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The Journal of Neuroscience, May 25, 2005, 25(21):5259-5271; doi:10.1523/JNEUROSCI.0827-05.2005

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Cellular/Molecular
Developmental Changes in AMPA and Kainate Receptor-Mediated Quantal Transmission at Thalamocortical Synapses in the Barrel Cortex

Neil J. Bannister,¹ Timothy A. Benke,² Jack Mellor,¹ Helen Scott,¹ Esra Gürdal,^1,3 John W. Crabtree,¹ and John T. R. Isaac^1,4

¹Medical Research Council Centre for Synaptic Plasticity, Department of Anatomy, University of Bristol, Bristol BS8 1TD, United Kingdom, ²Department of Pediatrics, University of Colorado Health Sciences Center, Denver, Colorado 80262, ³Department of Anatomy, Marmara University School of Medicine, Haydarpasa 34668, Istanbul, Turkey, and ⁴National Institute of Neurological Disorders and Stroke, National Institutes Health, Bethesda, Maryland 20892

During the first week of life, there is a shift from kainate to AMPA receptor-mediated thalamocortical transmission in layer IV barrel cortex. However, the mechanisms underlying this change and the differential properties of AMPA and kainate receptor-mediated transmission remain essentially unexplored. To investigate this, we studied the quantal properties of AMPA and kainate receptor-mediated transmission using strontium-evoked miniature EPSCs. AMPA and kainate receptor-mediated transmission exhibited very different quantal properties but were never coactivated by a single quantum of transmitter, indicating complete segregation to different synapses within the thalamocortical input. Nonstationary fluctuation analysis showed that synaptic AMPA receptors exhibited a range of single-channel conductance () and a strong negative correlation between and functional channel number, indicating that these two parameters are reciprocally regulated at thalamocortical synapses. We obtained the first estimate of for synaptic kainate receptors (<2 pS), and this primarily accounted for the small quantal size of kainate receptor-mediated transmission. Developmentally, the quantal contribution to transmission of AMPA receptors increased and that of kainate receptors decreased. No changes in AMPA or kainate quantal amplitude or in AMPA receptor were observed, demonstrating that the developmental change was attributable to a decrease in the number of kainate synapses and an increase in the number of AMPA synapses contributing to transmission. Therefore, we demonstrate fundamental differences in the quantal properties for these two types of synapse. Thus, the developmental switch in transmission will dramatically alter information transfer at thalamocortical inputs to layer IV.

Key words: glutamate; synaptic transmission; layer IV; neocortex; miniature EPSC; nonstationary fluctuation analysis

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Received Feb 27, 2004; revised April 19, 2005; accepted April 19, 2005.

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