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The Journal of Neuroscience, March 10, 2004, 24(10):2345-2356; doi:10.1523/JNEUROSCI.3349-03.2004

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Behavioral/Systems/Cognitive
Neuronal Integration of Synaptic Input in the Fluctuation-Driven Regime

Alexandre Kuhn,¹ Ad Aertsen,¹ and Stefan Rotter^1,2

¹Neurobiology and Biophysics, Institute of Biology III, Albert-Ludwigs-University, D-79104 Freiburg, Germany, and ²Theory and Data Analysis, Institute for Frontier Areas of Psychology and Mental Health, D-79098 Freiburg, Germany

During sensory stimulation, visual cortical neurons undergo massive synaptic bombardment. This increases their input conductance, and action potentials mainly result from membrane potential fluctuations. To understand the response properties of neurons operating in this regime, we studied a model neuron with synaptic inputs represented by transient membrane conductance changes. We show that with a simultaneous increase of excitation and inhibition, the firing rate first increases, reaches a maximum, and then decreases at higher input rates. Comodulation of excitation and inhibition, therefore, does not provide a straightforward way of controlling the neuronal firing rate, in contrast to coding mechanisms postulated previously. The synaptically induced conductance increase plays a key role in this effect: it decreases firing rate by shunting membrane potential fluctuations, and increases it by reducing the membrane time constant, allowing for faster membrane potential transients. These findings do not depend on details of the model and, hence, are relevant to cells of other cortical areas as well.

Key words: synaptic integration; membrane conductance; primary visual cortex; integrate-and-fire; intracellular recording; neural coding

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Received July 16, 2003; revised December 12, 2003; accepted December 12, 2003.

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