Whose Cortical Column Would that Be?

Abstract

The cortical column has been an invaluable concept to explain the functional organization of the neocortex. While this idea was born out of experiments that cleverly combined electrophysiological recordings with anatomy, no one has 'seen' the anatomy of a column. All we know is that when we record through the cortex of primates, ungulates, and carnivores in a trajectory perpendicular to its surface there is a remarkable constancy in the receptive field properties of the neurons regarding one set of stimulus features. There is no obvious morphological analog for this functional architecture, in fact much of the anatomical data seems to challenge it. Here we describe historically the origins of the concept of the cortical column and the struggles of the pioneers to define the columnar architecture. We suggest that in the concept of a 'canonical circuit' we may find the means to reconcile the structure of neocortex with its functional architecture. The canonical microcircuit respects the known connectivity of the neocortex, and it is flexible enough to change transiently the architecture of its network in order to perform the required computations.

Keywords: Daisy; bouton cluster; canonical microcircuit; cortical column; neuroanatomy.

Figure 1

Bouton distribution of four neurons from the primary visual cortex of cat. Axons of neurons from all layers spread over a distance covering the dimensions of many minicolumns. The boutons from a layer 2/3 pyramidal neurons are shown in yellow, from a layer 4 spiny stellate in red, from a layer 5 pyramidal neurons in blue and from a layer 6 pyramidal neuron in green. (A) Coronal view. (B) Top view. (C) Bouton clusters of the axons shown in (A) (adapted from Binzegger et al., 2007). (D) Comparison of the size of a cortical column cover by the proximal cluster of boutons of each neuron (Binzegger et al., 2007). A cluster is considered proximal if it intersects with the vertical axis running through the soma.

Figure 2

Comparison of the size of the proximal cluster of boutons and functional domains for a single orientation recorded with optical imaging. Proximal clusters formed by neurons of layer 2, 3 and 6 are often larger than the orientation domains. Also apparent is the fact that the size of the proximal clusters varies between different neuronal types. (A–F) Show proximal clusters of different neurons (the cell bodies are shown as white dots) from a single cell type. The clusters are color-coded according to the layer in which they are located. In (C) one of the spiny stellates does not have any proximal cluster, and we show the closest cluster to the cell body. The optical imaging map was obtained by dividing the response to the preferred orientation by the sum response of all orientations (cocktail blank). The neurons had receptive fields that lay within 14° of the fovea. Clusters taken from Binzegger et al. (2007).

Figure 3

Spread of proximal boutons over multiple orientation domains. The proximal clusters of neurons in layer 2, 3 and 6 can overlap with dendrites of functional domains representing orthogonal orientations. Proximal cluster of two layer 2/3 pyramidal neurons (black ellipse, the cell body is shown as a white dot) superimposed on an orientation map of area 17. Each region of area 17 is color-coded for its preferred orientation. The white circles surrounding the left cluster represent the coverage of a typical dendritic arbor.

Figure 4

The diameter of the distal bouton clusters, scales with the distance between the clusters (adapted from Binzegger et al., 2007). Average measurement taken from various cortical areas and species (Rockland et al., ; Luhmann et al., ; Burkhalter and Bernardo, ; Kisvarday and Eysel, ; Yoshioka et al., ; Lund et al., ; Levitt et al., ; Fujita and Fujita, ; Kisvarday et al., 1997).

Figure 5

Representation of the major connections in the canonical microcircuit (adapted from Douglas et al., ; Douglas and Martin, 1991, 2004). Excitatory connections are represented by arrows and inhibitory ones as lines with round ends. Neurons from different cortical layers or brain structures are represented as circles. ‘Lx’ designates the cortical layer where the cell body is located, ‘Thal’ designates the thalamus and ‘Sub’ designates other subcortical structures.