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J Neurophysiol 102: 2273-2287, 2009. First published August 12, 2009; doi:10.1152/jn.00282.2009
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RESEARCH-ARTICLE

SK Channels Gate Information Processing In Vivo by Regulating an Intrinsic Bursting Mechanism Seen In Vitro

Natalia Toporikova1 and Maurice J. Chacron1,2

1Department of Physiology, Center for Nonlinear Dynamics, and 2Department of Physics, McGill University, Montreal, Quebec, Canada

Submitted 30 March 2009; accepted in final form 11 August 2009

ABSTRACT

Understanding the mechanistic substrates of neural computations that lead to behavior remains a fundamental problem in neuroscience. In particular, the contributions of intrinsic neural properties such as burst firing and dendritic morphology to the processing of behaviorally relevant sensory input have received much interest recently. Pyramidal cells within the electrosensory lateral line lobe of weakly electric fish display an intrinsic bursting mechanism that relies on somato-dendritic interactions when recorded in vitro: backpropagating somatic action potentials trigger dendritic action potentials that lead to a depolarizing afterpotential (DAP) at the soma. We recorded intracellularly from these neurons in vivo and found firing patterns that were quite different from those seen in vitro: we found no evidence for DAPs as each somatic action potential was followed by a pronounced afterhyperpolarization (AHP). Calcium chelators injected in vivo reduced the AHP, thereby unmasking the DAP and inducing in vitro-like bursting in pyramidal cells. These bursting dynamics significantly reduced the cell's ability to encode the detailed time course of sensory input. We performed additional in vivo pharmacological manipulations and mathematical modeling to show that calcium influx through N-methyl-D-aspartate (NMDA) receptors activate dendritic small conductance (SK) calcium-activated potassium channels, which causes an AHP that counteracts the DAP and leads to early termination of the burst. Our results show that ion channels located in dendrites can have a profound influence on the processing of sensory input by neurons in vivo through the modulation of an intrinsic bursting mechanism.


Address for reprint requests and other correspondence: M. J. Chacron, 3655 Sir William Osler, Rm. 1137, Montreal, Quebec H3G 1Y6, Canada (E-mail: maurice.chacron{at}mcgill.ca).




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M. J. Chacron, N. Toporikova, and E. S. Fortune
Differences in the Time Course of Short-Term Depression Across Receptive Fields Are Correlated With Directional Selectivity in Electrosensory Neurons
J Neurophysiol, December 1, 2009; 102(6): 3270 - 3279.
[Abstract] [Full Text] [PDF]




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