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The Journal of Neuroscience, September 6, 2006, 26(36):9084-9097; doi:10.1523/JNEUROSCI.1388-06.2006

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Cellular/Molecular
Nonlinear Interaction between Shunting and Adaptation Controls a Switch between Integration and Coincidence Detection in Pyramidal Neurons

Steven A. Prescott,¹ Stéphanie Ratté,² Yves De Koninck,³ and Terrence J. Sejnowski^1,4

¹Computational Neurobiology Laboratory, Howard Hughes Medical Institute, Salk Institute, La Jolla, California 92037, ²Département de Physiologie, Université de Montréal, Montréal, Québec, Canada H3C 3J7, ³Division de Neurobiologie Cellulaire, Centre de Recherche Université Laval Robert-Giffard, Québec, Québec, Canada G1J 2G3, and ⁴Division of Biological Sciences, University of California, San Diego, La Jolla, California 92093

Correspondence should be addressed to Steven A. Prescott, Computational Neurobiology Laboratory, Salk Institute, 10010 North Torrey Pines Road, La Jolla, CA 92037. Email: sprescott{at}salk.edu

The membrane conductance of a pyramidal neuron in vivo is substantially increased by background synaptic input. Increased membrane conductance, or shunting, does not simply reduce neuronal excitability. Recordings from hippocampal pyramidal neurons using dynamic clamp revealed that adaptation caused complete cessation of spiking in the high conductance state, whereas repetitive spiking could persist despite adaptation in the low conductance state. This behavior was reproduced in a phase plane model and was explained by a shunting-induced increase in voltage threshold. The increase in threshold allows greater activation of the M current (I_M) at subthreshold potentials and reduces the minimum adaptation required to stabilize the system; in contrast, activation of the afterhyperpolarization current is unaffected by the increase in threshold and therefore remains unable to stop repetitive spiking. The nonlinear interaction between shunting and I_M has other important consequences. First, timing of spikes elicited by brief stimuli is more precise when background spikes elicited by sustained input are prohibited, as occurs exclusively with I_M-mediated adaptation in the high conductance state. Second, activation of I_M at subthreshold potentials, which is increased in the high conductance state, hyperpolarizes average membrane potential away from voltage threshold, allowing only large, rapid fluctuations to reach threshold and elicit spikes. These results suggest that the shift from a low to high conductance state in a pyramidal neuron is accompanied by a switch from encoding time-averaged input with firing rate to encoding transient inputs with precisely timed spikes, in effect, switching the operational mode from integration to coincidence detection.

Key words: AHP current; coincidence detector; integrator; M current; membrane conductance; spike-time precision

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Received April 1, 2006; revised July 24, 2006; accepted July 28, 2006.

Correspondence should be addressed to Steven A. Prescott, Computational Neurobiology Laboratory, Salk Institute, 10010 North Torrey Pines Road, La Jolla, CA 92037. Email: sprescott{at}salk.edu

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