The Journal of Neuroscience, December 15, 2002, 22(24):10742-10750
Arcuate Plan of Chick Midbrain Development
Timothy A.
Sanders1,
Andrew
Lumsden2, and
Clifton W.
Ragsdale1
1 Department of Neurobiology, Pharmacology, and
Physiology, The University of Chicago, Chicago, Illinois 60637, and
2 The Medical Research Council Centre for Developmental
Neurobiology, King's College London, Guy's Hospital, London SE1 1UL,
United Kingdom
In spinal cord and hindbrain development, neurons are generated as
longitudinal cell columns aligned with the ventral and dorsal midlines.
For rostral brain, however, the fundamental structure of early neuronal
patterning remains poorly understood. We report here that, in the chick
embryo, the ventral midbrain is remarkably regular in its cellular and
molecular organization; it is arranged as a reiterative series of
arcuate territories arrayed bilateral to the ventral midline. In the
mantle layer of the ventral midbrain, an arcuate series of neuronal
cell columns (midbrain arcs) is demonstrated by acetylcholinesterase
histochemistry and gene expression for class III
-tubulin,
homeodomain transcription factors, and neurotransmitter synthetic
enzymes. In the ventricular layer of midbrain progenitor cells, WNT and
NOTCH ligand gene expression displays arcuate periodicities that form a
tight three-dimensional registration with the arcs of the underlying
mantle layer. Ventral midbrain arcuate patterning is even
macroscopically visible, forming ridges along the ventricular surface.
These observations establish that a single plan of arcuate organization
governs the morphogenesis and cell-type specification of the ventral
midbrain. Arcs are not restricted to the midbrain tegmentum but extend
through the subthalamic tegmentum of the forebrain. Thus, the chick
rostral brain, which is classically divided into midbrain and
forebrain, can also be partitioned into the following: (1) a neuraxial
region of arcs and (2) an anterodorsal cap that includes midbrain
tectum and nonsubthalamic forebrain. We show that this partition of
brain tissue is supported by the expression patterns of homologs of Drosophila gap genes.
Key words:
midbrain arcs; acetylcholinesterase; oculomotor neurons; nucleogenesis; NOTCH; WNT5A; Tailless
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