GluA4 Dependent Plasticity Mechanisms Contribute to Developmental Synchronization of the CA3-CA1 Circuitry in the Hippocampus

Overview

Journal Neurochem Res

Specialties Chemistry
Neurology

Date 2017 Sep 1

PMID 28856535

Citations 3

Authors

Tsvetomira Atanasova

Zoya Kharybina

Tiina Kaarela

Johanna Huupponen

Natalia V Luchkina

Tomi Taira

Sari E Lauri

Affiliations

Soon will be listed here.

Abstract

During the course of development, molecular mechanisms underlying activity-dependent synaptic plasticity change considerably. At immature CA3-CA1 synapses in the hippocampus, PKA-driven synaptic insertion of GluA4 AMPA receptors is the predominant mechanism for synaptic strengthening. However, the physiological significance of the developmentally restricted GluA4-dependent plasticity mechanisms is poorly understood. Here we have used microelectrode array (MEA) recordings in GluA4 deficient slice cultures to study the role of GluA4 in early development of the hippocampal circuit function. We find that during the first week in culture (DIV2-6) when GluA4 expression is restricted to pyramidal neurons, loss of GluA4 has no effect on the overall excitability of the immature network, but significantly impairs synchronization of the CA3 and CA1 neuronal populations. In the absence of GluA4, the temporal correlation of the population spiking activity between CA3-CA1 neurons was significantly lower as compared to wild-types at DIV6. Our data show that synapse-level defects in transmission and plasticity mechanisms are efficiently compensated for to normalize population firing rate at the immature hippocampal network. However, lack of the plasticity mechanisms typical for the immature synapses may perturb functional coupling between neuronal sub-populations, a defect frequently implicated in the context of developmentally originating neuropsychiatric disorders.

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References

Zhu J, Esteban J, Hayashi Y, Malinow R . Postnatal synaptic potentiation: delivery of GluR4-containing AMPA receptors by spontaneous activity. Nat Neurosci. 2000; 3(11):1098-106. DOI: 10.1038/80614. View

Yasuda H, Barth A, Stellwagen D, Malenka R . A developmental switch in the signaling cascades for LTP induction. Nat Neurosci. 2002; 6(1):15-6. DOI: 10.1038/nn985. View

Makino C, Fujii Y, Kikuta R, Hirata N, Tani A, Shibata A . Positive association of the AMPA receptor subunit GluR4 gene (GRIA4) haplotype with schizophrenia: linkage disequilibrium mapping using SNPs evenly distributed across the gene region. Am J Med Genet B Neuropsychiatr Genet. 2002; 116B(1):17-22. DOI: 10.1002/ajmg.b.10041. View

Esteban J, Shi S, Wilson C, Nuriya M, Huganir R, Malinow R . PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci. 2003; 6(2):136-43. DOI: 10.1038/nn997. View

Kasyanov A, Safiulina V, Voronin L, Cherubini E . GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus. Proc Natl Acad Sci U S A. 2004; 101(11):3967-72. PMC: 374353. DOI: 10.1073/pnas.0305974101. View

Quian Quiroga R, Nadasdy Z, Ben-Shaul Y . Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput. 2004; 16(8):1661-87. DOI: 10.1162/089976604774201631. View

Groc L, Gustafsson B, Hanse E . AMPA signalling in nascent glutamatergic synapses: there and not there!. Trends Neurosci. 2006; 29(3):132-9. DOI: 10.1016/j.tins.2006.01.005. View

Lauri S, Vesikansa A, Segerstrale M, Collingridge G, Isaac J, Taira T . Functional maturation of CA1 synapses involves activity-dependent loss of tonic kainate receptor-mediated inhibition of glutamate release. Neuron. 2006; 50(3):415-29. DOI: 10.1016/j.neuron.2006.03.020. View

Boehm J, Kang M, Johnson R, Esteban J, Huganir R, Malinow R . Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1. Neuron. 2006; 51(2):213-25. DOI: 10.1016/j.neuron.2006.06.013. View

10.

Beneyto M, Meador-Woodruff J . Lamina-specific abnormalities of AMPA receptor trafficking and signaling molecule transcripts in the prefrontal cortex in schizophrenia. Synapse. 2006; 60(8):585-98. DOI: 10.1002/syn.20329. View

11.

Fuchs E, Zivkovic A, Cunningham M, Middleton S, LeBeau F, Bannerman D . Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron. 2007; 53(4):591-604. DOI: 10.1016/j.neuron.2007.01.031. View

12.

Huupponen J, Molchanova S, Taira T, Lauri S . Susceptibility for homeostatic plasticity is down-regulated in parallel with maturation of the rat hippocampal synaptic circuitry. J Physiol. 2007; 581(Pt 2):505-14. PMC: 2075179. DOI: 10.1113/jphysiol.2007.130062. View

13.

Vesikansa A, Sallert M, Taira T, Lauri S . Activation of kainate receptors controls the number of functional glutamatergic synapses in the area CA1 of rat hippocampus. J Physiol. 2007; 583(Pt 1):145-57. PMC: 2277228. DOI: 10.1113/jphysiol.2007.133975. View

14.

Mohajerani M, Sivakumaran S, Zacchi P, Aguilera P, Cherubini E . Correlated network activity enhances synaptic efficacy via BDNF and the ERK pathway at immature CA3 CA1 connections in the hippocampus. Proc Natl Acad Sci U S A. 2007; 104(32):13176-81. PMC: 1941828. DOI: 10.1073/pnas.0704533104. View

15.

Lee H, Takamiya K, Kameyama K, He K, Yu S, Rossetti L . Identification and characterization of a novel phosphorylation site on the GluR1 subunit of AMPA receptors. Mol Cell Neurosci. 2007; 36(1):86-94. PMC: 2443358. DOI: 10.1016/j.mcn.2007.06.003. View

16.

Yashiro K, Philpot B . Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology. 2008; 55(7):1081-94. PMC: 2590778. DOI: 10.1016/j.neuropharm.2008.07.046. View

17.

Fatemi S, Folsom T . The neurodevelopmental hypothesis of schizophrenia, revisited. Schizophr Bull. 2009; 35(3):528-48. PMC: 2669580. DOI: 10.1093/schbul/sbn187. View

18.

Hanse E, Taira T, Lauri S, Groc L . Glutamate synapse in developing brain: an integrative perspective beyond the silent state. Trends Neurosci. 2009; 32(10):532-7. DOI: 10.1016/j.tins.2009.07.003. View

19.

Lee H, Takamiya K, He K, Song L, Huganir R . Specific roles of AMPA receptor subunit GluR1 (GluA1) phosphorylation sites in regulating synaptic plasticity in the CA1 region of hippocampus. J Neurophysiol. 2009; 103(1):479-89. PMC: 2807233. DOI: 10.1152/jn.00835.2009. View

20.

Sagata N, Iwaki A, Aramaki T, Takao K, Kura S, Tsuzuki T . Comprehensive behavioural study of GluR4 knockout mice: implication in cognitive function. Genes Brain Behav. 2010; 9(8):899-909. DOI: 10.1111/j.1601-183X.2010.00629.x. View