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This Article Full Text Full Text (PDF) All Versions of this Article: 101/5/2239    most recent 90711.2008v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Schreiber, S. Articles by Herz, A. V.M. Search for Related Content PubMed PubMed Citation Articles by Schreiber, S. Articles by Herz, A. V.M.

Two Distinct Mechanisms Shape the Reliability of Neural Responses

¹Institute for Theoretical Biology, Humboldt-Universität zu Berlin; ²Bernstein Center for Computational Neuroscience Berlin, Germany; ⁴Department of Biology, Ludwig-Maximilians-Universität München, Martinsried; ⁵Bernstein Center for Computational Neuroscience Munich, Germany; and ³Consejo de Investigaciones Científicas y Técnicas, Centro Atómico Bariloche and Instituto Balseiro, Bariloche, Argentina

Submitted 24 June 2008; accepted in final form 26 January 2009

Despite intrinsic noise sources, neurons can generate action potentials with remarkable reliability. This reliability is influenced by the characteristics of sensory or synaptic inputs, such as stimulus frequency. Here we use conductance-based models to study the frequency dependence of reliability in terms of the underlying single-cell properties. We are led to distinguish a mean-driven firing regime, where the stimulus mean is sufficient to elicit continuous firing, and a fluctuation-driven firing regime, where spikes are generated by transient stimulus fluctuations. In the mean-driven regime, the stimulus frequency that induces maximum reliability coincides with the firing rate of the cell, whereas in the fluctuation-driven regime, it is determined by the resonance properties of the subthreshold membrane potential. When the stimulus frequency does not match the optimal frequency, the two firing regimes exhibit different "symptoms" of decreased reliability: reduced spike-time precision and reduced spike probability, respectively. As a signature of stochastic resonance, reliable spike generation in the fluctuation-driven regime can benefit from intermediate amounts of noise that boost spike probability without significantly impairing spike-time precision. Our analysis supports the view that neurons are endowed with selection mechanisms that allow only certain stimulus frequencies to induce reliable spiking. By modulating the intrinsic cell properties, the nervous system can thus tune individual neurons to pick out specific input frequency bands with enhanced spike precision or spike probability.