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Journal of Neuroscience, Vol 6, 1781-1795, Copyright © 1986 by Society for Neuroscience
Pioneer growth cone steering along a series of neuronal and non- neuronal cues of different affinities
M Caudy and D Bentley
We have analyzed the morphology of over 5000 Ti1 pioneer growth cones
labeled with anti-HRP, which reveals the disposition of axons, growth cone
branches, and filopodia. Ti1 axon pathways typically consist of a sequence
of 7 characteristically oriented segments, with a single, distinct
reorientation point between each segment. Growth cones exhibit the same
orientations and reorientations in a given region as do axon segments at
later stages. The single, distinct reorientations suggest that growth cones
make discrete switches between guidance cues as they grow. Ti1 growth cones
are guided by various types of cues. A set of 3 immature identified neurons
serves as nonadjacent guidepost cells and lies at the proximal end of 3 of
the axon segments. To form another segment, growth cones reorient along a
limb segment boundary within the epithelium. Growth cones also respond
consistently to, and orient toward, a specific mesodermal cell, which may
be a muscle pioneer. Thus, growth cones respond to at least 3 different
types of cells in the leg. Ti1 growth cones exhibit a hierarchy of affinity
for these cues. Guidepost neurons are the dominant cues in that contact
with them reorients growth cones from guidance by the other types of cues.
Growth cone branches are exclusively oriented to specific cues. Growth
cones reorient by extending a branch directly to the cue of highest
affinity and by withdrawing any branches that are extended to a cue of
lesser affinity. A single filopodium in direct contact with a guidepost
neuron can reorient a growth cone that still has multiple filopodia or even
prominent branches specifically oriented to a previous cue of lesser
affinity. These observations suggest that growth cone steering may not
result simply from passive adhesion and filopodial traction, but may
involve more active processes.
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