Intrinsic subthreshold oscillations extend the influence of inhibitory synaptic inputs on cortical pyramidal neurons.

Klaus M Stiefel,Peter J Thomas,Jean-Marc Fellous,Terrence J Sejnowski

doi:10.1111/j.1460-9568.2010.07146.x

Abstract

Fast inhibitory synaptic inputs, which cause conductance changes that typically last for 10–100 ms, participate in the generation and maintenance of cortical rhythms. We show here that these fast events can have influences that outlast the duration of the synaptic potentials by interacting with subthreshold membrane potential oscillations. Inhibitory postsynaptic potentials (IPSPs) in cortical neurons in vitro shifted the oscillatory phase for several seconds. The phase shift caused by two IPSPs or two current pulses summed non-linearly. Cholinergic neuromodulation increased the power of the oscillations and decreased the magnitude of the phase shifts. These results show that the intrinsic conductances of cortical pyramidal neurons can carry information about inhibitory inputs and can extend the integration window for synaptic input.

Highlights

Spontaneous membrane potential oscillations are observed in cortical layer 2 ⁄ 3 pyramidal neurons
Neurons have a rich repertoire of ionic currents capable of subthreshold oscillations that can store the information about the arrival of an inhibitory postsynaptic potential (IPSP) for periods of time much greater than the duration of the initial perturbation
As the phase of the oscillation can be influenced by IPSPs for up to at least 1 s, this mechanism can create an extended synaptic integration window

Summary

Introduction

Spontaneous membrane potential oscillations are observed in cortical layer 2 ⁄ 3 pyramidal neurons. The oscillations that we investigated are generated intrinsically by the interplay of ionic conductances in the neuronal membrane, rather than being forced by an external source (such as the surrounding neural network). These oscillations occur in the voltage range just below threshold, and are caused by the interaction of a persistent sodium current and at least one slower potassium current. They are typically about 5 mV in amplitude, 4–15 Hz in frequency, and have a stochastic component (Klink & Alonso, 1993, 1997; White et al, 1998; Fellous et al, 2001)

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Conclusion