The responses of cortical neurons are highly variable across repeated presentations of a stimulus. Understanding this variability is critical for theories of both sensory and motor processing, since response variance affects the accuracy of neural codes. Despite this influence, the cellular and circuit mechanisms that shape the trial-to-trial variability of population responses remain poorly understood. We used a combination of experimental and computational techniques to uncover the mechanisms underlying response variability of populations of pyramidal (E) cells in layer 2/3 of rat whisker barrel cortex. Spike trains recorded from pairs of E-cells during either spontaneous activity or whisker deflected responses show similarly low levels of spiking co-variability, despite large differences in network activation between the two states. We developed network models that show how spike threshold non-linearities dilute E-cell spiking co-variability during spontaneous activity and low velocity whisker deflections. In contrast, during high velocity whisker deflections, cancelation mechanisms mediated by feedforward inhibition maintain low E-cell pairwise co-variability. Thus, the combination of these two mechanisms ensure low E-cell population variability over a wide range of whisker deflection velocities. Finally, we show how this active decorrelation of population variability leads to a drastic increase in the population information about whisker velocity. The prevalence of spiking non-linearities and feedforward inhibition in the nervous system suggests that the mechanisms for low network variability presented in our study may generalize throughout the brain.
Keywords: layer 2/3 somatosensory cortex, whisker stimulation, noise correlation, Fisher information
Citation: Ly C, Middleton JW and Doiron B (2012) Cellular and circuit mechanisms maintain low spike co-variability and enhance population coding in somatosensory cortex. Front. Comput. Neurosci. 6:7. doi: 10.3389/fncom.2012.00007
Received: 14 October 2011;
Accepted: 24 January 2012;
Published online: 08 March 2012.
Edited by:David Hansel, University of Paris, France
Reviewed by:Germán Mato, Centro Atomico Bariloche, Argentina
Copyright: © 2012 Ly, Middleton and Doiron. This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.
*Correspondence: Cheng Ly, Department of Mathematics, University of Pittsburgh, 139 University Place, Room 505, Thackeray Hall, Pittsburgh, PA, USA. e-mail: firstname.lastname@example.org