Beyond the cortical column: Subcellular structural organization principles in rat vibrissal cortex

The cortical column is regarded as an elementary functional unit of the mammalian brain. In the vibrissal cortex of rodents, so called barrel columns primarily process the information obtained from a related principal whisker on the animal’s snout. We reconstructed the 3D geometry of the entire rat vibrissal cortex with high precision. We found that the 3D layout of the vibrissal cortex was preserved across animals. In contrast, barrel columns differed substantially within the same animal. To investigate whether the differences in column geometry result in structural differences at the network level, we determined (i) the number and distribution of excitatory/inhibitory neurons in the vibrissal cortex, (ii) the number and distribution of neurons in vibrissal thalamus, (iii) the number and distribution of cell types in cortex and thalamus and (iv) reconstructed the 3D dendrite and axon innervation patterns of neurons from all cell types. First, we found that the neuron density was similar in each barrel column, resulting in 3-fold differences in numbers of neurons between columns. Second, the number of thalamic input neurons correlated with the number of neurons per column. Third, the vibrissal cortex and thalamus contained 9 and 4 types of excitatory neurons, respectively. Forth, dendrite and axon morphologies were characteristic for each cell type. Further, neurons of most cell types projected the majority of their axon to surrounding cortical columns. Finally, we created a standardized 3D model of the entire vibrissal cortex and combined it with the 3D distributions of excitatory/inhibitory neurons and the 3D reconstructions of dendrites and axons from all cell types. Using this anatomically realistic model of the vibrissal cortex, we estimated the number and 3D subcellular distribution of synaptic contacts between approximately 600,000 neurons. The resultant average ‘connectome’ of the vibrissal cortex reveals structural organization principles beyond individual cortical columns and allows for interpretation or simulation of functional data, measured in vivo