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Journal of Neuroscience, Vol 10, 2096-2112, Copyright © 1990 by Society for Neuroscience
Construction of a protoglomerular template by olfactory axons initiates the formation of olfactory glomeruli in the insect brain
LA Oland, G Orr and LP Tolbert
Arizona Research Laboratories, University of Arizona, Tucson 85721.
Olfactory glomeruli in insects share many features of organization with
their vertebrate counterparts, and yet offer distinct advantages for study
of neuronal development. Previous studies have revealed that the olfactory
lobes of the brain of the moth Manduca sexta arise postembryonically and
that glomeruli in the lobe are induced by olfactory afferent axons
(Hildebrand et al., 1979; Oland and Tolbert, 1987). In the present study,
we have used the Golgi method, intracellular labeling of neurons with
Lucifer yellow, and electron microscopy to follow neuronal development in
the antennal lobe through the period when glomeruli develop. Our results,
taken together with other results from our laboratory, suggest that
olfactory sensory axons have the intrinsic ability to form protoglomeruli,
and that an interaction between these axons and glial cells (but not the
majority of the neurons of the antennal lobe) causes the glial cells to
surround the protoglomeruli. Ingrowth of the neurites of most antennal-lobe
neurons into the protoglomeruli occurs after a small delay and appears to
be constrained to glomerular units by the presence of the glial boundaries.
Synapses, initially not detected in the protoglomeruli, begin to appear as
soon as the neurites of antennal-lobe neurons appear in the glomeruli.
Thus, antennal axons, instead of immediately seeking out postsynaptic
targets, first form the template for organization of future glomeruli. The
neurites of most of the neurons of the antennal lobe grow outward to meet
the olfactory sensory axons, and in doing so, join with these axons to form
glomeruli. Preliminary results concerning the development of a second class
of neuron in the lobe, the projection neurons, indicate that at least some
of these neurons may arborize in the region of the protoglomeruli very
early and therefore participate with the afferent axons in laying the
foundation for glomeruli.
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