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The Journal of Neuroscience, January 26, 2005, 25(4):1024-1033; doi:10.1523/JNEUROSCI.3951-04.2005

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Cellular/Molecular
Target-Specific Regulation of Synaptic Amplitudes in the Neocortex

Junryo Watanabe,¹ Andrei Rozov,² and Lonnie P. Wollmuth¹

¹Department of Neurobiology and Behavior, State University of New York at Stony Brook, Stony Brook, New York 11794-5230, and ²Department of Clinical Neurobiology, University Hospital for Neurology, University of Heidelberg, 69120 Heidelberg, Germany

In layers 2/3 in the rat visual cortex, glutamatergic synapses, between pyramidal neurons and GABAergic interneurons, show target-specific depression or facilitation. To study the mechanisms regulating these short-term synaptic modifications, we recorded from synaptically connected pyramidal neurons (presynaptic) and multipolar or bitufted interneurons (postsynaptic). Evoked AMPA receptor (AMPAR)- or NMDA receptor (NMDAR)-mediated EPSCs were pharmacologically isolated at these pyramidal-to-interneuron synapses while altering release probability (P_r) by changing the extracellular Ca²⁺ concentration ([Ca²⁺]_o). At the pyramidal-to-multipolar synapse, which shows paired-pulse depression, elevation of [Ca²⁺]_o from physiological concentrations (2 mM) to 3 mM increased the amplitude of the initial AMPAR-mediated EPSC and enhanced paired-pulse depression. In contrast, the initial NMDAR-mediated EPSC did not change in amplitude with raised P_r nor was paired-pulse depression altered. This lack of an increase of NMDAR-mediated currents is not a result of Ca²⁺-dependent effects on the NMDAR. Rather, at the pyramidal-to-multipolar synapse, raised P_r increases the transient glutamate concentration at individual release sites, possibly reflecting multivesicular release. In contrast, at the pyramidal-to-bitufted synapse, which shows facilitation, AMPAR- and NMDAR-meditated EPSCs showed parallel increases in response to raised P_r. Thus, our results reveal differential recruitment of AMPA and NMDARs at depressing and facilitating synapses in layers 2/3 of the cortex and suggest that the mechanisms regulating dynamic aspects of synaptic transmission are target specific.

Key words: glutamatergic synapses; interneurons; short-term synaptic plasticity; glutamate receptors; multivesicular release; NMDA

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Received Sep 23, 2004; revised November 20, 2004; accepted December 13, 2004.

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