Development of olfactory glomeruli: Temporal and spatial interactions between olfactory receptor axons and mitral cells in opossums and rats

Mitral cells are the primary output neurons of the vertebrate olfactory bulb and are major recipients of sensory input from the periphery. The morphogenesis of mitral cell dendrites was followed to elucidate their early spatial and temporal interactions with olfactory receptor neurons and glia during the construction of olfactory glomeruli. Monodelphis domestica, a marsupial born at an extremely immature stage, and rats were examined. Mitral cells were retrogradely labeled by application of the lipophilic dye 1,1′dihexadecyl‐3,3,3′3′‐tetramethylindocarbocyanine perchlorate (DiI) to the lateral olfactory tract. In double‐labeling experiments, olfactory receptor neurons were stained with 3,3′ dihexadecyloxacarbocyanine perchlorate (DiO), or olfactory nerve Schwann cells were visualized using S‐100 protein immunohistochemistry. Tissue was examined with a confocal laser scanning microscope. Some preparations were subsequently investigated with an electron microscope. In Monodelphis, differentiation of mitral cells starts with an outgrowth of numerous, uniform, and widespread dendrites. As soon as terminals of olfactory receptor axons coalesce into glomerular knots within the presumptive glomerular layer, dendrites of individual mitral cells innervate several adjacent glomeruli where they receive sensory synaptic input. With maturation, supernumerary mitral cell dendrites retract, leaving one primary dendrite bearing a terminal glomerular tuft. Simultaneously, secondary dendrites begin to arise. The formation of glomeruli begins earlier and progresses faster in the rat compared to Monodelphis. Nevertheless, mitral cell differentiation in both species follows a common sequence: overproduction of dendrites, selection of usually one primary apical dendrite, and elimination of supernumerary processes. Since olfactory receptor neurons form synaptic contacts with the widespread mitral cell dendrites, considerable synaptic rearrangement must occur within the olfactory glomeruli during maturation. © 1996 Wiley‐Liss, Inc.