New Features of Connectivity in Piriform Cortex Visualized by Intracellular Injection of Pyramidal Cells Suggest that "Primary" Olfactory Cortex ...

Associational connections of pyramidal cells in rat posterior piriform cortex were studied by direct visualization of axons stained by intracellular injection in vivo. The results revealed that individual cells have widespread axonal arbors that extend over nearly the full length of the cerebral hemisphere. Within piriform cortex these arbors are highly distributed with no regularly arranged patchy concentrations like those associated with the columnar organization in other primary sensory areas (i.e., where periodically arranged sets of cells have common response properties, inputs, and outputs). A lack of columnar organization was also indicated by a marked disparity in the intrinsic projection patterns of neighboring injected cells. Analysis of axonal branching patterns, bouton distributions, and dendritic arbors suggested that each pyramidal cell makes a small number of synaptic contacts on a large number (>1000) of other cells in piriform cortex at disparate locations. Axons from individual pyramidal cells also arborize extensively within many neighboring cortical areas, most of which send strong projections back to piriform cortex. These include areas involved in high-order functions in prefrontal, amygdaloid, entorhinal, and perirhinal cortex, to which there are few projections from other primary sensory areas. Our results suggest that piriform cortex performs correlative functions analogous to those in association areas of neocortex rather than those typical of primary sensory areas with which it has been traditionally classed. Findings from other studies suggest that the olfactory bulb subserves functions performed by primary areas in other sensory systems.






Figure 1. Axon from a single pyramidal cell in layer II of rat piriform cortex. Note that axon branches extend over nearly the entire length of the cerebral hemisphere and are widely distributed within piriform cortex and other olfactory and nonolfactory areas. The SP cell in posterior piriform cortex was stained by intracellular injection of biotinylated dextran amine in vivo, and the axon was reconstructed through serial sections with a computer microscope system. A, Spatial distribution of axon branches in surface view. The inset at top right shows the illustrated portion of the rat brain (dashed rectangle) and orientation (45° upward rotation); the hatched area is piriform cortex, and the shaded area is lateral olfactory tract. APC, Anterior piriform cortex; PPC, posterior piriform cortex. B, Depth distribution of same axon within PPC. View is parallel to layers after 90° rotation; rostral is at left as in A; branches outside PPC have been removed; size scale is expanded relative to that in A. Roman numerals indicate layers: Ib, association fiber zone in layer I (molecular layer); IIIs, IIId, superficial and deep portions of layer III; dotted lines, superficial and deep borders of layer II (compact cell body layer). Open arrowheads mark branch points for axon collaterals that ascend to layer I. Open arrows in A and B indicate cell body; dendritic tree is not illustrated (Fig. 3). Ant, Anterior; ctx, cortex; nuc, nucleus; olfac, olfactory.

Dawn M. G. Johnson, Kurt R. Illig, Mary Behan, and Lewis B. Haberly
New Features of Connectivity in Piriform Cortex Visualized by Intracellular Injection of Pyramidal Cells Suggest that "Primary" Olfactory Cortex Functions Like "Association" Cortex in Other Sensory Systems
J. Neurosci. 20: 6974-6982; doi:

http://www.jneurosci.org/cgi/content/full/20/18/6974