Localized denervation demonstrates the innervation pattern of olfactory bulb glomeruli and second order cells

Abstract

Sensory systems rely upon spatially organized projections for the faithful transfer of receptor activity into the central nervous system. While the mammalian olfactory nerve shows a regional topographical organization, data on the sources of variation within this projection are scarce. We evaluated the degree of precision of olfactory bulb glomerular innervation from the olfactory nerve layer (ONL) by making small cuts across the trajectory of the olfactory nerve fibers and assessing the resulting denervation by wheat germ agglutinin-horseradish peroxidase (WGA-HRP) labeling of primary nerve fibers. In control animals (no ONL cut), the ONL and glomerular layer showed intense labeling around the entire circumference of the bulb. Transneuronal labeling of the mitral cell layer and the external plexiform layer was also observed in animals surviving at least 2 days, which allowed us to study the nerve fiber innervation of second order cells as well. ONL cuts on the lateral face of the bulb produced a stripe of denervation, as evidenced by the absence of primary and transneuronal label in a well-defined region. Fascicles of fibers within the ONL were never observed to enter the denervated region from more than one or two glomerular widths away, indicating a relatively tight limit of variation in the spatial termination of olfactory nerve fibers on the lateral bulb surface. This limit of variation does not hold around the circumference of the bulb since similar ONL cuts on the dorsal surface failed to produce a distinct stripe of denervation. Field potential measurements from the ONL after similar cuts supported the anatomic findings. These results show that primary olfactory axons and their terminals lie in parallel along the lateral face of the olfactory bulb. These spatial relationships of olfactory input to the bulb are maintained in the second order connections. This organization allows one to study the spatial aspects of interneuronally mediated synaptic mechanisms involved in olfactory coding.