Journal of Neuroscience, Vol 1, 721-735, Copyright © 1981 by Society for Neuroscience
Prenatal formation of cortical input and development of cytoarchitectonic compartments in the neostriatum of the rhesus monkey
PS Goldman-Rakic
The timing, hemispheric laterality, and mode of termination of input from
the prefrontal association cortex to the neostriatum were studied in fetal
and neonatal rhesus monkeys using autoradiography for tracing connections.
In addition, the cytological maturation of the neostriatum was examined in
Nissl-stained sections from the same and other monkeys of selected prenatal
and postnatal ages. A small contingent of corticostriatal axons reaches
both the caudate nucleus and the putamen by the 69th embryonic day (E69) of
the 165-day gestation period in this species and steadily expands over the
next 3 fetal months. Throughout this period, ipsilateral perfrontostriatal
connections predominate, and only a small and variable amount of label is
detectable over the contralateral neostriatum. A major feature of the
developing corticostriatal projection is a transfiguration in the
distribution of its terminals: from E69 to E95, cortical terminals are
distributed uniformly among neostriatal neurons; beginning around E105,
areas of higher and lower grain density begin to emerge until finally, by
E133, 250- to 500-micrometers-wide circular and elliptically shaped label-
free cores perforate a field of densely labeled cortical terminals as in
the neostriatum of the adult monkey (Goldman, P. S., and W. J. H. Nauta
(1977) J. Comp. Neurol. 171: 369-386). The cytoarchitectonic composition of
the neostriatum also changes during gestation: from E69 through E95, the
small postmitotic neurons of the immature neostriatum are packed densely
and, for the most part, are distributed homogeneously; by E105, they become
segregated into cellular islands consisting of densely packed neurons that
are encapsulated by fiber- rich annuli and embedded in a matrix of less
densely arrayed neurons. The shape and size of the islands in Nissl-stained
sections correspond to label-free cores in autoradiograms of fetuses with
cortical injections, while the surrounding annuli and adjacent matrix cells
correspond to areas of dense accumulation of label. Thus, the formation of
the corticostriatal projection in primates involves a transformation in the
distribution of ingrowing terminals synchronized with changes in cellular
organization of the neostriatum.
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