Lattice System of Functionally Distinct Cell Types in the Neocortex

 

Science  03 Nov 2017: Vol. 358, Issue 6363, pp. 610-615

Lattice system of functionally distinct cell types in the neocortex

Hisato Maruoka, et.al.

RIKEN Brain Science Institute, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan.

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The mammalian neocortex contains many cell types, but whether they organize into repeated structures has been unclear. We discovered that major cell types in neocortical layer 5 form a lattice structure in many brain areas. Large-scale three-dimensional imaging revealed that distinct types of excitatory and inhibitory neurons form cell type–specific radial clusters termed microcolumns. Thousands of microcolumns, in turn, are patterned into a hexagonal mosaic tessellating diverse regions of the neocortex. Microcolumn neurons demonstrate synchronized in vivo activity and visual responses with similar orientation preference and ocular dominance. In early postnatal development,    microcolumns are coupled by cell type–specific gap junctions and later serve as hubs for convergent synaptic inputs. Thus, layer 5 neurons organize into a brainwide modular system, providing a template for cortical processing.

In neocortical layer 5,    subcerebral projection neurons (SCPNs) are one of the two major excitatory neuron types and have well-defined anatomical and genetic specifications. SCPNs constitute the major cortical output pathway, sending massive axonal projections to subcortical targets including the pons, spinal cord, and superior colliculus. Prior studies described a local arrangement of SCPNs in radial clusters with a diameter of one to two cells and tangential distances of a few cell diameters. These clusters, here termed microcolumns, have been reported in visual and somatosensory cortical areas in mice and in language areas in humans. To study the cellular organization of neocortical layer 5, we conducted structural and functional analyses of SCPN microcolumns and investigated whether other cell types    organize into microcolumnar structures.

We discovered that wide areas of neocortical layer 5 are organized into a cellular lattice system composed of cell type–specific microcolumns. The functional modularity suggests that single microcolumns perform elementary circuit functions that collectively constitute large-scale parallel processing. The descriptions of microcolumns in multiple cortical areas in mice and humans suggest that the lattice system is a neuronal architecture    common to cortical functions as diverse as sensory, motor, and language processing. The coordinated in vivo activity of SCPN microcolumns and their convergent inputs indicate that they constitute a brainwide system of modular, repeated synaptic circuits and discrete cortical output channels.

Several mammalian species, but not rodents, possess ocular dominance columns and orientation columns. We hypothesize that in species that have orientation columns and ocular dominance columns, neighboring microcolumns may be progressively arranged to have similar functions, thereby contributing to the anatomy of known cortical columns. Orientation columns have a width roughly similar to microcolumn spacing and exhibit a hexagonal arrangement; therefore, they may be constructed on the basis of the lattice system.

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