N-acetyl-lactosamine in the rat olfactory system: expression and potential role in neurite growth.

Abstract

Primary sensory olfactory neurons exhibit a mosaic topographical projection from the olfactory neuroepithelium in the nasal cavity to the olfactory bulb formation of the telencephalon. Axons from primary neurons that are widely scattered in the epithelium terminate in discrete regions of the olfactory bulb. It has been hypothesised that carbohydrates present on the surface of primary olfactory axons mediate selective fasciculation and the formation of the topographical pathway. We examined the expression of the disaccharide N-acetyl-lactosamine in both the developing and the adult rat olfactory system. N-acetyl-lactosamine was expressed by all primary sensory olfactory neurons and by their terminations in the olfactory bulb throughout embryonic development and early postnatal life. In adults, N-acetyl-lactosamine was restricted to a subpopulation of primary sensory olfactory neurons that were dispersed throughout the neuroepithelium but that projected predominantly to the ventrolateral and ventromedial surfaces of the olfactory bulb. The axons of these neurons sort out in the outer layer of the bulb and preferentially self-fasciculate to form distinct axon bundles that terminate within select glomeruli. The role of N-acetyl-lactosamine in axon growth was tested by culturing primary sensory olfactory neurons on substrate-bound carbohydrates. Olfactory neuroepithelium cultures from both embryonic and postnatal rats revealed that substrate-bound N-acetyl-lactosamine was a strong and specific neurite growth-promoting agent. These data suggest that, during development of the olfactory projection, N-acetyl-lactosamine, which is present on all olfactory axons, acts as a nonselective permissive substrate for axon growth. In adults, however, the restricted distribution of N-acetyl-lactosamine on a subpopulation of axons may facilitate sorting out and self-fasciculation, which is necessary for preserving the mosaic nature of the olfactory pathway in this highly plastic region of the nervous system. These results support the hypothesis that cell surface carbohydrates are involved in axon growth in the olfactory system.