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Journal of Neuroscience, Vol 13, 3773-3792, Copyright © 1993 by Society for Neuroscience
Contact-mediated mechanisms of motor axon segmentation
RA Oakley and KW Tosney
Neuroscience Program, University of Michigan, Ann Arbor 48109.
In the chick embryo, the segmental pattern of motor outgrowth depends on
guidance cues provided by sclerotome cells. Motor axons preferentially
invade the anterior sclerotome but avoid the posterior sclerotome. To
determine how motor growth cone motility is influenced by these cells, we
used videomicroscopy to analyze the behavior of motor growth cones as they
confronted identified sclerotome cells in vitro. After contact, motor
growth cones invariably avoided posterior sclerotome cells by either
branching or turning. Both types of avoidance behavior were initiated by a
local inhibition of veil protrusion: veils failed to progress along the
contacting filopodia. This inhibition was specific to veils since contact
failed to alter the number of filopodia protruded. Moreover, motor growth
cones turned away from posterior cells despite more persistent filopodial
contacts with these cells than with the laminin substratum. In no case did
contact with posterior cells cause a complete loss of growth cone motility
or a complete collapse of growth cone structure. In contrast, motor growth
cones exhibited a selective affinity for anterior cells, preferring the
surfaces of these cells to the laminin substratum. Contact with anterior
cells stimulated a generalized increase in protrusive activity: contact
caused a net increase in the extension of veils and filopodia both locally
and at sites distant from the site of contact. Contact also elicited a
localized thickening of contacting processes, suggesting that contact with
anterior cells promotes neurite consolidation. This behavior of motor
growth cones in vitro suggests that both an inhibition of veil formation by
posterior cells and an enhancement of motility and axon consolidation by
anterior cells contribute to the preferential advance of motor axons into
anterior sclerotome in vivo. We suggest that patterned outgrowth results
from the juxtaposition of two contrasting environments that differentially
influence growth cone motility.
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