Linear versus nonlinear signal transmission in neuron models with adaptation-currents or dynamic thresholds

Jan Benda, Leonard Maler & André Longtin

Journal of Neurophysiology 104: 2806-2820

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Abstract

Spike-frequency adaptation is a prominent aspect of neuronal dynamics that shapes a neuron's signal processing properties on timescales ranging from about 10 ms to more than 1 s. For integrate-and-fire model neurons spike-frequency adaptation is incorporated either as an adaptation current or as a dynamic firing threshold. Whether a physiologically observed adaptation mechanism should be modeled as an adaptation current or a dynamic threshold is, however, not known. Here we show that a dynamic threshold has a divisive effect on the onset f-I curve (the initial maximal firing rate following a step increase in an input current) measured at increasing mean threshold levels, i.e. adaptation states. In contrast, an adaptation current subtractively shifts this f-I curve to higher inputs without affecting its slope. As a consequence, an adaptation current acts essentially linearly, resulting in a high-pass filter component of the neuron's transfer function for current stimuli. With a dynamic threshold, however, the transfer function strongly depends on the input range, because of the multiplicative effect on the f-I curves. Simulations of conductance-based spiking models with adaptation currents, such as AHP-type, M-type, and sodium activated potassium currents, do not show the divisive effects of a dynamic threshold, but agree with the properties of integrate-and-fire neurons with adaptation current. Notably, the effects of slow inactivation of sodium currents cannot be reproduced by either model. Our results suggests that, when lateral shifts of the onset f-I curve are seen in response to adapting inputs, adaptation should be modeled with adaptation currents and not with a dynamic threshold. In contrast, when the slope of onset f-I curves depends on the adaptation state, then adaptation should be modeled with a dynamic threshold. Further, the observation of divisively altered onset f-I curves in adapted neurons with notable variability of their spike threshold could hint to yet unknown biophysical mechanisms directly affecting the threshold.


Last modified: Wed Aug 31 09:08:17 CEST 2011