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Journal of Neuroscience, Vol 12, 1194-1211, Copyright © 1992 by Society for Neuroscience
Growth and targeting of subplate axons and establishment of major cortical pathways [published erratum appears in J Neurosci 1993 Mar;13(3):following table of contents]
JA De Carlos and DD O'Leary
Molecular Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, California 92037.
In the developing mammalian neocortex, the first postmitotic neurons form
the "preplate" superficial to the neuroepithelium. The preplate is later
split into a marginal zone (layer 1) and subplate by cortical plate neurons
that form layers 2-6. Cortical efferent axons from layers 5 and 6 and
cortical afferent axons from thalamus pass between cortex and subcortical
structures through the internal capsule. Here, we identify in rats the
axonal populations that establish the internal capsule, and characterize
the potential role of subplate axons in the development of cortical
efferent and afferent projections. The early growth of cortical efferent
and afferent axons was studied using 1-1'-
dioctodecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (Dil) as an
anterograde and retrograde tracer in aldehyde-fixed brains of embryonic
rats. Cortical axons first enter the nascent internal capsule on embryonic
day (E) 14 and originate from lateral and anterior cortex; axons from
posterior cortex extend rostrally but do not yet exit cortex. The labeled
axons, tipped by growth cones with complex morphologies, take a pathway
deep to the preplate. Preplate neurons extend these early cortical
efferents, based on the developmental stage of the cortex, and on their
location and morphology. Most of these cells later occupy the subplate.
Cortical plate neurons extend axons into the internal capsule by E16. En
route to the internal capsule, cortical plate axons take the same path as
the earlier-growing preplate axons, through the intermediate zone deep to
subplate. Subplate axons reach thalamus by E16; the first cortical plate
axons enter thalamus about a day later. Thalamic axons enter cortex by E16,
prior to other cortical afferents. On E15, both preplate and thalamic axons
reach the midpoint of the internal capsule. To determine the subcortical
distribution of subplate axons, we used Dil as a retrograde tracer in
aldehyde-fixed brains and fast blue and rhodamine-B-isothiocyanate as in
vivo retrograde markers in neonatal rats. Tracers were injected into the
superior colliculus, the principal midbrain target of layer 5 neurons, at
times before, during, and after the arrival of cortical axons, or into the
subcortical pathway of primary layer 5 axons at two points, the cerebral
peduncle caudal to the internal capsule, and the pyramidal decussation at
the junction of the hindbrain and spinal cord, at times shortly after the
passing of cortical axons. In every case, the labeled neurons are confined
to layer 5; subplate neurons are not labeled.(ABSTRACT TRUNCATED AT 400
WORDS)
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