3D reconstruction of neuronal networks uncovers hidden organizational principles of sensory cortex

Most cortical circuitry interconnects neurons across cortical columns, rather than within
May 11, 2015

3D reconstruction of individual cortical neurons in rats. Top: Examples of neuron reconstructions for each of the 10 major cell types of the vibrissal (whisker-related) part of rat sensory cortex (dendrites are shown in red; axons are colored according to the respective cell type). Bottom: Superposition of all reconstructed axons (colored according to the respective cell type) located within a single cortical column (horizontal white lines in the center represent the edges of this column). The axons from all cell type project beyond the dimensions of the column, interconnecting multiple columns (white open circles) via highly specialized horizontal pathways. (credit: Max Planck Florida Institute for Neuroscience)

An international research team has reconstructed anatomically realistic 3D models of cortical columns of the rat brain, providing unprecedented insight into how neurons in the elementary functional units of the sensory cortex called cortical columns are interconnected.

The models suggest that cortical circuitry interconnects most neurons across cortical columns, rather than within and that these “trans-columnar” networks are not uniformly structured: they are highly specialized and integrate signals from multiple sensory receptors.

For example, rodents are nocturnal animals that use facial whiskers as their primary sensory receptors to orient themselves in their environment. For example, to determine the position, size and texture of objects, they rhythmically move the whiskers back and forth, thereby exploring and touching objects within their immediate surroundings. Such tactile sensory information is then relayed from the periphery to the sensory cortex via whisker-specific neuronal pathways, where each individual whisker activates neurons located within a dedicated cortical column. The one-to-one correspondence between a facial whisker and a cortical column renders the rodent vibrissal system as an ideal model to investigate the structural and functional organization of cortical columns.

In an open-access paper in Cerebral Cortex, the researchers at the Max Planck Institute for Biological Cybernetics (Germany), VU University Amsterdam (Netherlands) and Max Planck Florida Institute for Neuroscience (U.S.) describe how their research sheds light on the organization of cortical columns in the rodent brain via systematic reconstruction of more than 150 individual neurons from all cell types.

The researchers used custom-designed high-resolution 3D reconstruction technologies to create an accurate model of the cortical circuitry, creating the most comprehensive investigation of cortical circuitry to date, and revealing surprising principles of cortex organization, according to the scientists:

  • Neurons of all cell types projected the majority of their axon — the part of the neuron that transmits information to other neurons — far beyond the borders of the cortical column they were located in. That means information from a single whisker spreads into multiple cortical columns.
  • These trans-columnar pathways were not uniformly structured. Instead, each cell type showed specific asymmetric axon projection patterns. For example, interconnecting columns represent whiskers with similar distance to the bottom of the snout.
  • The observed principles of trans-columnar pathways could be advantageous, compared to any previously postulated cortex model, for understanding the brain’s encoding of complex sensory information, the researchers suggest.

According to Marcel Oberlaender, neuroscientist at the Max Planck Institute for Biological Cybernetics and guest-scientist at the Max Planck Florida Institute for Neuroscience, “There has been evidence for decades that cortical columns are connected horizontally to neighboring columns. However, because of the dominance of the columnar concept as the elementary functional unit of the cortex, and methodological limitations that prevented from reconstructing complete 3D neuron morphologies, previous descriptions of the cortical circuitry have largely focused on vertical pathways within an individual cortical column.

“Our novel approach of studying cortex organization can serve as a roadmap [for] reconstructing complete 3D circuit diagrams for other sensory systems and species, which will help to uncover generalizable, and thus fundamental aspects of brain circuitry and organization,” he said.


Abstract of Beyond Columnar Organization: Cell Type- and Target Layer-Specific Principles of Horizontal Axon Projection Patterns in Rat Vibrissal Cortex

Vertical thalamocortical afferents give rise to the elementary functional units of sensory cortex, cortical columns. Principles that underlie communication between columns remain however unknown. Here we unravel these by reconstructing in vivo-labeled neurons from all excitatory cell types in the vibrissal part of rat primary somatosensory cortex (vS1). Integrating the morphologies into an exact 3D model of vS1 revealed that the majority of intracortical (IC) axons project far beyond the borders of the principal column. We defined the corresponding innervation volume as the IC-unit. Deconstructing this structural cortical unit into its cell type-specific components, we found asymmetric projections that innervate columns of either the same whisker row or arc, and which subdivide vS1 into 2 orthogonal [supra-]granular and infragranular strata. We show that such organization could be most effective for encoding multi whisker inputs. Communication between columns is thus organized by multiple highly specific horizontal projection patterns, rendering IC-units as the primary structural entities for processing complex sensory stimuli.