Cellular organization of cortical barrel columns is whisker-specific

Abstract

The cellular organization of the cortex is of fundamental importance for elucidating the structural principles that underlie its functions. It has been suggested that reconstructing the structure and synaptic wiring of the elementary functional building block of mammalian cortices, the cortical column, might suffice to reverse engineer and simulate the functions of entire cortices. In the vibrissal area of rodent somatosensory cortex, whisker-related "barrel" columns have been referred to as potential cytoarchitectonic equivalents of functional cortical columns. Here, we investigated the structural stereotypy of cortical barrel columns by measuring the 3D neuronal composition of the entire vibrissal area in rat somatosensory cortex and thalamus. We found that the number of neurons per cortical barrel column and thalamic "barreloid" varied substantially within individual animals, increasing by ∼2.5-fold from dorsal to ventral whiskers. As a result, the ratio between whisker-specific thalamic and cortical neurons was remarkably constant. Thus, we hypothesize that the cellular architecture of sensory cortices reflects the degree of similarity in sensory input and not columnar and/or cortical uniformity principles.T wo major concepts of cortical neuronal organization have been proposed. Structurally, correlations between stereologybased measurements (1) of neuron density and cortical thickness resulted in the hypothesis of structural uniformity, arguing that the number of neurons beneath a square millimeter of cortical surface is constant and independent of cortical area and species (2, 3). Functionally, cortex is organized in a columnar fashion, reflecting similar neuronal activity along the vertical cortex axis in response to peripheral stimuli (4-8). Similar spatial extents of functional cortical columns in the horizontal plane, combined with the idea of cortical uniformity, resulted in the notion that a stereotypic columnar network may also represent the elementary structural building block of sensory cortices (9). In combination, the two concepts thus suggested a common organization of all sensory cortices, which led to reverse engineering and simulation efforts that build up large-scale network models of repeatedly occurring identical cortical circuits (10, 11).The ideal model system for investigating columnar structure and function is the vibrissal area of rodent somatosensory cortex. There, "barrels" of neurons in layer 4 (L4) have been identified as somatotopically organized structural correlates of peripheral receptor organs (i.e., facial whiskers). Whisker/barrel columns have thus been regarded as both structural and functional elementary cortical units (12)(13)(14). To investigate the structural stereotypy of cortical barrel columns, independent of the drawbacks associated with stereology (i.e., extrapolations from small sampling regions), we decided to locate each excitatory and inhibitory neuron soma within the entire volume of interest. Using high-resolution, large-scale confocal microscopy (15) and a...

Cortical and thalamic contributions to response dynamics across layers of the primary somatosensory cortex during tactile discrimination

“…Anatomical studies have shown that VPM sends multiple projections to the barrels in layer IV and to layer VI of S1 (Bernardo and Woolsey 1987;Killackey 1973;Lorente de No 1922;Woolsey and Van der Loos 1970), whereas POM projections to layer IV terminate mostly in the septa (Chmielowska et al 1989;Fabri and Burton 1991;Koralek et al 1988;Lu and Lin 1993). As the area occupied by barrels in layer IV is considerably larger than the area occupied by septa (Meyer et al 2013;Wimmer et al 2010;Woolsey and Van der Loos 1970), the observation that layer IV matches VPM neural state maps is in line with this anatomical data. However, the existence of clear differences between layer IV and VPM neural state maps during the animal behavioral response and reward epochs also suggests that other afferents influence S1 granular layer dynamics.…”

Predicting visual acuity from the structure of visual cortex

“…The fraction of cells that are neurons, as determined with NeuN alone, is uncertain because immunostaining is not all-ornone, there is no check by directly staining glia (we are not aware of a nuclear glial antibody), glia and neurons may not survive the disaggregation step equally, and the error magnitude in counting total cells (see above) is unknown. This issue is also relevant for stereology studies (38) that use NeuN for getting neuron and glia estimates.…”

An automated workflow for the anatomo-functional mapping of the barrel cortex

“…The rodent primary somatosensory cortex is a very convenient model for studying the cortical processing of sensory information because of its well defined structural and functional layout that is invariant from animal to animal (Welker and Van der Loos, 1986;Meyer et al, 2013;Egger et al, 2012). In its layer IV, neurons are gathered into clusters called barrels that respect the same topology as the whiskers on the snout of the animal (Woosley and Loos, 1970).…”