, 2004). In line with previous evidence showing a developmental increase in the efficiency of exocytosis (Taschenberger et al, 2002), we suggest that tight coupling between VGCCs and vesicles may represent a critical adaptation that ensures a strong synaptic drive for high-fidelity neurotransmission with minimal jitter in synaptic delay.…”

Section: Discussionsupporting

confidence: 85%

Developmental Transformation of the Release Modality at the Calyx of Held Synapse

Fedchyshyn¹,

Wang²

2005

J. Neurosci.

267

326

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] o and was independent of postsynaptic receptor desensitization. We demonstrated that release from P8 -P12 terminals involved both N-and P/Q-type VGCCs, but P/Q-type-associated release sites specifically displayed low m values. These results suggest a developmental transformation of the release modality from "microdomain," involving cooperative action of many loosely coupled N-and P/Q-type VGCCs, to "nanodomain," in which opening of fewer tightly coupled P/Q-type VGCCs effectively induce a fusion event. Spatial tightening improves the release efficiency and is likely a critical step for the development of high-fidelity neurotransmission in this and other central synapses.

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Section: Discussionsupporting

confidence: 85%

Developmental Transformation of the Release Modality at the Calyx of Held Synapse

Fedchyshyn¹,

Wang²

2005

J. Neurosci.

267

326

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“…2 D) ( p Ͻ 0.01). These results are similar to those reported recently in mice (Joshi et al, 2004). From P14 to P21, however, neither the desensitization time constants nor the deactivation time constant changed significantly (Fig.…”

Section: Developmental Speeding Of Desensitization and Deactivationsupporting

confidence: 92%

“…In contrast, Joshi et al (2004) reported that GluR2 immunoreactivity is virtually absent in MNTB neurons in mice throughout development (P5-P18). Consistent with GluR2 deficiency, in mice the current-voltage relationship of AMPA-EPSCs shows a strong rectification with little outward current in the presence of intracellular spermine in the MNTB neurons (Joshi et al, 2004). In contrast, in rats GluR2 immunoreactivity was present throughout development both in the synaptic and extrasynaptic regions of MNTB neurons (supplemental Fig.…”

Section: Developmental Changes In the Glur Transcriptsmentioning

confidence: 88%

“…However, in MNTB neurons, despite abundant GluR flop variants throughout development, desensitization of AMPAR currents was dramatically reduced by CTZ. At the mouse calyx of Held, Joshi et al (2004) postulated that a shift in the dominance of AMPAR subunit from GluR1 to GluR3/4 may account for the developmental speeding of AMPA-EPSC kinetics. Although our RT-PCR results are consistent with the results of immunoreactivity by Joshi et al (2004) regarding the developmental decrease in GluR1 and increase in GluR4, our results indicate that developmental speeding of the AMPA-EPSC kinetics cannot simply be attributed to the switch of AMPAR subunits.…”

Section: Developmental Changes In the Glur Transcriptsmentioning

confidence: 99%

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Mechanisms Underlying Developmental Speeding in AMPA-EPSC Decay Time at the Calyx of Held

Koike-Tani

Saitoh²,

Takahashi³

2005

J. Neurosci.

116

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The time course of synaptic conductance is important in temporal precision of information processing in the neuronal network. The AMPA receptor (AMPAR)-mediated EPSCs at the calyx of Held become faster in decay time as animals mature. To clarify how desensitization and deactivation of AMPARs contribute to developmental speeding of EPSCs, we compared the decay time of quantal EPSCs (qEPSCs) with the deactivation and desensitization times of AMPAR currents induced in excised patches by fast glutamate application (AMPA patch currents). Both the deactivation and desensitization times of AMPA patch currents became markedly faster from postnatal day 7 (P7) to P14 and changed little thereafter. In individual neurons, throughout development (P7-P21), the time constants of deactivation and fast desensitization in AMPA patch currents were similar to each other and close to the qEPSC decay time constant. Cyclothiazide (CTZ) abolished the fast desensitization, prolonged deactivation of AMPA patch currents, and slowed the decay time of EPSCs. The effects of CTZ on AMPA patch currents were unchanged throughout development, whereas its effect on EPSCs became weaker as animals matured. In single-cell reverse transcription-PCR analysis, glutamate receptor subunit 4 (GluR4) flop increased from P7 to P14 and changed little thereafter. At P7, the GluR4 flop abundance had an inverse correlation with the qEPSC decay time. These results together suggest that both desensitization and deactivation of AMPARs are involved in the EPSC decay time, but the contribution of desensitization decreases during postnatal development at the calyx of Held.

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“…Such differences in the decay or deactivation of NGIC responses can profoundly impact the window of synaptic excitability and integration (4,7,8). Control over NGIC kinetics is also a powerful force during development, where slower receptor subtypes tend to be used early on, broadening the window of plasticity during critical periods, and later give way to faster decaying subunits providing greater temporal precision (9)(10)(11)(12)(13). This trade-off between the window of integration on the one hand and temporal precision on the other persists in the mature brain.…”

mentioning

confidence: 99%

Deactivation kinetics of acid-sensing ion channel 1a are strongly pH-sensitive

MacLean

Jayaraman

2017

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

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Acid-sensing ion channels (ASICs) are trimeric cation-selective ion channels activated by protons in the physiological range. Recent reports have revealed that postsynaptically localized ASICs contribute to the excitatory postsynaptic current by responding to the transient acidification of the synaptic cleft that accompanies neurotransmission. In response to such brief acidic transients, both recombinant and native ASICs show extremely rapid deactivation in outside-out patches when jumping from a pH 5 stimulus to a single resting pH of 8. Given that the resting pH of the synaptic cleft is highly dynamic and depends on recent synaptic activity, we explored the kinetics of ASIC1a and 1a/2a heteromers to such brief pH transients over a wider [H + ] range to approximate neuronal conditions better. Surprisingly, the deactivation of ASICs was steeply dependent on the pH, spanning nearly three orders of magnitude from extremely fast (<1 ms) at pH 8 to very slow (>300 ms) at pH 7. This study provides an example of a ligand-gated ion channel whose deactivation is sensitive to agonist concentrations that do not directly activate the receptor. Kinetic simulations and further mutagenesis provide evidence that ASICs show such steeply agonist-dependent deactivation because of strong cooperativity in proton binding. This capacity to signal across such a large synaptically relevant bandwidth enhances the response to smallamplitude acidifications likely to occur at the cleft and may provide ASICs with the ability to shape activity in response to the recent history of the synapse.acid-sensing ion channel | gating | kinetics | ligand-gated ion channel N eurotransmitter levels within the synaptic cleft rise and fall very rapidly, with clearance times generally on the order of a few hundred microseconds to 2 ms (1-3). However, the duration of responses from neurotransmitter-gated ion channels (NGICs) varies widely across several orders of magnitude depending on the receptors involved. For example, in certain regions, glutamatergic excitatory postsynaptic currents (EPSCs) decay with submillisecond time constants (4), but the EPSCs of GluN2D-containing NMDA receptors decay over roughly 200 ms (5, 6). Such differences in the decay or deactivation of NGIC responses can profoundly impact the window of synaptic excitability and integration (4,7,8). Control over NGIC kinetics is also a powerful force during development, where slower receptor subtypes tend to be used early on, broadening the window of plasticity during critical periods, and later give way to faster decaying subunits providing greater temporal precision (9-13). This trade-off between the window of integration on the one hand and temporal precision on the other persists in the mature brain. There, synapses host an NGIC compliment kinetically suited to their input patterns (14) but are also capable of dynamically shifting between the priorities of integration and precision (8). Unsurprisingly then, influencing the deactivation kinetics of specific NGIC subtypes using allosteri...

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The Role of AMPA Receptor Gating in the Development of High-Fidelity Neurotransmission at the Calyx of Held Synapse

Cited by 85 publications

References 69 publications

Developmental Transformation of the Release Modality at the Calyx of Held Synapse

Developmental Transformation of the Release Modality at the Calyx of Held Synapse

Mechanisms Underlying Developmental Speeding in AMPA-EPSC Decay Time at the Calyx of Held

Deactivation kinetics of acid-sensing ion channel 1a are strongly pH-sensitive

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