Olfactory glomeruli are innervated by more than one distinct subset of primary sensory olfactory neurons in mice

J Comp Neurol. 1996 Apr 15;367(4):550-62. doi: 10.1002/(SICI)1096-9861(19960415)367:4<550::AID-CNE6>3.0.CO;2-3.

Abstract

The rodent olfactory epithelium consists of a mosaic of primary sensory olfactory neurons (PONs) which express distinct putative olfactory receptor proteins. Recent evidence suggests that individual subsets of these sensory neurons project to separate glomeruli in the olfactory bulb (Vassar et al., [1994] Cell 79:981-991). In the present study we have identified two distinct subsets of primary sensory olfactory neurons (PONs) in the H-OMP-LacZ-6 transgenic mouse. In these transgenic mice, a LacZ reporter gene under the control of a 294 base pair element from the 5' promoter region of the olfactory marker protein (OMP) gene was expressed in a subset of PONs located in a discrete band of neuroepithelium in the nasal cavity. These LacZ positive neurons were not randomly located within this band but were more concentrated within a locus between endoturbinates IIb and III. The axons of these neurons densely innervated three adjacent and bilaterally symmetrical glomeruli present in the ventromedial olfactory bulb. Labeling of tissue sections with the plant lectin Dolichos biflorus (DBA) revealed an independent subset of PONs in the transgenic mice. These neurons were present in a wide region of the nasal cavity that included the neuroepithelial band containing the LacZ expressing neurons. The DBA labeled axons terminated in glomeruli in the rostromedial and dorsolateral olfactory bulb surfaces. Although the glomeruli innervated by the LacZ and DBA positive axons were predominantly non-overlapping there were glomeruli in the ventral olfactory bulb that were labeled by both DBA and LacZ markers. Eight different types of glomeruli were characterized. Most notably, glomeruli were identified which were innervated partially by both or by either subset alone. In these cases, axon subsets were observed to terminate within discrete subregions of a glomerulus. These results support the hypothesis that phenotypically distinct subsets of PONs converge on to the same glomeruli but also indicate that some glomeruli are innervated by more than one subset of sensory neuron. These findings have implications for understanding how the olfactory projection is formed and how olfactory information is processed.

MeSH terms

  • Animals
  • Axons / metabolism
  • Axons / ultrastructure
  • Cell Count
  • Epithelium / innervation
  • Epithelium / physiology
  • Histocytochemistry
  • Lactose Factors
  • Lectins
  • Mice
  • Mice, Transgenic
  • Nerve Tissue Proteins / biosynthesis
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Neurons, Afferent / metabolism
  • Neurons, Afferent / physiology*
  • Neurons, Afferent / ultrastructure
  • Olfactory Bulb / metabolism
  • Olfactory Marker Protein
  • Olfactory Mucosa / innervation*
  • Olfactory Mucosa / metabolism
  • Olfactory Mucosa / ultrastructure
  • Plant Lectins*
  • Smell / physiology*

Substances

  • Lectins
  • Nerve Tissue Proteins
  • Olfactory Marker Protein
  • Omp protein, mouse
  • Plant Lectins
  • dolichos biflorus agglutinin