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The Journal of Neuroscience, January 11, 2006, 26(2):708-715; doi:10.1523/JNEUROSCI.4409-05.2006

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Cellular/Molecular
NMDA Receptors in Layer 4 Spiny Stellate Cells of the Mouse Barrel Cortex Contain the NR2C Subunit

Alexander M. Binshtok,¹ Ilya A. Fleidervish,¹ Rolf Sprengel,² and Michael J. Gutnick¹

¹Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot 76100, Israel, and ²Department of Molecular Neurobiology, Max-Planck Institute for Medical Research, D-69120 Heidelberg, Germany

In layer 4 of the somatosensory cortex, the glutamatergic synapses that interconnect spiny stellate (SpS) neurons, which are the major targets of thalamocortical input, differ from most other neocortical excitatory synapses in that they have an extremely large NMDA receptor (NMDAR)-mediated component that is relatively insensitive to voltage-dependent Mg²⁺ blockade. We now report that this unique feature of the NMDA response reflects the distinctive subunit composition of the underlying receptors. We studied NMDAR-mediated miniature EPSCs (mEPSCs) and NMDA channel currents in tangential brain slices of mouse barrel cortex, which exclusively contain layer 4. NMDAR-mediated mEPSCs in SpS neurons were prominent at negative membrane potentials, and NMDA channels in outside-out patches excised from the somata of the same neurons had relatively low conductance and reduced susceptibility to Mg²⁺ block. These are characteristic features of heteromeric NMDAR assemblies that contain the NR2C subunit. Some patches also contained NMDA channels with higher conductance and a greater sensitivity to Mg²⁺. In the neocortex of transgenic mice in which a -galactosidase (lacZ) indicator gene was controlled by the NR2C promoter, the lacZ indicator was densely expressed in layer 4. In current-clamp recordings, blockade of NMDARs caused hyperpolarization and an increase in apparent input resistance. Our data demonstrate that the SpS neurons of layer 4 functionally express NR2C subunits; this is the likely explanation for their ability to generate large NMDAR-mediated EPSPs that are effective at resting potential, without previous depolarization.

Key words: somatosensory cortex; tangential slice; excitatory postsynaptic current; NMDA channels; patch clamp; spiny stellate neuron

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Received April 7, 2005; revised November 22, 2005; accepted November 23, 2005.

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