Developmental Origin Dictates Interneuron AMPA and NMDA Receptor Subunit Composition and Plasticity

Overview

Journal Nat Neurosci

Date 2013 Jul 16

PMID 23852113

Citations 70

Authors

Jose A Matta

Kenneth A Pelkey

Michael T Craig

Ramesh Chittajallu

Brian W Jeffries

Chris J McBain

Affiliations

Soon will be listed here.

Abstract

Disrupted excitatory synapse maturation in GABAergic interneurons may promote neuropsychiatric disorders such as schizophrenia. However, establishing developmental programs for nascent synapses in GABAergic cells is confounded by their sparsity, heterogeneity and late acquisition of subtype-defining characteristics. We investigated synaptic development in mouse interneurons targeting cells by lineage from medial ganglionic eminence (MGE) or caudal ganglionic eminence (CGE) progenitors. MGE-derived interneuron synapses were dominated by GluA2-lacking AMPA-type glutamate receptors (AMPARs), with little contribution from NMDA-type receptors (NMDARs) throughout development. In contrast, CGE-derived cell synapses had large NMDAR components and used GluA2-containing AMPARs. In neonates, both MGE- and CGE-derived interneurons expressed primarily GluN2B subunit-containing NMDARs, which most CGE-derived interneurons retained into adulthood. However, MGE-derived interneuron NMDARs underwent a GluN2B-to-GluN2A switch that could be triggered acutely with repetitive synaptic activity. Our findings establish ganglionic eminence-dependent rules for early synaptic integration programs of distinct interneuron cohorts, including parvalbumin- and cholecystokinin-expressing basket cells.

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References

Isaac J, Crair M, Nicoll R, Malenka R . Silent synapses during development of thalamocortical inputs. Neuron. 1997; 18(2):269-80. DOI: 10.1016/s0896-6273(00)80267-6. View

Sanz-Clemente A, Matta J, Isaac J, Roche K . Casein kinase 2 regulates the NR2 subunit composition of synaptic NMDA receptors. Neuron. 2010; 67(6):984-96. PMC: 2947143. DOI: 10.1016/j.neuron.2010.08.011. View

Stoop R, Conquet F, Zuber B, Voronin L, Pralong E . Activation of metabotropic glutamate 5 and NMDA receptors underlies the induction of persistent bursting and associated long-lasting changes in CA3 recurrent connections. J Neurosci. 2003; 23(13):5634-44. PMC: 6741217. View

Ito I, Kawakami R, Sakimura K, Mishina M, Sugiyama H . Input-specific targeting of NMDA receptor subtypes at mouse hippocampal CA3 pyramidal neuron synapses. Neuropharmacology. 2000; 39(6):943-51. DOI: 10.1016/s0028-3908(99)00217-8. View

Traynelis S, Wollmuth L, McBain C, Menniti F, Vance K, Ogden K . Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev. 2010; 62(3):405-96. PMC: 2964903. DOI: 10.1124/pr.109.002451. View

Mierau S, Meredith R, Upton A, Paulsen O . Dissociation of experience-dependent and -independent changes in excitatory synaptic transmission during development of barrel cortex. Proc Natl Acad Sci U S A. 2004; 101(43):15518-23. PMC: 524435. DOI: 10.1073/pnas.0402916101. View

Williams K, Russell S, Shen Y, Molinoff P . Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro. Neuron. 1993; 10(2):267-78. DOI: 10.1016/0896-6273(93)90317-k. View

Szabo A, Somogyi J, Cauli B, Lambolez B, Somogyi P, Lamsa K . Calcium-permeable AMPA receptors provide a common mechanism for LTP in glutamatergic synapses of distinct hippocampal interneuron types. J Neurosci. 2012; 32(19):6511-6. PMC: 3355374. DOI: 10.1523/JNEUROSCI.0206-12.2012. View

Pickard L, Noel J, DUCKWORTH J, Fitzjohn S, Henley J, Collingridge G . Transient synaptic activation of NMDA receptors leads to the insertion of native AMPA receptors at hippocampal neuronal plasma membranes. Neuropharmacology. 2001; 41(6):700-13. DOI: 10.1016/s0028-3908(01)00127-7. View

10.

Oren I, Nissen W, Kullmann D, Somogyi P, Lamsa K . Role of ionotropic glutamate receptors in long-term potentiation in rat hippocampal CA1 oriens-lacunosum moleculare interneurons. J Neurosci. 2009; 29(4):939-50. PMC: 2668821. DOI: 10.1523/JNEUROSCI.3251-08.2009. View

11.

Zhang L, Warren R . Postnatal development of excitatory postsynaptic currents in nucleus accumbens medium spiny neurons. Neuroscience. 2008; 154(4):1440-9. DOI: 10.1016/j.neuroscience.2008.05.002. View

12.

Tricoire L, Pelkey K, Erkkila B, Jeffries B, Yuan X, McBain C . A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity. J Neurosci. 2011; 31(30):10948-70. PMC: 3163481. DOI: 10.1523/JNEUROSCI.0323-11.2011. View

13.

Petralia R, Wang Y, Mayat E, Wenthold R . Glutamate receptor subunit 2-selective antibody shows a differential distribution of calcium-impermeable AMPA receptors among populations of neurons. J Comp Neurol. 1997; 385(3):456-76. DOI: 10.1002/(sici)1096-9861(19970901)385:3<456::aid-cne9>3.0.co;2-2. View

14.

Bellone C, Mameli M, Luscher C . In utero exposure to cocaine delays postnatal synaptic maturation of glutamatergic transmission in the VTA. Nat Neurosci. 2011; 14(11):1439-46. DOI: 10.1038/nn.2930. View

15.

Kerchner G, Nicoll R . Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci. 2008; 9(11):813-25. PMC: 2819160. DOI: 10.1038/nrn2501. View

16.

Morin F, Beaulieu C, Lacaille J . Membrane properties and synaptic currents evoked in CA1 interneuron subtypes in rat hippocampal slices. J Neurophysiol. 1996; 76(1):1-16. DOI: 10.1152/jn.1996.76.1.1. View

17.

McMahon L, Kauer J . Hippocampal interneurons express a novel form of synaptic plasticity. Neuron. 1997; 18(2):295-305. DOI: 10.1016/s0896-6273(00)80269-x. View

18.

Quinlan E, Philpot B, Huganir R, Bear M . Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat Neurosci. 1999; 2(4):352-7. DOI: 10.1038/7263. View

19.

Daw M, Tricoire L, Erdelyi F, Szabo G, McBain C . Asynchronous transmitter release from cholecystokinin-containing inhibitory interneurons is widespread and target-cell independent. J Neurosci. 2009; 29(36):11112-22. PMC: 2762613. DOI: 10.1523/JNEUROSCI.5760-08.2009. View

20.

Wonders C, Anderson S . The origin and specification of cortical interneurons. Nat Rev Neurosci. 2006; 7(9):687-96. DOI: 10.1038/nrn1954. View