T-Type Calcium Channels Consolidate Tonic Action Potential Output of Thalamic Neurons to Neocortex
Charlotte Deleuze,1,2
François David,2
Sébastien Béhuret,1
Gérard Sadoc,1
Hee-Sup Shin,3
Victor N. Uebele,4
John J. Renger,4
Régis C. Lambert,2 *
Nathalie Leresche,2 * , and
Thierry Bal1 *
1Unité de Neurosciences, Information et Complexité (UNIC), UPR 3293 CNRS, 91198 Gif-sur-Yvette, France, 2Université Pierre et Marie Curie (UPMC), Université Paris 6, UMR7102 CNRS, 75005 Paris, France, 3Center for Neural Science, Korea Institute of Science and Technology, Seoul 136-791, Korea, and 4Merck Research laboratories, West Point, Pennsylvania 19486
Correspondence should be addressed to Thierry Bal, UNIC, CNRS UPR 3293, 1, Avenue de la Terrasse, Batiment 32-33, 91198 Gif-sur-Yvette, France. Email: thierry.bal{at}unic.cnrs-gif.fr
Abstract:
The thalamic output during different behavioral states is strictly controlled by the firing modes of thalamocortical neurons. During sleep, their hyperpolarized membrane potential allows activation of the T-type calcium channels, promoting rhythmic high-frequency burst firing that reduces sensory information transfer. In contrast, in the waking state thalamic neurons mostly exhibit action potentials at low frequency (i.e., tonic firing), enabling the reliable transfer of incoming sensory inputs to cortex. Because of their nearly complete inactivation at the depolarized potentials that are experienced during the wake state, T-channels are not believed to modulate tonic action potential discharges. Here, we demonstrate using mice brain slices that activation of T-channels in thalamocortical neurons maintained in the depolarized/wake-like state is critical for the reliable expression of tonic firing, securing their excitability over changes in membrane potential that occur in the depolarized state. Our results establish a novel mechanism for the integration of sensory information by thalamocortical neurons and point to an unexpected role for T-channels in the early stage of information processing.
Received for publication March 19, 2012.
Revision received July 4, 2012.
Accepted for publication July 12, 2012.
Correspondence should be addressed to Thierry Bal, UNIC, CNRS UPR 3293, 1, Avenue de la Terrasse, Batiment 32-33, 91198 Gif-sur-Yvette, France. Email: thierry.bal{at}unic.cnrs-gif.fr
