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Journal of Neuroscience, Vol 13, 4301-4315, Copyright © 1993 by Society for Neuroscience
An electron microscopic analysis of hippocampal neurons developing in culture: early stages in the emergence of polarity
JS Deitch and GA Banker
Department of Cell Biology, UMDNJ-School of Osteopathic Medicine, Stratford 08084.
In culture, hippocampal neurons initially establish several short, minor
processes. The initial step in the emergence of polarity is marked by the
rapid and selective growth of one of these processes, which becomes the
axon. Subsequently the remaining processes become dendrites. We examined
the ultrastructure of hippocampal neurons before and after the emergence of
the axon. The minor processes in cells that had not yet formed axons were
somewhat variable in appearance, but we found no ultrastructural feature
that indicated which minor process might become the axon. The emergence of
the axon was marked by several changes in its ultrastructure. The axon
contained a sevenfold lower density of polyribosomes than the minor
processes. In addition, axonal growth cones contained a pronounced
concentration of membranous elements that resembled endoplasmic reticulum,
elements that were rare in the growth cones of minor processes. Axons and
minor processes did not differ in microtubule density. In order to gauge
how rapidly these ultrastructural changes occur, we examined cells with
short axons that, from their length, were estimated to have emerged only
hours earlier. The preferential exclusion of polyribosomes from the axon
and the concentration of reticular membrane in the axonal growth cone were
already evident in such cells. These observations demonstrate that
exclusion of ribosomes from the axon occurs early in development, about as
soon as the axon can be identified. In contrast, previous work has shown
that the differences in microtubule polarity orientation that distinguish
mature axons and dendrites, and that have been proposed to account for the
selective segregation of some constituents in neurons, first appear at a
later stage of development (Baas et al., 1989). These observations also
demonstrate that the accumulation of reticular membrane elements in growth
cones, which has been noted previously, occurs preferentially in axonal
growth cones and is closely correlated in time with the initial
specification of the axon. The selective concentration of these elements in
axonal growth cones could be associated with the uniquely rapid rate of
axonal growth.
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