High Stimulus-Related Information in Barrel Cortex Inhibitory Interneurons.

Vicente Reyes-Puerta,Werner Kilb,Suam Kim,Barbara Imbrosci,Jyh-Jang Sun,Heiko J Luhmann,Lyle Graham

doi:10.1371/journal.pcbi.1004121

Abstract

The manner in which populations of inhibitory (INH) and excitatory (EXC) neocortical neurons collectively encode stimulus-related information is a fundamental, yet still unresolved question. Here we address this question by simultaneously recording with large-scale multi-electrode arrays (of up to 128 channels) the activity of cell ensembles (of up to 74 neurons) distributed along all layers of 3–4 neighboring cortical columns in the anesthetized adult rat somatosensory barrel cortex in vivo. Using two different whisker stimulus modalities (location and frequency) we show that individual INH neurons – classified as such according to their distinct extracellular spike waveforms – discriminate better between restricted sets of stimuli (≤6 stimulus classes) than EXC neurons in granular and infra-granular layers. We also demonstrate that ensembles of INH cells jointly provide as much information about such stimuli as comparable ensembles containing the ~20% most informative EXC neurons, however presenting less information redundancy – a result which was consistent when applying both theoretical information measurements and linear discriminant analysis classifiers. These results suggest that a consortium of INH neurons dominates the information conveyed to the neocortical network, thereby efficiently processing incoming sensory activity. This conclusion extends our view on the role of the inhibitory system to orchestrate cortical activity.

Highlights

A fundamental goal in neuroscience is to understand the complex mechanisms by which populations of neurons process sensory information [1,2]
Barrel-related columns were located by voltage sensitive dye (VSD) imaging upon singlewhisker stimulation, which determined the insertion points of the electrode arrays
In the remaining 9 animals an 8x16 channels probe was employed, allowing simultaneous recordings from 21–74 neurons in 3–4 barrelrelated columns. From these 437 neurons, putative inhibitory (INH, 14.2%, n = 62) and excitatory (EXC, 85.8%, n = 375) neurons were identified according to their spike width and waveform asymmetry [15,16,17], from which 7% (4 INH, 27 EXC) were located in layer 2/3 (L2/3), 14.9% (15 INH, 50 EXC) in L4, 44.6% (14 INH, 181 EXC) in L5A and 33.4% (29 INH, 117 EXC) in L5B/6

Summary

Introduction

A fundamental goal in neuroscience is to understand the complex mechanisms by which populations of neurons process sensory information [1,2]. Substantial progress has been made (1) in estimating the amount of information carried by individual neurons about sensory inputs [3,4], and (2) in determining the importance of functional correlations among neurons for the collective encoding of information [5,6] Despite these advances, little is known about how specific subpopulations of cortical neurons differ in their encoding capabilities, and the impact of these differences on the processing of sensory information. In vivo intracellular recordings from different neuronal subpopulations, combined with pharmacological or optogenetic manipulation of GABAergic transmission have started to elucidate the functional role of individual inhibitory cells in different behavioral contexts [9,10,11] It is largely unknown how the activity of interneuron populations contribute to the processing of sensory information in neocortical networks

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