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The Journal of Neuroscience, September 24, 2008, 28(39):9652-9663; doi:10.1523/JNEUROSCI.1554-08.2008

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Cellular/Molecular
Driver or Coincidence Detector: Modal Switch of a Corticothalamic Giant Synapse Controlled by Spontaneous Activity and Short-Term Depression

Alexander Groh, Christiaan P. J. de Kock, Verena C. Wimmer, Bert Sakmann, and Thomas Kuner

Department of Cell Physiology, Max Planck Institute for Medical Research, 69120 Heidelberg, Germany

Correspondence should be addressed to Thomas Kuner at his present address, Department of Anatomy and Cell Biology, University of Heidelberg, Im Neuenheimer Feld 307, Jahnstrasse 29, 69120 Heidelberg, Germany. Email: kuner{at}uni-heidelberg.de

Giant synapses between layer 5B (L5B) neurons of somatosensory (barrel) cortex and neurons of the posteromedial nucleus (POm) of thalamus reside in a key position of the cortico-thalamo-cortical (CTC) loop, yet their synaptic properties and contribution to CTC information processing remain poorly understood. Fluorescence-guided local stimulation of terminals were combined with postsynaptic whole-cell recordings in thalamus to study synaptic transmission at an identified giant synapse. We found large EPSCs mediated by Ca²⁺-permeable AMPA and NMDA receptors. A single presynaptic electrical stimulus evoked a train of postsynaptic action potentials, indicating that a single L5B input can effectively drive the thalamic neuron. Repetitive stimulation caused strong short-term depression (STD) with fast recovery. To examine how these synaptic properties affect information transfer, spontaneous and evoked activity of L5B neurons was recorded in vivo and played back to giant terminals in vitro. We found that suprathreshold synaptic transmission was suppressed because of spontaneous activity causing strong STD of the L5B–POm giant synapse. Thalamic neurons only spiked after intervals of presynaptic silence or when costimulating two giant terminals. Therefore, STD caused by spontaneous activity of L5B neurons can switch the synapse from a "driver mode" to a "coincidence mode." Mechanisms decreasing spontaneous activity in L5B neurons and inputs synchronized by a sensory stimulus may thus gate the cortico-thalamo-cortical loop.

Key words: giant synapse; corticothalamic; short-term depression; low-pass filtering; virus-mediated gene expression; posteromedial nucleus of thalamus

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Received April 9, 2008; revised Aug. 11, 2008; accepted Aug. 19, 2008.

Correspondence should be addressed to Thomas Kuner at his present address, Department of Anatomy and Cell Biology, University of Heidelberg, Im Neuenheimer Feld 307, Jahnstrasse 29, 69120 Heidelberg, Germany. Email: kuner{at}uni-heidelberg.de

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