Postnatal development of olfactory receptor cell axonal arbors

Abstract

The mechanisms that subserve the distribution of the terminal arbors of olfactory receptor cell axons remain unknown. Elsewhere in the central nervous system, a common theme is early axonal exuberance followed by activity-dependent pruning to achieve the mature distribution. This led to the hypothesis that the orderly morphology of afferent axons in the olfactory glomerulus may follow a similar developmental scheme of exuberance followed by pruning. To test this hypothesis, we studied morphological features of olfactory receptor neuron (ORN) axonal arbors on postnatal days 0, 3, 6, 9, 12, and 21. The olfactory bulbs from Sprague-Dawley rats were processed using a Golgi technique that impregnated ORN axons. Axons from each age group were reconstructed by using camera lucida at x100, oil immersion, and morphometrically characterized. In the adult, the percent glomerular area occupied by a single ORN axon was 14%, whereas the mean length of branches was 169.67 microm, the sum of branches and varicosities was 27, and the distance to first branch point in glomeruli was 21.98 microm. The values from the younger age groups were not statistically different from those in the adult. Because there was no evidence of early exuberance, our data suggest that ORN axons must innervate single glomeruli and arborize in a highly specific manner to achieve the adult pattern. Because our data suggest that ORN axons do not follow the hypothesized scheme, it is plausible to suggest that as ORN axons innervate a glomerulus during development they arborize to their adult levels but not beyond. This argues strongly that specific cell surface and trophic factors are used by the ORN axon to guide glomerular targeting and innervation.

Evidence for Developmentally Regulated Local Translation of Odorant Receptor mRNAs in the Axons of Olfactory Sensory Neurons

“…Each olfactory sensory neuron projects a single, unbranched axon into a single glomerulus of the olfactory bulb (Klenoff and Greer, 1998). Hence, a given odorant receptor mRNA is expressed by only a few thousand sensory neurons and only a few thousand axon terminal segments containing these odorant receptor mRNAs are present in the bulb.…”

An Energy Budget for the Olfactory Glomerulus

“…Volume of presynaptic axonal elements. We have derived a model of the ORN axonal tree based on camera lucida reconstructions and exhaustive work on axon morphology by Klenoff et al (1998) (Fig. 2a).…”

“…Thus, although the surface areas are weighted in favor of the axons, the numbers of synapses come to dominate the energy demands. This is mainly attributable to the fact that each afferent axon gives rise to on average 26 synapses (Klenoff et al, 1998). This divergence is a critical factor in determining the ratio between axonal energy demands and postsynaptic energy demands.…”

Principles of Glomerular Organization in the Human Olfactory Bulb – Implications for Odor Processing

“…In rodents, each OSN expresses only 1 of ∼1100 odor receptors (OR) [1], [2], [3]. Moreover, each OSN projects one axon to a single glomerulus [4], and all of the OSN axons innervating a glomerulus express the same OR [5]. Thus, the molecular specificity of OSNs established by OR expression is maintained in molecularly homogeneous target glomeruli, creating a stereotyped glomerular map of ORs, with any 1 OR typically represented by two glomeruli [6], [7], [8].…”