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Journal of Neuroscience, Vol 14, 3500-3510, Copyright © 1994 by Society for Neuroscience
Thalamocortical axons extend along a chondroitin sulfate proteoglycan- enriched pathway coincident with the neocortical subplate and distinct from the efferent path
AR Bicknese, AM Sheppard, DD O'Leary and AL Pearlman
Department of Cell Biology, Washington University School of Medicine, St. Louis, Missouri 63110.
The distinct axonal tracts of the mature nervous system are defined during
development by sets of substrate-bound and diffusible molecular signals
that promote or restrict axonal elongation. In the adult cerebral cortex,
efferent and afferent axons are segregated within the white matter. To
define the relationship of growing efferent and afferent axons in the
developing murine cortex to chondroitin sulfate proteoglycans (CSPGs) in
the pericellular and extracellular matrix, we used the fluorescent tracer
Dil to determine axonal trajectories and immunolabeling to disclose the
distribution of CSPGs. Axons of neurons in the preplate are the first to
leave the cortex; they arise in the CSPG-rich preplate and extend obliquely
across it to enter the CSPG- poor intermediate zone. Slightly later, axons
of cortical plate neurons extend directly across the CSPG-rich subplate,
and then turn abruptly to run in the upper intermediate zone. In contrast,
once afferent axons from the thalamus reach the developing cortical wall,
their intracortical trajectory is centered on the CSPG-rich subplate, above
the path taken by efferent axons. Our findings demonstrate a molecular
difference between the adjacent but distinct efferent and afferent pathways
in developing neocortex. Early efferents cross the subplate and follow a
pathway that contains very little CSPG, while afferents preferentially
travel more superficially within the CSPG-rich subplate. Thus, CSPGs and
associated extracellular matrix (ECM) components in the preplate/subplate
do not form a barrier to axonal initiation or outgrowth in the neocortex as
they may in other locations. Instead, their distribution suggests a role in
defining discrete axonal pathways during early cortical development.
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