Metabotropic Regulation of Intrinsic Excitability by Synaptic Activation of Kainate Receptors

Melyan, Zare; Lancaster, Barrie; Wheal, H.V.

doi:10.1523/jneurosci.5356-03.2004

Cited by 108 publications

(107 citation statements)

References 39 publications

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“…Activity-dependent plasticity of intrinsic excitability in postsynaptic neurons could target on modulating Na ϩ , K ϩ , and Ca 2ϩ channels. Modulation of K ϩ channels has been previously reported and expressed as inhibition of the A-type K ϩ channel (Frick et al, 2004) and inhibition of AHP (Saar et al, 1998(Saar et al, , 2001Ireland and Abraham, 2002;Melyan et al, 2002Melyan et al, , 2004Sourdet et al, 2003). In our study, CS also induced a reduction in AHP (Fig.…”

Section: Cooperation Of Activity-dependent Intrinsic Plasticitysupporting

confidence: 73%

“…6 B, inset, 3) that is different from the observation of 10 Hz burst stimulationinduced attenuation of AHP in neocortical neurons (Ireland and Abraham, 2002;Sourdet et al, 2003). Thus, the mGluRindependent part of CS-induced reduction of AHP may involve other cellular mechanisms, such as activation of KA receptors (Melyan et al, 2002(Melyan et al, , 2004 and cholinergic-muscarinic receptors (Saar et al, 1998(Saar et al, , 2001. Consistent with NMDAR independency, blockade of CaMK and protein synthesis did not inhibit CSinduced reduction of AHP, further suggesting the decreased AP threshold and attenuated AHP are different forms of intrinsic plasticity through separate cellular mechanisms.…”

Section: Cooperation Of Activity-dependent Intrinsic Plasticitymentioning

confidence: 87%

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Activity-Dependent Long-Term Potentiation of Intrinsic Excitability in Hippocampal CA1 Pyramidal Neurons

Kang²,

Jiang³

et al. 2005

J. Neurosci.

159

178

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The efficiency of neural circuits is enhanced not only by increasing synaptic strength but also by increasing intrinsic excitability. In contrast to the detailed analysis of long-term potentiation (LTP), less attention has been given to activity-dependent changes in the intrinsic neuronal excitability. By stimulating hippocampal CA1 pyramidal neurons with synaptic inputs correlating with postsynaptic neuronal spikes, we elicited an LTP of intrinsic excitability (LTP-IE) concurring with synaptic LTP. LTP-IE was manifested as a decrease in the action potential threshold that was attributable to a hyperpolarized shift in the activation curve of voltage-gated sodium channels (VGSCs) rather than activity-dependent changes in synaptic inputs or A-type K ϩ channels. Cell-attached patch recording of VGSC activities indicated such an activity-dependent change in VGSCs. Induction of LTP-IE was blocked by the NMDA receptor antagonist APV, intracellular BAPTA, the CaM kinase inhibitors KN-62 and autocamtide-2-related inhibitory peptide, and the protein synthesis inhibitors emetine and anisomycin. The results suggest that induction of LTP-IE shares a similar signaling pathway with the late phase of synaptic LTP and requires activation of the NMDA glutamate receptor subtype, Ca 2ϩ influx, activity of CaM kinase II, and function of the protein synthesis. This new form of hippocampal neuronal plasticity could be a cellular correlate of learning and memory besides synaptic LTP.

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Section: Cooperation Of Activity-dependent Intrinsic Plasticitysupporting

confidence: 73%

Section: Cooperation Of Activity-dependent Intrinsic Plasticitymentioning

confidence: 87%

Activity-Dependent Long-Term Potentiation of Intrinsic Excitability in Hippocampal CA1 Pyramidal Neurons

Kang²,

Jiang³

et al. 2005

J. Neurosci.

159

178

View full text Add to dashboard Cite

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“…Kainate receptors are widely expressed in the central nervous system (Wisden and Seeburg, 1993), where they can act pre-and post-synaptically. In the hippocampus, postsynaptic kainate receptors are thought to mediate excitatory transmission via an ionotropic action (Castillo et al, 1997;Cossart et al, 2002;Cossart et al, 1998) and to regulate excitability via a metabotropic function (Melyan et al, 2004;Melyan et al, 2002;Ruiz et al, 2005). Activation of presynaptic kainate receptors regulates glutamate and GABA release (Kullmann, 2001;Rodriguez-Moreno and Lerma, 1998) and modulates excitability in mature (Schmitz et al, 2000) and developing hippocampus.…”

Section: Introductionmentioning

confidence: 99%

KRIP6: A novel BTB/kelch protein regulating function of kainate receptors

Laezza

Wilding

Sequeira

et al. 2007

Molecular and Cellular Neuroscience

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Whereas many interacting proteins have been identified for AMPA and NMDA glutamate receptors, fewer are known to directly bind and regulate function of kainate receptors. Using a yeast two-hybrid screen for interacting partners of the C-terminal domain of GluR6a, we identified a novel neuronal protein of the BTB/kelch family, KRIP6. KRIP6 binds to the GluR6a C-terminal domain at a site distinct from the PDZ-binding motif and it co-immunoprecipitates with recombinant and endogenous GluR6. Co-expression of KRIP6 alters GluR6 mediated currents in a heterologous expression system reducing peak current amplitude and steady-state desensitization, without affecting surface levels of GluR6. Endogenous KRIP6 is widely expressed in brain and overexpression of KRIP6 reduces endogenous kainate receptor-mediated responses evoked in hippocampal neurons. Taken together, these results suggest that KRIP6 can directly regulate native kainate receptors and provide the first evidence for a BTB/kelch protein in direct functional regulation of a mammalian glutamate receptor.

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“…Because of this technical constraint, the mechanism underlying postburst AHP reduction have been studied to date at two time windows. The first, during and up to 45 min after HFS application (Melyan et al, 2002(Melyan et al, , 2004, and the second, after 1 to several days after behavioral manipulations Zelcer et al, 2006). The combination of these two approaches leaves the time window of several hours after synaptic activation, when protein synthesis-dependent processes are expected to occur (Krug et al, 1984;Otani et al, 1989;Frey et al, 1993Frey et al, , 1988Nguyen et al, 1994), unexplored.…”

Section: Long-lasting Maintenance Of Hfs-induced Ahp Reductionmentioning

confidence: 99%

A Novel Role for Protein Synthesis in Long-Term Neuronal Plasticity: Maintaining Reduced Postburst Afterhyperpolarization

Cohen-Matsliah

Motanis²,

Rosenblum³

et al. 2010

J. Neurosci.

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Memory consolidation, the process of transformation of short-term to long-term memory, has been shown to be protein synthesis dependent in a variety of different learning paradigms, brain structures, and species. At the cellular level, protein synthesis was shown to be crucial for induction of long-term synaptic plasticity; application of protein synthesis inhibitors prevents the transformation of early long-term potentiation (LTP) to late LTP. Thus, protein synthesis has been traditionally thought to affect long-term memory consolidation by stabilizing synaptic transmission. However, long-term memory is not supported only by modulation of synaptic strength; modifications in intrinsic neuronal properties also subserve learning-related behavioral changes. Learning-induced reduction in the postburst afterhyperpolarization (AHP), which results with enhanced neuronal excitability and decreased spike frequency adaptation, is apparent in hippocampal and cortical pyramidal neurons. Such postburst AHP reduction lasts for days after training completion and is implicated in maintaining learned skills. Short-term modulation of intrinsic neuronal excitability can be also induced in vitro. Intense synaptic activation induces AHP reduction and enhanced neuronal excitability in hippocampal pyramidal neurons. Here, we show that synaptic activation-induced short-term postburst AHP reduction can be transformed to long-term AHP reduction, such that persists for prolonged time periods. This long-lasting AHP reduction is protein synthesis dependent for up to 1 h after induction. We suggest that, much like synaptic plasticity, activity-induced long-lasting modulation of intrinsic neuronal excitability requires molecular consolidation. It would appear that both synaptic and intrinsic modifications and maintenance are activated jointly to enable long-lasting memories.

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Metabotropic Regulation of Intrinsic Excitability by Synaptic Activation of Kainate Receptors

Cited by 108 publications

References 39 publications

Activity-Dependent Long-Term Potentiation of Intrinsic Excitability in Hippocampal CA1 Pyramidal Neurons

Activity-Dependent Long-Term Potentiation of Intrinsic Excitability in Hippocampal CA1 Pyramidal Neurons

KRIP6: A novel BTB/kelch protein regulating function of kainate receptors

A Novel Role for Protein Synthesis in Long-Term Neuronal Plasticity: Maintaining Reduced Postburst Afterhyperpolarization

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