Developmental Expression of Ca<sup>2+</sup>-Permeable AMPA Receptors Underlies Depolarization-Induced Long-Term Depression at Mossy Fiber–CA3 Pyramid Synapses

Ho, Michelle Tsz-Wan; Pelkey, Kenneth A.; Topolnik, Lisa; Petralia, Ronald S.; Takamiya, Kogo; Xia, Jun; Huganir, Richard L.; Lacaille, Jean-Claude; McBain, Chris J.

doi:10.1523/jneurosci.2671-07.2007

Cited by 93 publications

(105 citation statements)

References 74 publications

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“…This result is consistent with predominant expression of GluA4 'flip' during early development (Monyer et al, 1991). Additionally, the data suggest that the observed developmental increase in the decay time of AMPA EPSCs depends on mechanisms that operate in the absence of GluA4, such as alternative splicing (Monyer et al, 1991), heteromerization with GluA2 (Kumar et al 2002, Ho et al 2007 or increased dendritic filtering (Hausser and Roth, 1997).…”

Section: Maturation Of Ampar-mediated Transmission Is Perturbed In Thsupporting

confidence: 66%

Molecular mechanisms controlling synaptic recruitment of GluA4 subunit-containing AMPA-receptors critical for functional maturation of CA1 glutamatergic synapses

et al. 2017

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Synaptic recruitment of AMPA receptors (AMPARs) represents a key postsynaptic mechanism driving functional development and maturation of glutamatergic synapses. At immature hippocampal synapses, PKA-driven synaptic insertion of GluA4 is the predominant mechanism for synaptic reinforcement. However, the physiological significance and molecular determinants of this developmentally restricted form of plasticity are not known. Here we show that PKA activation leads to insertion of GluA4 to synaptic sites with initially weak or silent AMPAR-mediated transmission. This effect depends on a novel mechanism involving the extreme C-terminal end of GluA4, which interacts with the membrane proximal region of the C-terminal domain to control GluA4 trafficking. In the absence of GluA4, strengthening of AMPAR-mediated transmission during postnatal development was significantly delayed. These data suggest that the GluA4-mediated activation of silent synapses is a critical mechanism facilitating the functional maturation of glutamatergic circuitry during the critical period of experience-dependent fine-tuning.

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Section: Maturation Of Ampar-mediated Transmission Is Perturbed In Thsupporting

confidence: 66%

Molecular mechanisms controlling synaptic recruitment of GluA4 subunit-containing AMPA-receptors critical for functional maturation of CA1 glutamatergic synapses

et al. 2017

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“…To determine the rectification index (RI), a straight line was fitted to the data points for negative voltages. The RI was taken as the amplitude ratio of the actual current at 50 mV divided by the linearly extrapolated value (Ho et al, 2007).…”

Section: Methodsmentioning

confidence: 99%

“…Previous experiments showed that CPAMPARs can be incorporated into active synapses (Takahashi et al, 2003;Clem and Barth, 2006;Plant et al, 2006;Zhu 2009), which may tag those for additional modifications. In hippocampal CA3 pyramidal cells, CP-AMPARs are selectively removed at mossy fiber synapses by postsynaptic depolarizations (Ho et al, 2007). A recent study showed that the slope of field potentials and the expression of AMPA receptor subunit proteins depend on the wake state of the animal (Vyazovskiy et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Removal of Synaptic Ca²⁺-Permeable AMPA Receptors during Sleep

Lanté

Toledo-Salas²,

Ondrejčák³

et al. 2011

J. Neurosci.

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There is accumulating evidence that sleep contributes to memory formation and learning, but the underlying cellular mechanisms are incompletely understood. To investigate the impact of sleep on excitatory synaptic transmission, we obtained whole-cell patch-clamp recordings from layer V pyramidal neurons in acute slices of somatosensory cortex of juvenile rats (postnatal days 21-25). In animals after the dark period, philanthotoxin 74 (PhTx)-sensitive calcium-permeable AMPA receptors (CP-AMPARs) accounted for ϳ25% of total EPSP size, and current-voltage (I-V) relationships of the underlying EPSCs showed inward rectification. In contrast, in similar experiments after the light period, EPSPs were PhTx insensitive with linear I-V characteristics, indicating that CP-AMPARs were less abundant. Combined EEG and EMG recordings confirmed that slow-wave sleep-associated delta wave power peaked at the onset of the more quiescent, lights-on phase of the cycle. Subsequently, we show that burst firing, a characteristic action potential discharge mode of layer V pyramidal neurons during slow-wave sleep has a dual impact on synaptic AMPA receptor composition: repetitive burst firing without synaptic stimulation eliminated CP-AMPARs by activating serine/threonine phosphatases. Additionally, repetitive burst-firing paired with EPSPs led to input-specific long-term depression (LTD), affecting Ca 2ϩ impermeable AMPARs via protein kinase C signaling. In agreement with two parallel mechanisms, simple bursts were ineffective after the light period but paired bursts induced robust LTD. In contrast, incremental LTD was generated by both conditioning protocols after the dark cycle. Together, our results demonstrate qualitative changes at neocortical glutamatergic synapses that can be induced by discharge patterns characteristic of non-rapid eye movement sleep.

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“…It has been demonstrated previously that PICK1 mediates certain GluA2-dependent trafficking events (Terashima et al, 2004;Ho et al, 2007;Dixon et al, 2009). We therefore investigated the possibility that PICK1 is involved in the delayed forward traffic of GluA2 during LTP, by manipulating PICK1 expression levels using overexpression and RNAi-mediated knockdown.…”

Section: Delayed Insertion Of Glua2 After Glycine Stimulation Is Pickmentioning

confidence: 99%

PICK1 Mediates Transient Synaptic Expression of GluA2-Lacking AMPA Receptors during Glycine-Induced AMPA Receptor Trafficking

2012

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The number and subunit composition of postsynaptic AMPA receptors (AMPARs) is a key determinant of synaptic transmission. The vast majority of AMPARs contain GluA2 subunit, which renders the channel impermeable to calcium. However, a small proportion are GluA2 lacking and therefore calcium permeable (CP-AMPARs). It has been proposed recently that long-term potentiation (LTP) involves not only an increase in the total number of AMPARs at the synapse but also a transient switch to CP-AMPARs in the first few minutes after LTP induction. The molecular mechanisms that underlie this switch to CP-AMPARs and the subsequent switch back to calciumimpermeable AMPARs are unknown. Here, we show that endogenous GluA1 is rapidly inserted at the synaptic plasma membrane of rat hippocampal neurons immediately after stimulation with elevated glycine, a treatment known to induce LTP. In contrast, GluA2 is restricted from trafficking to the cell surface by a glycine-induced increase in PICK1-GluA2 binding on endosomal compartments. Between 5 and 20 min after stimulus, activation of CP-AMPARs triggers a release of GluA2 from PICK1, allowing GluA2-containing AMPARs to traffic to the synaptic plasma membrane. These results define a PICK1-dependent mechanism that underlies transient alterations in the subunit composition and calcium permeability of synaptic AMPARs that is important during the early phase after stimulation with glycine and therefore is likely to be important during the expression of LTP.

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Developmental Expression of Ca²⁺-Permeable AMPA Receptors Underlies Depolarization-Induced Long-Term Depression at Mossy Fiber–CA3 Pyramid Synapses

Cited by 93 publications

References 74 publications

Molecular mechanisms controlling synaptic recruitment of GluA4 subunit-containing AMPA-receptors critical for functional maturation of CA1 glutamatergic synapses

Molecular mechanisms controlling synaptic recruitment of GluA4 subunit-containing AMPA-receptors critical for functional maturation of CA1 glutamatergic synapses

Removal of Synaptic Ca²⁺-Permeable AMPA Receptors during Sleep

PICK1 Mediates Transient Synaptic Expression of GluA2-Lacking AMPA Receptors during Glycine-Induced AMPA Receptor Trafficking

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Developmental Expression of Ca2+-Permeable AMPA Receptors Underlies Depolarization-Induced Long-Term Depression at Mossy Fiber–CA3 Pyramid Synapses

Cited by 93 publications

References 74 publications

Molecular mechanisms controlling synaptic recruitment of GluA4 subunit-containing AMPA-receptors critical for functional maturation of CA1 glutamatergic synapses

Molecular mechanisms controlling synaptic recruitment of GluA4 subunit-containing AMPA-receptors critical for functional maturation of CA1 glutamatergic synapses

Removal of Synaptic Ca2+-Permeable AMPA Receptors during Sleep

PICK1 Mediates Transient Synaptic Expression of GluA2-Lacking AMPA Receptors during Glycine-Induced AMPA Receptor Trafficking

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Developmental Expression of Ca²⁺-Permeable AMPA Receptors Underlies Depolarization-Induced Long-Term Depression at Mossy Fiber–CA3 Pyramid Synapses

Removal of Synaptic Ca²⁺-Permeable AMPA Receptors during Sleep