Evaluation of projection patterns in the primary olfactory system of rainbow trout

Neuroscience Program, University of Michigan, Ann Arbor 48109.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 01/1992; 11(12):3752-62.
Source: PubMed


Topographic projections are important for coding sensory information in the visual, auditory, and somatosensory systems but are of uncertain importance in the coding of olfactory information. We searched for topographic projections between olfactory receptor cells and the olfactory bulb of the rainbow trout Oncorhynchus mykiss. Anterograde axonal tracing with HRP revealed that the olfactory axons arising from discrete regions of the olfactory epithelium travel together within the olfactory nerve. The abrupt resorting and redistribution of these axons at the interface between the olfactory nerve and olfactory bulb imply that local cues control and organize axonal projections. The sites of termination of HRP-labeled axons in the glomerular layer could not be predicted from the location of their cell bodies in the periphery. Retrograde tracing with fluorescently labeled latex beads, injected into glomerular subregions as small as 1% of the total glomerular volume, labeled receptor cells dispersed throughout the olfactory epithelium. The distributions of labeled receptor cells were uncorrelated with the bulbar injection sites. Double-labeling experiments revealed that even widely separated sites in the glomerular layer receive axons from comingled populations of receptor cells. Hence, the evidence indicates that the spatial arrangement of olfactory receptor cells in the epithelium is not preserved in the termination of their axons in the olfactory bulb. We conclude that the primary olfactory in trout lacks point-to-point or regionally topographic organization and that the entire extent of the olfactory epithelium contributes axons to each region of the glomerular layer.

Full-text preview

Available from:
  • Source
    • "Our study supports the results of Dryer and Graziadei (1993) and Daniel (1934). Teleost fishes, along with most other vertebrates, exhibit a functional or chemotopic OB organization in which ORNs widely distributed over the epithelium converge to particular glomeruli in the OB based on the ORN morphotype (Riddle and Oakley, 1991; Baier et al., 1994; Sato et al,, 2005; Hamdani and Døving, 2007; Sato et al., 2007). As a result, the OB possesses separate functional zones that process different types of odorants (Nikonov and Caprio, 2001, 2004). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The olfactory bulbs (OBs) are bilaterally paired structures in the vertebrate forebrain that receive and process odor information from the olfactory receptor neurons (ORNs) in the periphery. Virtually all vertebrate OBs are arranged chemotopically, with different regions of the OB processing different types of odorants. However, there is some evidence that elasmobranch fishes (sharks, rays, and skates) may possess a gross somatotopic organization instead. To test this hypothesis, we used histological staining and retrograde tracing techniques to examine the morphology and organization of ORN projections from the olfactory epithelium (OE) to the OB in three elasmobranch species with varying OB morphologies. In all three species, glomeruli in the OB received projections from ORNs located on only the three to five lamellae situated immediately anterior within the OE. These results support that the gross arrangement of the elasmobranch OB is somatotopic, an organization unique among fishes and most other vertebrates. In addition, certain elasmobranch species possess a unique OB morphology in which each OB is physically subdivided into two or more "hemi-olfactory bulbs." Somatotopy could provide a preadaptation which facilitated the evolution of olfactory hemibulbs in these species. J. Morphol., 2012. © 2012 Wiley Periodicals, Inc.
    Full-text · Article · Apr 2013 · Journal of Morphology
  • Source
    • "In mammals, ORC axons become sorted in the nerve layer of the olfactory bulb (Mombaerts et al., 1996; Whitesides and La- Mantia, 1996), where they are surrounded by glial cells peculiar to the olfactory system (Doucette, 1984, 1989; Raisman, 1985; Marin-Padilla and Amieva, 1989; Valverde et al., 1992). Resorting of ORC axons has also been described at the interface between the olfactory nerve and the olfactory bulb in fish (Riddle and Oakley, 1991). In Manduca, ORC axons undergo a massive reorganization in a glia-rich region near the entrance of the antennal nerve (AN) into the AL (Oland et al., 1998a). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Olfactory receptor cells (ORCs) of a particular odor tuning are dispersed in the olfactory epithelium, but their axons converge on distinct glomeruli in primary olfactory centers. As a consequence, axon associations must change to bring axons of ORCs with the same odor specificity together. Studies in Manduca sexta have indicated that just before they enter the antennal lobe (AL), ORC axons undergo extreme reorganization, finally entering the AL in fascicles destined for subsets of glomeruli. This axon-sorting zone is heavily populated by glial cells, and ORC axon growth cones often are in close physical contact with the glia. In moths rendered glia deficient, ORC axons fail to fasciculate in this region. Using propidium iodide to label nuclei and 5-bromo-2'-deoxyuridine to monitor proliferation, we found that the glia in the sorting zone arise from the AL, appearing shortly after the first ORC axons arrive. Experimental removal of some or all of the sensory innervation revealed that proliferation of sorting-zone glia is triggered by ORC axons. A second set of glia arises in the antenna and migrates along the antennal nerve toward the brain, populating the nerve after the establishment of the sorting zone. Development of this type of glial cell is independent of contact of the ORC axons with their central targets. We conclude that the sorting zone arises from CNS glia in response to ingrowth of ORC axons, and a critical number of glia must be present in the sorting zone for axons to correctly establish new neighbor-neighbor associations.
    Full-text · Article · Dec 1999 · The Journal of Neuroscience : The Official Journal of the Society for Neuroscience
  • Source
    • "Little is known about how the axons of the first olfactory sensory neurons navigate to the C NS and initiate patterned connections with the developing olfactory bulb. Dye labeling has shown that individual glomeruli in the olfactory bulb receive inputs from sensory neurons scattered throughout the olfactory epithelium (Riddle and Oakley, 1991). Recent studies indicate that the axons of sensory neurons expressing the same olfactory receptor converge on the same glomerulus (Mombaerts et al., 1996), express receptor transcript in their axon terminals (Ressler et al., 1993; Vassar et al., 1994), and respond to the same small subset of odorants (Zhao et al., 1998). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Mechanisms guiding the first axons from the olfactory placode of the peripheral nervous system (PNS) to the olfactory bulb in the vertebrate CNS are unknown. We analyzed the initial outgrowth of axons from the olfactory placode in zebrafish and found a precocious transient class of pioneer neurons that prefigure the primary olfactory pathway before outgrowth of olfactory sensory axons or expression of olfactory receptor genes. Not only are the pioneers antigenically, morphologically, and spatially distinct from olfactory sensory neurons, they are also developmentally distinct; via fate mapping, we show that they arise from a more anterior region of the lateral neural plate than do the first sensory neurons. After the axons of the sensory neurons grow into the CNS, the pioneer neurons undergo apoptotic cell death. When we ablated the pioneers before axonogenesis, the following sensory axons showed severe misrouting. We propose that the pioneers provide the first necessary connection from the PNS to the CNS and that they establish an axonal scaffold for the later-arriving olfactory sensory neurons.
    Full-text · Article · Dec 1998 · The Journal of Neuroscience : The Official Journal of the Society for Neuroscience
Show more